Isolation of putative progenitor endothelial cells for angiogenesis

Science

Volumn 275, Issue 5302, 1997, Pages 964-967

  Asahara, Takayuki ^a   Murohara, Toyoaki ^a   Sullivan, Alison ^a   Silver, Marcy ^a   Van Der Zee, Rien ^a   Li, Tong ^a   Witzenbichler, Bernhard ^a   Schatteman, Gina ^a   Isner, Jeffrey M ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GROWTH FACTOR RECEPTOR; MEMBRANE ANTIGEN; MESSENGER RNA; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; COLLATERAL CIRCULATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTER; HINDLIMB; HUMAN; HUMAN CELL; LIMB ISCHEMIA; MONONUCLEAR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RABBIT; STEM CELL; UMBILICAL VEIN;

ANIMALS; ANTIGENS, CD34; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL SEPARATION; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; FLOW CYTOMETRY; HINDLIMB; HUMANS; ISCHEMIA; MICE; MICE, INBRED C57BL; MICE, NUDE; MICE, TRANSGENIC; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE; RABBITS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, GROWTH FACTOR; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; STEM CELLS;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0031019745     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.275.5302.964     Document Type: Article

References (46)

1. J. Folkman and Y. Shing, J. Biol. Chem. 267, 10931 (1992); W. Schaper, M. D. Brahander, P. Lewi, Circ. Res. 28, 671 (1971); W. Risau, FASEB J. 9, 926 (1995).
2. J. Folkman and Y. Shing, J. Biol. Chem. 267, 10931 (1992); W. Schaper, M. D. Brahander, P. Lewi, Circ. Res. 28, 671 (1971); W. Risau, FASEB J. 9, 926 (1995).
3. J. Folkman and Y. Shing, J. Biol. Chem. 267, 10931 (1992); W. Schaper, M. D. Brahander, P. Lewi, Circ. Res. 28, 671 (1971); W. Risau, FASEB J. 9, 926 (1995).
4. W. Risau et al., Development 102, 471 (1988); L. Pardanaud, C. Altman, P. Kitos, F. Dieterien-Lievre, ibid. 105, 473 (1989).
5. W. Risau et al., Development 102, 471 (1988); L. Pardanaud, C. Altman, P. Kitos, F. Dieterien-Lievre, ibid. 105, 473 (1989).
6. I. Flamme and W. Risau, ibid. 116, 435 (1992).
7. W. His, Abhandl. K.S. Ges. Wiss. Math.-Phys. 22, 171 (1900); M. Weiss and S. H. Orkin, J. Clin. Invest. 97, 591 (1996).
8. W. His, Abhandl. K.S. Ges. Wiss. Math.-Phys. 22, 171 (1900); M. Weiss and S. H. Orkin, J. Clin. Invest. 97, 591 (1996).
9. W. Brugger, S. Heimfeld, R. J. Berenson, R. Mertelsmann, L. Kanz, N. Engl. J. Med. 333, 283 (1995).
10. M. Wu et al., J. Vasc. Surg. 21, 862 (1995); Q. Shi et al., ibid. 20, 546 (1994); Y. Noishiki, Y. Tomizawa, Y. Yamane, A. Matsumoto, Nature Med. 2, 90 (1996).
11. M. Wu et al., J. Vasc. Surg. 21, 862 (1995); Q. Shi et al., ibid. 20, 546 (1994); Y. Noishiki, Y. Tomizawa, Y. Yamane, A. Matsumoto, Nature Med. 2, 90 (1996).
12. M. Wu et al., J. Vasc. Surg. 21, 862 (1995); Q. Shi et al., ibid. 20, 546 (1994); Y. Noishiki, Y. Tomizawa, Y. Yamane, A. Matsumoto, Nature Med. 2, 90 (1996).
13. C. I. Civin et al., J. Immunol. 133, 157 (1984); F. Katz, R. W. Tindle, D. R. Sutherland, M. D. Greaves, Leukemia Res. 9, 191 (1985); R. G. Andrews, J. W. Singer, I. D. Bernstein, Blood 67, 842 (1986).
14. C. I. Civin et al., J. Immunol. 133, 157 (1984); F. Katz, R. W. Tindle, D. R. Sutherland, M. D. Greaves, Leukemia Res. 9, 191 (1985); R. G. Andrews, J. W. Singer, I. D. Bernstein, Blood 67, 842 (1986).
15. C. I. Civin et al., J. Immunol. 133, 157 (1984); F. Katz, R. W. Tindle, D. R. Sutherland, M. D. Greaves, Leukemia Res. 9, 191 (1985); R. G. Andrews, J. W. Singer, I. D. Bernstein, Blood 67, 842 (1986).
16. J. Fina et al., Blood 75, 2417 (1990); D. Soligo et al., Leukemia (Basingstoke) 5, 1026 (1991); A. Ito, S. Nomura, S. Hirota, T. Suda, Y. Kitamura, Lab. Invest. 72, 532 (1995).
17. J. Fina et al., Blood 75, 2417 (1990); D. Soligo et al., Leukemia (Basingstoke) 5, 1026 (1991); A. Ito, S. Nomura, S. Hirota, T. Suda, Y. Kitamura, Lab. Invest. 72, 532 (1995).
18. J. Fina et al., Blood 75, 2417 (1990); D. Soligo et al., Leukemia (Basingstoke) 5, 1026 (1991); A. Ito, S. Nomura, S. Hirota, T. Suda, Y. Kitamura, Lab. Invest. 72, 532 (1995).
19. C. deVries et al., Science 255, 989 (1992); B. I. Terman et al., Biochem. Biophys. Res. Commun. 187, 1579 (1992); F. Shalaby et al., Nature 376, 62 (1995).
20. C. deVries et al., Science 255, 989 (1992); B. I. Terman et al., Biochem. Biophys. Res. Commun. 187, 1579 (1992); F. Shalaby et al., Nature 376, 62 (1995).
21. C. deVries et al., Science 255, 989 (1992); B. I. Terman et al., Biochem. Biophys. Res. Commun. 187, 1579 (1992); F. Shalaby et al., Nature 376, 62 (1995).
22. W. Matthews et al., Proc. Natl. Acad. Sci. U.S.A. 88, 9026 (1991).
23. B. Millauer et al., Cell 72, 835 (1993); T. P. Yamaguchi, D. J. Dumont, R. A. Conlon, M. L. Breitman, J. Rossant, Development 118, 489 (1993).
24. B. Millauer et al., Cell 72, 835 (1993); T. P. Yamaguchi, D. J. Dumont, R. A. Conlon, M. L. Breitman, J. Rossant, Development 118, 489 (1993).
25. Single-donor human peripheral blood was obtained with a 20-gauge intravenous catheter. The first 3 ml was discarded, and the leukocyte fraction was obtained by Ficoll density gradient centrifugation. The cells were plated on plastic tissue culture for 1 hour to avoid contamination by differentiated adhesive cells.
26. 6 of each) were analyzed with anti-CD34 (Biodesign, Kennebunkport, ME) and anti-Flk-1 (Santa Cruz Biotechnologies, Santa Cruz, CA).
27. The medium for all cell culture experiments was M-199 with 20% fetal bovine serum and bovine brain extract (Clonetics, San Diego).
28. P. J. Newman et al., Science 247, 1219 (1990); T. N. Sato et al., Nature 376, 70 (1995); H. Schnurch and W. Risau, Development 119, 957 (1993); M. P. Bevilacqua, Annu. Rev. Immunol. 11, 767 (1993).
29. P. J. Newman et al., Science 247, 1219 (1990); T. N. Sato et al., Nature 376, 70 (1995); H. Schnurch and W. Risau, Development 119, 957 (1993); M. P. Bevilacqua, Annu. Rev. Immunol. 11, 767 (1993).
30. P. J. Newman et al., Science 247, 1219 (1990); T. N. Sato et al., Nature 376, 70 (1995); H. Schnurch and W. Risau, Development 119, 957 (1993); M. P. Bevilacqua, Annu. Rev. Immunol. 11, 767 (1993).
31. P. J. Newman et al., Science 247, 1219 (1990); T. N. Sato et al., Nature 376, 70 (1995); H. Schnurch and W. Risau, Development 119, 957 (1993); M. P. Bevilacqua, Annu. Rev. Immunol. 11, 767 (1993).
32. T. Asashara et al., data not shown.
33. R. van der Zee et al., Circulation, in press.
34. The mean percent of Dil-labeled capillaries among total CD31-positive capillaries was determined by averaging counts made in 10 randomly selected fields (×400).
35. New Zealand White rabbits (3.8 to 4.2 kg, n = 4, Pine Acre Rabbitry, Norton, MA) underwent ligation of the popliteal and saphenous arteries distally, the external iliac artery proximally, and all femoral arterial branches, after which the femoral artery was excised [S. Takeshita et al., J. Clin. Invest. 93, 662 (1994); L. Q. Pu et al., Circulation 88, 208 (1993); R. Baffour et al., J. Vasc. Surg. 16, 181 (1992)].
36. New Zealand White rabbits (3.8 to 4.2 kg, n = 4, Pine Acre Rabbitry, Norton, MA) underwent ligation of the popliteal and saphenous arteries distally, the external iliac artery proximally, and all femoral arterial branches, after which the femoral artery was excised [S. Takeshita et al., J. Clin. Invest. 93, 662 (1994); L. Q. Pu et al., Circulation 88, 208 (1993); R. Baffour et al., J. Vasc. Surg. 16, 181 (1992)].
37. New Zealand White rabbits (3.8 to 4.2 kg, n = 4, Pine Acre Rabbitry, Norton, MA) underwent ligation of the popliteal and saphenous arteries distally, the external iliac artery proximally, and all femoral arterial branches, after which the femoral artery was excised [S. Takeshita et al., J. Clin. Invest. 93, 662 (1994); L. Q. Pu et al., Circulation 88, 208 (1993); R. Baffour et al., J. Vasc. Surg. 16, 181 (1992)].
38. J. M. Isner et al., Lancet 348, 370 (1996).
39. M. R. Tschudi et al., J. Clin. Invest. 98, 899 (1996).
40. Y. Sato et al., Exp. Cell Res. 204, 223 (1993); M. S. Pepper, N. Ferrara, L. Orci, R. Montesano, Biochem. Biophys. Res. Commun. 181, 902 (1991); D. R. Senger et al., Am. J. Pathol. 149, 293 (1996).
41. Y. Sato et al., Exp. Cell Res. 204, 223 (1993); M. S. Pepper, N. Ferrara, L. Orci, R. Montesano, Biochem. Biophys. Res. Commun. 181, 902 (1991); D. R. Senger et al., Am. J. Pathol. 149, 293 (1996).
42. Y. Sato et al., Exp. Cell Res. 204, 223 (1993); M. S. Pepper, N. Ferrara, L. Orci, R. Montesano, Biochem. Biophys. Res. Commun. 181, 902 (1991); D. R. Senger et al., Am. J. Pathol. 149, 293 (1996).
43. Glyceraldehyde phosphate dehydrogenase (GAPDH) was used as a positive control. The paired primers used (sense/antisense) were as follows: for ecNOS,
44. AAG ACA TTT TCG GGC TCA CGC TGC GCA CCC/ TGG GGT AGG CAC TTT AGT AGT TCT CCT AAC [548-base pairs (bp) PCR product]; for Flk-1 (KDR), CAA CAA AGT CGG GAG AGG AG/ATG ACG ATG GAC AAG TAG CC (819-bp PCR product); for CD31, GCT GTT GGT GGA AGG AGT GC/GAA GTT GGC TGG AGG TGC TC (645-bp PCR product); for GAPDH, TGA AGG TCG GAG TCA ACG GAT TTG/ CAT GTG GGC CAT GAG GTC CAC CAC (983-bp PCR product).
45. CD34- cells cultured in six-well plates were washed and then bathed in 5 ml of filtered Krebs-Henseleit solution. Cell plates were kept on a slide warmer (Lab Line Instruments, Melrose Park, IL) to maintain temperature between 35° and 37°C. The sensor probe was inserted vertically into the wells, and the tip of the electrode was positioned 2 mm under the surface of the solution.
46. Supported by grants from NIH National Heart, Lung, and Blood Institute numbers 02824, 53354, and 57516, the American Heart Association, the E. L. Wiegand Foundation, and in part by the Uehara Memorial Foundation (T.M.).