Engagement of β-arrestin by transactivated insulin-like growth factor receptor is needed for V2 vasopressin receptor-stimulated ERK1/2 activation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 17, 2012, Pages

  Oligny Longpré, Geneviève ^a   Corbani, Maithé ^b   Zhou, Joris ^a   Hogue, Mireille ^a   Guillon, Gilles ^b   Bouvier, Michel ^a  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

Author keywords

Cell signalling; MAPK; Paracrine factor; Protein protein interactions

Indexed keywords

BETA ARRESTIN; GUANINE NUCLEOTIDE BINDING PROTEIN; METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SOMATOMEDIN RECEPTOR; TYROSINE KINASE RECEPTOR; VASOPRESSIN V2 RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; COMPLEX FORMATION; ENZYME ACTIVATION; ENZYME ACTIVITY; KIDNEY MEDULLA; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ARRESTINS; CELLS, CULTURED; ENZYME ACTIVATION; KIDNEY MEDULLA; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; RATS; RECEPTORS, SOMATOMEDIN; RECEPTORS, VASOPRESSIN; TRANSCRIPTIONAL ACTIVATION;

EID: 84860159281     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1112422109     Document Type: Article

References (76)

1. Charest PG, Bouvier M (2003) Palmitoylation of the V2 vasopressin receptor carboxyl tail enhances beta-arrestin recruitment leading to efficient receptor endocytosis and ERK1/2 activation. J Biol Chem 278:41541-41551. (Pubitemid 37280984)
2. Tohgo A, et al. (2003) The stability of the G protein-coupled receptor-beta-arrestin interaction determines the mechanism and functional consequence of ERK activation. J Biol Chem 278:6258-6267. (Pubitemid 36800882)
3. Charest PG, Oligny-Longpré G, Bonin H, Azzi M, Bouvier M (2007) The V2 vasopressin receptor stimulates ERK1/2 activity independently of heterotrimeric G protein signalling. Cell Signal 19:32-41. (Pubitemid 44880240)
4. Werry TD, Sexton PM, Christopoulos A (2005) "Ins and outs" of seven-transmembrane receptor signalling to ERK. Trends Endocrinol Metab 16:26-33. (Pubitemid 40037724)
5. Wetzker R, Böhmer FD (2003) Transactivation joins multiple tracks to the ERK/MAPK cascade. Nat Rev Mol Cell Biol 4:651-657. (Pubitemid 36934967)
6. Prenzel N, et al. (1999) EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402: 884-888.
7. Oak JN, Lavine N, Van Tol HH (2001) Dopamine D(4) and D(2L) receptor stimulation of the mitogen-activated protein kinase pathway is dependent on trans-activation of the platelet-derived growth factor receptor. Mol Pharmacol 60:92-103. (Pubitemid 32595237)
8. Tsuchioka M, Takebayashi M, Hisaoka K, Maeda N, Nakata Y (2008) Serotonin (5-HT) induces glial cell line-derived neurotrophic factor (GDNF) mRNA expression via the transactivation of fibroblast growth factor receptor 2 (FGFR2) in rat C6 glioma cells. J Neurochem 106:244-257. (Pubitemid 351840206)
9. Korzh A, Keren O, Gafni M, Bar-Josef H, Sarne Y (2008) Modulation of extracellular signal-regulated kinase (ERK) by opioid and cannabinoid receptors that are expressed in the same cell. Brain Res 1189:23-32.
10. El Zein N, Badran BM, Sariban E (2007) The neuropeptide pituitary adenylate cyclase activating protein stimulates human monocytes by transactivation of the Trk/NGF pathway. Cell Signal 19:152-162. (Pubitemid 44880250)
11. Keely SJ, Calandrella SO, Barrett KE (2000) Carbachol-stimulated transactivation of epidermal growth factor receptor and mitogen-activated protein kinase in T(84) cells is mediated by intracellular ca(2+), PYK-2, and p60(src). J Biol Chem 275: 12619-12625. (Pubitemid 30241410)
12. Biscardi JS, et al. (1999) c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J Biol Chem 274:8335-8343.
13. Drube S, Stirnweiss J, Valkova C, Liebmann C (2006) Ligand-independent and EGF receptor-supported transactivation: Lessons from beta2-adrenergic receptor signalling. Cell Signal 18:1633-1646. (Pubitemid 44216121)
14. Maudsley S, et al. (2000) The beta(2)-adrenergic receptor mediates extracellular signal-regulated kinase activation via assembly of a multi-receptor complex with the epidermal growth factor receptor. J Biol Chem 275:9572-9580. (Pubitemid 30185188)
15. DeFea KA, et al. (2000) Beta-arrestin-dependent endocytosis of proteinase-activated receptor 2 is required for intracellular targeting of activated ERK1/2. J Cell Biol 148: 1267-1281.
16. Luttrell LM, et al. (2001) Activation and targeting of extracellular signal-regulated kinases by beta-arrestin scaffolds. Proc Natl Acad Sci USA 98:2449-2454. (Pubitemid 32209502)
17. Buchanan FG, et al. (2006) Role of beta-arrestin 1 in the metastatic progression of colorectal cancer. Proc Natl Acad Sci USA 103:1492-1497. (Pubitemid 43191193)
18. Luttrell LM, et al. (1999) Beta-arrestin-dependent formation of beta2 adrenergic receptor-Src protein kinase complexes. Science 283:655-661.
19. DeFea KA, et al. (2000) The proliferative and antiapoptotic effects of substance P are facilitated by formation of a beta-arrestin-dependent scaffolding complex. Proc Natl Acad Sci USA 97:11086-11091.
20. Dalle S, Ricketts W, Imamura T, Vollenweider P, Olefsky JM (2001) Insulin and insulin-like growth factor I receptors utilize different G protein signaling components. J Biol Chem 276:15688-15695.
21. Hupfeld CJ, Olefsky JM (2007) Regulation of receptor tyrosine kinase signaling by GRKs and beta-arrestins. Annu Rev Physiol 69:561-577. (Pubitemid 46457655)
22. Rakhit S, Pyne S, Pyne NJ (2001) Nerve growth factor stimulation of p42/p44 mitogen-activated protein kinase in PC12 cells: Role of G(i/o), G protein-coupled receptor kinase 2, beta-arrestin I, and endocytic processing. Mol Pharmacol 60:63-70. (Pubitemid 32595234)
23. Girnita L, et al. (2007) Beta-arrestin and Mdm2 mediate IGF-1 receptor-stimulated ERK activation and cell cycle progression. J Biol Chem 282:11329-11338. (Pubitemid 47100796)
24. Povsic TJ, Kohout TA, Lefkowitz RJ (2003) Beta-arrestin1 mediates insulin-like growth factor 1 (IGF-1) activation of phosphatidylinositol 3-kinase (PI3K) and anti-apoptosis. J Biol Chem 278:51334-51339. (Pubitemid 38020372)
25. Sachdev D, Hartell JS, Lee AV, Zhang X, Yee D (2004) A dominant negative type I insulin-like growth factor receptor inhibits metastasis of human cancer cells. J Biol Chem 279:5017-5024. (Pubitemid 38199098)
26. Peterson JE, et al. (1996) Src phosphorylates the insulin-like growth factor type I receptor on the autophosphorylation sites. Requirement for transformation by src. J Biol Chem 271:31562-31571. (Pubitemid 26408616)
27. Hernández-Sánchez C, Blakesley V, Kalebic T, Helman L, LeRoith D (1995) The role of the tyrosine kinase domain of the insulin-like growth factor-I receptor in intracellular signaling, cellular proliferation, and tumorigenesis. J Biol Chem 270:29176-29181.
28. Schäfer B, Gschwind A, Ullrich A (2004) Multiple G-protein-coupled receptor signals converge on the epidermal growth factor receptor to promote migration and invasion. Oncogene 23:991-999. (Pubitemid 38250945)
29. Rozengurt E (2007) Mitogenic signaling pathways induced by G protein-coupled receptors. J Cell Physiol 213:589-602.
30. Biscardi JS, Ishizawar RC, Silva CM, Parsons SJ (2000) Tyrosine kinase signalling in breast cancer: Epidermal growth factor receptor and c-Src interactions in breast cancer. Breast Cancer Res 2:203-210. (Pubitemid 32223586)
31. Kim LC, Song L, Haura EB (2009) Src kinases as therapeutic targets for cancer. Nat Rev Clin Oncol 6:587-595.
32. Boney CM, Sekimoto H, Gruppuso PA, Frackelton AR, Jr. (2001) Src family tyrosine kinases participate in insulin-like growth factor I mitogenic signaling in 3T3-L1 cells. Cell Growth Differ 12:379-386. (Pubitemid 32685639)
33. Lieskovska J, Ling Y, Badley-Clarke J, Clemmons DR (2006) The role of Src kinase in insulin-like growth factor-dependent mitogenic signaling in vascular smooth muscle cells. J Biol Chem 281:25041-25053. (Pubitemid 44401892)
34. DeWire SM, Ahn S, Lefkowitz RJ, Shenoy SK (2007) Beta-arrestins and cell signaling. Annu Rev Physiol 69:483-510.
35. Galandrin S, et al. (2008) Conformational rearrangements and signaling cascades involved in ligand-biased mitogen-activated protein kinase signaling through the beta1-adrenergic receptor. Mol Pharmacol 74:162-172. (Pubitemid 351872167)
36. Lin FT, Daaka Y, Lefkowitz RJ (1998) Beta-arrestins regulate mitogenic signaling and clathrin-mediated endocytosis of the insulin-like growth factor I receptor. J Biol Chem 273:31640-31643. (Pubitemid 29177090)
37. Oakley RH, Laporte SA, Holt JA, Barak LS, Caron MG (1999) Association of betaarrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J Biol Chem 274:32248-32257.
38. Barak LS, Oakley RH, Laporte SA, Caron MG (2001) Constitutive arrestin-mediated desensitization of a human vasopressin receptor mutant associated with nephrogenic diabetes insipidus. Proc Natl Acad Sci USA 98:93-98. (Pubitemid 32095869)
39. Oakley RH, Laporte SA, Holt JA, Barak LS, Caron MG (2001) Molecular determinants underlying the formation of stable intracellular G protein-coupled receptor-beta-arrestin complexes after receptor endocytosis*. J Biol Chem 276:19452-19460.
40. Alonso G, et al. (2009) Sustained elevated levels of circulating vasopressin selectively stimulate the proliferation of kidney tubular cells via the activation of V2 receptors. Endocrinology 150:239-250.
41. Daub H, Weiss FU, Wallasch C, Ullrich A (1996) Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379:557-560. (Pubitemid 26049585)
42. Rao GN, Delafontaine P, Runge MS (1995) 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 270:27871-27875.
43. Spartà A, Baiula M, Campbell G, Spampinato S (2010) beta-Arrestin 2-mediated heterologous desensitization of IGF-IR by prolonged exposure of SH-SY5Y neuroblastoma cells to a mu opioid agonist. FEBS Lett 584:3580-3586.
44. Tu H, et al. (2010) GABAB receptor activation protects neurons from apoptosis via IGF- 1 receptor transactivation. J Neurosci 30:749-759.
45. Zahradka P, Litchie B, Storie B, Helwer G (2004) Transactivation of the insulin-like growth factor-I receptor by angiotensin II mediates downstream signaling from the angiotensin II type 1 receptor to phosphatidylinositol 3-kinase. Endocrinology 145: 2978-2987. (Pubitemid 38686247)
46. Gschwind A, Hart S, Fischer OM, Ullrich A (2003) TACE cleavage of proamphiregulin regulates GPCR-induced proliferation and motility of cancer cells. EMBO J 22: 2411-2421. (Pubitemid 36604980)
47. Li X, et al. (2000) PDGF-C is a new protease-activated ligand for the PDGF alpha-receptor. Nat Cell Biol 2:302-309.
48. Bergsten E, et al. (2001) PDGF-D is a specific, protease-activated ligand for the PDGF beta-receptor. Nat Cell Biol 3:512-516. (Pubitemid 32422089)
49. Bunn RC, Fowlkes JL (2003) Insulin-like growth factor binding protein proteolysis. Trends Endocrinol Metab 14:176-181. (Pubitemid 36733903)
50. Byun D, et al. (2001) Pregnancy-associated plasma protein-A accounts for the insulin-like growth factor (IGF)-binding protein-4 (IGFBP-4) proteolytic activity in human pregnancy serum and enhances the mitogenic activity of IGF by degrading IGFBP-4 in vitro. J Clin Endocrinol Metab 86:847-854. (Pubitemid 32207505)
51. Lawrence JB, et al. (1999) The insulin-like growth factor (IGF)-dependent IGF binding protein-4 protease secreted by human fibroblasts is pregnancy-associated plasma protein-A. Proc Natl Acad Sci USA 96:3149-3153. (Pubitemid 29148859)
52. Boldt HB, Conover CA (2007) Pregnancy-associated plasma protein-A (PAPP-A): A local regulator of IGF bioavailability through cleavage of IGFBPs. Growth Horm IGF Res 17: 10-18.
53. Yan X, Baxter RC, Firth SM (2010) Involvement of pregnancy-associated plasma protein-A2 in insulin-like growth factor (IGF) binding protein-5 proteolysis during pregnancy: A potential mechanism for increasing IGF bioavailability. J Clin Endocrinol Metab 95:1412-1420.
54. Hemers E, et al. (2005) Insulin-like growth factor binding protein-5 is a target of matrix metalloproteinase-7: Implications for epithelial-mesenchymal signaling. Cancer Res 65:7363-7369. (Pubitemid 41161269)
55. Imai Y, et al. (1997) Protease-resistant form of insulin-like growth factor-binding protein 5 is an inhibitor of insulin-like growth factor-I actions on porcine smooth muscle cells in culture. J Clin Invest 100:2596-2605. (Pubitemid 27514900)
56. Schäfer B, Marg B, Gschwind A, Ullrich A (2004) Distinct ADAM metalloproteinases regulate G protein-coupled receptor-induced cell proliferation and survival. J Biol Chem 279:47929-47938. (Pubitemid 39540944)
57. Fischer OM, Hart S, Gschwind A, Ullrich A (2003) EGFR signal transactivation in cancer cells. Biochem Soc Trans 31:1203-1208. (Pubitemid 38030939)
58. Ohtsu H, Dempsey PJ, Eguchi S (2006) ADAMs as mediators of EGF receptor transactivation by G protein-coupled receptors. Am J Physiol Cell Physiol 291:C1-C10.
59. Masuda S, et al. (2003) Involvement of the V2 receptor in vasopressin-stimulated translocation of placental leucine aminopeptidase/ oxytocinase in renal cells. Eur J Biochem 270:1988-1994. (Pubitemid 36560820)
60. Nyalendo C, et al. (2007) Src-dependent phosphorylation of membrane type I matrix metalloproteinase on cytoplasmic tyrosine 573: Role in endothelial and tumor cell migration. J Biol Chem 282:15690-15699. (Pubitemid 47093303)
61. Suzuki A, et al. (2000) Meltrin alpha cytoplasmic domain interacts with SH3 domains of Src and Grb2 and is phosphorylated by v-Src. Oncogene 19:5842-5850. (Pubitemid 32005364)
62. Poghosyan Z, et al. (2002) Phosphorylation-dependent interactions between ADAM15 cytoplasmic domain and Src family protein-tyrosine kinases. J Biol Chem 277:4999-5007. (Pubitemid 34968539)
63. Pierce KL, et al. (2001) Epidermal growth factor (EGF) receptor-dependent ERK activation by G protein-coupled receptors: A co-culture system for identifying intermediates upstream and downstream of heparin-binding EGF shedding. J Biol Chem 276:23155-23160.
64. Girnita L, et al. (2005) beta-Arrestin is crucial for ubiquitination and down-regulation of the insulin-like growth factor-1 receptor by acting as adaptor for the MDM2 E3 ligase. J Biol Chem 280:24412-24419. (Pubitemid 40934525)
65. Palmitessa A, Benovic JL (2010) Arrestin and the multi-PDZ domain-containing protein MPZ-1 interact with phosphatase and tensin homolog (PTEN) and regulate Caenorhabditis elegans longevity. J Biol Chem 285:15187-15200.
66. Kara E, et al. (2006) A phosphorylation cluster of five serine and threonine residues in the C-terminus of the follicle-stimulating hormone receptor is important for desensitization but not for beta-arrestin-mediated ERK activation. Mol Endocrinol 20:3014-3026. (Pubitemid 44833552)
67. Ren XR, et al. (2005) Different G protein-coupled receptor kinases govern G protein and beta-arrestin-mediated signaling of V2 vasopressin receptor. Proc Natl Acad Sci USA 102:1448-1453.
68. Kim J, et al. (2005) Functional antagonism of different G protein-coupled receptor kinases for beta-arrestin-mediated angiotensin II receptor signaling. Proc Natl Acad Sci USA 102:1442-1447. (Pubitemid 40209189)
69. Alderton F, et al. (2001) Tethering of the platelet-derived growth factor beta receptor to G-protein-coupled receptors. A novel platform for integrative signaling by these receptor classes in mammalian cells. J Biol Chem 276:28578-28585. (Pubitemid 37391573)
70. Tilley DG, Kim IM, Patel PA, Violin JD, Rockman HA (2009) beta-Arrestin mediates beta1-adrenergic receptor-epidermal growth factor receptor interaction and downstream signaling. J Biol Chem 284:20375-20386.
71. Cagnol S, Chambard JC (2010) ERK and cell death: Mechanisms of ERK-induced cell death - apoptosis, autophagy and senescence. FEBS J 277:2-21.
72. Hidalgo M, Eckhardt SG (2001) Development of matrix metalloproteinase inhibitors in cancer therapy. J Natl Cancer Inst 93:178-193. (Pubitemid 32166488)
73. Rosendahl A, Forsberg G (2004) Influence of IGF-IR stimulation or blockade on proliferation of human renal cell carcinoma cell lines. Int J Oncol 25:1327-1336.
74. Cheung CW, Vesey DA, Nicol DL, Johnson DW (2004) The roles of IGF-I and IGFBP-3 in the regulation of proximal tubule, and renal cell carcinoma cell proliferation. Kidney Int 65:1272-1279. (Pubitemid 38406965)
75. Yuen JS, et al. (2009) Validation of the type 1 insulin-like growth factor receptor as a therapeutic target in renal cancer. Mol Cancer Ther 8:1448-1459.
76. Major JM, Pollak MN, Snyder K, Virtamo J, Albanes D (2010) Insulin-like growth factors and risk of kidney cancer in men. Br J Cancer 103:132-135.