Abstract
Cyclic GMP-dependent protein kinase, purified to homogeneity from bovine lung, was shown to activate hormone-sensitive lipase partially purified from chicken adipose tissue. The degree of activation was the same as that effected by cyclic AMP-dependent protein kinase although higher concentrations of the cyclic GMP-dependent enzyme were required (relative activities expressed in terms of histone H2b phosphorylation units). Activation by cyclic AMP-dependent protein kinase was completely blocked by the heat-stable protein kinase inhibitor protein from skeletal muscle but activation by the cyclic GMP enzyme was not inhibited. Lipase fully activated by cyclic AMP-dependent protein kinase showed no further change in activity when treated with cyclic GMP-dependent protein kinase. Lipase activated by cyclic GMP-dependent protein kinase was reversibly deactivated by purified phosphorylase phosphatase (from bovine heart); full activity was restored by reincubation with cyclic GMP and cyclic GMP-dependent protein kinase. Cholesterol esterase activity in the chicken adipose tissue fraction, previously shown to be activated along with the triglyceride lipase by cyclic AMP-dependent protein kinase, was also activated by cyclic GMP-dependent protein kinase. Crude preparations of hormone-sensitive triglyceride lipase from human or rat adipose tissue and cholesterol esterase from rat adrenal were also activated by cyclic GMP-dependent protein kinase. Purified phosphorylase kinase (rabbit skeletal muscle) was also shown to be activated by cyclic GMP-dependent protein kinase. The present results, together with those of other workers on histone phosphorylation, suggest that the substrate specificities of cyclic GMP-dependent and cyclic AMP-dependent protein kinase may be similar. This is discussed in the light of a model recently proposed with regard to the relationship between the subunit structures of the two kinases. The physiologic significance of the findings remains to be established.
Keywords: cyclic AMP-dependent protein kinase, protein kinase inhibitor, cholesterol esterase
Full text
PDF




Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Brandt H., Capulong Z. L., Lee E. Y. Purification and properties of rabbit liver phosphorylase phosphatase. J Biol Chem. 1975 Oct 25;250(20):8038–8044. [PubMed] [Google Scholar]
- Cohen P. The subunit structure of rabbit-skeletal-muscle phosphorylase kinase, and the molecular basis of its activation reactions. Eur J Biochem. 1973 Apr 2;34(1):1–14. doi: 10.1111/j.1432-1033.1973.tb02721.x. [DOI] [PubMed] [Google Scholar]
- Donnelly T. E., Jr, Kuo J. F., Miyamoto E., Greengard P. Protein kinase modulator from lobster tail muscle. II. Effects of the modulator on holoenzyme and catalytic subunit of guanosine 3',5'-monophosphate-dependent and adenosine 3',5'-monophosphate-dependent protein kinases. J Biol Chem. 1973 Jan 10;248(1):199–203. [PubMed] [Google Scholar]
- Exton J. H., Hardman J. G., Williams T. F., Sutherland E. W., Park C. R. Effects of guanosine 3',5'-monophosphate on the perfused rat liver. J Biol Chem. 1971 Apr 25;246(8):2658–2664. [PubMed] [Google Scholar]
- Fain J. N., Butcher F. R. Cyclic guanosine 3':5'-monophosphate and the regulation of lipolysis in rat fat cells. J Cyclic Nucleotide Res. 1976;2(2):71–78. [PubMed] [Google Scholar]
- Gardner R. M., Allen D. O. Regulation of cyclic nucleotide levels and glycogen phosphorylase activity by acetylcholine and epinephrine in perfused rat hearts. J Pharmacol Exp Ther. 1976 Aug;198(2):412–419. [PubMed] [Google Scholar]
- Gill G. N. A hypothesis concerning the structure of cAMP-and cGMP-dependent protein kinases. J Cyclic Nucleotide Res. 1977 Jun;3(3):153–162. [PubMed] [Google Scholar]
- Gill G. N., Holdy K. E., Walton G. M., Kanstein C. B. Purification and characterization of 3':5'-cyclic GMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3918–3922. doi: 10.1073/pnas.73.11.3918. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gill G. N., Walton G. M., Sperry P. J. Guanosine 3':5'-monophosphate-dependent protein kinase from bovine lung. Subunit structure and characterization of the purified enzyme. J Biol Chem. 1977 Sep 25;252(18):6443–6449. [PubMed] [Google Scholar]
- Glynn I. M., Chappell J. B. A simple method for the preparation of 32-P-labelled adenosine triphosphate of high specific activity. Biochem J. 1964 Jan;90(1):147–149. doi: 10.1042/bj0900147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldberg N. D., Haddox M. K., Nicol S. E., Glass D. B., Sanford C. H., Kuehl F. A., Jr, Estensen R. Biologic regulation through opposing influences of cyclic GMP and cyclic AMP: the Yin Yang hypothesis. Adv Cyclic Nucleotide Res. 1975;5:307–330. [PubMed] [Google Scholar]
- Goldberg N. D., O'Dea R. F., Haddox M. K. Cyclic GMP. Adv Cyclic Nucleotide Res. 1973;3:155–223. [PubMed] [Google Scholar]
- Hardman J. G., Mayer S. E., Clark B. Cocaine potentiation of the cardiac inotropic and phosphorylase responses to catecholamines as related to the uptake of H3-catecholamines. J Pharmacol Exp Ther. 1965 Dec;150(3):341–348. [PubMed] [Google Scholar]
- Hashimoto E., Takeda M., Nishizuka Y., Hamana K., Iwai K. Studies on the sites in histones phosphorylated by adenosine 3':5'-monophosphate-dependent and guanosine 3':5'-monophosphate-dependent protein kinases. J Biol Chem. 1976 Oct 25;251(20):6287–6293. [PubMed] [Google Scholar]
- Hofmann F., Beavo J. A., Bechtel P. J., Krebs E. G. Comparison of adenosine 3':5'-monophosphate-dependent protein kinases from rabbit skeletal and bovine heart muscle. J Biol Chem. 1975 Oct 10;250(19):7795–7801. [PubMed] [Google Scholar]
- Huttunen J. K., Steinberg D. Activation and phosphorylation of purified adipose tissue hormone-sensitive lipase by cyclic AMP-dependent protein kinase. Biochim Biophys Acta. 1971 Sep 1;239(3):411–427. doi: 10.1016/0005-2760(71)90034-8. [DOI] [PubMed] [Google Scholar]
- Illiano G., Tell G. P., Siegel M. E., Cuatrecasas P. Guanosine 3':5'-cyclic monophosphate and the action of insulin and acetylcholine. Proc Natl Acad Sci U S A. 1973 Aug;70(8):2443–2447. doi: 10.1073/pnas.70.8.2443. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Inoue M., Kishimoto A., Takai Y., Nishizuka Y. Guanosine 3':5'-monophosphate-dependent protein kinase from silkworm, properties of a catalytic fragment obtained by limited proteolysis. J Biol Chem. 1976 Jul 25;251(14):4476–4478. [PubMed] [Google Scholar]
- KREBS E. G., LOVE D. S., BRATVOLD G. E., TRAYSER K. A., MEYER W. L., FISCHER E. H. PURIFICATION AND PROPERTIES OF RABBIT SKELETAL MUSCLE PHOSPHORYLASE B KINASE. Biochemistry. 1964 Aug;3:1022–1033. doi: 10.1021/bi00896a003. [DOI] [PubMed] [Google Scholar]
- Khoo J. C., Aquino A. A., Steinberg D. The mechanism of activation of hormone-sensitive lipase in human adipose tissue. J Clin Invest. 1974 Apr;53(4):1124–1131. doi: 10.1172/JCI107650. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Khoo J. C. Ca2+-dependent activation of phosphorylase by phosphorylase kinase in adipose tissue. Biochim Biophys Acta. 1976 Jan 23;422(1):87–97. doi: 10.1016/0005-2744(76)90010-3. [DOI] [PubMed] [Google Scholar]
- Khoo J. C., Steinberg D., Huang J. J., Vagelos P. R. Triglyceride, diglyceride, monoglyceride, and cholesterol ester hydrolases in chicken adipose tissue activated by adenosine 3':5'-Monophosphate-dependent protein kinase. Chromatographic resolution and immunochemical differentiation from lipoprotein lipase. J Biol Chem. 1976 May 25;251(10):2882–2890. [PubMed] [Google Scholar]
- Khoo J. C., Steinberg D. Reversible protein kinase activation of hormone-sensitive lipase from chicken adipose tissue. J Lipid Res. 1974 Nov;15(6):602–610. [PubMed] [Google Scholar]
- Krebs E. G. Protein kinases. Curr Top Cell Regul. 1972;5:99–133. [PubMed] [Google Scholar]
- Kuo J. F., Greengard P. Cyclic nucleotide-dependent protein kinases. VI. Isolation and partial purification of a protein kinase activated by guanosine 3',5'-monophosphate. J Biol Chem. 1970 May 25;245(10):2493–2498. [PubMed] [Google Scholar]
- Kuo J. F., Kuo W. N., Shoji M., Davis C. W., Seery V. L., Donnelly T. E., Jr Purification and general properties of guanosine 3':5'-monophosphate-dependent protein kinase from guinea pig fetal lung. J Biol Chem. 1976 Mar 25;251(6):1759–1766. [PubMed] [Google Scholar]
- Lincoln T. M., Corbin J. D. Adenosine 3':5'-cyclic monophosphate- and guanosine 3':5'-cyclic monophosphate-dependent protein kinases: possible homologous proteins. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3239–3243. doi: 10.1073/pnas.74.8.3239. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lincoln T. M., Hall C. L., Park C. R., Corbin J. D. Guanosine 3':5'-cyclic monophosphate binding proteins in rat tissues. Proc Natl Acad Sci U S A. 1976 Aug;73(8):2559–2563. doi: 10.1073/pnas.73.8.2559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nesbitt J. A., 3rd, Anderson W. B., Miller Z., Pastan I., Russell T. R., Gospodarowicz D. Guanylate cyclase and cyclic guanosine 3':5'-monophosphate phosphodiesterase activities and cyclic guanosine 3':5'-monophosphate levels in normal and transformed fibroblasts in culture. J Biol Chem. 1976 Apr 25;251(8):2344–2352. [PubMed] [Google Scholar]
- Nishiyama K., Katakami H., Yamamura H., Takai Y., Shimomura R. Functional specificity of guanosine 3':5'-monophosphate-dependent and adenosine 3':5'-monophosphate-dependent protein kinases from silkworm. J Biol Chem. 1975 Feb 25;250(4):1297–1300. [PubMed] [Google Scholar]
- Pittman R. C., Khoo J. C., Steinberg D. Cholesterol esterase in rat adipose tissue and its activation by cyclic adenosine 3':5'-monophosphate-dependent protein kinase. J Biol Chem. 1975 Jun 25;250(12):4505–4511. [PubMed] [Google Scholar]
- Pittman R. C., Steinberg D. Activatable cholesterol esterase and triacylglycerol lipase activities of rat adrenal and their relationship. Biochim Biophys Acta. 1977 Jun 22;487(3):431–444. doi: 10.1016/0005-2760(77)90214-4. [DOI] [PubMed] [Google Scholar]
- Pointer R. H., Butcher F. R., Fain J. N. Studies on the role of cyclic guanosine 3':5'-monophosphate and extracellular Ca2+ in the regulation of glycogenolysis in rat liver cells. J Biol Chem. 1976 May 25;251(10):2987–2992. [PubMed] [Google Scholar]
- Rosen O. M., Erlichman J. Reversible autophosphorylation of a cyclic 3':5'-AMP-dependent protein kinase from bovine cardiac muscle. J Biol Chem. 1975 Oct 10;250(19):7788–7794. [PubMed] [Google Scholar]
- Rubin C. S., Erlichman J., Rosen O. M. Molecular forms and subunit composition of a cyclic adenosine 3',5'-monophosphate-dependent protein kinase purified from bovine heart muscle. J Biol Chem. 1972 Jan 10;247(1):36–44. [PubMed] [Google Scholar]
- Steinberg D. Interconvertible enzymes in adipose tissue regulated by cyclic AMP-dependent protein kinase. Adv Cyclic Nucleotide Res. 1976;7:157–198. [PubMed] [Google Scholar]
- Takai Y., Nishiyama K., Yamamura H., Nishizuka Y. Guanosine 3':5'-monophosphate-dependent protein kinase from bovine cerebellum. Purification and characterization. J Biol Chem. 1975 Jun 25;250(12):4690–4695. [PubMed] [Google Scholar]
- Trzeciak W. H., Boyd G. S. Activation of cholesteryl esterase in bovine adrenal cortex. Eur J Biochem. 1974 Jul 1;46(1):201–207. doi: 10.1111/j.1432-1033.1974.tb03612.x. [DOI] [PubMed] [Google Scholar]
- Walsh D. A., Ashby C. D., Gonzalez C., Calkins D., Fischer E. H. Krebs EG: Purification and characterization of a protein inhibitor of adenosine 3',5'-monophosphate-dependent protein kinases. J Biol Chem. 1971 Apr 10;246(7):1977–1985. [PubMed] [Google Scholar]
- Walsh D. A., Perkins J. P., Krebs E. G. An adenosine 3',5'-monophosphate-dependant protein kinase from rabbit skeletal muscle. J Biol Chem. 1968 Jul 10;243(13):3763–3765. [PubMed] [Google Scholar]
- Wastila W. B., Stull J. T., Mayer S. E., Walsh D. A. Measurement of cyclic 3',5'-denosine monophosphate by the activation of skeletal muscle protein kinase. J Biol Chem. 1971 Apr 10;246(7):1996–2003. [PubMed] [Google Scholar]
