Akt and hypoxia-inducible factor-1 independently enhance tumor growth and angiogenesis

Cancer Research

Volumn 64, Issue 10, 2004, Pages 3500-3507

  Arsham, Andrew M ^a,b   Plas, David R ^b   Thompson, Craig B ^b   Simon, M Celeste ^b,c  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c 438 BRB II/III ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; PROTEIN KINASE B;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CONTROLLED STUDY; GENE ACTIVATION; GENE ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; IN VIVO STUDY; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; TUMOR GROWTH; TUMOR VOLUME;

ANIMALS; CELL DIVISION; DNA-BINDING PROTEINS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIVER NEOPLASMS, EXPERIMENTAL; MICE; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; NUCLEAR PROTEINS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; TRANSCRIPTION FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 2442669295     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-03-2239     Document Type: Article

References (71)

1. Wenger RH. Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxiainducible transcription factors, and O2-regulated gene expression. FASEB J 2002;16:1151-62.
2. Vivanco I, Sawyers CL. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2002;2:489-501.
3. Bilton RL, Booker GW. The subtle side to hypoxia inducible factor (HIFα) regulation. Eur J Biochem 2003;270:791-8.
4. Jones A, Fujiyama C, Blanche C, et al. Relation of vascular endothelial growth factor production to expression and regulation of hypoxia-inducible factor-1 α and hypoxia-inducible factor-2 α in human bladder tumors and cell lines. Clin Cancer Res 2001;7:1263-72.
5. Arsham AM, Plas DR, Thompson CB, Simon MC. Phosphatidylinositol 3- kinase/Akt signaling is neither required for hypoxic stabilization of HIF-1 α nor sufficient for HIF-1-dependent target gene transcription. J Biol Chem 2002;277:15162-70.
6. Alvarez-Tejado M, Alfranca A, Aragones J, Vara A, Landazuri MO, del Peso L. Lack of evidence for the involvement of the phosphoinositide 3-kinase/Akt pathway in the activation of hypoxia-inducible factors by low oxygen tension. J Biol Chem 2002;277:13508-17.
7. Alessi DR, James SR, Downes CP, et al. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr Biol 1997;7:261-9.
8. Bellacosa A, Chan TO, Ahmed NN, et al. Akt activation by growth factors is a multiple-step process: the role of the PH domain. Oncogene 1998;17:313-25.
9. Taha C, Liu Z, Jin J, Al-Hasani H, Sonenberg N, Klip A. Opposite translational control of GLUT1 and GLUT4 glucose transporter mRNAs in response to insulin. Role of mammalian target of rapamycin, protein kinase b, and phosphatidylinositol 3-kinase in GLUT1 mRNA translation. J Biol Chem 1999;274:33085-91.
10. Barthel A, Okino ST, Liao J, et al. Regulation of GLUT1 gene transcription by the serine/threonine kinase Akt1. J Biol Chem 1999;274:20281-6.
11. von der Crone S, Deppe C, Barthel A, Sasson S, Joost HG, Schurmann A. Glucose deprivation induces Akt-dependent synthesis and incorporation of GLUT1, but not of GLUT4, into the plasma membrane of 3T3-L1 adipocytes. Eur J Cell Biol 2000;79:943-9.
12. Plas DR, Talapatra S, Edinger AL, Rathmell JC, Thompson CB. Akt and Bcl-xL promote growth factor-independent survival through distinct effects on mitochondrial physiology. J Biol Chem 2001;276:12041-8.
13. Gottlob K, Majewski N, Kennedy S, Kandel E, Robey RB, Hay N. Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev 2001;15:1406-18.
14. Frauwirth KA, Riley JL, Harris MH, et al. The CD28 signaling pathway regulates glucose metabolism. Immunity 2002;16:769-77.
15. Sonoda Y, Ozawa T, Aldape KD, Deen DF, Berger MS, Pieper RO. Akt pathway activation converts anaplastic astrocytoma to glioblastoma multiforme in a human astrocyte model of glioma. Cancer Res 2001;61:6674-8.
16. Sonoda Y, Ozawa T, Hirose Y, et al. Formation of intracranial tumors by genetically modified human astrocytes defines four pathways critical in the development of human anaplastic astrocytoma. Cancer Res 2001;61:4956-60.
17. Stiles B, Gilman V, Khanzenzon N, et al. Essential role of AKT-1/protein kinase B α in PTEN-controlled tumorigenesis. Mol Cell Biol 2002;22:3842-51.
18. Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE, Fuller GN. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet 2000;25:55-7.
19. Orsulic S, Li Y, Soslow RA, Vitale-Cross LA, Gutkind JS, Varmus HE. Induction of ovarian cancer by defined multiple genetic changes in a mouse model system. Cancer Cell 2002;1:53-62.
20. Segrelles C, Ruiz S, Perez P, et al. Functional roles of Akt signaling in mouse skin tumorigenesis. Oncogene 2002;21:53-64.
21. Malstrom S, Tili E, Kappes D, Ceci JD, Tsichlis PN. Tumor induction by an Lck-MyrAkt transgene is delayed by mechanisms controlling the size of the thymus. Proc Natl Acad Sci USA 2001;98:14967-72.
22. Mende I, Malstrom S, Tsichlis PN, Vogt PK, Aoki M. Oncogenic transformation induced by membrane-targeted Akt2 and Akt3. Oncogene 2001;20:4419-23.
23. Graff JR, Konicek BW, McNulty AM, et al. Increased AKT activity contributes to prostate cancer progression by dramatically accelerating prostate tumor growth and diminishing p27Kip1 expression. J Biol Chem 2000;275:24500-5.
24. Arboleda MJ, Lyons JF, Kabbinavar FF, et al. Overexpression of AKT2/protein kinase β leads to up-regulation of β1 integrins, increased invasion, and metastasis of human breast and ovarian cancer cells. Cancer Res 2003;63:196-206.
25. Saeki Y, Seya T, Hazeki K, Ui M, Hazeki O, Akedo H. Involvement of phosphoinositide 3-kinase in regulation of adhesive activity of highly metastatic hepatoma cells. J Biochem (Tokyo) 1998;124:1020-5.
26. Kim D, Kim S, Koh H, et al Akt/PKB promotes cancer cell invasion via increased motility and metalloproteinase production. FASEB J 2001;15:1953-62.
27. Dong G, Chen Z, Li ZY, Yeh NT, Bancroft CC, Van Waes C. Hepatocyte growth factor/scatter factor-induced activation of mek and pi3k signal pathways contributes to expression of proangiogenic cytokines interleukin-8 and vascular endothelial growth factor in head and neck squamous cell carcinoma. Cancer Res 2001;61:5911-8.
28. Jiang BH, Zheng JZ, Aoki M, Vogt PK. Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells. Proc Natl Acad Sci USA 2000;97:1749-53.
29. Miele C, Rochford JJ, Filippa N, Giorgetti-Peraldi S, Van Obberghen E. Insulin and insulin-like growth factor-1 induce vascular endothelial growth factor mRNA expression via different signaling pathways. J Biol Chem 2000;275:21695-702.
30. Pore N, Liu S, Haas-Kogan DA, O'Rourke DM, Maity A. PTEN mutation and epidermal growth factor receptor activation regulate vascular endothelial growth factor (VEGF) mRNA expression in human glioblastoma cells by transactivating the proximal VEGF promoter. Cancer Res 2003;63:236-41.
31. Gomez-Manzano C, Fueyo J, Jiang H, et al. Mechanisms underlying PTEN regulation of vascular endothelial growth factor and angiogenesis. Ann Neurol 2003;53:109-17.
32. Rak J, Mitsuhashi Y, Sheehan C, et al. Oncogenes and tumor angiogenesis: differential modes of vascular endothelial growth factor up-regulation in ras-transformed epithelial cells and fibroblasts. Cancer Res 2000;60:490-8.
33. Kozawa O, Matsuno H, Uematsu T. Involvement of p70 S6 kinase in bone morphogenetic protein signaling: vascular endothelial growth factor synthesis by bone morphogenetic protein-4 in osteoblasts. J Cell Biochem 2001;81:430-6.
34. Arbiser JL, Moses MA, Fernandez CA, et al. Oncogenic H-ras stimulates tumor angiogenesis by two distinct pathways. Proc Natl Acad Sci USA 1997;94:861-6.
35. Wen S, Stolarov J, Myers MP, et al. PTEN controls tumor-induced angiogenesis. Proc Natl Acad Sci USA 2001;98:4622-7.
36. Akeno N, Robins J, Zhang M, Czyzyk-Krzeska MF, Clemens TL. Induction of vascular endothelial growth factor by IGF-I in osteoblast-like cells is mediated by the PI3K signaling pathway through the hypoxia-inducible factor-2α. Endocrinology 2002;143:420-5.
37. Takahashi A, Kureishi Y, Yang J, et al. Myogenic Akt signaling regulates blood vessel recruitment during myofiber growth. Mol Cell Biol 2002;22:4803-14.
38. Kosmidou I, Xagorari A, Roussos C, Papapetropoulos A. Reactive oxygen species stimulate VEGF production from C(2)C(12) skeletal myotubes through a PI3K/Akt pathway. Am J Physiol Lung Cell Mol Physiol 2001;280:L585-92.
39. Chung J, Bachelder RE, Lipscomb EA, Shaw LM, Mercurio AM. Integrin (α 6 β 4) regulation of eIF-4E activity and VEGF translation: a survival mechanism for carcinoma cells. J Cell Biol 2002;158:165-74.
40. DeFatta RJ, Nathan CA, De Benedetti A. Antisense RNA to eIF4E suppresses oncogenic properties of a head and neck squamous cell carcinoma cell line. Laryngoscope 2000;110:928-33.
41. Kevil CG, De Benedetti A, Payne DK, Coe LL, Laroux FS, Alexander JS. Translational regulation of vascular permeability factor by eukaryotic initiation factor 4E: implications for tumor angiogenesis. Int J Cancer 1996;65:785-90.
42. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001;294:1337-40.
43. Epstein AC, Gleadle JM, McNeill LA, et al. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001;107:43-54.
44. Ivan M, Kondo K, Yang H, et al HIFα targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 2001;292:464-8.
45. Jaakkola P, Mole DR, Tian YM, et al. Targeting of HIF-α to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001;292:468-72.
46. Masson N, Willam C, Maxwell PH, Pugh CW, Ratcliffe PJ. Independent function of two destruction domains in hypoxia-inducible factor-α chains activated by prolyl hydroxylation. EMBO J 2001;20:5197-206.
47. Yu F, White SB, Zhao Q, Lee FS. HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc Natl Acad Sci USA 2001;98:9630-5.
48. Kung AL, Wang S, Klco JM, Kaelin WG, Livingston DM. Suppression of tumor growth through disruption of hypoxia-inducible transcription. Nat Med 2000;6:1335-40.
49. Ryan HE, Poloni M, McNulty W, et al. Hypoxia-inducible factor-1α is a positive factor in solid tumor growth. Cancer Res 2000;60:4010-5.
50. Williams KJ, Telfer BA, Airley RE, et al. A protective role for HIF-1 in response to redox manipulation and glucose deprivation: implications for tumorigenesis. Oncogene 2002;21:282-90.
51. Akakura N, Kobayashi M, Horiuchi I, et al. Constitutive expression of hypoxia-inducible factor-1α renders pancreatic cancer cells resistant to apoptosis induced by hypoxia and nutrient deprivation. Cancer Res 2001;61:6548-54.
52. Griffiths JR, McSheehy PM, Robinson SP, et al. Metabolic changes detected by in vivo magnetic resonance studies of HEPA-1 wild-type tumors and tumors deficient in hypoxia-inducible factor-1β (HIF-1β): evidence of an anabolic role for the HIF-1 pathway. Cancer Res 2002;62:688-95.
53. Carmeliet P, Dor Y, Herbert JM, et al. Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumor angiogenesis. Nature 1998;394:485-90.
54. Yu JL, Rak JW, Carmeliet P, Nagy A, Kerbel RS, Coomber BL. Heterogeneous vascular dependence of tumor cell populations. Am J Pathol 2001;158:1325-34.
55. Blancher C, Moore JW, Talks KL, Houlbrook S, Harris AL. Relationship of hypoxia-inducible factor (HIF)-1α and HIF-2α expression to vascular endothelial growth factor induction and hypoxia survival in human breast cancer cell lines. Cancer Res 2000;60:7106-13.
56. Semenza GL. HIF-1 and tumor progression: pathophysiology and therapeutics. Trends Mol Med 2002;8:S62-7.
57. Tsuzuki Y, Fukumura D, Oosthuyse B, Koike C, Carmeliet P, Jain RK. Vascular endothelial growth factor (VEGF) modulation by targeting hypoxia-inducible factor-1α-> hypoxia response element-> VEGF cascade differentially regulates vascular response and growth rate in tumors. Cancer Res 2000;60:6248-52.
58. Maxwell PH, Dachs GU, Gleadle JM, et al. Hypoxia-inducible factor-1 modulates gene expression in solid tumors and influences both angiogenesis and tumor growth. Proc Natl Acad Sci USA 1997;94:8104-9.
59. Hopfl G, Wenger RH, Ziegler U, et al. Rescue of hypoxia-inducible factor-1α-deficient tumor growth by wild-type cells is independent of vascular endothelial growth factor. Cancer Res 2002;62:2962-70.
60. Maltepe E, Keith B, Arsham AM, Brorson JR, Simon MC. The role of ARNT2 in tumor angiogenesis and the neural response to hypoxia. Biochem Biophys Res Commun 2000;273:231-8.
61. Pear WS, Nolan GP, Scott ML, Baltimore D. Production of high-titer helper-free retroviruses by transient transfection. Proc Natl Acad Sci USA 1993;90:8392-6.
62. Miller AG, Whitlock JP Jr. Novel variants in benzo(a)pyrene metabolism. Isolation by fluorescence-activated cell sorting J Biol Chem 1981;256:2433-7.
63. Miller AG, Israel D, Whitlock JP Jr. Biochemical and genetic analysis of variant mouse hepatoma cells defective in the induction of benzo(a)pyrene-metabolizing enzyme activity. J Biol Chem 1983;258:3523-7.
64. Mazure NM, Brahimi-Horn MC, Pouyssegur J. Protein kinases and the hypoxia-inducible factor-1, two switches in angiogenesis. Curr Pharm Des 2003;9:531-41.
65. Sanchez-Elsner T, Botella LM, Velasco B, Corbi A, Attisano L, Bernabeu C. Synergistic cooperation between hypoxia and transforming growth factor-β pathways on human vascular endothelial growth factor gene expression. J Biol Chem 2001;276:38527-35.
66. Huang S, Robinson JB, Deguzman A, Bucana CD, Fidler U. Blockade of nuclear factor-κB signaling inhibits angiogenesis and tumorigenicity of human ovarian cancer cells by suppressing expression of vascular endothelial growth factor and interleukin 8. Cancer Res 2000;60:5334-9.
67. Testa JR, Bellacosa A. AKT plays a central role in tumorigenesis. Proc Natl Acad Sci USA 2001;98:10983-5.
68. Chan DA, Sutphin PD, Denko NC, Giaccia AJ. Role of prolyl hydroxylation in oncogenically stabilized hypoxia-inducible factor-1α. J Biol Chem 2002;277:40112-7.
69. Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1α (HIF-1α) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol 2001;21:3995-4004.
70. Arsham AM, Howell JJ, Simon MC. A novel HIF-independent hypoxic response regulating mTOR and its targets. J Biol Chem 2003;278:29655-60.
71. Hudson CC, Liu M, Chiang GG, et al. Regulation of hypoxia-inducible factor 1α expression and function by the mammalian target of rapamycin. Mol Cell Biol 2002;22:7004-14.