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. 1990 Jan;87(1):293–297. doi: 10.1073/pnas.87.1.293

Bovine cone photoreceptor cGMP phosphodiesterase structure deduced from a cDNA clone.

T S Li 1, K Volpp 1, M L Applebury 1
PMCID: PMC53249  PMID: 2153291

Abstract

A full-length cDNA clone encoding the alpha' subunit of cGMP phosphodiesterase (PDE) from bovine cone photoreceptors was selected by probing a retinal library with a DNA fragment encoding the catalytic core of the rod cGMP PDE alpha subunit. Identity of the clone was confirmed by comparing its deduced sequence with cone PDE peptide sequences determined by Charbonneau et al. [Charbonneau, H., Prusti, R. K., LeTrong, H., Sonnenburg, W. K., Mullaney, P. J., Walsh, K. A. & Beavo, J. A. (1990) Proc. Natl. Acad. Sci. USA, pp. 288-292]. The cone PDE alpha' and the rod PDE alpha and beta subunits are encoded by distinct genes. cGMP PDE subunits share a common ancestry with cAMP PDEs and cyclic nucleotide-binding proteins. Sequence comparisons predict the presence of a catalytic core and possible secondary sites for noncatalytic cGMP binding. The presence of a C-terminal CAAX (Cys-aliphatic-aliphatic-Xaa) motif suggests the cone enzyme may be posttranslationally modified by proteolysis, methylation, and isoprenylation.

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Selected References

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

  1. Aiba H., Fujimoto S., Ozaki N. Molecular cloning and nucleotide sequencing of the gene for E. coli cAMP receptor protein. Nucleic Acids Res. 1982 Feb 25;10(4):1345–1361. doi: 10.1093/nar/10.4.1345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baehr W., Devlin M. J., Applebury M. L. Isolation and characterization of cGMP phosphodiesterase from bovine rod outer segments. J Biol Chem. 1979 Nov 25;254(22):11669–11677. [PubMed] [Google Scholar]
  4. Birnstiel M. L., Busslinger M., Strub K. Transcription termination and 3' processing: the end is in site! Cell. 1985 Jun;41(2):349–359. doi: 10.1016/s0092-8674(85)80007-6. [DOI] [PubMed] [Google Scholar]
  5. Charbonneau H., Beier N., Walsh K. A., Beavo J. A. Identification of a conserved domain among cyclic nucleotide phosphodiesterases from diverse species. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9308–9312. doi: 10.1073/pnas.83.24.9308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Charbonneau H., Prusti R. K., LeTrong H., Sonnenburg W. K., Mullaney P. J., Walsh K. A., Beavo J. A. Identification of a noncatalytic cGMP-binding domain conserved in both the cGMP-stimulated and photoreceptor cyclic nucleotide phosphodiesterases. Proc Natl Acad Sci U S A. 1990 Jan;87(1):288–292. doi: 10.1073/pnas.87.1.288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cheung W. Y. Properties of cyclic 3',5'-nucleotide phosphodiesterase from rat brain. Biochemistry. 1967 Apr;6(4):1079–1087. doi: 10.1021/bi00856a017. [DOI] [PubMed] [Google Scholar]
  8. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  9. Clarke S., Vogel J. P., Deschenes R. J., Stock J. Posttranslational modification of the Ha-ras oncogene protein: evidence for a third class of protein carboxyl methyltransferases. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4643–4647. doi: 10.1073/pnas.85.13.4643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Colicelli J., Birchmeier C., Michaeli T., O'Neill K., Riggs M., Wigler M. Isolation and characterization of a mammalian gene encoding a high-affinity cAMP phosphodiesterase. Proc Natl Acad Sci U S A. 1989 May;86(10):3599–3603. doi: 10.1073/pnas.86.10.3599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cossart P., Gicquel-Sanzey B. Cloning and sequence of the crp gene of Escherichia coli K 12. Nucleic Acids Res. 1982 Feb 25;10(4):1363–1378. doi: 10.1093/nar/10.4.1363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Davis R. L., Takayasu H., Eberwine M., Myres J. Cloning and characterization of mammalian homologs of the Drosophila dunce+ gene. Proc Natl Acad Sci U S A. 1989 May;86(10):3604–3608. doi: 10.1073/pnas.86.10.3604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Deterre P., Bigay J., Forquet F., Robert M., Chabre M. cGMP phosphodiesterase of retinal rods is regulated by two inhibitory subunits. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2424–2428. doi: 10.1073/pnas.85.8.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
  15. Gillespie P. G., Beavo J. A. Characterization of a bovine cone photoreceptor phosphodiesterase purified by cyclic GMP-sepharose chromatography. J Biol Chem. 1988 Jun 15;263(17):8133–8141. [PubMed] [Google Scholar]
  16. Gillespie P. G., Beavo J. A. cGMP is tightly bound to bovine retinal rod phosphodiesterase. Proc Natl Acad Sci U S A. 1989 Jun;86(11):4311–4315. doi: 10.1073/pnas.86.11.4311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hancock J. F., Magee A. I., Childs J. E., Marshall C. J. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell. 1989 Jun 30;57(7):1167–1177. doi: 10.1016/0092-8674(89)90054-8. [DOI] [PubMed] [Google Scholar]
  18. Holbrook S. R., Kim S. H. Molecular model of the G protein alpha subunit based on the crystal structure of the HRAS protein. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1751–1755. doi: 10.1073/pnas.86.6.1751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hurwitz R. L., Bunt-Milam A. H., Chang M. L., Beavo J. A. cGMP phosphodiesterase in rod and cone outer segments of the retina. J Biol Chem. 1985 Jan 10;260(1):568–573. [PubMed] [Google Scholar]
  20. Jones K. A., Yamamoto K. R., Tjian R. Two distinct transcription factors bind to the HSV thymidine kinase promoter in vitro. Cell. 1985 Sep;42(2):559–572. doi: 10.1016/0092-8674(85)90113-8. [DOI] [PubMed] [Google Scholar]
  21. Jurnak F. The three-dimensional structure of c-H-ras p21: implications for oncogene and G protein studies. Trends Biochem Sci. 1988 Jun;13(6):195–198. doi: 10.1016/0968-0004(88)90080-1. [DOI] [PubMed] [Google Scholar]
  22. Kimmel A. R., Berger S. L. Preparation of cDNA and the generation of cDNA libraries: overview. Methods Enzymol. 1987;152:307–316. doi: 10.1016/0076-6879(87)52035-3. [DOI] [PubMed] [Google Scholar]
  23. Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 1986 Jan 31;44(2):283–292. doi: 10.1016/0092-8674(86)90762-2. [DOI] [PubMed] [Google Scholar]
  24. Kroll S., Phillips W. J., Cerione R. A. The regulation of the cyclic GMP phosphodiesterase by the GDP-bound form of the alpha subunit of transducin. J Biol Chem. 1989 Mar 15;264(8):4490–4497. [PubMed] [Google Scholar]
  25. Lerea C. L., Somers D. E., Hurley J. B., Klock I. B., Bunt-Milam A. H. Identification of specific transducin alpha subunits in retinal rod and cone photoreceptors. Science. 1986 Oct 3;234(4772):77–80. doi: 10.1126/science.3529395. [DOI] [PubMed] [Google Scholar]
  26. Magee T., Hanley M. Protein modification. Sticky fingers and CAAX boxes. Nature. 1988 Sep 8;335(6186):114–115. doi: 10.1038/335114a0. [DOI] [PubMed] [Google Scholar]
  27. Martin R. L., Wood C., Baehr W., Applebury M. L. Visual pigment homologies revealed by DNA hybridization. Science. 1986 Jun 6;232(4755):1266–1269. doi: 10.1126/science.3010467. [DOI] [PubMed] [Google Scholar]
  28. McKay D. B., Steitz T. A. Structure of catabolite gene activator protein at 2.9 A resolution suggests binding to left-handed B-DNA. Nature. 1981 Apr 30;290(5809):744–749. doi: 10.1038/290744a0. [DOI] [PubMed] [Google Scholar]
  29. McKay D. B., Weber I. T., Steitz T. A. Structure of catabolite gene activator protein at 2.9-A resolution. Incorporation of amino acid sequence and interactions with cyclic AMP. J Biol Chem. 1982 Aug 25;257(16):9518–9524. [PubMed] [Google Scholar]
  30. McKnight S. L., Kingsbury R. Transcriptional control signals of a eukaryotic protein-coding gene. Science. 1982 Jul 23;217(4557):316–324. doi: 10.1126/science.6283634. [DOI] [PubMed] [Google Scholar]
  31. Nathans J., Hogness D. S. Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell. 1983 Oct;34(3):807–814. doi: 10.1016/0092-8674(83)90537-8. [DOI] [PubMed] [Google Scholar]
  32. Nathans J., Thomas D., Hogness D. S. Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science. 1986 Apr 11;232(4747):193–202. doi: 10.1126/science.2937147. [DOI] [PubMed] [Google Scholar]
  33. Ovchinnikov YuA, Gubanov V. V., Khramtsov N. V., Ischenko K. A., Zagranichny V. E., Muradov K. G., Shuvaeva T. M., Lipkin V. M. Cyclic GMP phosphodiesterase from bovine retina. Amino acid sequence of the alpha-subunit and nucleotide sequence of the corresponding cDNA. FEBS Lett. 1987 Oct 19;223(1):169–173. doi: 10.1016/0014-5793(87)80530-6. [DOI] [PubMed] [Google Scholar]
  34. Pugh E. N., Jr, Cobbs W. H. Visual transduction in vertebrate rods and cones: a tale of two transmitters, calcium and cyclic GMP. Vision Res. 1986;26(10):1613–1643. doi: 10.1016/0042-6989(86)90051-9. [DOI] [PubMed] [Google Scholar]
  35. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Stryer L. Cyclic GMP cascade of vision. Annu Rev Neurosci. 1986;9:87–119. doi: 10.1146/annurev.ne.09.030186.000511. [DOI] [PubMed] [Google Scholar]
  37. Swanson R. J., Applebury M. L. Methylation of proteins in photoreceptor rod outer segments. J Biol Chem. 1983 Sep 10;258(17):10599–10605. [PubMed] [Google Scholar]
  38. Takio K., Smith S. B., Krebs E. G., Walsh K. A., Titani K. Amino acid sequence of the regulatory subunit of bovine type II adenosine cyclic 3',5'-phosphate dependent protein kinase. Biochemistry. 1984 Aug 28;23(18):4200–4206. doi: 10.1021/bi00313a029. [DOI] [PubMed] [Google Scholar]
  39. Tamanoi F., Hsueh E. C., Goodman L. E., Cobitz A. R., Detrick R. J., Brown W. R., Fujiyama A. Posttranslational modification of ras proteins: detection of a modification prior to fatty acid acylation and cloning of a gene responsible for the modification. J Cell Biochem. 1988 Mar;36(3):261–273. doi: 10.1002/jcb.240360307. [DOI] [PubMed] [Google Scholar]
  40. Titani K., Sasagawa T., Ericsson L. H., Kumar S., Smith S. B., Krebs E. G., Walsh K. A. Amino acid sequence of the regulatory subunit of bovine type I adenosine cyclic 3',5'-phosphate dependent protein kinase. Biochemistry. 1984 Aug 28;23(18):4193–4199. doi: 10.1021/bi00313a028. [DOI] [PubMed] [Google Scholar]
  41. Weber I. T., Shabb J. B., Corbin J. D. Predicted structures of the cGMP binding domains of the cGMP-dependent protein kinase: a key alanine/threonine difference in evolutionary divergence of cAMP and cGMP binding sites. Biochemistry. 1989 Jul 11;28(14):6122–6127. doi: 10.1021/bi00440a059. [DOI] [PubMed] [Google Scholar]
  42. Weber I. T., Steitz T. A., Bubis J., Taylor S. S. Predicted structures of cAMP binding domains of type I and II regulatory subunits of cAMP-dependent protein kinase. Biochemistry. 1987 Jan 27;26(2):343–351. doi: 10.1021/bi00376a003. [DOI] [PubMed] [Google Scholar]
  43. Yamazaki A., Bartucca F., Ting A., Bitensky M. W. Reciprocal effects of an inhibitory factor on catalytic activity and noncatalytic cGMP binding sites of rod phosphodiesterase. Proc Natl Acad Sci U S A. 1982 Jun;79(12):3702–3706. doi: 10.1073/pnas.79.12.3702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yamazaki A., Sen I., Bitensky M. W., Casnellie J. E., Greengard P. Cyclic GMP-specific, high affinity, noncatalytic binding sites on light-activated phosphodiesterase. J Biol Chem. 1980 Dec 10;255(23):11619–11624. [PubMed] [Google Scholar]

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