Ubiquitin-proteasome pathway function is required for lens cell proliferation and differentiation

Investigative Ophthalmology and Visual Science

Volumn 47, Issue 6, 2006, Pages 2569-2575

  Guo, Weimin ^a   Shang, Fu ^a   Liu, Qing ^a   Urim, Lyudmila ^b   Zhang, Minlei ^b   Taylor, Allen ^a  

^a TUFTS UNIVERSITY   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; BETA CRYSTALLIN; BROXURIDINE; CP49 PROTEIN; CRYSTALLIN; CYTOPLASM PROTEIN; FILENSIN; GAMMA CRYSTALLIN; LACTACYSTIN BETA LACTONE; MAJOR INTRINSIC PROTEIN 26; PROTEASOME; PROTEIN; UBIQUITIN; AQUAPORIN; AQUAPORIN 0; CLASTO-LACTACYSTIN BETA-LACTONE; CYSTEINE PROTEINASE INHIBITOR; EYE PROTEIN; FIBROBLAST GROWTH FACTOR 2; INTERMEDIATE FILAMENT PROTEIN; LACTONE; MEMBRANE PROTEIN; PHAKININ;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME INHIBITION; EPITHELIUM CELL; LENS EPITHELIUM; LENS FIBER; MORPHOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; ANIMAL; CYTOLOGY; DRUG EFFECT; LENS; METABOLISM; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; WESTERN BLOTTING; WISTAR RAT;

ANIMALS; AQUAPORINS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CRYSTALLINS; CYSTEINE PROTEINASE INHIBITORS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EYE PROTEINS; FIBROBLAST GROWTH FACTOR 2; INTERMEDIATE FILAMENT PROTEINS; LACTONES; LENS, CRYSTALLINE; MEMBRANE GLYCOPROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; RATS, WISTAR; UBIQUITIN;

EID: 33745675537     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.05-0261     Document Type: Article

References (64)

1. Lee A, Fischer RS, Fowler VM. Stabilization and remodeling of the membrane skeleton during lens fiber cell differentiation and maturation. Dev Dyn. 2000;217:257-270.
2. Mousa GY, Trevithick JR. Actin in the lens: changes in actin during differentiation of lens epithelial cells in vivo. Exp Eye Res. 1979;29:71-81.
3. Lang RA. Which factors stimulate lens fiber cell differentiation in vivo? Invest Ophthalmol Vis Sci. 1999;40:3075-3078.
4. Chamberlain CG, McAvoy JW. Evidence that fibroblast growth factor promotes lens fibre differentiation. Curr Eye Res. 1987;6:1165-1169.
5. Kuszak JR. The ultrastructure of epithelial and fiber cells in the crystalline lens. Int Rev Cytol. 1995;163:305-350.
6. Nakamura T, Pichel JG, Williams-Simons L, Westphal H. An apoptotic defect in lens differentiation caused by human p53 is rescued by a mutant allele. Proc Natl Acad Sci USA. 1995;92:6142-6146.
7. Pan H, Griep AE. Altered cell cycle regulation in the lens of HPV-16 E6 or E7 transgenic mice: implications for tumor suppressor gene function in development. Genes Dev. 1994;8:1285-1299.
8. Wang Y, He H, Zigler JS Jr, et al. bFGF suppresses serum-deprivation- induced apoptosis in a human lens epithelial cell line. Exp Cell Res. 1999;249:123-130.
9. McAvoy JW, Chamberlain CG. Fibroblast growth factor (FGF) induces different responses in lens epithelial cells depending on its concentration. Development. 1989;107:221-228.
10. Ibaraki N, Lin LR, Reddy VN. Effects of growth factors on proliferation and differentiation in human lens epithelial cells in early subculture. Invest Ophthalmol Vis Sci. 1995;36:2304-2312.
11. Lovicu FJ, McAvoy JW. FGF-induced lens cell proliferation and differentiation is dependent on MAPK (ERK1/2) signalling. Development. 2001;128:5075-5084.
12. Liu J, Chamberlain CG, McAvoy JW. IGF enhancement of FGF-induced fibre differentiation and DNA synthesis in lens explants. Exp Eye Res. 1996;63:621-629.
13. Mousa GY, Trevithick JR. Differentiation of rat lens epithelial cells in tissue culture, II: effects of cytochalasins B and D on actin organization and differentiation. Dev Biol. 1977;60:14-25.
14. Hershko A, Ciechanover A, Varshavsky A. Basic Medical Research Award: the ubiquitin system. Nat Med. 2000;6:1073-1081.
15. Bebok Z, Mazzochi C, King SA, Hong JS, Sorscher EJ. The mechanism underlying cystic fibrosis transmembrane conductance regulator transport from the endoplasmic reticulum to the proteasome includes Sec61beta and a cytosolic, deglycosylated intermediary. J Biol Chem. 1998;273:29873-29878.
16. Spataro V, Norbury C, Harris AL. The ubiquitin-proteasome pathway in cancer. Br J Cancer. 1998;77:448-455.
17. Rossi S, Loda M. The role of the ubiquitination-proteasome pathway in breast cancer: use of mouse models for analyzing ubiquitination processes. Breast Cancer Res. 2003;5:16-22.
18. Wang GP, Khatoon S, Iqbal K, Grundke-Iqbal I. Brain ubiquitin is markedly elevated in Alzheimer disease. Brain Res. 1991;566:146-151.
19. Shimura H, Hattori N, Kubo S, et al. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat Genet. 2000;25:302-305.
20. Alves-Rodrigues A, Gregori L, Figueiredo-Pereira ME. Ubiquitin, cellular inclusions and their role in neurodegeneration. Trends Neurosci. 1998;21:516-520.
21. Dobson CM. Protein folding and misfolding. Nature. 2003;426:884-890.
22. Shang F, Gong X, Taylor A. Activity of ubiquitin-dependent pathway in response to oxidative stress: ubiquitin-activating enzyme is transiently up-regulated. J Biol Chem. 1997;272:23086-23093.
23. Shang F, Taylor A. Oxidative stress and recovery from oxidative stress are associated with altered ubiquitin conjugating and proteolytic activities in bovine lens epithelial cells. Biochem J. 1995;307(pt 1):297-303.
24. Huang LL, Jahngen-Hodge J, Taylor A. Bovine lens epithelial cells have a ubiquitin-dependent proteolysis system. Biochim Biophys Acta. 1993;1175:181-187.
25. Huang LL, Shang F, Nowell TR Jr, Taylor A. Degradation of differentially oxidized alpha-crystallins in bovine lens epithelial cells. Exp Eye Res. 1995;61:45-54.
26. Jahngen JH, Haas AL, Ciechanover A, et al. The eye lens has an active ubiquitin-protein conjugation system. J Biol Chem. 1986;261:13760-13767.
27. Jahngen JH, Lipman RD, Eisenhauer DA, Jahngen EG Jr, Taylor A. Aging and cellular maturation cause changes in ubiquitin-eye lens protein conjugates. Arch Biochem Biophys. 1990;276:32-37.
28. Shang F, Gong X, McAvoy JW, et al. Ubiquitin-dependent pathway is up-regulated in differentiating lens cells. Exp Eye Res. 1999;68:179-192.
29. Shang F, Gong X, Palmer HJ, Nowell TR Jr, Taylor A. Age-related decline in ubiquitin conjugation in response to oxidative stress in the lens. Exp Eye Res. 1997;64:21-30.
30. Guo W, Shang F, Liu Q, et al. Differential regulation of components of the ubiquitin-proteasome pathway during lens cell differentiation. Invest Ophthalmol Vis Sci. 2004;45:1194-1201.
31. McAvoy JW, Fernon VT. Neural retinas promote cell division and fibre differentiation in lens epithelial explants. Curr Eye Res. 1984;3:827-834.
32. Cai H, Singh I, Wagner BJ. Gene expression of the proteasome in rat lens development. Exp Eye Res. 1998;66:339-346.
33. Chamberlain CG, McAvoy JW. Induction of lens fibre differentiation by acidic and basic fibroblast growth factor (FGF). Growth Factors. 1989;1:125-134.
34. Kuwabara T. The maturation of the lens cell: a morphologic study. Exp Eye Res. 1975;20:427-443.
35. Lovicu FJ, McAvoy JW. The age of rats affects the response of lens epithelial explants to fibroblast growth factor: an ultrastructural analysis. Invest Ophthalmol Vis Sci. 1992;33:2269-278.
36. Weber GF, Menko AS. The canonical intrinsic mitochondrial death pathway has a non-apoptotic role in signaling lens cell differentiation. J Biol Chem. 2005;280:22135-22145.
37. McAvoy JW. Cell division, cell elongation and distribution of alpha-, beta- and gamma-crystallins in the rat lens. J Embryol Exp Morphol. 1978;44:149-165.
38. Yancey SB, Koh K, Chung J, Revel JP. Expression of the gene for main intrinsic polypeptide (MIP): separate spatial distributions of MIP and beta-crystallin gene transcripts in rat lens development. J Cell Biol. 1988;106:705-714.
39. Wang X, Garcia CM, Shui YB, Beebe DC. Expression and regulation of α-, β-, and γ-crystallins in mammalian lens epithelial cells. Invest Ophthalmol Vis Sci. 2004;45:3608-3619.
40. Shubert EE, Trevithick JR, Hollenberg MJ. Localization of gamma crystallins in the developing lens of the rat. Can J Ophthalmol. 1970;5:353-365.
41. Sussman MA, McAvoy JW, Rudisill M, et al. Lens tropomodulin: developmental expression during differentiation. Exp Eye Res. 1996;63:223-232.
42. Kim S, Ge H, Ohtaka-Maruyama C, Chepelinsky AB. The transcription factor Sp3 interacts with promoter elements of the lens specific MIP gene. Mol Vis. 1999;5:12.
43. Shiels A, Bassnett S. Mutations in the founder of the MIP gene family underlie cataract development in the mouse. Nat Genet. 1996;12:212-215.
44. FitzGerald PG. Age-related changes in a fiber cell-specific extrinsic membrane protein. Curr Eye Res. 1988;7:1255-1262.
45. FitzGerald PG, Gottlieb W. The Mr 115 kd fiber cell-specific protein is a component of the lens cytoskeleton. Curr Eye Res. 1989;8:801-811.
46. Ireland M, Maisel H. A cytoskeletal protein unique to lens fiber cell differentiation. Exp Eye Res. 1984;38:637-645.
47. Zhang P, Liegeois NJ, Wong C, et al. Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature. 1997;387:151-158.
48. Yoshida K, Kim JI, Imaki J, et al. Proliferation in the posterior region of the lens of c-maf-/- mice. Curr Eye Res. 2001;23:116-119.
49. Shirke S, Faber SC, Hallem E, et al. Misexpression of IGF-I in the mouse lens expands the transitional zone and perturbs lens polarization. Mech Dev. 2001;101:167-174.
50. McCaffrey J, Yamasaki L, Dyson NJ, Harlow E, Griep AE. Disruption of retinoblastoma protein family function by human papillomavirus type 16 E7 oncoprotein inhibits lens development in part through E2F-1. Mol Cell Biol. 1999;19:6458-6468.
51. He HY, Gao C, Vrensen G, Zelenka P. Transient activation of cyclin B/Cdc2 during terminal differentiation of lens fiber cells. Dev Dyn. 1998;211:26-34.
52. Peters JM. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol Cell. 2002;9:931-943.
53. Shang F, Taylor A. Function of the ubiquitin proteolytic pathway in the eye. Exp Eye Res. 2004;78:1-14.
54. Nahreini P, Andreatta C, Prasad KN. Proteasome activity is critical for the cAMP-induced differentiation of neuroblastoma cells. Cell Mol Neurobiol. 2001;21:509-521.
55. Nahreini P, Andreatta C, Hanson A, Prasad KN. Concomitant differentiation and partial proteasome inhibition trigger apoptosis in neuroblastoma cells. J Neurooncol. 2003;63:15-23.
56. Chen CY, Pajak L, Tamburlin J, Bofinger D, Koury ST. The effect of proteasome inhibitors on mammalian erythroid terminal differentiation. Exp Hematol. 2002;30:634-639.
57. Prince AM, May JS, Burton GR, Lyle RE, McGehee RE Jr. Proteasomal degradation of retinoblastoma-related p130 during adipocyte differentiation. Biochem Biophys Res Commun. 2002;290:1066-1071.
58. Kim SS, Rhee S, Lee KH, et al. Inhibitors of the proteasome block the myogenic differentiation of rat L6 myoblasts. FEBS Lett. 1998;433:47-50.
59. Pasquini LA, Paez PM, Moreno MA, Pasquini JM, Soto EF. Inhibition of the proteasome by lactacystin enhances oligodendroglial cell differentiation. J Neurosci. 2003;23:4635-4644.
60. Omura S, Matsuzaki K, Fujimoto T, et al. Structure of lactacystin, a new microbial metabolite which induces differentiation of neuroblastoma cells. J Antibiot (Tokyo). 1991;44:117-118.
61. Obin M, Mesco E, Gong X, et al. Neurite outgrowth in PC12 cells: distinguishing the roles of ubiquitylation and ubiquitin-dependent proteolysis. J Biol Chem. 1999;274:11789-11795.
62. Muratani M, Tansey WP. How the ubiquitin-proteasome system controls transcription. Nat Rev Mol Cell Biol. 2003;4:192-201.
63. Gwon A, Gruber LJ, Mantras C. Restoring lens capsule integrity enhances lens regeneration in New Zealand albino rabbits and cats. J Cataract Refract Surg. 1993;19:735-746.
64. Gwon A, Gruber L, Mantras C, Cunanan C. Lens regeneration in New Zealand albino rabbits after endocapsular cataract extraction. Invest Ophthalmol Vis Sci. 1993;34:2124-2129.