Abstract
The basement membrane (BM) constitutes a specialised form of the extracellular matrix (ECM) and plays important roles in many biological processes, such as cell migration, organ and tissue integrity, cell polarity, and the formation of metastases. In metazoans, a canonical BM is formed by only a few conserved structural core proteins: Laminin, Collagen IV, Nidogen and Perlecan. Depending on the tissue’s function and mechanical load, additional matrix proteins interact with, or are incorporated into the BM, resulting in tissue-specific mechanical properties, such as higher stiffness or elasticity, or special resistance to mechanical stress or harmful environmental conditions. In flies, the collagen IV-like protein Pericardin forms an integral constituent of matrices around the heart and tension sensors (chordotonal organs) of the peripheral nervous system. The function and integrity of both organ systems strongly relies on the appropriate establishment of a Pericardin (Prc) matrix and the function of its adapter protein—Lonely heart (Loh). In this review, we provide an overview of the four collagens present in flies, and will discuss our recent work on the formation and function of Pericardin-containing matrices, the role of the adapter protein Lonely heart and the necessity of specialised ECM molecules in tissue architecture and function.
Funding source: Deutsche Forschungsgemeinschaft
Award Identifier / Grant number: SFB944
Acknowledgements
We wish to thank Kai Jürgens for assistance with SEM images.
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Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
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Research funding: This work was supported by funding from the German Research Foundation (SFB 944: Physiology and Dynamics of Cellular Microcompartments) to A. P.
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Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Abrams, E.W. and Andrew, D.J. (2002). Prolyl 4-hydroxylase alpha-related proteins in Drosophila melanogaster: tissue-specific embryonic expression of the 99F8-9 cluster. Mech. Dev. 112: 165–171, https://doi.org/10.1016/s0925-4773(01)00636-0.Search in Google Scholar PubMed
Ackley, B.D., Crew, J.R., Elamaa, H., Pihlajaniemi, T., Kuo, C.J., and Kramer, J.M. (2001). The NC1/endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance. J. Cell Biol. 152: 1219–1232, https://doi.org/10.1083/jcb.152.6.1219.Search in Google Scholar PubMed PubMed Central
Annunen, P., Koivunen, P., and Kivirikko, K.I. (1999). Cloning of the alpha subunit of prolyl 4-hydroxylase from Drosophila and expression and characterization of the corresponding enzyme tetramer with some unique properties. J. Biol. Chem. 274: 6790–6796, https://doi.org/10.1074/jbc.274.10.6790.Search in Google Scholar PubMed
Apte, S.S. (2009). A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms. J. Biol. Chem. 284: 31493–31497, https://doi.org/10.1074/jbc.r109.052340.Search in Google Scholar PubMed PubMed Central
Arnaud, P., Mougin, Z., Boileau, C., and Le Goff, C. (2021). Cooperative mechanism of ADAMTS/ADAMTSL and fibrillin-1 in the Marfan syndrome and acromelic dysplasias. Front. Genet. 12: 734718, https://doi.org/10.3389/fgene.2021.734718.Search in Google Scholar PubMed PubMed Central
Aumailley, M., Wiedemann, H., Mann, K., and Timpl, R. (1989). Binding of nidogen and the laminin-nidogen complex to basement membrane collagen type IV. Eur. J. Biochem. 184: 241–248, https://doi.org/10.1111/j.1432-1033.1989.tb15013.x.Search in Google Scholar PubMed
Bindhani, B., Maity, S., Chakrabarti, I., and Saha, S.K. (2022). Roles of matrix metalloproteinases in development, immunology, and ovulation in fruit fly (Drosophila). Arch. Insect Biochem. Physiol. 109: e21849, https://doi.org/10.1002/arch.21849.Search in Google Scholar PubMed
Borchiellini, C., Coulon, J., and Le Parco, Y. (1996). The function of type IV collagen during Drosophila muscle development. Mech. Dev. 58: 179–191, https://doi.org/10.1016/s0925-4773(96)00574-6.Search in Google Scholar PubMed
Bouska, M.J. and Bai, H. (2022). Loxl2 is a mediator of cardiac aging in Drosophila melanogaster, genetically examining the role of aging clock genes. G3 12: jkab381, https://doi.org/10.1093/g3journal/jkab381.Search in Google Scholar PubMed PubMed Central
Braden, A.W., Austin, C.R., and David, H.A. (1954). The reaction of zona pellucida to sperm penetration. Aust. J. Biol. Sci. 7: 391–409, https://doi.org/10.1071/bi9540391.Search in Google Scholar PubMed
Bunt, S., Denholm, B., and Skaer, H. (2011). Characterisation of the Drosophila procollagen lysyl hydroxylase, dPlod. Gene Expr. Patterns 11: 72–78, https://doi.org/10.1016/j.gep.2010.09.006.Search in Google Scholar PubMed PubMed Central
Bunt, S., Hooley, C., Hu, N., Scahill, C., Weavers, H., and Skaer, H. (2010). Hemocyte-secreted type IV collagen enhances BMP signaling to guide renal tubule morphogenesis in Drosophila. Dev. Cell 19: 296–306, https://doi.org/10.1016/j.devcel.2010.07.019.Search in Google Scholar PubMed PubMed Central
Campbell, A.G., Fessler, L.I., Salo, T., and Fessler, J.H. (1987). Papilin: a Drosophila proteoglycan-like sulfated glycoprotein from basement membranes. J. Biol. Chem. 262: 17605–17612, https://doi.org/10.1016/s0021-9258(18)45424-5.Search in Google Scholar
Cecchini, J.P., Knibiehler, B., Mirre, C., and Le Parco, Y. (1987). Evidence for a type-IV-related collagen in Drosophila melanogaster. Evolutionary constancy of the carboxyl-terminal noncollagenous domain. Eur. J. Biochem. 165: 587–593, https://doi.org/10.1111/j.1432-1033.1987.tb11480.x.Search in Google Scholar PubMed
Cevik, D., Acker, M., Michalski, C., and Jacobs, J.R. (2019). Pericardin, a Drosophila collagen, facilitates accumulation of hemocytes at the heart. Dev. Biol. 454: 52–65, https://doi.org/10.1016/j.ydbio.2019.06.006.Search in Google Scholar PubMed
Chang, S.W., Shefelbine, S.J., and Buehler, M.J. (2012). Structural and mechanical differences between collagen homo- and heterotrimers: relevance for the molecular origin of brittle bone disease. Biophys. J. 102: 640–648, https://doi.org/10.1016/j.bpj.2011.11.3999.Search in Google Scholar PubMed PubMed Central
Chartier, A., Zaffran, S., Astier, M., Sémériva, M., and Gratecos, D. (2002). Pericardin, a Drosophila type IV collagen-like protein is involved in the morphogenesis and maintenance of the heart epithelium during dorsal ectoderm closure. Development 129: 3241–3253, https://doi.org/10.1242/dev.129.13.3241.Search in Google Scholar PubMed
Chipman, S.D., Sweet, H.O., McBride, D.J.Jr., Davisson, M.T., Marks, S.C.Jr, Shuldiner, A.R., Wenstrup, R.J., Rowe, D.W., and Shapiro, J.R. (1993). Defective pro alpha2(I) collagen synthesis in a recessive mutation in mice: a model of human osteogenesis imperfecta. Proc. Natl. Acad. Sci. USA 90: 1701–1705, https://doi.org/10.1073/pnas.90.5.1701.Search in Google Scholar PubMed PubMed Central
Clamp, A., Blackhall, F.H., Henrioud, A., Jayson, G.C., Javaherian, K., Esko, J., Gallagher, J.T., and Merry, C.L. (2006). The morphogenic properties of oligomeric endostatin are dependent on cell surface heparan sulfate. J. Biol. Chem. 281: 14813–14822, https://doi.org/10.1074/jbc.m512400200.Search in Google Scholar PubMed
Csordás, G., Grawe, F., and Uhlirova, M. (2020). Eater cooperates with Multiplexin to drive the formation of hematopoietic compartments. Elife 9: e57297, https://doi.org/10.7554/eLife.57297.Search in Google Scholar PubMed PubMed Central
Dai, J., Estrada, B., Jacobs, S., Sánchez-Sánchez, B.J., Tang, J., Ma, M., Magadán-Corpas, P., Pastor-Pareja, J.C., and Martín-Bermudo, M.D. (2018). Dissection of Nidogen function in Drosophila reveals tissue-specific mechanisms of basement membrane assembly. PLoS Genet. 14: e1007483, https://doi.org/10.1371/journal.pgen.1007483.Search in Google Scholar PubMed PubMed Central
Davis, M.N., Horne-Badovinac, S., and Naba, A. (2019). In-silico definition of the Drosophila melanogaster matrisome. Matrix Biol. 4: 100015, https://doi.org/10.1016/j.mbplus.2019.100015.Search in Google Scholar PubMed PubMed Central
Dietzel, E., Wessling, J., Floehr, J., Schäfer, C., Ensslen, S., Denecke, B., Rösing, B., Neulen, J., Veitinger, T., Spehr, M., et al.. (2013). Fetuin-B, a liver-derived plasma protein is essential for fertilization. Dev. Cell 25: 106–112, https://doi.org/10.1016/j.devcel.2013.03.001.Search in Google Scholar PubMed
Dold, C. and Holland, C.V. (2011). Ascaris and ascariasis. Microb. Infect. 13: 632–637, https://doi.org/10.1016/j.micinf.2010.09.012.Search in Google Scholar PubMed
Drechsler, M., Schmidt, A., and Paululat, A. (2013). The conserved ADAMTS-like protein Lonely heart mediates matrix formation and cardiac tissue integrity. PLoS Genet. 9: e1003616, https://doi.org/10.1371/journal.pgen.1003616.Search in Google Scholar PubMed PubMed Central
Dubail, J. and Apte, S.S. (2015). Insights on ADAMTS proteases and ADAMTS-like proteins from mammalian genetics. Matrix Biol. 44–46: 24–37, https://doi.org/10.1016/j.matbio.2015.03.001.Search in Google Scholar PubMed
Eklund, L., Piuhola, J., Komulainen, J., Sormunen, R., Ongvarrasopone, C., Fässler, R., Muona, A., Ilves, M., Ruskoaho, H., Takala, T.E., et al.. (2001). Lack of type XV collagen causes a skeletal myopathy and cardiovascular defects in mice. Proc. Natl. Acad. Sci. USA 98: 1194–1199, https://doi.org/10.1073/pnas.98.3.1194.Search in Google Scholar PubMed PubMed Central
Elbjeirami, W.M., Yonter, E.O., Starcher, B.C., and West, J.L. (2003). Enhancing mechanical properties of tissue-engineered constructs via lysyl oxidase crosslinking activity. J. Biomed. Mater. Res. A. 66: 513–521, https://doi.org/10.1002/jbm.a.10021.Search in Google Scholar PubMed
Felbor, U., Dreier, L., Bryant, R.A., Ploegh, H.L., Olsen, B.R., and Mothes, W. (2000). Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J. 19: 1187–1194, https://doi.org/10.1093/emboj/19.6.1187.Search in Google Scholar PubMed PubMed Central
Fetterer, R.H. and Rhoads, M.L. (1993). Biochemistry of the nematode cuticle: relevance to parasitic nematodes of livestock. Vet. Parasitol. 46: 103–111, https://doi.org/10.1016/0304-4017(93)90051-n.Search in Google Scholar PubMed
Frantz, C., Stewart, K.M., and Weaver, V.M. (2010). The extracellular matrix at a glance. J. Cell Sci. 123: 4195–4200, https://doi.org/10.1242/jcs.023820.Search in Google Scholar PubMed PubMed Central
Fukai, N., Eklund, L., Marneros, A.G., Oh, S.P., Keene, D.R., Tamarkin, L., Niemela, M., Ilves, M., Li, E., Pihlajaniemi, T., et al.. (2002). Lack of collagen XVIII/endostatin results in eye abnormalities. EMBO J. 21: 1535–1544, https://doi.org/10.1093/emboj/21.7.1535.Search in Google Scholar PubMed PubMed Central
Gera, J., Budakoti, P., Suhag, M., Mandal, L., and Mandal, S. (2022). Physiological ROS controls Upd3-dependent modeling of ECM to support cardiac function in Drosophila. Sci. Adv. 8: eabj4991, https://doi.org/10.1126/sciadv.abj4991.Search in Google Scholar PubMed PubMed Central
Ghosh, S., Singh, A., Mandal, S., and Mandal, L. (2015). Active hematopoietic hubs in Drosophila adults generate hemocytes and contribute to immune response. Dev. Cell 33: 478–488, https://doi.org/10.1016/j.devcel.2015.03.014.Search in Google Scholar PubMed PubMed Central
Godenschwege, T.A., Pohar, N., Buchner, S., and Buchner, E. (2000). Inflated wings, tissue autolysis and early death in tissue inhibitor of metalloproteinases mutants of Drosophila. Eur. J. Cell Biol. 79: 495–501, https://doi.org/10.1078/0171-9335-00072.Search in Google Scholar PubMed
Gorres, K.L. and Raines, R.T. (2010). Prolyl 4-hydroxylase. Crit. Rev. Biochem. Mol. Biol. 45: 106–124, https://doi.org/10.3109/10409231003627991.Search in Google Scholar PubMed PubMed Central
Hanai, J., Gloy, J., Karumanchi, S.A., Kale, S., Tang, J., Hu, G., Chan, B., Ramchandran, R., Jha, V., Sukhatme, V.P., et al.. (2002). Endostatin is a potential inhibitor of Wnt signaling. J. Cell Biol. 158: 529–539, https://doi.org/10.1083/jcb.200203064.Search in Google Scholar PubMed PubMed Central
Harpaz, N., Ordan, E., Ocorr, K., Bodmer, R., and Volk, T. (2013). Multiplexin promotes heart but not aorta morphogenesis by polarized enhancement of Slit/Robo activity at the heart lumen. PLoS Gent. 9: e1003597, https://doi.org/10.1371/journal.pgen.1003597.Search in Google Scholar PubMed PubMed Central
Hassan, A., Sapir, L., Nitsan, I., Ben-El, R.T.G., Halachmi, N., Salzberg, A., and Tzlil, S. (2019). A change in ECM composition affects sensory organ mechanics and function. Cell Rep. 27: 2272–2280.e4, https://doi.org/10.1016/j.celrep.2019.04.092.Search in Google Scholar PubMed
He, C.W., Liao, C.P., and Pan, C.L. (2018). Wnt signalling in the development of axon, dendrites and synapses. Open Biol. 8: 180116, https://doi.org/10.1098/rsob.180116.Search in Google Scholar PubMed PubMed Central
Heljasvaara, R., Nyberg, P., Luostarinen, J., Parikka, M., Heikkila, P., Rehn, M., Sorsa, T., Salo, T., and Pihlajaniemi, T. (2005). Generation of biologically active endostatin fragments from human collagen XVIII by distinct matrix metalloproteases. Exp. Cell Res. 307: 292–304, https://doi.org/10.1016/j.yexcr.2005.03.021.Search in Google Scholar PubMed
Henke, E., Nandigama, R., and Ergun, S. (2019). Extracellular matrix in the tumor microenvironment and its impact on cancer therapy. Front. Mol. Biosci. 6: 160, https://doi.org/10.3389/fmolb.2019.00160.Search in Google Scholar PubMed PubMed Central
Hollfelder, D., Frasch, M., and Reim, I. (2014). Distinct functions of the laminin β LN domain and collagen IV during cardiac extracellular matrix formation and stabilization of alary muscle attachments revealed by EMS mutagenesis in Drosophila. BMC Dev. Biol. 14: 26, https://doi.org/10.1186/1471-213x-14-26.Search in Google Scholar PubMed PubMed Central
Hubmacher, D. and Apte, S.S. (2015). ADAMTS proteins as modulators of microfibril formation and function. Matrix Biol. 47: 34–43, https://doi.org/10.1016/j.matbio.2015.05.004.Search in Google Scholar PubMed PubMed Central
Hubmacher, D., Wang, L.W., Mecham, R.P., Reinhardt, D.P., and Apte, S.S. (2015). Adamtsl2 deletion results in bronchial fibrillin microfibril accumulation and bronchial epithelial dysplasia--a novel mouse model providing insights into geleophysic dysplasia. Dis. Model Mech. 8: 487–499, https://doi.org/10.1242/dmm.017046.Search in Google Scholar PubMed PubMed Central
Hughes, C.J.R., Turner, S., Andrews, R.M., Vitkin, A., and Jacobs, J.R. (2020). Matrix metalloproteinases regulate ECM accumulation but not larval heart growth in Drosophila melanogaster. J. Mol. Cell. Cardiol. 140: 42–55, https://doi.org/10.1016/j.yjmcc.2020.02.008.Search in Google Scholar PubMed
Hynes, R.O. and Naba, A. (2012). Overview of the Matrisome – an inventory of extracellular matrix constituents and functions. In: Hynes, R.O. and Yamada, K.M. (Eds.), Extracellular matrix biology. Cold Spring Harbor Laboratory Press, NY, USA, pp. 1–16.10.1101/cshperspect.a004903Search in Google Scholar PubMed PubMed Central
Jimenez, S.A., Bashey, R.I., Benditt, M., and Yankowski, R. (1977). Identification of collagen alpha1(I) trimer in embryonic chick tendons and calvaria. Biochem. Biophys. Res. Commun. 78: 1354–1361, https://doi.org/10.1016/0006-291x(77)91441-3.Search in Google Scholar PubMed
Johnstone, I.L. (1994). The cuticle of the nematode Caenorhabditis elegans: a complex collagen structure. Bioessays 16: 171–178, https://doi.org/10.1002/bies.950160307.Search in Google Scholar PubMed
Johnstone, I.L. (2000). Cuticle collagen genes. Expression in Caenorhabditis elegans. Trends Genet. 16: 21–27, https://doi.org/10.1016/s0168-9525(99)01857-0.Search in Google Scholar PubMed
Kadler, K.E., Holmes, D.F., Trotter, J.A., and Chapman, J.A. (1996). Collagen fibril formation. Biochem. J. 316: 1–11, https://doi.org/10.1042/bj3160001.Search in Google Scholar
Kagan, H.M. and Li, W. (2003). Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell. J. Cell. Biochem. 88: 660–672, https://doi.org/10.1002/jcb.10413.Search in Google Scholar
Kanda, H., Shimamura, R., Koizumi-Kitajima, M., and Okano, H. (2019). Degradation of extracellular matrix by matrix metalloproteinase 2 is essential for the establishment of the blood-brain barrier in Drosophila. iScience 16: 218–229, https://doi.org/10.1016/j.isci.2019.05.027.Search in Google Scholar
Kelemen-Valkony, I., Kiss, M., Csiha, J., Kiss, A., Bircher, U., Szidonya, J., Maróy, P., Juhász, G., Komonyi, O., Csiszár, K., et al.. (2012). Drosophila basement membrane collagen col4a1 mutations cause severe myopathy. Matrix Biol. 31: 29–37, https://doi.org/10.1016/j.matbio.2011.09.004.Search in Google Scholar
Kellokumpu, S., Sormunen, R., Heikkinen, J., and Myllylä, R. (1994). Lysyl hydroxylase, a collagen processing enzyme, exemplifies a novel class of luminally-oriented peripheral membrane-proteins in the endoplasmic reticulum. J. Biol. Chem. 269: 30524–30529, https://doi.org/10.1016/s0021-9258(18)43845-8.Search in Google Scholar
Khoshnoodi, J., Pedchenko, V., and Hudson, B.G. (2008). Mammalian collagen IV. Microsc. Res. Tech. 71: 357–370, https://doi.org/10.1002/jemt.20564.Search in Google Scholar
Kim, S.N., Jeibmann, A., Halama, K., Witte, H.T., Walte, M., Matzat, T., Schillers, H., Faber, C., Senner, V., Paulus, W., et al.. (2014). ECM stiffness regulates glial migration in Drosophila and mammalian glioma models. Development 141: 3233–3242, https://doi.org/10.1242/dev.106039.Search in Google Scholar
Kim, Y., Peyrol, S., So, C.K., Boyd, C.D., and Csiszar, K. (1999). Coexpression of the Lysyl Oxidase-like gene (LOXL) and the gene encoding type III procollagen in induced liver fibrosis. J. Cell. Biochem. 72: 181–188, https://doi.org/10.1002/(sici)1097-4644(19990201)72:2%3c181::aid-jcb3%3e3.0.co;2-d.10.1002/(SICI)1097-4644(19990201)72:2<181::AID-JCB3>3.0.CO;2-DSearch in Google Scholar
Kim, Y.M., Hwang, S., Kim, Y.M., Pyun, B.J., Kim, T.Y., Lee, S.T., Gho, Y.S., and Kwon, Y.G. (2002). Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J. Biol. Chem. 277: 27872–27879, https://doi.org/10.1074/jbc.m202771200.Search in Google Scholar
Kiss, A.A., Popovics, N., Szabo, G., Csiszar, K., and Mink, M. (2016a). Altered stress fibers and integrin expression in the Malpighian epithelium of Drosophila type IV collagen mutants. Data Brief 7: 868–872, https://doi.org/10.1016/j.dib.2016.03.059.Search in Google Scholar
Kiss, M., Kiss, A.A., Radics, M., Popovics, N., Hermesz, E., Csiszar, K., and Mink, M. (2016b). Drosophila type IV collagen mutation associates with immune system activation and intestinal dysfunction. Matrix Biol. 49: 120–131, https://doi.org/10.1016/j.matbio.2015.09.002.Search in Google Scholar PubMed
Kiss, A.A., Somlyai-Popovics, N., Tubak, V., Boldogkői, Z., Csiszár, K., and Mink, M. (2019). Novel phenotypic elements of type IV collagenopathy revealed by the Drosophila model. Appl. Sci. 9: 2083, https://doi.org/10.3390/app9102083.Search in Google Scholar
Kivirikko, K.I. and Myllyharju, J. (1998). Prolyl 4-hydroxylases and their protein disulfide isomerase subunit. Matrix Biol. 16: 357–368, https://doi.org/10.1016/s0945-053x(98)90009-9.Search in Google Scholar PubMed
Kuo, C.J., LaMontagne, K.R.Jr., Garcia-Cardena, G., Ackley, B.D., Kalman, D., Park, S., Christofferson, R., Kamihara, J., Ding, Y.H., Lo, K.M., et al.. (2001). Oligomerization-dependent regulation of motility and morphogenesis by the collagen XVIII NC1/endostatin domain. J. Cell Biol. 152: 1233–1246, https://doi.org/10.1083/jcb.152.6.1233.Search in Google Scholar PubMed PubMed Central
LaFever, K.S., Wang, X., Page-McCaw, P., Bhave, G., and Page-McCaw, A. (2017). Both Drosophila matrix metalloproteinases have released and membrane-tethered forms but have different substrates. Sci. Rep. 7: 44560, https://doi.org/10.1038/srep44560.Search in Google Scholar PubMed PubMed Central
Lamberg, A., Helaakoski, T., Myllyharju, J., Peltonen, S., Notbohm, H., Pihlajaniemi, T., and Kivirikko, K.I. (1996). Characterization of human type III collagen expressed in a baculovirus system. Production of a protein with a stable triple helix requires coexpression with the two types of recombinant prolyl 4-hydroxylase subunit. J. Biol. Chem. 271: 11988–11995, https://doi.org/10.1074/jbc.271.20.11988.Search in Google Scholar PubMed
Lau, Y.K., Gobin, A.M., and West, J.L. (2006). Overexpression of lysyl oxidase to increase matrix crosslinking and improve tissue strength in dermal wound healing. Ann. Biomed. Eng. 34: 1239–1246, https://doi.org/10.1007/s10439-006-9130-8.Search in Google Scholar PubMed
Laurie, G.W., Leblond, C.P., Inoue, S., Martin, G.R., and Chung, A. (1984). Fine structure of the glomerular basement membrane and immunolocalization of five basement membrane components to the lamina densa (basal lamina) and its extensions in both glomeruli and tubules of the rat kidney. Am. J. Anat. 169: 463–481, https://doi.org/10.1002/aja.1001690408.Search in Google Scholar PubMed
Le Bleu, V.S., MacDonald, B., and Kalluri, R. (2007). Structure and function of basement membranes. Exp. Biol. Med. 232: 1121–1129, https://doi.org/10.3181/0703-mr-72.Search in Google Scholar PubMed
Le Goff, C., Morice-Picard, F., Dagoneau, N., Wang, L.W., Perrot, C., Crow, Y.J., Bauer, F., Flori, E., Prost-Squarcioni, C., Krakow, D., et al.. (2008). ADAMTSL2 mutations in geleophysic dysplasia demonstrate a role for ADAMTS-like proteins in TGF-β bioavailability regulation. Nat. Genet. 40: 1119–1123, https://doi.org/10.1038/ng.199.Search in Google Scholar PubMed PubMed Central
Levental, K.R., Yu, H., Kass, L., Lakins, J.N., Egeblad, M., Erler, J.T., Fong, S.F., Csiszar, K., Giaccia, A., Weninger, W., et al.. (2009). Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139: 891–906, https://doi.org/10.1016/j.cell.2009.10.027.Search in Google Scholar PubMed PubMed Central
Li, M., Popovic, Z., Chu, C., Krämer, B.K., and Hocher, B. (2021). Endostatin in renal and cardiovascular diseases. Kidney Dis. 7: 468–481, https://doi.org/10.1159/000518221.Search in Google Scholar PubMed PubMed Central
Lin, C.J., Cocciolone, A.J., and Wagenseil, J.E. (2022). Elastin, arterial mechanics, and stenosis. Am. J. Physiol. Cell Physiol. 322: C875–C886, https://doi.org/10.1152/ajpcell.00448.2021.Search in Google Scholar PubMed PubMed Central
Lindner, J.R., Hillman, P.R., Barrett, A.L., Jackson, M.C., Perry, T.L., Park, Y., and Datta, S. (2007). The Drosophila Perlecan gene trol regulates multiple signaling pathways in different developmental contexts. BMC Dev. Biol. 7: 121, https://doi.org/10.1186/1471-213x-7-121.Search in Google Scholar PubMed PubMed Central
Llano, E., Adam, G., Pendas, A.M., Quesada, V., Sanchez, L.M., Santamaria, I., Noselli, S., and Lopez-Otin, C. (2002). Structural and enzymatic characterization of Drosophila Dm2-MMP, a membrane-bound matrix metalloproteinase with tissue-specific expression. J. Biol. Chem. 277: 23321–23329, https://doi.org/10.1074/jbc.m200121200.Search in Google Scholar PubMed
Makareeva, E., Han, S., Vera, J.C., Sackett, D.L., Holmbeck, K., Phillips, C.L., Visse, R., Nagase, H., and Leikin, S. (2010). Carcinomas contain a matrix metalloproteinase-resistant isoform of type I collagen exerting selective support to invasion. Cancer Res. 70: 4366–4374, https://doi.org/10.1158/0008-5472.can-09-4057.Search in Google Scholar PubMed PubMed Central
Mäki, J. (2002). Lysyl oxidases. University of Oulu, Oulu, PhD thesis. p. 71.Search in Google Scholar
Martínez-González, J., Varona, S., Cañes, L., Galán, M., Briones, A.M., Cachofeiro, V., and Rodríguez, C. (2019). Emerging roles of lysyl oxidases in the cardiovascular system: new concepts and therapeutic challenges. Biomolecules 9: 610, https://doi.org/10.3390/biom9100610.Search in Google Scholar PubMed PubMed Central
Matsubayashi, Y. (2022). Dynamic movement and turnover of extracellular matrices during tissue development and maintenance. Fly 16: 248–274, https://doi.org/10.1080/19336934.2022.2076539.Search in Google Scholar PubMed PubMed Central
Matsubayashi, Y., Louani, A., Dragu, A., Sánchez-Sánchez, B.J., Serna-Morales, E., Yolland, L., Gyoergy, A., Vizcay, G., Fleck, R.A., Heddleston, J.M., et al.. (2017). A moving source of matrix components is essential for de novo basement membrane formation. Curr. Biol. 27: 3526–3534.e4, https://doi.org/10.1016/j.cub.2017.10.001.Search in Google Scholar PubMed PubMed Central
Matsubayashi, Y., Sánchez-Sánchez, B.J., Marcotti, S., Serna-Morales, E., Dragu, A., Diaz-de-la-Loza, M.-D.-C., Vizcay-Barrena, G., Fleck, R.A., and Stramer, B.M. (2020). Rapid homeostatic turnover of embryonic ECM during tissue morphogenesis. Dev. Cell 54: 33–42.e9, https://doi.org/10.1016/j.devcel.2020.06.005.Search in Google Scholar PubMed PubMed Central
McKenzie, F., Mina, K., Callewaert, B., Beyens, A., Dickinson, J.E., Jevon, G., Papadimitriou, J., Diness, B.R., Steensberg, J.N., Ek, J., et al.. (2021). Severe congenital cutis laxa: identification of novel homozygous LOX gene variants in two families. Clin. Genet. 100: 168–175, https://doi.org/10.1111/cge.13969.Search in Google Scholar PubMed
Mead, T.J. and Apte, S.S. (2018). ADAMTS proteins in human disorders. Matrix Biol. 71–72: 225–239, https://doi.org/10.1016/j.matbio.2018.06.002.Search in Google Scholar PubMed PubMed Central
Meyer, F. and Moussian, B. (2009). Drosophila multiplexin (Dmp) modulates motor axon pathfinding accuracy. Dev. Growth Differ. 51: 483–498, https://doi.org/10.1111/j.1440-169x.2009.01111.x.Search in Google Scholar PubMed
Meyer, S., Schmidt, I., and Klämbt, C. (2014). Glia ECM interactions are required to shape the Drosophila nervous system. Mech. Dev. 133: 105–116, https://doi.org/10.1016/j.mod.2014.05.003.Search in Google Scholar PubMed
Mirre, C., Cecchini, J.P., Le Parco, Y., and Knibiehler, B. (1988). De novo expression of a type IV collagen gene in Drosophila embryos is restricted to mesodermal derivatives and occurs at germ band shortening. Development 102: 369–376, https://doi.org/10.1242/dev.102.2.369.Search in Google Scholar PubMed
Misof, K., Landis, W.J., Klaushofer, K., and Fratzl, P. (1997). Collagen from the osteogenesis imperfecta mouse model (oim) shows reduced resistance against tensile stress. J. Clin. Invest. 100: 40–45, https://doi.org/10.1172/jci119519.Search in Google Scholar
Molnar, J., Ujfaludi, Z., Fong, S.F.T., Bollinger, J.A., Waro, G., Fogelgren, B., Dooley, D.M., Mink, M., and Csiszar, K. (2005). Drosophila lysyl oxidases Dmloxl-1 and Dmloxl-2 are differentially expressed and the active DmLOXL-1 influences gene expression and development. J. Biol. Chem. 280: 22977–22985, https://doi.org/10.1074/jbc.m503006200.Search in Google Scholar PubMed
Momota, R., Naito, I., Ninomiya, Y., and Ohtsuka, A. (2011). Drosophila type XV/XVIII collagen, Mp, is involved in Wingless distribution. Matrix Biol. 30: 258–266, https://doi.org/10.1016/j.matbio.2011.03.008.Search in Google Scholar PubMed
Myllyharju, J. (2003). Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol. 22: 15–24, https://doi.org/10.1016/s0945-053x(03)00006-4.Search in Google Scholar PubMed
Myllyharju, J. and Kivirikko, K.I. (2004). Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20: 33–43, https://doi.org/10.1016/j.tig.2003.11.004.Search in Google Scholar PubMed
Myllylä, R., Wang, C., Heikkinen, J., Juffer, A., Lampela, O., Risteli, M., Ruotsalainen, H., Salo, A., and Sipila, L. (2007). Expanding the lysyl hydroxylase toolbox: new insights into the localization and activities of lysyl hydroxylase 3 (LH3). J. Cell. Physiol. 212: 323–329, https://doi.org/10.1002/jcp.21036.Search in Google Scholar PubMed
Narayanan, A.S., Page, R.C., and Meyers, D.F. (1980). Characterization of collagens of diseased human gingiva. Biochemistry 19: 5037–5043, https://doi.org/10.1021/bi00563a016.Search in Google Scholar PubMed
Natzle, J.E., Monson, J.M., and McCarthy, B.J. (1982). Cytogenetic location and expression of collagen-like genes in Drosophila. Nature 296: 368–371, https://doi.org/10.1038/296368a0.Search in Google Scholar PubMed
O’Reilly, M.S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., Lane, W.S., Flynn, E., Birkhead, J.R., Olsen, B.R., and Folkman, J. (1997). Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88: 277–285, https://doi.org/10.1016/s0092-8674(00)81848-6.Search in Google Scholar PubMed
Oh, S.P., Warman, M.L., Seldin, M.F., Cheng, S.D., Knoll, J.H., Timmons, S., and Olsen, B.R. (1994). Cloning of cDNA and genomic DNA encoding human type XVIII collagen and localization of the alpha 1(XVIII) collagen gene to mouse chromosome 10 and human chromosome 21. Genomics 19: 494–499, https://doi.org/10.1006/geno.1994.1098.Search in Google Scholar PubMed
Ornitz, D.M. and Itoh, N. (2001). Fibroblast growth factors. Genome Biol. 2: REVIEWS3005, https://doi.org/10.1186/gb-2001-2-3-reviews3005.Search in Google Scholar PubMed PubMed Central
Page, A.P., Stepek, G., Winter, A.D., and Pertab, D. (2014). Enzymology of the nematode cuticle: a potential drug target? Int. J. Parasitol. Drugs Drug Resist. 4: 133–141, https://doi.org/10.1016/j.ijpddr.2014.05.003.Search in Google Scholar PubMed PubMed Central
Page-McCaw, A., Serano, J., Sante, J.M., and Rubin, G.M. (2003). Drosophila matrix metalloproteinases are required for tissue remodeling, but not embryonic development. Dev. Cell 4: 95–106, https://doi.org/10.1016/s1534-5807(02)00400-8.Search in Google Scholar PubMed
Pastor-Pareja, J.C. (2020). Atypical basement membranes and basement membrane diversity – what is normal anyway? J. Cell Sci. 133: jcs241794, https://doi.org/10.1242/jcs.241794.Search in Google Scholar PubMed
Pastor-Pareja, J.C. and Xu, T. (2011). Shaping cells and organs in Drosophila by opposing roles of fat body-secreted Collagen IV and Perlecan. Dev. Cell 21: 245–256, https://doi.org/10.1016/j.devcel.2011.06.026.Search in Google Scholar PubMed PubMed Central
Paulsson, M. (1993). Laminin and collagen IV variants and heterogeneity in basement membrane composition. In: Rohrbach, D.H. and Timpl, R. (Eds.), Molecular and cellular aspects of basement membranes. Academic Press, Elsevier, Cambridge, Massachusetts, pp. 177–187.10.1016/B978-0-12-593165-6.50015-2Search in Google Scholar
Paululat, A. and Post, Y. (2018). Commentary: distinct domains in the matricellular protein, Lonely heart, are crucial for cardiac extracellular matrix formation and heart function in Drosophila. J. Cardiol. Cardiovasc. Sciences 2: 1–5, https://doi.org/10.29245/2578-3025/2018/5.1143.Search in Google Scholar
Pöschl, E., Schlotzer-Schrehardt, U., Brachvogel, B., Saito, K., Ninomiya, Y., and Mayer, U. (2004). Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131: 1619–1628.10.1242/dev.01037Search in Google Scholar PubMed
Radke, R.M. and Baumgartner, H. (2014). Diagnosis and treatment of Marfan syndrome: an update. Heart 100: 1382–1391, https://doi.org/10.1136/heartjnl-2013-304709.Search in Google Scholar PubMed
Ramachandran, G.N. and Kartha, G. (1955). Structure of collagen. Nature 176: 593–595, https://doi.org/10.1038/176593a0.Search in Google Scholar PubMed
Rautavuoma, K., Takaluoma, K., Sormunen, R., Myllyharju, J., Kivirikko, K.I., and Soininen, R. (2004). Premature aggregation of type IV collagen and early lethality in lysyl hydroxylase 3 null mice. Proc. Natl. Acad. Sci. USA 101: 14120–14125, https://doi.org/10.1073/pnas.0404966101.Search in Google Scholar PubMed PubMed Central
Rodriguez, A., Zhou, Z., Tang, M.L., Meller, S., Chen, J., Bellen, H., and Kimbrell, D.A. (1996). Identification of immune system and response genes, and novel mutations causing melanotic tumor formation in Drosophila melanogaster. Genetics 143: 929–940, https://doi.org/10.1093/genetics/143.2.929.Search in Google Scholar PubMed PubMed Central
Rodríguez-Manzaneque, J.C., Westling, J., Thai, S.N., Luque, A., Knauper, V., Murphy, G., Sandy, J.D., and Iruela-Arispe, M.L. (2002). ADAMTS1 cleaves aggrecan at multiple sites and is differentially inhibited by metalloproteinase inhibitors. Biochem. Biophys. Res. Commun. 293: 501–508, https://doi.org/10.1016/S0006-291X(02)00254-1.Search in Google Scholar PubMed
Rotstein, B., Post, Y., Reinhardt, M., Lammers, K., Buhr, A., Heinisch, J.J., Meyer, H., and Paululat, A. (2018). Distinct domains in the matricellular protein Lonely heart are crucial for cardiac extracellular matrix formation and heart function in Drosophila. J. Biol. Chem. 293: 7864–7879, https://doi.org/10.1074/jbc.m117.817940.Search in Google Scholar PubMed PubMed Central
Rupard, J.H., Dimari, S.J., Damjanov, I., and Haralson, M.A. (1988). Synthesis of type I homotrimer collagen molecules by cultured human lung adenocarcinoma cells. Am. J. Pathol. 133: 316–326.Search in Google Scholar
Saito, M., Kurokawa, M., Oda, M., Oshima, M., Tsutsui, K., Kosaka, K., Nakao, K., Ogawa, M., Manabe, R.I., Suda, N., et al.. (2011). ADAMTSL6ß rescues fibrillin-1 microfibril disorder in Marfan syndrome mouse model through the promotion of fibrillin-1 assembly. J. Biol. Chem. 286: 38602–38613, https://doi.org/10.1074/jbc.m111.243451.Search in Google Scholar
Saito, K., Maeda, M., and Katada, T. (2017). Regulation of the Sar1 GTPase cycle is necessary for large cargo secretion from the endoplasmic reticulum. Front. Cell Dev. Biol. 5: 75, https://doi.org/10.3389/fcell.2017.00075.Search in Google Scholar PubMed PubMed Central
Sandhu, A., Badal, D., Sheokand, R., Tyagi, S., and Singh, V. (2021). Specific collagens maintain the cuticle permeability barrier in Caenorhabditis elegans. Genetics 217: iyaa047, https://doi.org/10.1093/genetics/iyaa047.Search in Google Scholar PubMed PubMed Central
Schmitt, F.O., Hall, C.E., and Jakus, M.A. (1942). Electron microscope investigations of the structure of collagen. J. Cell. Comp. Physiol. 20: 11–33, https://doi.org/10.1002/jcp.1030200103.Search in Google Scholar
Steinmann, B., Royce, P.M., and Superti-Furga, A. (2002). The Ehlers-Danlos syndrome. In: Royce, P.M. and Steinmann, B. (Eds.), Connective tissue and its heritable disorders: molecular, genetic, and medical aspects, 2nd ed. Wiley-Liss, New York.10.1002/0471221929Search in Google Scholar
Sun, B. (2021). The mechanics of fibrillar collagen extracellular matrix. Cell. Rep. Phys. Sci. 2: 100515, https://doi.org/10.1016/j.xcrp.2021.100515.Search in Google Scholar PubMed PubMed Central
Takei, Y., Minamizaki, T., and Yoshiko, Y. (2015). Functional diversity of fibroblast growth factors in bone formation. Int. J. Endocrinol. 2015(Suppl. 729352), https://doi.org/10.1155/2015/729352.Search in Google Scholar PubMed PubMed Central
Teuscher, A.C., Jongsma, E., Davis, M.N., Statzer, C., Gebauer, J.M., Naba, A., and Ewald, C.Y. (2019). The in-silico characterization of the Caenorhabditis elegans matrisome and proposal of a novel collagen classification. Matrix Biol. 1: 100001, https://doi.org/10.1016/j.mbplus.2018.11.001.Search in Google Scholar PubMed PubMed Central
Timpl, R., Wiedemann, H., van Delden, V., Furthmayr, H., and Kuhn, K. (1981). A network model for the organization of type IV collagen molecules in basement membranes. Eur. J. Biochem. 120: 203–211, https://doi.org/10.1111/j.1432-1033.1981.tb05690.x.Search in Google Scholar PubMed
Töpfer, U., Guerra Santillan, K.Y., Fischer-Friedrich, E., and Dahmann, C. (2022). Distinct contributions of ECM proteins to basement membrane mechanical properties in Drosophila. Development 149: dev200456.10.1242/dev.200456Search in Google Scholar PubMed
Trackman, P.C. (2016). Lysyl oxidase isoforms and potential therapeutic opportunities for fibrosis and cancer. Expert Opin. Ther. Targets 20: 935–945, https://doi.org/10.1517/14728222.2016.1151003.Search in Google Scholar PubMed PubMed Central
Urbano, J.M., Torgler, C.N., Molnar, C., Tepass, U., López-Varea, A., Brown, N.H., de Celis, J.F., and Martín-Bermudo, M.D. (2009). Drosophila laminins act as key regulators of basement membrane assembly and morphogenesis. Development 136: 4165–4176, https://doi.org/10.1242/dev.044263.Search in Google Scholar PubMed PubMed Central
Van Agtmael, T., Bailey, M.A., Schlotzer-Schrehardt, U., Craigie, E., Jackson, I.J., Brownstein, D.G., Megson, I.L., and Mullins, J.J. (2010). Col4a1 mutation in mice causes defects in vascular function and low blood pressure associated with reduced red blood cell volume. Hum. Mol. Genet. 19: 1119–1128, https://doi.org/10.1093/hmg/ddp584.Search in Google Scholar PubMed PubMed Central
Verzijl, N., DeGroot, J., Thorpe, S.R., Bank, R.A., Shaw, J.N., Lyons, T.J., Bijlsma, J.W., Lafeber, F.P., Baynes, J.W., and TeKoppele, J.M. (2000). Effect of collagen turnover on the accumulation of advanced glycation end products. J. Biol. Chem. 275: 39027–39031, https://doi.org/10.1074/jbc.m006700200.Search in Google Scholar
Volk, T., Wang, S., Rotstein, B., and Paululat, A. (2014). Matricellular proteins in development: perspectives from the Drosophila heart. Matrix Biol. 37: 162–166, https://doi.org/10.1016/j.matbio.2014.03.006.Search in Google Scholar PubMed
Wang, T., Hauswirth, A.G., Tong, A., Dickman, D.K., and Davis, G.W. (2014). Endostatin is a trans-synaptic signal for homeostatic synaptic plasticity. Neuron 83: 616–629, https://doi.org/10.1016/j.neuron.2014.07.003.Search in Google Scholar PubMed PubMed Central
Wei, S., Xie, Z., Filenova, E., and Brew, K. (2003). Drosophila TIMP is a potent inhibitor of MMPs and TACE: similarities in structure and function to TIMP-3. Biochemistry 42: 12200–12207, https://doi.org/10.1021/bi035358x.Search in Google Scholar PubMed
Wickström, S.A., Alitalo, K., and Keski-Oja, J. (2002). Endostatin associates with integrin alpha5beta1 and caveolin-1, and activates Src via a tyrosyl phosphatase-dependent pathway in human endothelial cells. Cancer Res. 62: 5580–5589.Search in Google Scholar
Wilmarth, K.R. and Froines, J.R. (1992). In vitro and in vivo inhibition of lysyl oxidase by aminopropionitriles. J. Toxicol. Environ. Health 37: 411–423, https://doi.org/10.1080/15287399209531680.Search in Google Scholar PubMed
Wilmes, A., Klinke, N., Rotstein, B., Meyer, H., and Paululat, A. (2018). Biosynthesis and assembly of the collagen IV-like protein pericardin in Drosophila melanogaster. Biol. Open 7: bio030361, https://doi.org/10.1242/bio.030361.Search in Google Scholar PubMed PubMed Central
Wolfstetter, G., Dahlitz, I., Pfeifer, K., Topfer, U., Alt, J.A., Pfeifer, D.C., Lakes-Harlan, R., Baumgartner, S., Palmer, R.H., and Holz, A. (2019). Characterization of Drosophila Nidogen/Entactin reveals roles in basement membrane stability, barrier function and nervous system patterning. Development 146: dev168948, https://doi.org/10.1242/dev.168948.Search in Google Scholar PubMed
Yasothornsrikul, S., Davis, W.J., Cramer, G., Kimbrell, D.A., and Dearolf, C.R. (1997). Viking: identification and characterization of a second type IV collagen in Drosophila. Gene 198: 17–25, https://doi.org/10.1016/s0378-1119(97)00274-6.Search in Google Scholar PubMed
Ylikärppä, R., Eklund, L., Sormunen, R., Muona, A., Fukai, N., Olsen, B.R., and Pihlajaniemi, T. (2003). Double knockout mice reveal a lack of major functional compensation between collagens XV and XVIII. Matrix Biol. 22: 443–448, https://doi.org/10.1016/s0945-053x(03)00074-x.Search in Google Scholar PubMed
Yurchenco, P.D. and Ruben, G.C. (1987). Basement membrane structure in situ: evidence for lateral associations in the type IV collagen network. J. Cell Biol. 105: 2559–2568, https://doi.org/10.1083/jcb.105.6.2559.Search in Google Scholar PubMed PubMed Central
Zang, Y., Wan, M., Liu, M., Ke, H., Ma, S., Liu, L.-P., Ni, J.-Q., and Pastor-Pareja, J.C. (2015). Plasma membrane overgrowth causes fibrotic collagen accumulation and immune activation in Drosophila adipocytes. Elife 4: e07187, https://doi.org/10.7554/eLife.07187.Search in Google Scholar PubMed PubMed Central
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