Frontiers in nephrology: The evolving therapeutic applications of endothelial progenitor cells

Journal of the American Society of Nephrology

Volumn 18, Issue 11, 2007, Pages 2843-2852

  Tongers, Jörn ^a   Losordo, Douglas W ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTERY DISEASE; CARDIOMYOPATHY; CARDIOVASCULAR DISEASE; CELL HOMING; CELL REGENERATION; CELL TRANSPORT; CORONARY ARTERY DISEASE; CYTOLOGY; ENDOTHELIUM CELL; HEART FAILURE; HEART INFARCTION; HUMAN; KIDNEY DISEASE; NEPHROLOGY; PRIORITY JOURNAL; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION;

EID: 35848963199     PISSN: 10466673     EISSN: None     Source Type: Journal    
DOI: 10.1681/ASN.2007050597     Document Type: Review

References (123)

1. Gheorghiade M, Bonow RO: Chronic heart failure in the United States: A manifestation of coronary artery disease. Circulation 97: 282-289, 1998
2. Criqui MH, Fronek A, Barrett-Connor E, Klauber MR, Gabriel S, Goodman D: The prevalence of peripheral arterial disease in a defined population. Circulation 71: 510-515, 1985
3. Golomb BA, Dang TT, Criqui MH: Peripheral arterial disease: Morbidity and mortality implications. Circulation 114: 688-699, 2006
4. Hiatt WR: Medical treatment of peripheral arterial disease and claudication. N Engl J Med 344: 1608-1621, 2001
5. Levey AS: Clinical practice: Nondiabetic kidney disease. N Engl J Med 347: 1505-1511, 2002
6. Drueke TB: Aspects of cardiovascular burden in pre-dialysis patients. Nephron 85[Suppl 1]: 9-14, 2000
7. 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 5: 434-438, 1999
8. 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 86: 1198-1202, 2000
9. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S: Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 7: 430-436, 2001
10. Asahara T, Takeshita S, Tsurumi Y, Feldman L, Isner JM: Arterial gene therapy: A molecular biological perspective for the treatment of arterial ischemia. Z Kardiol 86[Suppl 1]: 65-69, 1997
11. Urbich C, Dimmeler S: Endothelial progenitor cells: Characterization and role in vascular biology. Circ Res 95: 343-353, 2004
12. 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 275: 964-967, 1997
13. Pillarisetti K, Gupta SK: Cloning and relative expression analysis of rat stromal cell derived factor-1 (SDF-1): SDF-1 alpha mRNA is selectively induced in rat model of myocardial infarction. Inflammation 25: 293-300, 2001
14. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC: Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10: 858-864, 2004
15. Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, Kiedrowski M, Rovner A, Ellis SG, Thomas JD, DiCorleto PE, Topol EJ, Penn MS: Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet 362: 697-703, 2003
16. Lee SH, Wolf PL, Escudero R, Deutsch R, Jamieson SW, Thistlethwaite PA: Early expression of angiogenesis factors in acute myocardial ischemia and infarction. N Engl J Med 342: 626-633, 2000
17. 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 85: 221-228, 1999
18. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA, Werb Z, Rafii S: Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109: 625-637, 2002
19. 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 9: 1370-1376, 2003
20. Springer TA: Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 76: 301-314, 1994
21. Yamaguchi J, Kusano KF, Masuo O, Kawamoto A, Silver M, Murasawa S, Bosch-Marce M, Masuda H, Losordo DW, Isner JM, Asahara T: Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107: 1322-1328, 2003
22. Wright DE, Bowman EP, Wagers AJ, Butcher EC, Weissman IL: Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J Exp Med 195: 1145-1154, 2002
23. Britten MB, Abolmaali ND, Assmus B, Lehmann R, Honold J, Schmitt J, Vogl TJ, Martin H, Schachinger V, Dimmeler S, Zeiher AM: Infarct remodeling after intracoronary progenitor cell treatment in patients with acute myocardial infarction (TOPCARE-AMI): Mechanistic insights from serial contrast-enhanced magnetic resonance imaging. Circulation 108: 2212-2218, 2003
24. Landmesser U, Hornig B, Drexler H: Endothelial function: A critical determinant in atherosclerosis? Circulation 109: II27-II33, 2004
25. Lerman A, Zeiher AM: Endothelial function: Cardiac events. Circulation 111: 363-368, 2005
26. Rafii S, Lyden D: Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9: 702-712, 2003
27. Shi Q, Rafii S, Wu MH, Wijelath ES, Yu C, Ishida A, Fujita Y, Kothari S, Mohle R, Sauvage LR, Moore MA, Storb RF, Hammond WP: Evidence for circulating bone marrow-derived endothelial cells. Blood 92: 362-367, 1998
28. Walter DH, Rittig K, Bahlmann FH, Kirchmair R, Silver M, Murayama T, Nishimura H, Losordo DW, Asahara T, Isner JM: Statin therapy accelerates reendothelialization: A novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation 105: 3017-3024, 2002
29. Werner N, Junk S, Laufs U, Link A, Walenta K, Bohm M, Nickenig G: Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circ Res 93: e17-e24, 2003
30. Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M, Li T, Isner JM, Asahara T: Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A 97: 3422-3427, 2000
31. Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S, Masuda H, Silver M, Ma H, Kearney M, Isner JM, Asahara T: Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103: 634-637, 2001
32. Urbich C, Heeschen C, Aicher A, Dernbach E, Zeiher AM, Dimmeler S: Relevance of monocytic features for neovascularization capacity of circulating endothelial progenitor cells. Circulation 108: 2511-2516, 2003
33. Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, Sasaki K, Shimada T, Oike Y, Imaizumi T: Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 103: 2776-2779, 2001
34. Goodell MA, Jackson KA, Majka SM, Mi T, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK: Stem cell plasticity in muscle and bone marrow. Ann N Y Acad Sci 938: 208-218; discussion 218-220, 2001
35. Orlic D, Kajstura J, Chimenti S, Bodine DM, Leri A, Anversa P: Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann N Y Acad Sci 938: 221-229, discussion 229-230, 2001
36. Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M, Pasumarthi KB, Virag JI, Bartelmez SH, Poppa V, Bradford G, Dowell JD, Williams DA, Field LJ: Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428: 664-668, 2004
37. Balsam LB, Wagers AJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC: Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428: 668-673, 2004
38. Hillebrands JL, Klatter FA, van Dijk WD, Rozing J: Bone marrow does not contribute substantially to endothelial-cell replacement in transplant arteriosclerosis. Nat Med 8: 194-195, 2002
39. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL: Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297: 2256-2259, 2002
40. 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 94: 230-238, 2004
41. Kamihata H, Matsubara H, Nishiue T, Fujiyama S, Tsutsumi Y, Ozono R, Masaki H, Mori Y, Iba O, Tateishi E, Kosaki A, Shintani S, Murohara T, Imaizumi T, Iwasaka T: Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines. Circulation 104: 1046-1052, 2001
42. Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S, Epstein SE: Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 94: 678-685, 2004
43. Rehman J, Li J, Orschell CM, March KL: Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107: 1164-1169, 2003
44. Folkman J, Merler E, Abernathy C, Williams G: Isolation of a tumor factor responsible for angiogenesis. J Exp Med 133: 275-288, 1971
45. 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 109: 1543-1549, 2004
46. Heil M, Ziegelhoeffer T, Mees B, Schaper W: A different outlook on the role of bone marrow stem cells in vascular growth: Bone marrow delivers software not hardware. Circ Res 94: 573-574, 2004
47. Losordo DW, Dimmeler S: Therapeutic angiogenesis and vasculogenesis for ischemic disease: Part II - Cell-based therapies. Circulation 109: 2692-2697, 2004
48. Kalka C, Tehrani H, Laudenberg B, Vale PR, Isner JM, Asahara T, Symes JF: VEGF gene transfer mobilizes endothelial progenitor cells in patients with inoperable coronary disease. Ann Thorac Surg 70: 829-834, 2000
49. Iwaguro H, Yamaguchi J, Kalka C, Murasawa S, Masuda H, Hayashi S, Silver M, Li T, Isner JM, Asahara T: Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 105: 732-738, 2002
50. Iba O, Matsubara H, Nozawa Y, Fujiyama S, Amano K, Mori Y, Kojima H, Iwasaka T: Angiogenesis by implantation of peripheral blood mononuclear cells and platelets into ischemic limbs. Circulation 106: 2019-2025, 2002
51. 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 18: 3964-3972, 1999
52. Fuchs S, Satler LF, Kornowski R, Okubagzi P, Weisz G, Baffour R, Waksman R, Weissman NJ, Cerqueira M, Leon MB, Epstein SE: Catheter-based autologous bone marrow myocardial injection in no-option patients with advanced coronary artery disease: A feasibility study. J Am Coll Cardiol 41: 1721-1724, 2003
53. Kamihata H, Matsubara H, Nishiue T, Fujiyama S, Amano K, Iba O, Imada T, Iwasaka T: Improvement of collateral perfusion and regional function by implantation of peripheral blood mononuclear cells into ischemic hibernating myocardium. Arterioscler Thromb Vasc Biol 22: 1804-1810, 2002
54. Kawamoto A, Tkebuchava T, Yamaguchi J, Nishimura H, Yoon YS, Milliken C, Uchida S, Masuo O, Iwaguro H, Ma H, Hanley A, Silver M, Kearney M, Losordo DW, Isner JM, Asahara T: Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation 107: 461-468, 2003
55. Orlic D, Kajstura J, Chimenti S, Limana F, Jakoniuk I, Quaini F, Nadal-Ginard B, Bodine DM, Leri A, Anversa P: Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A 98: 10344-10349, 2001
56. Scheubel RJ, Zorn H, Silber RE, Kuss O, Morawietz H, Holtz J, Simm A: Age-dependent depression in circulating endothelial progenitor cells in patients undergoing coronary artery bypass grafting. J Am Coll Cardiol 42: 2073-2080, 2003
57. Heiss C, Keymel S, Niesler U, Ziemann J, Kelm M, Kalka C: Impaired progenitor cell activity in age-related endothelial dysfunction. J Am Coll Cardiol 45: 1441-1448, 2005
58. Kondo T, Hayashi M, Takeshita K, Numaguchi Y, Kobayashi K, Iino S, Inden Y, Murohara T: Smoking cessation rapidly increases circulating progenitor cells in peripheral blood in chronic smokers. Arterioscler Thromb Vasc Biol 24: 1442-1447, 2004
59. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, Gurtner GC: Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 106: 2781-2786, 2002
60. Vasa M, Fichtlscherer S, Adler K, Aicher A, Martin H, Zeiher AM, Dimmeler S: Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation 103: 2885-2890, 2001
61. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T: Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 348: 593-600, 2003
62. Lambiase PD, Edwards RJ, Anthopoulos P, Rahman S, Meng YG, Bucknall CA, Redwood SR, Pearson JD, Marber MS: Circulating humoral factors and endothelial progenitor cells in patients with differing coronary collateral support. Circulation 109: 2986-2992, 2004
63. Adams V, Lenk K, Linke A, Lenz D, Erbs S, Sandri M, Tarnok A, Gielen S, Emmrich F, Schuler G, Hambrecht R: Increase of circulating endothelial progenitor cells in patients with coronary artery disease after exercise-induced ischemia. Arterioscler Thromb Vasc Biol 24: 684-690, 2004
64. Heeschen C, Lehmann R, Honold J, Assmus B, Aicher A, Walter DH, Martin H, Zeiher AM, Dimmeler S: Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation 109: 1615-1622, 2004
65. Massa M, Rosti V, Ferrario M, Campanelli R, Ramajoli I, Rosso R, De Ferrari GM, Ferlini M, Goffredo L, Bertoletti A, Klersy C, Pecci A, Moratti R, Tavazzi L: Increased circulating hematopoietic and endothelial progenitor cells in the early phase of acute myocardial infarction. Blood 105: 199-206, 2005
66. Valgimigli M, Rigolin GM, Fucili A, Porta MD, Soukhomovskaia O, Malagutti P, Bugli AM, Bragotti LZ, Francolini G, Mauro E, Castoldi G, Ferrari R: CD34+ and endothelial progenitor cells in patients with various degrees of congestive heart failure. Circulation 110: 1209-1212, 2004
67. George J, Goldstein E, Abashidze S, Deutsch V, Shmilovich H, Finkelstein A, Herz I, Miller H, Keren G: Circulating endothelial progenitor cells in patients with unstable angina: Association with systemic inflammation. Eur Heart J 25: 1003-1008, 2004
68. Laufs U, Werner N, Link A, Endres M, Wassmann S, Jurgens K, Miche E, Bohm M, Nickenig G: Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation 109: 220-226, 2004
69. Dimmeler S, Aicher A, Vasa M, Mildner-Rihm C, Adler K, Tiemann M, Rutten H, Fichtischerer S, Martin H, Zeiher AM: HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway. J Clin Invest 108: 391-397, 2001
70. Bahlmann FH, de Groot K, Mueller O, Hertel B, Haller H, Fliser D: Stimulation of endothelial progenitor cells: A new putative therapeutic effect of angiotensin II receptor antagonists. Hypertension 45: 526-529, 2005
71. Witzgall R, Brown D, Schwarz C, Bonventre JV: Localization of proliferating cell nuclear antigen, vimentin, c-Fos, and clusterin in the postischemic kidney: Evidence for a heterogenous genetic response among nephron segments, and a large pool of mitotically active and dedifferentiated cells. J Clin Invest 93: 2175-2188, 1994
72. Ito T, Suzuki A, Imai E, Okabe M, Hori M: Bone marrow is a reservoir of repopulating mesangial cells during glomerular remodeling. J Am Soc Nephrol 12: 2625-2635, 2001
73. de Groot K, Bahlmann FH, Sowa J, Koenig J, Menne J, Haller H, Fliser D: Uremia causes endothelial progenitor cell deficiency. Kidney Int 66: 641-646, 2004
74. Choi JH, Kim KL, Huh W, Kim B, Byun J, Suh W, Sung J, Jeon ES, Oh HY, Kim DK: Decreased number and impaired angiogenic function of endothelial progenitor cells in patients with chronic renal failure. Arterioscler Thromb Vasc Biol 24: 1246-1252, 2004
75. Herbrig K, Pistrosch F, Oelschlaegel U, Wichmann G, Wagner A, Foerster S, Richter S, Gross P, Passauer J: Increased total number but impaired migratory activity and adhesion of endothelial progenitor cells in patients on long-term hemodialysis. Am J Kidney Dis 44: 840-849, 2004
76. Soler MJ, Martinez-Estrada OM, Puig-Mari JM, Marco-Feliu D, Oliveras A, Vila J, Mir M, Orfila A, Vilaro S, Lloveras J: Circulating endothelial progenitor cells after kidney transplantation. Am J Transplant 5: 2154-2159, 2005
77. Eizawa T, Murakami Y, Matsui K, Takahashi M, Muroi K, Amemiya M, Takano R, Kusano E, Shimada K, Ikeda U: Circulating endothelial progenitor cells are reduced in hemodialysis patients. Curr Med Res Opin 19: 627-633, 2003
78. Westerweel PE, Hoefer IE, Blankestijn PJ, de Bree P, Groeneveld DJ, van Oostrom O, Braam B, Koomans HA, Verhaar M: End-stage renal disease causes an imbalance between endothelial and smooth muscle progenitor cells. Am J Physiol Renal Physiol 292: F1132-F1140, 2007
79. de Groot K, Bahlmann FH, Bahlmann E, Menne J, Haller H, Fliser D: Kidney graft function determines endothelial progenitor cell number in renal transplant recipients. Transplantation 79: 941-945, 2005
80. Herbrig K, Gebier K, Oelschlaegel U, Pistrosch F, Foerster S, Wagner A, Gross P, Passauer J: Kidney transplantation substantially improves endothelial progenitor cell dysfunction in patients with end-stage renal disease. Am J Transplant 6: 2922-2928, 2006
81. Chan CT, Li SH, Verma S: Nocturnal hemodialysis is associated with restoration of impaired endothelial progenitor cell biology in end-stage renal disease. Am J Physiol Renal Physiol 289: F679-F684, 2005
82. Haller H, de Groot K, Bahlmann F, Elger M, Fliser D: Stem cells and progenitor cells in renal disease. Kidney Int 68: 1932-1936, 2005
83. Heeschen C, Aicher A, Lehmann R, Fichtlscherer S, Vasa M, Urbich C, Mildner-Rihm C, Martin H, Zeiher AM, Dimmeler S: Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 102: 1340-1346, 2003
84. Arriero M, Brodsky SV, Gealekman O, Lucas PA, Goligorsky MS: Adult skeletal muscle stem cells differentiate into endothelial lineage and ameliorate renal dysfunction after acute ischemia. Am J Physiol Renal Physiol 287: F621-F627, 2004
85. Pabst R, Sterzel RB: Cell renewal of glomerular cell types in normal rats. An autoradiographic analysis. Kidney Int 24: 626-631, 1983
86. Rookmaaker MB, Smits AM, Tolboom H, Van 't Wout K, Martens AC, Goldschmeding R, Joles JA, Van Zonneveld AJ, Grone HJ, Rabelink TJ, Verhaar MC: Bone-marrow-derived cells contribute to glomerular endothelial repair in experimental glomerulonephritis. Am J Pathol 163: 553-562, 2003
87. Ikarashi K, Li B, Suwa M, Kawamura K, Morioka T, Yao J, Khan F, Uchiyama M, Oite T: Bone marrow cells contribute to regeneration of damaged glomerular endothelial cells. Kidney Int 67: 1925-1933, 2005
88. Lagaaij EL, Cramer-Knijnenburg GF, van Kemenade FJ, van Es LA, Bruijn JA, van Krieken JH: Endothelial cell chimerism after renal transplantation and vascular rejection. Lancet 357: 33-37, 2001
89. Uchimura H, Marumo T, Takase O, Kawachi H, Shimizu F, Hayashi M, Saruta T, Hishikawa K, Fujita T: Intrarenal injection of bone marrow-derived angiogenic cells reduces endothelial injury and mesangial cell activation in experimental glomerulonephritis. J Am Soc Nephrol 16: 997-1004, 2005
90. Imasawa T, Utsunomiya Y, Kawamura T, Zhong Y, Nagasawa R, Okabe M, Maruyama N, Hosoya T, Ohno T: The potential of bone marrow-derived cells to differentiate to glomerular mesangial cells. J Am Soc Nephrol 12: 1401-1409, 2001
91. Masuya M, Drake CJ, Fleming PA, Reilly CM, Zeng H, Hill WD, Martin-Studdard A, Hess DC, Ogawa M: Hematopoietic origin of glomerular mesangial cells. Blood 101: 2215-2218, 2003
92. Kale S, Karihaloo A, Clark PR, Kashgarian M, Krause DS, Cantley LG: Bone marrow stem cells contribute to repair of the ischemically injured renal tubule. J Clin Invest 112: 42-49, 2003
93. Gupta S, Verfaillie C, Chmielewski D, Kim Y, Rosenberg ME: A role for extrarenal cells in the regeneration following acute renal failure. Kidney Int 62: 1285-1290, 2002
94. Strauer BE, Brehm M, Zeus T, Kostering M, Hernandez A, Sorg RV, Kogler G, Wernet P: Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 106: 1913-1918, 2002
95. Frangogiannis NG, Smith CW, Entman ML: The inflammatory response in myocardial infarction. Cardiovasc Res 53: 31-47, 2002
96. Barbash IM, Chouraqui P, Baron J, Feinberg MS, Etzion S, Tessone A, Miller L, Guetta E, Zipori D, Kedes LH, Kloner RA, Leor J: Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: Feasibility, cell migration, and body distribution. Circulation 108: 863-868, 2003
97. Aicher A, Brenner W, Zuhayra M, Badorff C, Massoudi S, Assmus B, Eckey T, Henze E, Zeiher AM, Dimmeler S: Assessment of the tissue distribution of transplanted human endothelial progenitor cells by radioactive labeling. Circulation 107: 2134-2139, 2003
98. Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L, Hertenstein B, Ganser A, Knapp WH, Drexler H: Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 111: 2198-2202, 2005
99. Ohtsuka M, Takano H, Zou Y, Toko H, Akazawa H, Qin Y, Suzuki M, Hasegawa H, Nakaya H, Komuro I: Cytokine therapy prevents left ventricular remodeling and dysfunction after myocardial infarction through neovascularization. FASEB J 18: 851-853, 2004
100. Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R, Dobert N, Grunwald F, Aicher A, Urbich C, Martin H, Hoelzer D, Dimmeler S, Zeiher AM: Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation 106: 3009-3017, 2002
101. Fernandez-Aviles F, San Roman JA, Garcia-Frade J, Fernandez ME, Penarrubia MJ, de la Fuente L, Gomez-Bueno M, Cantalapiedra A, Fernandez J, Gutierrez O, Sanchez PL, Hernandez C, Sanz R, Garcia-Sancho J, Sanchez A: Experimental and clinical regenerative capability of human bone marrow cells after myocardial infarction. Circ Res 95: 742-748, 2004
102. Schachinger V, Assmus B, Britten MB, Honold J, Lehmann R, Teupe C, Abolmaali ND, Vogl TJ, Hofmann WK, Martin H, Dimmeler S, Zeiher AM: Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction: Final one-year results of the TOPCARE-AMI Trial. J Am Coll Cardiol 44: 1690-1699, 2004
103. Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Breidenbach C, Fichtner S, Korte T, Hornig B, Messinger D, Arseniev L, Hertenstein B, Ganser A, Drexler H: Intracoronary autologous bone-marrow cell transfer after myocardial infarction: The BOOST randomised controlled clinical trial. Lancet 364: 141-148, 2004
104. Janssens S, Dubois C, Bogaert J, Theunissen K, Deroose C, Desmet W, Kalantzi M, Herbots L, Sinnaeve P, Dens J, Maertens J, Rademakers F, Dymarkowski S, Gheysens O, Van Cleemput J, Bormans G, Nuyts J, Belmans A, Mortelmans L, Boogaerts M, Van de Werf F: Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. Lancet 367: 113-121, 2006
105. Lunde K, Solheim S, Aakhus S, Arnesen H, Abdelnoor M, Egeland T, Endresen K, Ilebekk A, Mangschau A, Fjeld JG, Smith HJ, Taraldsrud E, Grogaard HK, Bjornerheim R, Brekke M, Muller C, Hopp E, Ragnarsson A, Brinchmann JE, Forfang K: lntracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N Engl J Med 355: 1199-1209, 2006
106. Schachinger V, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Holschermann H, Yu J, Corti R, Mathey DG, Hamm CW, Suselbeck T, Assmus B, Tonn T, Dimmeler S, Zeiher AM: Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med 355: 1210-1221, 2006
107. Meyer GP, Wollen KC, Lotz J, Steffens J, Lippolt P, Fichtner S, Hecker H, Schaefer A, Arseniev L, Hertenstein B, Ganser A, Drexler H: Intracoronary bone marrow cell transfer after myocardial infarction: Eighteen months' follow-up data from the randomized, controlled BOOST (BOne marrOw transfer to enhance ST-elevation infarct regeneration) trial. Circulation 113: 1287-1294, 2006
108. Kang HJ, Kim HS, Zhang SY, Park KW, Cho HJ, Koo BK, Kim YJ, Soo Lee D, Sohn DW, Han KS, Oh BH, Lee MM, Park YB: Effects of intracoronary infusion of peripheral blood stem-cells mobilised with granulocyte-colony stimulating factor on left ventricular systolic function and restenosis after coronary stenting in myocardial infarction: The MAGIC cell randomised clinical trial. Lancet 363: 751-756, 2004
109. Ince H, Petzsch M, Kleine HD, Eckard H, Rehders T, Burska D, Kische S, Freund M, Nienaber CA: Prevention of left ventricular remodeling with granulocyte colony-stimulating factor after acute myocardial infarction: Final 1-year results of the Front-Integrated Revascularization and Stem Cell Liberation in Evolving Acute Myocardial Infarction by Granulocyte Colony-Stimulating Factor (FIRSTUNE-AMI) Trial. Circulation 112: 173-80, 2005
110. Valgimigli M, Rigolin GM, Cittanti C, Malagutti P, Curello S, Percoco G, Bugli AM, Della Porta M, Bragotti LZ, Ansani L, Maura E, Lanfranchi A, Giganti M, Feggi L, Castoldi G, Ferrari R: Use of granulocyte-colony stimulating factor during acute myocardial infarction to enhance bone marrow stem cell mobilization in humans: Clinical and angiographic safety profile. Eur Heart J 26: 1838-1845, 2005
111. Hamano K, Nishida M, Hirata K, Mikamo A, Li TS, Harada M, Miura T, Matsuzaki M, Esato K: Local implantation of autologous bone marrow cells for therapeutic angiogenesis in patients with ischemic heart disease: Clinical trial and preliminary results. Jpn Circ J 65: 845-847, 2001
112. Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Mesquita CT, Rossi MI, Carvalho AC, Dutra HS, Dohmann HJ, Silva GV, Belem L, Vivacqua R, Rangel FO, Esporcatte R, Geng YJ, Vaughn WK, Assad JA, Mesquita ET, Willerson JT: Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 107: 2294-2302, 2003
113. Tse HF, Kwong YL, Chan JK, Lo G, Ho CL, Lau CP: Angiogenesis in ischaemic myocardium by intramyocardial autologous bone marrow mononuclear cell implantation. Lancet 361: 47-49, 2003
114. Hill JM, Syed MA, Arai AE, Powell TM, Paul JD, Zalos G, Read EJ, Khuu HM, Leitman SF, Horne M, Csako G, Dunbar CE, Waclawiw MA, Cannon RO 3rd: Outcomes and risks of granulocyte colony-stimulating factor in patients with coronary artery disease. J Am Coll Cardiol 46: 1643-1648, 2005
115. Stamm C, Kleine HD, Westphal B, Petzsch M, Kittner C, Nienaber CA, Freund M, Steinhoff G: CABG and bone marrow stem cell transplantation after myocardial infarction. Thorac Cardiovasc Surg 52: 152-158, 2004
116. Stamm C, Westphal B, Kleine HD, Petzsch M, Kittner C, Klinge H, Schumichen C, Nienaber CA, Freund M, Steinhoff G: Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 361: 45-46, 2003
117. Strauer BE, Brehm M, Zeus T, Bartsch T, Schannwell C, Antke C, Sorg RV, Kogler G, Wernet P, Muller HW, Kostering M: Regeneration of human infarcted heart muscle by lntracoronary autologous bone marrow cell transplantation in chronic coronary artery disease: The IACT Study. J Am Coll Cardiol 46: 1651-1658, 2005
118. Assmus B, Honold J, Schachinger V, Britten MB, Fischer-Rasokat U, Lehmann R, Teupe C, Pistorius K, Martin H, Abolmaali ND, Tonn T, Dimmeler S, Zeiher AM: Transcoronary transplantation of progenitor cells after myocardial infarction. N Engl J Med 355: 1222-1232, 2006
119. Tateishi-Yuyama E, Matsubara H, Murohara T, Ikeda U, Shintani S, Masaki H, Amano K, Kishimoto Y, Yoshimoto K, Akashi H, Shimada K, Iwasaka T, Imaizumi T: Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: A pilot study and a randomised controlled trial. Lancet 360: 427-435, 2002
120. Bahlmann FH, De Groot K, Spandau JM, Landry AL, Hertel B, Duckert T, Boehm SM, Menne J, Haller H, Fliser D: Erythropoietin regulates endothelial progenitor cells. Blood 103: 921-926, 2004
121. Dimmeler S, Zeiher AM, Schneider MD: Unchain my heart: The scientific foundations of cardiac repair. J Clin Invest 115: 572-583, 2005
122. Losordo DW, Dimmeler S: Therapeutic angiogenesis and vasculogenesis for ischemic disease: Part I - Angiogenic cytokines. Circulation 109: 2487-2491, 2004
123. Dzau VJ, Gnecchi M, Pachori AS, Morello F, Melo LG: Therapeutic potential of endothelial progenitor cells in cardiovascular diseases. Hypertension 46: 7-18, 2005