Regulation of the human bradykinin B2 receptor expressed in sf21 insect cells: A possible role for tyrosine kinases

Journal of Cellular Biochemistry

Volumn 76, Issue 4, 2000, Pages 658-673

  Reyes Cruz, Guadalupe ^a,c   Vázquez Prado, José ^a   Müller Esterl, Werner ^b   Vaca, Luis ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Human bradykinin receptor; Intracellular calcium; Receptor desensitization; Sf21 cells

Indexed keywords

BRADYKININ; BRADYKININ B2 RECEPTOR; CALCIUM; PROTEIN TYROSINE KINASE;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; DOSE RESPONSE; ENZYME ACTIVATION; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

ANIMALS; BACULOVIRIDAE; BRADYKININ; CALCIUM; CELL MEMBRANE; CELLS, CULTURED; GENE EXPRESSION; GENISTEIN; GTP-BINDING PROTEINS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HUMANS; MICROSCOPY, CONFOCAL; OCTOPAMINE; PHOSPHOAMINO ACIDS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; RECEPTOR, BRADYKININ B2; RECEPTORS, BRADYKININ; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; SPODOPTERA; THAPSIGARGIN; TYRPHOSTINS;

INSECTA; UNIDENTIFIED BACULOVIRUS;

EID: 0343938837     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4644(20000315)76:4<658::AID-JCB14>3.0.CO;2-7     Document Type: Article

References (59)

1. Abd Alla S, Buschko J, Quitterer U, Maidhof A, Haasemann M, Breipohl G, Knolle J, Müller-Esterl W. 1993. Structural features of the human bradykinin B2 receptor probed by agonists, antagonists, and anti-idiotypic antibodies. J Biol Chem 268:17277-17285.
2. Abd Alla S, Quitterer U, Grigoriev S, Maidhof A, Haasemann M, Jarnagin K, Müller-Esterl W. 1996. Extracellular domains of the bradykinin B2 receptor involved in ligand binding and agonist sensing defined by antipeptide antibodies. J Biol Chem 271:1748-1755.
3. Alblas J, Etten I van, Khanum A, Moolenaar WH. 1995. C-terminal truncation of the neurokinin-2 receptor causes enhanced and sustained agonist-induced signaling. Role of receptor phosphorylation in signal attenuation. J Biol Chem 270:8944-8951.
4. Alblas J, Etten IV, Moolenaar WH. 1996. Truncated desensitization-defective neurokinin receptors mediate sustained MAP kinase activation, cell growth and transformation by a Ras-independent mechanism. EMBO J 15: 3351-3360.
5. Babnigg G, Bowersox SR, Villereal ML. 1997. The role of pp60 c-src in the regulation of calcium entry via store-operated calcium channels. J Biol Chem 272:29434-29437.
6. Baenziger NL, Jong YJI, Yocum SA, Dalemar RL, Wilhelm B, Vavrek R, Stewart JM. 1992. Diversity of B2 bradykinin receptors with nanomolar affinity expressed in passaged IMR90 human lung fibroblasts. Eur J Cell Biol 58:71-80.
7. Barr AJ, Brass LF, Manning DR. 1997. Reconstitution of receptors and GTP-binding regulatory proteins (G proteins) in Sf9 cells. A direct evaluation of selectivity in receptor G protein coupling. J Biol Chem 272:2223-2294.
8. Beukers MW, Klaassen CH, De Grip WJ, Verzijl D, Timmerman H, Leurs R. 1997. Heterologous expression of rat epitope-tagged histamine H2 receptors in insect Sf9 cells. Br J Pharmacol 122:867-874.
9. Blaukat A, Alla SA, Lohse MJ, Müller-Esterl W. 1996. Ligand-induced phosphorylation/dephosphorylation of the endogenous bradykinin B2 receptor from human fibroblasts. J Biol Chem 271:32366-32374.
10. Boyle WJ, van der Geer P, Hunter T. 1991. Phosphopeptide mapping and phosphoaminoacid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol 201:110-149.
11. Cauzabon S, Parker PJ, Strosberg AD, Couraud PO. 1993. Endothelins stimulate tyrosine phosphorylation and activity of p42/mitogen-activated protein kinase in astrocytes. Biochem J 293:381-386.
12. Chen X, Earley K, Luo W, Lin SH, Schilling WP. 1996. Functional expression of a human thrombin receptor in Sf9 insect cells, evidence for an active tethered ligand. Biochem J 314 (Pt 2):603-611.
13. Chuang TT, Iacovelli L, Sallese M, De Blasi A. 1996. G protein-coupled receptors, heterologous regulation of homologous desensitization and its implications. Trends Pharmacol Sci 17:416-421.
14. Chuang TT, LeVine H III, De Blasi A. 1995. Phosphorylation and activation of beta-adrenergic receptor kinase by protein kinase C. J Biol Chem 270:18660-18665.
15. Clerk A, Gillespie-Brown J, Fuller SJ, Sugden PH. 1996. Stimulation of phosphatidylinositol hydrolysis, protein kinase C translocation, and mitogen-activated protein kinase activity by bradykinin in rat ventricular myocytes: dissociation from the hypertrophic response. Biochem J 317:109-118.
16. Cyr CR, Rudy B, Kris RM. 1993. Prolonged desensitization of the human endothelin A receptor in Xenopus oocytes. J Biol Chem 268:26071-26074.
17. Dalemar LR, Jong YJI, Wilhelm B, Baenziger NL. 1996. Protein kinases A and C rapidly modulate expression of human flbroblast B2 bradykinin receptor affinity forms. Eur J Cell Biol 69:236-244.
18. Denning MF, Dlugosz AA, Threadgill DW, Magnuson T, Yuspa SH. 1996. Activation of the epidermal growth factor receptor signal transduction pathway stimulates tyrosine phosphorylation of protein kinase C delta. J Biol Chem 271:5325-5331.
19. 1 MF-2 smooth muscle cells. J Biol Chem 272:17858-17866.
20. Dong Y, Kunze DL, Vaca L, Schilling WP. 1995. Ins(1,4,5)P3 activates Drosophila cation channel Trpl in recombinant baculovirus-infected Sf9 insect cells. Am J Physiol 269: C1332-C1339.
21. Falcone RC, Hubbs SJ, Vanderloo JD, Prosser JC, Little J, Gomes G, Aharony D, Krell RD. 1993. Characterization of bradykinin receptors in guinea pig gall bladder. J Pharmacol Exp Ther 266:1291-1299.
22. Fukushima Y, Asano T, Saitoh T, Anai M, Funaki M, Ogihara T, Katagiri H, Matsuhashi N, Yazaki Y, Sugano K. 1997. Oligomer formation of histamine H2 receptors expressed in Sf9 and COS-7 cells. FEBS Lett 409:283-286.
23. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
24. Hall JM. 1992. Bradykinin receptors: pharmacological properties and biological roles. J Pharmacol Ther 56:131-190.
25. Harteneck C, Obukhov AG, Zobel A, Kalkbrenner F, Schultz G. 1995. The Drosophila cation channel trpl expressed in insect Sf9 cells is stimulated by agonists of G-protein-coupled receptors. FEBS Lett 358:297-300.
26. Hasler WL, Kurosawa S, Takahashi T, Feng H, Gaginella TS, Owyang C. 1995. Bradykinin acting on B2 receptors contracts colon circular muscle cells by IP3 generation and adenylate cyclase inhibition. J Pharmacol Exp Ther 273:344-350.
27. Hu Y, Rajan L, Schilling WP. 1994. Ca2+ signaling in Sf9 insect cells and the functional expression of a rat brain M5 muscarinic receptor. Am J Physiol 266:C1736-C1643.
28. Humemori H, Inoue T, Kume S, Sekiyama N, Nagao M, Itoh H, Nakanishi S, Mikoshiba K, Yamamoto T. 1997. Activation of the G protein Gq/11 through tyrosine phosphorylation of the a subunit. Science 276:1878-1881.
29. Jong YJI, Dalemar LR, Wilhelm B, Baezinger NL. 1993. Human bradykinin B2 receptors isolated by receptor-specific monoclonal antibodies are tyrosine phosphorylated. Proc Natl Acad Sci USA 90:10994-10998.
30. Kenakin T. 1997. Differences between natural and recombinant G protein-coupled receptor systems with varying receptor/G protein stoichiometry. Trends Pharmacol Sci 12:456-464.
31. Kleymann G, Boege F, Hahn M, Hampe W, Vasudevan S, Reilander H. 1993. Human beta 2-adrenergic receptor produced in stably transformed insect cells is functionally coupled via endogenous GTP-binding protein to adenylyl cyclase. Eur J Biochem 213:797-804.
32. Kukkonen JP, Nasman J, Ojala P, Oker-Blom C, Akerman KE. 1996. Functional properties of muscarinic receptor subtypes Hm1, Hm3 and Hm5 expressed in Sf9 cells using the baculovirus expression system. J Pharmacol Exp Ther 279:593-601.
33. 2+ mobilization by muscarinic antagonists. Biochem Biophys Res Commun 243:41-46.
34. Kunze DL, Sinkins WG, Vaca L, Schilling WP. 1997. Properties of single Drosophila Trpl channels expressed in Sf9 insect cells. Am J Physiol 272:C27-C34.
35. FAK in bradykinin-stimulated fibroblasts. Am J Physiol 270 (Cell Physiol 39): C1430-C1437.
36. Lee KM, Toscas K, Villereal ML. 1993. Inhibition of bradykinin- and thapsigargin-induced Ca2+ entry by tyrosine kinase inhibitors. J Biol Chem 268:9945-9948.
37. Lefkowitz RJ, Cotecchia S, Kjelsberg MA, Pitcher J, Koch WJ, Inglese J, Caron MG. 1993. Adrenergic receptors: recent insights into their mechanism of activation and desensitization. Adv Second Messenger Phosphoprotein Res 28:1-9.
38. Leopoldt D, Harteneck C, Nurnberg B. 1997. G proteins endogenously expressed in Sf9 cells: interactions with mammalian histamine receptors. Naunyn Schmiedebergs Arch Pharmacol 356:216-224.
39. Luo H, Lindeman RP, Chase HS Jr. 1992. Participation of protein kinase C in desensitization to bradykinin and to carbachol in MDCK cells. Am J Physiol 262:F499-F506.
40. Nishimura K, Frederick J, Kwatra MM. 1998a. Human substance P receptor expressed in Sf9 cells couples with multiple endogenous G proteins. J Recept Signal Transduct Res 18:51-65.
41. Nishimura K, Warabi K, Roush ED, Frederick J, Schwinn DA, Kwatra MM. 1998b. Characterization of GRK2-catalyzed phosphorylation of the human substance P receptor in Sf9 membranes. Biochemistry 37:1192-1198.
42. O'Relly DR, Miller LK, Luckow UA. 1992. Baculovirus expression vectors: a laboratory manual. New York: Freeman.
43. Pizard A, Marchetti J, Allegrini J, Alhenc-Gelas F, Rajerison RM. 1998. Negative cooperativity in the human bradykinin B2 receptor. J Biol Chem 273:1309-1315.
44. Prado GN, Taylor L, Polgar P. 1997. Effects of intracellular tyrosine residue mutation and carboxyl terminus truncation on signal transduction and internalization of the rat bradykinin B2 receptor. J Biol Chem 272:14638-14642.
45. Regoli D, Jukic D, Gobeil F, Rhaleb NE. 1993. Receptor for bradykinin and related kinins: a critical analysis. Can J Physiol Pharmacol 71:556-567.
46. 2 subtypes. Life Sci 55:735-749.
47. Richardson RM, Hosey MM. 1992. Agonist-induced phosphorylation and desensitization of human m2 muscarinic cholinergic receptors in Sf9 insect cells. J Biol Chem 267:22249-22455.
48. Rodriguez-Fernandez JL, Rozengurt E. 1996. Bombesin, bradykinin, vasopressin and phorbol esters rapidly and transiently activate Src family tyrosine kinases in Swiss 3T3 cells. J Biol Chem 271:27895-27901.
49. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
50. Satoh M, Miyamoto C, Terashima H, Tachibana Y, Wada K, Watanabe T, Hayes AE, Gentz R, Furuichi Y. 1997. Human endothelin receptors ET(A) and ET(B) expressed in baculovirus-infected insect cells-direct application for signal transduction analysis. Eur J Biochem 249:803-811.
51. Schroeder C, Beug H, Müller-Esterl W. 1997. Cloning and functional characterization of the ornithokinin receptor. Recognition of the major kinin receptor antagonist, HOE140, as a full agonist. J Biol Chem 272:12475-12481.
52. Sharif NA, Whiting RL. 1993. The neuropeptide bradykinin stimulates phosphoinositide turnover in HSDM1C1 cells: B2-antagonist-sensitive responses and receptor binding studies. Neurochem Res 18:1313-1320.
53. Soskic V, Nyakatura E, Roos M, Müller-Esterl W, Godovac-Zimmermann J. 1999. Correlations in palmitoylation and multiple phosphorylation of rat bradykinin B2 receptor in Chinese hamster ovary cells. J Biol Chem 274:8539-8545.
54. Taketo M, Yokoyama S, Kimura Y, Higashida H. 1997. Ca2+ release and Ca2+ influx in Chinese hamster ovary cells expressing the cloned mouse B2 bradykinin receptor: tyrosine kinase inhibitor-sensitive and -insensitive processes. Biochim Biophys Acta 1355:89-98.
55. Trogadis JE, Ng GY, O'Dowd BF, George SR, Stevens JK. 1995. Dopamine D1 receptor distribution in Sf9 cells imaged by confocal microscopy: a quantitative evaluation. J Histochem Cytochem 43:497-506.
56. Vaca L, Kunze DL. 1994. Depletion of intracellular Ca2+ stores activates a Ca(2-)-selective channel in vascular endothelium. Am J Physiol 267:C920-C925.
57. 1b-adrenoreceptors in rat-1 fibroblasts. J Biol Chem 272:27330-27333.
58. Wieland T, Jakobs KH. 1994. Measurement of receptor-stimulated guanosine 5′-O-(-γ-thio)triphosphate binding by G proteins. Methods Enzymol 237:3-12.
59. Zang Q, Lu Z, Curto M, Barile X, Shalloway D, Foster DA. 1997. Association between v-Src and protein kinase C delta in v-Src-transformed fibroblasts. J Biol Chem 272: 13275-13280.