Expression of myocilin mutants sensitizes cells to oxidative stress-induced apoptosis: Implication for glaucoma pathogenesis

American Journal of Pathology

Volumn 176, Issue 6, 2010, Pages 2880-2890

  Joe, Myung Kuk ^a   Tomarev, Stanislav I ^a  

^a NATIONAL EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; ARYLDIALKYLPHOSPHATASE 2; CCAAT ENHANCER BINDING PROTEIN; GLUCOSE REGULATED PROTEIN 78; GLUTATHIONE PEROXIDASE 3; HYDROGEN PEROXIDE; MUTANT PROTEIN; MYOCILIN; PROTEIN I 477 N; PROTEIN Y 437 H; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; CYTOSKELETON PROTEIN; DDIT3 PROTEIN, MOUSE; EYE PROTEIN; GLYCOPROTEIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; OXIDIZING AGENT; TRABECULAR MESHWORK-INDUCED GLUCOCORTICOID RESPONSE PROTEIN;

AGED; ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL CULTURE; CELL LINE; CELL STRAIN HEK293; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; GENE MUTATION; GENETIC TRANSFECTION; GLAUCOMA; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS; SENSITIZATION; TRANSGENIC MOUSE; UPREGULATION; WILD TYPE; ADOLESCENT; ADULT; ANIMAL; CHILD; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; MICROARRAY ANALYSIS; MOLECULAR GENETICS; MUTATION; OPEN ANGLE GLAUCOMA; PHYSIOLOGY; PRESCHOOL CHILD; TRABECULAR MESHWORK; YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; APOPTOSIS; CELL LINE; CHILD; CHILD, PRESCHOOL; CYTOSKELETAL PROTEINS; EYE PROTEINS; GLAUCOMA, OPEN-ANGLE; GLYCOPROTEINS; HUMANS; HYDROGEN PEROXIDE; MICE; MICE, TRANSGENIC; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; MUTATION; OXIDANTS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; TRABECULAR MESHWORK; TRANSCRIPTION FACTOR CHOP; YOUNG ADULT;

EID: 77953179589     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090853     Document Type: Article

References (59)

1. Quigley HA, Broman AT: The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol 2006, 90:262-267
2. Weinreb RN, Khaw PT: Primary open-angle glaucoma. Lancet 2004, 363:1711-1720
3. Gabelt BT, Kaufman PL: Changes in aqueous humor dynamics with age and glaucoma. Prog Retin Eye Res 2005, 24:612-637
4. Kwon YH, Fingert JH, Kuehn MH, Alward WL: Primary open-angle glaucoma. N Engl J Med 2009, 360:1113-1124
5. Stone EM, Fingert JH, Alward WL, Nguyen TD, Polansky JR, Sunden SL, Nishimura D, Clark AF, Nystuen A, Nichols BE, Mackey DA, Ritch R, Kalenak JW, Craven ER, Sheffield VC: Identification of a gene that causes primary open angle glaucoma. Science 1997, 275:668-670
6. Adam MF, Belmouden A, Binisti P, Brezin AP, Valtot F, Bechetoille A, Dascotte JC, Copin B, Gomez L, Chaventre A, Bach JF, Garchon HJ: Recurrent mutations in a single exon encoding the evolutionarily conserved olfactomedin-homology domain of TIGR in familial open-angle glaucoma. Hum Mol Genet 1997, 6:2091-2097
7. Fingert JH, Heon E, Liebmann JM, Yamamoto T, Craig JE, Rait J, Kawase K, Hoh ST, Buys YM, Dickinson J, Hockey RR, Williams-Lyn D, Trope G, Kitazawa Y, Ritch R, Mackey DA, Alward WL, Sheffield VC, Stone EM: Analysis of myocilin mutations in 1703 glaucoma patients from five different populations. Hum Mol Genet 1999, 8:899-905
8. Fingert JH, Stone EM, Sheffield VC, Alward WL: Myocilin glaucoma. Surv Ophthalmol 2002, 47:547-561
9. Tamm ER: Myocilin and glaucoma: facts and ideas. Prog Retin Eye Res 2002, 21:395-428
10. Torrado M, Trivedi R, Zinovieva R, Karavanova I, Tomarev SI: Optimedin: a novel olfactomedin-related protein that interacts with myocilin. Hum Mol Genet 2002, 11:1291-1301 (Pubitemid 34555526)
11. Tomarev SI, Wistow G, Raymond V, Dubois S, Malyukova I: Gene expression profile of the human trabecular meshwork: nEIBank sequence tag analysis. Invest Ophthalmol Vis Sci 2003, 44:2588-2596
12. Kubota R, Noda S, Wang Y, Minoshima S, Asakawa S, Kudoh J, Mashima Y, Oguchi Y, Shimizu N: A novel myosin-like protein (myocilin) expressed in the connecting cilium of the photoreceptor: molecular cloning, tissue expression, and chromosomal mapping. Genomics 1997, 41:360-369
13. Nguyen TD, Chen P, Huang WD, Chen H, Johnson D, Polansky JR: Gene structure and properties of TIGR, an olfactomedin-related glycoprotein cloned from glucocorticoid-induced trabecular meshwork cells. J Biol Chem 1998, 273:6341-6350
14. Ortego J, Escribano J, Coca-Prados M: Cloning and characterization of subtracted cDNAs from a human ciliary body library encoding TIGR, a protein involved in juvenile open angle glaucoma with homology to myosin and olfactomedin. FEBS Lett 1997, 413:349-353
15. Snyder DA, Rivers AM, Yokoe H, Menco BP, Anholt RR: Olfactomedin: purification, characterization, and localization of a novel olfactory glycoprotein. Biochemistry 1991, 30:9143-9153
16. Tomarev SI, Nakaya N: Olfactomedin domain-containing proteins: Possible mechanisms of action and functions in normal development and pathology. Molec Neurobiol 2009, 40:122-138
17. Fautsch MP, Vrabel AM, Johnson DH: The identification of myocilin-associated proteins in the human trabecular meshwork. Exp Eye Res 2006, 82:1046-1052
18. Ueda J, Wentz-Hunter K, Yue BY: Distribution of myocilin and extracellular matrix components in the juxtacanalicular tissue of human eyes. Invest Ophthalmol Vis Sci 2002, 43:1068-1076 (Pubitemid 34258275)
19. Joe MK, Sohn S, Choi YR, Park H, Kee C: Identification of flotillin-1 as a protein interacting with myocilin: implications for the pathogenesis of primary open-angle glaucoma. Biochem Biophys Res Commun 2005, 336:1201-1206
20. Filla MS, Liu X, Nguyen TD, Polansky JR, Brandt CR, Kaufman PL, Peters DM: In vitro localization of TIGR/MYOC in trabecular meshwork extracellular matrix and binding to fibronectin. Invest Ophthalmol Vis Sci 2002, 43:151-161
21. Li Y, Aroca-Aguilar JD, Ghosh S, Sanchez-Sanchez F, Escribano J, Coca-Prados M: Interaction of myocilin with the C-terminal region of hevin. Biochem Biophys Res Commun 2006, 339:797-804
22. Kwon HS, Lee HS, Ji Y, Rubin JS, Tomarev SI: Myocilin is a modulator of Wnt signaling. Mol Cell Biol 2009, 29:2139-2154
23. Lam DS, Leung YF, Chua JK, Baum L, Fan DS, Choy KW, Pang CP: Truncations in the TIGR gene in individuals with and without primary open-angle glaucoma. Invest Ophthalmol Vis Sci 2000, 41:1386-1391 (Pubitemid 30261861)
24. Wiggs JL, Vollrath D: Molecular and clinical evaluation of a patient hemizygous for TIGR/MYOC. Arch Ophthalmol 2001, 119:1674-1678 (Pubitemid 33035710)
25. Gong G, Kosoko-Lasaki O, Haynatzki GR, Wilson MR: Genetic dissection of myocilin glaucoma. Hum Mol Genet 2004, 13 Spec No 1:R91-R102
26. Jacobson N, Andrews M, Shepard AR, Nishimura D, Searby C, Fingert JH, Hageman G, Mullins R, Davidson BL, Kwon YH, Alward WL, Stone EM, Clark AF, Sheffield VC: Non-secretion of mutant proteins of the glaucoma gene myocilin in cultured trabecular meshwork cells and in aqueous humor. Hum Mol Genet 2001, 10:117-125
27. Zhou Z, Vollrath D: A cellular assay distinguishes normal and mutant TIGR/myocilin protein. Hum Mol Genet 1999, 8:2221-2228
28. Sohn S, Hur W, Joe MK, Kim JH, Lee ZW, Ha KS, Kee C: Expression of wild-type and truncated myocilins in trabecular meshwork cells: their subcellular localizations and cytotoxicities. Invest Ophthalmol Vis Sci 2002, 43:3680-3685 (Pubitemid 35470604)
29. Malyukova I, Lee HS, Fariss RN, Tomarev SI: Mutated mouse and human myocilins have similar properties and do not block general secretory pathway. Invest Ophthalmol Vis Sci 2006, 47:206-212
30. Gobeil S, Rodrigue MA, Moisan S, Nguyen TD, Polansky JR, Morissette J, Raymond V: Intracellular sequestration of hetero-oligomers formed by wild-type and glaucoma-causing myocilin mutants. Invest Ophthalmol Vis Sci 2004, 45:3560-3567
31. Caballero M, Rowlette LL, Borras T: Altered secretion of a TIGR/MYOC mutant lacking the olfactomedin domain. Biochim Biophys Acta 2000, 1502:447-460
32. Joe MK, Sohn S, Hur W, Moon Y, Choi YR, Kee C: Accumulation of mutant myocilins in ER leads to ER stress and potential cytotoxicity in human trabecular meshwork cells. Biochem Biophys Res Commun 2003, 312:592-600
33. Liu Y, Vollrath D: Reversal of mutant myocilin non-secretion and cell killing: implications for glaucoma. Hum Mol Genet 2004, 13:1193-1204
34. Gould DB, Reedy M, Wilson LA, Smith RS, Johnson RL, John SW: Mutant myocilin nonsecretion in vivo is not sufficient to cause glaucoma. Mol Cell Biol 2006, 26:8427-8436
35. Senatorov V, Malyukova I, Fariss R, Wawrousek EF, Swaminathan S, Sharan SK, Tomarev S: Expression of mutated mouse myocilin induces open-angle glaucoma in transgenic mice. J Neurosci 2006, 26:11903-11914
36. Sacca SC, Izzotti A: Oxidative stress and glaucoma: injury in the anterior segment of the eye. Prog Brain Res 2008, 173:385-407
37. Tezel G: Oxidative stress in glaucomatous neurodegeneration: mechanisms and consequences. Prog Retin Eye Res 2006, 25:490-513
38. Izzotti A, Sacca SC, Longobardi M, Cartiglia C: Sensitivity of ocular anterior chamber tissues to oxidative damage and its relevance to the pathogenesis of glaucoma. Invest Ophthalmol Vis Sci 2009, 50:5251-5258
39. Yam GH, Gaplovska-Kysela K, Zuber C, Roth J: Aggregated myocilin induces russell bodies and causes apoptosis: implications for the pathogenesis of myocilin-caused primary open-angle glaucoma. Am J Pathol 2007, 170:100-109
40. Malhotra JD, Miao H, Zhang K, Wolfson A, Pennathur S, Pipe SW, Kaufman RJ: Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc Natl Acad Sci USA 2008, 105:18525-18530
41. Kim BS, Savinova OV, Reedy MV, Martin J, Lun Y, Gan L, Smith RS, Tomarev SI, John SW, Johnson RL: Targeted disruption of the myocilin gene (Myoc) suggests that human glaucoma-causing mutations are gain of function. Mol Cell Biol 2001, 21:7707-7713
42. Alward WL, Fingert JH, Coote MA, Johnson AT, Lerner SF, Junqua D, Durcan FJ, McCartney PJ, Mackey DA, Sheffield VC, Stone EM: Clinical features associated with mutations in the chromosome 1 open-angle glaucoma gene (GLC1A). N Engl J Med 1998, 338:1022-1027 (Pubitemid 128753791)
43. Wurm FM: Production of recombinant protein therapeutics in cultivated mammalian cells. Nature Biotechnol 2004, 22:1393-1398
44. Soldani C, Scovassi AI: Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis 2002, 7:321-328
45. He Y, Leung KW, Zhuo YH, Ge J: Pro370Leu mutant myocilin impairs mitochondrial functions in human trabecular meshwork cells. Mol Vis 2009, 15:815-825
46. Kryukov GV, Castellano S, Novoselov SV, Lobanov AV, Zehtab O, Guigo R, Gladyshev VN: Characterization of mammalian selenoproteomes. Science 2003, 300:1439-1443
47. Brigelius-Flohe R, Lotzer K, Maurer S, Schultz M, Leist M: Utilization of selenium from different chemical entities for selenoprotein biosynthesis by mammalian cell lines. Biofactors 1995, 5:125-131 (Pubitemid 26359669)
48. Zhou Y, Grinchuk O, Tomarev SI: Transgenic mice expressing the Tyr437His mutant of human myocilin protein develop glaucoma. Invest Ophthalmol Vis Sci 2008, 49:1932-1939
49. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D: CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998, 12:982-995 (Pubitemid 28204605)
50. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ: Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001, 21:1249-1259
51. Friedman AD: GADD153/CHOP, a DNA damage-inducible protein, reduced CAAT/enhancer binding protein activities and increased apoptosis in 32D c13 myeloid cells. Cancer Res 1996, 56:3250-3256
52. Wang L, Zhuo Y, Liu B, Huang S, Hou F, Ge J: Pro370Leu mutant myocilin disturbs the endoplasm reticulum stress response and mitochondrial membrane potential in human trabecular meshwork cells. Mol Vis 2007, 13:618-625
53. Malhotra JD, Kaufman RJ: Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 2007, 9:2277-2293
54. Horke S, Witte I, Wilgenbus P, Kruger M, Strand D, Forstermann U: Paraoxonase-2 reduces oxidative stress in vascular cells and decreases endoplasmic reticulum stress-induced caspase activation. Circulation 2007, 115:2055-2064
55. Voetsch B, Jin RC, Bierl C, Benke KS, Kenet G, Simioni P, Ottaviano F, Damasceno BP, Annichino-Bizacchi JM, Handy DE, Loscalzo J: Promoter polymorphisms in the plasma glutathione peroxidase (GPx-3) gene: a novel risk factor for arterial ischemic stroke among young adults and children. Stroke 2007, 38:41-49
56. Chung SS, Kim M, Youn BS, Lee NS, Park JW, Lee IK, Lee YS, Kim JB, Cho YM, Lee HK, Park KS: Glutathione peroxidase 3 mediates the antioxidant effect of peroxisome proliferator-activated receptor gamma in human skeletal muscle cells. Mol Cell Biol 2009, 29:20-30
57. Martin-Alonso JM, Ghosh S, Coca-Prados M: Cloning of the bovine plasma selenium-dependent glutathione peroxidase (GP) cDNA from the ocular ciliary epithelium: expression of the plasma and cellular forms within the mammalian eye. J Biochem 1993, 114:284-291 (Pubitemid 23254388)
58. Csiszar A, Podlutsky A, Wolin MS, Losonczy G, Pacher P, Ungvari Z: Oxidative stress and accelerated vascular aging: implications for cigarette smoking. Front Biosci 2009, 14:3128-3144
59. Edwards R, Thornton J, Ajit R, Harrison RA, Kelly SP: Cigarette smoking and primary open angle glaucoma: a systematic review. J Glaucoma 2008, 17:558-566