AKT as locus of cancer angiogenic robustness and fragility

Journal of Cellular Physiology

Volumn 228, Issue 1, 2013, Pages 21-24

  Radisavljevic, Ziv ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; MAMMALIAN TARGET OF RAPAMYCIN; NITRIC OXIDE SYNTHASE; OXIDIZING AGENT; PROTEIN KINASE B;

ANGIOGENESIS; LEUKEMIA RELAPSE; LYMPHOMA; METASTASIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW;

GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL;

EID: 84867145579     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24115     Document Type: Review

References (79)

1. Aguayo A, Estey E, Kantarjian H, Mansouri T, Gidel C, Keating M, Giles F, Estrov Z, Barlogie B, Albitar M. 1999. Cellular vascular endothelial growth factor is a predictor of outcome in patients with acute myeloid leukemia. Blood 94: 3717-3721.
2. Aguayo A, Kantarjian H, Manshouri T, Gidel C, Estey E, Thomas D, Koller C, Estrov Z, O'Brien S, Keating M, Freireich E, Albitar M. 2000. Angiogenesis in acute and chronic leukemias and myelodysplastic syndromes. Blood 96: 2240-2245.
3. Ayala F, Dewar R, Kieran M, Kalluri R. 2009. Contribution of bone microenvironment to leukemogenesis and leukemia progression. Leukemia 23: 2233-2241.
4. Bergers G, Hanahan D. 2008. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 8: 592-603.
5. Brown JM, Giaccia AJ. 1998. The unique physiology of solid tumours: Opportunities (and problems) for cancer therapy. Cancer Res 58: 1408-1416.
6. Bussolino F, Albini A, Camussi G, Presta M, Viglietto G, Ziche M, Persico G. 1996. Role of soluble mediators in angiogenesis. Eur J Cancer 32A: 2401-2412.
7. Carlson JM, Doyle J. 1999. Highly optimized tolerance: A mechanism for power laws in designed systems. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 60: 1412-1427.
8. Carlson JM, Doyle J. 2002. Complexity and robustness. Proc Natl Acad Sci USA 99: 2538-2545.
9. Chen CN, Hsieh FJ, Cheng YM, Chang KJ, Lee PH. 2006. Expression of inducible nitric oxide synthase and cyclooxygenase-2 in angiogenesis and clinical outcome of human gastric cancer. J Surg Oncol 94: 226-233.
10. Csete ME, Doyle JC. 2002. Reverse engineering of biological complexity. Science 295: 1664-1669.
11. de Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT. 1992. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 255: 989-991.
12. Dunn CA, Su V, Lau AF, Lampe PD. 2012. Activation of AKT, not connexin 43 protein ubiquitination, regulates gap junction stability. J Biol Chem 287: 2600-2607.
13. Ferrajoli A, Manshouri T, Estrov Z, Keating MJ, O'Brien S, Lerner S, Beran M, Kantarjian HM, Freireich EJ, Albitar M. 2001. High levels of vascular endothelial growth factor receptor-2 correlate with shortened survival in chronic lymphocytic leukemia. Clin Cancer Res 7: 795-799.
14. Ferrara N. 1996. Vascular endothelial growth factor. Eur J Cancer 32A: 2413-2422.
15. Fidler IJ, Ellis LM. 2004. Neoplastic angiogenesis-not all blood vessels are created equal. N Engl J Med 351: 215-216.
16. Fiedler W, Graeven U, Ergun S, Kilic N, Stockschläder M, Hossfeld DK. 1997. Vascular endothelial growth factor, a possible paracrine growth factor in human acute myeloid leukemia. Blood 89: 1870-1875.
17. Folkman J. 1971. Tumor angiogenesis: Therapeutic implications. N Engl J Med 285: 1182-1186.
18. Folkman J. 1995. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1: 27-31.
19. Folkman J, Klagsbrun M. 1987. Angiogenic factors. Science 235: 442-447.
20. Folkman J, Shing Y. 1992. Angiogenesis. J Biol Chem 267: 10931-10934.
21. Fukumura D, Jain RK. 2007. Tumor microvasculature and microenvironment: Targets for anti-angiogenesis and normalization. Microvasc Res 74: 72-84.
22. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N. 1998. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/AKT signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273: 30336-30343.
23. Gerber HP, Malik AK, Solar GP, Sherman D, Liang XH, Meng G, Hong K, Marsters JC, Ferrara N. 2002. VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 417: 954-958.
24. Giatromanolaki A, Harris AL. 2001. Tumour hypoxia, hypoxia signaling pathways and hypoxia inducible factor expression in human cancer. Anticancer Res 21: 4317-4324.
25. Graeber T, Osmanian C, Jacks T. 1996. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379: 88-91.
26. Gratzinger D, Advani R, Zhao S, Talreja N, Tibshirani RJ, Shyam R, Horning S, Sehn LH, Farinha P, Briones J, Lossos IS, Gascoyne RD, Natkunam Y. 2010. Lymphoma cell VEGFR2 expression detected by immunohistochemistry predicts poor overall survival in diffuse large B cell lymphoma treated with immunochemotherapy (R-CHOP). Br J Haematol 148: 235-244.
27. Gray LH, Conger AD, Ebert M. 1953. The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. Br J Radiol 26: 638-648.
28. Gunsilius E, Duba HC, Petzer AL, Kähler CM, Grünewald K, Stockhammer G, Gabl C, Dirnhofer S, Clausen J, Gastl G. 2000. Evidence from a leukaemia model for maintenance of vascular endothelium by bone-marrow-derived endothelial cells. Lancet 355: 1688-1691.
29. Hanahan D, Folkman J. 1996. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86: 353-364.
30. Harris AL. 2002. Hypoxia-A key regulatory factor in tumour growth. Nat Rev Cancer 2: 38-47.
31. Hattori K, Heissig B, Wu Y, Dias S, Tejada R, Ferris B, Hicklin DJ, Zhu Z, Bohlen P, Witte L, Hendrikx J, Hackett NR, Crystal RG, Moore MA, Werb Z, Lyden D, Rafii S. 2002. Placental growth factor reconstitutes hematopoiesis by recruiting VEGFR1(+) stem cells from bone-marrow microenvironment. Nat Med 8: 841-849.
32. Hussong JW, Rodgers GM, Shami PJ. 2000. Evidence of increased angiogenesis in patients with acute myeloid leukemia. Blood 95: 309-313.
33. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin WG, Jr. 2001. HIF-alpha targeted for VHL-mediated destruction by proline hydroxylation: Implications for O2 sensing. Science 292: 464-468.
34. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, Kriegsheim Av, Hebestreit HF, Mukherji M, Schofield CJ, Maxwell PH, Pugh CW, Ratcliffe PJ. 2001. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472.
35. Jain RK. 2005. Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science 307: 58-62.
36. Jain RK. 2008. Lessons from multidisciplinary translational trials on anti-angiogenic therapy of cancer. Nature Rev Cancer 8: 309-316.
37. Jain RK, Finn AV, Kolodgie FD, Gold HK, Virmani R. 2007. Antiangiogenic therapy for normalization of atherosclerotic plaque vasculature: A potential strategy for plaque stabilization. Nature Clin Pract Cardiovasc Med 4: 491-502.
38. Jin DK, Shido K, Kopp HG, Petit I, Shmelkov SV, Young LM, Hooper AT, Amano H, Avecilla ST, Heissig B, Hattori K, Zhang F, Hicklin DJ, Wu Y, Zhu Z, Dunn A, Salari H, Werb Z, Hackett NR, Crystal RG, Lyden D, Rafii S. 2006. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med 12: 557-567.
39. Kaelin WG, Jr. 2007. The von Hippel-Lindau tumor suppressor protein and clear cell renal carcinoma. Clin Cancer Res 13: 680s-684s.
40. Kini AR, Peterson LA, Tallman MS, Lingen MW. 2001. Angiogenesis in acute promyelocytic leukemia: Induction by vascular endothelial growth factor and inhibition by all-trans retinoic acid. Blood 97: 3919-3924.
41. Klagsbrun M, D'Amore PA. 1996. Vascular endothelial growth factor and its receptors. Cytokine Growth Factor Rev 7: 259-270.
42. Koong AC, Denko NC, Hudson KM. 2000. Canditate genes for the hypoxic tumour phenotype. Cancer Res 60: 883-887.
43. Kortemme T, Baker D. 2002. A simple physical model for binding energy hot spots in protein-protein complexes. Proc Natl Acad Sci USA 99: 14116-14121.
44. Lee BL, Kim WH, Jung J, Cho SJ, Park J-W, Kim J, Chung H-Y, Chang MS, Nam SY. 2008. A hypoxia-independent up-regulation of hypoxia-inducible factor-1 by AKT contributes to angiogenesis in human gastric cancer. Carcinogenesis 29: 44-51.
45. Mazzucchelli R, Montironi R, Santinelli A, Lucarini G, Pugnaloni A, Biagini G. 2000. Vascular endothelial growth factor expression and capillary architecture in high-grade PIN and prostate cancer in untreated and androgen-ablated patients. Prostate 45: 72-79.
46. Metzen E, Zhou J, Jelkmann W, Fandrey J, Brune B. 2003. Nitric oxide impairs normoxic degradation of HIF-1a byinhibition of prolyl hydroxylases. Mol Biol Cell 14: 3470-3481.
47. Nogueira V, Park Y, Chen CC, Xu PZ, Chen ML, Tonic I, Unterman T, Hay N. 2008. AKT determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer Cell 14: 458-470.
48. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. 2003. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 3: 347-361.
49. Perez-Atayde AR, Sallan SE, Tedrow U, Connors S, Allred E, Folkman J. 1997. Spectrum of tumor angiogenesis in the bone marrow of children with acute lymphoblastic leukemia. Am J Pathol 150: 815-821.
50. Podar K, Anderson KC. 2005. The pathophysiologic role of VEGF in hematologic malignancies: Therapeutic implications. Blood 105: 1383-1395.
51. Pries AR, Höpfner M, le Noble F, Dewhirst MW, Secomb TW. 2010. The shunt problem: Control of functional shunting in normal and tumour vasculature. Nat Rev Cancer 10: 587-593.
52. Radisavljevic Z. 2003. Nitric oxide suppression triggers apoptosis through the FKHRL1 (FOXO3a)/ROCK kinase pathway in human breast carcinoma cells. Cancer 97: 1358-1363.
53. Radisavljevic Z. 2004a. Locus of fragility in robust breast cancer system. J Cell Biochem 92: 711-715.
54. Radisavljevic Z. 2004b. Inactivated tumor suppressor Rb by nitric oxide promotes mitosis in human breast cancer cells. J Cell Biochem 92: 1-5.
55. Radisavljevic Z. 2008. AKT as locus of fragility in robust cancer system. J Cell Biochem 104: 2071-2077.
56. 2-induced mitosis in primary type II pneumocytes. Biochim Biophys Acta Mol Cell Res 1640: 163-170.
57. 2-induced mitosis. J Cell Biochem 91: 1293-1300.
58. Radisavljevic Z, Avraham H, Avraham S. 2000. Vascular endothelial growth factor up-regulates ICAM-1 expression via the phosphatidylinositol 3 OH-kinase/AKT/Nitric oxide pathway and modulates migration of brain microvascular endothelial cells. J Biol Chem 275: 20770-20774.
59. Rafii S. 2000. Circulating endothelial precursors: Mystery, reality, and promise. J Clin Invest 105: 17-19.
60. Ruan J, Leonard JP. 2009. Targeting angiogenesis: A novel, rational therapeutic approach for non-Hodgkin lymphoma. Leuk Lymphoma 50: 679-681.
61. Ruan J, Hajjar K, Rafii S, Leonard JP. 2009. Angiogenesis and antiangiogenic therapy in non-Hodgkin's lymphoma. Ann Oncol 20: 413-424.
62. Salven P, Teerenhovi L, Joensuu H. 1997. A high pretreatment serum vascular endothelial growth factor concentration is associated with poor outcome in non-Hodgkin's lymphoma. Blood 90: 3167-3172.
63. Semenza GL. 2003. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732.
64. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376: 62-66.
65. Solan JL, Marquez-Rosado L, Sorgen PL, Thornton PJ, Gafken PR, Lampe PD. 2007. Phosphorylation at S365 is a gatekeeper event that changes the structure of Cx43 and prevents down-regulation by PKC. J Cell Biol 179: 1301-1309.
66. Streubel B, Chott A, Huber D, Exner M, Jäger U, Wagner O, Schwarzinger I. 2004. Lymphoma-specific genetic aberrations in microvascular endothelial cells in B-cell lymphomas. N Engl J Med 351: 250-259.
67. Suarez S, Ballmer-Hofer K. 2001. VEGF transiently disrupts gap junctional communication in endothelial cells. J Cell Sci 114: 1229-1235.
68. Takahashi Y, Kitadai Y, Bucana CD, Cleary KR, Ellis LM. 1995. Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res 55: 3964-3968.
69. Tammela T, Zarkada G, Wallgard E, Murtomäki A, Suchting S, Wirzenius M, Waltari M, Hellström M, Schomber T, Peltonen R, Freitas C, Duarte A, Isoniemi H, Laakkonen P, Christofori G, Ylä-Herttuala S, Shibuya M, Pytowski B, Eichmann A, Betsholtz C, Alitalo K. 2008. Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454: 656-660.
70. Tennant MK, Thrasher JB, Twomey PA, Birnbaum RS, Plymate SR. 1996. Insulin-like growth factor-binding protein-2 and -3 expression in benign human prostate epithelium, prostate intraepithelial neoplasia, and adenocarcinoma of the prostate. J Clin Endocrinol Metabol 81: 411-420.
71. Terman BI, Dougher-Vermazen M, Carrion ME, Dimitrov D, Armellino DC, Gospodarowicz D, Böhlen P. 1992. Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor. Biochem Biophys Res Commun 187: 1579-1586.
72. Trusolino L, Comoglio PM. 2002. Scater-factor and semaphoring receptors: Cell signaling for invasive growth. Nat Rev Cancer 2: 289-300.
73. Tzankov A, Heiss S, Ebner S, Sterlacci W, Schaefer G, Augustin F, Fiegl M, Dirnhofer S. 2007. Angiogenesis in nodal B cell lymphomas: A high throughput study. J Clin Pathol 60: 476-482.
74. Uddin S, Hussain AR, Siraj AK, Manogaran PS, Al-Jomah NA, Moorji A, Atizado V, Al-Dayel F, Belgaumi A, El-Solh H, Ezzat A, Bavi P, Al-Kuraya KS. 2006. Role of phosphatidylinositol 3'-kinase/AKT pathway in diffuse large B-cell lymphoma survival. Blood 108: 4178-4186.
75. Upham BL, Kang KS, Cho HY, Trosko JE. 1997. Hydrogen peroxide inhibits gap junctional intercellular communication in glutathione sufficient but not glutathione deficient cells. Carcinogenesis 18: 37-42.
76. Yuen HF, Chan KK, Grills C, Murray JT, Platt-Higgins A, Eldin OS, O'Byrne K, Janne P, Fennell DA, Johnston PG, Rudland PS, El-Tanani M. 2012. Ran is a potential therapeutic target for cancer cells with molecular changes associated with activation of the PI3K/AKT/mTORC1 and Ras/MEK/ERK pathways. Clin Cancer Res 18: 380-391.
77. Zhong H, Bowen JP. 2006. Antiangiogenesis drug design: Multiple pathways targeting tumor vasculature. Curr Med Chem 13: 849-862.
78. Zhou T, Carlson JM, Doyle J. 2002. Mutation, specialization, and hypersensitivity in highly optimized tolerance. Proc Natl Acad Sci USA 99: 2049-2054.
79. Ziegler BL, Valtieri M, Porada GA, De Maria R, Müller R, Masella B, Gabbianelli M, Casella I, Pelosi E, Bock T, Zanjani ED, Peschle C. 1999. KDR receptor: A key marker defining hematopoietic stem cells. Science 285: 1553-1558.