Akt1 and Akt3 exert opposing roles in the regulation of vascular tumor growth

Cancer Research

Volumn 75, Issue 1, 2015, Pages 40-50

  Phung, Thuy L ^a   Du, Wa ^a   Xue, Qi ^b   Ayyaswamy, Sriram ^a   Gerald, Damien ^b   Antonello, Zeus ^c   Nhek, Sokha ^b   Perruzzi, Carole A ^b   Acevedo, Isabel ^c   Ramanna Valmiki, Rajesh ^a   Rodriguez Waitkus, Paul ^a   Enayati, Ladan ^a   Hochman, Marcelo L ^d   Lev, Dina ^e   Geeganage, Sandaruwan ^b   Benjamin, Laura E ^b,c  

^a TEXAS CHILDREN S HOSPITAL   (United States)

^b ELI LILLY AND COMPANY   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^d Hemangioma International Treatment Center   (United States)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AKT1 PROTEIN; AKT3 PROTEIN; LY 2584702; PROTEIN KINASE; PROTEIN RICTOR; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE INHIBITOR; RAPAMYCIN; S6 KINASE; UNCLASSIFIED DRUG; AKT1 PROTEIN, HUMAN; AKT1 PROTEIN, MOUSE; AKT3 PROTEIN, HUMAN; AKT3 PROTEIN, MOUSE; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CARCINOGENESIS; CELL GROWTH; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; FEMALE; HEMANGIOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR GROWTH; TUMOR PROMOTION; VASCULAR TUMOR; ANIMAL; C57BL MOUSE; CELL PROLIFERATION; ENZYMOLOGY; METABOLISM; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; HUMANS; MICE; MICE, INBRED C57BL; MICE, NUDE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; VASCULAR NEOPLASMS;

EID: 84920507185     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2961     Document Type: Article

References (40)

1. Young RJ, Brown NJ, Reed MW, Hughes D, Woll PJ. Angiosarcoma. Lancet Oncol 2010;11:983-91.
2. Shiojima I, Walsh K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res 2002;90:1243-50.
3. Jinnin M, Medici D, Park L, Limaye N, Liu Y, Boscolo E, et al. Suppressed NFAT-dependent VEGFR1 expression and constitutive VEGFR2 signaling in infantile hemangioma. Nat Med 2008;14:1236-46.
4. Itakura E, Yamamoto H, Oda Y, Tsuneyoshi M. Detection and characterization of vascular endothelial growth factors and their receptors in a series of angiosarcomas. J Surg Oncol 2008;97:74-81.
5. Lahat G, Dhuka AR, Hallevi H, Xiao L, Zou G, Smith KD, et al. Angiosarcoma: clinical and molecular insights. Ann Surg 2010;251:1098-106.
6. Bader AG, Kang S, Vogt PK. Cancer-specific mutations in PIK3CA are oncogenic in vivo. Proc Natl Acad Sci U S A 2006;103:1475-9.
7. Yoeli-Lerner M, Yiu GK, Rabinovitz I, Erhardt P, Jauliac S, Toker A. Akt blocks breast cancer cell motility and invasion through the transcription factor NFAT. Mol Cell 2005;20:539-50.
8. Hutchinson JN, Jin J, Cardiff RD, Woodgett JR, Muller WJ. Activation of Akt-1 (PKB-alpha) can accelerate ErbB-2-mediated mammary tumorigenesis but suppresses tumor invasion. Cancer Res 2004;64:3171-8.
9. Maroulakou IG, Oemler W, Naber SP, Tsichlis PN. Akt1 ablation inhibits, whereas Akt2 ablation accelerates, the development of mammary adenocarcinomas in mouse mammary tumor virus (MMTV)-ErbB2/neu and MMTV-polyoma middle T transgenic mice. Cancer Res 2007;67:167-77.
10. Chin YR, Yoshida T, Marusyk A, Beck AH, Polyak K, Toker A. Targeting Akt3 signaling in triple-negative breast cancer. Cancer Res 2014;74:964-73.
11. Banerji S, Cibulskis K, Rangel-Escareno C, Brown KK, Carter SL, Frederick AM, et al. Sequence analysis of mutations and translocations across breast cancer subtypes. Nature 2012;486:405-9.
12. Chung S, Yao J, Suyama K, Bajaj S, Qian X, Loudig OD, et al. N-cadherin regulates mammary tumor cell migration through Akt3 suppression. Oncogene 2013;32:422-30.
13. Hollander MC, Maier CR, Hobbs EA, Ashmore AR, Linnoila RI, Dennis PA. Akt1 deletion prevents lung tumorigenesis by mutant K-ras. Oncogene 2011;30:1812-21.
14. Linnerth-Petrik NM, Santry LA, Petrik JJ, Wootton SK. Opposing functions of akt isoforms in lung tumor initiation and progression. PLoS ONE 2014;9:e94595.
15. Sarbassov dos D, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005;307:1098-101.
16. Hara K, Maruki Y, Long X, Yoshino K, Oshiro N, Hidayat S, et al. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 2002;110:177-89.
17. Burnett PE, Barrow RK, Cohen NA, Snyder SH, Sabatini DM. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc Natl Acad Sci U S A 1998;95:1432-7.
18. Dufner A, Thomas G. Ribosomal S6 kinase signaling and the control of translation. Exp Cell Res 1999;253:100-9.
19. Ip CK, Cheung AN, Ngan HY, Wong AS. p70 S6 kinase in the control of actin cytoskeleton dynamics and directed migration of ovarian cancer cells. Oncogene 2011;30:2420-32.
20. Proud CG. mTORC1 signalling and mRNA translation. Biochem Soc Trans 2009;37:227-31.
21. Phung TL, Ziv K, Dabydeen D, Eyiah-Mensah G, Riveros M, Perruzzi C, et al. Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 2006;10:159-70.
22. Easton RM, Cho H, Roovers K, Shineman DW, Mizrahi M, Forman MS, et al. Role for Akt3/protein kinase Bgamma in attainment of normal brain size. Mol Cell Biol 2005;25:1869-78.
23. Du W, Gerald D, Perruzzi CA, Rodriguez-Waitkus P, Enayati L, Krishnan B, et al. Vascular tumors have increased p70 S6-kinase activation and are inhibited by topical rapamycin. Lab Invest 2013;93:1115-27.
24. Krump-Konvalinkova V, Bittinger F, Olert J, Brauninger W, Brunner J, Kirkpatrick CJ. Establishment and characterization of an angiosarcom-aderived cell line, AS-M. Endothelium 2003;10:319-28.
25. Obeso J, Weber J, Auerbach R. A hemangioendothelioma-derived cell line: its use as a model for the study of endothelial cell biology. Lab Invest 1990;63:259-69.
26. Xue Q, Nagy JA, Manseau EJ, Phung TL, Dvorak HF, Benjamin LE. Rapamycin inhibition of the Akt/mTOR pathway blocks select stages of VEGF-A164-driven angiogenesis, in part by blocking S6Kinase. Arterioscler Thromb Vasc Biol 2009;29:1172-8.
27. Shao Y, Aplin AE. Akt3-mediated resistance to apoptosis in B-RAF-targeted melanoma cells. Cancer Res 2010;70:6670-81.
28. Franke TF, Hornik CP, Segev L, Shostak GA, Sugimoto C. PI3K/Akt and apoptosis: size matters. Oncogene 2003;22:8983-98.
29. North PE, Waner M, Mizeracki A, Mihm MC Jr. GLUT1: a newly discovered immunohistochemical marker for juvenile hemangiomas. Hum Pathol 2000;31:11-22.
30. Kuo CJ, Chung J, Fiorentino DF, Flanagan WM, Blenis J, Crabtree GR. Rapamycin selectively inhibits interleukin-2 activation of p70 S6 kinase. Nature 1992;358:70-3.
31. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, et al. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 2006;66:1500-8.
32. Corum DG, Tsichlis PN, Muise-Helmericks RC. AKT3 controls mitochondrial biogenesis and autophagy via regulation of the major nuclear export protein CRM-1. FASEB J 2013;28:395-407.
33. Cheung M, Sharma A, Madhunapantula SV, Robertson GP. Akt3 and mutant V600E B-Raf cooperate to promote early melanoma development. Cancer Res 2008;68:3429-39.
34. Cristiano BE, Chan JC, Hannan KM, Lundie NA, Marmy-Conus NJ, Campbell IG, et al. A specific role for AKT3 in the genesis of ovarian cancer through modulation of G(2)-M phase transition. Cancer Res 2006;66:11718-25.
35. Liby TA, Spyropoulos P, Buff Lindner H, Eldridge J, Beeson C, Hsu T, et al. Akt3 controls vascular endothelial growth factor secretion and angiogenesis in ovarian cancer cells. Int J Cancer 2012;130:532-43.
36. Mure H, Matsuzaki K, Kitazato KT, Mizobuchi Y, Kuwayama K, Kageji T, et al. Akt2 and Akt3 play a pivotal role in malignant gliomas. Neuro Oncol 2010;12:221-32.
37. Gonzalez E, McGraw TE. Insulin-modulated Akt subcellular localization determines Akt isoform-speci fic signaling. Proc Natl Acad Sci U S A 2009;106:7004-9.
38. Nukazuka A, Tamaki S, Matsumoto K, Oda Y, Fujisawa H, Takagi S. A shift of the TOR adaptor from Rictor towards Raptor by semaphorin in C. elegans. Nat Commun 2011;2:484.
39. Sarbassov dos D, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, et al. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 2006;22:159-68.
40. Cherrin C, Haskell K, Howell B, Jones B, Leander K, Robinson R, et al. An allosteric Akt inhibitor effectively blocks Akt signaling and tumor growth with only transient effects on glucose and insulin levels in vivo. Cancer Biol Ther 2010;9:493-503.