Gp130-signaling synergizes with FL and TPO for the long-term expansion of cord blood progenitors

Leukemia

Volumn 13, Issue 12, 1999, Pages 2036-2048

  Rappold, I ^a   Watt, S M ^a   Kusadasi, N ^b   Rose John, S ^c   Hatzfeld, J ^d   Ploemacher, R E ^b  

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^b ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d CNRS   (France)

Author keywords

Ex vivo expansion; Gp130 signaling; Hematopoiesis

Indexed keywords

CD34 ANTIGEN; FLT3 LIGAND; GLYCOPROTEIN GP 130; HYBRID PROTEIN; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; STEM CELL FACTOR; THROMBOPOIETIN;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UMBILICAL CORD BLOOD;

EID: 0032760571     PISSN: 08876924     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.leu.2401597     Document Type: Article

References (53)

1. Rubinstein P, Carrier C, Scaradavou A, Kurtzberg I, Adamson J, Migliaccio AR, Berkowitz RL, Cabbad M, Dobrila NL, Taylor PE, Rosenfield RE, Stevens CE. Outcomes among 562 recipients of placental blood transplants from unrelated donors. New Engl J Med 1998; 339: 1565-1577.
2. Wang JC, Doedens M, Dick JE. Primitive human hematopoietic cells are enriched in cord blood compared with adult bone marrow or mobilized peripheral blood as measured by the quantitative in vivo SCID-repopulating cells assay. Blood 1997; 89: 3919-3924.
3. Cairo MS, Wagner JE. Placental and/or umbilical cord blood: an alternative source of hematopoietic stem cells for transplantation. Blood 1997; 90: 4665-4678.
4. Koller MR, Emerson SG, Palsson BO. Large-scale expansion of human stem and progenitor cells from bone marrow mononuclear cells in continuous perfusion cultures. Blood 1993; 82: 378-384.
5. + cells. Blood 1993; 82: 3600-3609.
6. Haylock DN, Makino S, Dowse TL, Trimboli S, Niutta S, To LB, Juttner CA, Simmons PJ. Ex vivo hematopoietic progenitor cell expansion. Immunomethods 1994; 5: 217-225.
7. Fraser CC, Szilvassy SJ, Eaves CJ, Humphries RK. Proliferation of totipotent hematopoietic stem cells in vitro with retention of long-term competitive in vivo reconstituting ability. Proc Natl Acad Sci USA 1992; 89: 1968-1972.
8. Szilvassy SJ, Weller KP, Lin W, Sharma AK, Ho AS, Tsukamoto A, Hoffman R, Leiby KR, Gearing DP. Leukemia inhibitory factor upregulates cytokine expression by a murine stromal cell line enabling the maintenance of highly enriched competitive repopulating stem cells. Blood 1996; 87: 4618-4628.
9. Wineman J, Moore K, Lemischka I, Muller-Sieburg C. Functional heterogeneity of the hematopoietic microenvironment: rare stromal elements maintain long-term repopulating stem cells. Blood 1996; 87: 4082-4090.
10. Miller CL, Eaves CJ. Expansion in vitro of adult murine hematopoietic stem cells with transplantable lympho-myeloid reconstituting ability. Proc Natl Acad Sci USA 1997; 94: 13648-13653.
11. Conneally E, Cashman J, Petzer A, Eaves C. Expansion in vitro of transplantable human cord blood stem cells demonstrated using a quantitative assay of their lympho-myeloid repopulating activity in nonobese diabetic-scid/scid mice. Proc Natl Acad Sci USA 1997; 94: 9836-9041.
12. Bhatia M, Bonnet D, Kapp U, Wang JC, Murdoch B, Dick JE. Quantitative analysis reveals expansion of human hematopoietic repopulating cells after short-term ex vivo culture. J Exp Med 1997; 186: 619-624.
13. Petzer AL, Hogge DE, Landsdorp PM, Reid DS, Eaves CJ. Self-renewal of primitive human hematopoietic cells (long-term-culture-initiating cells) in vitro and their expansion in defined medium. Proc Natl Acad Sci USA 1996; 93: 1470-1474.
14. Shah AJ, Smogorzewska EM, Hannum C, Crooks GM. Flt3 ligand induces proliferation of quiescent human bone marrow CD34+CD38-cells and maintains progenitor cells in in vitro. Blood 1996; 87: 3563-3570.
15. Dooley DC, Xiao M, Oppenlander BK, Plunkett JM, Lyman SD. Flt3 ligand enhances the yield of primitive cells after ex vivo cultivation of CD34+ CD38dim cells and CD34+ CD38dim CD33dim HLA-DR+ cells. Blood 1997; 90: 3903-3913.
16. Haylock DN, Horsfall MJ, Dowse TL, Ramshaw HS, Niutta S, Protopsaltis S, Peng L, Burell C, Rappold I, Buhring HJ, Simmons PJ. Increased recruitment of hematopoietic progenitor cells underlies the ex vivo expansion potential of FLT3 ligand. Blood 1997; 90: 2260-2272.
17. Zandstra PW, Conneally E, Petzer AL, Piret JM, Eaves CJ. Cytokine manipulation of primitive human hematopoietic cell self-renewal. Proc Natl Acad Sci USA 1997; 94: 4698-4703.
18. Lyman SD, Jacobsen SE. c-kit ligand and Flt3 ligand: stem/progenitor cell factors with overlapping yet distinct activities. Blood 1998; 91: 1101-1134.
19. Borge OJ, Ramstjell V, Cui L, Jacobsen SE. Ability of early acting cytokines to directly promote survival and suppress apoptosis of human primitive CD34+CD38-bone marrow cells with multilineage potential at the single-cell level: key role of thrombopoietin. Blood 1997; 90: 2282-2292.
20. Kimura S, Roberts AW, Metcalf D, Alexander WS. Hematopoietic stem cell deficiencies in mice lacking c-Mpl, the receptor for thrombopoietin. Proc Natl Acad Sci USA 1998; 95: 1195-1200.
21. Luens KM, Travis MA, Chen BP, Hill BL, Scollay R, Murray LJ. Thrombopoietin, kit ligand, and flk2/flt3 ligand together induce increased numbers of primitive hematopoietic progenitors from human CD34+Thy-1+Lin-cells with preserved ability to engraft SCID-hu bone. Blood 1998; 91: 1206-1215.
22. Matsunaga T, Kato T, Miyazaki H, Ogawa M. Thrombopoietin promotes the survival of murine hematopoietic long-term reconstituting cells: comparison with the effects of FLT3/FLK-2 ligand and interleukin-6. Blood 1998; 92: 452-461.
23. Solar GP, Kerr WG, Zeigler FC, Hess D, Donahue C, de Sauvage FJ, Eaton DL. Role of c-mpl in early hematopoiesis. Blood 1998; 92: 4-10.
24. Piacibello W, Sanavio F, Garetto L, Severino A, Bergandi D, Ferrario I, Fagioli F, Berger M, Aglietta M. Extensive amplification and self-renewal of human primitive hematopoietic stem cells from cord blood. Blood 1997; 89: 2644-2653.
25. Piacibello W, Sanavio F, Garetto L, Severino A, Dane A, Gammaitoni L, Aglietta M. Differential growth factor requirement of primitive cord blood hematopoietic stem cell for self-renewal and amplification vs proliferation and differentiation. Leukemia 1998; 12: 718-727.
26. Young JC, Varma A, DiGiusto D, Backer MP. Retention of quiescent hematopoietic cells with high proliferative potential during ex vivo stem cell culture. Blood 1996; 87: 545-556.
27. Hauser SP, Kajkenova O, Lipschitz DA. The pivotal role of interleukin 6 in formation and function of hematopoietically active murine long-term bone marrow cultures. Stem Cells 1997; 15: 125-132.
28. Ikebuchi K, Wong GG, Clark SC, Ihle JN, Hirai Y, Ogawa M. Interleukin 6 enhancement of interleukin 3-dependent proliferation of multipotential hemopoietic progenitors. Proc Natl Acad Sci USA 1987; 84: 9035-9039.
29. Tanaka R, Koike K, Imai T, Shiohara M, Kubo T, Amano Y, Komiyama A, Nakahata T. Stem cell factor enhances proliferation, but not maturation, of murine megakaryocytic progenitors in serum-free culture. Blood 1992; 80: 1743-1749.
30. Kishimoto T, Akira S, Narazaki M, Taga T. Interleukin-6 family of cytokines and gp130. Blood 1995; 86: 1243-1254.
31. Yoshida K, Taga T, Saito M, Suematsu S, Kumanogoh A, Tanaka T, Fujiwara H, Hirata M, Yamagami T, Nakahata T, Hirabayashi T, Yoneda Y, Tanaka K, Wang WZ, Mori C, Shiota K, Yoshida N, Kishimoto T. Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc Natl Acad Sci USA 1996; 93: 407-411.
32. Tajima S, Tsuji K, Ebihara Y, Sui X, Tanaka R, Muraoka K, Yoshida M, Yamada K, Yasukawa K, Taga T, Kishimoto T, Nakahata T. Analysis of interleukin 6 receptor and gp130 expressions and proliferative capability of human CD34+ cells. J Exp Med 1996; 184: 1357-1364.
33. Kimura T, Sakabe H, Tanimukai S, Abe T, Urata Y, Yasukawa K, Okano A, Taga T, Sugiyama H, Kishimoto T, Sonoda Y. Simultaneous activation of signals through gp130, c-kit, and interleukin-3 receptor promotes a trilineage blood cell production in the absence of terminally acting lineage-specific factors. Blood 1997; 90. 4767-4778.
34. Peters M, Muller AM, Rose-John S. Interleukin-6 and soluble interleukin-6 receptor: direct stimulation of gp130 and hematopoiesis. Blood 1998; 92: 3495-3504.
35. Sui X, Tsuji K, Tanaka R, Tajima S, Muraoka K, Ebihara Y, Ikebuchi K, Yasukawa K, Taga T, Kishimoto T, Nakahata N. gp130 and c-Kit signalings synergize for ex vivo expansion of human primitive hemopoietic progenitor cells. Proc Natl Acad Sci USA 1995; 92: 2859-2863.
36. Sui X, Tsuji K, Tajima S, Tanaka R, Muraoka K, Ebihara Y, Ikebuchi K, Yasukawa K, Taga T, Kishimoto T, Nakahata T. Erythropoietin-independent erythrocyte production: signals through gp130 and c-kit dramatically promote erythropoiesis from human CD34+ cells. J Exp Med 1996; 183: 837-045.
37. Ebihara Y, Tsuji K, Lyman SD, Sui X, Yoshida M, Muraoka K, Yamada K, Tanaka R, Nakahata T. Synergistic action of Flt3 and gp130 signalings in human hematopoiesis. Blood 1997; 90 4363-4368.
38. Sui X, Tsuji K, Ebihara Y, Tanaka R, Muraoka K, Yoshida M, Yamada K, Yasukawa K, Taga T, Kishimoto T, Nakahata. . Soluble interleukin-6 (IL-6) receptor with IL-6 stimulates megakaryopoiesis from human CD34(+) cells through glycoprotein (gp)130 signaling. Blood 1999; 93: 2525-2532.
39. Peters M, Schirmacher P, Goldschmitt J, Odenthal M, Peschel C, Fattori E, Ciliberto G, Dienes HP, Meyer zum Buschenfelde KH, Rose-John S. Extramedullary expansion of hematopoietic progenitor cells in interleukin (IL)-6-sIL-6R double transgenic mire. J Exp Med 1997; 185: 755-766.
40. Schirmacher P, Peters M, Ciliberto G, Blessing M, Lotz J, Meyer zum Buschenfelde KH, Rose-John S. Hepatocellular hyperplasia, plasmacytoma formation, and extramedullary hematopoiesis in interleukin (IL)-6/soluble IL-6 receptor double-transgenic mice. Am J Pathol 1998: 153: 639-648.
41. Fischer M, Goldschmitt J, Peschel C, Brakenhoff JP, Kallen KJ, Wollmer A, Grotzinger J, Rose-John S.I.A bioactive designer cytokine for human hematopoietic progenitor cell expansion. Nat Biotechnol 1997; 15: 142-145.
42. Breems DA, Blokland EA, Neben S, Ploemacher RE. Frequency analysis of human primitive haematopoietic stem cell subsets using a cobblestone area forming cell assay. Leukemia 1994; 8: 1095-1104.
43. Metcalf D. Hematopoietic regulators: redundancy or subtlety? Blood 1993; 82: 3515-3523.
44. Petzer AL, Zandstra PW, Piret JM, Eaves CJ. Differential cytokine effects on primitive (CD34+CD38-) human hematopoietic cells: novel responses to Flt3-ligand and thrombopoietin. J Exp Med 1996; 183: 2551-2558.
45. Zandstra PW, Conneally E, Piret JM, Eaves CJ. Ontogeny-associated changes in the cytokine responses of primitive human haemopoietic cells. Br J Haematol 1998; 101: 770-778.
46. McKinstry WJ, Li CL, Rasko JE, Nicola NA, Johnson GR, Metcalf D. Cytokine receptor expression on hematopoietic stem and progenitor cells. Blood 1997; 89: 65-71.
47. Tsuji K, Lyman SD, Sudo T, Clark SC, Ogawa M. Enhancement of murine hematopoiesis by synergistic interactions between steel factor (ligand for c-kit), interleukin-11, and other early acting factors in culture. Blood 1992; 79: 2855-2860.
48. Hirota H, Yoshida K, Kishimoto T, Taga T. Continuous activation of gp130, a signal-transducing receptor component for interleukin 6-related cytokines, causes myocardial hypertrophy in mice. Proc Natl Acad Sci USA 1995; 92: 4862-4866.
49. Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, Olweus J, Kearney J, Buck DW. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997; 90: 5002-5012.
50. de Wynter EA, Buck D, Hart C, Heywood R, Coutinho LH, Clayton A, Rafferty JA, Burt D, Cuenechea G, Bueren JA, Gagen D, Fairbairn LJ, Lord BJ, Testa NG. CD34+AC133+ cells isolated from cord blood are highly enriched in long-term culture-initiating cells, NOD/SCID-repopulating cells and dendritic cell progenitors (in process citation). Stem Cells 1998; 16: 387-396.
51. Rakemann T, Niehof M, Kubicka S, Fischer M, Manns MP, Rose-John S, Trautwein C. The designer cytokine hyper-interleukin-6 is a potent activator of STAT3-dependent gene transcription in vivo and in vitro. J Biol Chem 1999; 274: 1257-1266.
52. Peled A, Petit I, Kollet O, Magid M, Ponomaryov T, Byk T, Nagler A, Ben-Hur H, Many A, Shultz L, Lider O, Alon R, Zipori D, Lapidot T. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 1999; 283: 845-848.
53. Piacibello W, Sanavio F, Severino A, Danc A, Gammaitoni L, Fagioli F, Perissinotto E, Cavalloni G, Kollet O, Lapidot T, Aglietta M. Engraftment in nonobese diabetic severe combined immunodeficient mice of human CD34+ cord blood cells after ex vivo expansion: evidence for the amplification and self-renewal of repopulating stem cells. Blood 1999; 11: 3736-3746.