Endothelial progenitor cells do not contribute to tumor endothelium in primary and metastatic tumors

International Journal of Cancer

Volumn 125, Issue 8, 2009, Pages 1771-1777

  Wickersheim, Anke ^a   Kerber, Mark ^a   De Miguel, Lourdes Sanchez ^a   Plate, Karl H ^b   Machein, Marcia Regina ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

Author keywords

Angiogenesis; Endothelial progenitor cells; Postnatal vasculogenenesis; Tumor vascularization; VEGF

Indexed keywords

GREEN FLUORESCENT PROTEIN; VASCULOTROPIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL WALL; BONE MARROW CELL; CANCER GENETICS; CANCER GROWTH; CANCER LOCALIZATION; CANCER MODEL; CARCINOGENESIS; CELL COUNT; CELL DIFFERENTIATION; CELL INFILTRATION; CELL MIGRATION; CELL STRUCTURE; CHIMERA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE SEVERITY; ENDOTHELIUM CELL; GENE OVEREXPRESSION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMAGE RECONSTRUCTION; IMMUNOFLUORESCENCE TEST; LEUKOCYTE MIGRATION; LEWIS CARCINOMA; LUNG METASTASIS; MELANOMA B16; MOUSE; NONHUMAN; ORTHOTOPIC TRANSPLANTATION; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN SYNTHESIS; THREE DIMENSIONAL IMAGING; TUMOR VASCULARIZATION; VASCULAR ENDOTHELIUM; ANIMAL; BONE MARROW; BONE MARROW TRANSPLANTATION; C57BL MOUSE; ENZYME IMMUNOASSAY; EXPERIMENTAL MELANOMA; LUNG TUMOR; MALE; METABOLISM; METASTASIS; PATHOLOGY; PROSTATE TUMOR; STEM CELL;

ANIMALS; BONE MARROW; BONE MARROW TRANSPLANTATION; CARCINOMA, LEWIS LUNG; ENDOTHELIUM, VASCULAR; HUMANS; IMMUNOENZYME TECHNIQUES; LUNG NEOPLASMS; MALE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; PROSTATIC NEOPLASMS; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 70349248272     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24605     Document Type: Article

References (43)

1. Carmeliet P. Angiogenesis in health and disease. Nat Med 2003;9:653-660
2. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, Iwaguro H, Inai Y, Silver M, Isner JM. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J 1999;18:3964-3972 (Pubitemid 29335849)
3. Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, Chadburn A, Heissig B, Marks W, Witte L, Wu Y, Hicklin D, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 2001;7:1194-1201 (Pubitemid 33063774)
4. Shaked Y, Ciarrocchi A, Franco M, Lee CR, Man S, Cheung AM, Hicklin DJ, Chaplin D, Foster FS, Benezra R, Kerbel RS. Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors. Science 2006;313:1785-1787 (Pubitemid 44454154)
5. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 1999;5:434-438 (Pubitemid 29180584)
6. Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med 2001;193:727-740
7. De Palma M, Venneri MA, Galli R, Sergi SL, Politi LS, Sampaolesi M, Naldini L. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 2005;8:211-226 (Pubitemid 41317592)
8. Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, Matrisian LM, Carbone DP, Lin PC. Expansion of myeloid immune suppressor Gr1CD11b1 cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004;6:409-421 (Pubitemid 39361441)
9. Spring H, Schuler T, Arnold B, Hammerling GJ, Ganss R. Chemokines direct endothelial progenitors into tumor neovessels. Proc Natl Acad Sci USA 2005;102:18111-18116 (Pubitemid 41798510)
10. Nolan DJ, Ciarrocchi A, Mellick AS, Jaggi JS, Bambino K, Gupta S, Heikamp E, McDevitt MR, Scheinberg DA, Benezra R, Mittal V. Bone marrow-derived endothelial progenitor cells are a major determinant of nascent tumor neovascularization. Genes Dev 2007;21:1546-1558 (Pubitemid 46955726)
11. Garcia-Barros M, Paris F, Cordon-Cardo C, Lyden D, Rafii S, Haimovitz-Friedman A, Fuks Z, Kolesnick R. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 2003;300:1155-1159 (Pubitemid 36583102)
12. Peters BA, Diaz LA, Polyak K, Meszler L, Romans K, Guinan EC, Antin JH, Myerson D, Hamilton SR, Vogelstein B, Kinzler KW, Lengauer C. Contribution of bone marrow-derived endothelial cells to human tumor vasculature. Nat Med 2005;11:261-262 (Pubitemid 40460552)
13. De Palma M, Venneri MA, Roca C, Naldini L. Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med 2003;9:789-795 (Pubitemid 36749231)
14. Taverna D, Moher H, Crowley D, Borsig L, Varki A, Hynes RO. Increased primary tumor growth in mice null for beta3- or beta3/beta5-integrins or selectins. Proc Natl Acad Sci USA 2004;101:763-768 (Pubitemid 38121032)
15. Machein MR, Renninger S, Lima-Hahn E, Plate KH. Minor contribution of bone marrow-derived endothelial progenitors to the vascularization of murine gliomas. Brain Pathol 2003;13:582-597 (Pubitemid 37420701)
16. Gothert JR, Gustin SE, van Eekelen JA, Schmidt U, Hall MA, Jane SM, Green AR, Gottgens B, Izon DJ, Begley CG. Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium. Blood 2004;104:1769-1777 (Pubitemid 39202286)
17. Purhonen S, Palm J, Rossi D, Kaskenpaa N, Rajantie I, Yla-Herttuala S, Alitalo K, Weissman IL, Salven P. Bone marrow-derived circulating endothelial precursors do not contribute to vascular endothelium and are not needed for tumor growth. Proc Natl Acad Sci USA 2008;105:6620-6625 (Pubitemid 351754556)
18. Gao D, Nolan DJ, Mellick AS, Bambino K, McDonnell K, Mittal V. Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science 2008;319:195-198
19. Asahara T, Murohara T, Sullivan A, Silver M, van der ZR, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997;275:964-967 (Pubitemid 27087709)
20. Gehling UM, Ergun S, Schumacher U, Wagener C, Pantel K, Otte M, Schuch G, Schafhausen P, Mende T, Kilic N, Kluge K, Schafer B, et al. In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 2000;95:3106-3112
21. Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M, Oz MC, Hicklin DJ, Witte L, Moore MA, Rafii S. Expression of VEGFR- 2 and AC133 by circulating human CD34(1) cells identifies a population of functional endothelial precursors. Blood 2000;95:952-958
22. Nishikawa SI, Nishikawa S, Hirashima M, Matsuyoshi N, Kodama H. Progressive lineage analysis by cell sorting and culture identifies FLK11VE-cadherin1 cells at a diverging point of endothelial and hemopoietic lineages. Development 1998;125:1747-1757 (Pubitemid 28256742)
23. Shaked Y, Bertolini F, Man S, Rogers MS, Cervi D, Foutz T, Rawn K, Voskas D, Dumont DJ, Ben David Y, Lawler J, Henkin J, et al. Genetic heterogeneity of the vasculogenic phenotype parallels angiogenesis: implications for cellular surrogate marker analysis of antiangiogenesis. Cancer Cell 2005;7:101-111 (Pubitemid 40126386)
24. Ruzinova MB, Schoer RA, Gerald W, Egan JE, Pandolfi PP, Rafii S, Manova K, Mittal V, Benezra R. Effect of angiogenesis inhibition by Id loss and the contribution of bone-marrow-derived endothelial cells in spontaneous murine tumors. Cancer Cell 2003;4:277-289 (Pubitemid 37329792)
25. Li H, Gerald WL, Benezra R. Utilization of bone marrow-derived endothelial cell precursors in spontaneous prostate tumors varies with tumor grade. Cancer Res 2004;64:6137-6143 (Pubitemid 39129414)
26. Duda DG, Cohen KS, Kozin SV, Perentes JY, Fukumura D, Scadden DT, Jain RK. Evidence for incorporation of bone marrow-derived endothelial cells into perfused blood vessels in tumors. Blood 2006;107:2774-2776
27. Hattori K, Dias S, Heissig B, Hackett NR, Lyden D, Tateno M, Hicklin DJ, Zhu Z, Witte L, Crystal RG, Moore MA, Rafii S. Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells. J Exp Med 2001;193:1005-1014 (Pubitemid 32436194)
28. Moore MA, Hattori K, Heissig B, Shieh JH, Dias S, Crystal RG, Rafii S. Mobilization of endothelial and hematopoietic stem and progenitor cells by adenovector-mediated elevation of serum levels of SDF-1, VEGF, and angiopoietin-1. Ann NY Acad Sci 2001;938:36-45. (Pubitemid 32620016)
29. Kalka C, Masuda H, Takahashi T, Gordon R, Tepper O, Gravereaux E, Pieczek A, Iwaguro H, Hayashi SI, Isner JM, Asahara T. Vascular endothelial growth factor(165) gene transfer augments circulating endothelial progenitor cells in human subjects. Circ Res 2000;86:1198-1202
30. Young PP, Hofling AA, Sands MS. VEGF increases engraftment of bone marrow-derived endothelial progenitor cells (EPCs) into vasculature of newborn murine recipients. Proc Natl Acad Sci USA 2002;99:11951-11956
31. Li B, Sharpe EE, Maupin AB, Teleron AA, Pyle AL, Carmeliet P, Young PP. VEGF and PlGF promote adult vasculogenesis by enhancing EPC recruitment and vessel formation at the site of tumor neovascularization. FASEB J 2006;20:1495-1497 (Pubitemid 44961985)
32. Conejo-Garcia JR, Benencia F, Courreges MC, Kang E, Mohamed- Hadley A, Buckanovich RJ, Holtz DO, Jenkins A, Na H, Zhang L, Wagner DS, Katsaros D, et al. Tumor-infiltrating dendritic cell precursors recruited by a beta-defensin contribute to vasculogenesis under the influence of Vegf-A. Nat Med 2004;10:950-958 (Pubitemid 39273736)
33. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Jung S, Chimenti S, Landsman L, Abramovitch R, Keshet E. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 2006;124:175-189 (Pubitemid 43069318)
34. Kerber M, Reiss Y, Wickersheim A, Jugold M, Kiessling F, Heil M, Tchaikovski V, Waltenberger J, Shibuya M, Plate KH, Machein MR. Flt-1 signaling in macrophages promotes glioma growth in vivo. Cancer Res 2008;68:7342-7351
35. Foster BA, Gingrich JR, Kwon ED, Madias C, Greenberg NM. Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res 1997;57:3325-3330 (Pubitemid 27355467)
36. Sasaki M, Wizigmann-Voos S, Risau W, Plate KH. Retrovirus producer cells encoding antisense VEGF prolong survival of rats with intracranial GS9L gliomas. Int J Dev Neurosci 1999;17:579-591 (Pubitemid 29421844)
37. Greenberg NM, DeMayo F, Finegold MJ, Medina D, Tilley WD, Aspinall JO, Cunha GR, Donjacour AA, Matusik RJ, Rosen JM. Prostate cancer in a transgenic mouse. Proc Natl Acad Sci USA 1995;92:3439-3443
38. Doki Y, Murakami K, Yamaura T, Sugiyama S, Misaki T, Saiki I. Mediastinal lymph node metastasis model by orthotopic intrapulmonary implantation of Lewis lung carcinoma cells in mice. Br J Cancer 1999;79:1121-1126 (Pubitemid 29087884)
39. Bertolini F, Shaked Y, Mancuso P, Kerbel RS. The multifaceted circulating endothelial cell in cancer: towards marker and target identification. Nat Rev Cancer 2006;6:835-845 (Pubitemid 44629895)
40. Zentilin L, Tafuro S, Zacchigna S, Arsic N, Pattarini L, Sinigaglia M, Giacca M. Bone marrow mononuclear cells are recruited to the sites of VEGF-induced neovascularization but are not incorporated into the newly formed vessels. Blood 2006;107:3546-3554
41. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999;85:221-228 (Pubitemid 29377293)
42. Ziegelhoeffer T, Fernandez B, Kostin S, Heil M, Voswinckel R, Helisch A, Schaper W. Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ Res 2004;94:230-238 (Pubitemid 38197456)
43. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 2003;9:702-712 (Pubitemid 36749219)