Targeting adrenomedullin receptors with systemic delivery of neutralizing antibodies inhibits tumor angiogenesis and suppresses growth of human tumor xenografts in mice

FASEB Journal

Volumn 23, Issue 10, 2009, Pages 3424-3435

  Kaafarani, Itidal ^a,b   Fernandez Sauze, Samantha ^a,b   Berenguer, Caroline ^a,b   Chinot, Olivier ^a,b   Delfino, Christine ^a,b   Dussert, Christophe ^a,b   Metellus, Philippe ^a,b   Boudouresque, Françoise ^a,b   Mabrouk, Kamel ^b   Grisoli, François ^d   Figarella Branger, Dominique ^a   Martin, Pierre Marie ^a,b,c   Ouafik, L'Houcine ^a,b,c  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE MARSEILLE   (France)

^d TIMONE HOSPITAL   (France)

Author keywords

CLR RAMP2; CLR RAMP3; Endothelial cells; Pericytes; Proangiogenic cells

Indexed keywords

ADRENOMEDULLIN RECEPTOR; ALPHA ADRENOMEDULLIN RECEPTOR; MATRIGEL; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL PROLIFERATION; CELL STRAIN HT29; CHANNEL GATING; COLORECTAL CANCER; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; GLIOBLASTOMA; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LUNG CANCER; MACROPHAGE; MOUSE; MYELOID PROGENITOR CELL; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; NUDE MOUSE; PERICYTE; PRIORITY JOURNAL; TUMOR CELL; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; WESTERN BLOTTING;

MUS;

EID: 70349659021     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-127852     Document Type: Article

References (35)

1. Carmeliet, P., and Jain, R. K. (2000) Angiogenesis in cancer and other diseases. Nature 407, 249-257
2. Hanahan, D., and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86, 353-364 (Pubitemid 26272076)
3. De Palma, M., Venneri, M. A., Roca, C., and Naldini, L. (2003) Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat. Med. 9, 789-795 (Pubitemid 36749231)
4. Jiang, Y., Jahagirdar, B. N., Reinhardt, R. L., Schwartz, R. E., Keene, C. D., Ortiz-Gonzalez, X. R., Reyes, M., Lenvik, T., Lund, T., Blackstad, M., Du, J., Aldrich, S., Lisberg, A., Low, W. C., Largaespada, D. A., and Verfaillie, C. M. (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418, 41-49 (Pubitemid 34742565)
5. Dvorak, H. F. (2002) Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J. Clin. Oncol. 20, 4368-4380
6. Plate, K. H., Breier, G., Weich, H. A., and Risau, W. (1992) Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 359, 845-848
7. Folkman, J. (2007) Angiogenesis: an organizing principle for drug discovery? Nat. Rev. Drug Discov. 6, 273-286 (Pubitemid 46505878)
8. Neri, D., and Bicknell, R. (2005) Tumour vascular targeting. Nat. Rev. Cancer 5, 436-446
9. Klagsbrun, M., and D'Amore, P. A. (1991) Regulators of angiogenesis. Annu. Rev. Physiol. 53, 217-239
10. Ouafik, L., Sauze, S., Boudouresque, F., Chinot, O., Delfino, C., Fina, F., Vuaroqueaux, V., Dussert, C., Palmari, J., Dufour, H., Grisoli, F., Casellas, P., Brunner, N., and Martin, P. M. (2002) Neutralization of adrenomedullin inhibits the growth of human glioblastoma cell lines in vitro and suppresses tumor xenograft growth in vivo. Am. J. Pathol. 160, 1279-1292 (Pubitemid 34411632)
11. Fernandez-Sauze, S., Delfino, C., Mabrouk, K., Dussert, C., Chinot, O., Martin, P. M., Grisoli, F., Ouafik, L., and Boudouresque, F. (2004) Effects of adrenomedullin on endothelial cells in the multistep process of angiogenesis: involvement of CRLR/ RAMP2 and CRLR/RAMP3 receptors. Int. J. Cancer 108, 797-804 (Pubitemid 38112605)
12. Nikitenko, L. L., Fox, S. B., Kehoe, S., Rees, M. C., and Bicknell, R. (2006) Adrenomedullin and tumour angiogenesis. Br. J. Cancer 94, 1-7
13. Hinson, J. P., Kapas, S., and Smith, D. M. (2000) Adrenomedullin, a multifunctional regulatory peptide. Endocr. Rev. 21, 138-167
14. Lopez, J., and Martinez, A. (2002) Cell and molecular biology of the multifunctional peptide, adrenomedullin. Int. Rev. Cytol. 221, 1-92 (Pubitemid 35429860)
15. Kapas, S., and Clark, A. J. (1995) Identification of an orphan receptor gene as a type 1 calcitonin gene-related peptide receptor. Biochem. Biophys. Res. Commun. 217, 832-838 (Pubitemid 26019731)
16. Kapas, S., Catt, K. J., and Clark, A. J. (1995) Cloning and expression of cDNA encoding a rat adrenomedullin receptor. J. Biol. Chem. 270, 25344-25347
17. Njuki, F., Nicholl, C. G., Howard, A., Mak, J. C., Barnes, P. J., Girgis, S. I., and Legon, S. (1993) A new calcitonin-receptor-like sequence in rat pulmonary blood vessels. Clin. Sci. (Lond.) 85, 385-388 (Pubitemid 23308448)
18. McLatchie, L. M., Fraser, N. J., Main, M. J., Wise, A., Brown, J., Thompson, N., Solari, R., Lee, M. G., and Foord, S. M. (1998) RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393, 333-339 (Pubitemid 28269699)
19. Caron, K. M., and Smithies, O. (2001) Extreme hydrops fetalis and cardiovascular abnormalities in mice lacking a functional adrenomedullin gene. Proc. Natl. Acad. Sci. U. S. A. 98, 615-619
20. Shindo, T., Kurihara, Y., Nishimatsu, H., Moriyama, N., Kakoki, M., Wang, Y., Imai, Y., Ebihara, A., Kuwaki, T., Ju, K. H., Minamino, N., Kangawa, K., Ishikawa, T., Fukuda, M., Akimoto, Y., Kawakami, H., Imai, T., Morita, H., Yazaki, Y., Nagai, R., Hirata, Y., and Kurihara, H. (2001) Vascular abnormalities and elevated blood pressure in mice lacking adrenomedullin gene. Circulation 104, 1964-1971 (Pubitemid 32983242)
21. Fritz-Six, K. L., Dunworth, W. P., Li, M., and Caron, K. M. (2008) Adrenomedullin signaling is necessary for murine lymphatic vascular development. J. Clin. Invest. 118, 40-50
22. Ichikawa-Shindo, Y., Sakurai, T., Kamiyoshi, A., Kawate, H., Iinuma, N., Yoshizawa, T., Koyama, T., Fukuchi, J., Iimuro, S., Moriyama, N., Kawakami, H., Murata, T., Kangawa, K., Nagai, R., and Shindo, T. (2008) The GPCR modulator protein RAMP2 is essential for angiogenesis and vascular integrity. J. Clin. Invest. 118, 29-39
23. Miller, M. J., Martinez, A., Unsworth, E. J., Thiele, C. J., Moody, T. W., Elsasser, T., and Cuttitta, F. (1996) Adrenomedullin expression in human tumor cell lines. Its potential role as an autocrine growth factor. J. Biol. Chem. 271, 23345-23351
24. Rocchi, P., Boudouresque, F., Zamora, A. J., Muracciole, X., Lechevallier, E., Martin, P. M., and Ouafik, L. (2001) Expression of adrenomedullin and peptide amidation activity in human prostate cancer and in human prostate cancer cell lines. Cancer Res. 61, 1196-1206 (Pubitemid 32174443)
25. Ramachandran, V., Arumugam, T., Hwang, R. F., Greenson, J. K., Simeone, D. M., and Logsdon, C. D. (2007) Adrenomedullin is expressed in pancreatic cancer and stimulates cell proliferation and invasion in an autocrine manner via the adrenomedullin receptor, ADMR. Cancer Res. 67, 2666-2675 (Pubitemid 46548954)
26. Keleg, S., Kayed, H., Jiang, X., Penzel, R., Giese, T., Buchler, M. W., Friess, H., and Kleeff, J. (2007) Adrenomedullin is induced by hypoxia and enhances pancreatic cancer cell invasion. Int. J. Cancer 121, 21-32 (Pubitemid 46759489)
27. Cuttitta, F., Pio, R., Garayoa, M., Zudaire, E., Julian, M., Elsasser, T. H., Montuenga, L. M., and Martinez, A. (2002) Adrenomedullin functions as an important tumor survival factor in human carcinogenesis. Microsc. Res. Tech. 57, 110-119 (Pubitemid 34438617)
28. Ishikawa, T., Chen, J., Wang, J., Okada, F., Sugiyama, T., Kobayashi, T., Shindo, M., Higashino, F., Katoh, H., Asaka, M., Kondo, T., Hosokawa, M., and Kobayashi, M. (2003) Adrenomedullin antagonist suppresses in vivo growth of human pancreatic cancer cells in SCID mice by suppressing angiogenesis. Oncogene 22, 1238-1242 (Pubitemid 36363387)
29. Moody, T. W., Miller, M. J., Martinez, A., Unsworth, E., and Cuttitta, F. (1997) Adrenomedullin binds with high affinity, elevates cyclic AMP, and stimulates c-fos mRNA in C6 glioma cells. Peptides 18, 1111-1115 (Pubitemid 28026878)
30. Weidner, N., Semple, J. P., Welch, W. R., and Folkman, J. (1991) Tumor angiogenesis and metastasis- correlation in invasive breast carcinoma. N. Engl. J. Med. 324, 1-8 (Pubitemid 24058195)
31. Kerbel, R., and Folkman, J. (2002) Clinical translation of angiogenesis inhibitors. Nat. Rev. Cancer 2, 727-739
32. Hirschi, K. K., and D'Amore, P. A. (1996) Pericytes in the microvasculature. Cardiovasc. Res. 32, 687-698
33. Hellstrom, M., Gerhardt, H., Kalen, M., Li, X., Eriksson, U., Wolburg, H., and Betsholtz, C. (2001) Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J. Cell Biol. 153, 543-553 (Pubitemid 34280141)
34. Zudaire, E., Martinez, A., Garayoa, M., Pio, R., Kaur, G., Woolhiser, M. R., Metcalfe, D. D., Hook, W. A., Siraganian, R. P., Guise, T. A., Chirgwin, J. M., and Cuttitta, F. (2006) Adrenomedullin is a cross-talk molecule that regulates tumor and mast cell function during human carcinogenesis. Am. J. Pathol. 168, 280-291 (Pubitemid 43062580)
35. Drew, E., Merkens, H., Chelliah, S., Doyonnas, R., and Mc- Nagny, K. M. (2002) CD34 is a specific marker of mature murine mast cells. Exp. Hematol. 30, 1211-1218