Interaction of myocilin with γ-synuclein affects its secretion and aggregation

Cellular and Molecular Neurobiology

Volumn 25, Issue 6, 2005, Pages 1009-1033

  Surgucheva, Irina ^a,d   Park, Bum Chan ^b   Yue, Beatrice Y J T ^b   Tomarev, Stanislav ^c   Surguchov, Andrei ^a,d  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c NATIONAL EYE INSTITUTE   (United States)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Ganglion cells; Glaucoma; Myocilin; Synuclein

Indexed keywords

ALPHA SYNUCLEIN; DEXAMETHASONE; DIMER; GAMMA SYNUCLEIN; MONOMER; MYOCILIN; TETRAMER;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL CULTURE; CELLULAR DISTRIBUTION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RAT; TRABECULAR MESHWORK; UPREGULATION; WESTERN BLOTTING;

ADOLESCENT; ADULT; ALPHA-SYNUCLEIN; ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL LINE; CYTOSKELETAL PROTEINS; DEXAMETHASONE; EYE PROTEINS; GAMMA-SYNUCLEIN; GLAUCOMA; GLYCOPROTEINS; HIPPOCAMPUS; HUMANS; IMMUNOPRECIPITATION; NEURONS; RATS; RETINAL GANGLION CELLS;

ANIMALIA;

EID: 31544462086     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10571-005-8471-4     Document Type: Article

References (74)

1. Adam, M. F., Belmouden, A., Binisti, P., Brezin, A. P., Valtot, F., Bechetoille, A., Dascotte, J. C., Copin, B., Gomez, L., Chaventre, 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. Gen. 6:2091-2097.
2. Allingham, R. R., Wiggs, J. L., De La Paz, M. A., Vollrath, D., Tallett, D. A., Broomer, B., Jones, K. H., Del Bono, E. A., Kern, J., Patterson, K., Haines, J. L., and Pericak-Vance, M. A. (1998). Gln368STOP myocilin mutation in families with late-onset primary open angle glaucoma. Invest. Ophthalmol. Vis. Sci. 39:2288-2295.
3. Alward, W. L. M., 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.
4. Alward, W. L., Kwon, Y. H., Khanna, C. L., Johnson, A. T., Hayreh, S. S., Zimmerman, M. B., Narkiewicz, J., Andorf, J. L., Moore, P. A., Fingert, J. H., Sheffield, V. C., and Stone, E. M. (2002). Variations in the myocilin gene in patients with open-angle glaucoma. Arch. Ophthalmol. 120:1189-1197.
5. Brenz Verca, M. S., Bahi, A., Boyer, F., Wagner, G. C., and Dreyer, J. L. (2003). Distribution of alpha-and gamma-synucleins in the adult rat brain and their modification by high-dose cocaine treatment. Eur. J. Neurosci. 18:1923-1938.
6. Bross, P., Corydon, T. J., Andresen, B. S., Jorgensen, M. M., Bolund, L., and Gregersen, N. (1999). Protein misfolding and degradation in genetic diseases. Hum. Mutat. 14:186-198.
7. Buchman, V. L., Hunter, H. J., Pinon, L. G. Thompson, J., Privalova, E. M., Ninkina, N. N., and Davies, A. M. (1998a). Persyn, a member of the synuclein family, has a distinct pattern of expression in the developing nervous system. J. Neurosci. 18:9335-9341.
8. Buchman, V. L., Adu, J., Pinon, L. G., Ninkina, N. N., and Davies, A. M. (1998b). Persyn, a member of the synuclein family. Nat. Neurosci. 1:101-103.
9. Caballero, M., Rowlette, L. L., and Borras, T. (2000). Altered secretion of a TIGR/MYOC mutant lacking the olfactomedin domain. Biochim. Biophys. Acta 1502:447-460.
10. Caballero, M., and Borras, T. (2001). Inefficient processing of an olfactomedin-deficient myocilin mutant: Potential physiological relevance to glaucoma. Biochem. Biophys. Res. Commun. 282:662-670.
11. Clark, A. F., Steely, H. T., Dickerson, J. E., Jr., English-Wright, S., Stropki, K., McCartney, M. D., Jacobson, N., Shepard, A. R., Clark, J. I., Matsushima, H., Peskind, E. R., Leverenz, J. B., Wilkinson, C. W., Swiderski, R. E., Fingert, J. H., Sheffield, V. C., and Stone, E. M. (2001). Glucocorticoid induction of the glaucoma gene MYOC in human and monkey trabecular meshwork cells and tissues. Invest. Ophthalmol. Vis. Sci. 42:1769-1780.
12. Clayton, D. F., and George, J. M. (1999). Synucleins in synaptic plasticity and neurodegenerative disorders. J. Neurosci. Res. 58(1):120-129.
13. Duda, J. E., Shah, U. Arnold, S. E., Lee, V. M., and Trojanowski, J. Q. (1999). The expression of alpha-, beta-, and gamma-synucleins in olfactory mucosa from patients with and without neurodegenerative diseases. Exp. Neurol. 160:515-522.
14. Farkas, R. H., Qian, J. Goldberg, J. L., Quigley, H. A., and Zack, D. J. (2004). Gene expression profiling of purified rat retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 45:2503-2513.
15. Fautsch, M. P., and Johnson, D. H. (2001). Characterization of myocilin-myocilin interactions. Invest. Ophthalmol. Vis. Sci. 42:2324-2331.
16. Fautsch, M. P., Vrabel, A. M., Peterson, S. L., and Johnson, D. H. (2004). In vitro and in vivo characterization of disulfide bond use in myocilin complex formation. Mol. Vis. 10:417-425.
17. Fingert, J. H., Heon, 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. 6:2091-2097.
18. Friedman, J. S., and Walter, M. A. (1999). Glaucoma genetics, present and future. Clin. Genet. 55:71-79.
19. Fung, K. M., Rorke, L. B., Giasson, B., Lee, V. M., and Trojanowski, J. Q. (2003). Expression of alpha-, beta-, and gamma-synuclein in glial tumors and medulloblastomas. Acta Neuropathol. 106:167-175.
20. Giasson, B. I., Forman, M. S., Higuchi, M., Golbe, L. I., Graves, C. L., Kotzbauer, P. T., Trojanowski, J. Q., and Lee, V. M. (2003). Initiation and synergistic fibrillization of tau- and alpha-synuclein. Science 300:636-640.
21. 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.
22. Iwai, A., Masliah, E., Yoshimoto, M., Ge, N., Flanagan, L., de Silva, H. A., Kittel, A., and Saitoh, T. (1995). The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 14:467-475.
23. 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. Gen. 10:117-125.
24. Ji, H., Liu, Y. E., Jia, T., Wang, M., Liu, J., Xiao, G. Joseph, B. K., Rosen, C., and Shi, Y. E. (1997). Identification of a breast cancer-specific gene, BCSG1, by direct differential cDNA sequencing. Cancer Res. 57:759-764.
25. Jiang, Y., Liu, Y. E., Goldberg, I. D., and Shi, Y. E. (2004). Gamma synuclein, a novel heat-shock protein-associated chaperone, stimulates ligand-dependent estrogen receptor alpha signaling and mammary tumorigenesis. Cancer Res. 64:4539-4546.
26. Johnson, A. T., Alward, W. L. M., Sheffield, V. C., and Stone, E. M. (1996). Genetics and glaucoma. In Ritch, R., Shields, M. B., and Krupin, T. (eds.), The Glaucomas, CV Mosby, St. Louis, pp. 39-54.
27. Jurynec, M. J. Riley, C. P., Gupta, D. K., Nguyen, T. D., McKeon, R. J., and Buck, C. R. (2003). TIGR is upregulated in the chronic glial scar in response to central nervous system injury and inhibits neurite outgrowth. Mol. Cell. Neurosci. 23:69-80.
28. Kirstein, L., Cvekl, A., Chauhan, B. K., and Tamm, E. R. (2000). Regulation of human myocilin/TIGR gene transcription in trabecular meshwork cells and astrocytes: Role of upstream stimulatory factor. Genes Cells 5:661-676.
29. Krishnamoorthy, R. R., Agarwal, P., Prasanna, G., Vopat, K., Lambert, W., Sheedlo, H. J., Pang, I. H., Shade, D., Wordinger, R. J., Yorio, T., Clark, A. F., and Agarwal, N. (2001). Characterization of a transformed rat retinal ganglion cell line. Mol. Brain Res. 86:1-12.
30. Krüger, R., Kuhn, W. Muller, T., Woitalla, D., Graeber, M., Kosel, S., Przuntek, H., Epplen, J. T., Schols, L., and Riess, O. (1998). Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Genet. 18:106-108.
31. Kulkarni, N. H., Karavanich, C. A., Atchley, W. R., and Anholt, R. R. (2000). Characterization and differential expression of a human gene family of olfactomedin-related proteins. Genet. Res. 76:41-50.
32. Lavedan, C., Leroy, E., Dehejia, A., Buchholtz, S., Dutra, A., Nussbaum, R. L., and Polymeropoulos, M. H. (1998). Identification, localization and characterization of the human gamma-synuclein gene. Hum. Genet. 103:106-112.
33. Lindersson, E., Beedholm, R., Hojrup, P., Moos, T., Gai, W. Hendil, K. B., and Jensen, P. H. (2004). Proteasomal inhibition by alpha-synuclein filaments and oligomers. J. Biol. Chem. 279:12924-12934.
34. Ling, L., Cao, Z., and Goeddel, D. V. (1998). NF-kappaB-inducing kinase activates IKK-alpha by phosphorylation of Ser-176. Proc. Natl. Acad. Sci. U.S.A. 95:3792-3797.
35. Liu, Y., and Vollrath, D. (2004). Reversal of mutant myocilin non-secretion and cell killing: Implications for glaucoma. Hum. Mol. Genet. 13:1193-1204.
36. 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. 6:2091-2097.
37. Malinin, N. L., Boldinm, M. P., Kovalenko, A. V., and Wallach, D. (1997). MAP3K-related kinase involved in NF-kappaB induction by TNF, CD95 and IL-1. Nature 385:540-544.
38. Merits, M., Garfield, S., Tanemoto, K., and Tomarev, S. I. (1999). Identification of the region in the N-terminal domain responsible for the cytoplasmic localization of Myoc/Tigr and its association with microtubules. Lab. Invest. 79:1237-1245.
39. Michels-Rautenstrauss, K. G. Mardin, C. Y., Budde, W. M., Liehr, T., Polansky, J., Nguyen, T., Timmerman, V., Van Broeckhoven, C., Naumann, G. O., Pfeiffer, R. A., and Rautenstrauss, B. W. (1998). Juvenile open-angle glaucoma: Fine mapping of the myocilin gene to 1q243-q252 and mutation analysis. Hum. Genet. 102:103-106.
40. Michels-Rautenstrauss, K., Mardin, C., Wakili, N., Junemann, A. M., Villalobos, L., Mejia, C., Soley, G. C. Azofeifa, J., Ozbey, S., Naumann, G. O., Reis, A., and Rautenstrauss, B. (2002). Novel mutations in the MYOC/GLC1A gene in a large group of glaucoma patients. Hum. Mutat. 20:479-480.
41. Nakaya, K. (1994). Localization of phosphoneuroprotein 14 (PNP 14) and its mRNA expression in rat brain determined by immunocytochemistry and in situ hybridization. Brain. Res. Mol. Brain. Res. 27:81-86.
42. Nguyen, T. D., Chen, P., Huang, W. D., Chen, H., Johnson, D., and Polansky, 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.
43. Noda, S., Mashima, Y., Obazawa, M., Kubota, R., Oguchi, Y., Kudoh, J., Minoshima, S., and Shimizu, N. (2000). Myocilin expression in the astrocytes of the optic nerve head. Biochem. Biophys. Res. Commun. 276:1129-1135.
44. O'Brien, E. T., Ren, X., and Wang, Y. (2000). Localization of myocilin to the Golgi apparatus in Schlemm's canal cells. Invest. Ophthalmol. Vis. Sci. 41:3842-3849.
45. Ohlmann, A., Goldwich, A., Flugel-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.
46. Pang, C. P., Leung, Y. F., Fan, B., Baum, L., Tong, W. C., Lee, W. S., Chua, J. K., Fan, D. S., Liu, Y., and Lam, D. S. (2002). TIGR/MYOC gene sequence alterations in individuals with and without primary open-angle glaucoma. Invest. Ophthalmol. Vis. Sci. 43:3231-3235.
47. Park, S. M., Jung, H. Y. Kim, H. O., Rhim, H., Paik, S. R., Chung, K. C., Park, J. H., and Kim, J. (2002). Evidence that alpha-synuclein functions as a negative regulator of Ca(++)-dependent alpha-granule release from human platelets. Blood 100:2506-2514.
48. Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., Stenroos, E. S., Chandrasekharappa, S., Athanassiadou, A., Papapetropoulos, T., Johnson, W. G., Lazzarini, A. M., Duvoisin, R. C., Di Iorio, G., Golbe, L. I., and Nussbaum, R. L. (1997). Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276:2045-2047.
49. Quigley, H. A. (1996). Number of people with glaucoma worldwide. Br. J. Ophthalmol. 80:389-393.
50. Royds, J. A., Parsons, M. A., Taylor, C. B., and Timperley, W. R. (1982). Enolase isoenzyme distribution in the human brain and its tumors. J. Pathol. 137:37-49.
51. Shepard, A. R., Jacobson, N., Fingert, J. H., Stone, E. M., Sheffield, V. C., and Clark, A. F. (2001). Delayed secondary glucocorticoid rewponsiveness of MYOC in human trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 42:3173-3181.
52. Shepard, A. R., Jacobson, N., Sui, R., Steely, T., Lotery, A. J. Stone, E. M., and Clark, A. F. (2003). Characterization of rabbit myocilin: Implications for human myocilin glycosylation and signal peptide usage. BMC Genet. 4:1-10.
53. Singleton, A. B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R., Lincoln, S., Crawley, A., Hanson, M., Maraganore, D. Adler, C., Cookson, M. R., Muenter, M., Baptista, M., Miller, D. Blancato, I. Hardy, J., and Gwinn-Hardy, K. (2003). alpha-Synuclein locus triplication causes Parkinson's disease. Science 302:841.
54. Snyder, H., Mensah, K., Theisler, C., Lee, J., Matouschek, A., and Wolozin, B. (2003). Aggregated and monomeric alpha-synuclein bind to the S6′ proteasomal protein and inhibit proteasomal function. J. Biol Chem. 278:11753-11759.
55. Snyder, H. M., Mensah, K., Surgucheva, I., Festoff, B., Surguchov, A., and Wolozin, B. (2005). β-Synuclein prevents proteasomal inhibition by α-synuclein but not γ-synuclein. J. Biol. Chem. 280:7562-7569.
56. Souza, J. M., Giasson, B. I., Lee, V. M., and Ischiropoulos, H. (2000). Chaperone-like activity of synucleins. FEBS Lett. 474:116-119.
57. Stamer, W. D. Roberts, B. C., Howell, D. N., and Epstein, D. L. (1998). Isolation, culture, and characterization of endothelial cells from Schlemm's canal. Invest. Ophthalmol. Vis. Sci. 39:1804-1812.
58. 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). The identification of a gene that causes primary open-angle glaucoma. Science 5300:668-670.
59. Surguchov, A., McMahon, B., Masliah, E., and Surgucheva, I. (2001a). Synucleins in ocular tissues. J. Neurosci. Res. 65:68-77.
60. Surguchov, A., Palazzo, R. E., and Surgucheva, I. (2001b). Gamma synucleins: Subcellular localization in neuronal and non-neuronal cells and effect on signal transduction. Cell Motil. Cytoskeleton 49:218-228.
61. Surgucheva, I., McMahon, B., Ahmed, F., Tomarev, S., Wax, M. B., and Surguchov, A. (2002). Synucleins in glaucoma: Implication of γ-synuclein in glaucomatous alterations in the optic nerve. J. Nerosci. Res. 68:97-106.
62. Swiderski, R. E., Ying, L., Cassell, M. D., Alward, W. L., Stone, E. M., and Sheffield, V. C. (1999). Expression pattern and in situ localization of the mouse homologue of the human MYOC (GLC1A) gene in adult brain. Brain Res. Mol. Brain Res. 68:64-72.
63. Tamm, E. R. (2002). Myocilin and glaucoma: Facts and ideas. Prog. Retin. Eye Res. 21:395-428.
64. Tanji, K., Mori, F., Imaizumi, T., Yoshida, H., Matsumiya, T., Tamo, W., Yoshimoto, M., Odagiri, H., Sasaki, M., Takahashi, H., Satoh, K., and Wakabayashi, K. (2002). Upregulation of alpha-synuclein by lipopolysaccharide and interleukin-1 in human macrophages. Pathol. Int. 52:572-577.
65. Tompkins, M. M., Gai, W. P., Douglas, S., and Bunn, S. J. (2003). Alpha-synuclein expression localizes to the Golgi apparatus in bovine adrenal medullary chromaffin cells. Brain Res. 984:233-236.
66. 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.
67. Tripathi, B. J., and Tripathi, R. C. (1989). Neural crest origin of human trabecular meshwork and its implications for the pathogenesis of glaucoma. Am. J. Ophthalmol. 107:583-590.
68. Ueda, J., Wentz-Hunter, K. K., Cheng, E. L., Fukuchi, T. Abe, H., and Yue, B. Y. (2000). Ultrastructural localization of myocilin in human trabecular meshwork cells and tissues. J. Histochem. Cytochem. 48:1321-1330.
69. Wentz-Hunter, K., Ueda, J., and Yue, B. Y. (2002). Protein interactions with myocilin. Invest. Ophthalmol. Vis. Sci. 43:176-182.
70. Wentz-Hunter, K., Shen, X., and Yue, B. Y. (2003). Distribution of myocilin, a glaucoma gene product, in human corneal fibroblasts. Mol. Vis. 9:308-314.
71. Wentz-Hunter, K., Shen, X., Okazaki, K., Tanihara, H., and Yue, B. Y. (2004). Overexpression of myocilin in cultured human trabecular meshwork cells. Exp. Cell. Res. 297:39-48.
72. Wordinger, R. J., Lambert, W. Agarwal, R., Talati, M., and Clark, A. F. (2000). Human trabecular meshwork cells secrete neurotrophins and express neurotrophin receptors (Trk). Invest. Ophthal. Vis. Sci. 41:3833-3841.
73. WuDunn, D. (2002). Genetic basis of glaucoma. Curr. Opin. Ophthalmol. 13:55-60.
74. Zhou, Z., and Vollrath, D. (1999). A cellular assay distinguishes normal and mutant TIGR/myocilin protein. Hum. Mol. Genet. 8:2221-2228.