Tumor exploits alternative strategies to achieve vascularization

FASEB Journal

Volumn 25, Issue 9, 2011, Pages 2874-2882

  Bussolati, Benedetta ^a,b   Grange, Cristina ^a,b   Camussi, Giovanni ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Angiogenesis; Anti angiogenic therapy; Exosomes; Vasculogenesis

Indexed keywords

ALPHA4 INTEGRIN; BETA1 INTEGRIN; CD133 ANTIGEN; CD147 ANTIGEN; CD24 ANTIGEN; CD34 ANTIGEN; ENDOGLIN; ENDOSIALIN; ENDOSTATIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EPIDERMAL GROWTH FACTOR RECEPTOR; HLA G ANTIGEN; HU ANTIGEN; MESSENGER RNA; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE; NOTCH RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; TETRASPANIN; TETRASPANIN 8; THROMBOSPONDIN 1; TRANSCRIPTION FACTOR PAX2; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN D;

ANEUPLOIDY; ANGIOGENESIS; ANTIANGIOGENIC THERAPY; CANCER RESISTANCE; CANCER STEM CELL; CELL ACTIVATION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CHROMOSOME TRANSLOCATION; CYTOPLASM; DRUG RESISTANCE; ENDOTHELIUM CELL; EXOSOME; GENE EXPRESSION; GLIOMA CELL; HEMATOPOIETIC STEM CELL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CARCINOMA; METASTASIS; MUTATION; NONHUMAN; NUCLEAR REPROGRAMMING; OVARY CANCER; PERICYTE; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; TUMOR CELL; TUMOR ENDOTHELIAL CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; UPREGULATION;

ANGIOGENESIS INHIBITORS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 80052655345     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-180323     Document Type: Review

References (89)

1. Medvinsky, A., and Dzierzak, E. (1996) Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86, 897-906 (Pubitemid 26336794)
2. Zambidis, E. T., Sinka, L., Tavian, M., Jokubaitis, V., Park, T. S., Simmons, P., and Péault, B. (2007) Emergence of human angiohematopoietic cells in normal development and from cultured embryonic stem cells. Ann. N. Y. Acad. Sci. 1106, 223-232 (Pubitemid 47443046)
3. Folkman, J. (2002) Role of angiogenesis in tumor growth and metastasis. Semin. Oncol. 29, 15-18
4. Tepper, O. M., Capla, J. M., Galiano, R. D., Ceradini, D. J., Callaghan, M. J., Kleinman, M. E., and Gurtner, G. C. (2005) Adult vasculogenesis occurs through in situ recruitment, proliferation and tubulization of circulating bone marrow-derived cells. Blood 105, 1068-1077 (Pubitemid 40170877)
5. Ahn, G. O., and Brown, J. M. (2009) Role of endothelial progenitors and other bone marrow-derived cells in the development of the tumor vasculature. Angiogenesis 12, 159-164
6. Baluk, P., Hashizume, H., and McDonald, D. M. (2005) Cellular abnormalities of blood vessels as targets in cancer. Curr. Opin. Genet. Dev. 15, 102-111 (Pubitemid 40127638)
7. De Bock, K., Cauwenberghs, S., and Carmeliet, P. (2011) Vessel abnormalization: another hallmark of cancer? Molecular mechanisms and therapeutic implications. Curr. Opin. Genet. Dev. 21, 73-79
8. Hida, K., and Klagsbrun, M. (2005) A new perspective on tumor endothelial cells: unexpected chromosome and centrosome abnormalities. Cancer Res. 65, 2507-2510 (Pubitemid 40490041)
9. Hida, K., Hida, Y., Amin, D. N., Flint, A. F., Panigrahy, D., Morton, C. C., and Klagsbrun, M. (2004) Tumor-associated endothelial cells with cytogenetic abnormalities. Cancer Res. 64, 8249-8255 (Pubitemid 39491762)
10. Hida, K., Hida, Y., and Shindoh, M. (2008) Understanding tumor endothelial cell abnormalities to develop ideal antiangiogenic therapies. Cancer Sci. 99, 459-466 (Pubitemid 351228561)
11. Akino, T., Hida, K., Hida, Y., Tsuchiya, K., Freedman, D., Muraki, C., Ohga, N., Matsuda, K., Akiyama, K., Harabayashi, T., Shinohara, N., Nonomura, K., Klagsbrun, M., and Shindoh, M. (2009) Cytogenetic abnormalities of tumor-associated endothelial cells in human malignant tumors. Am. J. Pathol. 175, 2657-2667
12. Gunsilius, E., Duba, H. C., Petzer, A. L., Kähler, C. M., Grünewald, K., Stockhammer, G., Gabl, C., Dirnhofer, S., Clausen, J., and Gastl, G. (2000) Evidence from a leukaemia model for maintenance of vascular endothelium by bonemarrow- derived endothelial cells. Lancet 355, 1688-1691 (Pubitemid 30248482)
13. Streubel, B., Chott, A., Huber, D., Exner, M., Jäger, U., Wagner, O., and Schwarzinger, I. (2004) Lymphoma-specific genetic aberrations in microvascular endothelial cells in B-cell lymphomas. N. Engl. J. Med. 351, 250-259 (Pubitemid 38916042)
14. Rigolin, G. M., Fraulini, C., Ciccone, M., Mauro, E., Bugli, A. M., De Angeli, C., Negrini, M., Cuneo, A., and Castoldi, G. (2006) Neoplastic circulating endothelial cells in multiple myeloma with 13q14 deletion. Blood 107, 2531-2535 (Pubitemid 43345578)
15. Pezzolo, A., Parodi, F., Corrias, M. V., Cinti, R., Gambini, C., and Pistoia, V. (2007) Tumor origin of endothelial cells in human neuroblastoma. J. Clin. Oncol. 25, 376-383 (Pubitemid 350002985)
16. Ricci-Vitiani, L., Pallini, R., Biffoni, M., Todaro, M., Invernici, G., Cenci, T., Maira, G., Parati, E. A., Stassi, G., Larocca, L. M., and De Maria, R. (2010) Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 468, 824-828
17. Seaman, S., Stevens, J., Yang, M. Y., Logsdon, D., Graff-Cherry, C., and St Croix, B. (2007) Genes that distinguish physiological and pathological angiogenesis. Cancer Cell 11, 539-554 (Pubitemid 46856908)
18. St Croix, B., Rago, C., Velculescu, V., Traverso, G., Romans, K. E., Montgomery, E., Lal, A., Riggins, G. J., Lengauer, C., Vogelstein, B., and Kinzler, K. W. (2000) Genes expressed in human tumor endothelium. Science 289, 1197-1202 (Pubitemid 30650733)
19. Parker, B. S., Argani, P., Cook, B. P., Liangfeng, H., Chartrand, S. D., Zhang, M., Saha, S., Bardelli, A., Jiang, Y., St Martin, T. B., Nacht, M., Teicher, B. A., Klinger, K. W., Sukumar, S., and Madden, S. L. (2004) Alterations in vascular gene expression in invasive breast carcinoma. Cancer Res. 64, 7857-7866 (Pubitemid 39446919)
20. Madden, S. L., Cook, B. P., Nacht, M., Weber, W. D., Callahan, M. R., Jiang. Y., Dufault, M. R., Zhang, X., Zhang, W., Walter- Yohrling, J., Rouleau, C., Akmaev, V. R., Wang, C. J., Cao, X., St Martin, T. B., Roberts, B. L., Teicher, B. A., Klinger, K. W., Stan, R. V., Lucey, B., Carson-Walter, E. B., Laterra, J., and Walter, K. A. (2004) Vascular gene expression in nonneoplastic and malignant brain. Am. J. Pathol. 165, 601-608 (Pubitemid 38971389)
21. Van Beijnum, J. R., Dings, R. P., Van Der Linden, E., Zwaans, B. M., Ramaekers, F. C., Mayo, K. H., and Griffioen, A. W. (2006) Gene expression of tumor angiogenesis dissected: specific targeting of colon cancer angiogenic vasculature. Blood 108, 2339-2348 (Pubitemid 44497518)
22. Lu, C., Bonome, T., Li, Y., Kamat, A. A., Han, L. Y., Schmandt, R., Coleman, R. L., Gershenson, D. M., Jaffe, R. B., Birrer, M. J., and Sood, A. K. (2007) Gene alterations identified by expression profiling in tumor-associated endothelial cells from invasive ovarian carcinoma. Cancer Res. 67, 1757-1768 (Pubitemid 46383403)
23. Bhati, R., Patterson, C., Livasy, C. A., Fan, C., Ketelsen, D., Hu, Z., Reynolds, E., Tanner, C., Moore, D. T., Gabrielli, F., Perou, C. M., and Klauber-DeMore, N. (2008) Molecular characterization of human breast tumor vascular cells. Am. J. Pathol. 172, 1381-1390 (Pubitemid 351671550)
24. Buckanovich, R. J., Sasaroli, D., O'Brien-Jenkins, A., Botbyl, J., Hammond, R., Katsaros, D., Sandaltzopoulos, R., Liotta, L. A., Gimotty, P. A., and Coukos, G. (2007) Tumor vascular proteins as biomarkers in ovarian cancer. J. Clin. Oncol. 25, 852-861 (Pubitemid 350002886)
25. Nanda, A., Carson-Walter, E. B., Seaman, S., Barber, T. D., Stampfl, J., Singh, S., Vogelstein, B., Kinzler, K. W., and St Croix, B. (2004) TEM8 interacts with the cleaved C5 domain of collagen alpha 3(VI). Cancer Res. 64, 817-820 (Pubitemid 38176877)
26. Bussolati, B., Deambrosis, I., Russo, S., Deregibus, M. C., and Camussi, G. (2003) Altered angiogenesis and survival in human tumor-derived endothelial cells. FASEB J. 17, 1159-1161
27. Bussolati, B., Grange, C., Bruno, S., Buttiglieri, S., Deregibus, M. C., Tei, L., Aime, S., and Camussi, G. (2006) Neural-cell adhesion molecule (NCAM) expression by immature and tumor- derived endothelial cells favors cell organization into capillary- like structures. Exp. Cell. Res. 312, 913-924
28. Fonsato, V., Buttiglieri, S., Deregibus, M. C., Puntonieri, V., Bussolati, B., and Camussi, G. (2006) Expression of PAX2 in human renal tumor-derived endothelial cells sustains apoptosis resistance and angiogenesis. Am. J. Pathol. 168, 706-713 (Pubitemid 43271166)
29. Fonsato, V., Buttiglieri, S., Deregibus, M. C., Bussolati, B., Caselli, E., Di Luca, D., and Camussi, G. (2008) PAX2 expression by HHV-8-infected endothelial cells induced a proangiogenic and proinvasive phenotype. Blood 111, 2806-2815
30. Dudley, A. C., and Klagsbrun, M. (2009) Tumor endothelial cells have features of adult stem cells. Cell Cycle 8, 236-238
31. Miebach, S., Grau, S., Hummel, V., Rieckmann, P., Tonn, J. C., and Goldbrunner, R. H. (2006) Isolation and culture of microvascular endothelial cells from gliomas of different WHO grades. J. Neurooncol. 76, 39-48 (Pubitemid 43115757)
32. Kurosu, T., Ohga, N., Hida, Y., Maishi, N., Akiyama, K., Kakuguchi, W., Kuroshima, T., Kondo, M., Akino, T., Totsuka, Y., Shindoh, M., Higashino, F., and Hida, K. (2011) HuR keeps an angiogenic switch on by stabilising mRNA of VEGF and COX-2 in tumour endothelium. Br. J. Cancer 104, 819-829
33. Amin, D. N., Hida, K., Bielenberg, D. R., and Klagsbrun, M. (2006) Tumor endothelial cells express epidermal growth factor receptor (EGFR) but not ErbB3 and are responsive to EGF and to EGFR kinase inhibitors. Cancer Res. 66, 2173-2180
34. Bussolati, B., Assenzio, B., Deregibus, M. C., and Camussi, G. (2006) The proangiogenic phenotype of human tumor-derived endothelial cells depends on thrombospondin-1 downregulation via phosphatidylinositol 3-kinase/Akt pathway. J. Mol. Med. 84, 852-863 (Pubitemid 44477419)
35. Mangieri, D., Nico, B., Benagiano, V., De Giorgis, M., Vacca, A., and Ribatti, D. (2008) Angiogenic activity of multiple myeloma endothelial cells in vivo in the chick embryo chorioallantoic membrane assay is associated to a down-regulation in the expression of endogenous endostatin. J. Cell. Mol. Med. 12, 1023-1028 (Pubitemid 351718079)
36. Grange, C., Bussolati, B., Bruno, S., Fonsato, V., Sapino, A., and Camussi, G. (2006) Isolation and characterization of human breast tumor-derived endothelial cells. Oncol. Rep. 15, 381-386
37. Virrey, J. J., Golden, E. B., Sivakumar, W., Wang, W., Pen, L., Schönthal, A. H., Hofman, F. M., and Chen, T. C. (2009) Glioma-associated endothelial cells are chemoresistant to temozolomide. J. Neurooncol. 95, 13-22
38. Xiong, Y. Q., Sun, H. C., Zhang, W., Zhu, X. D., Zhuang, P. Y., Zhang, J. B., Wang, L., Wu, W. Z., Qin, L. X., and Tang, Z. Y. (2009) Human hepatocellular carcinoma tumor-derived endothelial cells manifest increased angiogenesis capability and drug resistance compared with normal endothelial cells. Clin. Cancer Res. 15, 4838-4846
39. Camussi, G., Deregibus, M. C., Bruno, S., Grange, C., Fonsato, V., and Tetta, C. (2011) Exosome/microvesicle-mediated epigenetic reprogramming of cells. Am. J. Cancer Res. 1, 98-110
40. Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A., and Ratajczak, M. Z. (2006) Membrane-derived microvesicles: important and underappreciated mediators of cellto- cell communication. Leukemia 20, 1487-1495 (Pubitemid 44264090)
41. Deregibus, M. C., Cantaluppi, V., Calogero, R., Lo Iacono, M., Tetta, C., Biancone, L., Bruno, S., Bussolati, B., and Camussi, G. (2007) Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110, 2440-2448 (Pubitemid 47523165)
42. Bruno, S., Grange, C., Deregibus, M. C., Calogero, R. A., Saviozzi, S., Collino, F., Morando, L., Busca, A., Falda, M., Bussolati, B., Tetta, C., and Camussi, G. (2009) Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J. Am. Soc. Nephrol. 20, 1053-1067
43. Collino, F., Deregibus, M. C., Bruno, S., Sterpone, L., Aghemo, G., Viltono, L., Tetta, C., and Camussi, G. (2010) Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS One 5, e11803
44. Valadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J., and Lötvall, J. O. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654-659 (Pubitemid 47214727)
45. Skog, J., Würdinger, T., Van Rijn, S., Meijer, D. H., Gainche, L., Sena-Esteves, M., Curry, W. T., Jr., Carter, B. S., Krichevsky, A. M., and Breakefield, X. O. (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10, 1470-1476
46. Castellana, D., Zobairi, F., Martinez, M. C., Panaro, M. A., Mitolo, V., Freyssinet, J. M., and Kunzelmann, C. (2009) Membrane microvesicles as actors in the establishment of a favorable prostatic tumoral niche: a role for activated fibroblasts and CX3CL1-CX3CR1 axis. Cancer Res. 69, 785-793
47. Wysoczynski, M., and Ratajczak, M. Z. (2009) Lung cancer secreted microvesicles: underappreciated modulators of microenvironment in expanding tumors. Int. J. Cancer 125, 1595-1603
48. Muralidharan-Chari, V., Clancy, J. W., Sedgwick, A., and D'Souza-Schorey, C. (2010) Microvesicles: mediators of extracellular communication during cancer progression. J. Cell Sci. 123, 1603-1611
49. Ratajczak, J., Miekus, K., Kucia, M., Zhang, J., Reca, R., Dvorak, P., and Ratajczak, M. Z. (2006) Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20, 847-856
50. Hong, B. S., Cho, J. H., Kim, H., Choi, E. J., Rho, S., Kim, J., Kim, J. H., Choi, D. S., Kim, Y. K., Hwang, D., and Gho, Y. S. (2009) Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells. BMC Genomics 25, 556
51. Balaj, L., Lessard, R., Dai, L., Cho, Y. J., Pomeroy, S. L., Breakefield, X. O., and Skog, J. (2011) Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat. Commun. 2, 180
52. Bergsmedh, A., Szeles, A., Henriksson, M., Bratt, A., Folkman, M. J., Spetz, A. L., and Holmgren, L. (2001) Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc. Natl. Acad. Sci. U. S. A. 98, 6407-6411 (Pubitemid 32488250)
53. Pelham, R. J., Rodgers, L., Hall, I., Lucito, R., Nguyen, K. C., Navin, N., Hicks, J., Mu, D., Powers, S., Wigler, M., and Botstein, D. (2006) Identification of alterations in DNA copy number in host stromal cells during tumor progression. Proc. Natl. Acad. Sci. U. S. A. 103, 19848-19853 (Pubitemid 46037519)
54. Baj-Krzyworzeka, M., Szatanek, R., Weglarczyk, K., Baran, J., Urbanowicz, B., Brański, P., Ratajczak, M. Z., and Zembala, M. (2006) Tumour-derived microvesicles carry several surface determinants and mRNA of tumour cells and transfer some of these determinants to monocytes. Cancer Immunol. Immunother. 55, 808-818
55. Millimaggi, D., Mari, M., D'Ascenzo, S., Carosa, E., Jannini, E. A., Zucker, S., Carta, G., Pavan, A., and Dolo, V. (2007) Tumor vesicle-associated CD147 modulates the angiogenic capability of endothelial cells. Neoplasia 9, 349-357 (Pubitemid 46608302)
56. Kim, C. W., Lee, H. M., Lee, T. H., Kang, C., Kleinman, H. K., and Gho, Y. S. (2002) Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res. 62, 6312-6317 (Pubitemid 35244486)
57. Nazarenko, I., Rana, S., Baumann, A., McAlear, J., Hellwig, A., Trendelenburg, M., Lochnit, G., Preissner, K. T., and Zöller, M. (2010) Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res. 70, 1668-1678
58. Marhaba, R., Klingbeil, P., Nuebel, T., Nazarenko, I., Buechler, M. W., and Zoeller, M. (2008) CD44 and EpCAM: cancerinitiating cell markers. Curr. Mol. Med. 8, 784-804
59. Al-Nedawi, K., Meehan, B., Kerbel, R. S., Allison, A. C., and Rak, J. (2009) Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc. Natl. Acad. Sci. U. S. A. 106, 3794-3799
60. Al-Nedawi, K., Meehan, B., Micallef, J., Lhotak, V., May, L., Guha, A., and Rak, J. (2008) Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 10, 619-624 (Pubitemid 351627382)
61. Sheldon, H., Heikamp, E., Turley, H., Dragovic, R., Thomas, P., Oon, C. E., Leek, R., Edelmann, M., Kessler, B., Sainson, R. C., Sargent, I., Li, J. L., and Harris, A. L. (2010) New mechanism for notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes. Blood 116, 2385-2394
62. Li Calzi, S., Neu, M. B., Shaw, L. C., Kielczewski, J. L., Moldovan, N. I., and Grant, M. B. (2010) EPCs and pathological angiogenesis: when good cells go bad. Microvasc. Res. 79, 207-216
63. Dudley, A. C., Udagawa, T., Melero-Martin, J. M., Shih, S. C., Curatolo, A., Moses, M. A., and Klagsbrun, M. (2010) Bone marrow is a reservoir for proangiogenic myelomonocytic cells but not endothelial cells in spontaneous tumors. Blood 116, 3367-3371
64. Asahara, T., Masuda, H., Takahashi, T., Kalka, C., Pastore, C., Silver, M., Kearne, M., Magner, M., and Isner, J. M. (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 85, 221-228 (Pubitemid 29377293)
65. Lyden, D., Hattori, K., Dias, S., Costa, C., Blaikie, P., Butros, L., Chadburn, A., Heissig, B., Marks, W., Witte, L., Wu, Y., Hicklin, D., Zhu, Z., Hackett, N. R., Crystal, R. G., Moore, M. A., Hajjar, K. A., Manova, K., Benezra, R., and Rafii, S. (2001) Impaired recruitment of bonemarrow- derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat. Med. 7, 1194-1201 (Pubitemid 33063774)
66. Patenaude, A., Parker, J., and Karsan, A. (2010) Involvement of endothelial progenitor cells in tumor vascularization. Microvasc. Res. 79, 217-223
67. Hill, P. A. (2010) Recipient origin of vasculature in renal cell carcinoma in a kidney allograft. Pathology 42, 479-480
68. Kioi, M., Vogel, H., Schultz, G., Hoffman, R. M., Harsh, G. R., Brown, and J. M. (2010) Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J. Clin. Invest. 120, 694-705
69. Collino, F., Revelli, A., Massobrio, M., Katsaros, D., Schmitt-Ney, M., Camussi, G., and Bussolati, B. (2009) Epithelial-mesenchymal transition of ovarian tumor cells induces an angiogenic monocyte cell population. Exp. Cell. Res. 315, 2982-2994
70. + renal progenitor cells contribute to tumor angiogenesis. Am. J. Pathol. 169, 2223-2235
71. Clarke, M. F., Dick, J. E., Dirks, P. B., Eaves, C. J., Jamieson, C. H., Jones, D. L., Visvader, J., Weissman, I. L., and Wahl, G. M. (2006) Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 66, 9339-9344
72. Al-Hajj, M., and Clarke, M. F. (2004) Self-renewal and solid tumor stem cells. Oncogene 23, 7274-7282 (Pubitemid 39382161)
73. Fang, D., Nguyen, T. K., Leishear, K., Finko, R., Kulp, A. N., Hotz, S., Van Belle, P. A., Xu, X., Elder, D. E., and Herlyn, M. (2005) A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 65, 328-337
74. Shen, R., Ye, Y., Chen, L., Yan, Q., Barsky, S. H., and Gao, J. X. (2008) Precancerous stem cells can serve as tumor vasculogenic progenitors. PLoS One 3, e1652
75. Bussolati, B., Grange, C., Sapino, A., and Camussi, G. (2009) Endothelial cell differentiation of human breast tumour stem/ progenitor cells. J. Cell. Mol. Med. 13, 309-319
76. Bussolati, B., Bruno, S., Grange, C., Ferrando, U., and Camussi, G. (2008) Identification of a tumor-initiating stem cell population in human renal carcinomas. FASEB J. 22, 3696-3705
77. Alvero, A. B., Fu, H. H., Holmberg, J., Visintin, I., Mor, L., Marquina, C. C., Oidtman, J., Silasi, D. A., and Mor, G. (2009) Stem-like ovarian cancer cells can serve as tumor vascular progenitors. Stem Cells 27, 2405-2413
78. Wang, R., Chadalavada, K., Wilshire, J., Kowalik, U., Hovinga, K. E., Geber, A., Fligelman, B., Leversha, M., Brennan, C., and Tabar, V. (2010) Glioblastoma stem-like cells give rise to tumour endothelium. Nature 468, 829-833
79. Pezzolo, A., Parodi, F., Marimpietri, D., Raffaghello, L., Cocco, C., Pistorio, A., Mosconi, M., Gambini, C., Cilli, M., Deaglio, S., Malavasi, F., and Pistoia, V. (2011) Oct-4(+)/Tenascin C(+) neuroblastoma cells serve as progenitors of tumor-derived endothelial cells. [E-pub ahead of print] Cell Res. doi: 10.1038/ cr.2011.38
80. Maniotis, A. J., Folberg, R., Hess, A., Seftor, E. A., Gardner, L. M., Pe'er, J., Trent, J. M., Meltzer, P. S., and Hendrix, M. J. (1999) Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am. J. Pathol. 155, 739-752 (Pubitemid 29426820)
81. Folberg, R., Hendrix, M. J., and Maniotis, A. J. (2000) Vasculogenic mimicry and tumor angiogenesis. Am. J. Pathol. 156, 361-381 (Pubitemid 30648785)
82. El Hallani, S., Boisselier, B., Peglion, F., Rousseau, A., Colin, C., Idbaih, A., Marie, Y., Mokhtari, K., Thomas, J. L., Eichmann, A., Delattre, J. Y., Maniotis, A. J., and Sanson, M. (2010) A new alternative mechanism in glioblastoma vascularization: tubular vasculogenic mimicry. Brain 133, 973-982
83. Yao, X. H., Ping, Y. F., and Bian, X. W. (2011) Contribution of cancer stem cells to tumor vasculogenic mimicry. Protein Cell 2, 266-272
84. Seftor, E. A., Meltzer, P. S., Schatteman, G. C., Gruman, L. M., Hess, A. R., Kirschmann, D. A., Seftor, R. E., and Hendrix, M. J. (2002) Expression of multiple molecular phenotypes by aggressive melanoma tumor cells: role in vasculogenic mimicry. Crit. Rev. Oncol. Hematol. 44, 17-27 (Pubitemid 35175468)
85. Ebos, J. M., Lee, C. R., and Kerbel, R. S. (2009) Tumor and host-mediated pathways of resistance and disease progression in response to antiangiogenic therapy. Clin. Cancer Res. 15, 5020-5025
86. Ribatti, D. (2010) The inefficacy of antiangiogenic therapies. J. Angiogenes. Res. 10, 2-27
87. Pàez-Ribes, M., Allen, E., Hudock, J., Takeda, T., Okuyama, H., Viñals, F., Inoue, M., Bergers, G., Hanahan, D., and Casanovas, O. (2009) Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15, 220-231
88. Ebos, J. M., Lee, C. R., Cruz-Munoz, W., Bjarnason, G. A., Christensen, J. G., and Kerbel, R. S. (2009) Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15, 232-239
89. Narayana, A., Kelly, P., Golfinos, J., Parker, E., Johnson, G., Knopp, E., Zagzag, D., Fischer, I., Raza, S., Medabalmi, P., Eagan, P., and Gruber, M. L. (2009) Antiangiogenic therapy using bevacizumab in recurrent high-grade glioma: impact on local control and patient survival. J. Neurosurg. 110, 173-180