Evidence of an important and direct role for protein kinase C in agonist-induced phosphorylation leading to desensitization of the angiotensin AT(1A) receptor

British Journal of Pharmacology

Volumn 122, Issue 7, 1997, Pages 1469-1477

  Balmforth, A J ^a   Shepherd, F H ^a   Warburton, P ^a   Ball, S G ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

(His)6 affinity tag; Angiotensin II; AT(1A) receptor; Desensitization; G protein coupled receptor kinase; HEK 293 cells; Inositol 1,4,5 trisphosphate; Phosphorylation; Protein kinase C; Stable expression

Indexed keywords

2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; ANGIOTENSIN; ANGIOTENSIN 1 RECEPTOR; HISTIDINE; PROTEIN KINASE; PROTEIN KINASE C; RECEPTOR PROTEIN; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL LINE; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION;

EID: 0030734648     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0701522     Document Type: Article

References (51)

1. ABDELLATIF, M.M., NEUBAUER, C.F., LEDERER, W.J. & ROGERS, T.B. (1991). Angiotensin-induced desensitization of the phosphoinositide pathway in cardiac cells occurs at the level of the receptor. Circ. Res., 69, 800-809.
2. ALALUF, S., MULVIHILL, E.R. & MCILHINNEY, R.A.J. (1995). Rapid agonist mediated phosphorylation of the metabotropic glutamate receptor 1α by protein kinase C in permanently transfected BHK cells. FEBS. Lett., 367, 301-305.
3. ALI, H., RICHARDSON, R.M., TOMHAVE, E.D., DIDSBURY, J.R. & SNYDERMAN, R. (1993). Differences in phosphorylation of formylpeptide and C5a chemoattractant receptors correlate with differences in desensitization. J. Biol. Chem., 268, 24247-24254.
4. ALI, H., RICHARDSON, R.M., TOMHAVE, E.D., DUBOSE, R.A., HARIBABU, B. & SNYDERMAN, R. (1994). Regulation of stably transfected platelet activating factor receptor in RBL-2H3 cells. J. Biol. Chem., 269, 24247-24254.
5. 1A receptor possessing an IMAC affinity tag. J. Hypertens., 12 (Suppl. 3), S179.
6. 1A receptor. Eur. J. Pharmacol., 291, 135-141.
7. 1A receptor possessing an IMAC affinity tag. J. Hypertens., 12 (Suppl. 3), S65.
8. BOULAY, G., CHRETIEN, L., RICHARD, D.E. & GUILLEMETTE, G. (1994). Short-term desensitization of the angiotensin II receptor of bovine adrenal glomerulosa cells corresponds to a shift from high to a low affinity state. Endocrinology, 135, 2130-2136.
9. BOUSCAREL, B., WILSON, P.B., BLACKMORE, P.F., LYNCH, C.J. & EXON, J.H. (1988). Agonist-induced down-regulation of the angiotensin II receptor in primary cultures of rat hepatocytes. J. Biol. Chem., 263, 14920-14924.
10. BROCK, T.A., RITTENHOUSE, S.F., POWERS, C.W., EKSTEIN, L.S., GIMBRONE, M.A. & ALEXANDER, R.W. (1985). Phorbol ester and 1-oleoyl-2-acetylglycerol inhibit angiotensin activation of phospholipase C in cultured vascular smooth muscle cells. J. Biol. Chem., 260, 14158-14162.
11. CAPPONI, A.M. & CATT, K.J. (1980). Solubilization and characterization of adrenal and uterine angiotensin II receptors after photoaffinity labelling. J. Biol. Chem., 255, 12081-12086.
12. CARSON, M.C., HARPER, C.M., BAUKAL, A.J., AGUILERA, G. & CATT, K.J. (1987). Physiochemical characterization of photoaffinity-labeled angiotensin II receptors. Mol. Endocrinol., 1, 147-153.
13. DESARNAUD, F., MARIE, J., LOMBARD, C., LARGUIER, R., SEYER, R., LORCA, T., JARD, S. & BONNAFOUS, J-C. (1993). Deglycosylation and fragmentation of a purified rat liver angiotensin II receptor: application to the mapping of hormone-binding domains. Biochem. J., 289, 289-297.
14. 2A-adrenergic receptor. J. Biol. Chem., 270, 4681-4688.
15. GUILLEMETTE, G., GUILLON, G., MARIE, J., BALESTRE M.-N., ESCHER, E. & JARD, S. (1986). High yield photoaffinity labelling of angiotensin II receptors. Mol. Pharmacol., 30, 544-551.
16. 2-adrenergic receptor are involved in distinct pathways of receptor desensitization. J. Biol. Chem., 264, 12657-12665.
17. HAUSDORFF, W.P., CARON, M.G. & LEFKOWITZ, R.J. (1990). Turning off the signal: desensitization of β-adrenergic receptor function. FASEB J., 4, 2881-2889.
18. HOCHULI, E., BANNWARTH, W., DOBELI, H., GENTZ, R. & STUBER, D. (1988). Genetic approaches to facilitate purification of recombinant proteins with a novel metal chelate adsorbent. Bio/Technology, 6, 1321-1325.
19. ISHII, K., CHEN, J., ISHII, M., KOCH, W.J., FREEDMAN, N.J., LEFKOWITZ, R.J. & COUGHLIN, S.R. (1994). Inhibition of thrombin receptor signalling by a G-protein coupled receptor kinase. J. Biol. Chem., 269, 1125-1130.
20. IWAI, N. & INAGAMI, T. (1992). Identification of two subtypes in the rat type 1 angiotensin II receptor. FEBS Lett., 298, 257-260.
21. JANKNECHT, R., DE MARTYNOFF, G., LOU, J., HIPSKIND, R.A., NORDHEIM, A. & STUNNENBERG, H.G. (1991). Rapid and efficient purification of native histidine-tagged protein expressed by recombinant vaccinia virus. Proc. Natl. Acad. Sci. U.S.A., 88, 8972-8976.
22. KAI, H., GRIENDLING, K.K., LASSEGUE, B., OLLERENSHAW, J.D., RUNG, M.S. & ALEXANDER, R.W. (1994). Agonist-induced phosphorylation of the vascular type I angiotensin II receptor. Hypertension, 24, 523-527.
23. KAMBAYASHI, Y., BARDHAN, S., TAKAHASHI, K., TSUZUKI, S., INUI, H., HAMAKUBO, T. & INAGAMI, T. (1993). Molecular cloning of a novel angiotensin II receptor isoform involved in phosphotyrosine phosphatase inhibition. J. Dial. Chem., 268, 24543-24546.
24. KROOG, G.S., SAINZ, E., WORLAND, P.J., AKESON, M.A., BENYA, R.V., JENSEN, R.T. & BATTEY, J.F. (1995). The gastrin-releasing peptide receptor is rapidly phosphorylated by a kinase other than protein kinase C after exposure to agonist. J. Biol. Chem., 270, 8217-8224.
25. 1B-adrenergic receptor. J. Biol. Chem., 269, 22887-22893.
26. LOWRY, O.H., ROSEBROUGH, N.J., FARR, A.L. & RONDELL, R.J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193, 265-275.
27. MARIE, J.M., SEYER, R., LOMBARD, C., DESARNAUD, F., AUMELAS, A., JERD, S. & BONNASFOUS, J.C. (1990). Affinity chromatography purification of angiotensin II receptor using photoactivable biotinylated probes. Biochemistry, 29, 8943-8950.
28. MORRISSEY, J.H. (1981). Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal. Biochem., 117, 307-310.
29. MUKOYAMA, M., NAKAJIMA, M., HORIUCHI, M., SASAMURA, H., PRATT, R.E. & DZAU, V.J. (1993). Expression cloning of type 2 angiotensin II receptor reveals a unique class of seven-transmembrane receptors. J. Biol. Chem., 268, 24539-24542.
30. MURPHY, T.J., ALEXANDER, R.W., GRIENDLING, K.K., RUNGE, M.S. & BERNSTEIN, K.E. (1991). Isolation of a cDNA encoding the vascular type-1 angiotensin II receptor. Nature, 351, 233-236.
31. OPPERMANN, M., FREEDMAN, N.J., ALEXANDER, R.W. & LEFKOWITZ, R.J. (1996). Phosphorylation of the type 1A angiotensin II receptor by G protein receptor kinases and protein kinase C. J. Biol. Chem., 271, 13266-13272.
32. 2+ mobilization in renal mesangial cells. Eur. J. Pharmacol., 245, 15-21.
33. PALCZEWSKI, K. & BENOVIC, J.L. (1991). G protein-coupled receptor kinases. Trends Biochem. Sci., 16, 387-391.
34. 2+ rise in rat renal mesangial cells. FEBS Lett., 203, 262-266.
35. PFEILSCHIFTER, J. (1988). Protein kinase C from rat renal mesangial cells: its role in homologous desensitization of angiotensin II-induced polyphosphoinositide hydrolysis. Biochem. Biophys. Acta, 969, 263-270.
36. PFEILSCHIFTER, J. & BAUER, C. (1987). Different effects of phorbol ester on angiotensin II- and stable GTP analogue-induced activation of polyphosphoinositide phosphodiesterase in mem-branes isolated from rat mesangial cells. Biochem. J., 248, 209-215.
37. PFEILSCHIFTER, J., FANDREY, J., OCHSNER, M., WHITEBREAD, S & DE GASPARO, M (1990). Potentiation of Angiotensin II stimulated phosphoinositide hydrolysis, calcium mobilisation and contraction of renal mesangial cells upon down-regulation of protein kinase C. FEBS. Lett., 261, 307-311.
38. PFEILSCHIFTER, J., OCHSNER, M., WHITEBREAD, S & DE GASPARO, M. (1989). Downregulation of protein kinase C potentiates angiotensin II-stimulated polyphosphoinositide hydrolysis in vascular smooth-muscle cells. Biochem. J., 262, 285-291.
39. RONDEAU, J-J., MCNICOLL, N., ESCHER, E, MELOCHE, S., ONG, H. & DE LEAN, A. (1990). Hydrodynamic properties of the angiotensin II receptor from bovine adrenal zona glomerulosa. Biochem. J., 268, 443-448.
40. SAKUTA, H., SEKIGUCHI, M., OKAMOTO, K. & SAKAI, Y. (1991). Desensitization of endogenous angiotensin II receptors in Xenopus oocytes: a role of protein kinase C. Eur. J. Pharmacol., 208, 41-47.
41. SASAKI, K., YAMANO, Y., BARDHAM, S., IWAI, N., MURRAY, J.J., HASEGAWA, M., MATSUDA, Y. & INAGAMI, T. (1991). Cloning and expression of a complementary DNA encoding a bovine adrenal angiotensin II type-1 receptor. Nature, 351, 230-232.
42. SASAMURA, H., DZAU, V.J. & PRATT, R.E. (1994). Desensitization of angiotensin receptor function. Kidney Int., 46, 1499-1501.
43. SASAMURA, H., HEIN, L., KRIEGER, J.E., PRATT, R.E., KOBILKA, B.K. & DZAU, V.J. (1992). Cloning, characterization, and expression of two angiotensin (AT-1) isoforms from the mouse genome. Biochem. Biophys. Res. Commun., 185, 253-259.
44. STERNE-MARR, R. & BENOVIC, J.L. (1995). Regulation of G protein-coupled receptors by receptor kinases and arrestins. Vitamins Hormones, 51, 193-234.
45. TANG, H., SHIRAI, H. & INAGAMI, T. (1995). Inhibition of protein kinase C prevents rapid desensitization of type 1B angiotensin II receptor. Circ. Res., 77, 239-248.
46. TENCE, M. & PETIT, A. (1989). Characterization of angiotensin II binding sites in the human term placenta. Mol. Cell Endocrinol., 63, 111-119.
47. THEKKUMKARA, T.J., DU, J., DOSTAL, D.E., MOTEL, T.J., THOMAS, W.G. & BAKER, K.M. (1995). Stable expression of a functional rat angiotensin II (AT1A) receptor in CHO-K1 cells: rapid desensitization by angiotensin II. Mol. Cell. Biochem., 146, 79-89.
48. TIMMERMANS, P.B.M.W.M., WONG, P.C., CHIU, A.T. & HERBLIN, W.F. (1991). Nonpeptide angiotensin II receptor antagonists. Trends Pharmacol. Sci., 12, 55-62.
49. TIMMERMANS, P.B.M.W.M., WONG, P.C., CHIU, A.T., HERBLIN, W.F., BENFIELD, P., CARINI, D.J., LEE, R.J., WEXLER, R.R., SAYE, J.A.M. & SMITH, R.D. (1993). Angiotensin II receptors and angiotensin II receptor antagonists. Pharmacol. Rev., 45, 205-251.
50. TOBIN, A.B. & NAHORSKI, S.R. (1993). Rapid agonist-mediated phosphorylation of m3-muscarinic receptors revealed by immunoprecipitation. J. Biol. Chem., 268, 9817-9823.
51. WINTERSGILL, H.P., WARBURTON, P. BRYSON, S.E., BALL, S.G. & BALMFORTH, A.J. (1992). Characterisation of the angiotensin II receptor expressed by the human hepatoma cell line PLC-PRF-5. Eur. J. Pharmacol., 227, 283-291.