Mobilization of bone marrow-derived cells enhances the angiogenic response to hypoxia without transdifferentiation into endothelial cells

Circulation Research

Volumn 97, Issue 10, 2005, Pages 1027-1035

  O'Neill IV, Thomas J ^a,b   Wamhoff, Brian R ^a   Owens, Gary K ^a   Skalak, Thomas C ^b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b University of Virginia   (United States)

Author keywords

Adult stem cells; Angiogenesis; Bone marrow; Hypoxia

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GROWTH FACTOR; MATRIX METALLOPROTEINASE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL MOTILITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; HYPOXIA; MOUSE; NONHUMAN; PARACRINE SIGNALING; PERICYTE; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; TRAPEZIUS MUSCLE;

ANIMALS; ANOXIA; BONE MARROW CELLS; CELL COUNT; CELL DIFFERENTIATION; ENDOTHELIAL CELLS; HEMATOPOIETIC STEM CELL MOBILIZATION; HEMATOPOIETIC STEM CELLS; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; MUSCLE, SMOOTH, VASCULAR; NEOVASCULARIZATION, PHYSIOLOGIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 27944479679     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000189259.69645.25     Document Type: Article

References (34)

1. Lee MS, Makkar RR. Stem-cell transplantation in myocardial infarction: a status report. Ann Intern Med. 2004;140:729-737.
2. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med. 2003;9:702-712.
3. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, Zeiher AM, Dimmeler S. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med. 2003;9:1370-1376.
4. Olivetti G, Ricci R, Beghi C, Guideri G, Anversa P. Response of the border zone to myocardial infarction in rats. Am J Pathol. 1986;125:476-483.
5. Pichiule P, LaManna JC. Angiopoietin-2 and rat brain capillary remodeling during adaptation and deadaptation to prolonged mild hypoxia. J Appl Physiol. 2002;93:1131-1139.
6. Hoppeler H. Vascular growth in hypoxic skeletal muscle. Adv Exp Med Biol. 1999;474:277-286.
7. Deveci D, Marshall JM, Egginton S. Chronic hypoxia induces prolonged angiogenesis in skeletal muscles of rat. Exp Physiol. 2002;87:287-291.
8. Price RJ, Skalak TC. Arteriolar remodeling in skeletal muscle of rats exposed to chronic hypoxia. J Vasc Res. 1998;35:238-244.
9. Li TS, Hamano K, Suzuki K, Ito H, Zempo N, Matsuzaki M. Improved angiogenic potency by implantation of ex vivo hypoxia prestimulated bone marrow cells in rats. Am J Physiol Heart Circ Physiol. 2002;283:H468-H473.
10. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-966.
11. Grant MB, May WS, Caballero S, Brown GA, Guthrie SM, Mames RN, Byrne BJ, Vaught T, Spoerri PE, Peck AB, Scott EW. Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat Med. 2002;8:607-612.
12. 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.
13. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Keame 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.
14. Price RJ, Owens GK, Skalak TC. Immunohistochemical identification of arteriolar development using markers of smooth muscle differentiation. Evidence that capillary arterialization proceeds from terminal arterioles. Circ Res. 1994;75:520-527.
15. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Keamey 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.
16. Smith K, Marshall JM. Physiological adjustments and arteriolar remodelling within skeletal muscle during acclimation to chronic hypoxia in the rat. J Physiol (Lond). 1999;521:261-272.
17. 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.
18. Espinosa-Heidmann DG, Caicedo A, Hernandez EP, Csaky KG, Cousins SW. Bone marrow-derived progenitor cells contribute to experimental choroidal neovascularization. Invest Ophthalmol Vis Sci. 2003;44:4914-4919.
19. Badiavas EV, Abedi M, Butmarc J, Falanga V, Quesenberry P. Participation of bone marrow derived cells in cutaneous wound healing. J Cell Physiol. 2003;196:245-250.
20. Akita T, Murohara T, Ikeda H, Sasaki Ki, Shimada T, Egami K, Imaizumi T. Hypoxic preconditioning augments efficacy of human endothelial progenitor cells for therapeutic neovascularization. Lab Invest. 2003;83:65-73.
21. Rabelink TJ, de Boer HC, de Koning EJP, van Zonneveld AJ. Endothelial progenitor cells: more than an inflammatory response? Arterioscler Thromb Vasc Biol. 2004;24:834-838.
22. 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.
23. Cho HJ, Kim HS, Lee MM, Kim DH, Yang HJ, Hur J, Hwang KK, Oh S, Choi YJ, Chae IH, Oh BH, Choi YS, Walsh K, Park YB. Mobilized endothelial progenitor cells by granulocyte-macrophage colony-stimulating factor accelerate reendothelialization and reduce vascular inflammation after intravascular radiation. Circulation. 2003;108:2918-2925.
24. Silvestre JS, Mallat Z, Tamarat R, Duriez M, Tedgui A, Levy BI. Regulation of matrix metalloproteinase activity in ischemic tissue by interleukin-10: role in ischemia-induced angiogenesis. Circ Res. 2001;89:259-264.
25. Kinnaird T, Stabile E, Burnett MS, Shou M, Lee CW, Barr S, Fuchs S, Epstein SE. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation. 2004;109:1543-1549.
26. Hess DC, Hill WD, Martin-Studdard A, Carroll J, Brailer J, Carothers J. Bone marrow as a source of endothelial cells and NeuN-expressing cells after stroke. Stroke. 2002;33:1362-1368.
27. 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.
28. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science. 2002;297:2256-2259.
29. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature. 2005;433:760-764.
30. Heil M, Ziegelhoeffer T, Pipp F, Kostin S, Martin S, Clauss M, Schaper W. Blood monocyte concentration is critical for enhancement of collateral artery growth. Am J Physiol Heart Circ Physiol. 2002;283:H2411-H2419.
31. Manoonkitiwongsa PS, Jackson-Friedman C, McMillan PJ, Schultz RL, Lyden PD. Angiogenesis after stroke is correlated with increased numbers of macrophages: the clean-up hypothesis. J Cereb Blood Flow Metab. 2001;21:1223-1231.
32. Lewis JS, Lee JA, Underwood JC, Harris AL, Lewis CE. Macrophage responses to hypoxia: relevance to disease mechanisms. J Leukoc Biol. 1999;66:889-900.
33. 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 NR, Crystal RG, Moore MA, Hajjar KA, Manova K, Benezra R, Rafii S. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med. 2001;7:1194-1201.
34. 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.