Peripheral infusion of rat bone marrow derived endothelial progenitor cells leads to homing in acute lung injury

Respiratory Research

Volumn 8, Issue , 2007, Pages

  Kähler, Christian M ^a   Wechselberger, Jutta ^a   Hilbe, Wolfgang ^a   Gschwendtner, Andreas ^a   Colleselli, Daniela ^a   Niederegger, Harald ^a   Boneberg, Eva Maria ^b   Spizzo, Gilbert ^a   Wendel, Albrecht ^c   Gunsilius, Eberhard ^a   Patsch, Josef R ^a   Hamacher, Jürg ^c,d  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF KONSTANZ   (Switzerland)

^c UNIVERSITY OF KONSTANZ   (Germany)

^d SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT RESPIRATORY DISTRESS SYNDROME; ANGIOGENESIS; ANIMAL; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; FEMALE; INFUSION; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; METHODOLOGY; PATHOLOGY; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; FEMALE; INFUSIONS, PARENTERAL; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; NEOVASCULARIZATION, PHYSIOLOGIC; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY DISTRESS SYNDROME, ADULT;

EID: 35548992707     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/1465-9921-8-50     Document Type: Article

References (97)

1. Weibel ER, Taylor CR. Design and structure of the human lung. Pulmonary diseases and disorders 1988, 2:11-60. New York, St. Louis, San Francisco, McGraw-Hill, Fishman AP, 2.
2. Lin Y, Weisdorf DJ, Solovey A, Hebbel RP. Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 2000, 105:71-77. 382587, 10619863, 10.1172/JCI8071.
3. Rafii S. Circulating endothelial precursors: mystery, reality, and promise. J Clin Invest 2000, 105:17-19. 382591, 10619857, 10.1172/JCI8774.
4. Matute-Bello G, Liles WC, Steinberg KP, Kiener PA, Mongovin S, Chi EY, Jonas M, Martin TR. Soluble Fas ligand induces epithelial cell apoptosis in humans with acute lung injury (ARDS). J Immunol 1999, 163:2217-2225.
5. Bernard GR, Artigas A, Drighan DL, Carlet J, Falke K, Hudson L, Lamy N, Legall JR, Maurice A, Spragg R, committee. The American-European consensus on ARDS: Definition, mechanisms, relevant outcome, and clinical trial coordination. Am J Respir Crit Care Med 1994, 149:818-824.
6. Tomashefski JF, Davies P, Boggis C, Greene R, Zapol WM, Reid LM. The pulmonary vascular lesions of the adult respiratory distress syndrome. Am J Pathol 1983, 112:112-126. 1916312, 6859225.
7. Bachofen M, Weibel ER. Alterations of the gas exchange apparatus in adult respiratory insufficiency associated with septicemia. Am Rev Respir Dis 1977, 116:589-615.
8. Fujita M, Kuwano K, Kunitake R, Hagimoto N, Miyazaki H, Kaneko Y, Kawasaki M, Maeyama T, Hara N. Endothelial cell apoptosis in lipopolysaccharide-induced lung injury in mice. Int Arch Allergy Immunol 1998, 117:202-208. 10.1159/000024011, 9831808.
9. Kawasaki M, Kuwano K, Hagimoto N, Matsuba T, Kunitake R, Tanaka T, Maeyama T, Hara N. Protection from lethal apoptosis in lipopolysaccharide-induced acute lung injury in mice by a caspase inhibitor. Am J Pathol 2000, 157:597-603. 1850133, 10934162.
10. Kitamura Y, Hashimoto S, Mizuta N, Kobayashi A, Kooguchi K, Fujiwara I, Nakajima H. Fas/FasL-dependent apoptosis of alveolar cells after lipopolysaccharide-induced lung injury in mice. Am J Respir Crit Care Med 2001, 163:762-769.
11. Kim CFB, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, Crowley D, Bronson RT, Jacks T. Identification of Bronchioalveolar Stem Cells in Normal Lung and Lung Cancer. Cell 2005, 121:823-835. 10.1016/j.cell.2005.03.032, 15960971.
12. Springer ML, Brazelton TR, Blau HM. Not the usual suspects: the unexpected sources of tissue regeneration. J Clin Invest 2001, 107:1355-1356. 209330, 11390416, 10.1172/JCI13248.
13. Yamada M, Kubo H, Kobayashi S, Ishizawa K, Numasaki M, Ueda S, Suzuki T, Sasaki H. Bone marrow-derived progenitor cells are important for lung repair after lipopolysaccharide-induced lung injury. J Immunol 2004, 172:1266-1272.
14. Herzog EL, Van Arnam J, Hu BQ, Krause DS. Threshold of Lung Injury Required for the Appearance of Marrow-Derived Lung Epithelia. Stem Cells 2006, 24:1986-1992. 10.1634/stemcells.2005-0579, 16868209.
15. Krause DS. Plasticity of marrow-derived stem cells. Gene Ther 2002, 9:754-758. 10.1038/sj.gt.3301760, 12032704.
16. Rafii S, Oz MC, Seldomridge JA, Ferris B, Asch AS, Nachman RL, Shapiro F, Rose EA, Levin HR. Characterization of hematopoietic cells arising on the textured surface of left ventricular assist devices. Ann Thorac Surg 1995, 60:1627-1632. 10.1016/0003-4975(95)00807-1, 8787455.
17. 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. 10.1126/science.275.5302.964, 9020076.
18. Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, Neutzel S, Sharkis SJ. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 2001, 105:369-377. 10.1016/S0092-8674(01)00328-2, 11348593.
19. Okamoto R, Yajima T, Yamazaki M, Kanai T, Mukai M, Okamoto S, Ikeda Y, Hibi T, Inazawa J, Watanabe M. Damaged epithelia regenerated by bone marrow-derived cells in the human gastrointestinal tract. Nat Med 2002, 8:1011-1017. 10.1038/nm755, 12195435.
20. Kotton DN, Ma BY, Cardoso WV, Sanderson EA, Summer RS, Williams MC, Fine A. Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development 2001, 128:5181-5188.
21. Suratt BT, Cool CD, Serls AE, Chen L, Varella-Garcia M, Shpall EJ, Brown KK, Worthen GS. Human pulmonary chimerism after hematopoietic stem cell transplantation. Am J Respir Crit Care Med 2003, 168:318-322. 10.1164/rccm.200301-145OC, 12724127.
22. Abe S, Boyer C, Liu X, Wen FQ, Kobayashi T, Fang Q, Wang X, Hashimoto M, Sharp JG, Rennard SI. Cells derived from the circulation contribute to the repair of lung injury. Am J Respir Crit Care Med 2004, 170:1158-1163. 10.1164/rccm.200307-908OC, 15282197.
23. Spencer H, Rampling D, Aurora P, Bonnet D, Hart SL, Jaffe A. Transbronchial biopsies provide longitudinal evidence for epithelial chimerism in children following sex mismatched lung transplantation. Thorax 2005, 60:60-62. 10.1136/thx.2004.029678, 15618585.
24. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 2002, 8:403-409. 10.1038/nm0402-403, 11927948.
25. Rochefort GY, Vaudin P, Bonnet N, Pages JC, Domenech J, Charbord P, Eder V. Influence of hypoxia on the domiciliation of mesenchymal stem cells after infusion into rats: possibilities of targeting pulmonary artery remodeling via cells therapies?. Respir Res 2005, 6:125.:125.
26. Lagasse E, Connors H, Al Dhalimy M, Reitsma M, Dohse M, Osborne L, Wang X, Finegold M, Weissman IL, Grompe M. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 2000, 6:1229-1234. 10.1038/81326, 11062533.
27. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM, Leri A, Anversa P. Bone marrow cells regenerate infarcted myocardium. Nature 2001, 410:701-705. 10.1038/35070587, 11287958.
28. Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998, 279:1528-1530. 10.1126/science.279.5356.1528, 9488650.
29. Hillebrands JL, Klatter FA, van den Hurk BM, Popa ER, Nieuwenhuis P, Rozing J. Origin of neointimal endothelium and alpha-actin-positive smooth muscle cells in transplant arteriosclerosis. J Clin Invest 2001, 107:1411-1422. 209313, 11390423, 10.1172/JCI10233.
30. Pereira RF, Halford KW, O'Hara MD, Leeper DB, Sokolov BP, Pollard MD, Bagasra O, Prockop DJ. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci U S A 1995, 92:4857-4861. 41806, 7761413, 10.1073/pnas.92.11.4857.
31. Epperly MW, Guo H, Gretton JE, Greenberger JS. Bone marrow origin of myofibroblasts in irradiation pulmonary fibrosis. Am J Respir Cell Mol Biol 2003, 29:213-224. 10.1165/rcmb.2002-0069OC, 12649121.
32. Eglitis MA, Mezey E. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci U S A 1997, 94:4080-4085. 20571, 9108108, 10.1073/pnas.94.8.4080.
33. Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 2000, 290:1779-1782. 10.1126/science.290.5497.1779, 11099419.
34. Kotton DN, Fabian AJ, Mulligan RC. Failure of Bone Marrow to Reconstitute Lung Epithelium. Am J Respir Cell Mol Biol 2005, 2005-0175RC. 15961722.
35. 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 2002, 360:427-435. 10.1016/S0140-6736(02)09670-8, 12241713.
36. 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 2002, 106:3009-3017. 10.1161/01.CIR.0000043246.74879.CD, 12473544.
37. 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 2002, 106:1913-1918. 10.1161/01.CIR.0000034046.87607.1C, 12370212.
38. 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 2006, 355:1222-1232. 10.1056/NEJMoa051779, 16990385.
39. 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, the REPA. Intracoronary Bone Marrow-Derived Progenitor Cells in Acute Myocardial Infarction. N Engl J Med 2006, 355:1210-1221. 10.1056/NEJMoa060186, 16990384.
40. 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. Intracoronary Injection of Mononuclear Bone Marrow Cells in Acute Myocardial Infarction. N Engl J Med 2006, 355:1199-1209. 10.1056/NEJMoa055706, 16990383.
41. 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 WF. Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. Lancet 2006, 367:113-121. 10.1016/S0140-6736(05)67861-0, 16413875.
42. Meyer GP, Wollert 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 2006, 113:1287-1294. 10.1161/CIRCULATIONAHA.105.575118, 16520413.
43. 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 2003, 348:593-600. 10.1056/NEJMoa022287, 12584367.
44. Bull TM, Golpon H, Hebbel RP, Solovey A, Cool CD, Tuder RM, Geraci MW, Voelkel NF. Circulating endothelial cells in pulmonary hypertension. Thromb Haemost 2003, 90:698-703.
45. Bompais H, Chagraoui J, Canron X, Crisan M, Liu XH, Anjo A, Tolla-Le Port C, Leboeuf M, Charbord P, Bikfalvi A, Uzan G. Human endothelial cells derived from circulating progenitors display specific functional properties as compared to mature vessel wall endothelial cells. Blood 2004, 103:2577-2584. 10.1182/blood-2003-08-2770, 14630797.
46. 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 2003, 93:17e-24.
47. 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. 10.1167/iovs.03-0371, 14578417.
48. Xu Q, Zhang Z, Davison F, Hu Y. Circulating progenitor cells regenerate endothelium of vein graft atherosclerosis, which is diminished in ApoE-deficient mice. Circ Res 2003, 93:e76-e86. 10.1161/01.RES.0000097864.24725.60, 14512446.
49. Sata M. Circulating vascular progenitor cells contribute to vascular repair, remodeling, and lesion formation. Trends Cardiovasc Med 2003, 13:249-253. 10.1016/S1050-1738(03)00106-3, 12922022.
50. Park S, Tepper OM, Galiano RD, Capla JM, Baharestani S, Kleinman ME, Pelo CR, Levine JP, Gurtner GC. Selective recruitment of endothelial progenitor cells to ischemic tissues with increased neovascularization. Plast Reconstr Surg 2004, 113:284-293. 10.1097/01.PRS.0000091169.51035.A5, 14707648.
51. Hu Y, Davison F, Zhang Z, Xu Q. Endothelial replacement and angiogenesis in arteriosclerotic lesions of allografts are contributed by circulating progenitor cells. Circulation 2003, 108:3122-3127. 10.1161/01.CIR.0000105722.96112.67, 14656919.
52. Peinado VI, Ramirez J, Roca J, Rodriguez-Roisin R, Barbera JA. Identification of Vascular Progenitor Cells in Pulmonary Arteries of Patients with Chronic Obstructive Pulmonary Disease. Am J Respir Cell Mol Biol 2006, 34:257-263. 10.1165/rcmb.2005-0255OC, 16239642.
53. Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, Bohm M, Nickenig G. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 2005, 353:999-1007. 10.1056/NEJMoa043814, 16148285.
54. Blann AD, Woywodt A, Bertolini F, Bull TM, Buyon JP, Clancy RM, Haubitz M, Hebbel RP, Lip GY, Mancuso P, Sampol J, Solovey A, Dignat-George F. Circulating endothelial cells. Biomarker of vascular disease. Thromb Haemost 2005, 93:228-235.
55. Burnham EL, Taylor WR, Quyyumi AA, Rojas M, Brigham KL, Moss M. Increased Circulating Endothelial Progenitor Cells are Associated with Survival in Acute Lung Injury. Am J Respir Crit Care Med 2005, 200410-1325OC. 15976374.
56. Yamada M, Kubo H, Ishizawa K, Kobayashi S, Shinkawa M, Sasaki H. Increased circulating endothelial progenitor cells in patients with bacterial pneumonia: evidence that bone marrow derived cells contribute to lung repair. Thorax 2005, 60:410-413. 10.1136/thx.2004.034058, 15860717.
57. Mancuso P, Burlini A, Pruneri G, Goldhirsch A, Martinelli G, Bertolini F. Resting and activated endothelial cells are increased in the peripheral blood of cancer patients. Blood 2001, 97:3658-3661. 10.1182/blood.V97.11.3658, 11369666.
58. Kahler CM, Wechselberger J, Hilbe W, Gschwendtner A, Colleselli D, Hinteregger B, Boneberg EM, Wiedermann CJ, Gunsilius E, Hamacher J. Endothelial progenitor cells home in the transplanted lung after ischemia-reperfusion injury. European Respiratory Journal 2004, 2004:30s.
59. Khakoo AY, Finkel T. Endothelial progenitor cells. Annual Review of Medicine 2005, 56:79-101. 10.1146/annurev.med.56.090203.104149, 15660503.
60. Novak K. Angiogenesis: Trojan horses. Nat Rev Cancer 2003, 3:396.
61. Jamur MC, Grodzki AC, Moreno AN, de Mello LF, Pastor MV, Berenstein EH, Siraganian RP, Oliver C. Identification and isolation of rat bone marrow-derived mast cells using the mast cell-specific monoclonal antibody AA4. J Histochem Cytochem 2001, 49:219-228.
62. Kahler CM, Herold M, Reinisch N, Wiedermann CJ. Interaction of substance P with epidermal growth factor and fibroblast growth factor in cyclooxygenase-dependent proliferation of human skin fibroblasts. J Cell Physiol 1996, 166:601-608. 10.1002/(SICI)1097-4652(199603)166:3<601::AID-JCP15>3.0.CO;2-9, 8600164.
63. Stammberger U, Hamacher J, Hillinger S, Schmid RA. sCR1sLeX ameliorates ischemia/reperfusion injury in experimental lung transplantation. J Thorac Cardiovasc Surg 2000, 120:1078-1084. 10.1067/mtc.2000.111175, 11088029.
64. Gunsilius E, Petzer AL, Duba HC, Kahler CM, Gastl G. Circulating endothelial cells after transplantation. Lancet 2001, 357:1449-1450. 10.1016/S0140-6736(00)04605-5, 11360955.
65. Nagaya N, Kangawa K, Kanda M, Uematsu M, Horio T, Fukuyama N, Hino J, Harada-Shiba M, Okumura H, Tabata Y, Mochizuki N, Chiba Y, Nishioka K, Miyatake K, Asahara T, Hara H, Mori H. Hybrid cell-gene therapy for pulmonary hypertension based on phagocytosing action of endothelial progenitor cells. Circulation 2003, 108:889-895. 10.1161/01.CIR.0000079161.56080.22, 12835224.
66. Zhao YD, Courtman DW, Deng Y, Kugathasan L, Zhang Q, Stewart DJ. Rescue of monocrotaline-induced pulmonary arterial hypertension using bone marrow-derived endothelial-like progenitor cells: efficacy of combined cell and eNOS gene therapy in established disease. Circ Res 2005, 96:442-450. 10.1161/01.RES.0000157672.70560.7b, 15692087.
67. Davie NJ, Crossno JT, Frid MG, Hofmeister SE, Reeves JT, Hyde DM, Carpenter TC, Brunetti JA, McNiece IK, Stenmark KR. Hypoxia-induced pulmonary artery adventitial remodeling and neovascularization: contribution of progenitor cells. Am J Physiol Lung Cell Mol Physiol 2004, 286:L668-L678. 10.1152/ajplung.00108.2003, 12754186.
68. Murohara T, Ikeda H, Duan J, Shintani S, Sasaki K, Eguchi H, Onitsuka I, Matsui K, Imaizumi T. Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J Clin Invest 2000, 105:1527-1536. 300847, 10841511, 10.1172/JCI8296.
69. 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 2000, 97:3422-3427. 16255, 10725398, 10.1073/pnas.070046397.
70. Grassmé H, Kirschnek S, Riethmueller J, Riehle A, von Kürthy G, Lang F, Weller M, Gulbins E. CD95/CD95 ligand interactions of epithelial cells in host defense to Pseudomonas aeruginosa. Science 2000, 290:527-530. 10.1126/science.290.5491.527, 11039936.
71. Stammberger U, Gaspert A, Hillinger S, Vogt P, Odermatt B, Weder W, Schmid RA. Apoptosis induced by ischemia and reperfusion in experimental lung transplantation. Ann Thorac Surg 2000, 69:1532-1536. 10.1016/S0003-4975(00)01228-5, 10881837.
72. Matthay MA, Zimmerman GA, Esmon C, Bhattacharya J, Coller B, Doerschuk CM, Floros J, Gimbrone MA, Hoffman E, Hubmayr RD, Leppert M, Matalon S, Munford R, Parsons P, Slutsky AS, Tracey KJ, Ward P, Gail DB, Harabin AL. Future Research Directions in Acute Lung Injury: Summary of a National Heart, Lung, and Blood Institute Working Group. Am J Respir Crit Care Med 2003, 167:1027-1035. 10.1164/rccm.200208-966WS, 12663342.
73. Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell MA. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 2001, 107:1395-1402. 209322, 11390421, 10.1172/JCI12150.
74. Moore MAS. Putting the neo into neoangiogenesis. J Clin Invest 2002, 109:313-315. 150863, 11827990, 10.1172/JCI200214940.
75. Badorff C, Brandes RP, Popp R, Rupp S, Urbich C, Aicher A, Fleming I, Busse R, Zeiher AM, Dimmeler S. Transdifferentiation of blood-derived human adult endothelial progenitor cells into functionally active cardiomyocytes. Circulation 2003, 107:1024-1032. 10.1161/01.CIR.0000051460.85800.BB, 12600917.
76. Gulati R, Jevremovic D, Peterson TE, Chatterjee S, Shah V, Vile RG, Simari RD. Diverse origin and function of cells with endothelial phenotype obtained from adult human blood. Circ Res 2003, 93:1023-1025. 10.1161/01.RES.0000105569.77539.21, 14605020.
77. Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L, Petersen BE, Scott EW. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 2002, 416:542-545. 10.1038/nature730, 11932747.
78. Wang X, Willenbring H, Akkari Y, Torimaru Y, Foster M, Al Dhalimy M, Lagasse E, Finegold M, Olson S, Grompe M. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 2003, 422:897-901. 10.1038/nature01531, 12665832.
79. Vassilopoulos G, Wang PR, Russell DW. Transplanted bone marrow regenerates liver by cell fusion. Nature 2003, 422:901-904. 10.1038/nature01539, 12665833.
80. Rehman J, Li J, Orschell CM, March KL. Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 2003, 107:1164-1169. 10.1161/01.CIR.0000058702.69484.A0, 12615796.
81. Voswinckel R, Ziegelhoeffer T, Heil M, Kostin S, Breier G, Mehling T, Haberberger R, Clauss M, Gaumann A, Schaper W, Seeger W. Circulating vascular progenitor cells do not contribute to compensatory lung growth. Circ Res 2003, 93:372-379. 10.1161/01.RES.0000087643.60150.C2, 12881479.
82. Theise ND, Nimmakayalu M, Gardner R, Illei PB, Morgan G, Teperman L, Henegariu O, Krause DS. Liver from bone marrow in humans. Hepatology 2000, 32:11-16. 10.1053/jhep.2000.9124, 10869283.
83. 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 2001, 98:10344-10349. 56963, 11504914, 10.1073/pnas.181177898.
84. Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Breidenbach C, Fichtner S, Korte T, Hornig B, Messinger D. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. The Lancet 2004, 364:141-148.
85. Vernooy JH, Dentener MA, van Suylen RJ, Buurman WA, Wouters EF. Intratracheal instillation of lipopolysaccharide in mice induces apoptosis in bronchial epithelial cells: no role for tumor necrosis factor-alpha and infiltrating neutrophils. Am J Respir Cell Mol Biol 2001, 24:569-576.
86. 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 2003, 102:1340-1346. 10.1182/blood-2003-01-0223, 12702503.
87. Schuch G, Heymach JV, Nomi M, Machluf M, Force J, Atala A, Eder JP, Folkman J, Soker S. Endostatin inhibits the vascular endothelial growth factor-induced mobilization of endothelial progenitor cells. Cancer Res 2003, 63:8345-8350.
88. Dorrell MI, Otani A, Aguilar E, Moreno SK, Friedlander M. Adult bone marrow-derived stem cells utilize R-cadherin to target sites of neovascularization in the developing retina. Blood 2004,
89. Grefte A, van der GM, van Son W, The TH. Circulating cytomegalovirus (CMV)-infected endothelial cells in patients with an active CMV infection. J Infect Dis 1993, 167:270-277.
90. Monestiroli S, Mancuso P, Burlini A, Pruneri G, Dell'Agnola C, Gobbi A, Martinelli G, Bertolini F. Kinetics and viability of circulating endothelial cells as surrogate angiogenesis marker in an animal model of human lymphoma. Cancer Res 2001, 61:4341-4344.
91. Beerepoot LV, Mehra N, Vermaat JS, Zonnenberg BA, Gebbink MF, Voest EE. Increased levels of viable circulating endothelial cells are an indicator of progressive disease in cancer patients. Ann Oncol 2004, 15:139-145. 10.1093/annonc/mdh017, 14679134.
92. Hilbe W, Dirnhofer S, Oberwasserlechner F, Schmid T, Gunsilius E, Hilbe G, Woll E, Kahler CM. CD133 positive endothelial progenitor cells contribute to the tumour vasculature in non-small cell lung cancer. Journal of Clinical Pathology 2004, 57:965-969. 10.1136/jcp.2004.016444, 15333659, 1770433.
93. Shinde P, Friedrich EB, Wolley AE, Gerszten RE, Allport JR, Weissleder R. Bone marrow-derived lin(-)c-kit(+)Sca-1+ stem cells do not contribute to vasculogenesis in Lewis lung carcinoma. Neoplasia 2005, 7:234-240. 1501134, 15799823, 10.1593/neo.04523.
94. Griese DP, Ehsan A, Melo LG, Kong D, Zhang L, Mann MJ, Pratt RE, Mulligan RC, Dzau VJ. Isolation and transplantation of autologous circulating endothelial cells into denuded vessels and prosthetic grafts: implications for cell-based vascular therapy. Circulation 2003, 108:2710-2715. 10.1161/01.CIR.0000096490.16596.A6, 14597586.
95. Conte MS, Birinyi LK, Miyata T, Fallon JT, Gold HK, Whittemore AD, Mulligan RC. Efficient repopulation of denuded rabbit arteries with autologous genetically modified endothelial cells. Circulation 1994, 89:2161-2169.
96. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 2003, 9:702-712. 10.1038/nm0603-702, 12778169.
97. Grove JE, Lutzko C, Priller J, Henegariu O, Theise ND, Kohn DB, Krause DS. Marrow-derived cells as vehicles for delivery of gene therapy to pulmonary epithelium. Am J Respir Cell Mol Biol 2002, 27:645-651.