Rapamycin induces transactivation of the EGFR and increases cell survival

Oncogene

Volumn 28, Issue 9, 2009, Pages 1187-1196

  Chaturvedi, D ^a   Gao, X ^a   Cohen, M S ^b,c   Taunton, J ^b   Patel, T B ^a  

^a LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Apoptosis; c Src; EGFR; mTOR; Rapamycin; Transactivation

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN P90; PROTEIN TYROSINE KINASE; RAPAMYCIN; S6 KINASE;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; EMBRYO; FEMALE; HUMAN; HUMAN CELL; LUNG FIBROBLAST; MOUSE; NONHUMAN; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

CELL SURVIVAL; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SIROLIMUS; TRANSCRIPTIONAL ACTIVATION;

MAMMALIA;

EID: 62049084546     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2008.490     Document Type: Article

References (61)

1. Abraham RT. (1998). Mammalian target of rapamycin: immunosuppressive drugs uncover a novel pathway of cytokine receptor signaling. Curr Opin Immunol 10: 330-336.
2. Arteaga CL, Ramsey TT, Shawver LK, Guyer CA. (1997). Unliganded epidermal growth factor receptor dimerization induced by direct interaction of quinazolines with the ATP binding site. J Biol Chem 272: 23247-23254.
3. Asakura M, Kitakaze M, Takashima S, Liao Y, Ishikura F, Yoshinaka T et al. (2002). Cardiac hypertrophy is inhibited by antagonism of ADAM12 processing of HB-EGF: metalloproteinase inhibitors as a new therapy. Nat Med 8: 35-40.
4. Azzariti A, Porcelli L, Gatti G, Nicolin A, Paradiso A. (2008). Synergic antiproliferative and antiangiogenic effects of EGFR and mTOR inhibitors on pancreatic cancer cells. Biochem Pharmacol 75: 1035-1044.
5. Banko JL, Hou L, Poulin F, Sonenberg N, Klann E. (2006). Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J Neurosci 26: 2167-2173.
6. Bjornsti MA, Houghton PJ. (2004). The TOR pathway: a target for cancer therapy. Nat Rev Cancer 4: 335-348.
7. Boluyt MO, Li ZB, Loyd AM, Scalia AF, Cirrincione GM, Jackson RR. (2004). The mTOR/p70S6K signal transduction pathway plays a role in cardiac hypertrophy and influences expression of myosin heavy chain genes in vivo. Cardiovasc Drugs Ther 18: 257-267.
8. Chaturvedi D, Poppleton HM, Stringfield T, Barbier A, Patel TB. (2006). Subcellular localization and biological actions of activated RSK1 are determined by its interactions with subunits of cyclic AMP-dependent protein kinase. Mol Cell Biol 26: 4586-4600.
9. Chen RH, Sarnecki C, Blenis J. (1992). Nuclear localization and regulation of Erk- and RSK-encoded protein kinases. Mol Cell Biol 12: 915-927.
10. Cohen MS, Zhang C, Shokat KM, Taunton J. (2005). Structural bioinformatics-based design of selective, irreversible kinase inhibitors. Science 308: 1318-1321.
11. Costa LJ, Gemmill RM, Drabkin HA. (2007). Upstream signaling inhibition enhances rapamycin effect on growth of kidney cancer cells. Urology 69: 596-602.
12. Daub H, Wallasch C, Lankenau A, Herrlich A, Ullrich A. (1997). Signal characteristics of G protein-transactivated EGF receptor. EMBO J 16: 7032-7044.
13. Dormond O, Madsen JC, Briscoe DM. (2007). The effects of mTOR-AKT interactions on anti-apoptotic signaling in vascular endothelial cells. J Biol Chem 282: 23679-23686.
14. Dummler BA, Hauge C, Silber J, Yntema HG, Kruse LS, Kofoed B et al. (2005). Functional characterization of human RSK4, a new 90-kDa ribosomal S6 kinase, reveals constitutive activation in most cell types. J Biol Chem 280: 13304-13314.
15. Fischer OM, Hart S, Gschwind A, Ullrich A. (2003). EGFR signal transactivation in cancer cells. Biochem Soc Trans 31: 1203-1208.
16. Frias MA, Thoreen CC, Jaffe JD, Schroder W, Sculley T, Carr SA et al. (2006). mSin1 is necessary for Akt/PKB phosphorylation, and its isoforms define three distinct mTORC2s. Curr Biol 16: 1865-1870.
17. Frodin M, Gammeltoft S. (1999). Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction. Mol Cell Endocrinol 151: 65-77.
18. Fumarola C, La Monica S, Alfieri RR, Borra E, Guidotti GG. (2005). Cell size reduction induced by inhibition of the mTOR/S6K-signaling pathway protects Jurkat cells from apoptosis. Cell Death Differ 12: 1344-1357.
19. Galanis E, Buckner JC, Maurer MJ, Kreisberg JI, Ballman K, Boni J et al. (2005). Phase II trial of temsirolimus (CCI-779) in recurrent glioblastoma multiforme: a North Central Cancer Treatment Group Study. J Clin Oncol 23: 5294-5304.
20. Goudar RK, Shi Q, Hjelmeland MD, Keir ST, McLendon RE, Wikstrand CJ et al. (2005). Combination therapy of inhibitors of epidermal growth factor receptor/vascular endothelial growth factor receptor 2 (AEE788) and the mammalian target of rapamycin (RAD001) offers improved glioblastoma tumor growth inhibition. Mol Cancer Ther 4: 101-112.
21. 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.
22. Guertin DA, Sabatini DM. (2005). An expanding role for mTOR in cancer. Trends Mol Med 11: 353-361.
23. Hardie DG, Hawley SA, Scott JW. (2006). AMP-activated protein kinase - development of the energy sensor concept. J Physiol 574: 7-15.
24. Harrington LS, Findlay GM, Gray A, Tolkacheva T, Wigfield S, Rebholz H et al. (2004). The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins. J Cell Biol 166: 213-223.
25. Huang S, Houghton PJ. (2003). Targeting mTOR signaling for cancer therapy. Curr Opin Pharmacol 3: 371-377.
26. Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y, Zhang X et al. (2006). TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126: 955-968.
27. Jacinto E, Facchinetti V, Liu D, Soto N, Wei S, Jung SY et al. (2006). SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 127: 125-137.
28. Jacinto E, Loewith R, Schmidt A, Lin S, Ruegg MA, Hall A et al. (2004). Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol 6: 1122-1128.
29. Jin W, Yun C, Hobbie A, Martin MJ, Sorensen PH, Kim SJ. (2007). Cellular transformation and activation of the phosphoinositide-3-kinase-Akt cascade by the ETV6-NTRK3 chimeric tyrosine kinase requires c-Src. Cancer Res 67: 3192-3200.
30. Kiley SC, Chevalier RL. (2007). Species differences in renal Src activity direct EGF receptor regulation in life or death response to EGF. Am J Physiol Renal Physiol 293: F895-F903.
31. Kris M, Riely G, Azzoli C, Heelan R, Krug L, Pao W et al. (2007). Combined inhibition of mTOR and EGFR with everolimus (RAD001) and gefitinib in patients with non-small cell lung cancer who have smoked cigarettes: A phase II trial. J Clin Oncol 25: 18S.
32. Kudo N, Gillespie JG, Kung L, Witters LA, Schulz R, Clanachan AS et al. (1996). Characterization of 5′AMP-activated protein kinase activity in the heart and its role in inhibiting acetyl-CoA carboxylase during reperfusion following ischemia. Biochim Biophys Acta 1301: 67-75.
33. Li J, Lin ML, Wiepz GJ, Guadarrama AG, Bertics PJ. (1999). Integrin-mediated migration of murine B82L fibroblasts is dependent on the expression of an intact epidermal growth factor receptor. J Biol Chem 274: 11209-11219.
34. Lorenz MC, Heitman J. (1995). TOR mutations confer rapamycin resistance by preventing interaction with FKBP12-rapamycin. J Biol Chem 270: 27531-27537.
35. Manning BD. (2004). Balancing Akt with S6K: implications for both metabolic diseases and tumorigenesis. J Cell Biol 167: 399-403.
36. McMullen JR, Sherwood MC, Tarnavski O, Zhang L, Dorfman AL, Shioi T et al. (2004). Inhibition of mTOR signaling with rapamycin regresses established cardiac hypertrophy induced by pressure overload. Circulation 109: 3050-3055.
37. Metro G, Finocchiaro G, Toschi L, Bartolini S, Magrini E, Cancellieri A et al. (2006). Epidermal growth factor receptor (EGFR) targeted therapies in non-small cell lung cancer (NSCLC). Rev Recent Clin Trials 1: 1-13.
38. Milton DT, Riely GJ, Azzoli CG, Gomez JE, Heelan RT, Kris MG et al. (2007). Phase 1 trial of everolimus and gefitinib in patients with advanced nonsmall-cell lung cancer. Cancer 110: 599-605.
39. Myers AP, Corson LB, Rossant J, Baker JC. (2004). Characterization of mouse Rsk4 as an inhibitor of fibroblast growth factor-RAS-extracellular signal-regulated kinase signaling. Mol Cell Biol 24: 4255-4266.
40. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D et al. (2006). mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 66: 1500-1508.
41. Parry TJ, Brosius R, Thyagarajan R, Carter D, Argentieri D, Falotico R et al. (2005). Drug-eluting stents: sirolimus and paclitaxel differentially affect cultured cells and injured arteries. Eur J Pharmacol 524: 19-29.
42. Prenzel N, Zwick E, Daub H, Leserer M, Abraham R, Wallasch C et al. (1999). EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402: 884-888.
43. Roux PP, Richards SA, Blenis J. (2003). Phosphorylation of p90 ribosomal S6 kinase (RSK) regulates extracellular signal-regulated kinase docking and RSK activity. Mol Cell Biol 23: 4796-4804.
44. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J et al. (2007). RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J Biol Chem 282: 14056-14064.
45. Sabatini DM. (2006). mTOR and cancer: insights into a complex relationship. Nat Rev Cancer 6: 729-734.
46. Saito Y, Haendeler J, Hojo Y, Yamamoto K, Berk BC. (2001). Receptor heterodimerization: essential mechanism for platelet-derived growth factor-induced epidermal growth factor receptor transactivation. Mol Cell Biol 21: 6387-6394.
47. Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR, Erdjument-Bromage H et al. (2004). Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol 14: 1296-1302.
48. Sarbassov DD, Ali SM, Sabatini DM. (2005). Growing roles for the mTOR pathway. Curr Opin Cell Biol 17: 596-603.
49. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF et al. (2006). Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 22: 159-168.
50. Sharma S, Ying J, Razeghi P, Stepkowski S, Taegtmeyer H. (2006). Atrophic remodeling of the transplanted rat heart. Cardiology 105: 128-136.
51. Shimamura A, Ballif BA, Richards SA, Blenis J. (2000). Rsk1 mediates a MEK-MAP kinase cell survival signal. Curr Biol 10: 127-135.
52. Sun SY, Rosenberg LM, Wang X, Zhou Z, Yue P, Fu H et al. (2005). Activation of Akt and eIF4E survival pathways by rapamycin-mediated mammalian target of rapamycin inhibition. Cancer Res 65: 7052-7058.
53. Tice DA, Biscardi JS, Nickles AL, Parsons SJ. (1999). Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc Natl Acad Sci USA 96: 1415-1420.
54. Tzatsos A, Kandror KV. (2006). Nutrients suppress phosphatidylinositol 3-kinase/Akt signaling via raptor-dependent mTOR-mediated insulin receptor substrate 1 phosphorylation. Mol Cell Biol 26: 63-76.
55. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M et al. (2004). Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431: 200-205.
56. VanderWeele DJ, Zhou R, Rudin CM. (2004). Akt up-regulation increases resistance to microtubule-directed chemotherapeutic agents through mammalian target of rapamycin. Mol Cancer Ther 3: 1605-1613.
57. Vega F, Medeiros LJ, Leventaki V, Atwell C, Cho-Vega JH, Tian L et al. (2006). Activation of mammalian target of rapamycin signaling pathway contributes to tumor cell survival in anaplastic lymphoma kinase-positive anaplastic large cell lymphoma. Cancer Res 66: 6589-6597.
58. Vivanco I, Sawyers CL. (2002). The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2: 489-501.
59. Wan X, Harkavy B, Shen N, Grohar P, Helman LJ. (2007). Rapamycin induces feedback activation of Akt signaling through an IGF-1R-dependent mechanism. Oncogene 26: 1932-1940.
60. Wendel HG, De Stanchina E, Fridman JS, Malina A, Ray S, Kogan S et al. (2004). Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 428: 332-337.
61. Wullschleger S, Loewith R, Hall MN. (2006). TOR signaling in growth and metabolism. Cell 124: 471-484.