Abstract
Mesothelial cells (MCs) form the superficial anatomic layer of serosal membranes, including pleura, pericardium, peritoneum, and the tunica of the reproductive organs. MCs produce a protective, non-adhesive barrier against physical and biochemical damages. MCs express a wide range of phenotypic markers, including vimentin and cytokeratins. MCs play key roles in fluid transport and inflammation, as reflected by the modulation of biochemical markers such as transporters, adhesion molecules, cytokines, growth factors, reactive oxygen species and their scavengers. MCs synthesize extracellular matrix related molecules, and the surface of MC microvilli secretes a highly hydrophilic protective barrier, “glycocalyx”, consisting mainly of glycosaminoglycans. MCs maintain a balance between procoagulant and fibrinolytic activation by producing a whole range of regulators, can synthetize fibrin and therefore form adhesions. Synthesis and recognition of hyaluronan and sialic acids might be a new insight to explain immunoactive and immunoregulatory properties of MCs. Epithelial to mesenchymal transition of MCs may involve serosal repair and remodeling. MCs might also play a role in the development and remodeling of visceral adipose tissue. Taken together, MCs play important roles in health and disease in serosal cavities of the body. The mesothelium is not just a membrane and should be considered as an organ.
Introduction
The pleura is the serous membrane which forms the lining of the pleural cavity and the peritoneum is the serous membrane covering the abdominal cavity. Further serosal membranes are the pericardium, the tunica vaginalis testis (covering the male reproductive organs in the scrotum) and the tunica serosa uteri (covering the internal female reproductive organs). The peritoneum is a large structure with a surface equivalent to the skin. However, relatively few is known about the functional anatomy of the serosal surfaces, in comparison with other organs of the body. Most data available in the literature have been generated by nephrologists interested in peritoneal dialysis, and focus on the peritoneum as a membrane. This short review gives an overview of the morphological anatomy of the mesothelial surfaces in the body and of the related, various functions of these organs.
Serosal surfaces are composed of mesothelial cells (MCs) attached on the basement membrane and subsequent connective tissue containing blood and lymph vessels, fibroblasts, mast cells, monocytes/macrophages, leukocytes, adipocytes, and nerve fibers (Figure 1A) [1, 2]. However, at the organ level, the structure of serosal membranes is not the same in all locations. For example, small lymph vessels are abundant in the submesothelial tissue of the intestines, rectum, uterus, urinary bladder and testis, while they are rare in other locations. Nerve fibers are more commonly observed in the organs of the lesser pelvis, where there are located in close contact to blood vessels in the submesothelial connective tissue [3].
Figure 1:
Morphology of the mesothelium.
The morphological characteristics of MC at the cellular level are also varying along their anatomical localization. For example, cubic MCs (tall and narrow-shaped cells with hollow reservoir function) are characteristic for the mediastinal pleura, the peritoneal side of the diaphragm, the parenchymal organs such as liver and spleen, lymphatic lacunae and milky spots, while the flat MCs are more uniform and widespread in the parietal mesothelium [3]. The parietal peritoneum can be easily detached from the retroperitoneal tissue, whereas the visceral peritoneum is tightly fixed to the bowel and to the parenchymatous organs. These morphological differences have been confirmed by gene profiling and protein expression analysis showing that peritoneal and pleural MCs have different phenotypic patterns [4]. Moreover, visceral and parietal MCs are also fundamentally different in their ability to adhere, migrate and invade [5] and are showing different properties in the process of fibrosis [6].
Besides being morphological components of serosal membranes, MC also plays several key functional roles (Figure 2). One of the basic functions of MC is to form a smooth surface allowing the internal organs to glide. In addition, MC plays a variety of physiological roles or biological functions in several processes such as tissue repair, fibrinolysis, regulation of inflammation, epithelial to mesenchymal transition (EMT) and mediation of the intraperitoneal dissemination of cancer cells. Clinical research has highlighted the role of MC in several pathological settings such as ageing, response to peritoneal dialysis, tissue injury and repair, and cancer progression [7, 8]. Moreover, recent genetic lineage tracing suggested that the mesothelium lining visceral adipose depots might be a potential contributor to tissue dysfunction in obesity, including the development of fibrosis and inflammation [9, 10].
Figure 2:
Functions and roles of methothelial cells.
Phenotypic or biochemical markers of MC
MC expresses a wide range of phenotypic markers observed in simple epithelial-like tissues such as the vascular endothelium or the corneal endothelium. These phenotypic markers include vimentin and cytokeratins (Figure 1D) [11, 12], E-cadherin [13–16], N-cadherin, Calretinin [17], Zo-1 [13, 15, 18] (Figure 1D), β-catenin [13, 19, 20], Wilms’ tumor protein 1 (WT1) [21, 22], mesothelin [4, 23] and podoplanin [24, 25], etc. (Table 1).
Table 1:
Molecules produced by mesothelial cells in pleura and peritoneum.
| Molecule | Site | Stimulus | References |
| Phenotypic or adhesion marker | |||
| Cytokeratin | Pl, Pet | [11, 12] | |
| Vimentin | Pl, Pet | [11, 12] | |
| E-cadhelin | Pl, Pet | [13–16] | |
| N-cadhelin | Pl, Pet | [17] | |
| Zo-1 | Pl, Pet | [13, 15, 18] | |
| β-Catenin | Pl, Pet | [13, 19, 20] | |
| WT1 | Pl, Pet | [21, 22] | |
| Mesothelin | Pl, Pet | [4, 23] | |
| Podoplanin | Pl, Pet | [24, 25] | |
| Aquaporin 1 | Pet | [20] | |
| Na+/K+−ATPase | Pet | [20] | |
| SLC | Pet | [20] | |
| CD40 | Pet | IFN-γ, TNF-α | [29] |
| HCAM (CD44) | Pl, Pet | IL-1, EGF, PDGF | [30, 31] |
| ICAM-1 (CD54) | Pl, Pet | IL-1, TNF-α, IFN-γ | [26, 32–34] |
| VCAM-1 (CD106) | Pl, Pet | IL-1, TNF-α, IFN-γ | [26, 32–34] |
| ALCAM (CD166) | Pet | [25] | |
| Cytokines or growth factors | |||
| IL-1 | Pl, Pet | EGF, TNF-α, LPS | [35, 36] |
| IL-6 | Pl, Pet | TNF-α, IL-1 | [36, 37] |
| IL-8 | Pl, Pet | IL-1, TNF-α, LPS | [32, 37–39] |
| IL15 | Per | IFN-γ, TNF-α | [29] |
| CSF (G, GM, M) | Pl, Pet | IL-1, TNF-α, EGF, LPS | [35, 36] |
| MCP-1 | Pl, Pet | IL-1, TNF-α, IFN-γ | [35, 36] |
| RANTES | Pet | IL-1, TNF-α, LPS | [29, 40] |
| VEGF | Pl, Pet | IL-1, TNF-α, TGF-β | [41–46] |
| FGF | Pl, Pet | IL-1 | [47] |
| TGF-β | Pl, Pet | IL-1, hypoxia | [48–51] |
| PDGF | Pl, Pet | [52, 53] | |
| ET-1 | Pl | [54] | |
| IGF-1 | Pl | [55] | |
| KGF | Pl | [56] | |
| HGF | Pl | [56] | |
| HB-EGF | Pet | [31, 33] | |
| HIF | Pl, Pet | hypoxia | [46] |
| MMP | Pl, Pet | [14, 46, 57–59] | |
| Snail-1 | Pl, Pet | [14, 46] | |
| ECM related molecules | |||
| Collagen I | Pl, Pet | IL-1, TNF-α, EGF, PDGF | [65–75] |
| Collagen III | Pl, Pet | TGF-β, EGF, PDGF, hypoxia | [65–75] |
| Collagen IV | Pl | ||
| Elastin | Pl | [65] | |
| Fibronectin | Pl, Pet | IL-1 | [65] |
| Laminin | Pl | [65] | |
| Hyalronan | Per | [79, 96] | |
| Coagulation cascade proteins | |||
| TF | Pl | [81–83] | |
| tPA | Pl, Pet | TNF-α | [85–90] |
| uPA | Pet | TGF-β | [85, 87–92] |
| PAI-1 | Pl, Pet | IL-1, TNF-α, TGF-β | [85–90, 92] |
MC expresses additional biochemical markers suggesting an active role of these cells in fluid transport, initiation and resolution of inflammation. These biochemical markers include aquaporin 1, sodium-potassium adenosine triphosphatase (Na+/K+-ATPase), sodium bicarbonate cotransporter (SLC) [20], integrin β1 (CD29) [26–28], CD40 as a member of the tumor necrosis factor (TNF)-receptor superfamily [29], homing cell adhesion molecule (HCAM, CD44) [30, 31], intercellular cell adhesion molecule 1 (ICAM-1, CD54), vascular cell adhesion molecule 1 (VCAM-1, CD106) [26, 32–34] and activated leukocyte cell adhesion molecule (ALCAM, CD166) [25].
Production of cytokines and growth factors
MC produces several cytokines spontaneously or after stimulation, such as interleukin 1 (IL-1) [35, 36] IL-6 [36, 37], IL-8 [32, 37–39] and IL-15 [29] granulocyte colony stimulating factor (G-CSF), granulocyte monocyte CSF (GM-CSF), macrophage CSF (M-CSF), monocyte chemoattractant protein-1 (MCP-1) [35, 36] and regulated on activation normal T expressed and secreted chemokine (RANTES) [29, 40]. MC also synthesizes vascular endothelial growth factor (VEGF) [41–46], basic fibroblast growth factor (bFGF) [47], transforming growth factor β (TGF-β) [48–51], platelet-derived growth factor (PDGF) [52, 53], endothelin-1 [54], insulin-like growth factor (IGF) [55], keratinocyte growth factor (KGF) and hepatocyte growth factor (HGF) [56], heparin-binding epidermal growth factor-like growth factor (HB-EGF) [31, 33], Hypoxia-inducible factor (HIF) [46], metalloproteinase (MMP) [14, 46, 57–59] and Snail-1 (known as a zinc finger transcriptional repressor) [14, 46]. Finally, MCs are able to produce both reactive oxygen species (ROS) such as nitric oxide (NO) and ROS-scavengers, in particular under presence of stressors such as lipopolysaccharides (LPS), asbestos, methylglyoxal (MGO) and advanced glycation end products (AGEs) [45, 60–64].
Synthesis of extracellular matrix (ECM)
MC synthesizes extracellular matrix (ECM)-related molecules such as type I, III, and IV collagen, elastin, fibronectin, laminin and proteoglycans. The production level of ECM is increased by IL-1β, TNF-α, EGF, and TGF-β [65–75]. The renin-angiotensin system or AGEs also stimulates ECM production [76, 77]. MC provides a protective and non-adhesive surface for intracoelomic organs and tissues. The microvilli on the surface of MC (Figure 1F) secrete a protective barrier, “glycocalyx”, composed by glycosaminoglycans (GAGs) that may protect the body against infection and tumor dissemination [78], in particular hyaluronan, which has a high hydrophilicity by forming a hydrated gel polymer [1, 2, 79]. Meanwhile, MCs also produce fibronectin through a TGF-β receptor 1/RAC1/SMAD-dependent signaling pathway in the presence of TGF-β1 from ovarian cancer cells [80]. The activated MCs, “cancer-associated MCs” may promote metastasis by supporting tumor cell adhesion, invasion, and proliferation.
Procoagulant and fibrinolytic properties
MC maintains a balance between procoagulant and fibrinolytic activation by producing a whole range of corresponding regulators. MC expresses a powerful procoagulant, tissue factor (TF), which form fibrin by cleaving fibrinogen [81–83]. MC also expresses TF pathway inhibitor [84]. On the other hand, MC produces fibrinolytic activators such as tissue plasminogen activator (tPA) [85–90] urokinase plasminogen activator (uPA) and uPA receptor (uPA-R) [85, 87–92]. MC also secretes the corresponding inhibitor, plasminogen activator inhibitor 1 (PAI-1) and this secretion is regulated by TGF-β, thrombin and other inflammatory factors such as lipopolysaccharide (LPS), TNF-α, and IL-1 [85–90, 92]. MC defects and lesions cause an unbalance between procoagulant and fibrinotic properties and formation of fibrin bands between tissue and organs is observed. These bands eventually develop to fibrous adhesion that can be observed in postoperative intra-abdominal and pelvic adhesions [93], and similarly in pleural fibrosis [8].
Hyaluronan synthesis and recognition
Hyaluronan (HA) is a non-sulfated, linear GAG composed of repeating disaccharides of β-(1, 4) glucuronic acid (GlcUA) and β-(1, 3) N-acetyl glucosamine (GlcNAc). HA is synthesized by three synthase (HAS) proteins. HA play crucial roles in structuring tissue architecture, in cell motility, in cell adhesion, and in proliferation processes [94]. MC generates predominantly large HA (HMW-HA) with a high molecular weight between 200 and 2,000 kDa. HA catabolism is mediated by hyaluronidases, mechanical forces, and oxidative stress. The degradation generates HA polymers of smaller sizes, abbreviated low molecular weight-HA (LMW-HA; <200 kDa) and HA oligomers [95]. Generally, LMW-HA has a pro-inflammatory and carcinogenetic function, whereas HMW-HA has the opposite functions [94]. HA of MC increases the synthesis of by inflammation, including exposition to non-physiological solutions such as peritoneal dialysis. Increased HA levels can induce EMT in MC under physiological conditions, which is essential for cell migration during wound healing and re-mesothelialization [79, 96].
Meanwhile, CD44, the principal receptor for HA [97] is involved in binding gastric cancer [98, 99] and ovarian cancer cells [100] to the mesothelium. HA-CD44 interaction is required for the extravasation of activated T cells from circulating blood to inflammatory sites [101]. There is also evidence that the HA-binding ability of CD44 correlates with the suppressor activity of CD4+/CD25+ regulatory T cells [102]. CD44 expression on MC has also been reported in tissue cultured MCs [103] or in the human hyperplastic mesothelium in vivo [104], although a recent in vivo study showed that intact mesothelium lacked CD44 expression [105]. High CD44 expression in cultured MCs could be explained by the isolation method, by the different composition of growth factors like HB-EGF in the culture medium [106] or by cells undergoing EMT [96]. Various post-translational modifications of CD44, including glycosylation, chondroitin sulfate addition, and sulfation could affect the HA-binding ability of this surface receptor. In spite of this extensive body of evidence, the membrane based regulation of CD44’s hyaluronan-binding ability has not yet been clarified [107].
Sialic acid synthesis and recognition
Sialic acid (Sias) is a diverse family of molecules found at the outer edge of the glycan forest covering all vertebrate cells [108]. Given their high expression and ubiquitous location, Sias has many roles in biology, evolution and disease. The two most common mammalian Sias are N-acetylneuraminic acid (Neu5Ac) and N-glycolylneuraminic acid (Neu5Gc). Neu5Gc is hydroxylated from Neu5Ac by cytidine monophosphate-N-acetylneuraminic acid hydroxylase (CMAH). Humans cannot synthesize Neu5Gc due to inactivation of the CMAH gene during phylogenesis (about 2.8 million years ago) [109]. In spite of this inactivation, small amounts of Neu5Gc were detected using antibodies and high performance liquid chromatography and mass spectrometry analyses (HPLC-MS) in normal human epithelia and endothelia, and larger amounts are found in human carcinomas and inflamed tissues [110]. Notably, human cells express the Sias-binding immunoglobulin-like lectins (Siglecs), a family of immunomodulatory receptors whose functions are regulated by their glycan ligands. Siglecs are attractive therapeutic targets because of their cell type-specific expression pattern, endocytic properties, high expression on certain lymphoma/leukemia, and their ability to modulate receptor signaling [111]. Although only a few studies have been published on Sias in MCs, Neu5Gc were detected in malignant mesothelioma [112] and Sias-binding lectin (SBL) induced selective apoptosis in malignant mesothelioma cells in combination with tumor necrosis factor-related apoptosis inducing ligand (TRAIL) [113]. Otherwise, mucin 16 (MUC-16), a cell surface mucin expressed at high levels by epithelial ovarian tumors and its repeating domain is detected in the serum of cancer patients as the tumor marker, cancer antigen 125 (CA-125). Interestingly CA-125 is also well known as MC marker [114]. MUC16 binds to Siglec-9, which is an inhibitory receptor attenuating T cell and NK cell, and likely mediates inhibition of anti-tumor immune responses [115] or contribute to tolerance of the fetal allograft from maternal responses [116].
Immunoactive or regulatory properties
MCs also express toll-like receptors (TLRs) that can detect microbial components ubiquitous to most microbes and induce inflammation by activation of nuclear factor-κB (NF-κB) and signaling transduction pathways, and induction of chemokines [117, 118]. TLR-4 expression of human peritoneal cell is increased in murine after LPS stimulation [118]. Interestingly TLR-4 is also an important receptor of HA [95]. Meanwhile, recent studies of human malignant mesotheliomas showed that mesothelial tumorigenic cells escape from the control of the immune system through suppression of the proliferation and functions of T lymphocytes and increased recruitment of immunosuppressive regulatory T cells [119]. Furthermore, benign MCs also may suppress proliferation of pro-inflammatory γδ T cells as well as of CD4+ and CD8+ T cells by secreting the immunosuppressor TGF-β [120]. Other researchers also indicated that CD90+/CD45− MCs from human peritoneal fluid could immunosuppress CD4+ T cells through expression of arginase [121]. These findings suggest that role of HA-CD44 or Sias-Siglecs interactions in the immunomodulatory mechanism of MCs should be researched more actively.
Epithelial to mesenchymal transition (EMT)
Epithelial to mesenchymal transition (EMT) occurs when MC loses their epithelial-like characteristics, including dissolution of cell-cell junctions, tight junctions, adherence junctions and desmosomes, and loss of apical-basolateral polarity, and acquire a mesenchymal phenotype, characterized by actin reorganization and stress fiber formation, migration, and invasion [122]. Several study associated with peritoneal dialysis therapy have shown that TGF-β1 signaling play a key role in EMT [123–125], following inducers, for example, integrins/integrin-linked kinase (ILK), Notch, NF-κB, phosphatidylinositol 3-kinase (PI3K)/Akt/mTOR pathway, extracellular-signal regulated kinases 1/2 (ERKs1/2), TGF-β activated kinase-1 (TAK1), c-jun-N terminal kinase (JNK) [126–130]. At the early stage EMT is a reversible process and the following factors promote mesenchymal to epithelial transition (MET) or modulate EMT; HGF, bone morphogenetic protein-7 (BMP-7) [131–133], Smad7 [134–136], and p38 mitogen-activated protein (MAP) kinase [137]. Meanwhile, recent genetic lineage analysis produced a new insight of the primary source of the myofibroblasts observed in peritoneal fibrosis; submesothelial fibroblasts were the major precursors of myofibroblasts during peritoneal fibrogenesis, and the surviving MCs serve as the principal cells for mesothelium repair, arguing against the transition of MCs to myofibroblasts via EMT [138]. Although a lot of works need to clarify the biological role of MCs during serosal inflammation and tissue repair, such as pleural and peritoneal fibrogenesis and adhesion formation, MCs may play a key role, contributing by balancing EMT/reversible EMT and procoagulant/fibrinolytic properties [8, 139].
Visceral adipose tissue development and remodeling
MCs might also play a role in the development and remodeling of visceral adipose tissue. MCs line visceral white adipose tissue (WAT), such as omental adipose tissue. Visceral adiposity is known to be a higher risk factor for chronic metabolic disease, such as type 2 diabetes or cardiovascular complications, than subcutaneous adipose tissue [140, 141]. Omental MCs show proinflammatory phenotype in obesity [142] and lineage tracing showed that intra-abdominal WAT has a different embryological origin that subcutaneous WAT [9, 143]. Beside WT1 and mesothelin, MCs also express adipose precursors markers such as CD29, CD34 and Sca1. Epicardium-derived cell cultures suggest that MCs differentiate into chondrocytes, osteocytes and adipocyte [10, 144]. MCs can respond to proinflammatory signals through TLR pathways and secrete cytokines as described above, so that a role of MCs in the development of a systemic inflammatory response in morbid adiposity can be postulated. Further research is required, however, to further explore the interaction of MCs with visceral adipocyte, in particular to determine how MCs are involved in the development and remodeling of visceral adipose tissue.
Conclusions
MC plays decisive roles in health and disease. The mesothelium surfaces are not just a membrane and should be considered as polyvalent organs. Diseases of the serosal surfaces, such as peritonitis or peritoneal carcinomatosis, are often life-threatening. Further research is needed to better understand the various functions of MCs in order to develop effective therapies for these diseases.
Acknowledgments
I thank Prof. Marc A. Reymond for his critical reading of the manuscript and helpful suggestions.
Author contributions: The author has accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
References
1. Mutsaers SE. Mesothelial cells: their structure, function and role in serosal repair. Respirology 2002;7:171–91.10.1046/j.1440-1843.2002.00404.xSearch in Google Scholar
2. Mutsaers SE. The mesothelial cell. Int J Biochem Cell Biol 2004;36:9–16.10.1016/S1357-2725(03)00242-5Search in Google Scholar
3. Michailova KN, Usunoff KG. Serosal membranes (pleura, pericardium, peritoneum). Normal structure, development and experimental pathology. Adv Anat Embryol Cell Biol 2006;183:i-vii, 1–144.Search in Google Scholar
4. Kanamori-Katayama M, Kaiho A, Ishizu Y, Okamura-Oho Y, Hino O, Abe M, et al. LRRN4 and UPK3B are markers of primary mesothelial cells. PLoS One 2011;6:e25391.10.1371/journal.pone.0025391Search in Google Scholar
5. Shelton EL, Galindo CL, Williams CH, Pfaltzgraff E, Hong CC, Bader DM. Autotaxin signaling governs phenotypic heterogeneity in visceral and parietal mesothelia. PLoS One 2013;8:e69712.10.1371/journal.pone.0069712Search in Google Scholar
6. Lua I, Li Y, Pappoe LS, Asahina K. Myofibroblastic conversion and regeneration of mesothelial cells in peritoneal and liver fibrosis. Am J Pathol 2015;185:3258–73.10.1016/j.ajpath.2015.08.009Search in Google Scholar
7. Książek K. Mesothelial cell: a multifaceted model of aging. Ageing Res Rev 2013;12:595–604.10.1016/j.arr.2013.01.008Search in Google Scholar
8. Mutsaers SE, Birnie K, Lansley S, Herrick SE, Lim CB, Prêle CM. Mesothelial cells in tissue repair and fibrosis. Front Pharmacol 2015;6:113.10.3389/fphar.2015.00113Search in Google Scholar
9. Chau YY, Bandiera R, Serrels A, Martínez-Estrada OM, Qing W, Lee M, et al. Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source. Nat Cell Biol 2014;16:367–75.10.1038/ncb2922Search in Google Scholar
10. Liu Q, Huang X, Oh JH, Lin RZ, Duan S, Yu Y, et al. Epicardium-to-fat transition in injured heart. Cell Res 2014;24:1367–9.10.1038/cr.2014.125Search in Google Scholar
11. Wu YJ, Parker LM, Binder NE, Beckett MA, Sinard JH, Griffiths CT, et al. The mesothelial keratins: a new family of cytoskeletal proteins identified in cultured mesothelial cells and nonkeratinizing epithelia. Cell 1982;31:693–703.10.1016/0092-8674(82)90324-5Search in Google Scholar
12. Chung-Welch N, Patton WF, Yen-Patton GP, Hechtman HB, Shepro D. Phenotypic comparison between mesothelial and microvascular endothelial cell lineages using conventional endothelial cell markers, cytoskeletal protein markers and in vitro assays of angiogenic potential. Differentiation 1989;42:44–53.10.1111/j.1432-0436.1989.tb00606.xSearch in Google Scholar
13. Ito T, Yorioka N, Yamamoto M, Kataoka K, Yamakido M. Effect of glucose on intercellular junctions of cultured human peritoneal mesothelial cells. J Am Soc Nephrol 2000;11:1969–79.10.1681/ASN.V11111969Search in Google Scholar
14. Sivertsen S, Hadar R, Elloul S, Vintman L, Bedrossian C, Reich R, et al. Expression of Snail, Slug and Sip1 in malignant mesothelioma effusions is associated with matrix metalloproteinase, but not with cadherin expression. Lung Cancer 2006;54:309–17.10.1016/j.lungcan.2006.08.010Search in Google Scholar
15. Zhang K, Zhang H, Zhou X, Tang WB, Xiao L, Liu YH, et al. miRNA589 regulates epithelial-mesenchymal transition in human peritoneal mesothelial cells. J Biomed Biotechnol 2012;2012:673096.10.1155/2012/673096Search in Google Scholar
16. Ye Z, Li M, Mei Z, Zhen G, Zhang P. The effects and mechanisms of interleukin-22 and interferon-γ on epithelial-mesenchymal transition of pleural mesothelial cells. Zhonghua Jie He He Hu Xi Za Zhi 2015;38:501–6.Search in Google Scholar
17. Davidson B, Nielsen S, Christensen J, Asschenfeldt P, Berner A, Risberg B, et al. The role of desmin and N-cadherin in effusion cytology: a comparative study using established markers of mesothelial and epithelial cells. Am J Surg Pathol 2001;25:1405–12.10.1097/00000478-200111000-00008Search in Google Scholar
18. Ando T, Jordan P, Wang Y, Jennings MH, Harper MH, Houghton J, et al. Homogeneity of mesothelial cells with lymphatic endothelium: expression of lymphatic endothelial markers by mesothelial cells. Lymphat Res Biol 2005;3:117–25.10.1089/lrb.2005.3.117Search in Google Scholar
19. Patel P, Sekiguchi Y, Oh KH, Patterson SE, Kolb MR, Margetts PJ. Smad3-dependent and -independent pathways are involved in peritoneal membrane injury. Kidney Int 2010;77:319–28.10.1038/ki.2009.436Search in Google Scholar
20. Lachaud CC, Soria F, Escacena N, Quesada-Hernández E, Hmadcha A, Alió J, et al. Mesothelial cells: a cellular surrogate for tissue engineering of corneal endothelium. Invest Ophthalmol Vis Sci 2014;55:5967–78.10.1167/iovs.14-14706Search in Google Scholar
21. Karki S, Surolia R, Hock TD, Guroji P, Zolak JS, Duggal R, et al. Wilms’ tumor 1 (Wt1) regulates pleural mesothelial cell plasticity and transition into myofibroblasts in idiopathic pulmonary fibrosis. FASEB J 2014;28:1122–31.10.1096/fj.13-236828Search in Google Scholar
22. Duim SN, Kurakula K, Goumans MJ, Kruithof BP. Cardiac endothelial cells express Wilms’ tumor-1: Wt1 expression in the developing, adult and infarcted heart. J Mol Cell Cardiol 2015 Apr;81:127–35.10.1016/j.yjmcc.2015.02.007Search in Google Scholar
23. Ma J, Tang WK, Esser L, Pastan I, Xia D. Recognition of mesothelin by the therapeutic antibody MORAb-009: structural and mechanistic insights. J Biol Chem 2012;287:33123–31.10.1074/jbc.M112.381756Search in Google Scholar
24. Schacht V, Dadras SS, Johnson LA, Jackson DG, Hong YK, Detmar M. Up-regulation of the lymphatic marker podoplanin, a mucin-type transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumors. Am J Pathol 2005;166:913–21.10.1016/S0002-9440(10)62311-5Search in Google Scholar
25. Asahina K, Tsai SY, Li P, Ishii M, Maxson Jr RE, Sucov HM, et al. Mesenchymal origin of hepatic stellate cells, submesothelial cells, and perivascular mesenchymal cells during mouse liver development. Hepatology 2009;49:998–1011.10.1002/hep.22721Search in Google Scholar
26. Yuan ML, Tong ZH, Jin XG, Zhang JC, Wang XJ, Ma WL, et al. Regulation of CD4(+) T cells by pleural mesothelial cells via adhesion molecule-dependent mechanisms in tuberculous pleurisy. PLoS One 2013;8:e74624.10.1371/journal.pone.0074624Search in Google Scholar
27. Kim YD, Jun YJ, Kim J, Kim CK. Effects of human adipose-derived stem cells on the regeneration of damaged visceral pleural mesothelial cells: a morphological study in a rabbit model. Interact Cardiovasc Thorac Surg 2014;19:363–7.10.1093/icvts/ivu124Search in Google Scholar
28. do Amaral RJ, Benac P, Andrade LR, Farina M, Bernardazzi C, Arcanjo KD, et al. Peritoneal submesothelial stromal cells support hematopoiesis and differentiate into osteogenic and adipogenic cell lineages. Cells Tissues Organs 2014;20:118–31.10.1159/000377624Search in Google Scholar
29. Basok A, Shnaider A, Man L, Chaimovitz C, Douvdevani A. CD40 is expressed on human peritoneal mesothelial cells and upregulates the production of interleukin-15 and RANTES. J Am Soc Nephrol 2001;12:695–702.10.1681/ASN.V124695Search in Google Scholar
30. Gardner MJ, Jones LM, Catterall JB, Turner GA. Expression of cell adhesion molecules on ovarian tumour cell lines and mesothelial cells, in relation to ovarian cancer metastasis. Cancer Lett 1995;91:229–34.10.1016/0304-3835(95)03743-GSearch in Google Scholar
31. Faull RJ, Stanley JM, Fraser S, Power DA, Leavesley DI. HB-EGF is produced in the peritoneal cavity and enhances mesothelial cell adhesion and migration. Kidney Int 2001;59:614–24.10.1046/j.1523-1755.2001.059002614.xSearch in Google Scholar
32. Jonjić N, Peri G, Bernasconi S, Sciacca FL, Colotta F, Pelicci P, et al. Expression of adhesion molecules and chemotactic cytokines in cultured human mesothelial cells. J Exp Med 1992;176:1165–74.10.1084/jem.176.4.1165Search in Google Scholar
33. Jayne DG, Perry SL, Morrison E, Farmery SM, Guillou PJ. Activated mesothelial cells produce heparin-binding growth factors: implications for tumour metastases. Br J Cancer 2000;82:1233–8.10.1054/bjoc.1999.1068Search in Google Scholar
34. Klein CL, Bittinger F, Skarke CC, Wagner M, Köhler H, Walgenbach S, et al. Effects of cytokines on the expression of cell adhesion molecules by cultured human omental mesothelial cells. Pathobiology 1995;63:204–12.10.1159/000163953Search in Google Scholar
35. Demetri GD, Zenzie BW, Rheinwald JG, Griffin JD. Expression of colony-stimulating factor genes by normal human mesothelial cells and human malignant mesothelioma cells lines in vitro. Blood 1989 Aug;15:940–6.10.1182/blood.V74.3.940.940Search in Google Scholar
36. Lanfrancone L, Boraschi D, Ghiara P, Falini B, Grignani F, Peri G, et al. Human peritoneal mesothelial cells produce many cytokines (granulocyte colony-stimulating factor [CSF], granulocyte-monocyte-CSF, macrophage-CSF, interleukin-1 [IL-1], and IL-6) and are activated and stimulated to grow by IL-1. Blood 1992;1:2835–42.10.1182/blood.V80.11.2835.2835Search in Google Scholar
37. Topley N, Brown Z, Jörres A, Westwick J, Davies M, Coles GA, et al. Human peritoneal mesothelial cells synthesize interleukin-8. Synergistic induction by interleukin-1 beta and tumor necrosis factor-alpha. Am J Pathol 1993;142:1876–86.Search in Google Scholar
38. Boylan AM, Rüegg C, Kim KJ, Hébert CA, Hoeffel JM, Pytela R, et al. Evidence of a role for mesothelial cell-derived interleukin 8 in the pathogenesis of asbestos-induced pleurisy in rabbits. J Clin Invest 1992;89:1257–67.10.1172/JCI115710Search in Google Scholar
39. Betjes MG, Tuk CW, Struijk DG, Krediet RT, Arisz L, Hart M, et al. Interleukin-8 production by human peritoneal mesothelial cells in response to tumor necrosis factor-alpha, interleukin-1, and medium conditioned by macrophages cocultured with Staphylococcus epidermidis. J Infect Dis 1993;168:1202–10.10.1093/infdis/168.5.1202Search in Google Scholar
40. Li FK, Davenport A, Robson RL, Loetscher P, Rothlein R, Williams JD, et al. Leukocyte migration across human peritoneal mesothelial cells is dependent on directed chemokine secretion and ICAM-1 expression. Kidney Int 1998;54:2170–83.10.1046/j.1523-1755.1998.00174.xSearch in Google Scholar
41. Gary Lee YC, Melkerneker D, Thompson PJ, Light RW, Lane KB. Transforming growth factor beta induces vascular endothelial growth factor elaboration from pleural mesothelial cells in vivo and in vitro. Am J Respir Crit Care Med 2002;165:88–94.10.1164/ajrccm.165.1.2104006Search in Google Scholar
42. Mandl-Weber S, Cohen CD, Haslinger B, Kretzler M, Sitter T. Vascular endothelial growth factor production and regulation in human peritoneal mesothelial cells. Kidney Int 2002;61:570–8.10.1046/j.1523-1755.2002.00143.xSearch in Google Scholar
43. Acencio MM, Vargas FS, Marchi E, Carnevale GG, Teixeira LR, Antonangelo L, et al. Pleural mesothelial cells mediate inflammatory and profibrotic responses in talc-induced pleurodesis. Lung 2007;185:343–8.10.1007/s00408-007-9041-ySearch in Google Scholar
44. Shukla A, MacPherson MB, Hillegass J, Ramos-Nino ME, Alexeeva V, Vacek PM, et al. Alterations in gene expression in human mesothelial cells correlate with mineral pathogenicity. Am J Respir Cell Mol Biol 2009;41:114–23.10.1165/rcmb.2008-0146OCSearch in Google Scholar
45. Hong FY, Bao JF, Hao J, Yu Q, Liu J. Methylglyoxal and advanced glycation end-products promote cytokines expression in peritoneal mesothelial cells via MAPK signaling. Am J Med Sci 2015;349:105–9.10.1097/MAJ.0000000000000394Search in Google Scholar
46. Morishita Y, Ookawara S, Hirahara I, Muto S, Nagata D. HIF-1α mediates Hypoxia-induced epithelial-mesenchymal transition in peritoneal mesothelial cells. Ren Fail 2016;38:282–9.10.3109/0886022X.2015.1127741Search in Google Scholar
47. Cronauer MV, Stadlmann S, Klocker H, Abendstein B, Eder IE, Rogatsch H, et al. Basic fibroblast growth factor synthesis by human peritoneal mesothelial cells: induction by interleukin-1. Am J Pathol 1999;155:1977–84.10.1016/S0002-9440(10)65516-2Search in Google Scholar
48. Offner FA, Feichtinger H, Stadlmann S, Obrist P, Marth C, Klingler P, et al. Transforming growth factor-beta synthesis by human peritoneal mesothelial cells. Induction by interleukin-1. Am J Pathol 1996;148:1679–88.Search in Google Scholar
49. Coker RK, Laurent GJ, Shahzeidi S, Lympany PA, du Bois RM, Jeffery PK, et al. Transforming growth factors-beta 1, -beta 2, and -beta 3 stimulate fibroblast procollagen production in vitro but are differentially expressed during bleomycin-induced lung fibrosis. Am J Pathol 1997;150:981–91.Search in Google Scholar
50. Abendstein B, Stadlmann S, Knabbe C, Buck M, Müller-Holzner E, Zeimet AG, et al. Regulation of transforming growth factor-beta secretion by human peritoneal mesothelial and ovarian carcinoma cells. Cytokine 2000;12:1115–19.10.1006/cyto.1999.0632Search in Google Scholar
51. Saed GM, Zhang W, Chegini N, Holmdahl L, Diamond MP. Transforming growth factor beta isoforms production by human peritoneal mesothelial cells after exposure to hypoxia. Am J Reprod Immunol 2000;43:285–91.10.1111/j.8755-8920.2000.430507.xSearch in Google Scholar
52. Versnel MA, Hagemeijer A, Bouts MJ, van der Kwast TH, Hoogsteden HC. Expression of c-sis (PDGF B-chain) and PDGF A-chain genes in ten human malignant mesothelioma cell lines derived from primary and metastatic tumors. Oncogene 1988;2:601–5.Search in Google Scholar
53. Patel P, West-Mays J, Kolb M, Rodrigues JC, Hoff CM, Margetts PJ. Platelet derived growth factor B and epithelial mesenchymal transition of peritoneal mesothelial cells. Matrix Biol 2010;29:97–106.10.1016/j.matbio.2009.10.004Search in Google Scholar
54. Kimura I, Sakamoto Y, Shibasaki M, Kobayashi Y, Matsuo H. Release of endothelins and platelet-activating factor by a rat pleural mesothelial cell line. Eur Respir J 2000;15:170–6.10.1183/09031936.00.15117000Search in Google Scholar
55. Lee TC, Zhang Y, Aston C, Hintz R, Jagirdar J, Perle MA, et al. Normal human mesothelial cells and mesothelioma cell lines express insulin-like growth factor I and associated molecules. Cancer Res 1993;53:2858–64.Search in Google Scholar
56. Adamson IY, Bakowska J. KGF and HGF are growth factors for mesothelial cells in pleural lavage fluid after intratracheal asbestos. Exp Lung Res 2001;27:605–16.10.1080/019021401753181854Search in Google Scholar
57. Marshall BC, Santana A, Xu QP, Petersen MJ, Campbell EJ, Hoidal JR, et al. Metalloproteinases and tissue inhibitor of metalloproteinases in mesothelial cells. Cellular differentiation influences expression. J Clin Invest 1993;91:1792–9.10.1172/JCI116390Search in Google Scholar
58. Rougier JP, Moullier P, Piedagnel R, Ronco PM. Hyperosmolality suppresses but TGF beta 1 increases MMP9 in human peritoneal mesothelial cells. Kidney Int 1997;51:337–47.10.1038/ki.1997.42Search in Google Scholar
59. Ma C, Tarnuzzer RW, Chegini N. Expression of matrix metalloproteinases and tissue inhibitor of matrix metalloproteinases in mesothelial cells and their regulation by transforming growth factor-beta1. Wound Repair Regen 1999;7:477–85.10.1046/j.1524-475X.1999.00477.xSearch in Google Scholar
60. Choe N, Tanaka S, Kagan E. Asbestos fibers and interleukin-1 upregulate the formation of reactive nitrogen species in rat pleural mesothelial cells. Am J Respir Cell Mol Biol 1998;19:226–36.10.1165/ajrcmb.19.2.3111Search in Google Scholar
61. Owens MW, Milligan SA, Grisham MB. Nitric oxide synthesis by rat pleural mesothelial cells: induction by growth factors and lipopolysaccharide. Exp Lung Res 1995;21:731–42.10.3109/01902149509050839Search in Google Scholar
62. Hillegass JM, Shukla A, MacPherson MB, Lathrop SA, Alexeeva V, Perkins TN, et al. Mechanisms of oxidative stress and alterations in gene expression by Libby six-mix in human mesothelial cells. Part Fibre Toxicol 2010;7:26.10.1186/1743-8977-7-26Search in Google Scholar
63. Thompson JK, Westbom CM, MacPherson MB, Mossman BT, Heintz NH, Spiess P, et al. Asbestos modulates thioredoxin-thioredoxin interacting protein interaction to regulate inflammasome activation. Part Fibre Toxicol 2014;11:24.10.1186/1743-8977-11-24Search in Google Scholar
64. Yu M, Chen R, Jia Z, Chen J, Lou J, Tang S, et al. MWCNTs induce ROS generation, ERK phosphorylation, and SOD-2 expression in human mesothelial cells. Int J Toxicol 2016;35:17–26.10.1177/1091581815591223Search in Google Scholar
65. Harvey W, Amlot PL. Collagen production by human mesothelial cells in vitro. J Pathol 1983;139:337–47.10.1002/path.1711390309Search in Google Scholar
66. Rennard SI, Jaurand MC, Bignon J, Kawanami O, Ferrans VJ, Davidson J, et al. Role of pleural mesothelial cells in the production of the submesothelial connective tissue matrix of lung. Am Rev Respir Dis 1984;130:267–74.10.1164/arrd.1984.130.2.267Search in Google Scholar
67. Kuwahara M, Kuwahara M, Bijwaard KE, Gersten DM, Diglio CA, Kagan E. Mesothelial cells produce a chemoattractant for lung fibroblasts: role of fibronectin. Am J Respir Cell Mol Biol 1991 Sep;5:256–64.10.1165/ajrcmb/5.3.256Search in Google Scholar
68. Owens MW, Grimes SR. Pleural mesothelial cell response to inflammation: tumor necrosis factor-induced mitogenesis and collagen synthesis. Am J Physiol 1993;265:L382–8.10.1152/ajplung.1993.265.4.L382Search in Google Scholar
69. Owens MW, Milligan SA. Growth factor modulation of rat pleural mesothelial cell mitogenesis and collagen synthesis. Effects of epidermal growth factor and platelet-derived factor. Inflammation 1994;18:77–87.10.1007/BF01534600Search in Google Scholar
70. Kuwahara M, Kuwahara M, Verma K, Ando T, Hemenway DR, Kagan E. Asbestos exposure stimulates pleural mesothelial cells to secrete the fibroblast chemoattractant, fibronectin. Am J Respir Cell Mol Biol 1994;10:167–76.10.1165/ajrcmb.10.2.8110473Search in Google Scholar
71. Owens MW, Milligan SA, Grisham MB. Inhibition of pleural mesothelial cell collagen synthesis by nitric oxide. Free Radic Biol Med 1996;21:601–7.10.1016/0891-5849(96)00159-1Search in Google Scholar
72. Saed GM, Zhang W, Chegini N, Holmdahl L, Diamond MP. Alteration of type I and III collagen expression in human peritoneal mesothelial cells in response to hypoxia and transforming growth factor-beta1. Wound Repair Regen 1999;7:504–10.10.1046/j.1524-475X.1999.00504.xSearch in Google Scholar
73. Yang WS, Kim BS, Lee SK, Park JS, Kim SB. Interleukin-1beta stimulates the production of extracellular matrix in cultured human peritoneal mesothelial cells. Perit Dial Int 1999;19:211–20.10.1177/089686089901900306Search in Google Scholar
74. Zhang H, Liu FY, Liu YH, Peng YM, Liao Q, Zhang K. Effect of TGF-β1. Stimulation on the smad signal transduction pathway of human peritoneal mesothelial cells. Int J Biomed Sci 2005;1:8–15.Search in Google Scholar
75. Xiao L, Sun L, Liu FY, Peng YM, Duan SB. Connective tissue growth factor knockdown attenuated matrix protein production and vascular endothelial growth factor expression induced by transforming growth factor-beta1 in cultured human peritoneal mesothelial cells. Ther Apher Dial 2010;14:27–34.10.1111/j.1744-9987.2009.00701.xSearch in Google Scholar
76. Noh H, Ha H, Yu MR, Kim YO, Kim JH, Lee HB. Angiotensin II mediates high glucose-induced TGF-beta1 and fibronectin upregulation in HPMC through reactive oxygen species. Perit Dial Int 2005;25:38–47.10.1177/089686080502500110Search in Google Scholar
77. Tong M, Wang Y, Wang Y, Chen H, Wang C, Yang L, et al. Genistein attenuates advanced glycation end product-induced expression of fibronectin and connective tissue growth factor. Am J Nephrol 2012;36:34–40.10.1159/000339168Search in Google Scholar
78. Baumann MH, Strange C, Sahn SA, Kinasewitz GT. Pleural macrophages differentially alter pleural mesothelial cell glycosaminoglycan production. Exp Lung Res 1996;22:101–11.10.3109/01902149609074020Search in Google Scholar
79. Yung S, Chan TM. Pathophysiology of the peritoneal membrane during peritoneal dialysis: the role of hyaluronan. J Biomed Biotechnol 2011;2011:180594.10.1155/2011/180594Search in Google Scholar
80. Kenny HA, Chiang CY, White EA, Schryver EM, Habis M. Mesothelial cells promote early ovarian cancer metastasis through fibronectin secretion. J Clin Invest 2014;124:4614–28.10.1172/JCI74778Search in Google Scholar
81. Kumar A, Koenig KB, Johnson AR, Idell S. Expression and assembly of procoagulant complexes by human pleural mesothelial cells. Thromb Haemost 1994;71:587–92.10.1055/s-0038-1642487Search in Google Scholar
82. Bottles KD, Laszik Z, Morrissey JH, Kinasewitz GT. Tissue factor expression inmesothelial cells: induction both in vivo and in vitro. Am J Respir Cell Mol Biol 1997;17:164–72.10.1165/ajrcmb.17.2.2438Search in Google Scholar
83. Dobbie JW, Jasani MK. Role of imbalance of intracavity fibrin formation and removal in the pathogenesis of peritoneal lesions in CAPD. Perit Dial Int 1997;17:121–4.10.1177/089686089701700204Search in Google Scholar
84. Bajaj MS, Pendurthi U, Koenig K, Pueblitz S, Idell S. Tissue factor pathway inhibitor expression by human pleural mesothelial and mesothelioma cells. Eur Respir J 2000;15:1069–78.10.1034/j.1399-3003.2000.01515.xSearch in Google Scholar
85. van Hinsbergh VW, Kooistra T, Scheffer MA, Hajo van Bockel J, van Muijen GN. Characterization and fibrinolytic properties of human omental tissue mesothelial cells. Comparison with endothelial cells. Blood 1990;75:1490–7.10.1182/blood.V75.7.1490.1490Search in Google Scholar
86. Idell S, Zwieb C, Kumar A, Koenig KB, Johnson AR. Pathways of fibrin turnover of human pleural mesothelial cells in vitro. Am J Respir Cell Mol Biol 1992;7:414–26.10.1165/ajrcmb/7.4.414Search in Google Scholar
87. Sitter T, Spannagl M, Schiffl H, Held E, van Hinsbergh VW, Kooistra T. Imbalance between intraperitoneal coagulation and fibrinolysis during peritonitis of CAPD patients: the role of mesothelial cells. Nephrol Dial Transplant 1995;10:677–83.Search in Google Scholar
88. Sitter T, Toet K, Quax P, Kooistra T. Fibrinolytic activity of human mesothelial cells is counteracted by rapid uptake of tissue-type plasminogen activator. Kidney Int 1999;55:120–9.10.1046/j.1523-1755.1999.00244.xSearch in Google Scholar
89. Rougier JP, Guia S, Hagège J, Nguyen G, Ronco PM. PAI-1 secretion and matrix deposition in human peritoneal mesothelial cell cultures: transcriptional regulation by TGF-beta 1. Kidney Int 1998;54:87–98.10.1046/j.1523-1755.1998.00955.xSearch in Google Scholar
90. Falk P, Ma C, Chegini N, Holmdahl L. Differential regulation of mesothelial cell fibrinolysis by transforming growth factor beta 1. Scand J Clin Lab Invest 2000;60:439–47.10.1080/003655100448419Search in Google Scholar
91. Perkins RC, Broaddus VC, Shetty S, Hamilton S, Idell S. Asbestos upregulates expression of the urokinase-type plasminogen activator receptor on mesothelial cells. Am J Respir Cell Mol Biol 1999;21:637–46.10.1165/ajrcmb.21.5.3225Search in Google Scholar
92. Ivarsson ML, Holmdahl L, Falk P, Mölne J, Risberg B. Characterization and fibrinolytic properties of mesothelial cells isolated from peritoneal lavage. Scand J Clin Lab Invest 1998;58:195–203.10.1080/00365519850186580Search in Google Scholar
93. Maciver AH, McCall M, James Shapiro AM. Intra-abdominal adhesions: cellular mechanisms and strategies for prevention. Int J Surg 2011;9:589–94.10.1016/j.ijsu.2011.08.008Search in Google Scholar
94. Naor D. Editorial: Interaction between hyaluronic acid and its receptors (CD44, RHAMM) regulates the activity of inflammation and cancer. Front Immunol 2016;7:39.10.3389/fimmu.2016.00039Search in Google Scholar
95. Jiang D, Liang J, Noble PW. Hyaluronan as an immune regulator in human diseases. Physiol Rev 2011;91:221–64.10.1152/physrev.00052.2009Search in Google Scholar
96. Yung S, Thomas GJ, Davies M. Induction of hyaluronan metabolism after mechanical injury of human peritoneal mesothelial cells in vitro. Kidney Int 2000;58:1953–62.10.1111/j.1523-1755.2000.00367.xSearch in Google Scholar
97. Borland G, Ross JA, Guy K. Forms and functions of CD44. Immunology 1998;93:139–48.10.1046/j.1365-2567.1998.00431.xSearch in Google Scholar
98. Nishimura S, Chung YS, Yashiro M, Inoue T, Sowa M. CD44H plays an important role in peritoneal dissemination of scirrhous gastric cancer cells. Jpn J Cancer Res 1996;87:1235–44.10.1111/j.1349-7006.1996.tb03138.xSearch in Google Scholar
99. Ohta S, Hiramoto S, Amano Y, Sato M, Suzuki Y, Shinohara M, et al. Production of Cisplatin-Incorporating Hyaluronan Nanogels via Chelating Ligand-Metal Coordination. Bioconjug Chem 2016;27:504–8.10.1021/acs.bioconjchem.5b00674Search in Google Scholar
100. Cannistra SA, Kansas GS, Niloff J, DeFranzo B, Kim Y, Ottensmeier C. Binding of ovarian cancer cells to peritoneal mesothelium in vitro is partly mediated by CD44H. Cancer Res 1993;53:3830–8.Search in Google Scholar
101. DeGrendele HC, Estess P, Siegelman MH. Requirement for CD44 in activated T cell extravasation into an inflammatory site. Science 1997;278:672–5.10.1126/science.278.5338.672Search in Google Scholar
102. Firan M, Dhillon S, Estess P, Siegelman MH. Suppressor activity and potency among regulatory T cells is discriminated by functionally active CD44. Blood 2006;107:619–27.10.1182/blood-2005-06-2277Search in Google Scholar
103. Lai KN, Szeto CC, Lai KB, Lam CW, Chan DT, Leung JC. Increased production of hyaluronan by peritoneal cells and its significance in patients on CAPD. Am J Kidney Dis 1999;33:318–24.10.1016/S0272-6386(99)70307-0Search in Google Scholar
104. Alì G, Borrelli N, Riccardo G, Proietti A, Pelliccioni S, Niccoli C, et al. Differential expression of extracellular matrix constituents and cell adhesion molecules between malignant pleural mesothelioma and mesothelial hyperplasia. J Thorac Oncol 2013;8:1389–95.10.1097/JTO.0b013e3182a59f45Search in Google Scholar
105. Koistinen V, Jokela T, Oikari S, Kärnä R, Tammi M, Rilla K. Hyaluronan-positive plasma membrane protrusions exist on mesothelial cells in vivo. Histochem Cell Biol 2016;145:531–44.10.1007/s00418-016-1405-zSearch in Google Scholar
106. Bennett KL, Jackson DG, Simon JC, Tanczos E, Peach R, Modrell B, et al. CD44 isoforms containing exon V3 are responsible for the presentation of heparin-binding growth factor. J Cell Biol 1995;128:687–98.10.1083/jcb.128.4.687Search in Google Scholar
107. Murai T. Lipid raft-mediated regulation of hyaluronan-CD44 interactions inflammation and cancer. Front Immunol 2015;6:420.10.3389/fimmu.2015.00420Search in Google Scholar
108. Varki A. Glycan-based interactions involving vertebrate sialic-acid-recognizing proteins. Nature 2007;446:1023–9.10.1038/nature05816Search in Google Scholar
109. Chou HH, Hayakawa T, Diaz S, Krings M, Indriati E. Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc Natl Acad Sci USA 2002;99:11736–41.10.1073/pnas.182257399Search in Google Scholar
110. Tangvoranuntakul P, Gagneux P, Diaz S, Bardor M, Varki N, Varki A, et al. Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc Natl Acad Sci USA 2003;100:12045–50.10.1073/pnas.2131556100Search in Google Scholar
111. Angata T, Nycholat CM, Macauley MS. Therapeutic targeting of siglecs using antibody- and glycan-based approaches. Trends Pharmacol Sci 2015;36:645–60.10.1016/j.tips.2015.06.008Search in Google Scholar
112. Tzanakakis GN, Syrokou A, Kanakis I, Karamanos NK. Determination and distribution of N-acetyl- and N-glycolylneuraminic acids in culture media and cell-associated glycoconjugates from human malignant mesothelioma and adenocarcinoma cells. Biomed Chromatogr 2006;20:434–9.10.1002/bmc.573Search in Google Scholar
113. Tatsuta T, Hosono M, Takahashi K, Omoto T, Kariya Y, Sugawara S, et al. Sialic acid-binding lectin (leczyme) induces apoptosis to malignant mesothelioma and exerts synergistic antitumor effects with TRAIL. Int J Oncol 2014;44:377–84.10.3892/ijo.2013.2192Search in Google Scholar
114. Krediet RT. Dialysate cancer antigen 125 concentration as marker of peritoneal membrane status in patients treated with chronic peritoneal dialysis. Perit Dial Int 2001;21:560–7.10.1177/089686080102100605Search in Google Scholar
115. Belisle JA, Horibata S, Jennifer GA, Petrie S, Kapur A. Identification of Siglec-9 as the receptor for MUC16 on human NK cells, B cells, and monocytes. Mol Cancer 2010;9:118.10.1186/1476-4598-9-118Search in Google Scholar
116. Tyler C, Kapur A, Felder M, Belisle JA, Trautman C, Gubbels JA, et al. The mucin MUC16 (CA125) binds to NK cells and monocytes from peripheral blood of women with healthy pregnancy and preeclampsia. Am J Reprod Immunol 2012;68:28–37.10.1111/j.1600-0897.2012.01113.xSearch in Google Scholar
117. Park JH, Kim YG, Shaw M, Kanneganti TD, Fujimoto Y, Fukase K, et al. Nod1/RICK and TLR signaling regulate chemokine and antimicrobial innate immune responses in mesothelial cells. J Immunol 2007;179:514–21.10.4049/jimmunol.179.1.514Search in Google Scholar
118. Kato S, Yuzawa Y, Tsuboi N, Maruyama S, Morita Y, Matsuguchi T, et al. Endotoxin-induced chemokine expression in murine peritoneal mesothelial cells: the role of toll-like receptor 4. J Am Soc Nephrol 2004;15:1289–99.Search in Google Scholar
119. Hegmans JP, Hemmes A, Hammad H, Boon L, Hoogsteden HC, Lambrecht BN. Mesothelioma environment comprises cytokines and T-regulatory cells that suppress immune responses. Eur Respir J 2006;27:1086–95.10.1183/09031936.06.00135305Search in Google Scholar
120. Lin CY, Kift-Morgan A, Moser B, Topley N, Eberl M. Suppression of pro-inflammatory T-cell responses by human mesothelial cells. Nephrol Dial Transplant 2013;28:1743–50.10.1093/ndt/gfs612Search in Google Scholar
121. Kitayama J, Emoto S, Yamaguchi H, Ishigami H, Yamashita H, Seto Y, et al. CD90(+)CD45(−) intraperitoneal mesothelial-like cells inhibit T cell activation by production of arginase I. Cell Immunol 2014;288:8–14.10.1016/j.cellimm.2014.01.008Search in Google Scholar
122. López-Cabrera M. Mesenchymal conversion of mesothelial cells is a key event in the pathophysiology of the peritoneum during peritoneal dialysis. Adv Med 2014;2014:473134.10.1155/2014/473134Search in Google Scholar
123. Lai KN, Lai KB, Lam CW, Chan TM, Li FK, Leung JC. Changes of cytokine profiles during peritonitis in patients on continuous ambulatory peritoneal dialysis. Am J Kidney Dis 2000;35:644–52.10.1016/S0272-6386(00)70011-4Search in Google Scholar
124. Gangji AS, Brimble KS, Margetts PJ. Association between markers of inflammation, fibrosis and hypervolemia in peritoneal dialysis patients. Blood Purif 2009;28:354–8.10.1159/000232937Search in Google Scholar
125. Yao Q, Pawlaczyk K, Ayala ER, Styszynski A, Breborowicz A, Heimburger O, et al. The role of the TGF/Smad signaling pathway in peritoneal fibrosis induced by peritoneal dialysis solutions. Nephron Exp Nephrol 2008;109:e71–8.10.1159/000142529Search in Google Scholar
126. Aroeira LS, Aguilera A, Sánchez-Tomero JA, Bajo MA, del Peso G, Jiménez-Heffernan JA, et al. Epithelial to mesenchymal transition and peritoneal membrane failure in peritoneal dialysis patients: pathologic significance and potential therapeutic interventions. J Am Soc Nephrol 2007;18:2004–13.10.1681/ASN.2006111292Search in Google Scholar
127. González-Mateo GT, Aroeira LS, López-Cabrera M, Ruiz-Ortega M, Ortiz A, Selgas R. Pharmacological modulation of peritoneal injury induced by dialysis fluids: is it an option? Nephrol Dial Transplant 2012 Feb;27:478–81.10.1093/ndt/gfr543Search in Google Scholar
128. Strippoli R, Benedicto I, Perez Lozano ML, Pellinen T, Sandoval P, Lopez-Cabrera M, et al. Inhibition of transforming growth factor-activated kinase 1 (TAK1) blocks and reverses epithelial to mesenchymal transition of mesothelial cells. PLoS One 2012;7:e31492.10.1371/journal.pone.0031492Search in Google Scholar
129. Strippoli R, Benedicto I, Pérez Lozano ML, Cerezo A, López-Cabrera M, del Pozo MA. Epithelial-to-mesenchymal transition of peritoneal mesothelial cells is regulated by an ERK/NF-kappaB/Snail1 pathway. Dis Model Mech 2008;1:264–74.10.1242/dmm.001321Search in Google Scholar
130. Zhu F, Li T, Qiu F, Fan J, Zhou Q, Ding X, et al. Preventive effect of Notch signaling inhibition by a gamma-secretase inhibitor on peritoneal dialysis fluid-induced peritoneal fibrosis in rats. Am J Pathol 2010;176:650–9.10.2353/ajpath.2010.090447Search in Google Scholar
131. Vargha R, Endemann M, Kratochwill K, Riesenhuber A, Wick N, Krachler AM, et al. Ex vivo reversal of in vivo transdifferentiation in mesothelial cells grown from peritoneal dialysate effluents. Nephrol Dial Transplant 2006;21:2943–7.10.1093/ndt/gfl355Search in Google Scholar
132. Yu MA, Shin KS, Kim JH, Kim YI, Chung SS, Park SH, et al. HGF and BMP-7 ameliorate high glucose-induced epithelial-to-mesenchymal transition of peritoneal mesothelium. J Am Soc Nephrol 2009;20:567–81.10.1681/ASN.2008040424Search in Google Scholar
133. Loureiro J, Schilte M, Aguilera A, Albar-Vizcaíno P, Ramírez-Huesca M, Pérez-Lozano ML, et al. BMP-7 blocks mesenchymal conversion of mesothelial cells and prevents peritoneal damage induced by dialysis fluid exposure. Nephrol Dial Transplant 2010;25:1098–108.10.1093/ndt/gfp618Search in Google Scholar
134. Wang X, Li X, Ye L, Chen W, Yu X. Smad7 inhibits TGF-β1-induced MCP-1 upregulation through a MAPK/p38 pathway in rat peritoneal mesothelial cells. Int Urol Nephrol 2013;45:899–907.10.1007/s11255-012-0350-6Search in Google Scholar
135. Guo H, Leung JC, Lam MF, Chan LY, Tsang AW, Lan HY, et al. Smad7 transgene attenuates peritoneal fibrosis in uremic rats treated with peritoneal dialysis. J Am Soc Nephrol 2007;18:2689–703.10.1681/ASN.2007010121Search in Google Scholar
136. Nie J, Dou X, Hao W, Wang X, Peng W, Jia Z, et al. Smad7 gene transfer inhibits peritoneal fibrosis. Kidney Int 2007;72:1336–44.10.1038/sj.ki.5002533Search in Google Scholar
137. Strippoli R, Benedicto I, Foronda M, Perez-Lozano ML, Sánchez-Perales S, López-Cabrera M, et al. p38 maintains E-cadherin expression by modulating TAK1-NF-kappa B during epithelial-to-mesenchymal transition. J Cell Sci 2010;123:4321–31.10.1242/jcs.071647Search in Google Scholar
138. Chen YT, Chang YT, Pan SY, Chou YH, Chang FC, Yeh PY, et al. Lineage tracing reveals distinctive fates for mesothelial cells and submesothelial fibroblasts during peritoneal injury. J Am Soc Nephrol 2014;25:2847–58.10.1681/ASN.2013101079Search in Google Scholar
139. Liu Y, Dong Z, Liu H, Zhu J, Liu F, Chen G. Transition of mesothelial cell to fibroblast in peritoneal dialysis: EMT, stem cell or bystander? Perit Dial Int 2015;35:14–25.10.3747/pdi.2014.00188Search in Google Scholar
140. Kissebah AH, Krakower GR. Regional adiposity and morbidity. Physiol Rev 1994;74:761–811.10.1152/physrev.1994.74.4.761Search in Google Scholar
141. Gaggini M, Saponaro C, Gastaldelli A. Not all fats are created equal: adipose vs. ectopic fat, implication in cardiometabolic diseases. Horm Mol Biol Clin Investig 2015;22:7–18.10.1515/hmbci-2015-0006Search in Google Scholar
142. Darimont C, Avanti O, Blancher F, Wagniere S, Mansourian R, Zbinden I. Contribution of mesothelial cells in the expression of inflammatory-related fetal actors in omental adipose tissue of obese subjects. Int J Obes (Lond) 2008;32:112–20.10.1038/sj.ijo.0803688Search in Google Scholar
143. Zhang H, Pu W, Liu Q, He L, Huang X, Tian X, et al. Endocardium contributes to cardiac fat. Circ Res 2016;118:254–65.10.1161/CIRCRESAHA.115.307202Search in Google Scholar
144. Lansley SM, Searles RG, Hoi A, Thomas C, Moneta H, HerrickSE, et al. Mesothelial cell differentiation into osteoblast- and adipocyte-like cells. J Cell Mol Med 2011;15:2095–105.10.1111/j.1582-4934.2010.01212.xSearch in Google Scholar
©2016 by De Gruyter Mouton