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Photoaffinity Labeling of Cyclic AMP-Dependent and Cyclic GMP-Dependent Protein Kinases

  • U. Walter
  • P. Greengard
Part of the Handbook of Experimental Pharmacology book series (HEP, volume 58 / 1)

Abstract

Photoaffinity labeling is a useful technique for the study of ligand-receptor interactions. Irradiation of chemically modified ligands with light produces highly reactive intermediates which are capable of forming covalent bonds with the receptors. Photoaffinity labeling has been used for many different ligands and has been especially successful for cyclic nucleotides. Several photoaffinity analogues of cAMP and cGMP are available. 8-Azido-cAMP (8-N3-cAMP) has been the one most widely and successfully used. 8-N3-cAMP binds to the regulatory subunit of a Type II cAMP-dependent protein kinase with a slightly lower affinity than cAMP and is able to label all cAMPbinding sites under saturating conditions. The data indicate that 8-N3-cAMP is an effective analogue of cAMP and a very efficient photoaffinity label for cAMP-binding sites. Regulatory subunits of Type I and Type II cAMP-dependent protein kinases are the only proteins present in all tissues studied which are specifically labeled by 8-N3-cAMP. Other minor labeled proteins appear to be proteolytic fragments of the two types of regulatory subunits. The finding that most, if not all, specific cAMP-receptor proteins are regulatory subunits of cAMP-dependent protein kinase strongly supports the hypothesis that cAMP-dependent protein kinases and their subunits mediate all the physiological effects of cAMP. Photoaffinity labeling has been used to detect and characterize proteolytic fragments of cAMP-dependent protein kinases and to study the regulation of the amounts of cAMP-dependent protein kinases and their subunits. Similarly, photoaffinity analogues of cGMP have been used to label cGMP-dependent protein kinases. Photoaffinity analogues of cyclic nucleotides are powerful tools for the investigation of cAMP- and cGMP-receptor proteins. Studies with these analogues should contribute substantially to an understanding of the mechanism of action of cyclic nucleotides as second messengers.

Keywords

Cyclic Nucleotide Regulatory Subunit Photoaffinity Label Dent Protein Kinase Pendent Protein Kinase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aiba H, Krakow JS (1979) Photoaffinity labeling of the E. coli cyclic AMP receptor protein with 8-azido-adenosine 3′,5′-monophosphate. Fed Proc 38:231Google Scholar
  2. Antonoff RS, Ferguson JJ (1974) Photoaffinity labeling with cyclic nucleotides. J Biol Chem 249:3319–3321PubMedGoogle Scholar
  3. Antonoff RS, Ferguson JJ, Idelkope G (1976) Direct photoaffinity labeling of cyclic nucleotide binding proteins with guanosine-3′,5′-monophosphate. Photochem Photobiol 23:327–329PubMedCrossRefGoogle Scholar
  4. Appleman MM, Thompson WJ, Russell TR (1973) Cyclic nucleotide phosphodiesterases. Adv Cyclic Nucleotide Res 3:65–98PubMedGoogle Scholar
  5. Ashman DF, Lipton R, Melicow MM, Price TD (1963) Isolation of adenosine 3′,5′-monophosphate and guanosine 3′,5′-monophosphate from rat urine. Biochem Biophys Res Commun 11:330–334PubMedCrossRefGoogle Scholar
  6. Bayley H, Knowles JR (1977) Photoaffinity labeling. Methods Enzymol 46:69–114PubMedCrossRefGoogle Scholar
  7. Bodwin JS, Clair T, Cho-Chung YS (1978) Inverse relation between estrogen receptors and cyclic adenosine 3′:5′-monophosphate-binding proteins in hormone-dependent mammary tumor regression due to dibutyryl cyclic adenosine 3′:5′-monophosphate treatment or ovariectomy. Cancer Res 38:3410–3413PubMedGoogle Scholar
  8. Brunswick J, Cooperman BS (1971) Photo-affinity labels for adenosine 3′:5′-cyclic monophosphate. Proc Natl Acad Sci USA 68:1801–1804PubMedCrossRefGoogle Scholar
  9. Cartwright JS, Hutchinson DW, Armstrong VW (1976) The reaction between thiols and 8-azidoadenosine derivatives. Nucleic Acids Res 3:2331–2339PubMedGoogle Scholar
  10. Casnellie JE, Schlichter DJ, Walter U, Greengard P (1978) Photoaffinity labeling of a guanosine 3′:5′-monophosphate-dependent protein kinase from vascular smooth muscle. J Biol Chem 253:4771–4776PubMedGoogle Scholar
  11. Casnellie JE, Ives HE, Jamieson JD, Greengard P (1980) cGMP-dependent protein phosphorylation in intact medial tissue and isolated cells from vascular smooth muscle. J Biol Chem 255:3770–3776PubMedGoogle Scholar
  12. Cho-Chung YS (1979) On the mechanism of cyclic AMP-mediated growth arrest of solid tumors. Adv Cyclic Nucleotide Res 12:in pressGoogle Scholar
  13. Chowdhry V, Westheimer FH (1979) Photoaffinity labeling of biological systems. Ann Rev Biochem 48:293–325PubMedCrossRefGoogle Scholar
  14. Christian CN, Nelson PG, Peacock J, Nirenberg M (1977) Synapse formation between two clonal cell lines. Science 196:995–998PubMedCrossRefGoogle Scholar
  15. Cooperman BS, Brunswick J (1973) On the photoaffinity labeling of rabbit muscle phosphofructokinase with O2 ′-(ethyl-2-diazomalonyl)adenosine 3′:5′-cyclic monophosphate. Biochemistry 12:4079–4084PubMedCrossRefGoogle Scholar
  16. Cooperman BS (1976) Photoaffinity labeling of proteins and more complex receptors. In: Smith KC (ed) Aging, carcinogenesis and radiation biology. Plenum, New York, pp 315–340Google Scholar
  17. Corbin JD, Keely SL, Park CR (1975) The distribution and dissociation of cyclic adenosine 3′,5′-monophosphate-dependent protein kinases in adipose, cardiac and other tissues. J Biol Chem 250:218–225PubMedGoogle Scholar
  18. Corbin JD, Keely SL (1977) Characterization and regulation of heart adenosine 3′,5′-monophosphate-dependent protein kinase isozymes. J Biol Chem 252:910–918PubMedGoogle Scholar
  19. Corbin JD, Sugden PH, Lincoln TM, Keely SL (1977) Compartmentalization of adenosine 3′:5′-monophosphate and adenosine 3′:5′-monopnosphate-dependent protein kinase in heart tissue. J Biol Chem 252:3854–3861PubMedGoogle Scholar
  20. Corbin JD, Sugden PH, West L, Flockhart DA, Lincoln TM, McCarthy D (1978) Studies on the properties and mode of action of the purified regulatory subunit of bovine heart adenosine 3′:5′-monophosphate-dependent protein kinase. J Biol Chem 253:3997–4003PubMedGoogle Scholar
  21. Creed D (1974) Photochemical probes for biological interactions. Photochem Photobiol 19:459–462PubMedCrossRefGoogle Scholar
  22. DeCrombrugghe B, Chen B, Anderson W, Nissley P, Gottesman M, Perlman M, Pastan I (1971) LacDNA, RNA polymerase, cyclic AMP receptor protein, cyclic AMP, Lac repressor and inducer are the essential elements for controlled Lac transcription. Nature 231:139–142Google Scholar
  23. DeJonge H, Rosen OM (1977) Self-phosphorylation of cyclic guanosine 3′:5′-monophosphate-dependent protein kinase from bovine lung. J Biol Chem 252:2780–2783Google Scholar
  24. Dreyfuss G, Schwartz K, Blout ER, Barrio JR, Lin FT, Leonard NJ (1978 a) Fluorescent photoaffinity labeling: Adenosine 3′,5′-cyclic monophosphate receptor sites. Proc Natl Acad Sci USA 75:1199–1203PubMedCrossRefGoogle Scholar
  25. Dreyfuss G, Schwartz KJ, Blout ER (1978 b) Compartmentalization of cyclic AMP-dependent protein kinases in human erythrocytes. Proc Natl Acad Sci USA 75:5926–5930PubMedCrossRefGoogle Scholar
  26. Fleischer N, Rosen OM, Reichlin M (1976) Radioimmunoassay of bovine heart protein kinase. Proc Natl Acad Sci USA 73:54–58PubMedCrossRefGoogle Scholar
  27. Flockerzi V, Speichermann N, Hofmann F (1978) A guanosine-3′:5′-monophosphate-dependent protein kinase from bovine heart muscle. J Biol Chem 253:3395–3399PubMedGoogle Scholar
  28. Friedman DL, Chambers DA (1978) Cyclic nucleotide-binding proteins detected by photoaffmity labeling in nucleus and cytoplasm of bovine liver. Proc Natl Acad Sci USA 75:5286–5290PubMedCrossRefGoogle Scholar
  29. Geahlen RL, Haley BE, Krebs EG (1979) Synthesis and use of 8-azido-guanosine 3′,5′-cyclic monophosphate as photoaffmity label for cyclic GMP-dependent protein kinase. Proc Natl Acad Sci USA 76:2213–2217PubMedCrossRefGoogle Scholar
  30. Gill GN, Holdy KE, Walton GM, Kanstein CB (1976) Purification and characterization of 3′:5′-cyclic GMP-dependent protein kinase. Proc Natl Acad Sci USA 73:3918–3922PubMedCrossRefGoogle Scholar
  31. Gill GN, Walton GM (1979) Assay of cyclic nucleotide-dependent protein kinase. Adv Cyclic Nucleotide Res 10:93–106PubMedGoogle Scholar
  32. Haley BE (1975) Photoaffinity labeling of adenosine 3′,5′-cyclic monophosphate binding sites of human red cell membranes. Biochemistry 14:3852–3857PubMedCrossRefGoogle Scholar
  33. Haley BE (1977) Adenosine 3′,5′-cyclic monophosphate binding sites. Methods Enzymol 46:339–346PubMedCrossRefGoogle Scholar
  34. Haley BE, Hoffman JF (1974) Interactions of a photoaffinity ATP analog with cation-stimulated adenosine triphosphatases of human red cell membranes. Proc Natl Acad Sci USA 71:3367–3371PubMedCrossRefGoogle Scholar
  35. Hamet P, Coquil JF (1978) Cyclic GMP binding and cyclic GMP phosphodiesterase in rat platelets. J Cyclic Nucleotide Res 4:281–290PubMedGoogle Scholar
  36. Hamprecht B (1976) Neuron models. Angew Chem Int Ed Engl 15:194–206PubMedCrossRefGoogle Scholar
  37. Hershfield MS, Kredich NM (1978) S-adenosylhomocysteine hydrolase is an adenosinebinding protein: A target for adenosine toxicity. Science 202:757–760PubMedCrossRefGoogle Scholar
  38. Hixson CS, Krebs EG (1979) Affinity labeling of catalytic subunit of bovine heart muscle cyclic AMP-dependent protein kinase by 5′-p-fluorosulfonylbenzoyl-adenosine. J Biol Chem 254:7509–7514PubMedGoogle Scholar
  39. Hofmann F, Beavo JA, Bechtel PJ, Krebs EG (1975) Comparison of adenosine 3′:5′-monophosphate-dependent protein kinases from rabbit skeletal and bovine heart muscle. J Biol Chem 250:7795–7801PubMedGoogle Scholar
  40. Hofmann F, Bechtel PJ, Krebs EG (1977) Concentrations of cyclic AMP-dependent protein kinase subunits in various tissues. J Biol Chem 252:1441–1447PubMedGoogle Scholar
  41. Hoppe J, Freist W (1979) Localization of the high-affinity ATP site in adenosine-3′:5′-monophosphate-dependent protein kinase type I. Eur J Biochem 93:141–146PubMedCrossRefGoogle Scholar
  42. Imashuku S, Fossett MC, Green AA (1979) Characterization of adenosine cyclic 3′:5′-monophosphate-binding proteins in human neuroblastoma. Cancer Res 39:3006–3013PubMedGoogle Scholar
  43. Jungmann RA, Russell DH (1977) Cyclic AMP, cyclic AMP-dependent protein kinase, and the regulation of gene expression. Life Sci 20:1787–1798PubMedCrossRefGoogle Scholar
  44. Kemp RG, Krebs EG (1967) Binding of metabolites by phosphofructokinase. Biochemistry 6:423–434PubMedCrossRefGoogle Scholar
  45. Knowles JR (1972) Photogenerated reagents for biological receptor-site labeling. Acc Chem Res 5:155–160CrossRefGoogle Scholar
  46. Kuo JF, Greengard P (1969) Cyclic nucleotide-dependent protein kinases. IV. Widespread occurrence of adenosine 3′,5′-monophosphate-dependent protein kinase in various tissues and phyla of the animal kingdom. Proc Natl Acad Sci USA 64:1349–1355PubMedCrossRefGoogle Scholar
  47. Kuo JF, Greengard P (1970) Cyclic nucleotide-dependent protein kinases. VI. Isolation and partial purification of a protein kinase activated by guanosine 3′,5′-monophosphate. J Biol Chem 245:2493–2498PubMedGoogle Scholar
  48. Kuo JF, Wyatt GR, Greengard P (1971) Cyclic nucleotide-dependent protein kinases. IX. Partial purification and some properties of guanosine 3′,5′-monophosphate-dependent and adenosine 3′,5′-monophosphate-dependent protein kinases from various tissues and species of arthropoda. J Biol Chem 246:7159–7167PubMedGoogle Scholar
  49. Kupfer A, Gani V, Jimenex JS, Shaltiel S (1979) Affinity labeling of the catalytic subunit of cyclic AMP-dependent protein kinase by Nα-tosyl-L-lysine chloromethyl ketone. Proc Natl Acad Sci USA 76:3073–3077PubMedCrossRefGoogle Scholar
  50. Lincoln TM, Hall CL, Park CR, Corbin JD (1976) Guanosine 3′:5′-cyclic monophosphate binding proteins in rat tissues. Proc Natl Acad Sci USA 73:2559–2563PubMedCrossRefGoogle Scholar
  51. Lincoln TM, Dills WL, Corbin JD (1977) Purification and subunit composition of guanosine 3′:5′-monophosphate-dependent protein kinase from bovine lung. J Biol Chem 252:4269–4275PubMedGoogle Scholar
  52. Lohmann SM, Walter U, Greengard P (1978) Protein kinases in developing rat brain. J Cyclic Nucleotide Res 4:445–452PubMedGoogle Scholar
  53. Maeno H, Johnson EM, Greengard P (1971) Subcellular distribution of adenosine 3′,5′-monophosphate-dependent protein kinase in rat brain. J Biol Chem 246:134–142PubMedGoogle Scholar
  54. Miller JP, Boswell KH, Muneyama K, Simon LN, Robins RK, Shuman DA (1973) Synthesis and biochemical studies of various 8-substituted derivatives of guanosine 3′,5′-cyclic phosphate, inosine 3′,5′-cyclic phosphate, and xanthosine 3′,5′-cyclic phosphate. Biochemistry 12:5310–5319PubMedCrossRefGoogle Scholar
  55. Muneyama K, Bauer RJ, Shuman DA, Robins RK, Simon LN (1971) Chemical synthesis and biological activity of 8-substituted adenosine 3′,5′-cyclic monophosphate derivatives. Biochemistry 10:2390–2395PubMedCrossRefGoogle Scholar
  56. Nelson P, Christian C, Nirenberg M (1976) Synapse formation between clonal neuroblastoma X glioma hybrid cells and striated muscle cells. Proc Natl Acad Sci USA 73:123–127PubMedCrossRefGoogle Scholar
  57. Nelson PG, Christian CN, Daniels MP, Henkart M, Bullock P, Mullinax D, Nirenberg M (1977) Formation of synapses between cells of neuroblastoma X glioma hybrid clone and mouse myotubes. Brain Res 147:245–259CrossRefGoogle Scholar
  58. Nimmo HG, Cohen P (1977) Hormonal control of protein phosphorylation. Adv Cyclic Nucleotide Res 8:145–266PubMedGoogle Scholar
  59. Owens JR, Haley BE (1978) Use of photoaffinity nucleotide analogs to determine the mechanism of ATP regulation of a membrane-bound, cAMP-activated protein kinase. J Supramol Struct 9:57–68PubMedCrossRefGoogle Scholar
  60. Pastan I, Perlman RL (1972) Regulation of gene transcription in E. coli by cyclic AMP. Adv Cyclic Nucleotide Res 1:11–16PubMedGoogle Scholar
  61. Pomerantz AH, Rudolph SA, Haley BE, Greengard P (1975) Photoaffinity labeling of a protein kinase from bovine brain with 8-azido-adenosine 3′,5′-monophosphate. Biochemistry 14:3858–3862PubMedCrossRefGoogle Scholar
  62. Potter RL, Taylor SS (1979 a) Relationship between structural domains and function in the regulatory subunit of cAMP-dependent protein kinases I and II from porcine skeletal muscle. J Biol Chem 254:2413–2418PubMedGoogle Scholar
  63. Potter RL, Taylor SS (1979 b) The structural and functional domains of cAMP-dependent protein kinase I and II. Fed Proc 38:316Google Scholar
  64. Prashad N, Rosenberg RN, Wischmeyer B, Ulrich C, Sparkman D (1979) Induction of adenosine 3′,5′-monophosphate-binding proteins by N6,O2′-dibutyryladenosine 3′,5′-monophosphate in mouse neuroblastoma cells. Analysis by two-dimensional gel electrophoresis. Biochemistry 18:2717–2725PubMedCrossRefGoogle Scholar
  65. Rangel-Aldao R, Rosen OM (1976) Mechanism of self-phosphorylation of adenosine 3′:5′-monophosphate-dependent protein kinase from bovine cardiac muscle. J Biol Chem 251:7526–7529PubMedGoogle Scholar
  66. Rangel-Aldao R, Kupiec JW, Rosen OM (1979) Resolution of the phosphorylated and dephosphorylated cAMP-binding proteins of bovine cardiac muscle by affinity labeling and two-dimensional electrophoresis. J Biol Chem 254:2499–2508PubMedGoogle Scholar
  67. Rannels SR, Corbin JD (1979) Characterization of small cAMP-binding fragments of cAMP-dependent protein kinases. J Biol Chem 254:8605–8610PubMedGoogle Scholar
  68. Rubin CS (1975) Adenosine 3′:5′-monophosphate-regulated phosphorylation of erythrocyte membrane proteins. J Biol Chem 250:9044–9052PubMedGoogle Scholar
  69. Rubin CS, Rangel-Aldao R, Sarkar D, Erlichman J, Fleischer N (1979) Characterization and comparison of membrane-associated and cytosolic cAMP-dependent protein kinases. J Biol Chem 254:3797–3805PubMedGoogle Scholar
  70. Rudolph SA, Krueger BK (1979) Endogenous protein phosphorylation and dephosphorylation. Adv Cyclic Nucleotide Res 10:107–133PubMedGoogle Scholar
  71. Ruoho AR, Kiefer H, Roeder PE, Singer S (1973) The mechanism of photoaffinity labeling. Proc Natl Acad Sci USA 70:2567–2571PubMedCrossRefGoogle Scholar
  72. Russell DH (1978) Type I cyclic AMP-dependent protein kinase as a positive effector of growth. Adv Cyclic Nucleotide Res 9:493–506PubMedGoogle Scholar
  73. Saebø J, Ueland PM (1978) An adenosine 3′:5′-monophosphate-adenosine-binding protein. from mouse liver. FEBS Lett 96:125–128PubMedCrossRefGoogle Scholar
  74. Schwechheimer K, Hofmann F (1977) Properties of regulatory subunit of cyclic AMP-dependent protein kinase (peak I) from rabbit skeletal muscle prepared by urea treatment of the holoenzyme. J Biol Chem 252:7690–7696PubMedGoogle Scholar
  75. Singh A, Thornton ER, Westheimer FH (1962) The photolysis of diazoacetyl chymotrypsin. J Biol Chem 237:3006–3008PubMedGoogle Scholar
  76. Srivastava AK, Stellwagen RH (1978) Presence of the sites for interacting with cyclic AMP and with catalytic subunit on small fragments of protein kinase regulatory subunit. J Biol Chem 253:1752–1755PubMedGoogle Scholar
  77. Staros JV, Bayley H, Standring DN, Knowles JR (1978) Reduction of aryl azides by thiols: Implications for the use of photoaffinity reagents. Biochem Biophys Res Commun 80:568–572PubMedCrossRefGoogle Scholar
  78. Sugden PH, Corbin JD (1976) Adenosine 3′:5′-cyclic monophosphate-binding proteins in bovine and rat tissues. Biochem J 159:423–437PubMedGoogle Scholar
  79. Ueland PM, Døskeland SO (1977) An adenosine 3′:5′-monophosphate-adenosine binding protein from mouse liver. J Biol Chem 252:677–686PubMedGoogle Scholar
  80. Uno I, Ueda T, Greengard P (1976) Differences in properties of cytosol and membrane-derived protein kinases. J Biol Chem 251:2192–2195PubMedGoogle Scholar
  81. Walsh DA, Perkins JP, Krebs EG (1968) An adenosine 3′,5′-monophosphate-dependent protein kinase from rabbit skeletal muscle. J Biol Chem 243:3763–3765PubMedGoogle Scholar
  82. Walter U, Uno I, Liu AY-C, Greengard P (1977 a) Identification, characterization, and quantitative measurement of cyclic AMP receptor proteins in cytosol of various tissues using a photoaffinity ligand. J Biol Chem 252:6494–6500PubMedGoogle Scholar
  83. Walter U, Uno I, Liu AY-C, Greengard P (1977 b) Study of autophosphorylation of isoenzymes of cyclic AMP-dependent protein kinases. J Biol Chem 252:6588–6590PubMedGoogle Scholar
  84. Walter U, Greengard P (1978) Quantitative labeling of the regulatory subunit of Type II cAMP-dependent protein kinase from bovine heart by a photoaffinity analog. J Cyclic Nucleotide Res 4:437–444PubMedGoogle Scholar
  85. Walter U, Kanof P, Schulman H, Greengard P (1978) Adenosine 3′:5′-monophosphate receptor proteins in mammalian brain. J Biol Chem 253:6275–6280PubMedGoogle Scholar
  86. Walter U, Costa MRC, Breakefield XO, Greengard P (1979) Presence of free cyclic AMP receptor protein and regulation of its level by cyclic AMP in neuroplastoma-glioma hybrid cells. Proc Natl Acad Sci USA 76:3251–3255PubMedCrossRefGoogle Scholar
  87. Weber W, Hilz H (1978) Adenosine-3′:5′-monophosphate-binding proteins from bovine kidney. Eur J Biochem 83:215–225PubMedCrossRefGoogle Scholar
  88. Wold F (1977) Affinity labeling. An overview. Methods in Enzymol 46:3–14CrossRefGoogle Scholar
  89. Yuh K-CM, Tao M (1974) Purification and characterization of adenosine cyclic 3′,5′-monophosphate binding protein factors from rabbit erythrocytes. Biochemistry 13:5220–5226PubMedCrossRefGoogle Scholar
  90. Zoller MJ, Taylor SS (1979) Affinity labeling of the nucleotide binding site of the catalytic subunit of cAMP-dependent protein kinase using p-fluorosulfonyl-[14C]benzoyl-5′-adenosine. Identification of a modified lysine residue. J Biol Chem 254:8363–8368PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 1982

Authors and Affiliations

  • U. Walter
  • P. Greengard

There are no affiliations available

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