Regulation of tyrosine kinase cascades by G-protein-coupled receptors

Current Opinion in Cell Biology

Volumn 11, Issue 2, 1999, Pages 177-183

  Luttrell, Louis M ^a   Daaka, Yehia ^a   Lefkowitz, Robert J ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CLATHRIN; GUANINE NUCLEOTIDE BINDING PROTEIN; INTEGRIN; PROTEIN TYROSINE KINASE; RAS PROTEIN; RECEPTOR;

DESENSITIZATION; ENZYME REGULATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; TRANSACTIVATION;

EID: 0032938716     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(99)80023-4     Document Type: Article

References (56)

1. Dhanasekaran N., Heasley L.E., Johnson G.L. G protein-coupled receptor systems involved in cell growth and oncogenesis. Endocrinol Rev. 16:1995;259-270.
2. van Biesen T., Luttrell L.M., Hawes B.E., Lefkowitz R.J. Mitogenic signaling via G protein-coupled receptors. Endocrinol Rev. 17:1996;698-714.
3. Gutkind J.S. The pathways connecting G protein-coupled receptors to the nucleus through divergent mitogen-activated protein kinase cascades. J Biol Chem. 273:1998;1839-1842.
4. Crespo P., Xu N., Simonds W.F., Gutkind J.S. Ras-dependent activation of MAP kinase pathway mediated by G-protein βγ subunits. Nature. 369:1994;418-420.
5. ras. Proc Natl Acad Sci USA. 91:1994;12706-12710.
6. ras by β2-adrenergic receptors expressed in fibroblasts. J Biol Chem. 268:1993;22235-22238.
7. van Corven E.J., Hordijk P.L., Medema R.H., Bos J.L., Moolenaar W.H. Pertussis toxin-sensitive activation of p21ras by G protein-coupled receptor agonists in fibroblasts. Proc Natl Acad Sci USA. 90:1993;1257-1261.
8. Winitz S., Russell M., Qian N.X., Gardner A., Dwyer L., Johnson G.L. Involvement of Ras and Raf in the Gi-coupled acetylcholine muscarinic m2 receptor activation of mitogen-activated protein (MAP) kinase kinase and MAP kinase. J Biol Chem. 268:1993;19196-19199.
9. van Biesen T., Hawes B.E., Luttrell D.K., Krueger K.M., Touhara K., Porfiri E., Sakaue M., Luttrell L.M., Lefkowitz R.J. Receptor-tyrosine-kinase- and Gβγ-mediated MAP kinase activation by a common signalling pathway. Nature. 376:1995;781-784.
10. Cazaubon S.M., Ramos-Morales F., Schweighoffer F., Strosberg A.D., Couraud P-O. Endothelin induces tyrosine phosphorylation and GRB2 association of Shc in astyrocytes. J Biol Chem. 269:1994;24805-24809.
11. Ohmichi M., Sawada T., Kanda Y., Koike K., Hirota K., Miyake A., Saltiel A.R. Thyrotropin-releasing hormone stimulates MAP kinase activity in GH3 cells by divergent pathways. J Biol Chem. 269:1994;3783-3788.
12. Chen Y-H., Gral D., Salcini A.E., Pelicci P.G., Pouyssegur J., Van Obberghen-Schilling E. Shc adaptor proteins are key transducers of mitogenic signaling mediated by the G protein-coupled thrombin receptor. EMBO J. 15:1996;1037-1044.
13. Sadoshima J., Izumo S. The heterotrimeric Gq protein-coupled angiotensin II receptor activates p21 ras via the tyrosine kinase-Shc-Grb2-Sos pathway in cardiac myocytes. EMBO J. 15:1996;775-787.
14. q-coupled receptor-mediated transactivation of EGF receptors in several cell types. It demonstrates that the EGF receptor-specific tyrphostin AG1478 (a pharmological tyrosine protein kinase inhibitor which binds to the substrate binding site of the kinase) blocks GPCR-stimulated EGF receptor Shc and Gab1 tyrosine phosphorylation, and ERK activation. The Src kinase inhibitor PP1 is also found to strongly inhibit LPA-stimulated signaling downstream of the transactivated EGF receptor.
15. Linseman D.A., Benjamin C.W., Jones D.A. Convergence of angiotensin II and platelet-derived growth factor receptor signaling cascades in vascular smooth muscle cells. J Biol Chem. 270:1995;12563-12568.
16. Daub H., Weiss F.U., Wallasch C., Ullrich A. Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature. 379:1996;557-560.
17. Rao G.N., Delafontaine P., Runge M.S. Thrombin stimulates phosphorylation of insulin-like growth factor-1 receptor, insulin receptor substrate-1, and phospholipase C-gamma 1 in rat aortic smooth muscle cells. J Biol Chem. 270:1995;27871-27875.
18. Luttrell L.A., Hawes B.E., Van Biesen T., Luttrell D.K., Lonsing T.J., Lefkowitz R.J. Role of c-Src tyrosine kinase in G protein-coupled receptor- and Gβγ subunit mediated activation of mitogen-activated protein kinases. J Biol Chem. 271:1996;19443-19450.
19. Herrich A., Daub H., Knebel A., Herrlich P., Ullrich A., Schultz G., Gudermann T. Ligand-independent activation of platelet-derived growth factor receptor is a necessary intermediate in lysophosphatidic acid-stimulated mitogenic activity in L cells. Proc Natl Acad Sci USA. 95:1998;8985-8990. This paper reports that crosstalk between GPCRs and RTKs is a general phenomenon, whereby multiple RTK species may be recruited to transduce GPCR signals. Using tyrphostins to specifically inhibit EGF and PDGF receptor catalytic activity, the authors find that in L cells, which lack endogenous EGF receptors, LPA-induced Shc phosphorylation and ERK activation proceed via transactivation of PDGF receptors. Conversely, in COS-7 cells, which lack endogenous PDGF receptors, EGF receptor transactivation is required. The transactivation signals are independent of PKC activity.
20. Luttrell L.M., Della Rocca G.J., van Biesen T., Luttrell D.K., Lefkowitz R.J. Gβγ subunits mediate Src-dependent phosphorylation of the epidermal growth factor receptor. J Biol Chem. 272:1997;4637-4644. This paper reports that LPA- and β2A-adrenergic receptor stimulation induces tyrosine phosphorylation of EGF receptor and Shc, and formation of a complex containing EGF receptor Shc, Grb2, and c-Src. Transient overexpression of Gβγ subunits mimics the effects of GPCR stimulation. Inhibition of Src activity by expression of either Csk or a catalytically inactive mutant of c-Src inhibits complex assembly.
21. Hawes B.E., van Biesen T., Koch W.J., Luttrell L.M., Lefkowitz R.J. Distinct pathways of Gi- and Gq-mediated mitogen-activated protein kinase activation. J Biol Chem. 270:1995;17148-17153.
22. Faure M., Voyno-Yasenetskaya T.A., Bourne H.R. cAMP and βγ subunits of heterotrimeric G proteins stimulate the mitogen-activated protein kinase pathway in COS-7 cells. J Biol Chem. 269:1994;7851-7854.
23. Hawes B.E., Luttrell L.M., van Biesen T., Lefkowitz R.J. Phosphatidylinositol 3-kinase is an early intermediate in the Gβγ-mediated mitogen-activated protein kinase signaling pathway. J Biol Chem. 271:1996;12133-12136.
24. Lopez-Ilasaca M., Crespo P., Pellici P.G., Gutkind J.S., Wetker R. Linkage of G protein coupled receptors to the MAPK signaling pathway through PI 3-kinase? Science. 275:1997;394-397. This paper reports that overexpression of the G-protein-regulated γ isoform of P13K, but not of the RTK-regulated α isoform, constitutively activates the ERK cascade in COS-7 cells, whereas a catalytically inactive P13K γ mutant blocks ERK activation mediated by the m2 muscarinic receptor or the Gβγ subunits.
25. Chen Y-H., Pouyssegur J., Courtneidge S.A., Van Obberghen-Schilling E. Activation of Src family kinase activity by the G protein-coupled thrombin receptor in growth-responsive fibroblasts. J Biol Chem. 269:1994;27372-27377.
26. Ishida M., Marrero M.B., Schieffer B., Ishida T., Bernstein K., Berk B.C. Angiotensin II activates pp60c-src in vascular smooth muscle cells. Circ Res. 77:1995;1053-1059.
27. Ptasznik A., Traynor-Kaplan A., Bokoch G.M. G protein-coupled chemoattractant receptors regulate Lyn tyrosine kinase Shc adapter protein signaling complexes. J Biol Chem. 270:1995;19969-19973.
28. Eguchi S., Numaguchi K., Iwasaki H., Matsumoto T., Yamakawa T., Utsunomiya H., Motley E.D., Owada K.M., Hirata Y., Marumo F., Inagami T. Calcium-dependent epidermal growth factor receptor transactivation mediates the angiotensin II-induced mitogen-activated protein kinase activation in vascular smooth muscle cells. J Biol Chem. 273:1998;8890-8896. This paper finds that both angiotensin stimulation and calcium ionophore treatment result in EGF receptor phosphorylation and EGF receptor-dependent ERK activation in rat vascular smooth muscle cells. Angiotensin stimulation results in association of activated c-Src with EGF receptor which is not affected by the EGF receptor kinase inhibitor tyrphostin AG1478, suggesting that AT1 receptor-mediated Src activation may precede EGF receptor transactivation.
29. Tsai W., Morielli A.D., Peralta E.G. The m1 muscarinic acetylcholine receptor transactivates the EGF receptor to modulate ion channel activity. EMBO J. 16:1997;4597-4605.
30. Schlaepfer D.D., Hunter T. Signal transduction from the extracellular matrix. A role for the focal adhesion protein-tyrosine kinase FAK. Cell Struct Funct. 21:1996;445-450.
31. 2+ mobilization, and the actin cytoskeleton. J Biol Chem. 268:1993;14262-14268.
32. Hordijk P.L., Verlaan I., van Corven E.J., Moolenaar W.H. Protein tyrosine phosphorylation induced by lysophosphatidic acid in Rat-1 fibroblasts. J Biol Chem. 269:1994;645-651.
33. Rodriguez-Fernandez J.L., Rozengurt E. Bombesin, vasopressin, lysophosphatidic acid, and sphingosylphosphorylcholine induce focal adhesion kinase activation in intact Swiss 3T3 cells. J Biol Chem. 273:1998;19321-19328. This paper demonstrates rapid GPCR-mediated activation of p125FAK in Swiss 3T3 cells. The GPCR signal is not dependent upon either PKC activity or calcium mobilization, but is blocked both by cytochalasin D treatment and by placing the cells in suspension. These data indicate that GPCR signaling via focal adhesion complexes requires cell adhesion as a costimulatory event.
34. •], the m3 receptor signal is sensitive to inhibition of PKC.
35. Rodriguez-Fernandez J.L., Rozengurt E. Bombesin, bradykinin, vasopressin and phorbol esters rapidly and transiently activate Src family tyrosine kinases in Swiss 3T3 cells. J Biol Chem. 271:1996;27895-27901.
36. Luttrell L.M., Daaka Y., Della Rocca G.J., Lefkowitz R.J. G protein coupled receptors mediate two functionally distinct pathways of tyrosine phosphorylation in Rat 1a fibroblasts. J Biol Chem. 272:1997;31648-31656. This paper demonstrates that ERK activation mediated by LPA, thrombin and bombesin receptors is dissociated from p125FAK phosphorylation in Rat 1 fibroblasts. FAK phosphorylation is mediated by pertussis-toxin-insensitive G-proteins and is sensitive to cytochalasin D treatment, whereas ERK activation is mediated by pertussis-toxin-sensitive G-proteins and is blocked by inhibitors of clathrin-mediated endocytosis.
37. Lev S., Moreno H., Martinez R., Canoll P., Peles E., Musacchio J.M., Plowman G.D., Rudy B., Schlessinger J. Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature. 376:1995;737-745.
38. •].
39. •] examine the activation mechanism of CADTK (a PYK2 homologue) in vascular smooth muscle and of a CADTK splice variant in monocytes. In both systems, CADTK activation is found to require both cell adhesion and a secondary calcium- or PKC-dependent signal, such as that triggered by angiotensin or chemokine receptor activation, thapsigargin, or phorbol ester.
40. Zheng C., Xing Z., Bian Z.C., Guo C., Akbay A., Warner L., Guan J.L. Differential regulation of Pyk2 and focal adhesion kinase (FAK). The C-terminal domain of FAK confers response to cell adhesion. J Biol Chem. 273:1998;2384-2389. Using Pyk2/p125FAK chimeric proteins, this paper identifies the carboxy-terminal region of Pyk2 as that part of the protein which is responsible for differential regulation of the two kinases by integrins and soluble stimuli. Unlike p125FAK, Pyk2 is found to be predominantly cytosolic in distribution, becoming phosphorylated and associated with focal adhesions in response to elevation of intracellular calcium levels.
41. Dikic I., Dikic I., Schlessinger J. Identification of a new Pyk2 isoform implicated in chemokine and antigen receptor signaling. J Biol Chem. 273:1998;14301-14308.
42. Dikic I., Tokiwa G., Lev S., Courtneidge S.A., Schlessinger J. A role for PYK2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature. 383:1996;547-550.
43. Freedman N.J., Lefkowitz R.J. Desensitization of G protein-coupled receptors. Recent Prog Hormone Res. 51:1996;319-353.
44. Lefkowitz R.J. G protein-coupled receptors. III. New roles for receptor kinases and β-arrestins in receptor signaling and desensitization. J Biol Chem. 273:1998;18677-18680.
45. Ferguson S.S.G., Downey W.E. III, Colapietro A-M., Barak L.S., Menard L., Caron M.G. Role of β-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science. 271:1996;363-366.
46. Goodman O.B., Krupnick J.G., Santini F., Gurevich V.V., Penn R.B., Gagnon A.W., Keen J.H., Benovic J.L. β-arrestin acts as a clathrin adaptor in endocytosis of the β2-adrenergic receptor. Nature. 383:1996;447-450.
47. Okamoto T., Murayama Y., Hayashi Y., Inagaki M., Ogata E., Nishimoto I. Identification of a Gs activator region of the β2-adrenergic receptor that is autoregulated via protein kinase A-dependent phosphorylation. Cell. 67:1991;723-730.
48. i. Activation of the ERK cascade is mediated via 'desensitized' β2-adrenergic receptors acting upon pertussis-toxin-sensitive G-proteins.
49. Vieira A.V., Lamaze C., Schmid S.L. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science. 274:1997;2086-2089. This paper demonstrates a role for clathrin-mediated endocytosis in some aspects of EGF receptor signaling. HeLa cells expressing a dominant-negative mutant of dynamin fail to internalize receptor in response to agonist. These cells exhibit reduced EGF-stimulated EGF receptor, PI3K, and ERK1 phosphorylation, but enhanced Shc and PLCγ phosphorylation.
50. Chow J.C., Condorelli G., Smith R.J. Insulin-like growth factor-I receptor internalization regulates signaling via the Shc/mitogen-activated protein kinase pathway, but not the insulin receptor substrate-1 pathway. J Biol Chem. 273:1998;4672-4680. Using low temperature and dansylcadaverine to inhibit IGF-1 receptor endocytosis, this paper shows that the ability of IGF-1 receptors to induce Shc phosphorylation and MAPK activation are dependent upon receptor internalization. In contrast, IGF-1 receptor signaling via insulin receptor substrate 1 (IRS-1) phosphorylation to PI3K is independent of receptor endocytosis.
51. Daaka Y., Luttrell L.M., Ahn S., Della Rocca G.J., Ferguson S.S.G., Caron M.G., Lefkowitz R.J. Essential role for G protein-coupled receptor endcytosis in the activation of MAP kinase. J Biol Chem. 273:1998;685-688. This paper reports that receptor endocytosis is required for signaling from β2 adrenergic receptors to ERKs. Inhibition of β2 adrenergic receptor sequestration using dominant-negative mutants of β-arrestin and dynamin blocks receptor endocytosis and ERK activation, without affecting G-protein coupling. β2 adrenergic receptor stimulated Shc phosphorylation and Raf activation are unaffected by the sequestration inhibitors, suggesting that endocytosis is required for signaling between Raf and MEK.
52. Pellegrini S., Dusanter-Fourt I. The structure, regulation and function of the Janus kinases (JAKs) and the signal transducers and activators of transcription (STATs). Eur J Biochem. 248:1997;615-633.
53. Marrero M.B., Schieffer B., Paxton W.C., Heerdt L., Berk B.C., Delafontaine P., Bernstein K.E. Direct stimulation of Jak/STAT pathway by the angiotensin II AT1 receptor. Nature. 375:1995;247-250.
54. Ali M.S., Sayeski P.P., Dirksen L.B., Hayzer D.J., Marrero M.B., Bernstein K.B. Dependence on the motif YIPP for the physical association of Jak2 kinase with the intracellular carboxyl tail of the angiotensin II AT1 receptor. J Biol Chem. 272:1997;23382-23388. This paper identifies the motif Tyr-Ile-Pro-Pro in the carboxyl tail of the AT1A receptor as the site of direct interaction between the receptor and JAK2. A mutant receptor lacking the motif is unable to activate JAK2. These data suggest that GPCRs can regulate tyrosine phosphorylation by physically associating with nonreceptor tyrosine kinases.
55. Luttrell L.M., Ferguson S.S.G., Daaka Y., Miller W.E., Maudsley S., Della Rocca G.J., Lin F-T., Kawakatsu H., Owada K., Luttrell D.K.et al. β-arrestin-dependent formation of β2 adrenergic receptor/Src protein kinase complexes. Science. 283:1999;655-661. This paper demonstrates that β-arrestins function as adaptor proteins, binding both agonist-occupied β2 adrenergic receptors and Src kinases, thus permitting the receptor to acquire agonist-regulated tyrosine kinase activity. β-arrestin mutants which are impaired in either Src binding or in clathrin-targeting inhibit β2 adrenergic receptor activation of ERKs, suggesting that both Src recruitment and receptor endocytosis are necessary for signal transduction.
56. Anderson R.G.W. The caveolae membrane system. Annu Rev Biochem. 67:1998;199-225.