Contribution of endothelial progenitors and proangiogenic hematopoietic cells to vascularization of tumor and ischemic tissue

Current Opinion in Hematology

Volumn 13, Issue 3, 2006, Pages 175-181

  Kopp, Hans Georg ^a   Ramos, Carlos A ^b   Rafii, Shahin ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Endothelial progenitor cells; Hematopoietic progenitor cells; Neoangiogenesis

Indexed keywords

ANGIOGENIC FACTOR; GELATINASE B; STEM CELL FACTOR; STROMAL CELL DERIVED FACTOR 1; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; B LYMPHOCYTE; BONE MARROW CELL; CELL SUBPOPULATION; DENDRITIC CELL; ENDOTHELIUM CELL; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; HUMAN; HYPOXIA; IMMUNOCOMPETENT CELL; INFLAMMATORY CELL; ISCHEMIA; MACROPHAGE; MEDIATOR RELEASE; MONOCYTE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PERIVASCULAR MURAL CELL; PRIORITY JOURNAL; REVASCULARIZATION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL MOBILIZATION; THERAPY; TUMOR GROWTH; TUMOR VASCULARIZATION; WOUND HEALING;

ANIMALS; CHEMOKINE CXCL12; CHEMOKINES, CXC; ENDOTHELIAL CELLS; HEMATOPOIETIC STEM CELLS; HUMANS; ISCHEMIA; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, CXCR4; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 33646812605     PISSN: 10656251     EISSN: 15317048     Source Type: Journal    
DOI: 10.1097/01.moh.0000219664.26528.da     Document Type: Review

References (102)

1. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 2003; 9:702-712.
2. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997; 275:964-967.
3. Asahara T, Masuda H, Takahashi T, et al. Bone marrow origin of EPCs responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999; 85:221-228.
4. Asahara T, Takahashi T, Masuda H, et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J 1999; 18:3964-3972.
5. Crisa L, Cirulli V, Smith KA, et al. Human cord blood progenitors sustain thymic T-cell development and a novel form of angiogenesis. Blood 1999; 94:3928-3940.
6. Carmeliet P, Luttun A. The emerging role of the bone marrow-derived stem cells in (therapeutic) angiogenesis. Thromb Haemost 2001; 86:289-297.
7. Orlic D, Kajstura J, Chimenti S, et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001; 410:701-705.
8. Orlic D, Kajstura J, Chimenti S, et al. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A 2001; 98:10344-10349.
9. Kocher AA, Schuster MD, Szabolcs MJ, et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 2001; 7:430-436.
10. Shintani S, Murohara T, Ikeda H, et al. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 2001; 103:2776-2779.
11. Jackson KA, Majka SM, Wang H, et al. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 2001; 107:1395-1402.
12. Edelberg JM, Tang LHK, Hattori K, et al. Young adult bone marrow-derived endothelial precursor cells restore aging-impaired cardiac angiogenic function. Circ Res 2002; 90:E89-E93.
13. Zhang ZG, Zhang L, Jiang Q, Chopp M. Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ Res 2002; 90:284-288.
14. Iwaguro H, Yamaguchi J, Kalka C, et al. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 2002; 105:732-738.
15. Kalka C, Masuda H, Takahashi T, et al. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci USA 2000; 97:3422-3427.
16. Schatteman GC, Hanlon HD, Jiao C, et al. Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J Clin Invest 2000; 106:571-578.
17. Murohara T. Therapeutic vasculogenesis using human cord blood-derived endothelial progenitors. Trends Cardiovasc Med 2001; 11:303-307.
18. Murohara T, Ikeda H, Duan J, et al. Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J Clin Invest 2000; 105:1527-1536.
19. Shi Q, Rafii S, Wu MH, et al. Evidence for circulating bone marrow-derived endothelial cells. Blood 1998; 92:362-367.
20. Bhattacharya V, McSweeney PA, Shi Q, et al. Enhanced endothelialization and microvessel formation in polyester grafts seeded with CD34(+) bone marrow cells. Blood 2000; 95:581-585.
21. Kaushal S, Amiel GE, Guleserian KJ, et al. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med 2001; 7:1035-1040.
22. Maeda M, Fukui A, Nakamura T, et al. Progenitor endothelial cells on vascular grafts: an ultrastructural study. J Biomed Mater Res 2000; 51:55-60.
23. Sata M, Saiura A, Kunisato A, et al. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 2002; 8:403-409.
24. Otani A, Kinder K, Ewalt K, et al. Bone marrow derived stem cells target retinal astrocytes and can promote or inhibit retinal angiogenesis. Nat Med 2002; 8:1004-1010.
25. Grant MB, May WS, Caballero S, et al. Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat Med 2002; 8:607-612.
26. Lyden D, Hattori K, Dias S, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 2001; 7:1194-1201.
27. Reyes M, Dudek A, Jahagirdar B, et al. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 2002; 109:337-346.
28. Moore MA. Putting the neo into neoangiogenesis. J Clin Invest 2002; 109: 313-315.
29. Gehling UM, Ergun S, Schumacher U, et al. In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 2000; 95:3106-3112.
30. Marchetti S, Gimond C, Iljin K, et al. Endothelial cells genetically selected from differentiating mouse embryonic stem cells incorporate at sites of neovascularization in vivo. J Cell Sci 2002; 115:2075-2085.
31. Davidoff AM, Ng CY, Brown P, et al. 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 2001; 7:2870-2879.
32. Ito H, Rovira II, Bloom ML, et al. Endothelial progenitor cells as putative targets for angiostatin. Cancer Res 1999; 59:5875-5877.
33. De Palma M, Venneri MA, Galli R, et al. 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. A report suggesting that monocytes expressing the Tie2-receptor (TEMs) promote angiogenesis in a paracrine manner.
34. Conejo-Garcia JR, Benencia F, Courreges MC, 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.
35. Riboldi E, Musso T, Moroni E, et al. Cutting edge: proangiogenic properties of alternatively activated dendritic cells. J Immunol 2005; 175:2788-2792. Alternatively activated myeloid dendritic cells are shown to produce VEGF165 and VEGF121 and therefore may contribute to the resolution of inflammatory reactions by promoting angiogenesis.
36. Schruefer R, Lutze N, Schymeinsky J, Walzog B. Human neutrophils promote angiogenesis by a paracrine feedforward mechanism involving endothelial interleukin-8. Am J Physiol Heart Circ Physiol 2005; 288:H1186-H1192.
37. Puxeddu I, Alian A, Piliponsky AM, et al. Human peripheral blood eosinophils induce angiogenesis. Int J Biochem Cell Biol 2005; 37:628-636.
38. Heissig B, Rafii S, Akiyama H, et al. Low-dose irradiation promotes tissue revascularization through VEGF release from mast cells and MMP-9-mediated progenitor cell mobilization. J Exp Med 2005; 202:739-750.
39. Rafii S. Circulating endothelial precursors: mystery, reality, and promise. J Clin Invest 2000; 105:17-19.
40. Takahashi T, Kalka C, Masuda H, et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 1999; 5:434-438.
41. Rafii S, Oz MC, Seldomridge JA, et al. Characterization of hematopoietic cells arising on the textured surface of left ventricular assist devices. Ann Thorac Surg 1995; 60:1627-1632.
42. Peichev M, Naiyer AJ, Pereira D, et al. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000; 95:952-958.
43. Ingram DA, Caplice NM, Yoder MC. Unresolved questions, changing definitions, and novel paradigms for defining endothelial progenitor cells. Blood 2005; 106:1525-1531. A review of approaches to identify a novel hierarchy of EPCs based on clonogenic and proliferative potential, analogous to the hematopoietic cell system.
44. Ingram DA, Mead LE, Moore DB, et al. Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 2005; 105:2783-2786.
45. Ingram DA, Mead LE, Tanaka H, et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 2004; 104:2752-2760.
46. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 2003; 9:702-712.
47. Urbich C, Dimmeler S. Endothelial progenitor cells functional characterization. Trends Cardiovasc Med 2004; 14:318-322.
48. Schmeisser A, Garlichs CD, Zhang H, et al. Monocytes coexpress endothelial and macrophagocytic lineage markers and form cord-like structures in Matrigel under angiogenic conditions. Cardiovasc Res 2001; 49:671-680.
49. Rohde E, Malischnik C, Thaler D, et al. Blood monocytes mimic endothelial progenitor cells. Stem Cells 2005; 1 September [Epub ahead of print]. A provocative study where bona fide monocytes were found to become phenotypically undistinguishable from endothelial cells after 4-6 days under traditional angiogenic culture conditions.
50. Jiang S, Walker L, Afentoulis M, et al. Transplanted human bone marrow contributes to vascular endothelium. Proc Natl Acad Sci USA 2004; 101:16891-16896.
51. Peters BA, Diaz LA, Polyak K, et al. Contribution of bone marrow-derived endothelial cells to human tumor vasculature. Nat Med 2005; 11:261-262.
52. Hilbe W, Dirnhofer S, Oberwasserlechner F, et al. CD133 positive endothelial progenitor cells contribute to the tumour vasculature in non-small cell lung cancer. J Clin Pathol 2004; 57:965-969.
53. Shaked Y, Bertolini F, Man S, et al. Genetic heterogeneity of the vasculogenic phenotype parallels angiogenesis: implications for cellular surrogate marker analysis of antiangiogenesis. Cancer Cell 2005; 7:101-111.
54. Willett CG, Boucher Y, di Tomaso E, et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 2004; 10:145-147.
55. 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.
56. Ruzinova MB, Schoer RA, Gerald W, et al. 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.
57. Kvasnicka HM, Wickenhauser C, Thiele J, et al. Mixed chimerism of bone marrow vessels (endothelial cells, myofibroblasts) following allogeneic transplantation for chronic myelogenous leukemia. Leuk Lymphoma 2003; 44:321-328.
58. Zhang F, Hackett NR, Lam G, et al. Green fluorescent protein selectively induces HSP70-mediated up-regulation of COX-2 expression in endothelial cells. Blood 2003; 102:2115-2121.
59. Luttun A, Tjwa M, Moons L, et al. Revascularization of ischemic tissues by PIGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med 2002; 8:831-840.
60. Coussens LM, Tinkle CL, Hanahan D, Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000; 103:481-490.
61. Coussens LM, Raymond WW, Bergers G, et al. Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev 1999; 13:1382-1397.
62. Hiratsuka S, Nakamura K, Iwai S, et al. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2002; 2:289-300.
63. Pipp F, Heil M, Issbrucker K, et al. VEGFR-1-selective VEGF homologue PIGF is arteriogenic: evidence for a monocyte-mediated mechanism. Circ Res 2003; 92:378-385.
64. Cursiefen C, Chen L, Borges LP, et al. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 2004; 113:1040-1050.
65. Rafii S, Lyden D, Benezra R, et al. Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy? Nat Rev Cancer 2002; 2:826-835.
66. Yang L, Debusk LM, Fukuda K, et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004; 6:409-421.
67. Okamoto R, Ueno M, Yamada Y, et al. Hematopoietic cells regulate the angiogenic switch during tumorigenesis. Blood 2005; 105:2757-2763. A suggestion that c-kit positive hematopoietic cells regulate the angiogenic switch in mouse tumor models.
68. Takakura N, Watanabe T, Suenobu S, et al. A role for hematopoietic stem cells in promoting angiogenesis. Cell 2000; 102:199-209.
69. Donovan MJ, Lin MI, Wiegn P, et al. Brain derived neurotrophic factor is an endothelial cell survival factor required for intramyocardial vessel stabilization. Development 2000; 127:4531-4540.
70. Kaplan RN, Riba RD, Zacharoulis S, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005; 438:820-827. A report suggesting that VEGFR1+ hematopoietic cells establish sites of future metastatic deposits and discussing the mechanisms by which this process occurs.
71. Gill M, Dias S, Hattori K, et al. Vascular trauma induces rapid but transient mobilization of VEGFR2(+)AC133(+) endothelial precursor cells. Circ Res 2001; 88:167-174.
72. Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003; 425:841-846.
73. Zhang J, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003; 425:836-841.
74. Kiel MJ, Yilmaz OH, Iwashita T, et al. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005; 121:1109-1121.
75. Cheng T, Rodrigues N, Shen H, et al. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 2000; 287:1804-1808.
76. Kopp HG, Avecilla ST, Hooper AT, Rafii S. The bone marrow vascular niche: home of HSC differentiation and mobilization. Physiology (Bethesda) 2005; 20:349-356.
77. Vu TH, Werb Z. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 2000; 14:2123-2133.
78. Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000; 2:737-744.
79. Engsig MT, Chen QJ, Vu TH, et al. Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J Cell Biol 2000; 151:879-890.
80. Heissig B, Hattori K, Dias S, et al. Recruitment of stem and progenitor cells from the bone marrow niche requires mmp-9 mediated release of kit-ligand. Cell 2002; 109:625-637.
81. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature 2000; 407:249-257.
82. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996; 86:353-364.
83. Kabrun N, Buhring HJ, Choi K, et al. Flk-1 expression defines a population of early embryonic hematopoietic precursors. Development 1997; 124:2039-2048.
84. Shalaby F, Rossant J, Yamaguchi TP, et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995; 376:62-66.
85. Shalaby F, Ho J, Stanford WL, et al. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 1997; 89:981-990.
86. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995; 376:66-70.
87. Fong GH, Zhang L, Bryce DM, Peng J. Increased hemangioblast commitment, not vascular disorganization, is the primary defect in flt-1 knock-out mice. Development 1999; 126:3015-3025.
88. Hiratsuka S, Minowa O, Kuno J, et al. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci U S A 1998; 95:9349-9354.
89. Hiratsuka S, Maru Y, Okada A, et al. Involvement of Flt-1 tyrosine kinase (vascular endothelial growth factor receptor-1) in pathological angiogenesis. Cancer Res 2001; 61:1207-1213.
90. Sawano A, Iwai S, Sakurai Y, et al. Flt-1, vascular endothelial growth factor receptor 1, is a novel cell surface marker for the lineage of monocyte-macrophages in humans. Blood 2001; 97:785-791.
91. Clauss M, Weich H, Breier G, et al. The vascular endothelial growth factor receptor Flt-1 mediates biological activities: implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J Biol Chem 1996; 271:17629-17634.
92. Barleon B, Sozzani S, Zhou D, et al. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood 1996; 87:3336-3343.
93. Hattori K, Dias S, Heissig B, et al. 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.
94. Cho NK, Keyes L, Johnson E, et al. Developmental control of blood cell migration by the Drosophila VEGF pathway. Cell 2002; 108:865-876.
95. De Falco E, Porcelli D, Torella AR, et al. SDF-1 involvement in endothelial phenotype and ischemia-induced recruitment of bone marrow progenitor cells. Blood 2004; 104:3472-3482.
96. Ceradini DJ, Gurtner GC. Homing to hypoxia: HIF-1 as a mediator of progenitor cell recruitment to injured tissue. Trends Cardiovasc Med 2005; 15:57-63.
97. Ceradini DJ, Kulkarni AR, Callaghan MJ, et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004; 10:858-864. Hypoxia induces SDF-1 expression in endothelial cells via HIF-1alpha, thereby recruiting CXCR4+ hematopoietic cells to sites of ischemia.
98. Dar A, Goichberg P, Shinder V, et al. Chemokine receptor CXCR4-dependent internalization and resecretion of functional chemokine SDF-1 by bone marrow endothelial and stromal cells. Nat Immunol 2005; 6:1038-1046. Bone marrow endothelial cells are shown to be able to transcytose SDF-1 from the circulation to the bone marrow interstitium, thereby increasing stem cell homing.
99. Walter DH, Haendeler J, Reinhold J, et al. Impaired CXCR4 signaling contributes to the reduced neovascularization capacity of endothelial progenitor cells from patients with coronary artery disease. Circ Res 2005; 97:1142-1151. This study suggests that CXCR4 is functionally expressed in EPCs and allows them to home to ischemic areas. In addition, SDF-1 signaling seemed to be disrupted in EPCs obtained from patients with cardiovascular disease.
100. Grunewald M, Avraham I, Dor Y, et al. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 2006; 124:175-189. A heterogeneous population of VEGFR1+/CXCR4+ bone marrow derived hematopoietic cells is shown to contribute to neoangiogenesis. SDF-1 expressed by perivascular myofibroblasts retains these cells, which in turn support angiogenesis in a paracrine manner.
101. Ruiz de Almodovar C, Luttun A, Carmeliet P. An SDF-1 trap for myeloid cells stimulates angiogenesis. Cell 2006; 124:18-21.
102. Arafat WO, Casado E, Wang M, et al. Genetically modified CD34+ cells exert a cytotoxic bystander effect on human endothelial and cancer cells. Clin Cancer Res 2000; 6:4442-4448.