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. 1988 May;85(10):3479–3483. doi: 10.1073/pnas.85.10.3479

Gene sharing by delta-crystallin and argininosuccinate lyase.

J Piatigorsky 1, W E O'Brien 1, B L Norman 1, K Kalumuck 1, G J Wistow 1, T Borras 1, J M Nickerson 1, E F Wawrousek 1
PMCID: PMC280235  PMID: 3368457

Abstract

The lens structural protein delta-crystallin and the metabolic enzyme argininosuccinate lyase (ASL; L-argininosuccinate arginine-lyase, EC 4.3.2.1) have striking sequence similarity. We have demonstrated that duck delta-crystallin has enormously high ASL activity, while chicken delta-crystallin has lower but significant activity. The lenses of these birds had much greater ASL activity than other tissues, suggesting that ASL is being expressed at unusually high levels as a structural component. In Southern blots of human genomic DNA, chicken delta 1-crystallin cDNA hybridized only to the human ASL gene; moreover, the two chicken delta-crystallin genes accounted for all the sequences in the chicken genome able to cross-hybridize with a human ASL cDNA, with preferential hybridization to the delta 2 gene. Correlations of enzymatic activity and recent data on mRNA levels in the chicken lens suggest that ASL activity depends on expression of the delta 2-crystallin gene. The data indicate that the same gene, at least in ducks, encodes two different functions, an enzyme (ASL) and a structural protein (delta-crystallin), although in chickens specialization and separation of functions may have occurred.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Agata K., Yasuda K., Okada T. S. Gene coding for a lens-specific protein, delta-crystallin, is transcribed in nonlens tissues of chicken embryos. Dev Biol. 1983 Nov;100(1):222–226. doi: 10.1016/0012-1606(83)90214-2. [DOI] [PubMed] [Google Scholar]
  2. Beacham I. R., Schweitzer B. W., Warrick H. M., Carbon J. The nucleotide sequence of the yeast ARG4 gene. Gene. 1984 Sep;29(3):271–279. doi: 10.1016/0378-1119(84)90056-8. [DOI] [PubMed] [Google Scholar]
  3. Bloemendal H. Lens proteins. CRC Crit Rev Biochem. 1982;12(1):1–38. doi: 10.3109/10409238209105849. [DOI] [PubMed] [Google Scholar]
  4. Blundell T., Lindley P., Miller L., Moss D., Slingsby C., Tickle I., Turnell B., Wistow G. The molecular structure and stability of the eye lens: x-ray analysis of gamma-crystallin II. Nature. 1981 Feb 26;289(5800):771–777. doi: 10.1038/289771a0. [DOI] [PubMed] [Google Scholar]
  5. Bower D. J., Errington L. H., Cooper D. N., Morris S., Clayton R. M. Chicken lens delta-crystallin gene expression and methylation in several non-lens tissues. Nucleic Acids Res. 1983 May 11;11(9):2513–2527. doi: 10.1093/nar/11.9.2513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carper D., Nishimura C., Shinohara T., Dietzchold B., Wistow G., Craft C., Kador P., Kinoshita J. H. Aldose reductase and p-crystallin belong to the same protein superfamily as aldehyde reductase. FEBS Lett. 1987 Aug 10;220(1):209–213. doi: 10.1016/0014-5793(87)80905-5. [DOI] [PubMed] [Google Scholar]
  7. Clayton R. M., Jeanny J. C., Bower D. J., Errington L. H. The presence of extralenticular crystallins and its relationship with transdifferentiation to lens. Curr Top Dev Biol. 1986;20:137–151. doi: 10.1016/s0070-2153(08)60660-2. [DOI] [PubMed] [Google Scholar]
  8. Delaye M., Tardieu A. Short-range order of crystallin proteins accounts for eye lens transparency. 1983 Mar 31-Apr 6Nature. 302(5907):415–417. doi: 10.1038/302415a0. [DOI] [PubMed] [Google Scholar]
  9. DiLella A. G., Kwok S. C., Ledley F. D., Marvit J., Woo S. L. Molecular structure and polymorphic map of the human phenylalanine hydroxylase gene. Biochemistry. 1986 Feb 25;25(4):743–749. doi: 10.1021/bi00352a001. [DOI] [PubMed] [Google Scholar]
  10. Driessen H. P., Herbrink P., Bloemendal H., de Jong W. W. Primary structure of the bovine beta-crystallin Bp chain. Internal duplication and homology with gamma-crystallin. Eur J Biochem. 1981 Dec;121(1):83–91. doi: 10.1111/j.1432-1033.1981.tb06433.x. [DOI] [PubMed] [Google Scholar]
  11. Hawkins J. W., Nickerson J. M., Sullivan M. A., Piatigorsky J. The chicken delta-crystallin gene family. Two genes of similar structure in close chromosomal approximation. J Biol Chem. 1984 Aug 10;259(15):9821–9825. [PubMed] [Google Scholar]
  12. Hendriks W., Leunissen J., Nevo E., Bloemendal H., de Jong W. W. The lens protein alpha A-crystallin of the blind mole rat, Spalax ehrenbergi: evolutionary change and functional constraints. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5320–5324. doi: 10.1073/pnas.84.15.5320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Inana G., Shinohara T., Maizel J. V., Jr, Piatigorsky J. Evolution and diversity of the crystallins. Nucleotide sequence of a beta-crystallin mRNA from the mouse lens. J Biol Chem. 1982 Aug 10;257(15):9064–9071. [PubMed] [Google Scholar]
  14. 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]
  15. Jackson M. J., Beaudet A. L., O'Brien W. E. Mammalian urea cycle enzymes. Annu Rev Genet. 1986;20:431–464. doi: 10.1146/annurev.ge.20.120186.002243. [DOI] [PubMed] [Google Scholar]
  16. Jakoby W. B. The enzymes of detoxication. Trans N Y Acad Sci. 1983;41:71–75. doi: 10.1111/j.2164-0947.1983.tb02786.x. [DOI] [PubMed] [Google Scholar]
  17. Jeanny J. C., Bower D. J., Errington L. H., Morris S., Clayton R. M. Cellular heterogeneity in the expression of the delta-crystallin gene in non-lens tissue. Dev Biol. 1985 Nov;112(1):94–99. doi: 10.1016/0012-1606(85)90123-x. [DOI] [PubMed] [Google Scholar]
  18. Linser P. J., Irvin C. K. Immunohistochemical characterization of delta crystallin-containing retina/optic nerve "boundary" cells in the chick embryo. Dev Biol. 1987 Jun;121(2):499–509. doi: 10.1016/0012-1606(87)90186-2. [DOI] [PubMed] [Google Scholar]
  19. Lusty C. J., Ratner S. Reaction of argininosuccinase with bromomesaconic acid: role of an essential lysine in the active site. Proc Natl Acad Sci U S A. 1987 May;84(10):3176–3180. doi: 10.1073/pnas.84.10.3176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mangia F., Erickson R. P., Epstein C. J. Synthesis of LDH-1 during mamalian oogenesis and early development. Dev Biol. 1976 Nov;54(1):146–150. doi: 10.1016/0012-1606(76)90293-1. [DOI] [PubMed] [Google Scholar]
  21. Miyada C. G., Klofelt C., Reyes A. A., McLaughlin-Taylor E., Wallace R. B. Evidence that polymorphism in the murine major histocompatibility complex may be generated by the assortment of subgene sequences. Proc Natl Acad Sci U S A. 1985 May;82(9):2890–2894. doi: 10.1073/pnas.82.9.2890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Naylor S. L., Klebe R. J., Shows T. B. Argininosuccinic aciduria: assignment of the argininosuccinate lyase gene to the pter to q22 region of human chromosome 7 by bioautography. Proc Natl Acad Sci U S A. 1978 Dec;75(12):6159–6162. doi: 10.1073/pnas.75.12.6159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nene V., Dunne D. W., Johnson K. S., Taylor D. W., Cordingley J. S. Sequence and expression of a major egg antigen from Schistosoma mansoni. Homologies to heat shock proteins and alpha-crystallins. Mol Biochem Parasitol. 1986 Nov;21(2):179–188. doi: 10.1016/0166-6851(86)90021-6. [DOI] [PubMed] [Google Scholar]
  24. Nickerson J. M., Piatigorsky J. Sequence of a complete chicken delta-crystallin cDNA. Proc Natl Acad Sci U S A. 1984 May;81(9):2611–2615. doi: 10.1073/pnas.81.9.2611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nickerson J. M., Wawrousek E. F., Borras T., Hawkins J. W., Norman B. L., Filpula D. R., Nagle J. W., Ally A. H., Piatigorsky J. Sequence of the chicken delta 2 crystallin gene and its intergenic spacer. Extreme homology with the delta 1 crystallin gene. J Biol Chem. 1986 Jan 15;261(2):552–557. [PubMed] [Google Scholar]
  26. Nickerson J. M., Wawrousek E. F., Hawkins J. W., Wakil A. S., Wistow G. J., Thomas G., Norman B. L., Piatigorsky J. The complete sequence of the chicken delta 1 crystallin gene and its 5' flanking region. J Biol Chem. 1985 Aug 5;260(16):9100–9105. [PubMed] [Google Scholar]
  27. O'Brien W. E., Barr R. H. Argininosuccinate lyase: purification and characterization from human liver. Biochemistry. 1981 Mar 31;20(7):2056–2060. doi: 10.1021/bi00510a049. [DOI] [PubMed] [Google Scholar]
  28. O'Brien W. E., McInnes R., Kalumuck K., Adcock M. Cloning and sequence analysis of cDNA for human argininosuccinate lyase. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7211–7215. doi: 10.1073/pnas.83.19.7211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ohno M., Sakamoto H., Yasuda K., Okada T. S., Shimura Y. Nucleotide sequence of a chicken delta-crystallin gene. Nucleic Acids Res. 1985 Mar 11;13(5):1593–1606. doi: 10.1093/nar/13.5.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ottaway J. H., Mowbray J. The role of compartmentation in the control of glycolysis. Curr Top Cell Regul. 1977;12:107–208. doi: 10.1016/b978-0-12-152812-6.50010-x. [DOI] [PubMed] [Google Scholar]
  31. Piatigorsky J. Delta crystallins and their nucleic acids. Mol Cell Biochem. 1984;59(1-2):33–56. doi: 10.1007/BF00231304. [DOI] [PubMed] [Google Scholar]
  32. Piatigorsky J., Norman B., Jones R. E. Conservation of delta-crystallin gene structure between ducks and chickens. J Mol Evol. 1987;25(4):308–317. doi: 10.1007/BF02603115. [DOI] [PubMed] [Google Scholar]
  33. Piatigorsky J., Zelenka P., Simpson R. T. Molecular weight and subunit structure of delta-crystallin from embryonic chick lens fibers. Exp Eye Res. 1974 May;18(5):435–446. doi: 10.1016/0014-4835(74)90080-3. [DOI] [PubMed] [Google Scholar]
  34. Ratner S. Enzymes of arginine and urea synthesis. Adv Enzymol Relat Areas Mol Biol. 1973;39:1–90. doi: 10.1002/9780470122846.ch1. [DOI] [PubMed] [Google Scholar]
  35. Ueda Y., Okada T. S. Transient expression of a 'lens-specific' gene, delta-crystallin, in the embryonic chicken adenohypophysis. Cell Differ. 1986 Oct;19(3):179–185. doi: 10.1016/0045-6039(86)90094-1. [DOI] [PubMed] [Google Scholar]
  36. Watanabe K., Fujii Y., Nakayama K., Ohkubo H., Kuramitsu S., Kagamiyama H., Nakanishi S., Hayaishi O. Structural similarity of bovine lung prostaglandin F synthase to lens epsilon-crystallin of the European common frog. Proc Natl Acad Sci U S A. 1988 Jan;85(1):11–15. doi: 10.1073/pnas.85.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wawrousek E. F., Nickerson J. M., Piatigorsky J. Two delta-crystallin polypeptides are derived from a cloned delta 1-crystallin cDNA. FEBS Lett. 1986 Sep 15;205(2):235–240. doi: 10.1016/0014-5793(86)80904-8. [DOI] [PubMed] [Google Scholar]
  38. Wistow G. J., Mulders J. W., de Jong W. W. The enzyme lactate dehydrogenase as a structural protein in avian and crocodilian lenses. Nature. 1987 Apr 9;326(6113):622–624. doi: 10.1038/326622a0. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. Wistow G. Domain structure and evolution in alpha-crystallins and small heat-shock proteins. FEBS Lett. 1985 Feb 11;181(1):1–6. doi: 10.1016/0014-5793(85)81102-9. [DOI] [PubMed] [Google Scholar]
  41. Wistow G., Piatigorsky J. Recruitment of enzymes as lens structural proteins. Science. 1987 Jun 19;236(4808):1554–1556. doi: 10.1126/science.3589669. [DOI] [PubMed] [Google Scholar]
  42. Wistow G., Summers L., Blundell T. Myxococcus xanthus spore coat protein S may have a similar structure to vertebrate lens beta gamma-crystallins. 1985 Jun 27-Jul 3Nature. 315(6022):771–773. doi: 10.1038/315771a0. [DOI] [PubMed] [Google Scholar]
  43. Yasuda K., Kondoh H., Okada T. S., Nakajima N., Shimura Y. Organization of delta-crystallin genes in the chicken. Nucleic Acids Res. 1982 May 11;10(9):2879–2891. doi: 10.1093/nar/10.9.2879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yasuda K., Nakajima N., Isobe T., Okada T. S., Shimura Y. The nucleotide sequence of a complete chicken delta-crystallin cDNA. EMBO J. 1984 Jun;3(6):1397–1402. doi: 10.1002/j.1460-2075.1984.tb01983.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zoller M. J., Smith M. Oligonucleotide-directed mutagenesis: a simple method using two oligonucleotide primers and a single-stranded DNA template. DNA. 1984 Dec;3(6):479–488. doi: 10.1089/dna.1.1984.3.479. [DOI] [PubMed] [Google Scholar]

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