Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Cellular and Molecular Biology Letters

Online
ISSN
1689-1392
See all formats and pricing
Online
Not available via Webshop
*Prices in US$ apply to orders placed in the Americas only. Prices in GBP apply to orders placed in Great Britain only. Prices in € represent the retail prices valid in Germany (unless otherwise indicated). Prices are subject to change without notice. Prices do not include postage and handling if applicable. RRP: Recommended Retail Price.
More options …
Volume 11, Issue 1

Issues

Volume 20 (2015)

Volume 19 (2014)

Volume 18 (2013)

Volume 17 (2012)

Volume 16 (2011)

Volume 15 (2010)

Volume 14 (2009)

Volume 13 (2008)

Volume 12 (2007)

Volume 11 (2006)

Direct Rho-associated kinase inhibiton induces cofilin dephosphorylation and neurite outgrowth in PC-12 cells

Zhiqun Zhang
  • Centers for Neuroproteomics and Biomarkers Research, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Traumatic Brain Injury Studies, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Departments of Neuroscience, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
 / Andrew Ottens
  • Centers for Neuroproteomics and Biomarkers Research, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Traumatic Brain Injury Studies, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Departments of Neuroscience, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
 / Stephen Larner
  • Traumatic Brain Injury Studies, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Departments of Neuroscience, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
 / Firas Kobeissy
  • Centers for Neuroproteomics and Biomarkers Research, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Traumatic Brain Injury Studies, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Departments of Neuroscience, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
 / Melissa Williams
  • Departments of Neuroscience, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
 / Ronald Hayes
  • Traumatic Brain Injury Studies, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Departments of Neuroscience, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Psychiatry, McKnight Brain Institute, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
 / Kevin Wang
  • Centers for Neuroproteomics and Biomarkers Research, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Traumatic Brain Injury Studies, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Departments of Neuroscience, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Psychiatry, McKnight Brain Institute, University of Florida, P.O. Box 100256, 100 S. Newell Drive, Gainesville, Florida, 32610, USA
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2006-03-01 | DOI: https://doi.org/10.2478/s11658-006-0002-x

Open Access

Download PDF

Abstract

Axons fail to regenerate in the adult central nervous system (CNS) following injury. Developing strategies to promote axonal regeneration is therapeutically attractive for various CNS pathologies such as traumatic brain injury, stroke and Alzheimer’s disease. Because the RhoA pathway is involved in neurite outgrowth, Rho-associated kinases (ROCKs), downstream effectors of GTP-bound Rho, are potentially important targets for axonal repair strategies in CNS injuries. We investigated the effects and downstream mechanisms of ROCK inhibition in promoting neurite outgrowth in a PC-12 cell model. Robust neurite outgrowth (NOG) was induced by ROCK inhibitors Y-27632 and H-1152 in a time-and dose-dependent manner. Dramatic cytoskeletal reorganization was noticed upon ROCK inhibition. NOG initiated within 5 to 30 minutes followed by neurite extension between 6 and 10 hours. Neurite processes were then sustained for over 24 hours. Rapid cofilin dephosphorylation was observed within 5 minutes of Y-27632 and H-1152 treatment. Re-phosphorylation was observed by 6 hours after Y-27632 treatment, while H-1152 treatment produced sustained cofilin dephosphorylation for over 24 hours. The results suggest that ROCK-mediated dephosphorylation of cofilin plays a role in the initiation of NOG in PC-12 cells.

Keywords: Neurite outgrowth; ROCK; Y-27632; PC-12; Cofilin; Actin dynamics

  • [1] McKerracher, L., David, S., Jackson, D.L., Kottis, V., Dunn, R.J. and Braun, P.E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13 (1994) 805–811. http://dx.doi.org/10.1016/0896-6273(94)90247-XCrossrefGoogle Scholar

  • [2] McKerracher, L. and David, S. Easing the brakes on spinal cord repair. Nat. Med. 10 (2004) 1052–1053. http://dx.doi.org/10.1038/nm1004-1052CrossrefGoogle Scholar

  • [3] Wang, K.C., Koprivica, V., Kim, J.A., Sivasankaran, R., Guo, Y., Neve, R.L. and He, Z. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417 (2002) 941–944. http://dx.doi.org/10.1038/nature00867CrossrefGoogle Scholar

  • [4] Fournier, A.E., Takizawa, B.T. and Strittmatter, S.M. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J. Neurosci. 23 (2003) 1416–1423. Google Scholar

  • [5] Lehmann, M., Fournier, A., Selles-Navarro, I., Dergham, P., Sebok, A., Leclerc, N., Tigyi, G. and McKerracher, L. Inactivation of Rho signaling pathway promotes CNS axon regeneration. J. Neurosci. 19 (1999) 7537–7547. Google Scholar

  • [6] Yamashita, T., Higuchi, H. and Tohyama, M. The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J. Cell Biol. 157 (2002) 565–570. http://dx.doi.org/10.1083/jcb.200202010CrossrefGoogle Scholar

  • [7] Yamashita, T., Fujitani, M., Yamagishi, S., Hata, K. and Mimura, F. Multiple signals regulate axon regeneration through the nogo receptor complex. Mol. Neurobiol. 32 (2005) 105–112. http://dx.doi.org/10.1385/MN:32:2:105CrossrefGoogle Scholar

  • [8] Bonini, S., Rasi, G., Bracci-Laudiero, M.L., Procoli, A. and Aloe, L. Nerve growth factor: neurotrophin or cytokine? Int. Arch. Allergy Immunol. 131 (2003) 80–84. http://dx.doi.org/10.1159/000070922CrossrefGoogle Scholar

  • [9] Ebadi, M., Bashir, R.M., Heidrick, M.L., Hamada, F.M., Refaey, H.E., Hamed, A., Helal, G., Baxi, M.D., Cerutis, D.R. and Lassi, N.K. Neurotrophins and their receptors in nerve injury and repair. Neurochem. Int. 30 (1997) 347–374. http://dx.doi.org/10.1016/S0197-0186(96)00071-XCrossrefGoogle Scholar

  • [10] Petruska, J.C. and Mendell, L.M. The many functions of nerve growth factor: multiple actions on nociceptors. Neurosci. Lett. 361 (2004) 168–171. http://dx.doi.org/10.1016/j.neulet.2003.12.012CrossrefGoogle Scholar

  • [11] Ozdinler, P.H. and Erzurumlu, R.S. Regulation of neurotrophin-induced axonal responses via Rho GTPases. J. Comp. Neurol. 438 (2001) 377–387. http://dx.doi.org/10.1002/cne.1321CrossrefGoogle Scholar

  • [12] Yamaguchi, Y., Katoh, H., Yasui, H., Mori, K. and Negishi, M. RhoA inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinase-dependent pathway. J. Biol. Chem. 276 (2001) 18977–18983. http://dx.doi.org/10.1074/jbc.M100254200CrossrefGoogle Scholar

  • [13] Kwon, B.K., Borisoff, J.F. and Tetzlaff, W. Molecular targets for therapeutic intervention after spinal cord injury. Mol. Intervent. 2 (2002) 244–258. http://dx.doi.org/10.1124/mi.2.4.244CrossrefGoogle Scholar

  • [14] Amano, M., Fukata, Y. and Kaibuchi, K. Regulation and functions of Rho-associated kinase. Exp. Cell Res. 261 (2000) 44–51. http://dx.doi.org/10.1006/excr.2000.5046CrossrefGoogle Scholar

  • [15] Hall, A. Rho GTPases and the control of cell behaviour. Biochem. Soc. Trans. 33 (2005) 891–895. http://dx.doi.org/10.1042/BST20050891CrossrefGoogle Scholar

  • [16] Somlyo, A.P. and Somlyo, A.V. Signal transduction by G-proteins, rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J. Physiol. 522 Pt 2 (2000) 177–185. http://dx.doi.org/10.1111/j.1469-7793.2000.t01-2-00177.xCrossrefGoogle Scholar

  • [17] Kawano, Y., Fukata, Y., Oshiro, N., Amano, M., Nakamura, T., Ito, M., Matsumura, F., Inagaki, M. and Kaibuchi, K. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J. Cell Biol. 147 (1999) 1023–1038. http://dx.doi.org/10.1083/jcb.147.5.1023CrossrefGoogle Scholar

  • [18] Riento, K. and Ridley, A.J. Rocks: multifunctional kinases in cell behaviour. Nat. Rev. Mol. Cell Biol. 4 (2003) 446–456. http://dx.doi.org/10.1038/nrm1128CrossrefGoogle Scholar

  • [19] Greene, L.A. and Tischler, A.S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. 73 (1976) 2424–2428. http://dx.doi.org/10.1073/pnas.73.7.2424CrossrefGoogle Scholar

  • [20] Park, Y.H., Kantor, L., Guptaroy, B., Zhang, M., Wang, K.K. and Gnegy, M.E. Repeated amphetamine treatment induces neurite outgrowth and enhanced amphetamine-stimulated dopamine release in rat pheochromocytoma cells (PC12 cells) via a protein kinase C-and mitogen activated protein kinase-dependent mechanism. J. Neurochem. 87 (2003) 1546–1557. http://dx.doi.org/10.1046/j.1471-4159.2003.02127.xCrossrefGoogle Scholar

  • [21] Sebok, A., Nusser, N., Debreceni, B., Guo, Z., Santos, M.F., Szeberenyi, J. and Tigyi, G. Different roles for RhoA during neurite initiation, elongation, and regeneration in PC12 cells. J. Neurochem. 73 (1999) 949–960. http://dx.doi.org/10.1046/j.1471-4159.1999.0730949.xCrossrefGoogle Scholar

  • [22] Tojima, T. and Ito, E. Signal transduction cascades underlying de novo protein synthesis required for neuronal morphogenesis in differentiating neurons. Prog. Neurobiol. 72 (2004) 183–193. http://dx.doi.org/10.1016/j.pneurobio.2004.03.002CrossrefGoogle Scholar

  • [23] Dent, E.W. and Gertler, F.B. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40 (2003) 209–227. http://dx.doi.org/10.1016/S0896-6273(03)00633-0CrossrefGoogle Scholar

  • [24] Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K. and Narumiya, S. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285 (1999) 895–898. http://dx.doi.org/10.1126/science.285.5429.895CrossrefGoogle Scholar

  • [25] Ohashi, K., Nagata, K., Maekawa, M., Ishizaki, T., Narumiya, S. and Mizuno, K. Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J. Biol. Chem. 275 (2000) 3577–3582. http://dx.doi.org/10.1074/jbc.275.5.3577CrossrefGoogle Scholar

  • [26] Hashimoto, R., Nakamura, Y., Goto, H., Wada, Y., Sakoda, S., Kaibuchi, K., Inagaki, M. and Takeda, M. Domain-and site-specific phosphorylation of bovine NF-L by Rho-associated kinase. Biochem. Biophys. Res. Commun. 245 (1998) 407–411. http://dx.doi.org/10.1006/bbrc.1998.8446CrossrefGoogle Scholar

  • [27] Amano, M., Kaneko, T., Maeda, A., Nakayama, M., Ito, M., Yamauchi, T., Goto, H., Fukata, Y., Oshiro, N., Shinohara, A., Iwamatsu, A. and Kaibuchi, K. Identification of Tau and MAP2 as novel substrates of Rho-kinase and myosin phosphatase. J. Neurochem. 87 (2003) 780–790. http://dx.doi.org/10.1046/j.1471-4159.2003.02054.xCrossrefGoogle Scholar

  • [28] Davies, S.P., Reddy, H., Caivano, M. and Cohen, P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351 (2000) 95–105. http://dx.doi.org/10.1042/0264-6021:3510095CrossrefGoogle Scholar

  • [29] Ikenoya, M., Hidaka, H., Hosoya, T., Suzuki, M., Yamamoto, N. and Sasaki, Y. Inhibition of rho-kinase-induced myristoylated alanine-rich C kinase substrate (MARCKS) phosphorylation in human neuronal cells by H-1152, a novel and specific Rho-kinase inhibitor. J. Neurochem. 81 (2002) 9–16. http://dx.doi.org/10.1046/j.1471-4159.2002.00801.xCrossrefGoogle Scholar

  • [30] Nakajima, M., Hayashi, K., Egi, Y., Katayama, K., Amano, Y., Uehata, M., Ohtsuki, M., Fujii, A., Oshita, K., Kataoka, H., Chiba, K., Goto, N. and Kondo, T. Effect of Wf-536, a novel ROCK inhibitor, against metastasis of B16 melanoma. Cancer Chemother. Pharmacol. 52 (2003) 319–324. http://dx.doi.org/10.1007/s00280-003-0641-9CrossrefGoogle Scholar

  • [31] Ishizaki, T., Uehata, M., Tamechika, I., Keel, J., Nonomura, K., Maekawa, M. and Narumiya, S. Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol. Pharmacol. 57 (2000) 976–983. Google Scholar

  • [32] Christensen, A.E., Selheim, F., de Rooij, J., Dremier, S., Schwede, F., Dao, K.K., Martinez, A., Maenhaut, C., Bos, J.L., Genieser, H.G. and Doskeland, S.O. cAMP analog mapping of Epac1 and cAMP kinase. Discriminating analogs demonstrate that Epac and cAMP kinase act synergistically to promote PC-12 cell neurite extension. J. Biol. Chem. 278 (2003) 35394–35402. http://dx.doi.org/10.1074/jbc.M302179200CrossrefGoogle Scholar

  • [33] Hundle, B., McMahon, T., Dadgar, J. and Messing, R.O. Overexpression of epsilon-protein kinase C enhances nerve growth factor-induced phosphorylation of mitogen-activated protein kinases and neurite outgrowth. J. Biol. Chem. 270 (1995) 30134–30140. http://dx.doi.org/10.1074/jbc.270.50.30134CrossrefGoogle Scholar

  • [34] Obara, Y., Aoki, T., Kusano, M. and Ohizumi, Y. Beta-eudesmol induces neurite outgrowth in rat pheochromocytoma cells accompanied by an activation of mitogen-activated protein kinase. J. Pharmacol. Exp. Ther. 301 (2002) 803–811. http://dx.doi.org/10.1124/jpet.301.3.803CrossrefGoogle Scholar

  • [35] Birkenfeld, J., Betz, H. and Roth, D. Inhibition of neurite extension by overexpression of individual domains of LIM kinase 1. J. Neurochem. 78 (2001) 924–927. http://dx.doi.org/10.1046/j.1471-4159.2001.00500.xCrossrefGoogle Scholar

  • [36] Fujita, A., Hattori, Y., Takeuchi, T., Kamata, Y. and Hata, F. NGF induces neurite outgrowth via a decrease in phosphorylation of myosin light chain in PC12 cells. Neuroreport 12 (2001) 3599–3602. http://dx.doi.org/10.1097/00001756-200111160-00045CrossrefGoogle Scholar

  • [37] Kishida, S., Yamamoto, H. and Kikuchi, A. Wnt-3a and Dvl induce neurite retraction by activating Rho-associated kinase. Mol. Cell Biol. 24 (2004) 4487–4501. http://dx.doi.org/10.1128/MCB.24.10.4487-4501.2004CrossrefGoogle Scholar

  • [38] Sasaki, Y., Suzuki, M. and Hidaka, H. The novel and specific Rho-kinase inhibitor (S)-(+)-2-methyl-1-[(4-methyl-5-isoquinoline)sulfonyl]-homopiperazine as a probing molecule for Rho-kinase-involved pathway. Pharmacol. Ther. 93 (2002) 225–232. http://dx.doi.org/10.1016/S0163-7258(02)00191-2CrossrefGoogle Scholar

  • [39] Braun, H., Schafer, K. and Hollt, V. BetaIII tubulin-expressing neurons reveal enhanced neurogenesis in hippocampal and cortical structures after a contusion trauma in rats. J. Neurotrauma 19 (2002) 975–983. http://dx.doi.org/10.1089/089771502320317122CrossrefGoogle Scholar

  • [40] Aizawa, H., Wakatsuki, S., Ishii, A., Moriyama, K., Sasaki, Y., Ohashi, K., Sekine-Aizawa, Y., Sehara-Fujisawa, A., Mizuno, K., Goshima, Y. and Yahara, I. Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat. Neurosci. 4 (2001) 367–373. http://dx.doi.org/10.1038/86011Google Scholar

  • [41] Niwa, R., Nagata-Ohashi, K., Takeichi, M., Mizuno, K. and Uemura, T. Control of actin reorganization by Slingshot, a family of phosphatases that dephosphorylate ADF/cofilin. Cell 108 (2002) 233–246. http://dx.doi.org/10.1016/S0092-8674(01)00638-9CrossrefGoogle Scholar

  • [42] Ambach, A., Saunus, J., Konstandin, M., Wesselborg, S., Meuer, S.C. and Samstag, Y. The serine phosphatases PP1 and PP2A associate with and activate the actin-binding protein cofilin in human T lymphocytes. Eur. J. Immunol. 30 (2000) 3422–3431. http://dx.doi.org/10.1002/1521-4141(2000012)30:12<3422::AID-IMMU3422>3.0.CO;2-JCrossrefGoogle Scholar

  • [43] Revenu, C., Athman, R., Robine, S. and Louvard, D. The co-workers of actin filaments: from cell structures to signals. Nat. Rev. Mol. Cell Biol. 5 (2004) 635–646. http://dx.doi.org/10.1038/nrm1437CrossrefGoogle Scholar

  • [44] Zhou, Y., Su, Y., Li, B., Liu, F., Ryder, J.W., Wu, X., Gonzalez-DeWhitt, P.A., Gelfanova, V., Hale, J.E., May, P.C., Paul, S.M. and Ni, B. Nonsteroidal anti-inflammatory drugs can lower amyloidogenic Abeta42 by inhibiting Rho. Science 302 (2003) 1215–1217. http://dx.doi.org/10.1126/science.1090154CrossrefGoogle Scholar

  • [45] Ellezam, B., Dubreuil, C., Winton, M., Loy, L., Dergham, P., Selles-Navarro, I. and McKerracher, L. Inactivation of intracellular Rho to stimulate axon growth and regeneration. Prog. Brain. Res. 137 (2002) 371–380. http://dx.doi.org/10.1016/S0079-6123(02)37028-6CrossrefGoogle Scholar

  • [46] Brabeck, C., Beschorner, R., Conrad, S., Mittelbronn, M., Bekure, K., Meyermann, R., Schluesener, H.J. and Schwab, J.M. Lesional expression of RhoA and RhoB following traumatic brain injury in humans. J. Neurotrauma 21 (2004) 697–706. http://dx.doi.org/10.1089/0897715041269597CrossrefGoogle Scholar

  • [47] Brabeck, C., Mittelbronn, M., Bekure, K., Meyermann, R., Schluesener, H.J. and Schwab, J.M. Effect of focal cerebral infarctions on lesional RhoA and RhoB expression. Arch. Neurol. 60 (2003) 1245–1249. http://dx.doi.org/10.1001/archneur.60.9.1245CrossrefGoogle Scholar

About the article

Published Online: 2006-03-01

Published in Print: 2006-03-01

Citation Information: Cellular and Molecular Biology Letters, Volume 11, Issue 1, Pages 12–29, ISSN (Online) 1689-1392, DOI: https://doi.org/10.2478/s11658-006-0002-x.

Export Citation

© 2006 University of Wrocław, Poland. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Hee-Jun Kim, Won-Haeng Lee, Mo-Jong Kim, Sunmee Shin, Byungki Jang, Jae-Bong Park, Wilma Wasco, Joseph Buxbaum, Yong-Sun Kim, and Eun-Kyoung Choi
International Journal of Molecular Sciences, 2018, Volume 19, Number 4, Page 1196
[2]
Najam A. Sharif
Journal of Ocular Pharmacology and Therapeutics, 2018
[3]
Arya Dahal and Shantá D. Hinton
Biochemical Society Transactions, 2017, Volume 45, Number 2, Page 381
[4]
Dallas A. Banks, Arya Dahal, Alexander G. McFarland, Brittany M. Flowers, Christina A. Stephens, Benjamin Swack, Ayele Gugssa, Winston A. Anderson, and Shantá D. Hinton
Frontiers in Molecular Biosciences, 2017, Volume 4
[5]
PING HUANG, JING WANG, XI SHEN, QIN JIAO, YU CHENG, BING XIE, and YISHENG ZHONG
Molecular Medicine Reports, 2012, Volume 6, Number 3, Page 662
[6]
Zen Kouchi, Takahiro Igarashi, Nami Shibayama, Shunichi Inanobe, Kazuyuki Sakurai, Hideki Yamaguchi, Toshifumi Fukuda, Shigeru Yanagi, Yoshikazu Nakamura, and Kiyoko Fukami
Journal of Biological Chemistry, 2011, Volume 286, Number 10, Page 8459
[7]
Brittany M. Flowers, Lauren E. Rusnak, Kristen E. Wong, Dallas A. Banks, Michelle R. Munyikwa, Alexander G. McFarland, Shantá D. Hinton, and Wenhui Hu
PLoS ONE, 2014, Volume 9, Number 12, Page e114535
[8]
AmiraSan Dekmak, Sarah Mantash, Abdullah Shaito, Amer Toutonji, Naify Ramadan, Hussein Ghazale, Nouhad Kassem, Hala Darwish, and Kazem Zibara
Behavioural Brain Research, 2016
[9]
Yosuke Ohtake, Daniella Wong, P. M. Abdul-Muneer, Michael E. Selzer, and Shuxin Li
Scientific Reports, 2016, Volume 6, Number 1
[10]
Yanlan Chen, Wen Huang, Wenlin Jiang, Xianghong Wu, Biao Ye, and Xiaoting Zhou
Oxidative Medicine and Cellular Longevity, 2016, Volume 2016, Page 1
[11]
Peter X. Shaw, Alan Sang, Yan Wang, Daisy Ho, Christopher Douglas, Lara Dia, and Jeffrey L. Goldberg
Experimental Eye Research, 2017, Volume 158, Page 33
[12]
Cheong-Meng Chong, Man-Teng Kou, Peichen Pan, Hefeng Zhou, Nana Ai, Chuwen Li, Hai-Jing Zhong, Chung-Hang Leung, Tingjun Hou, and Simon Ming-Yuen Lee
Mol. BioSyst., 2016, Volume 12, Number 9, Page 2713
[13]
Marion Gabel, Franck Delavoie, Valérie Demais, Cathy Royer, Yannick Bailly, Nicolas Vitale, Marie-France Bader, and Sylvette Chasserot-Golaz
The Journal of Cell Biology, 2015, Volume 210, Number 5, Page 785
[14]
Sarah Van de Velde, Lies De Groef, Ingeborg Stalmans, Lieve Moons, and Inge Van Hove
Progress in Neurobiology, 2015, Volume 131, Page 105
[15]
Deborah A. Corey and Thomas J. Kelley
Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 2007, Volume 1772, Number 7, Page 748
[16]
L. Huang, L.B. Zhao, Z.Y. Yu, X.J. He, L.P. Ma, N. Li, L.J. Guo, and W.Y. Feng
Neuroscience, 2014, Volume 277, Page 383
[17]
Mohamad Raad, Tala El Tal, Rukhsana Gul, Stefania Mondello, Zhiqun Zhang, Rose-Mary Boustany, Joy Guingab, Kevin K. Wang, and Firas Kobeissy
ELECTROPHORESIS, 2012, Volume 33, Number 24, Page 3659
[18]
L. Tonges, T. Frank, L. Tatenhorst, K. A. Saal, J. C. Koch, E. M. Szego, M. Bahr, J. H. Weishaupt, and P. Lingor
Brain, 2012, Volume 135, Number 11, Page 3355
[19]
Katerina Mardilovich, Michael F Olson, and Mark Baugh
Future Oncology, 2012, Volume 8, Number 2, Page 165
[20]
Lars Zulauf, Ovidiu Coste, Claudiu Marian, Christine Möser, Christian Brenneis, and Ellen Niederberger
Biochemical and Biophysical Research Communications, 2009, Volume 390, Number 4, Page 1408
[21]
Dharmendra Pandey, Pankaj Goyal, and Wolfgang Siess
Blood Cells, Molecules, and Diseases, 2007, Volume 38, Number 3, Page 269
[22]
Ming Dong, Bryan P. Yan, James K. Liao, Yat-Yin Lam, Gabriel W.K. Yip, and Cheuk-Man Yu
Drug Discovery Today, 2010, Volume 15, Number 15-16, Page 622
[23]
Zhiqun Zhang, Andrew K Ottens, Shankar Sadasivan, Firas H. Kobeissy, Tie Fang, Ronald L. Hayes, and Kevin K.W. Wang
Journal of Neurotrauma, 2007, Volume 24, Number 3, Page 460
[24]
Zhiqun Zhang, Stephen F. Larner, Ming Cheng Liu, Wenrong Zheng, Ronald L. Hayes, and Kevin K. W. Wang
Apoptosis, 2009, Volume 14, Number 11, Page 1289
[25]
Ian S. Miller, Iseult Lynch, Denis Dowling, Kenneth A. Dawson, and William M. Gallagher
Journal of Biomedical Materials Research Part A, 2009, Volume 9999A, Page NA
[26]
Sujatha M. Gopalakrishnan, Nicole Teusch, Christiane Imhof, Margot H. M. Bakker, Mark Schurdak, David J. Burns, and Usha Warrior
Journal of Neuroscience Research, 2008, Volume 86, Number 10, Page 2214

Comments (0)

Please log in or register to comment.
Log in