Functional and kinetic characterization of granulocyte colony-stimulating factor-primed CD34- human stem cells

British Journal of Haematology

Volumn 123, Issue 4, 2003, Pages 720-729

  Lemoli, Roberto M ^a,e   Bertolini, Francesco ^b   Petrucci, Maria T ^c   Gregorj, Chiara ^c   Ricciardi, Maria R ^c   Fogli, Miram ^a   Curti, Antonio ^a   Rabascio, Cristina ^b   Pandolfi, Simona ^a   Ferrari, Sergio ^d   Fo, Robin ^c   Baccarani, Michele ^a   Tafuri, Agostino ^c  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^e Ist Ematol/Oncol Medica L/A S   (Italy)

Author keywords

CD34; Cell cycle; Haematopoietic stem cells

Indexed keywords

BETA 2 MICROGLOBULIN; CD34 ANTIGEN; CYTOKINE; GRANULOCYTE COLONY STIMULATING FACTOR; PROTEIN P21; PROTEIN P27;

ANTIGEN EXPRESSION; ARTICLE; BLOOD CELL; CELL CULTURE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL FRACTIONATION; CELL FUNCTION; CELL ISOLATION; CELL KINETICS; CLONOGENESIS; CONTROLLED STUDY; DIABETES MELLITUS; DOWN REGULATION; GENE ACTIVATION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; INJECTION; LIQUID CULTURE; PRIORITY JOURNAL; STEM CELL; STROMA CELL;

ANIMALS; ANTIGENS, CD34; CELL CYCLE; CELL DIVISION; CELL SEPARATION; CELLS, CULTURED; GRANULOCYTE COLONY-STIMULATING FACTOR; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; INTEGRIN ALPHA4BETA1; INTEGRIN ALPHA5BETA1; MICE; MICE, INBRED NOD; MICE, SCID; RECEPTORS, CXCR4; TRANSPLANTATION, HETEROLOGOUS;

EID: 0344961113     PISSN: 00071048     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2141.2003.04673.x     Document Type: Article

References (41)

1. Andrews, R.G., Peterson, L.J., Morris, J., Potter, J., Heyward, S., Gough, M., Bryant, E. & Kiem, H.P. (2000) Differential engraftment of genetically modified CD34+ and CD34-hematopoietic cell subsets in lethally irradiated baboons. Experimental Hematology, 28, 508-518.
2. Bensinger, W.I., Buckner, C.D., Shannon-Dorcy, K., Rowley, S., Appelbaum, F.R., Benyunes, M., Clift, R., Martin, P., Demirer, T., Storb, R., Lee, M. & Schiller G. (1996) Transplantation of allogeneic CD34+ peripheral blood stem cells in patients with advanced hematologic malignancy. Blood, 88, 4132-4138.
3. Berenson, R.J., Andrews, R.G., Bensinger, W.I., Kalamasz, D., Knitter, G., Buckner, C.D. & Bernsrein, I.D. (1988) Antigen CD34+ marrow cells engraft lethally irradiated baboons. Journal of Clinical Investigation, 81, 951-955.
4. Bhatia, M., Bonnet, D., Murdoch, B., Gan, O.I. & Dick, J.E. (1998) A newly discovered class of human hematopoietic cells with SCID-repopulating activity. Nature Medicine, 9, 1038-1045.
5. Cheng, J., Baumhueter, S., Cacalano, G., Carver-Moore, K., Thibodeaux, H., Thomas, R., Broxmeyer, H.E., Cooper, S., Hague, N., Moore, M. & Lasky L.A. (1996) Hematopoietic defects in mice lacking the sialomucin CD34. Blood, 87, 479-484.
6. kip1. Nature Medicine, 6, 1235-1240.
7. kip1. Haematologica, 87, 373-380.
8. kip-1 coupled with transforming growth factor β neutralization induces cell-cycle entry and increases retroviral transduction of primitive human hematopoietic cells. Proceedings of the National Academy of Sciences of the United States of America, 95, 13 006-13 011.
9. Dao, M.A., Arevalo, J. & Nolta, J.A. (2003) Reversibility of CD34 expression on human hematopoietic stem cells that retain the capacity for secondary reconstitution. Blood, 101, 112-118.
10. Dell'Agnola, C., Rabascio, C., Mancuso, P., Capillo, M., Pruneri, G., Gobbi, A., Minucci, S., Ronzoni, S., Volorio, S., Calabrese, L., Tradati, N., Martinelli, G., Shultz, L. & Bertolini, F. (2002) In vitro and in vivo hematopoietic potential of human stem cells residing in muscle tissue. Experimental Hematology, 30, 905-914.
11. Dougherty, S. & Pluznik, D. (2002) Expression of the hematopoietic stem cell marker CD34 is related to the cell cycle status (Abstract). Experimental Hematology, 30(Suppl. 1), 57a.
12. Fujisaki, T., Berger, M.G., Rose-John, S. & Eaves, C.J. (1999) Rapid differentiation of a rare subset of adult human Lin-CD34-CD38-cells stimulated by multiple growth factors in vitro. Blood, 94, 1926-1932.
13. Gao, Z., Fackler, M.J., Leung, W., Lumkul, R., Ramirez, M., Theobald, N., Malech, H.L. & Civin, C.I. (2001) Human CD34+ cell preparations contain over 100-fold greater NOD/SCID mouse engrafting capacity than do CD34-cell preparations. Experimental Hematology, 29, 910-921.
14. Glimm. H.. Eisterer, W., Lee, K., Cashman, J.. Holyoake, T.L., Nicolini, F., Shultz, L.D., von Kalle, C. & Eaves. C.J. (2001) Previously undetected human hematopoietic cell populations with short-term repopulating activity selectively engraft NOD/SCID-beta2 microglobulin-null mice. Journal of Clinical Investigation, 107, 199-206.
15. Goodell, M.A., Rosenzweig, M., Kim, H., Marks, D.F., DeMaria, M., Paradis, G., Grupp, S.A., Sieff, C.A., Mulligan, R.C. & Johnson, R.P. (1997) Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nature Medicine, 3, 1337-1344.
16. Gothot, A., van der Loo, J.C. & Srour, E.F. (1998) Cell cycle-related changes in repopulating capacity of human mobilized peripheral blood CD34+ cells in non-obese diabetic/severe combined immune-deficient mice. Blood, 92, 2641-2649.
17. Hao, Q.L., Thiemann, F.T., Petersen, D., Smogorzewska, E.M. & Crooks, G.M. (1996) Extended long-term culture reveals a highly quiescent and primitive human hematopoietic progenitor population. Blood, 88, 3306-3313.
18. Hengst, L. & Reed, S. (1996) Translation control of p27 accumulation during the cell cycle. Science, 271, 1861-1864.
19. Huss, R., Gatsios, P., Graeve, L., Lange, C., Eissner, G., Kolb, H.J., Thalmeier, K. & Heinrich, P.C. (2000) Quiescence of CD34-negative hematopoietic stem cells is mediated by downregulation of cyclin B and no Stat activation. Cytokine, 12, 1195-1204.
20. Kollet, O., Peled, A., Byk, T., Ben-Hur, H., Greiner, D., Shultz, L. & Lapidot T. (2000) Beta2 microglobulin-deficient (B2m(null)) NOD/SCID mice are excellent recipients for studying human stem cell function. Blood, 95, 3102-3105.
21. Krause, D.S., Fackler, M.J., Civin, C.I. & May, W.S. (1996) CD34: structure, biology and clinical utility. Blood, 87, 1-13.
22. Lemoli, R.M., Tafuri, A., Fortuna, A., Petrucci, M.T., Ricciardi, M.R., Catani, L., Rondelli, D., Fogli, M., Leopardi, G., Ariola, C. & Tura S. (1997) Cycling status of CD 34+ cells mobilized into peripheral blood of healthy donors by recombinant human granulocyte colony-stimulating factor. Blood, 89, 1189-1196.
23. Lemoli, R.M., Martinelli, G., Zamagni, E., Motta, M.R., Rizzi, S., Terragna, C., Rondelli, R., Ronconi, S., Curti, A., Bonifazi, F., Tura, S. & Cavo, M. (2000) Engraftment, clinical, and molecular follow-up of patients with multiple myeloma who were reinfused with highly purified CD34+ cells to support single or tandem high-dose chemotherapy. Blood, 95, 2234-2239.
24. Nakamura, Y., Ando, K., Chargui, J., Sato, T., Tsuji, T., Hotta, T. & Kato, S. (1999) Ex vivo generation of CD34+ cells from CD34- hematopoietic cells. Blood, 94, 4053-4059.
25. Osawa, M., Kanada, K., Hamada, H. & Nakauchi, H. (1996) Long-term lymphohematopoietic reconstitution by a single Cd34-low/negative hematopoietic stem cell. Science, 273, 242-245.
26. Peled, A., Petit, L, 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. (1999) Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science, 283, 845-848.
27. + cells: role in transendhotelial/ stromal migration and engraftment of NOD/SCID mice. Blood, 95, 3289-3296.
28. Pierelli, L., Marone, M., Bonanno, G., Mozzetti, S., Rutella, S., Morosetti, R., Rumi, C., Mancuso, S., Leone, G. & Scambia, G. (2000) Modulation of bcl-2 and p27 in human primitive proliferating hematopoietic progenitors by autocrine TGF-β1 is a cell cycle-independent effect and influences their hematopoietic potential. Blood, 95, 3001-3010.
29. Quesenberry, P.J., Colvin, G.A. & Lambert, J.-F. (2002) The chiaroscuro stem cell: a unified stem cell theory. Blood, 100, 4266-4271.
30. Ricciardi, M.R., Petrucci, M.T., Gregorj, C., Ariola, C., Lemoli, R.M., Fogli, M., Mauro, F.R., Cerretti, R., Foa, R., Mandelli, F. & Tafuri A. (2001) Reduced susceptibility to apoptosis correlates with kinetic quiescence in disease progression of chronic lymphocytic leukemia. British Journal of Haematology, 113, 1-10.
31. Roberts, A.W. & Metcalf, D. (1995) Noncycling state of peripheral blood progenitor cells mobilized by granulocyte colony-stimulating factor and other cytokines. Blood, 86, 1600-1605.
32. Sato, T., Laver, J.H. & Ogawa, M. (1999) Reversible expression of CD34 by murine hematopoietic stem cells. Blood, 94, 2548-2554.
33. Shultz, L.D., Lang, P.A., Christianson, S.W., Gott, B., Lyons, B., Umeda, S., Leiter, E., Hesselton, R., Wagar, E.J., Leif, J.H., Kollet, O., Lapidot, T. & Greiner, D.L. (2000) NOD/LtSz-Rag1null mice: an immunodeficient and radioresistant model for engraftment of human hematolymphoid cells, HIV infection, and adoptive transfer of NOD mouse diabetogenic T cells. Journal of Immunology, 164, 2496-2507.
34. Tafuri, A., Lemoli, R.M., Petrucci, M.T., Ricciardi, M.R., Fogli, M., Bonsi, L., Ariola, C., Strippoli, P., Gregorj, C., Petti, M.C., Tura, S., Mandelli, F. & Bagnara, G.P. (1999) Thrombopoietin and interleukin-11 have different modulatory effects on cell cycle and programmed cell death in primary acute myeloid leukemia cells. Experimental Hematology, 27, 1255-1263.
35. Tafuri, A., Gregorj, C., Petrucci, M.T., Ricciardi, M.R., Mancini, M., Cimino, G., Mecucci, C., Tedeschi, A., Fioritoni, G., Ferrara, F., Di Raimondo, F., Gallo, E., Liso, V., Fabbiano, F., Cascavilla, N., Pizzolo, G., Camera, A., Pane, F., Lanza, F., Cilloni, D., Annino, L., Vitale, A., Vegna, M.L, Vignetti, M., Foa, R. & Mandelli, F for the GIMEMA Group. (2002) MDR1 protein expression is an independent predictor of complete remission in newly diagnosed adult acute lymphoblastic leukemia. Blood, 100, 974-981.
36. Tajima, F., Sato, T., Laver, J.H. & Ogawa, M. (2000) CD34 expression by murine hematopoietic stem cells mobilized by granulocyte colony-stimulating factor. Blood, 96, 1989-1993.
37. kip-1 Cyclin-dependent kinase inhibitors during human hematopoiesis. Blood, 93, 4167-4178.
38. Uchida, N., He, D., Friera, A.M., Reitsma, M., Sasaki, D., Chen, B. & Tsukamoto, A. (1997) The unexpected GO/G1 cell cycle status of mobilized hematopoietic stem cells from peripheral blood. Blood, 89, 465-472.
39. Verfaillie, C.M., Almeida-Porada, G., Wissink, S. & Zanjani, E.D. (2000) Kinetics of engraftment of CD34- and CD34+ cells from mobilized blood differs from that of CD34- and CD34+ cells from bone marrow. Experimental Hematology, 28, 1071-1079.
40. Zanjani, E.D., Almeida-Porada, G., Livingston, A.G., Flake, A.W. & Ogawa, M. (1998) Human bone marrow CD34- cells engraft in vivo and undergo multilineage expression that includes giving rise to CD34+ cells. Experimental Hematology, 26, 353-360.
41. Zanjani, E.D., Almeida-Porada, G., Livingston, A.G., Zeng, H.Q. & Ogawa, M. (2003) Reversible expression of CD34 by adult human bone marrow long-term engrafting hematopoietic stem cells. Experimental Hematology, 31, 406-412.