Myocilin regulates cell proliferation and survival

Journal of Biological Chemistry

Volumn 289, Issue 14, 2014, Pages 10155-10167

  Joe, Myung Kuk ^a   Kwon, Heung Sun ^a   Cojocaru, Radu ^a,b   Tomarev, Stanislav I ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b ELSEVIER MASSON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL ORGANS; BODY FLUIDS; CELL CULTURE; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; GENE EXPRESSION; GROWTH KINETICS; PHOSPHORYLATION; PLANTS (BOTANY);

CELLULAR PROLIFERATIONS; DIFFERENTIALLY EXPRESSED GENE; GENE EXPRESSION PROFILES; INDUCIBLE PROMOTER; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; OPEN-ANGLE GLAUCOMA; TRABECULAR MESHWORKS;

GENE EXPRESSION REGULATION;

CASPASE 7; MITOGEN ACTIVATED PROTEIN KINASE 1; MYOCILIN; POLY(ADENOSINE DIPHOSPHATE RIBOSE);

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL GROWTH; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CULTURE MEDIUM; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OPEN ANGLE GLAUCOMA; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

APOPTOSIS; CELL GROWTH; CELL PROLIFERATION; CELL SIGNALING; ERK; MESENCHYMAL STEM CELLS;

ANIMALS; APOPTOSIS; CASPASE 7; CELL PROLIFERATION; CELL SURVIVAL; CYTOSKELETAL PROTEINS; EYE PROTEINS; GLYCOPROTEINS; HEK293 CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MESENCHYMAL STROMAL CELLS; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION;

EID: 84898070110     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.547091     Document Type: Article

References (76)

1. Polansky, J. R., Fauss, D. J., Chen, P., Chen, H., Lütjen-Drecoll, E., Johnson, D., Kurtz, R. M., Ma, Z. D., Bloom, E., and Nguyen, T. D. (1997) Cellular pharmacology and molecular biology of the trabecular meshwork induc-ible glucocorticoid response gene product. Ophthalmologica. 211, 126-139
2. Kubota, R., Noda, S., Wang, Y., Minoshima, S., Asakawa, S., Kudoh, J., Mashima, Y., Oguchi, Y., and Shimizu, N. (1997) A novel myosin-like protein (myocilin) expressed in the connecting cilium of the photorecep-tor. Molecular cloning, tissue expression, and chromosomal mapping. Genomics 41, 360-369
3. Ortego, J., Escribano, J., and Coca-Prados, M. (1997) Cloning and characterization of subtracted cDNAs from a human ciliary body library encoding TIGR, a protein involved injuvenile open angle glaucoma with homol-ogy to myosin and olfactomedin. FEBS Lett. 413, 349-353
4. Tamm, E. R. (2002) Myocilin and glaucoma: facts and ideas. Prog. Retin. Eye Res. 21, 395-428
5. Tomarev, S. I., and Nakaya, N. (2009) Olfactomedin domain-containing proteins. Possible mechanisms of action and functions in normal development and pathology. Mol. Neurobiol. 40, 122-138
6. Nguyen, T. D., Chen, P., Huang, W. D., Chen, H., Johnson, D., and Polan-sky, J. R. (1998) Gene structure and properties of TIGR, an olfactomedin-related glycoprotein cloned from glucocorticoid-induced trabecular meshwork cells. J. Biol. Chem. 273, 6341-6350
7. Wentz-Hunter, K., Ueda, J., and Yue, B. Y.(2002) Protein interactions with myocilin. Invest. Ophthalmol. Vis. Sci. 43, 176-182
8. Fautsch, M. P., and Johnson, D. H. (2001) Characterization of myocilin-myocilin interactions. Invest. Ophthalmol. Vis. Sci. 42, 2324-2331
9. Gong, G., Kosoko-Lasaki, O., Haynatzki, G. R., and Wilson, M. R. (2004) Genetic dissectionof myocilin glaucoma.Hum. Mol. Genet.13, R91-R102
10. Fingert, J. H., Héon, E., Liebmann, J. M., Yamamoto, T., Craig, J. E., Rait, J., Kawase, K., Hoh, S. T., Buys, Y. M., Dickinson, J., Hockey, R. R., Williams-Lyn, D., Trope, G., Kitazawa, Y., Ritch, R., Mackey, D. A., Alward, W. L., Sheffield, V. C., and Stone, E. M. (1999) Analysis of myocilin mutations in 1703 glaucoma patients from five different populations. Hum. Mol. Genet. 8, 899-905
11. Stone, E. M., Fingert, J. H., Alward, W. L., Nguyen, T. D., Polansky, J. R., Sunden, S. L., Nishimura, D., Clark, A. F., Nystuen, A., Nichols, B. E., Mackey, D. A., Ritch, R., Kalenak, J. W., Craven, E. R., and Sheffield, V. C. (1997) Identification of a gene that causes primary open angle glaucoma. Science 275, 668-670
12. Adam, M. F., Belmouden, A., Binisti, P., Brézin, A. P., Valtot, F., Béchet-oille, A., Dascotte, J. C., Copin, B., Gomez, L., Chaventré, A., Bach, J. F., and Garchon, H. J. (1997) Recurrent mutations in a single exon encoding the evolutionarily conserved olfactomedin-homology domain of TIGR in familial open-angle glaucoma. Hum. Mol. Genet. 6, 2091-2097
13. Kwon, Y. H., Fingert, J. H., Kuehn, M. H., and Alward, W. L. (2009) Primary open-angle glaucoma. N. Engl. J. Med. 360, 1113-1124
14. Alward, W. L., Fingert, J. H., Coote, M. A., Johnson, A. T., Lerner, S. F., Junqua, D., Durcan, F. J., McCartney, P. J., Mackey, D. A., Sheffield, V. C., and Stone, E. M. (1998) Clinical features associated with mutations in the chromosome 1 open-angle glaucoma gene (GLC1A). N. Engl. J. Med. 338, 1022-1027
15. Zhou, Z., and Vollrath, D. (1999) A cellular assay distinguishes normal and mutant TIGR/myocilin protein. Hum. Mol. Genet. 8, 2221-2228
16. Joe, M. K., Sohn, S., Hur, W., Moon, Y., Choi, Y. R., and Kee, C. (2003) Accumulation of mutant myocilins in ER leads to ER stress and potential cytotoxicity in human trabecular meshwork cells. Biochem. Biophys. Res. Commun. 312, 592-600
17. Liu, Y., and Vollrath, D. (2004) Reversal of mutant myocilin non-secretion and cell killing: implications for glaucoma. Hum. Mol. Genet. 13, 1193-1204
18. Jacobson, N., Andrews, M., Shepard, A. R., Nishimura, D., Searby, C., Fingert, J. H., Hageman, G., Mullins, R., Davidson, B. L., Kwon, Y. H., Alward, W. L., Stone, E. M., Clark, A. F., and Sheffield, V. C. (2001) Non-secretion of mutant proteins of the glaucoma gene myocilin in cultured trabecular meshwork cells and in aqueous humor. Hum. Mol. Genet. 10, 117-125
19. Malyukova, I., Lee, H. S., Fariss, R. N., and Tomarev, S. I. (2006) Mutated mouse and human myocilins have similar properties and do not block general secretory pathway. Invest. Ophthalmol. Vis. Sci. 47, 206-212
20. Gobeil, S., Rodrigue, M. A., Moisan, S., Nguyen, T. D., Polansky, J. R., Morissette, J., and Raymond, V. (2004) Intracellular sequestration of hetero-oligomers formed by wild-type and glaucoma-causing myocilin mutants. Invest. Ophthalmol. Vis. Sci. 45, 3560-3567
21. Joe, M. K., and Tomarev, S. I. (2010) Expression of myocilin mutants sensitizes cells to oxidative stress-induced apoptosis: implication for glaucoma pathogenesis. Am. J. Pathol. 176, 2880-2890
22. Zhou, Y., Grinchuk, O., and Tomarev, S. I. (2008) Transgenic mice expressing the Tyr437His mutant of human myocilin protein develop glaucoma. Invest. Ophthalmol. Vis. Sci. 49, 1932-1939
23. Zode, G. S., Kuehn, M. H., Nishimura, D. Y., Searby, C. C., Mohan, K., Grozdanic, S. D., Bugge, K., Anderson, M.G., Clark, A. F., Stone, E. M., and Sheffield, V. C. (2011) Reduction of ER stress via a chemical chaperone prevents disease phenotypes in a mouse model of primary open angle glaucoma. J. Clin. Invest. 121, 3542-3553
24. Torrado, M., Trivedi, R., Zinovieva, R., Karavanova, I., and Tomarev, S. I. (2002) Optimedin: a novel olfactomedin-related protein that interacts with myocilin. Hum. Mol. Genet. 11, 1291-1301
25. Tomarev, S. I., Wistow, G., Raymond, V., Dubois, S., and Malyukova, I. (2003) Gene expression profile of the human trabecular meshwork: NEIBank sequence tag analysis. Invest. Ophthalmol. Vis. Sci. 44, 2588-2596
26. Fingert, J. H., Ying, L., Swiderski, R. E., Nystuen, A. M., Arbour, N. C., Alward, W. L., Sheffield, V. C., and Stone, E. M. (1998) Characterization and comparison of the human and mouse GLC1A glaucoma genes. Genome Res. 8, 377-384
27. Tomarev, S. I., Tamm, E. R., and Chang, B. (1998) Characterization of the mouse Myoc/Tigr gene. Biochem. Biophys. Res. Commun. 245, 887-893
28. Ohlmann, A., Goldwich, A., Flügel-Koch, C., Fuchs, A. V., Schwager, K., and Tamm, E. R. (2003) Secreted glycoprotein myocilin is a component of the myelin sheath in peripheral nerves. Glia 43, 128-140
29. Kwon, H. S., Lee, H. S., Ji, Y., Rubin, J. S., and Tomarev, S. I. (2009) Myo-cilin is a modulator of Wnt signaling. Mol. Cell. Biol. 29, 2139-2154
30. Aroca-Aguilar, J. D., Sánchez-Sanchez, F., Ghosh, S., Fernández-Navarro, A., Coca-Prados, M., and Escribano, J. (2011) Interaction of recombinant myocilin with the matricellular protein SPARC: functional implications. Invest. Ophthalmol. Vis. Sci. 52, 179-189
31. Ueda, J., Wentz-Hunter, K., and Yue, B. Y. (2002) Distribution of myocilin and extracellular matrix components in the juxtacanalicular tissue of human eyes. Invest. Ophthalmol. Vis. Sci. 43, 1068-1076
32. Fautsch, M. P., Vrabel, A. M., and Johnson, D. H.(2006) The identification of myocilin-associated proteins in the human trabecular meshwork. Exp. Eye Res. 82, 1046-1052
33. Joe, M. K., Kee, C., and Tomarev, S. I. (2012) Myocilin interacts with syntrophins and is member of dystrophin-associated protein complex. J. Biol. Chem. 287, 13216-13227
34. Dismuke, W. M., McKay, B. S., and Stamer, W. D. (2012) Myocilin, a component of a membrane-associated protein complex driven by a homologous Q-SNARE domain. Biochemistry 51, 3606-3613
35. Joe, M. K., Sohn, S., Choi, Y. R., Park, H., and Kee, C. (2005) Identification of flotillin-1 as a protein interacting with myocilin: implications for the pathogenesis of primary open-angle glaucoma. Biochem. Biophys. Res. Commun. 336, 1201-1206
36. Kim, B. S., Savinova, O. V., Reedy, M. V., Martin, J., Lun, Y., Gan, L., Smith, R. S., Tomarev, S. I., John, S. W., and Johnson, R. L. (2001) Targeted disruption of the myocilin gene (Myoc) suggests that human glaucoma-causing mutations are gain of function. Mol. Cell. Biol. 21, 7707-7713
37. Soleimani, M., and Nadri, S. (2009) A protocol for isolation and culture of mesenchymal stem cells from mouse bone marrow. Nat. Protoc. 4, 102-106
38. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264
39. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach for multiple testing. J. R. Stat. Soc. Ser. B 57, 289-300
40. Gerdes, J., Lemke, H., Baisch, H., Wacker, H. H., Schwab, U., and Stein, H. (1984) Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 133, 1710-1715
41. Starborg, M., Gell, K., Brundell, E., and Hoog, C. (1996) The murine Ki-67 cell proliferation antigen accumulates in the nucleolar and heterochro-matic regions of interphase cells and at the periphery of the mitotic chromosomes in a process essential for cell cycle progression. J. Cell Sci. 109, 143-153
42. Conlon, I., and Raff, M. (1999) Size control in animal development. Cell 96, 235-244
43. Raff, M. C. (1992) Social controls on cell survival and cell death. Nature 356, 397-400
44. Kwon, H. S., Johnson, T. V., and Tomarev, S. I. (2013) Myocilin stimulates osteogenic differentiation of mesenchymal stem cells through MAPK signaling. J. Biol. Chem. 288, 16882-16894
45. McCubrey, J. A., Steelman, L. S., Chappell, W. H., Abrams, S. L., Wong, E. W., Chang, F., Lehmann, B., Terrian, D. M., Milella, M., Tafuri, A., Stivala, F., Libra, M., Basecke, J., Evangelisti, C., Martelli, A. M., and Franklin, R. A. (2007) Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim. Biophys. Acta 1773, 1263-1284
46. Wada, T., and Penninger, J. M. (2004) Mitogen-activated protein kinases in apoptosis regulation. Oncogene 23, 2838-2849
47. Favata, M. F., Horiuchi, K. Y., Manos, E. J., Daulerio, A. J., Stradley, D. A., Feeser, W. S., Van Dyk, D. E., Pitts, W. J., Earl, R. A., Hobbs, F., Copeland, R. A., Magolda, R. L., Scherle, P. A., and Trzaskos, J. M. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273, 18623-18632
48. Gould, D. B., Miceli-Libby, L., Savinova, O. V., Torrado, M., Tomarev, S.I., Smith, R. S., and John, S. W. (2004) Genetically increasing Myoc expression supports a necessary pathologic role of abnormal proteins in glaucoma. Mol. Cell. Biol. 24, 9019-9025
49. Kwon, H. S., and Tomarev, S. I. (2011) Myocilin, a glaucoma-associated protein, promotes cell migration through activation of integrin-focal adhesion kinase-serine/threonine kinase signaling pathway. J. Cell Physiol. 226, 3392-3402
50. Kwon, H. S., Johnson, T. V., Joe, M. K., Abu-Asab, M., Zhang, J., Chan, C. C., and Tomarev, S. I. (2013) Myocilin mediates myelination in the peripheral nervous system through ErbB2/3 signaling. J. Biol. Chem. 288, 26357-26371
51. Chambard, J.C., Lefloch, R., Pouysségur, J., and Lenormand, P.(2007) ERK implication in cell cycle regulation. Biochim. Biophys. Acta 1773, 1299-1310
52. Roberts, P. J., and Der, C. J. (2007) Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 26, 3291-3310
53. Marshall, C. J. (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185
54. Eblen, S. T., Slack, J. K., Weber, M. J., and Catling, A. D. (2002) Rac-PAK signaling stimulates extracellular signal-regulated kinase (ERK) activation by regulating formation of MEK1-ERK complexes. Mol. Cell. Biol. 22, 6023-6033
55. Giancotti, F. G., and Ruoslahti, E. (1999) Integrin signaling. Science 285, 1028-1032
56. Wordinger, R. J., and Clark, A. F. (1999) Effects of glucocorticoids on the trabecular meshwork: towards a better understanding of glaucoma. Prog. Retin. Eye Res. 18, 629-667
57. Knepper, P. A., Goossens, W., Hvizd, M., and Palmberg, P. F. (1996) Gly-cosaminoglycans of the human trabecular meshwork in primary open-angle glaucoma. Invest. Ophthalmol. Vis. Sci. 37, 1360-1367
58. Lütjen-Drecoll, E., Futa, R., and Rohen, J. W. (1981) Ultrahistochemical studies on tangential sections of the trabecular meshwork in normal and glaucomatous eyes. Invest. Ophthalmol. Vis. Sci. 21, 563-573
59. Kurata, H., Thant, A. A., Matsuo, S., Senga, T., Okazaki, K., Hotta, N., and Hamaguchi, M. (2000) Constitutive activation of MAP kinase kinase (MEK1) is critical and sufficient for the activation of MMP-2. Exp. Cell Res. 254, 180-188
60. Sudbeck, B. D., Baumann, P., Ryan, G. J., Breitkopf, K., Nischt, R., Krieg, T., and Mauch, C. (1999) Selective loss of PMA-stimulated expression of matrix metalloproteinase 1 in HaCaT keratinocytes is correlated with the inability to induce mitogen-activated protein family kinases. Biochem. J. 339, 167-175
61. Shearer, T., and Crosson, C. E. (2001) Activation of extracellular signal-regulated kinase in trabecular meshwork cells. Exp. Eye Res. 73, 25-35
62. Alvarado, J., Murphy, C, Polansky, J., and Juster, R. (1981) Age-related changes in trabecular meshwork cellularity. Invest. Ophthalmol. Vis. Sci. 21, 714-727
63. Keating, A. (2012) Mesenchymal stromal cells: new directions. Cell Stem Cell 10, 709-716
64. Pittenger, M. F., Mackay, A. M., Beck, S. C, Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S., and Marshak, D. R. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147
65. Caplan, A. I., and Dennis, J. E. (2006) Mesenchymal stem cells as trophic mediators. J. CellBiochem. 98, 1076-1084
66. Johnson, T. V., Dekorver, N. W., Levasseur, V. A., Osborne, A., Tassoni, A., Lorber, B., Heller, J. P., Villasmil, R., Bull, N. D., Martin, K. R., and Tomarev, S. I. (2014) Identification of retinal ganglion cell neuroprotection conferred by platelet-derived growth factor through analysis of the mesenchymal stem cell secretome. Brain 137, 503-519
67. Kandyba, E., Leung, Y., Chen, Y. B., Widelitz, R., Chuong, C. M., and Kobielak, K. (2013) Competitive balance of intrabulge BMP/Wnt signaling reveals a robust gene network ruling stem cell homeostasis and cyclic activation. Proc. Natl. Acad. Sci. U.S.A. 110, 1351-1356
68. Boquest, A. C, Shahdadfar, A., Frønsdal, K., Sigurjonsson, O., Tunheim, S. H., Collas, P., and Brinchmann, J. E. (2005) Isolation and transcription profiling of purified uncultured human stromal stem cells: alteration of gene expression after in vitro cell culture. Mol. Biol. Cell 16, 1131-1141
69. van der Flier, L. G., van Gijn, M. E., Hatzis, P., Kujala, P., Haegebarth, A., Stange, D. E., Begthel, H., van den Born, M., Guryev, V., Oving, I., van Es, J. H., Barker, N., Peters, P. J., van de Wetering, M., and Clevers, H. (2009) Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 136, 903-912
70. van der Flier, L. G., Haegebarth, A., Stange, D. E., van de Wetering, M., and Clevers, H. (2009) OLFM4 is a robust marker for stem cells in human intestine and marks a subset of colorectal cancer cells. Gastroenterology 137, 15-17
71. Zhang, X., Huang, Q., Yang, Z., Li, Y., and Li, C. Y. (2004) GW112, a novel antiapoptotic protein that promotes tumor growth. Cancer Res. 64, 2474-2481
72. Kim, K. K., Park, K. S., Song, S. B., and Kim, K. E. (2010) Up regulation of GW112 Gene by NF promotes an antiapoptotic property in gastric cancer cells. Mol. Carcinog. 49, 259-270
73. Koshida, S., Kobayashi, D., Moriai, R., Tsuji, N., and Watanabe, N. (2007) Specific overexpression of OLFM4(GW112/HGC-1) mRNA in colon, breast and lung cancer tissues detected using quantitative analysis. Cancer Sci. 98, 315-320
74. Aung, P. P., Oue, N., Mitani, Y., Nakayama, H., Yoshida, K., Noguchi, T., Bosserhoff, A. K., and Yasui, W. (2006) Systematic search for gastric cancer-specific genes based on SAGE data: melanoma inhibitory activity and matrix metalloproteinase-10 are novel prognostic factors in patients with gastric cancer. Oncogene 25, 2546-2557
75. Marimuthu, A., Chavan, S., Sathe, G., Sahasrabuddhe, N. A., Srikanth, S. M., Renuse, S., Ahmad, S., Radhakrishnan, A., Barbhuiya, M. A., Kumar, R. V., Harsha, H. C, Sidransky, D., Califano, J., Pandey, A., and Chatterjee, A. (2013) Identification of head and neck squamous cell carcinoma bio-marker candidates through proteomic analysis of cancer cell secretome. Biochim. Biophys. Acta 1834, 2308-2316
76. Miljkovic-Licina, M., Hammel, P., Garrido-Urbani, S., Lee, B. P., Megue-nani, M., Chaabane, C, Bochaton-Piallat, M. L., and Imhof, B. A. (2012) Targeting olfactomedin-like 3 inhibits tumor growth by impairing angio-genesis and pericyte coverage. Mol. Cancer Ther. 11, 2588-2599