Tumor angiogenesis and anti-angiogenic therapy

Keio Journal of Medicine

Volumn 61, Issue 2, 2012, Pages 47-56

  Kubota, Yoshiaki ^a  

^a KEIO UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Anti angiogenic therapy; Macrophage; Tumor angiogenesis; VEGF

Indexed keywords

ANGIOGENESIS INHIBITOR; ANGIOPOIETIN; BEVACIZUMAB; COLONY STIMULATING FACTOR 1; FIBROBLAST GROWTH FACTOR; FLUOROURACIL; PAZOPANIB; PEGAPTANIB; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; SORAFENIB; SUNITINIB; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; VASCULOTROPIN INHIBITOR;

ANTIANGIOGENIC ACTIVITY; ANTIANGIOGENIC THERAPY; BLEEDING; CANCER RESISTANCE; COLORECTAL CANCER; DRUG EFFECT; DRUG MECHANISM; DRUG SAFETY; ENTEROPATHY; HAIR LOSS; HUMAN; HYPERTENSION; HYPOTHYROIDISM; IMMUNE DEFICIENCY; LEUKOPENIA; LYMPHOCYTOPENIA; MACROPHAGE ACTIVATION; NONHUMAN; OXYGEN CONSUMPTION; PROTEINURIA; RETINA MACULA AGE RELATED DEGENERATION; REVIEW; SIGNAL TRANSDUCTION; THROMBOSIS; TUMOR VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANGIOPOIETINS; ANTINEOPLASTIC AGENTS; CYTOKINES; DRUG RESISTANCE, NEOPLASM; FIBROBLAST GROWTH FACTORS; HUMANS; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MATRIX METALLOPROTEINASES; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PREGNANCY PROTEINS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84863867875     PISSN: 00229717     EISSN: 18801293     Source Type: Journal    
DOI: 10.2302/kjm.61.47     Document Type: Review

References (72)

1. Carmeliet P: Angiogenesis in life, disease and medicine. Nature 2005; 438: 932-936. [Medline] [CrossRef]
2. Risau W: Mechanisms of angiogenesis. Nature 1997; 386: 671-674. [Medline] [CrossRef]
3. Jain RK: Molecular regulation of vessel maturation. Nat Med 2003; 9: 685-693. [Medline] [CrossRef]
4. Ide AG, Baker NH, Warren SL: Vascularization of the Brown Pearce rabbit epithelioma transplant as seen in the transparent ear chamber. AJR Am J Roentgenol 1939; 42: 891-899.
5. Algire GH, Chalkley HW, Legallais FY, Park HD: Vascular reactions of normal and malignant tissues in vivo. I. Vascular reactions of mice to wounds and to normal and neoplastic transplants. J Natl Cancer Inst 1945; 6: 73-85.
6. Folkman J: Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285: 1182-1186. [Medline] [CrossRef]
7. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF: Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983; 219: 983-985. [Medline] [CrossRef]
8. Ferrara N: VEGF-A: a critical regulator of blood vessel growth. Eur Cytokine Netw 2009; 20: 158-163. [Medline]
9. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E: Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 1998; 394: 485-490. [Medline] [CrossRef]
10. Semenza GL, Agani F, Iyer N, Kotch L, Laughner E, Leung S, Yu A: Regulation of cardiovascular development and physiology by hypoxia-inducible factor 1. Ann N Y Acad Sci 1999; 874: 262-268. [Medline] [CrossRef]
11. Fukumura D, Xavier R, Sugiura T, Chen Y, Park EC, Lu N, Selig M, Nielsen G, Taksir T, Jain RK, Seed B: Tumor induction of VEGF promoter activity in stromal cells. Cell 1998; 94: 715-725. [Medline] [CrossRef]
12. Kim KJ, Li B, Winer J, Armanini M, Gillett N, Phillips HS, Ferrara N: Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 1993; 362: 841-844. [Medline] [CrossRef]
13. Ferrara N, Kerbel RS: Angiogenesis as a therapeutic target. Nature 2005; 438: 967-974. [Medline] [CrossRef]
14. Gragoudas ES, Adamis AP, Cunningham ET Jr, Feinsod M, Guyer DR: Pegaptanib for neovascular age-related macular degeneration. N Engl J Med 2004; 351: 2805-2816. [Medline] [CrossRef]
15. Carmeliet P, Jain RK: Molecular mechanisms and clinical applications of angiogenesis. Nature 2011; 473: 298-307. [Medline] [CrossRef]
16. Bergers G, Hanahan D: Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 2008; 8: 592-603. [Medline] [CrossRef]
17. Mancuso MR, Davis R, Norberg SM, O'Brien S, Sennino B, Nakahara T, Yao VJ, Inai T, Brooks P, Freimark B, Shalinsky DR, Hu-Lowe DD, McDonald DM: Rapid vascular regrowth in tumors after reversal of VEGF inhibition. J Clin Invest 2006; 116: 2610-2621. [Medline] [CrossRef]
18. Verheul HM, Pinedo HM: Possible molecular mechanisms involved in the toxicity of angiogenesis inhibition. Nat Rev Cancer 2007; 7: 475-485. [Medline] [CrossRef]
19. Ratner M: Genentech discloses safety concerns over Avastin. Nat Biotechnol 2004; 22: 1004-1198. [Medline] [CrossRef]
20. Maharaj AS, Walshe TE, Saint-Geniez M, Venkatesha S, Maldonado AE, Himes NC, Matharu KS, Karumanchi SA, D'Amore PA: VEGF and TGF-beta are required for the maintenance of the choroid plexus and ependyma. J Exp Med 2008; 205: 491-501. [Medline] [CrossRef]
21. Lee S, Chen TT, Barber CL, Jordan MC, Murdock J, Desai S, Ferrara N, Nagy A, Roos KP, Iruela-Arispe ML: Autocrine VEGF signaling is required for vascular homeostasis. Cell 2007; 130: 691-703. [Medline] [CrossRef]
22. Kamba T, McDonald DM: Mechanisms of adverse effects of anti-VEGF therapy for cancer. Br J Cancer 2007; 96: 1788-1795. [Medline] [CrossRef]
23. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber HP, Kikkawa Y, Miner JH, Quaggin SE: Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 2003; 111: 707-716. [Medline]
24. Gerber HP, Malik AK, Solar GP, Sherman D, Liang XH, Meng G, Hong K, Marsters JC, Ferrara N: VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 2002; 417: 954-958. [Medline] [CrossRef]
25. Yang JC, Haworth L, Sherry RM, Hwu P, Schwartzentruber DJ, Topalian SL, Steinberg SM, Chen HX, Rosenberg SA: A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med 2003; 349: 427-434 The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. [Medline] [CrossRef]
26. Murakami M, Simons M: Fibroblast growth factor regulation of neovascularization. Curr Opin Hematol 2008; 15: 215-220. [Medline] [CrossRef]
27. Augustin HG, Koh GY, Thurston G, Alitalo K: Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol 2009; 10: 165-177. [Medline] [CrossRef]
28. Koh YJ, Kim HZ, Hwang SI, Lee JE, Oh N, Jung K, Kim M, Kim KE, Kim H, Lim NK, Jeon CJ, Lee GM, Jeon BH, Nam DH, Sung HK, Nagy A, Yoo OJ, Koh GY: Double antiangiogenic protein, DAAP, targeting VEGF-A and angiopoietins in tumor angiogenesis, metastasis, and vascular leakage. Cancer Cell 2010; 18: 171-184. [Medline] [CrossRef]
29. Saharinen P, Eklund L, Pulkki K, Bono P, Alitalo K: VEGF and angiopoietin signaling in tumor angiogenesis and metastasis. Trends Mol Med 2011; [Epub ahead of print].
30. Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A: Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 2010; 7: 150-161. [Medline] [CrossRef]
31. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS: Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009; 15: 232-239. [Medline] [CrossRef]
32. Pàez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Viñals F, Inoue M, Bergers G, Hanahan D, Casanovas O: Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15: 220-231. [Medline] [CrossRef]
33. Miles D, Harbeck N, Escudier B, Hurwitz H, Saltz L, Van Cutsem E, Cassidy J, Mueller B, Sirzén F: Disease course patterns after discontinuation of bevacizumab: pooled analysis of randomized phase III trials. J Clin Oncol 2010; 29: 83-88. [Medline] [CrossRef]
34. Padera TP, Kuo AH, Hoshida T, Liao S, Lobo J, Kozak KR, Fukumura D, Jain RK: Differential response of primary tumor versus lymphatic metastasis to VEGFR-2 and VEGFR-3 kinase inhibitors cediranib and vandetanib. Mol Cancer Ther 2008; 7: 2272-2279. [Medline] [CrossRef]
35. Gaengel K, Genove G, Armulik A, Betsholtz C: Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol 2009; 29: 630-638. [Medline] [CrossRef]
36. Hellberg C, Ostman A, Heldin CH: PDGF and vessel maturation. Recent Results Cancer Res 2010; 180: 103-114. [Medline] [CrossRef]
37. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, Fligelman B, Leversha M, Brennan C, Tabar V: 2010 Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010; 468: 829-833. [Medline] [CrossRef]
38. Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T, Maira G, Parati EA, Stassi G, Larocca LM, De Maria R: Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010; 468: 824-828. [Medline] [CrossRef]
39. Ferrara N: Role of myeloid cells in vascular endothelial growth factor-independent tumor angiogenesis. Curr Opin Hematol 2010; 17: 219-224. [Medline]
40. Kerbel RS, Yu J, Tran J, Man S, Viloria-Petit A, Klement G, Coomber BL, Rak J: Possible mechanisms of acquired resistance to anti-angiogenic drugs: implications for the use of combination therapy approaches. Cancer Metastasis Rev 2001; 20: 79-86. [Medline] [CrossRef]
41. Naik E, O'Reilly LA, Asselin-Labat ML, Merino D, Lin A, Cook M, Coultas L, Bouillet P, Adams JM, Strasser A: Destruction of tumor vasculature and abated tumor growth upon VEGF blockade is driven by proapoptotic protein Bim in endothelial cells. J Exp Med 2011; 208: 1351-1358. [Medline] [CrossRef]
42. Lu C, Bonome T, Li Y, Kamat AA, Han LY, Schmandt R, Coleman RL, Gershenson DM, Jaffe RB, Birrer MJ, Sood AK: Gene alterations identified by expression profiling in tumor-associated endothelial cells from invasive ovarian carcinoma. Cancer Res 2007; 67: 1757-1768. [Medline] [CrossRef]
43. Lu C, Han HD, Mangala LS, Ali-Fehmi R, Newton CS, Ozbun L, Armaiz-Pena GN, Hu W, Stone RL, Munkarah A, Ravoori MK, Shahzad MM, Lee JW, Mora E, Langley RR, Carroll AR, Matsuo K, Spannuth WA, Schmandt R, Jennings NB, Goodman BW, Jaffe RB, Nick AM, Kim HS, Guven EO, Chen YH, Li LY, Hsu MC, Coleman RL, Calin GA, Denkbas EB, Lim JY, Lee JS, Kundra V, Birrer MJ, Hung MC, Lopez-Berestein G, Sood AK: Regulation of tumor angiogenesis by EZH2. Cancer Cell 2010; 18: 185-197. [Medline] [CrossRef]
44. Sato Y, Sonoda H: The vasohibin family: a negative regulatory system of angiogenesis genetically programmed in endothelial cells. Arterioscler Thromb Vasc Biol 2007; 27: 37-41. [Medline] [CrossRef]
45. Yoshida H, Hayashi S, Kunisada T, Ogawa M, Nishikawa S, Okamura H, Sudo T, Shultz LD, Nishikawa S. Nature 1990; 345: 442-444. [Medline] [CrossRef]
46. Cecchini MG, Dominguez MG, Mocci S, Wetterwald A, Felix R, Fleisch H, Chisholm O, Hofstetter W, Pollard JW, Stanley ER: Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 1994; 120: 1357-1372. [Medline]
47. Kubota Y, Takubo K, Shimizu T, Ohno H, Kishi K, Shibuya M, Saya H, Suda T: M-CSF inhibition selectively targets pathological angiogenesis and lymphangiogenesis. J Exp Med 2009; 206: 1089-1102. [Medline] [CrossRef]
48. Fantin A, Vieira JM, Gestri G, Denti L, Schwarz Q, Prykhozhij S, Peri F, Wilson SW, Ruhrberg C: Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 2010; 116: 829-840. [Medline] [CrossRef]
49. Rymo SF, Gerhardt H, Wolfhagen Sand F, Lang R, Uv A, Betsholtz C: A two-way communication between microglial cells and angiogenic sprouts regulates angiogenesis in aortic ring cultures. PLoS ONE 2011; 6: e15846. [Medline] [CrossRef]
50. Qian BZ, Pollard JW: Macrophage diversity enhances tumor progression and metastasis. Cell 2010; 141: 39-51. [Medline] [CrossRef]
51. Mantovani A, Sica A: Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol 2010; 22: 231-237. [Medline] [CrossRef]
52. Sica A, Bronte V: Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007; 117: 1155-1166. [Medline] [CrossRef]
53. Rolny C, Mazzone M, Tugues S, Laoui D, Johansson I, Coulon C, Squadrito ML, Segura I, Li X, Knevels E, Costa S, Vinckier S, Dresselaer T, Åkerud P, De Mol M, Salomäki H, Phillipson M, Wyns S, Larsson E, Buysschaert I, Botling J, Himmelreich U, Van Ginderachter JA, De Palma M, Dewerchin M, Claesson-Welsh L, Carmeliet P: HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 2011; 19: 31-44. [Medline] [CrossRef]
54. Werno C, Menrad H, Weigert A, Dehne N, Goerdt S, Schledzewski K, Kzhyshkowska J, Brüne B: Knockout of HIF-1α in tumor-associated macrophages enhances M2 polarization and attenuates their pro-angiogenic responses. Carcinogenesis 2010; 31: 1863-1872. [Medline] [CrossRef]
55. Liao X, Sharma N, Kapadia F, Zhou G, Lu Y, Hong H, Paruchuri K, Mahabeleshwar GH, Dalmas E, Venteclef N, Flask CA, Kim J, Doreian BW, Lu KQ, Kaestner KH, Hamik A, Clément K, Jain MK: Krüppel-like factor 4 regulates macrophage polarization. J Clin Invest 2011; 121: 2736-2749. [Medline] [CrossRef]
56. Whyte CS, Bishop ET, Rückerl D, Gaspar-Pereira S, Barker RN, Allen JE, Rees AJ, Wilson HM: Suppressor of cytokine signaling (SOCS)1 is a key determinant of differential macrophage activation and function. J Leukoc Biol 2011; [Epub ahead of print].
57. Lin EY, Li JF, Gnatovskiy L, Deng Y, Zhu L, Grzesik DA, Qian H, Xue XN, Pollard JW: Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res 2006; 66: 11238-11246. [Medline] [CrossRef]
58. Okuno Y, Nakamura-Ishizu A, Kishi K, Suda T, Kubota Y: Bone marrow-derived cells serve as proangiogenic macrophages but not endothelial cells in wound healing. Blood 2011; 117: 5264-5272. [Medline] [CrossRef]
59. Baluk P, Morikawa S, Haskell A, Mancuso M, McDonald DM: Abnormalities of basement membrane on blood vessels and endothelial sprouts in tumors. Am J Pathol 2003; 163: 1801-1815. [Medline] [CrossRef]
60. Jain RK: Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005; 307: 58-62. [Medline] [CrossRef]
61. Kashiwagi S, Tsukada K, Xu L, Miyazaki J, Kozin SV, Tyrrell JA, Sessa WC, Gerweck LE, Jain RK, Fukumura D: Perivascular nitric oxide gradients normalize tumor vasculature. Nat Med 2008; 14: 255-257. [Medline] [CrossRef]
62. Mazzone M, Dettori D, Leite de Oliveira R, Loges S, Schmidt T, Jonckx B, Tian YM, Lanahan AA, Pollard P, Ruiz de Almodovar C, De Smet F, Vinckier S, Aragonés J, Debackere K, Luttun A, Wyns S, Jordan B, Pisacane A, Gallez B, Lampugnani MG, Dejana E, Simons M, Ratcliffe P, Maxwell P, Carmeliet P: Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 2009; 136: 839-5. [Medline] [CrossRef]
63. St Croix B, Rago C, Velculescu V, Traverso G, Romans KE, Montgomery E, Lal A, Riggins GJ, Lengauer C, Vogelstein B, Kinzler KW: Genes expressed in human tumor endothelium. Science 2000; 289: 1197-1202. [Medline] [CrossRef]
64. Hida K, Klagsbrun M: A new perspective on tumor endothelial cells: unexpected chromosome and centrosome abnormalities. Cancer Res 2005; 65: 2507-2510. [Medline] [CrossRef]
65. Economopoulou M, Langer HF, Celeste A, Orlova VV, Choi EY, Ma M, Vassilopoulos A, Callen E, Deng C, Bassing CH, Boehm M, Nussenzweig A, Chavakis T: Histone H2AX is integral to hypoxia-driven neovascularization. Nat Med 2009; 15: 553-558. [Medline] [CrossRef]
66. Fischer C, Jonckx B, Mazzone M, Zacchigna S, Loges S, Pattarini L, Chorianopoulos E, Liesenborghs L, Koch M, De Mol M, Autiero M, Wyns S, Plaisance S, Moons L, van Rooijen N, Giacca M, Stassen JM, Dewerchin M, Collen D, Carmeliet P: Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 2007; 131: 463-475. [Medline] [CrossRef]
67. Casanovas O, Hicklin DJ, Bergers G, Hanahan D: Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005; 8: 299-309. [Medline] [CrossRef]
68. Kubota Y, Takubo K, Hirashima M, Nagoshi N, Kishi K, Okuno Y, Nakamura-Ishizu A, Sano K, Murakami M, Ema M, Omatsu Y, Takahashi S, Nagasawa T, Shibuya M, Okano H, Suda T: Isolation and function of mouse tissue resident vascular precursors marked by myelin protein zero. J Exp Med 2011; 208: 949-960. [Medline] [CrossRef]
69. 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: Angiogenesis in acute and chronic leukemias and myelodysplastic syndromes. Blood 2000; 96: 2240-2245. [Medline]
70. Li WW, Hutnik M, Gehr G: Antiangiogenesis in haematological malignancies. Br J Haematol 2008; 143: 622-631. [Medline] [CrossRef]
71. Schmidt T, Kharabi Masouleh B, Loges S, Cauwenberghs S, Fraisl P, Maes C, Jonckx B, De Keersmaecker K, Kleppe M, Tjwa M, Schenk T, Vinckier S, Fragoso R, De Mol M, Beel K, Dias S, Verfaillie C, Clark RE, Brümmendorf TH, Vandenberghe P, Rafii S, Holyoake T, Hochhaus A, Cools J, Karin M, Carmeliet G, Dewerchin M, Carmeliet P: Loss or Inhibition of Stromal-Derived PlGF Prolongs Survival of Mice with Imatinib-Resistant Bcr-Abl1(+). Leukemia. Cancer Cell 2011; 19: 740-753. [Medline] [CrossRef]
72. Rakhra K, Bachireddy P, Zabuawala T, Zeiser R, Xu L, Kopelman A, Fan AC, Yang Q, Braunstein L, Crosby E, Ryeom S, Felsher DW: CD4(+) T cells contribute to the remodeling of the microenvironment required for sustained tumor regression upon oncogene inactivation. Cancer Cell 2010; 18: 485-498. [Medline] [CrossRef]