Semaphorin 3A overcomes cancer hypoxia and metastatic dissemination induced by antiangiogenic treatment in mice

Journal of Clinical Investigation

Volumn 122, Issue 5, 2012, Pages 1832-1848

  Maione, Federica ^a   Capano, Stefania ^a   Regano, Donatella ^a   Zentilin, Lorena ^b   Giacca, Mauro ^b   Casanovas, Oriol ^c   Bussolino, Federico ^a,d   Serini, Guido ^a,d   Giraudo, Enrico ^a,d  

^a UNIVERSITY OF TURIN   (Italy)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^c CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MONOCLONAL ANTIBODY DC101; PARVOVIRUS VECTOR; SCATTER FACTOR RECEPTOR; SEMAPHORIN 3A; SUNITINIB;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIANGIOGENIC THERAPY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLOOD VESSEL PERFORATION; BLOOD VESSEL PERMEABILITY; CANCER CELL; CANCER INVASION; CANCER RESISTANCE; CANCER SURVIVAL; CANCER TISSUE; CONTROLLED STUDY; DISTANT METASTASIS; DRUG BIOAVAILABILITY; DRUG EFFECT; DRUG POTENTIATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HYPOXEMIA; LIVER METASTASIS; LUNG METASTASIS; METASTASIS; METASTASIS INHIBITION; MOUSE; NONHUMAN; PANCREATIC NEUROENDOCRINE TUMOR; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE OXYGENATION; TUMOR BLOOD FLOW; TUMOR VASCULARIZATION; UTERINE CERVIX CARCINOMA;

ANGIOGENESIS INHIBITORS; ANIMALS; CELL HYPOXIA; COMBINED MODALITY THERAPY; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE THERAPY; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INDOLES; LIVER NEOPLASMS; LYMPHATIC METASTASIS; MICE; MICE, TRANSGENIC; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROENDOCRINE TUMORS; NF-KAPPA B; PANCREATIC NEOPLASMS; PERICYTES; PROTO-ONCOGENE PROTEINS C-MET; PYRROLES; RECOMBINANT PROTEINS; SEMAPHORIN-3A; TUMOR BURDEN; UTERINE CERVICAL NEOPLASMS;

EID: 84860591982     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI58976     Document Type: Article

References (52)

1. Folkman J. Angiogenesis. Annu Rev Med. 2006;57:1-18.
2. Duda DG, Batchelor TT, Willett CG, Jain RK. VEGF-targeted cancer therapy strategies: current progress, hurdles and future prospects. Trends Mol Med. 2007;13(6):223-230. (Pubitemid 46836870)
3. Rapisarda A, Melillo G. Role of the hypoxic tumor microenvironment in the resistance to anti-angiogenic therapies. Drug Resist Updat. 2009;12(3):74-80.
4. 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(4):299-309. (Pubitemid 41443415)
5. Baluk P, Hashizume H, McDonald DM. Cellular abnormalities of blood vessels as targets in cancer. Curr Opin Genet Dev. 2005;15(1):102-111. (Pubitemid 40127638)
6. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307(5706):58-62. (Pubitemid 40093472)
7. Semenza GL. Hypoxia and cancer. Cancer Metastasis Rev. 2007;26(2):223-224. (Pubitemid 47101662)
8. Sabbah M, et al. Molecular signature and therapeutic perspective of the epithelial-to-mesenchymal transitions in epithelial cancers. Drug Resist Updat. 2008;11(4-5):123-151.
9. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell. 2003;3(4):347-361. (Pubitemid 38340304)
10. Paez-Ribes M, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009;15(3):220-231.
11. 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(3):232-239.
12. Galluzzo M, Pennacchietti S, Rosano S, Comoglio PM, Michieli P. Prevention of hypoxia by myoglobin expression in human tumor cells promotes differentiation and inhibits metastasis. J Clin Invest. 2009;119(4):865-875.
13. Maione F, et al. Semaphorin 3A is an endogenous angiogenesis inhibitor that blocks tumor growth and normalizes tumor vasculature in transgenic mouse models. J Clin Invest. 2009;119(11):3356-3372.
14. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer. 2008;8(8):592-603.
15. Christensen JG. A preclinical review of sunitinib, a multitargeted receptor tyrosine kinase inhibitor with anti-angiogenic and antitumour activities. Ann Oncol. 2007;18 suppl 10:x3-x10.
16. Casazza A, et al. Systemic and targeted delivery of semaphorin 3A inhibits tumor angiogenesis and progression in mouse tumor models. Arterioscler Thromb Vasc Biol. 2011;31(4):741-749.
17. Sathornsumetee S, et al. Tumor angiogenic and hypoxic profiles predict radiographic response and survival in malignant astrocytoma patients treated with bevacizumab and irinotecan. J Clin Oncol. 2008;26(2):271-278.
18. Winkler F, et al. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin- 1, and matrix metalloproteinases. Cancer Cell. 2004;6(6):553-563. (Pubitemid 40017699)
19. Goel S, et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev. 2011;91(3):1071-1121.
20. Bergers G, Song S, Meyer-Morse N, Bergsland E, Hanahan D. Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J Clin Invest. 2003;111(9):1287-1295. (Pubitemid 36554699)
21. Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 2009;28(1-2):15-33.
22. Perl AK, Wilgenbus P, Dahl U, Semb H, Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature. 1998;392(6672):190-193. (Pubitemid 28162793)
23. McConkey DJ, et al. Role of epithelial-to-mesenchymal transition (EMT) in drug sensitivity and metastasis in bladder cancer. Cancer Metastasis Rev. 2009;28(3-4):335-344.
24. Min C, Eddy SF, Sherr DH, Sonenshein GE. NF-kappaB and epithelial to mesenchymal transition of cancer. J Cell Biochem. 2008;104(3):733-744. (Pubitemid 351830825)
25. Sarkar FH, Li Y, Wang Z, Kong D. NF-kappaB signaling pathway and its therapeutic implications in human diseases. Int Rev Immunol. 2008;27(5):293-319.
26. van Uden P, Kenneth NS, Rocha S. Regulation of hypoxia-inducible factor-1alpha by NF-kappaB. Biochem J. 2008;412(3):477-484.
27. Cummins EP, et al. Prolyl hydroxylase-1 negatively regulates IkappaB kinase-beta, giving insight into hypoxia-induced NFkappaB activity. Proc Natl Acad Sci U S A. 2006;103(48):18154-18159. (Pubitemid 44871628)
28. Culver C, Sundqvist A, Mudie S, Melvin A, Xirodimas D, Rocha S. Mechanism of hypoxia-induced NF-kappaB. Mol Cell Biol. 2010;30(20):4901-4921.
29. Smith-McCune K, Zhu YH, Hanahan D, Arbeit J. Cross-species comparison of angiogenesis during the premalignant stages of squamous carcinogenesis in the human cervix and K14-HPV16 transgenic mice. Cancer Res. 1997;57(7):1294-1300. (Pubitemid 27152554)
30. Giraudo E, Inoue M, Hanahan D. An aminobisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J Clin Invest. 2004;114(5):623-633. (Pubitemid 39578752)
31. Arbeit JM, Howley PM, Hanahan D. Chronic estrogen-induced cervical and vaginal squamous carcinogenesis in human papillomavirus type 16 transgenic mice. Proc Natl Acad Sci U S A. 1996;93(7):2930-2935. (Pubitemid 26114341)
32. Seeber LM, et al. The role of hypoxia inducible factor-1alpha in gynecological cancer. Crit Rev Oncol Hematol. 2011;78(3):173-184.
33. Franco M, Paez-Ribes M, Cortez E, Casanovas O, Pietras K. Use of a mouse model of pancreatic neuroendocrine tumors to find pericyte biomarkers of resistance to anti-angiogenic therapy. Horm Metab Res. 2011;43(12):884-889.
34. Carmeliet P, Jain RK. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat Rev Drug Discov. 2011;10(6):417-427.
35. Goodman VL, et al. Approval summary: sunitinib for the treatment of imatinib refractory or intolerant gastrointestinal stromal tumors and advanced renal cell carcinoma. Clin Cancer Res. 2007;13(5):1367-1373. (Pubitemid 46450424)
36. Raymond E, et al. Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med. 2011;364(6):501-513.
37. Xian X, et al. Pericytes limit tumor cell metastasis. J Clin Invest. 2006;116(3):642-651. (Pubitemid 43326873)
38. Sorensen AG, et al. A "vascular normalization index" as potential mechanistic biomarker to predict survival after a single dose of cediranib in recurrent glioblastoma patients. Cancer Res. 2009;69(13):5296-5300.
39. Rapisarda A, et al. Schedule-dependent inhibition of hypoxia-inducible factor-1alpha protein accumulation, angiogenesis, and tumor growth by topotecan in U251-HRE glioblastoma xenografts. Cancer Res. 2004;64(19):6845-6848. (Pubitemid 39330988)
40. Vredenburgh JJ, et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol. 2007;25(30):4722-4729. (Pubitemid 350086473)
41. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011;473(7347):298-307.
42. Nam SY, et al. A hypoxia-dependent upregulation of hypoxia-inducible factor-1 by nuclear factorkappaB promotes gastric tumour growth and angiogenesis. Br J Cancer. 2011;104(1):166-174.
43. Shojaei F, et al. Bv8 regulates myeloid-cell-dependent tumour angiogenesis. Nature. 2007;450(7171):825-831. (Pubitemid 350231321)
44. Nozawa H, Chiu C, Hanahan D. Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci U S A. 2006;103(33):12493-12498. (Pubitemid 44267286)
45. Gocheva V, et al. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 2010;24(3):241-255.
46. Fitzpatrick SF, et al. An intact canonical NF-kappaB pathway is required for inflammatory gene expression in response to hypoxia. J Immunol. 2011;186(2):1091-1096.
47. Porta C, et al. Cellular and molecular pathways linking inflammation and cancer. Immunobiology. 2009;214(9-10):761-777.
48. Christensen J, Anderes K. Beyond VEGF: targeting tumor growth and angiogenesis via alternative mechanisms. Adv Exp Med Biol. 2008;610:43-53.
49. Abounader R, Laterra J. Scatter factor/hepatocyte growth factor in brain tumor growth and angiogenesis. Neuro Oncol. 2005;7(4):436-451. (Pubitemid 41555616)
50. Bussolino F, et al. Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J Cell Biol. 1992;119(3):629-641.
51. Hanahan D. Heritable formation of pancreatic beta-cell tumours in transgenic mice expressing recombinant insulin/simian virus 40 oncogenes. Nature. 1985;315(6015):115-122. (Pubitemid 15064530)
52. Coussens LM, Hanahan D, Arbeit JM. Genetic predisposition and parameters of malignant progression in K14-HPV16 transgenic mice. Am J Pathol. 1996;149(6):1899-1917. (Pubitemid 26415210)