Abstract
Two cis-acting promoter elements (-108 to -100 and -49 to -33) of the mouse alpha A-crystallin gene, which is highly expressed in the ocular lens, were studied. Here we show that DE1 (-108 to -100; 5'TGACGGTG3'), which resembles the consensus cyclic AMP (cAMP)-responsive element sequence (CRE; 5'TGACGT[A/C][A/G]3'), behaves like a functional CRE site. Transfection experiments and electrophoretic mobility shift assays (EMSAs) using site-specific mutations correlated a loss of function with deviations from the CRE consensus sequence. Results of EMSAs in the presence of antisera against CREB, delta CREB, and CREM were consistent with the binding of CREB-like proteins to the DE1 sequence. Stimulation of alpha A-crystallin promoter activity via 8-bromo-cAMP, forskolin, or human T-cell leukemia virus type I Tax1 in transfections and reduction of activity of this site in cell-free transcription tests by competition with the somatostatin CRE supported the idea that DE1 is a functional CRE. Finally, Pax-6, a member of the paired-box family of transcription factors, activated the mouse alpha A-crystallin promoter in cotransfected COP-8 fibroblasts and bound to the -59 to -29 promoter sequence in EMSAs. These data provide evidence for a synergistic role of Pax-6 and CREB-like proteins for high expression of the mouse alpha A-crystallin gene in the lens.
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- Adya N., Zhao L. J., Huang W., Boros I., Giam C. Z. Expansion of CREB's DNA recognition specificity by Tax results from interaction with Ala-Ala-Arg at positions 282-284 near the conserved DNA-binding domain of CREB. Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5642–5646. doi: 10.1073/pnas.91.12.5642. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Andrisani O. M., Pot D. A., Zhu Z., Dixon J. E. Three sequence-specific DNA-protein complexes are formed with the same promoter element essential for expression of the rat somatostatin gene. Mol Cell Biol. 1988 May;8(5):1947–1956. doi: 10.1128/mcb.8.5.1947. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berkowitz L. A., Gilman M. Z. Two distinct forms of active transcription factor CREB (cAMP response element binding protein). Proc Natl Acad Sci U S A. 1990 Jul;87(14):5258–5262. doi: 10.1073/pnas.87.14.5258. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berkowitz L. A., Riabowol K. T., Gilman M. Z. Multiple sequence elements of a single functional class are required for cyclic AMP responsiveness of the mouse c-fos promoter. Mol Cell Biol. 1989 Oct;9(10):4272–4281. doi: 10.1128/mcb.9.10.4272. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bhat S. P., Nagineni C. N. alpha B subunit of lens-specific protein alpha-crystallin is present in other ocular and non-ocular tissues. Biochem Biophys Res Commun. 1989 Jan 16;158(1):319–325. doi: 10.1016/s0006-291x(89)80215-3. [DOI] [PubMed] [Google Scholar]
- Brady J., Jeang K. T., Duvall J., Khoury G. Identification of p40x-responsive regulatory sequences within the human T-cell leukemia virus type I long terminal repeat. J Virol. 1987 Jul;61(7):2175–2181. doi: 10.1128/jvi.61.7.2175-2181.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carriere C., Plaza S., Martin P., Quatannens B., Bailly M., Stehelin D., Saule S. Characterization of quail Pax-6 (Pax-QNR) proteins expressed in the neuroretina. Mol Cell Biol. 1993 Dec;13(12):7257–7266. doi: 10.1128/mcb.13.12.7257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chalepakis G., Fritsch R., Fickenscher H., Deutsch U., Goulding M., Gruss P. The molecular basis of the undulated/Pax-1 mutation. Cell. 1991 Sep 6;66(5):873–884. doi: 10.1016/0092-8674(91)90434-z. [DOI] [PubMed] [Google Scholar]
- Chalepakis G., Wijnholds J., Giese P., Schachner M., Gruss P. Characterization of Pax-6 and Hoxa-1 binding to the promoter region of the neural cell adhesion molecule L1. DNA Cell Biol. 1994 Sep;13(9):891–900. doi: 10.1089/dna.1994.13.891. [DOI] [PubMed] [Google Scholar]
- Chepelinsky A. B., King C. R., Zelenka P. S., Piatigorsky J. Lens-specific expression of the chloramphenicol acetyltransferase gene promoted by 5' flanking sequences of the murine alpha A-crystallin gene in explanted chicken lens epithelia. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2334–2338. doi: 10.1073/pnas.82.8.2334. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cvekl A., Sax C. M., Bresnick E. H., Piatigorsky J. A complex array of positive and negative elements regulates the chicken alpha A-crystallin gene: involvement of Pax-6, USF, CREB and/or CREM, and AP-1 proteins. Mol Cell Biol. 1994 Nov;14(11):7363–7376. doi: 10.1128/mcb.14.11.7363. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Czerny T., Schaffner G., Busslinger M. DNA sequence recognition by Pax proteins: bipartite structure of the paired domain and its binding site. Genes Dev. 1993 Oct;7(10):2048–2061. doi: 10.1101/gad.7.10.2048. [DOI] [PubMed] [Google Scholar]
- Dasgupta S., Hohman T. C., Carper D. Hypertonic stress induces alpha B-crystallin expression. Exp Eye Res. 1992 Mar;54(3):461–470. doi: 10.1016/0014-4835(92)90058-z. [DOI] [PubMed] [Google Scholar]
- Dean D. C., Blakeley M. S., Newby R. F., Ghazal P., Hennighausen L., Bourgeois S. Forskolin inducibility and tissue-specific expression of the fibronectin promoter. Mol Cell Biol. 1989 Apr;9(4):1498–1506. doi: 10.1128/mcb.9.4.1498. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deutsch P. J., Hoeffler J. P., Jameson J. L., Lin J. C., Habener J. F. Structural determinants for transcriptional activation by cAMP-responsive DNA elements. J Biol Chem. 1988 Dec 5;263(34):18466–18472. [PubMed] [Google Scholar]
- Dignam J. D., Martin P. L., Shastry B. S., Roeder R. G. Eukaryotic gene transcription with purified components. Methods Enzymol. 1983;101:582–598. doi: 10.1016/0076-6879(83)01039-3. [DOI] [PubMed] [Google Scholar]
- Donovan D. M., Sax C. M., Klement J. F., Li X., Chepelinsky A. B., Piatigorsky J. Conservation of mouse alpha A-crystallin promoter activity in chicken lens epithelial cells. J Mol Evol. 1992 Oct;35(4):337–345. doi: 10.1007/BF00161171. [DOI] [PubMed] [Google Scholar]
- Dubin R. A., Wawrousek E. F., Piatigorsky J. Expression of the murine alpha B-crystallin gene is not restricted to the lens. Mol Cell Biol. 1989 Mar;9(3):1083–1091. doi: 10.1128/mcb.9.3.1083. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Epstein J. A., Glaser T., Cai J., Jepeal L., Walton D. S., Maas R. L. Two independent and interactive DNA-binding subdomains of the Pax6 paired domain are regulated by alternative splicing. Genes Dev. 1994 Sep 1;8(17):2022–2034. doi: 10.1101/gad.8.17.2022. [DOI] [PubMed] [Google Scholar]
- Epstein J., Cai J., Glaser T., Jepeal L., Maas R. Identification of a Pax paired domain recognition sequence and evidence for DNA-dependent conformational changes. J Biol Chem. 1994 Mar 18;269(11):8355–8361. [PubMed] [Google Scholar]
- Foulkes N. S., Borrelli E., Sassone-Corsi P. CREM gene: use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription. Cell. 1991 Feb 22;64(4):739–749. doi: 10.1016/0092-8674(91)90503-q. [DOI] [PubMed] [Google Scholar]
- Foulkes N. S., Mellström B., Benusiglio E., Sassone-Corsi P. Developmental switch of CREM function during spermatogenesis: from antagonist to activator. Nature. 1992 Jan 2;355(6355):80–84. doi: 10.1038/355080a0. [DOI] [PubMed] [Google Scholar]
- Glaser T., Jepeal L., Edwards J. G., Young S. R., Favor J., Maas R. L. PAX6 gene dosage effect in a family with congenital cataracts, aniridia, anophthalmia and central nervous system defects. Nat Genet. 1994 Aug;7(4):463–471. doi: 10.1038/ng0894-463. [DOI] [PubMed] [Google Scholar]
- Glaser T., Walton D. S., Maas R. L. Genomic structure, evolutionary conservation and aniridia mutations in the human PAX6 gene. Nat Genet. 1992 Nov;2(3):232–239. doi: 10.1038/ng1192-232. [DOI] [PubMed] [Google Scholar]
- Gonzalez G. A., Montminy M. R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell. 1989 Nov 17;59(4):675–680. doi: 10.1016/0092-8674(89)90013-5. [DOI] [PubMed] [Google Scholar]
- Habener J. F. Cyclic AMP response element binding proteins: a cornucopia of transcription factors. Mol Endocrinol. 1990 Aug;4(8):1087–1094. doi: 10.1210/mend-4-8-1087. [DOI] [PubMed] [Google Scholar]
- Hai T. W., Horikoshi M., Roeder R. G., Green M. R. Analysis of the role of the transcription factor ATF in the assembly of a functional preinitiation complex. Cell. 1988 Sep 23;54(7):1043–1051. doi: 10.1016/0092-8674(88)90119-5. [DOI] [PubMed] [Google Scholar]
- Hill R. E., Favor J., Hogan B. L., Ton C. C., Saunders G. F., Hanson I. M., Prosser J., Jordan T., Hastie N. D., van Heyningen V. Mouse Small eye results from mutations in a paired-like homeobox-containing gene. Nature. 1992 Feb 20;355(6362):750–750. doi: 10.1038/355750a0. [DOI] [PubMed] [Google Scholar]
- Hill R. E., Favor J., Hogan B. L., Ton C. C., Saunders G. F., Hanson I. M., Prosser J., Jordan T., Hastie N. D., van Heyningen V. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature. 1991 Dec 19;354(6354):522–525. doi: 10.1038/354522a0. [DOI] [PubMed] [Google Scholar]
- Hoeffler J. P., Meyer T. E., Yun Y., Jameson J. L., Habener J. F. Cyclic AMP-responsive DNA-binding protein: structure based on a cloned placental cDNA. Science. 1988 Dec 9;242(4884):1430–1433. doi: 10.1126/science.2974179. [DOI] [PubMed] [Google Scholar]
- Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10449–10453. doi: 10.1073/pnas.89.21.10449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Howard T., Balogh R., Overbeek P., Bernstein K. E. Sperm-specific expression of angiotensin-converting enzyme (ACE) is mediated by a 91-base-pair promoter containing a CRE-like element. Mol Cell Biol. 1993 Jan;13(1):18–27. doi: 10.1128/mcb.13.1.18. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hurst H. C., Masson N., Jones N. C., Lee K. A. The cellular transcription factor CREB corresponds to activating transcription factor 47 (ATF-47) and forms complexes with a group of polypeptides related to ATF-43. Mol Cell Biol. 1990 Dec;10(12):6192–6203. doi: 10.1128/mcb.10.12.6192. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hurst H. C., Totty N. F., Jones N. C. Identification and functional characterisation of the cellular activating transcription factor 43 (ATF-43) protein. Nucleic Acids Res. 1991 Sep 11;19(17):4601–4609. doi: 10.1093/nar/19.17.4601. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ingolia T. D., Craig E. A. Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2360–2364. doi: 10.1073/pnas.79.7.2360. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kantorow M., Becker K., Sax C. M., Ozato K., Piatigorsky J. Binding of tissue-specific forms of alpha A-CRYBP1 to their regulatory sequence in the mouse alpha A-crystallin-encoding gene: double-label immunoblotting of UV-crosslinked complexes. Gene. 1993 Sep 15;131(2):159–165. doi: 10.1016/0378-1119(93)90289-f. [DOI] [PubMed] [Google Scholar]
- Kantorow M., Cvekl A., Sax C. M., Piatigorsky J. Protein-DNA interactions of the mouse alpha A-crystallin control regions. Differences between expressing and non-expressing cells. J Mol Biol. 1993 Mar 20;230(2):425–435. doi: 10.1006/jmbi.1993.1160. [DOI] [PubMed] [Google Scholar]
- Kantorow M., Piatigorsky J. Alpha-crystallin/small heat shock protein has autokinase activity. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3112–3116. doi: 10.1073/pnas.91.8.3112. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klein-Hitpass L., Tsai S. Y., Weigel N. L., Allan G. F., Riley D., Rodriguez R., Schrader W. T., Tsai M. J., O'Malley B. W. The progesterone receptor stimulates cell-free transcription by enhancing the formation of a stable preinitiation complex. Cell. 1990 Jan 26;60(2):247–257. doi: 10.1016/0092-8674(90)90740-6. [DOI] [PubMed] [Google Scholar]
- Klement J. F., Wawrousek E. F., Piatigorsky J. Tissue-specific expression of the chicken alpha A-crystallin gene in cultured lens epithelia and transgenic mice. J Biol Chem. 1989 Nov 25;264(33):19837–19844. [PubMed] [Google Scholar]
- Klemenz R., Fröhli E., Steiger R. H., Schäfer R., Aoyama A. Alpha B-crystallin is a small heat shock protein. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3652–3656. doi: 10.1073/pnas.88.9.3652. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lin Y. S., Green M. R. Interaction of a common cellular transcription factor, ATF, with regulatory elements in both E1a- and cyclic AMP-inducible promoters. Proc Natl Acad Sci U S A. 1988 May;85(10):3396–3400. doi: 10.1073/pnas.85.10.3396. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Manley J. L., Fire A., Cano A., Sharp P. A., Gefter M. L. DNA-dependent transcription of adenovirus genes in a soluble whole-cell extract. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3855–3859. doi: 10.1073/pnas.77.7.3855. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martha A., Ferrell R. E., Mintz-Hittner H., Lyons L. A., Saunders G. F. Paired box mutations in familial and sporadic aniridia predicts truncated aniridia proteins. Am J Hum Genet. 1994 May;54(5):801–811. [PMC free article] [PubMed] [Google Scholar]
- Meyer T. E., Habener J. F. Cyclic adenosine 3',5'-monophosphate response element binding protein (CREB) and related transcription-activating deoxyribonucleic acid-binding proteins. Endocr Rev. 1993 Jun;14(3):269–290. doi: 10.1210/edrv-14-3-269. [DOI] [PubMed] [Google Scholar]
- Montminy M. R., Gonzalez G. A., Yamamoto K. K. Regulation of cAMP-inducible genes by CREB. Trends Neurosci. 1990 May;13(5):184–188. doi: 10.1016/0166-2236(90)90045-c. [DOI] [PubMed] [Google Scholar]
- Montminy M. R., Sevarino K. A., Wagner J. A., Mandel G., Goodman R. H. Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6682–6686. doi: 10.1073/pnas.83.18.6682. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakamura T., Donovan D. M., Hamada K., Sax C. M., Norman B., Flanagan J. R., Ozato K., Westphal H., Piatigorsky J. Regulation of the mouse alpha A-crystallin gene: isolation of a cDNA encoding a protein that binds to a cis sequence motif shared with the major histocompatibility complex class I gene and other genes. Mol Cell Biol. 1990 Jul;10(7):3700–3708. doi: 10.1128/mcb.10.7.3700. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nerenberg M., Hinrichs S. H., Reynolds R. K., Khoury G., Jay G. The tat gene of human T-lymphotropic virus type 1 induces mesenchymal tumors in transgenic mice. Science. 1987 Sep 11;237(4820):1324–1329. doi: 10.1126/science.2888190. [DOI] [PubMed] [Google Scholar]
- Overbeek P. A., Chepelinsky A. B., Khillan J. S., Piatigorsky J., Westphal H. Lens-specific expression and developmental regulation of the bacterial chloramphenicol acetyltransferase gene driven by the murine alpha A-crystallin promoter in transgenic mice. Proc Natl Acad Sci U S A. 1985 Dec;82(23):7815–7819. doi: 10.1073/pnas.82.23.7815. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Paca-Uccaralertkun S., Zhao L. J., Adya N., Cross J. V., Cullen B. R., Boros I. M., Giam C. Z. In vitro selection of DNA elements highly responsive to the human T-cell lymphotropic virus type I transcriptional activator, Tax. Mol Cell Biol. 1994 Jan;14(1):456–462. doi: 10.1128/mcb.14.1.456. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Piatigorsky J. Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation. 1981;19(3):134–153. doi: 10.1111/j.1432-0436.1981.tb01141.x. [DOI] [PubMed] [Google Scholar]
- Plaza S., Dozier C., Saule S. Quail Pax-6 (Pax-QNR) encodes a transcription factor able to bind and trans-activate its own promoter. Cell Growth Differ. 1993 Dec;4(12):1041–1050. [PubMed] [Google Scholar]
- Quiring R., Walldorf U., Kloter U., Gehring W. J. Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science. 1994 Aug 5;265(5173):785–789. doi: 10.1126/science.7914031. [DOI] [PubMed] [Google Scholar]
- Reddan J. R., Chepelinsky A. B., Dziedzic D. C., Piatigorsky J., Goldenberg E. M. Retention of lens specificity in long-term cultures of diploid rabbit lens epithelial cells. Differentiation. 1986;33(2):168–174. doi: 10.1111/j.1432-0436.1986.tb00422.x. [DOI] [PubMed] [Google Scholar]
- Saha M. S., Servetnick M., Grainger R. M. Vertebrate eye development. Curr Opin Genet Dev. 1992 Aug;2(4):582–588. doi: 10.1016/s0959-437x(05)80176-5. [DOI] [PubMed] [Google Scholar]
- Sax C. M., Ilagan J. G., Piatigorsky J. Functional redundancy of the DE-1 and alpha A-CRYBP1 regulatory sites of the mouse alpha A-crystallin promoter. Nucleic Acids Res. 1993 Jun 11;21(11):2633–2640. doi: 10.1093/nar/21.11.2633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sax C. M., Klement J. F., Piatigorsky J. Species-specific lens activation of the thymidine kinase promoter by a single copy of the mouse alpha A-CRYBP1 site and loss of tissue specificity by multimerization. Mol Cell Biol. 1990 Dec;10(12):6813–6816. doi: 10.1128/mcb.10.12.6813. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sax C. M., Piatigorsky J. Expression of the alpha-crystallin/small heat-shock protein/molecular chaperone genes in the lens and other tissues. Adv Enzymol Relat Areas Mol Biol. 1994;69:155–201. doi: 10.1002/9780470123157.ch5. [DOI] [PubMed] [Google Scholar]
- Shapiro D. J., Sharp P. A., Wahli W. W., Keller M. J. A high-efficiency HeLa cell nuclear transcription extract. DNA. 1988 Jan-Feb;7(1):47–55. doi: 10.1089/dna.1988.7.47. [DOI] [PubMed] [Google Scholar]
- Ton C. C., Hirvonen H., Miwa H., Weil M. M., Monaghan P., Jordan T., van Heyningen V., Hastie N. D., Meijers-Heijboer H., Drechsler M. Positional cloning and characterization of a paired box- and homeobox-containing gene from the aniridia region. Cell. 1991 Dec 20;67(6):1059–1074. doi: 10.1016/0092-8674(91)90284-6. [DOI] [PubMed] [Google Scholar]
- Treisman J., Harris E., Desplan C. The paired box encodes a second DNA-binding domain in the paired homeo domain protein. Genes Dev. 1991 Apr;5(4):594–604. doi: 10.1101/gad.5.4.594. [DOI] [PubMed] [Google Scholar]
- Tyndall C., La Mantia G., Thacker C. M., Favaloro J., Kamen R. A region of the polyoma virus genome between the replication origin and late protein coding sequences is required in cis for both early gene expression and viral DNA replication. Nucleic Acids Res. 1981 Dec 11;9(23):6231–6250. doi: 10.1093/nar/9.23.6231. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vallejo M., Miller C. P., Habener J. F. Somatostatin gene transcription regulated by a bipartite pancreatic islet D-cell-specific enhancer coupled synergetically to a cAMP response element. J Biol Chem. 1992 Jun 25;267(18):12868–12875. [PubMed] [Google Scholar]
- Wagner S., Green M. R. HTLV-I Tax protein stimulation of DNA binding of bZIP proteins by enhancing dimerization. Science. 1993 Oct 15;262(5132):395–399. doi: 10.1126/science.8211160. [DOI] [PubMed] [Google Scholar]
- Walther C., Gruss P. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development. 1991 Dec;113(4):1435–1449. doi: 10.1242/dev.113.4.1435. [DOI] [PubMed] [Google Scholar]
- Wawrousek E. F., Chepelinsky A. B., McDermott J. B., Piatigorsky J. Regulation of the murine alpha A-crystallin promoter in transgenic mice. Dev Biol. 1990 Jan;137(1):68–76. doi: 10.1016/0012-1606(90)90008-7. [DOI] [PubMed] [Google Scholar]
- Williams J. S., Dixon J. E., Andrisani O. M. Binding constant determination studies utilizing recombinant delta CREB protein. DNA Cell Biol. 1993 Mar;12(2):183–190. doi: 10.1089/dna.1993.12.183. [DOI] [PubMed] [Google Scholar]
- Wilson D., Sheng G., Lecuit T., Dostatni N., Desplan C. Cooperative dimerization of paired class homeo domains on DNA. Genes Dev. 1993 Nov;7(11):2120–2134. doi: 10.1101/gad.7.11.2120. [DOI] [PubMed] [Google Scholar]
- Wistow G. J., Piatigorsky J. Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem. 1988;57:479–504. doi: 10.1146/annurev.bi.57.070188.002403. [DOI] [PubMed] [Google Scholar]
- Yamada T., Nakamura T., Westphal H., Russell P. Synthesis of alpha-crystallin by a cell line derived from the lens of a transgenic animal. Curr Eye Res. 1990 Jan;9(1):31–37. doi: 10.3109/02713689009000052. [DOI] [PubMed] [Google Scholar]
- Yu C. C., Tsui L. C., Breitman M. L. Homologous and heterologous enhancers modulate spatial expression but not cell-type specificity of the murine gamma F-crystallin promoter. Development. 1990 Sep;110(1):131–139. doi: 10.1242/dev.110.1.131. [DOI] [PubMed] [Google Scholar]
- Zannini M., Francis-Lang H., Plachov D., Di Lauro R. Pax-8, a paired domain-containing protein, binds to a sequence overlapping the recognition site of a homeodomain and activates transcription from two thyroid-specific promoters. Mol Cell Biol. 1992 Sep;12(9):4230–4241. doi: 10.1128/mcb.12.9.4230. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zwaan J., Ikeda A. Macromolecular events during differentiation of the chicken lens. Exp Eye Res. 1968 Apr;7(2):301–311. doi: 10.1016/s0014-4835(68)80081-8. [DOI] [PubMed] [Google Scholar]
- de Groot R. P., Sassone-Corsi P. Hormonal control of gene expression: multiplicity and versatility of cyclic adenosine 3',5'-monophosphate-responsive nuclear regulators. Mol Endocrinol. 1993 Feb;7(2):145–153. doi: 10.1210/mend.7.2.8385737. [DOI] [PubMed] [Google Scholar]
- de Jong W. W., Leunissen J. A., Voorter C. E. Evolution of the alpha-crystallin/small heat-shock protein family. Mol Biol Evol. 1993 Jan;10(1):103–126. doi: 10.1093/oxfordjournals.molbev.a039992. [DOI] [PubMed] [Google Scholar]