Summary
Approximately 2 kb of 5′-flanking sequences of the lens-specific αA-crystallin genes from human and mouse are presented and compared with similar regions of the chicken gene. A repetitive element was found approximately 1 kb upstream from the coding sequences of the αA-crystallin gene in all three species (Alu in human, B2 in mouse, and CR1 in chicken), suggesting that they may have an important functional or structural role.
Despite the ability of αA-crystallin promoters to function across species, dot matrix analyses show only limited similarity among the 600 bp 5′ to the structural genes of these three species. The human 5′-flanking sequence is more similar to that of the mouse and chicken than the mouse and chicken are to each other. Numerous short sequences (8–13 bp) are common to all three genes but are distributed differently in each species. The locations and conservation of these sequence motifs suggest functional roles, possibly ascis-regulatory elements of transcription. One motif is similar to the αA-CRYBP1 binding site implicated earlier in the transcriptional regulation of the mouse αA-crystallin gene, and other motifs correspond to sites previously mapped by methylation interference studies in the mouse αA-crystallin promoter. The modular arrangement of conserved sequence motifs is consistent with evolutionary changes occurring at the level of gene regulation.
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Bains W, Temple-Smith K (1989) Similarity and divergence among rodent repetitive DNA sequences. J Mol Evol 18:191–199
Baniahmad A, Muller M, Steiner C, Renkawitz R (1987) Activity of two different silencer elements of the chicken lysozyme gene can be compensated by enhancer elements. EMBO J 6:2297–2303
Britten RJ, Baron WF, Stout DB, Davidson EH (1988) Sources and evolution of human Alu repeated sequences. Proc Natl Acad Sci USA 85:4770–4774
Carr CS, Sharp PA (1990) A helix-loop-helix protein related to the immunoglobulin E box-binding proteins. Mol Cell Biol 10:4384–4388
Chepelinsky AB, King CR, Zelenka PS, Piatigorsky J (1985) Lens-specific expression of the chloramphenicol acetyltransferase gene promoted by 5′ flanking sequences of the murine alpha A-crystallin in explanted chicken lens epithelia. Proc Natl Acad Sci USA 82:2334–2338
Chepelinsky AB, Sommer B, Piatigorsky J (1987) Interaction between two different regulatory elements activates the murine αA-crystallin gene promoter in explanted lens epithelia. Mol Cell Biol 7:1807–1814
Chepelinsky AB, Sommer B, Wawrousek EF, Piatigorsky J (1988) Activation of the murine alpha A-crystallin gene promoter in the lens. In: Piatigorsky J, Zelenka PS, Shinohara T (eds) Molecular biology of the eye: genes, vision, and ocular disease. Alan R. Liss, New York, pp 215–227
den Dunnen JT, Schoenmakers JG (1987) Consensus sequences of theRattus norvegicus B1- and B2 repeats. Nucleic Acids Res 15:2772
Hache RJG, Deeley RG (1988) Organization, sequence and nuclease hypersensitivity of repetitive elements flanking the chicken apo VLDLII gene: extended sequence similarity to elements flanking the chicken vitellogenin gene. Nucleic Acids Res 16:97–113
Hendriks W, Leunissen J, Nevo E, Bloemendal H, de Jong WW (1987) The lens protein alphaA-crystallin of the blind mole rat,Spalax ehrenbergi: evolutionary change and functional constraints. Proc Natl Acad Sci USA 84:5320–5324
Jurka J, Milosavljevic A (1991) Reconstruction and analysis of human Alu genes. J Mol Evol 32:105–121
King CR, Piatigorsky J (1983) Alternative RNA splicing of the murine alpha A-crystallin gene: protein-coding information within an intron. Cell 32:707–712
Kleinsek DA, Beattie WG, Tsai M-J, O'Malley BW (1986) Molecular cloning of a steroid regulated 108K heat shock protein gene from hen oviduct. Nucleic Acids Res 14:10053–10069
Klement JF, Wawrousek EF, Piatigorsky J (1989) Tissue-specific expression of the chicken alpha A-crystallin gene in cultured lens epithelia and transgenic mice. J Biol Chem 264:19837–19844
Koop BF, Goodman M (1988) Evolutionary and developmental aspects of two hemoglobin beta-chain genes (epsilon M and beta M) of opossum. Proc Natl Acad Sci USA 85:3893–3897
Korenberg JR, Rykowski MC (1988) Human genome organization: Alu, Lines and the molecular structure of metaphase chromosome bands. Cell 53:391–400
Lee JS, Latimer LJP, Haug BL, Pulleyblank DE, Skinner DM, Burkholder GD (1989) Triplex DNA in plasmids and chromosomes. Gene 82:191–199
Lenardo MJ, Baltimore D (1989) NF-B: a pleiotropic mediator of inducible and tissue-specific gene control. Cell 58:227–229
Lewin B (1990) Commitment and activation at Pol II promoters: a tai of protein-protein interactions. Cell 61:1161–1164
Lubsen NH, Aarts HJM, Schoenmakers JGG (1988) The evolution of lenticular proteins: the beta- and gamma-crystallin super gene family. Prog Biophys Mol Biol 51:47–76
Lyamichev VI, Mirkin SM, Frank-Kamenetskii MD, Cantor C (1988) A stable complex between homopyrimidine oligomers and the homologous regions of duplex DNAs. Nucleic Acids Res 16:2165–2178
Martinez-Cruzado JC, Swimmer C, Fenerjian MG, Kafatos FC (1988) Evolution of the autosomal chorion locus inDrosophila. General organization of the locus and sequence comparisons of genes s15 and s19 in evolutionarily distant species. Genetics 119:663–677
Murre C, McCaw PS, Baltimore D (1989) A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56:777–783
Nakamura T, Donovan DM, Hamada K, Sax CM, Norman B, Flanagan JR, Ozato K, Westphal H, Piatigorsky J (1990) Regulation of the mouse αA-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 10:3700–3708
Nathans J, Thomas D, Hogness DS (1986) Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science 232:193–202
Oliviero S, Monaci P (1988) RNA polymerase III promoter elements enhance transcription of RNA polymerase II genes. Nucleic Acids Res 16:1285–1293
Perez-Stable C, Shen Che-KJ (1986)Competitive and cooperative functioning of the anterior and posterior promoter elements of an Alu family repeat. Mol Cell Biol 6:2041–2052
Piatigorsky J, Zelenka PS (in press) Transcriptional regulation of crystallin genes: cis elements, trans-factors and signal transduction systems in the lens. In: Advances in Developmental Biochemistry, vol 1
Podgornaya OI, Perelygina LM, Tomilin NV (1988) Multi-site binding of human nuclear protein to the Alu-family repeated DNA. FEBS Lett 232:99–102
Quentin Y (1988) The Alu family developed through successive waves of fixation closely connected with primate lineage history. J Mol Evol 27:194–202
Saffer JD, Thurston SJ (1989) A negative regulatory element with properties similar to those of enhancers is contained within an Alu sequence. Mol Cell Biol 9:355–364
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467
Sax CM, Klement JF, Piatigorsky J (1990) 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 10:6813–6816
Silva R, Burch JBE (1989) Evidence that chicken CR1 elements represent a novel family of retroposons. Mol Cell Biol 9:3563–3566
Sommer B, Chepelinsky AB, Piatigorsky J (1988) Binding of nuclear proteins to promoter elements of the mouse alpha A-crystallin gene. J Biol Chem 263:15666–15672
Staden R (1977) Sequence data handling by computer. Nucleic Acids Res 4:4037–4051
Stumph WE, Baez M, Beattie WG, Tsai Ming-J, O'Malley BW (1983) Characterization of deoxyribonucleic acid sequences at the 5′ and 3′ borders of the 100 kilobase pair ovalbumin gene domain. Biochemistry 22:306–315
Stumph WE, Hodgson CP, Tsai Ming-J, O'Malley BW (1984) Genomic structure and possible retroviral origin of the chicken CR1 repetitive DNA sequence family. Proc Natl Acad Sci USA 81:6667–6671
Tagle DA, Koop BF, Goodman M, Slightom JL, Hess DL, Jones RT (1988) Embryonic epsilon and gamma globin genes of a prosimian primate (Falago crassicaudatus). J Mol Biol 203: 439–455
Thompson MA, Hawkins JW, Piatigorsky J (1987) Complete nucleotide sequence of the chicken alphaA-crystallin gene and its 5′ flanking region. Gene 56:173–184
Tomilin NV, Bozhkov VM (1989) Human nuclear protein interacting with a conservative sequence motif of Alu-family DNA repeats. FEBS Lett 251:79–83
Topol J, Ruden DM, Parker CS (1985) Sequences required for in vitro transcriptional activation of aDrosophila hsp 70 gene. Cell 42:527–537
van den Heuvel R, Hendriks W, Quax W, Bloemendal H (1985) Complete structure of the hamster alpha A-crystallin gene. Reflection of an evolutionary history by means of exon shuffling. J Mol Biol 185:273–284
Wawrousek EF, Chepelinsky AB, McDermott JB, Piatigorsky J (1990) Regulation of the murine αA-crystallin promoter in transgenic mice. Dev Biol 137:68–76
Wells RD, Collier DA, Hanvey JC, Shimizu M, Wohlrab F (1988) The chemistry and biology of unusual DNA structures adopted by oligopurine/oligopyrimidine sequences. FASEB J 2:2939–2949
Wilbur WJ, Lipman DJ (1983) Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci USA 80:726–730
Wistow G, Piatigorsky J (1988) The lens crystallins: evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57:479–504
Yu CC-K, Tsui L-C, Breitman ML (1990) Homologous and heterologous enhancers modulate spatial expression but not cell-type specificity of the murine gamma F-crystallin promoter. Development 110:131–139
Zucker-Aprison E, Blumenthal T (1989) Potential regulatory elements of nematode vitellogenin genes revealed by interspecies sequence comparisons. J Mol Evol 28:487–496
Zwaan J (1983) The appearance of alpha-crystallin in relation to cell cycle phase embryonic mouse lens. Dev Biol 96:173–181
Zwaan J, Ikeda A (1968) Macromolecular events during differentiation of the chicken lens. Exp Eye Res 7:301–311
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Jaworski, C.J., Chepelinsky, A.B. & Piatigorsky, J. The αA-crystallin gene: Conserved features of the 5′-flanking regions in human, mouse, and chicken. J Mol Evol 33, 495–505 (1991). https://doi.org/10.1007/BF02102802
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DOI: https://doi.org/10.1007/BF02102802