Overexpression of myocilin in the Drosophila eye activates the unfolded protein response: Implications for glaucoma

PLoS ONE

Volumn 4, Issue 1, 2009, Pages

  Carbone, Mary Anna ^a   Ayroles, Julien F ^a   Yamamoto, Akihiko ^a   Morozova, Tatiana V ^a   West, Steven A ^a   Magwire, Michael M ^a,b   Mackay, Trudy F C ^a   Anholt, Robert R H ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; MYOCILIN; REACTIVE OXYGEN METABOLITE; X BOX BINDING PROTEIN 1; CYTOSKELETON PROTEIN; EYE PROTEIN; GLYCOPROTEIN; PEPTIDE HYDROLASE; PROTEIN; TRABECULAR MESHWORK-INDUCED GLUCOCORTICOID RESPONSE PROTEIN;

AQUEOUS HUMOR; ARTICLE; CONTROLLED STUDY; DROSOPHILA; GLAUCOMA; IMMUNOBLOTTING; INTRAOCULAR HYPERTENSION; NONHUMAN; PATHOGENESIS; PHENOTYPE; PHOTORECEPTOR POTENTIAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN METABOLISM; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UBIQUITINATION; ANIMAL; BIOCHEMISTRY; EYE; GENETICS; HUMAN; INTRAOCULAR PRESSURE; METABOLISM; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOCHEMICAL PROCESSES; CYTOSKELETAL PROTEINS; DROSOPHILA; EYE; EYE PROTEINS; GLAUCOMA; GLYCOPROTEINS; HUMANS; INTRAOCULAR PRESSURE; PEPTIDE HYDROLASES; PROTEINS; UBIQUITINATION;

EID: 62649096850     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004216     Document Type: Article

References (64)

1. Quigley HA (1996) Number of people with glaucoma worldwide. Br J Ophthalmol 80: 389-393.
2. Tamm ER (2002) Myocilin and glaucoma: facts and ideas. Prog Retin Eye Res 21: 395-428.
3. Tan JC, Peters DM, Kaufman PL (2006) Recent developments in understanding the pathophysiology of elevated intraocular pressure. Curr Opin Ophthalmol 17: 168-174.
4. Bruttini M, Longo I, Frezzotti P, Ciappetta R, Randazzo A, et al. (2003) Mutations in the myocilin gene in families with primary open-angle glaucoma and juvenile open-angle glaucoma. Arch Ophthalmol 121: 1034-1038.
5. Wiggs JL, Allingham RR, Vollrath D, Jones KH, De La Paz M, et al. (1998) Prevalence of mutations in TIGR/Myocilin in patients with adult and juvenile primary open-angle glaucoma. Am J Hum Genet 63: 1549-1552.
6. Kubota R, Noda S, Wang Y, Minoshima S, Asakawa S, et al. (1997) A novel myosin-like protein (myocilin) expressed in the connecting cilium of the photoreceptor: molecular cloning, tissue expression, and chromosomal mapping. Genomics 41: 360-369.
7. Nguyen TD, Chen P, Huang WD, Chen H, Johnson D, et al. (1998) Gene structure and properties of TIGR, an olfactomedin-related glycoprotein cloned from glucocorticoid-induced trabecular meshwork cells. J Biol Chem 273: 6341-6350.
8. Caballero M, Borrás T (2001) Inefficient processing of an olfactomedin-deficient myocilin mutant: potential physiological relevance to glaucoma. Biochem Biophys Res Commun 282: 662-670.
9. Gobeil S, Letartre L, Raymond V (2006) Functional analysis of the glaucoma-causing TIGR/myocilin protein: integrity of amino-terminal coiled-coil regions and olfactomedin homology domain is essential for extracellular adhesion and secretion. Exp Eye Res 82: 1017-1029.
10. Gobeil S, Rodrigue MA, Moisan S, Nguyen TD, Polansky JR, et al. (2004) Intracellular sequestration of hetero-oligomers formed by wild-type and glaucoma-causing myocilin mutants. Invest Ophthalmol Vis Sci 45: 3560-3567.
11. Jacobson N, Andrews M, Shepard AR, Nishimura D, Searby C, et al. (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.
12. Joe MK, Sohn S, Hur W, Moon Y, Choi YR, et al. (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.
13. Liu Y, Vollrath D (2004) Reversal of mutant myocilin non-secretion and cell killing: implications for glaucoma. Hum Mol Genet 13: 1193-1204.
14. Uehara T, Nakamura T, Yao D, Shi ZQ, Gu Z, et al. (2006) S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441: 513-517.
15. Yam GH, Gaplovska-Kysela K, Zuber C, Roth J (2007) Aggregated myocilin induces russell bodies and causes apoptosis: implications for the pathogenesis of myocilin-caused primary open-angle glaucoma. Am J Pathol 170: 100-109.
16. Ryoo HD, Domingos PM, Kang MJ, Steller H (2007) Unfolded protein response in a Drosophila model for retinal degeneration. Embo J 26: 242-252.
17. Mackay TF, Anholt RR (2006) Of flies and man: Drosophila as a model for human complex traits. Annu Rev Genomics Hum Genet 7: 339-367.
18. Borrás T, Morozova TV, Heinsohn SL, Lyman RF, Mackay TF, et al. (2003) Transcription profiling in Drosophila eyes that overexpress the human glaucoma-associated trabecular meshwork-inducible glucocorticoid response protein/myocilin (TIGR/MYOC). Genetics 163: 637-645.
19. Kramer JM, Staveley BE (2003) GAL4 causes developmental defects and apoptosis when expressed in the developing eye of Drosophila melanogaster. Genet Mol Res 2: 43-47.
20. Mukhopadhyay A, Gupta A, Mukherjee S, Chaudhuri K, Ray K (2002) Did myocilin evolve from two different primordial proteins? Mol Vis 8: 271-279.
21. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
22. Yagi Y, Tomita S, Nakamura M, Suzuki T (2000) Overexpression of human amyloid precursor protein in Drosophila. Mol Cell Biol Res Commun 4: 43-49.
23. Feany MB, Bender WW (2000) A Drosophila model of Parkinson's disease. Nature 404: 394-398.
24. Chen L, Feany MB (2005) Alpha-synuclein phosphorylation controls neurotoxicity and inclusion formation in a Drosophila model of Parkinson disease. Nat Neurosci 8: 657-663.
25. Lee WC, Yoshihara M, Littleton JT (2004) Cytoplasmic aggregates trap polyglutamine-containing proteins and block axonal transport in a Drosophila model of Huntington's disease. Proc Natl Acad Sci U S A 101: 3224-3229.
26. Adam MF, Belmouden A, Binisti P, Brezin AP, Valtot F, et al. (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.
27. Alward WL, Fingert JH, Coote MA, Johnson AT, Lerner SF, et al. (1998) Clinical features associated with mutations in the chromosome 1 open-angle glaucoma gene (GLC1A). N Engl J Med 338: 1022-1027.
28. Richards JE, Ritch R, Lichter PR, Rozsa FW, Stringham HM, et al. (1998) Novel trabecular meshwork inducible glucocorticoid response mutation in an eight-generation juvenile-onset primary open-angle glaucoma pedigree. Ophthalmology 105: 1698-1707.
29. Stoilova D, Child A, Brice G, Crick RP, Fleck BW, et al. (1997) Identification of a new 'TIGR' mutation in a family with juvenile-onset primary open angle glaucoma. Ophthalmic Genet 18: 109-118.
30. Stone EM, Fingert JH, Alward WL, Nguyen TD, Polansky JR, et al. (1997) Identification of a gene that causes primary open angle glaucoma. Science 275: 668-670.
31. Fingert JH, Heon E, Liebmann JM, Yamamoto T, Craig JE, et al. (1999) Analysis of myocilin mutations in 1703 glaucoma patients from five different populations. Hum Mol Genet 8: 899-905.
32. Challa P, Herndon LW, Hauser MA, Broomer BW, Pericak-Vance MA, et al. (2002) Prevalence of myocilin mutations in adults with primary open-angle glaucoma in Ghana, West Africa. J Glaucoma 11: 416-420.
33. Morissette J, Clepet C, Moisan S, Dubois S, Winstall E, et al. (1998) Homozygotes carrying an autosomal dominant TIGR mutation do not manifest glaucoma. Nat Genet 19: 319-321.
34. Kim R, Emi M, Tanabe K, Murakami S (2006) Role of the unfolded protein response in cell death. Apoptosis 11: 5-13.
35. Forman MS, Lee VM, Trojanowski JQ (2003) 'Unfolding' pathways in neurodegenerative disease. Trends Neurosci 26: 407-410.
36. Lee JA, Anholt RR, Cole GJ (2007) Olfactomedin-2 mediates development of the anterior central nervous system and head structures in zebrafish. Mech Dev.
37. Moreno TA, Bronner-Fraser M (2005) Noelins modulate the timing of neuronal differentiation during development. Dev Biol 288: 434-447.
38. Naskar R, Thanos S (2006) Retinal gene profiling in a hereditary rodent model of elevated intraocular pressure. Mol Vis 12: 1199-1210.
39. Hart H, Samuelson DA, Tajwar H, MacKay EO, Lewis PA, et al. (2007) Immunolocalization of myocilin protein in the anterior eye of normal and primary open-angle glaucomatous dogs. Vet Ophthalmol 10 Suppl 1: 28-37.
40. Mackay EO, Kallberg ME, Gelatt KN (2008) Aqueous humor myocilin protein levels in normal, genetic carriers, and glaucoma Beagles. Vet Ophthalmol 11: 177-185.
41. Yam GH, Gaplovska-Kysela K, Zuber C, Roth J (2007) Sodium 4-phenylbutyrate acts as a chemical chaperone on misfolded myocilin to rescue cells from endoplasmic reticulum stress and apoptosis. Invest Ophthalmol Vis Sci 48: 1683-1690.
42. Gould DB, Reedy M, Wilson LA, Smith RS, Johnson RL, et al. (2006) Mutant myocilin nonsecretion in vivo is not sufficient to cause glaucoma. Mol Cell Biol 26: 8427-8436.
43. Senatorov V, Malyukova I, Fariss R, Wawrousek EF, Swaminathan S, et al. (2006) Expression of mutated mouse myocilin induces open-angle glaucoma in transgenic mice. J Neurosci 26: 11903-11914.
44. Shepard AR, Jacobson N, Millar JC, Pang IH, Steely HT, et al. (2007) Glaucoma-causing myocilin mutants require the Peroxisomal Targeting Signal-1 Receptor (PTS1R) to elevate intraocular pressure. Hum Mol Genet.
45. Tezel G (2006) Oxidative stress in glaucomatous neurodegeneration: mechanisms and consequences. Prog Retin Eye Res 25: 490-513.
46. Izzotti A, Bagnis A, Sacca SC (2006) The role of oxidative stress in glaucoma. Mutat Res 612: 105-114.
47. Achary MS, Reddy AB, Chakrabarti S, Panicker SG, Mandal AK, et al. (2006) Disease-causing mutations in proteins: structural analysis of the CYP1B1 mutations causing primary congenital glaucoma in humans. Biophys J 91: 4329-4339.
48. Lopez-Garrido MP, Sanchez-Sanchez F, Lopez-Martinez F, Aroca-Aguilar JD, Blanco-Marchite C, et al. (2006) Heterozygous CYP1B1 gene mutations in Spanish patients with primary open-angle glaucoma. Mol Vis 12: 748-755.
49. Acharya M, Mookherjee S, Bhattacharjee A, Bandyopadhyay AK, Daulat Thakur SK, et al. (2006) Primary role of CYP1B1 in Indian juvenile-onset POAG patients. Mol Vis 12: 399-404.
50. Reddy AB, Kaur K, Mandal AK, Panicker SG, Thomas R, et al. (2004) Mutation spectrum of the CYP1B1 gene in Indian primary congenital glaucoma patients. Mol Vis 10: 696-702.
51. Sena DF, Finzi S, Rodgers K, Del Bono E, Haines JL, et al. (2004) Founder mutations of CYP1B1 gene in patients with congenital glaucoma from the United States and Brazil. J Med Genet 41: e6.
52. Colomb E, Kaplan J, Garchon HJ (2003) Novel cytochrome P450 1B1 (CYP1B1) mutations in patients with primary congenital glaucoma in France. Hum Mutat 22: 496.
53. Belmouden A, Melki R, Hamdani M, Zaghloul K, Amraoui A, et al. (2002) A novel frameshift founder mutation in the cytochrome P450 1B1 (CYP1B1) gene is associated with primary congenital glaucoma in Morocco. Clin Genet 62: 334-339.
54. Rubin GM, Spradling AC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218: 348-353.
55. Ashburner M (1989) Drosophila, A laboratory handbook: Cold Spring Harbor Laboratory Press.
56. Gibbs SM, Becker A, Hardy RW, Truman JW (2001) Soluble guanylate cyclase is required during development for visual system function in Drosophila. J Neurosci 21: 7705-7714.
57. Benzer S (1967) Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc Natl Acad Sci U S A 58: 1112-1119.
58. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
59. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
60. Affymetrix (2001) Microarray Suite User Guide, Version 5. Santa Clara, CA: Affymetrix.
61. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B 57: 289-300.
62. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
63. Wu JS, Luo L (2006) A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat Protoc 1: 2110-2115.
64. Oliveros JC (2007) VENNY. An interactive tool for comparing lists with Venn Diagrams. http://bioinfogpcnbcsices/tools/venny/indexhtml.