Hematopoietic stem cells give rise to perivascular endothelial-like cells during brain tumor angiogenesis

Stem Cells and Development

Volumn 14, Issue 5, 2005, Pages 478-486

  Udani, V M ^a   Santarelli, J G ^a   Yung, Y C ^a   Wagers, A J ^b   Cheshier, S H ^a   Weissman, I L ^b   Tse, Victor ^a,c,d  

^a STANFORD UNIVERSITY MEDICAL CENTER   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SANTA CLARA VALLEY MEDICAL CENTER   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; CD11B ANTIGEN; CD3 ANTIGEN; CD34 ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CD5 ANTIGEN; CD8 ANTIGEN; ERYTHROCYTE ANTIGEN; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN G; VASCULOTROPIN RECEPTOR 2; VON WILLEBRAND FACTOR;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN TUMOR; CELL DIFFERENTIATION; CELL FUSION; CONTROLLED STUDY; CORPUS STRIATUM; FLUORESCENCE ACTIVATED CELL SORTER; GLIOMA CELL; HEMATOPOIETIC STEM CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PARENCHYMA; PHENOTYPE; PRIORITY JOURNAL; RAT; TRANSGENIC MOUSE; TUMOR GROWTH; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGENS; ANTIGENS, CD34; ANTIGENS, CD45; BIOLOGICAL MARKERS; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL LINEAGE; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GREEN FLUORESCENT PROTEINS; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, INBRED C57BL; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; RATS; TRANSPLANTATION CHIMERA;

ANIMALIA; MUS MUSCULUS;

EID: 28844502353     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2005.14.478     Document Type: Article

References (59)

1. + hematopoietic stem cells enhance tumor growth in a nonobese diabetic/severe combined immunodeficient mouse model of human non-Hodgkin's lymphoma. Cancer Res 61:1654-7659.
2. Choi K. (2002). The hemangioblast: a common progenitor of hematopoietic and endothelial cells. J Hematother Stem Cell Res 11:91-101.
3. Grant MB, WS May, S Caballero, GA Brown, SM Guthrie, RN Mames, BJ Byrne, T Vaught, PE Spoerri, AB Peck and EW Scott. (2002). Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nature Med 8:607-612.
4. Ribatti D, A Vacca, B Nico, R Ria and F Dammacco. (2002). Cross-talk between hematopoiesis and angiogenesis signaling pathways. Curr Mol Med 2:537-543.
5. Bhattacharya V, PA McSweeney, Q Shi, B Bruno, A Ishida, R Nash, RF Storb, LR Sauvage, WP Hammond and MH Wu. (2000). Enhanced endothelialization and microvessel formation in polyester grafts seeded with CD34(+) bone marrow cells. Blood 95:581-585.
6. Brazelton TR, FM Rossi, GI Keshet and HM Blau. (2000). From marrow to brain: expression of neuronal phenotypes in adult mice. Science 290:1775-1779.
7. Eglitis MA and E Mezey. (1997). Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci USA 94:4080-4085.
8. Ferrari G, G Cusella-De Angelis, M Coletta, E Paolucci, A Stornaiuolo, G Cossu and F Mavilio. (1998). Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279:1528-1530.
9. Gussoni E, Y Soneoka, CD Strickland, EA Buzney, MK Khan, AF Flint, LM Kunkel and RC Mulligan. (1999). Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401:390-394.
10. Jackson KA, SM Majka, H Wang, J Pocius, CJ Hartley, MW Majesky, ML Entman, LH Michael, KK Hirschi and MA Goodell. (2001). Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107:1395-1402.
11. Krause DS, ND Theise, Ml Collector, O Henegariu, S Hwang, R Gardner, S Neutzel and SJ Sharkis. (2001). Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105:369-377.
12. Lagasse E, H Connors, M Al-Dhalimy, M Reitsma, M Dohse, L Osborne, X Wang, M Finegold, IL Weissman and M Grompe. (2000). Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nature Med 6:1229-1234.
13. Mezey E, KJ Chandross, G Harta, RA Maki and SR McKercher. (2000). Turning blood into brain: cells baring neuronal antigens generated in vivo from bone marrow. Science 290:1779-1782.
14. Orlic D, J Kajstura, S Chimenti, DM Bodine, A Leri and P Anversa. (2001). Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann NY Acad Sci 938:221-229; discussion 229-230.
15. Petersen BE, WC Bowen, KD Patrene, WM Mars, AK Sullivan, N Murase, SS Boggs, JS Greenberger and JP Goff. (1999). Bone marrow as a potential source of hepatic oval cells. Science 284:1168-1170.
16. Sata M, A Saiura, A Kunisato, A Tojo, S Okada, T Tokuhisa, H Hirai, M Makuuchi, Y Hirata and R Nagai. (2002). Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nature Med 8:403-409.
17. Shimizu K, S Sugiyama, M Aikawa, Y Fukumoto, E Rabkin, P Libby and RN Mitchell. (2001). Host bone-marrow cells are a source of donor intimal smooth-muscle-like cells in murine aortic transplant arteriopathy. Nature Med 7:738-741.
18. Theise ND, S Badve, R Saxena, O Henegariu, S Sell, JM Crawford and DS Krause. (2000). Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 31:235-240.
19. Morrison SJ, AM Wandycz, HD Hemmati, DE Wright and IL Weissman. (1997). Identification of a lineage of multipotent hematopoietic progenitors. Development 124: 1929-1939.
20. Morrison SJ and IL Weissman. (1994). The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1:661-673.
21. Spangrude GJ, S Heimfeld and IL Weissman. (1988). Purification and characterization of mouse hematopoietic stem cells. Science 241:58-62.
22. Chung YS, WJ Zhang, E Arentson, PD Kingsley, J Palis and K Choi. (2002). Lineage analysis of the hemangioblast as defined by FLK1 and SCL expression. Development 129:5511-5520.
23. Terada N, T Hamazaki, M Oka, M Hoki, DM Mastalerz, Y Nakano, EM Meyer, L Morel, BE Petersen and EW Scott. (2002). Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 416: 542-545.
24. Jiang Y, BN Jahagirdar, RL Reinhardt, RE Schwartz, CD Keene, XR Ortiz-Gonzalez, M Reyes, T Lenvik, T Lund, M Blackstad, J Du, S Aldrich, A Lisberg, WC Low, DA Largaespada and CM Verfaillie. (2002). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49.
25. Wagers AJ, RI Sherwood, JL Christensen and IL Weissman. (2002). Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297:2256-2259.
26. Tse V, Y Yung, JG Santarelli, D Juan, M Hsiao, M Haas, GT Harsh and G Silverberg. (2004). Effects of tumor suppressor gene (p53) on brain tumor angiogenesis and expression of angiogenic modulators. Anticancer Res 24:1-10.
27. Ledbetter JA and LA Herzenberg. (1979). Xenogeneic monoclonal antibodies to mouse lymphoid differentiation antigens. Immunol Rev 47:63-90.
28. van Ewijk W, PL van Soest and GJ van den Engh. (1981). Fluorescence analysis and anatomic distribution of mouse T lymphocyte subsets defined by monoclonal antibodies to the antigens Thy-1, Lyt-1, Lyt-2, and T-200. J Immunol 127:2594-2604.
29. Yung YC, S Cheshier, JG Santarelli, Z Huang, A Wagers, I Weissman and V Tse. (2004). Incorporation of naive bone marrow derived cells into the vascular architecture of brain tumor. Microcirculation 11:699-708.
30. Carmeliet P. (2000). VEGF gene therapy: stimulating angiogenesis or angioma-genesis? Nature Med 6:1102-1103.
31. Folkman J. (1995). Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature Med 1:27-31.
32. Folkman J and R Kalluri. (2004). Cancer without disease. Nature 427:787.
33. Hanahan D and J Folkman. (1996). Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86:353-364.
34. Peoc'h M, G Le Due, A Trayaud, R Farion, JF Le Bas, B Pasquier and C Remy. (1999). Quantification and distribution of neovascularization following microinjection of C6 glioma cells in rat brain. Anticancer Res 19: 3025-3030.
35. Carmeliet P and A Luttun. (2001). The emerging role of the bone marrow-derived stem cells in (therapeutic) angiogenesis. Thromb Haemost 86:289-297.
36. Davidoff AM, CY Ng, P Brown, MA Leary, WW Spurbeck, J Zhou, E Horwitz, EF Vanin and AW Nienhuis. (2001). Bone marrow-derived cells contribute to tumor neovasculature and, when modified to express an angiogenesis inhibitor, can restrict tumor growth in mice. Clin Cancer Res 7:2870-2879.
37. De Palma M, MA Venneri, C Roca and L Naldini. (2003). Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nature Med 9:789-795.
38. Rafii S, D Lyden, R Benezra, K Hattori and B Heissig. (2002). Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy? Nature Rev Cancer 2:826-835.
39. Reyes M, A Dudek, B Jahagirdar, L Koodie, PH Marker and CM Verfaillie. (2002). Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 109: 337-346.
40. Asahara T, H Masuda, T Takahashi, C Kalka, C Pastore, M Silver, M Kearne, M Magner and JM Isner. (1999). Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85:221-228.
41. Asahara T, T Murohara, A Sullivan, M Silver, R van der Zee, T Li, B Witzenbichler, G Schatteman and JM Isner. (1997). Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964-967.
42. Bikfalvi A and ZC Han. (1994). Angiogenic factors are hematopoietic growth factors and vice versa. Leukemia 8:523-529.
43. Choi K, M Kennedy, A Kazarov, JC Papadimitriou and G Keller. (1998). A common precursor for hematopoietic and endothelial cells. Development 125:725-732.
44. Han ZC and JP Caen. (1993). Are megakaryocytes and endothelial cells sisters? J Lab Clin Med 121:821-825.
45. Ziegler BL, M Valtieri, GA Porada, R De Maria, R Muller, B Masella, M Gabbianelli, I Casella, E Pelosi, T Bock, ED Zanjani and C Peschle. (1999). KDR receptor: a key marker defining hematopoietic stem cells. Science 285:1553-1558.
46. Wagers AJ and IL Weissman. (2004). Plasticity of adult stem cells. Cell 116:639-648.
47. Cao B, B Zheng, RJ Jankowski, S Kimura, M Ikezawa, B Deasy, J Cummins, M Epperly, Z Qu-Petersen and J Huard. (2003). Muscle stem cells differentiate into haematopoietic lineages but retain myogenic potential. Nature Cell Biol 5:640-646.
48. Qu-Petersen Z, B Deasy, R Jankowski, M Ikezawa, J Cummins, R Pruchnic, J Mytinger, B Cao, C Gates, A Wernig and J Huard. (2002). Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol 157:851-864.
49. Toma JG, M Akhavan, KJ Fernandes, F Barnabe-Heider, A Sadikot, DR Kaplan and FD Miller. (2001). Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nature Cell Biol 3:778-784.
50. Ferrara N and K Alitalo. (1999). Clinical applications of angiogenic growth factors and their inhibitors. Nature Med 5:1359-1364.
51. Hess DC, WD Hill, A Martin-Studdard, J Carroll, J Brailer and J Carothers. (2002). Bone marrow as a source of endothelial cells and NeuN-expressing cells. After stroke. Stroke 33:1362-1368.
52. Kim KJ, B Li, J Winer, M Armanini, N Gillett, HS Phillips and N Ferrara. (1993). Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 362:841-844.
53. Lyden D, K Hattori, S Dias, C Costa, P Blaikie, L Butros, A Chadburn, B Heissig, W Marks, L Witte, Y Wu, D Hicklin, Z Zhu, NR Hackett, RG Crystal, MA Moore, KA Hajjar, K Manova, R Benezra and S Rafii. (2001). Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nature Med 7:1194-1201.
54. Goodell MA. (2003). Stem-cell "plasticity": befuddled by the muddle. Curr Opin Hematol 10:208-213.
55. Herzog EL, L Chai and DS Krause. (2003). Plasticity of marrow-derived stem cells. Blood 102:3483-3493.
56. Blau HM. (2002). A twist of fate. Nature 419:437.
57. Weimann JM, CA Charlton, TR Brazelton, RC Hackman and HM Blau. (2003). Contribution of transplanted bone marrow cells to Purkinje neurons in human adult brains. Proc Natl Acad Sci USA 100:2088-2093.
58. Zhao Y, D Glesne and E Huberman. (2003). A human peripheral blood monocyte-derived subset acts as pluripotent stem cells. Proc Natl Acad Sci USA 100:2426-2431.
59. Wright DE, SH Cheshier, AJ Wagers, TD Randall, JL Christensen and IL Weissman. (2001). Cyclophosphamide/granulocyte colony-stimulating factor causes selective mobilization of bone marrow hematopoietic cells into the blood after M phase of the cell cycle. Blood 97:2278-2285.