Intracellular sequestration of hetero-oligomers formed by wild-type and glaucoma-causing myocilin mutants

Investigative Ophthalmology and Visual Science

Volumn 45, Issue 10, 2004, Pages 3560-3567

  Gobeil, Stéphane ^a   Rodrigue, Marc André ^a   Moisan, Steve ^a,c   Nguyen, Thai D ^b   Polansky, Jon R ^b   Morissette, Jean ^a   Raymond, Vincent ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DiaTech Oncology   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; EPITOPE; HETERODIMER; MONOMER; MYOC MUTANT PROTEIN; MYOC PROTEIN; MYOC WT PROTEIN; MYOCILIN; OLIGOMER; POLYPEPTIDE; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; AQUEOUS HUMOR; ARTICLE; AUTOSOMAL DOMINANT DISORDER; CELL LINE; CELL STRAIN COS7; CONTROLLED STUDY; EXPRESSION VECTOR; GENE; GENE EXPRESSION; GENE MUTATION; GLAUCOMA; HUMAN; HUMAN TISSUE; MOLECULAR MECHANICS; MYOC GENE; NONHUMAN; OLFACTOMEDIN DOMAIN; OLIGOMERIZATION; OPEN ANGLE GLAUCOMA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION; TRABECULAR MESHWORK; TRABECULAR MESHWORK INDUCED GLUCOCORTICOID RESPONSE GENE; WESTERN BLOTTING; WT MYOC GENE;

ANIMALS; AQUEOUS HUMOR; BLOTTING, WESTERN; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOSKELETAL PROTEINS; DIMERIZATION; EXTRACELLULAR MATRIX PROTEINS; EYE PROTEINS; GLAUCOMA, OPEN-ANGLE; GLYCOPROTEINS; HUMANS; MUTAGENESIS, SITE-DIRECTED; MUTATION; TRABECULAR MESHWORK; TRANSFECTION;

EID: 4644359640     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.04-0300     Document Type: Article

References (58)

1. Quigley HA. Number of people with glaucoma worldwide. Br J Ophthalmol. 1996;80:389-393.
2. Quigley HA. Reappraising the risk and benefits of aggressive glaucoma therapy. Ophthalmology. 1997;104:1985-1986.
3. McKusick VA. Mendelian Inheritance in Man: a Catalog of Human Genes and Genetic Disorders. 11th ed. Baltimore: Johns Hopkins University Press; 1994.
4. Leske MC. The epidemiology of open-angle glaucoma: a review. Am J Epidemiol. 1983;118:166-191.
5. Thylefors B, Negrel AD. The global impact of glaucoma. Bull World Health Org. 1994;72:323-326.
6. Raymond V. Molecular genetics of the glaucomas: mapping of the first five "GLC" loci. Am J Hum Genet. 1997;60:272-277.
7. Sarfarazi M. Recent advances in molecular genetics of glaucomas. Hum Mol Genet. 1997;6:1667-1677.
8. Wirtz MK, Samples JR, Rust K, et al. GLC1F, a new primary open-angle glaucoma locus, maps to 7q35-q36. Arch Ophthalmol. 1999;117:237-241.
9. Stone EM, Fingert JH, Alward WL, et al. Identification of a gene that causes primary open angle glaucoma. Science. 1997;275:668-670.
10. Kubota R, Noda S, Wang Y, et al. 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.
11. Rezaie T, Child A, Hitchings R, et al. Adult-onset primary open-angle glaucoma caused by mutations in optineurin. Science. 2002; 295:1077-1079.
12. Fingert JH, Héon E, Liebmann JM, et al. Analysis of myocilin mutations in 1703 glaucoma patients from five different populations. Hum Mol Genet. 1999;8:899-905.
13. Fingert JH, Stone EM, Sheffield VC, Alward WL, Myocilin glaucoma. Surv Ophthalmol. 2002;47:547-561.
14. 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 mesh-work cells. J Biol Chem. 1998;273:6341-6350.
15. Adam MF, Belmouden A, Binisti P, et al. 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.
16. Mansergh FC, Kenna PF, Ayuso C, Kiang AS, Humphries P, Farrar GJ. Novel mutations in the TIGR gene in early and late onset open angle glaucoma. Hum Mutat. 1998;11:244-251.
17. Kennan AM, Mansergh FC, Fingert JH, et al. A novel Asp380Ala mutation in the GLC1A/myocilin gene in a family with juvenile onset primary open angle glaucoma. J Med Genet. 1998;35:957-960.
18. Wiggs JL, Allingham RR, Vollrath D, et al. Prevalence of mutations in TIGR/Myocilin in patients with adult and juvenile primary open-angle glaucoma. Am J Hum Genet. 1998;63:1549-1552.
19. Richards JE, Ritch R, Lichter PR, et al. Novel trabecular meshwork inducible glucocorticoid response mutation in an eight-generation juvenile-onset primary open-angle glaucoma pedigree. Ophthalmology. 1998;105:1698-1707.
20. Morissette J, Clépet C, Moisan S, et al. Homozygotes carrying an autosomal dominant TIGR mutation do not manifest glaucoma. Nat Genet. 1998;19:319-321.
21. Alward WL, Fingert JH, Coote MA, et al. Clinical features associated with mutations in the chromosome 1 open-angle glaucoma gene (GLC1A). N Engl J Med. 1998;338:1022-1027.
22. Faucher M, Anctil JL, Rodrigue MA, et al. Founder TIGR/myocilin mutations for glaucoma in the Québec population. Hum Mol Genet. 2002;11:2077-2090.
23. Pang CP, Leung YF, Fan B, et al. TIGR/MYOC gene sequence alterations in individuals with and without primary open-angle glaucoma. Invest Ophthalmol Vis Sci. 2002;43:3231-3235.
24. Karali A, Russell P, Stefani FH, Tamm ER. Localization of myocilin/trabecular meshwork-inducible glucocorticoid response protein in the human eye. Invest Ophthalmol Vis Sci. 2000;41:729-740.
25. Swiderski RE, Ross JL, Fingert JH, et al. Localization of MYOC transcripts in human eye and optic nerve by in situ hybridization. Invest Ophthalmol Vis Sci. 2000;41:3420-3428.
26. Filla MS, Liu X, Nguyen TD, et al. In vitro localization of TIGR/MYOC in trabecular meshwork extracellular matrix and binding to fibronectin. Invest Ophthalmol Vis Sci. 2002;43:151-161.
27. 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.
28. Fautsch MP, Johnson DH. Characterization of myocilin-myocilin interactions. Invest Ophthalmol Vis Sci. 2001;42:2324-2331.
29. Rao PV, Allingham RR, Epstein DL. TIGR/myocilin in human aqueous humor. Exp Eye Res. 2000;71:637-641.
30. Jacobson N, Andrews M, Shepard AR, et al. 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.
31. Russell P, Tamm ER, Grehn FJ, Picht G, Johnson M. The presence and properties of myocilin in the aqueous humor. Invest Ophthalmol Vis Sci. 2001;42:983-986.
32. Caballero M, Borras T. Inefficient processing of an olfactomedin- deficient myocilin mutant: potential physiological relevance to glaucoma. Biochem Biophys Res Commun. 2001;282:662-670.
33. Caballero M, Rowlette LL, Borras T. Altered secretion of a TIGR/MYOC mutant lacking the olfactomedin domain. Biochim Biophys Acta. 2000;1502:447-460.
34. Lo WR, Rowlette LL, Caballero M, Yang P, Hernandez MR, Borras T. Tissue differential microarray analysis of dexamethasone induction reveals potential mechanisms of steroid glaucoma. Invest Ophthalmol Vis Sci. 2003;44:473-485.
35. Izumi K, Mashima Y, Obazawa M, et al. Variants of the myocilin gene in Japanese patients with normal-tension glaucoma. Ophthalmic Res. 2003:35:345-350.
36. Zhou Z, Vollrath D. A cellular assay distinguishes normal and mutant TIGR/myocilin protein. Hum Mol Genet. 1999;8:2221-2228.
37. Wilkie AO, The molecular basis of genetic dominance. J Med Genet. 1994;31:89-98.
38. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254.
39. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 1989:77:51-59.
40. Polansky JR, Weinreb RN, Baxter JD, Alvarado J. Human trabecular cells. I. Establishment in tissue culture and growth characteristics. Invest Ophthalmol Vis Sci. 1979:18:1043-1049.
41. Shepard AR, Jacobson N, Sui R, et al. Characterization of rabbit myocilin: Implications for human myocilin glycosylation and signal peptide usage, BMC Genet. 2003:4:5.
42. 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.
43. Allen S, Naim HY, Bulleid NJ. Intracellular folding of tissue-type plasminogen activator: effects of disulfide bond formation on N-linked glycosylation and secretion. J Biol Chem. 1995:270:4797-4804.
44. Hoist B, Bruun AW, Kielland-Brandt MC, Winther JR. Competition between folding and glycosylation in the endoplasmic reticulum. EMBO J. 1996;15:3538-3546.
45. McGinnes LW, Morrison TG. Disulfide bond formation is a determinant of glycosylation site usage in the hemagglutinin-neuraminidase glycoprotein of Newcastle disease virus. J Virol. 1997;71: 3083-3089.
46. Quilty JA, Cordat E, Reithmeier RA. Impaired trafficking of human kidney anion exchanger (kAE1) caused by hetero-oligomer formation with a truncated mutant associated with distal renal tubular acidosis. Biochem J. 2002;368:895-903.
47. Kamsteeg EJ, Wormhoudt TA, Rijss JP, van Os CH, Deen PM. An impaired routing of wild-type aquaporin-2 after tetramerization with an aquaporin-2 mutant explains dominant nephrogenic diabetes insipidus. EMBO J. 1999:18:2394-2400.
48. Sidrauski C, Chapman R, Walter P. The unfolded protein response: an intracellular signalling pathway with many surprising features. Trends Cell Biol. 1998;8:245-249.
49. Brass P, Corydon TJ, Andresen BS, Jorgensen MM, Bolund L, Gregersen N. Protein misfolding and degradation in genetic diseases. Hum Mutat. 1999:14:186-198.
50. 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.
51. Liu Y, Vollrath D. Reversal of mutant myocilin non-secretion and cell killing: implications for glaucoma. Hum Mol Genet. 2004;13: 1193-1204.
52. Lam DS, Leung YF, Chua JK, et al. Truncations in the TIGR gene in individuals with and without primary open-angle glaucoma. Invest Ophthalmol Vis Sci. 2000;41:1386-1391.
53. Kim BS, Savinova OV, Reedy MV, et al. Targeted disruption of the myocilin gene (Myoc) suggests that human glaucoma-causing mutations are gain of function. Mol Cell Biol. 2001;21:7707-7713.
54. Wiggs JL, Vollrath D. Molecular and clinical evaluation of a patient hemizygous for TIGR/MYOC. Arch Ophthalmol. 2001;119:1674-1678.
55. Sohn S, Hur W, Joe MK, et al. Expression of wild-type and truncated myocilins in trabecular meshwork cells: their subcellular localizations and cytotoxicities. Invest Ophthalmol Vis Sci. 2002; 43:3680-3685.
56. Rawls JM Jr. Genetic complementation and enzyme correlates at the locus encoding the last two steps of de novo pyrimidine biosynthesis in Drosophila melanogaster. Mol Gen Genet. 1981; 184:174-179.
57. Johnson WG. Metabolic interference and the +/- heterozygote: a hypothetical form of simple inheritance which is neither dominant nor recessive. Am J Hum Genet. 1980;32:374-386.
58. Kopito RR. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 2000;10:524-530.