Lens-specific gene recruitment of ζ-crystallin through Pax6, Nrl-Maf, and brain suppressor sites

Molecular and Cellular Biology

Volumn 18, Issue 4, 1998, Pages 2067-2076

  Sharon Friling, Ronit ^a,d   Richardson, Jill ^a,e   Sperbeck, Sally ^a   Lee, Douglas ^a,f   Rauchman, Michael ^b   Maas, Richard ^b   Swaroop, Anand ^c   Wistow, Graeme ^a  

^a NATIONAL EYE INSTITUTE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d Columbia University ^*  (United States)

^e GLAXOSMITHKLINE   (United Kingdom)

^f BAYER CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN KINASE;

ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; TELOPHASE;

CAVIA PORCELLUS; MUS MUSCULUS; SACCHAROMYCES CEREVISIAE; SUS SCROFA;

EID: 0031900978     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.18.4.2067     Document Type: Article

References (68)

1. Carriere, C., S. Plaza, P. Martin, B. Quatannens, M. Bailly, D. Stehelin, and S. Saule. 1993. Characterization of quail Pax-6 (Pax-QNR) proteins expressed in the neuroretina. Mol. Cell. Biol. 13:7257-7266.
2. Chalepakis, G., J. Wijnholds, P. Giese, M. Schachner, and P. Gruss. 1994. Characterization of Pax-6 and Hoxa-1 binding to the promoter region of the neural cell adhesion molecule L1. DNA Cell Biol. 13:841-900.
3. Cvekl, A., and J. Piatigorsky. 1996. Lens development and crystallin gene expression: many roles for Pax-6. Bioossays 18:621-630.
4. de Jong, W. W., N. H. Lubsen, and H. J. Kraft. 1994. Molecular evolution of the eye lens, p. 391-442. In G. Chader and N. Osbourne (ed.), Progress in retinal and eye research, vol. 13. Elsevier Science Ltd., Oxford, United Kingdom.
5. Edlund, T., M. D. Walker, P. J. Barr, and W. J. Rutter. 1985. Cell-specific expression of the rat insulin gene: evidence for role of two distinct 5′ flanking elements. Science 230:912-916.
6. Epstein, J., J. Cai, T. Glaser, L. Jepeal, and R. Maas. 1994. Identification of a Pax paired domain recognition sequence and evidence for DNA-dependent conformational changes. J. Biol. Chem. 269:8355-8361.
7. Epstein, J. A., T. Glaser, J. Cai, L. Jepeal, D. S. Walton, and R. L. Maas. 1994. Two independent and interactive DNA-binding subdomains of the Pax6 paired domain are regulated by alternative splicing. Genes Dev. 8:2022-2035.
8. Farjo, Q., A. U. Jackson, J. Xu, M. Gryzenia, C. Skolnick, N. Agarwal, and A. Swaroop. 1993. Molecular characterization of the murine neural retina leucine zipper gene, Nrl. Genomics 18:216-222.
9. Fujioka, M., P. Miskiewicz, L. Raj, A. A. Gulledge, M. Weir, and T. Goto. 1996. Drosophila Paired regulates late even-skipped expression through a composite binding site for the paired domain and the homeodomain. Development 122:2697-2707.
10. Galas, D. J., and A. Schmitz. 1978. DNAse footprinting: a simple method for the detection of protein-DNA binding specificity. Nucleic Acids Res. 5:3157-3170.
11. Garland, D., P. V. Rao, A. Del Corso, U. Mura, and J. S. Zigler, Jr. 1991. ζ-Crystallin is a major protein in the lens of Camelus dromedarius. Arch. Biochem. Biophys. 285:134-136.
12. Gehring, W. J., M. Affolter, and T. Burglin. 1994. Homeodomain proteins. Annu. Rev. Biochem. 63:487-526.
13. Glaser, T., L. Jepeal, J. G. Edwards, S. R. Young, J. Favor, and R. L. Maas. 1994. Pax6 gene dosage effect in a family with congenital cataracts, aniridia, anophthalmia and central nervous system defects. Nat. Genet. 7:463-471.
14. Gonzalez, P., C. Hernandez-Calzadilla, P. V. Rao, I. R. Rodriguez, J. S. Zigler, Jr., and T. Borras. 1994. Comparative analysis of the ζ-crystallin/ quinone reductase gene in guinea pig and mouse. Mol. Biol. Evol. 11:305-315.
15. Gonzalez, P., P. V. Rao, S. B. Nunez, and J. S. Zigler, Jr. 1995. Evidence for independent recruitment of ζ-crystallin/quinone reductase (CRYZ) as a crystallin in camelids and hystricomorph rodents. Mol. Biol. Evol. 12:773-781.
16. Gorman, C., R. Padmanabhan, and B. H. Howard. 1983. High efficiency DNA-mediated transformation of primate cells. Science 221:551-553.
17. Gorman, C. M., L. F. Moffat, and B. H. Howard. 1982. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2:1044-1051.
18. Graham, C., J. Hodin, and G. Wistow. 1996. A retinaldehye dehydrogenase as a structural protein in a mammalian eye lens: gene recruitment of η-crystallin. J. Biol. Chem. 271:15623-15628.
19. Halder, G., P. Callaerts, and W. J. Gehring. 1995. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267:1788-1792.
20. Hanson, I., and V. van Heyningen. 1995. Pax6: more than meets the eye. Trends Genet. 11:268-272.
21. Henikoff, S. 1984. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351-359.
22. Hill, R. E., J. Favor, B. L. Hogan, C. C. Ton, G. F. Saunders, I. M. Hanson, J. Prosser, T. Jordan, N. D. Hastie, and V. van Heyningen. 1991. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354:522-525.
23. Ho, I. C., M. R. Hodge, J. W. Rooney, and L. H. Glimcher. 1996. The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 85:973-983.
24. Holst, B. D., Y. Wang, F. S. Jones, and G. M. Edelman. 1997. A binding site for Pax proteins regulates expression of the gene for the neural cell adhesion molecule in the embryonic spinal cord. Proc. Natl. Acad. Sci. USA 94:1465-1470.
25. Huang, Q. L., P. Russell, S. Stone, and J. S. Zigler. 1987. Zeta-crystallin, a novel lens protein from the guinea pig. Curr. Eye Res. 6:725-732.
26. Igarashi, K., K. Kataoka, K. Itoh, N. Hayashi, M. Nishizawa, and M. Yamamoto. 1994. Regulation of transcription by dimenzation of erythroid factor NF-E2 p45 with small Maf proteins. Nature 367:568-572.
27. Jaworski, C., S. Sperbeck, C. Graham, and G. Wistow. 1997. Alternative splicing of Pax6 in bovine eye and evolutionary conservation of intron sequences. Biochem. Biophys. Res. Commun. 240:196-202.
28. Jun, S., and C. Desplan. 1996. Cooperative interactions between paired domain and homeodomain. Development 122:2639-2650.
29. Kamachi, Y. 1996. Involvement of SOX proteins in activation of crystallin genes and lens development. Tanpakushitsu Kakusan Koso 41(Suppl. 8): 1113-1123.
30. Kamachi, Y., S. Sockanathan, Q. Liu, M. Breitman, R. Lovell-Badge, and H. Kondoh. 1995. Involvement of SOX proteins in lens-specific activation of crystallin genes. EMBO J. 14:3510-3519.
31. Kataoka, K., K. T. Fujiwara, M. Noda, and M. Nishizawa. 1994. MafB, a new Maf family transcription activator that can associate with Maf and Fos but not with Jun. Mol. Cell. Biol. 14:7581-7591.
32. Kataoka, K., K. Igarashi, K. Itoh, K. T. Fujiwara, M. Noda, M. Yamamoto, and M. Nishizawa. 1995. Small Maf proteins heterodimerize with Fos and may act as competitive repressers of the NF-E2 transcription factor. Mol. Cell. Biol. 15:21811-2190.
33. Kataoka, K., M. Noda, and M. Nishizawa. 1994. Maf nuclear oncoprotein recognizes sequences related to an AP-1 site and forms heterodimers with both Fos and Jun. Mol. Cell. Biol. 14:700-712.
34. Kataoka, K., M. Noda, and M. Nishizawa. 1996. Transactivation activity of Maf nuclear oncoprotein is modulated by Jun, Fos and small Maf proteins. Oncogene 12:53-62.
35. Kerppola, T. K., and T. Curran. 1994. Maf and Nrl can bind to AP-1 sites and form heterodimers with Fos and Jun. Oncogene 9:675-684.
36. Kumar, R., S. Chen, D. Scheurer, Q. L. Wang, E. Duh, C. H. Sung, A. Rehemtulla, A. Swaroop, R. Adler, and D. J. Zack. 1996. The bZIP transcription factor Nrl stimulates rhodopsin promoter activity in primary retinal cell cultures. J. Biol. Chem. 271:29612-29618.
37. Lee, D. C., P. Gonzalez, P. V. Rao, J. S. Zigler Jr., and G. J. Wistow. 1993. Carbonyl-metabolizing enzymes and their relatives recruited as structural proteins in the eye lens. Adv. Exp. Med. Biol. 284:159-168.
38. Lee, D. C., P. Gonzalez, and G. Wistow. 1994. ζ-Crystallin: a lens-specific promoter and the gene recruitment of an enzyme as a crystallin. J. Mol. Biol. 236:669-678.
39. Li, H. S., J. M. Yang, R. D. Jacobson, D. Pasko, and O. Sundin. 1994. Pax-6 is first expressed in a region of ectoderm anterior to the early neural plate: implications for stepwise determination of the lens. Dev. Biol. 162:181-194.
40. Liu, Q., X. Ji, M. L. Breitman, P. F. Hitchcock, and A. Swaroop. 1996. Expression of the bZIP transcription factor gene Nrl in the developing nervous system. Oncogene 12:207-211.
41. Matsuo, I., and K. Yasuda. 1992. The cooperative interaction between two motifs of an enhancer element of the chicken αA-crystallin gene, αCE1 and αCE2 confers lens-specific expression. Nucleic Acids Res. 20:3701-3712.
42. Miksicek, R., A. Heber, W. Schmid, U. Danesch, G. Posseckert, M. Beato, and G. Schutz. 1986. Glucocorticoid responsiveness of the transcriptional enhancer of Moloney murine sarcoma virus. Cell 46:283-290.
43. Miskiewicz, P., D. Morrissey, Y. Lan, L. Raj, S. Kessler, M. Fujioka, T. Goto, and M. Weir. 1996. Both the paired domain and homeodomain are required for in vivo function of Drosophila Paired. Development 122:2709-2718.
44. Nasrin, N., C. Buggs, X. F. Kong, J. Carnazza, M. Goebl, and M. Alexander-Bridges. 1991. DNA-binding properties of the product of the testis-determining gene and a related protein. Nature 354:317-320.
45. Ogino, H., and K. Yasuda. 1996. Involvement of maf gene family in crystallin gene regulation. Tanpakushitsu Kakusan Koso 41(Suppl. 8):1050-1057.
46. 45a. Okataka-Maruyama, R., and A. Chepelinsky. Personal communication.
47. Pontiggia, A., S. Whitfield, P. N. Goodfellow, R. Lovell-Badge, and M. E. Bianchi. 1995. Evolutionary conservation in the DNA-binding and -bending properties of HMG-boxes from SRY proteins of primates. Gene 154:277-280.
48. Prior, H. M., and M. A. Walter. 1996. SOX genes: architects of development. Mol. Med. 2:405-412.
49. Quiring, R., U. Walldorf, U. Kloter, and W. J. Gehring. 1994. Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science 265:785-789.
50. Rao, P. V., C. M. Krishna, and J. S. Zigler. 1992. Identification and characterization of the enzymatic activity of ζ-crystallin from guinea pig lens. A novel NADPH:quinone oxidoreductase. J. Biol. Chem. 267:96-102.
51. Reddan, J. R., A. B. Chepelinsky, D. C. Dziedzic, J. Piatigorsky, and E. M. Goldenberg. 1986. Retention of lens specificity in long-term cultures of diploid rabbit lens epithelial cells. Differentiation 33:168-174.
52. Rehemtulla, A., R. Warwar, R. Kumar, X. Ji, D. J. Zack, and A. Swaroop. 1996. The basic motif-leucine zipper transcription factor Nrl can positively regulate rhodopsin gene expression. Proc. Natl. Acad. Sci. USA 93:191-195.
53. Richardson, J., A. Cvekl, and G. Wistow. 1995. Pax-6 is essential for lens specific expression of ζ-crystallin. Proc. Natl. Acad. Sci. USA 92:4676-4680.
54. Sax, C., and J. Piatigorsky. 1994. Expression of the α-crystallin/small heat shock protein/molecular chaperone genes in the lens and other tissues. Adv. Enzymol. Relat. Areas Mol. Biol. 69:155-201.
55. Shapiro, D. J., P. A. Sharp, W. W. Wahli, and M. J. Keller. 1988. A high-efficiency HeLa cell nuclear transcription extract. DNA 7:47-55.
56. Sierra, F. 1990. BioMethods, vol. 2: a laboratory guide to in vitro transcription. Birkhauser, Boston, Mass.
57. Sinclair, A. H., P. Berta, M. S. Palmer, J. R. Hawkins, B. L. Griffiths, M. J. Smith, J. W. Foster, A. M. Frischauf, R. Lovell-Badge, and P. N. Goodfellow. 1990. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346:240-244.
58. St. Onge, L., B. Sosa-Pineda, K. Chowdhury, A. Mansouri, and P. Gruss. 1997. Pax6 is required for differentiation of glucagon-producing alpha-cells in mouse pancreas. Nature 387:406-409.
59. Swaroop, A., J. Z. Xu, H. Pawar, A. Jackson, C. Skolnick, and N. Agarwal. 1992. A conserved retina-specific gene encodes a basic motif/leucine zipper domain. Proc. Natl. Acad. Sci. USA 89:266-270.
60. Ton, C. C., H. Hirvonen, H. Miwa, M. M. Weil, P. Monaghan, T. Jordan, V. van Heyningen, N. D. Hastie, H. Meijers-Heijboer, M. Drechsler, et al. 1991. Positional cloning and characterization of a paired box- and homeobox-containing gene from the aniridia region. Cell 67:1059-1074.
61. Turque, N., S. Plaza, F. Radvanyi, C. Carriere, and S. Saule. 1994. Pax-QNR/Pax-6, a paired box- and homeobox-containing gene expressed in neurons, is also expressed in pancreatic endocrine cells. Mol. Endocrinol. 8:929-938.
62. van de Wetering, M., and H. Clevers. 1992. Sequence-specific interaction of the HMG box proteins TCF-1 and SRY occurs within the minor groove of a Watson-Crick double helix. EMBO J. 11:3039-3044.
63. Walther, C., and P. Gruss. 1991. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113:1435-1449.
64. Wistow, G. 1993. Lens crystallins: gene recruitment and evolutionary dynamism. Trends Biochem. Sci. 18:301-306.
65. Wistow, G. 1995. Molecular biology and evolution of crystallins: gene recruitment and multifunctional proteins in the eye lens. Molecular Biology Intelligence Series. R.G. Landes Co., Austin, Tex.
66. Xu, W., M. A. Rould, S. Jun, C. Desplan, and C. O. Pabo. 1995. Crystal structure of a paired domain-DNA complex at 2.5 A resolution reveals structural basis for Pax developmental mutations. Cell 80:639-650.
67. Yamada, T., T. Nakamura, H. Westphal, and P. Russell. 1990. Synthesis of α-crystallin by a cell line derived from the lens of a transgenic animal. Curr. Eye Res. 9:31-37.
68. Yuan, H., N. Corbi, C. Basilico, and L. Dailey. 1995. Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev. 9:2635-2645.