nature.com

CD34+ or CD34−: which is the more primitive? - Leukemia

  • ️Guo, Y
  • ️Fri Aug 30 2002

  • Civin CI, Strauss LC, Brovall C, Fackler MJ, Schwartz JF, Shaper JH . Antigenic analysis of hematopoiesis III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody against KG-1a cells J Immunol 1985 133: 157–164

    Google Scholar 

  • Andrews RE, Singer JW, Bernstein ID . Precursors of colony-forming cells in humans can be distinguished from colony-forming cells by expression of CD33 and CD34 antigen and light scatter J Exp Med 1989 169: 1721–1731

    Article  CAS  PubMed  Google Scholar 

  • Krause DS, Fackler MJ, Civin CI, May WS . CD34: structure, biology, and clinical utility Blood 1996 87: 1–13

    Article  CAS  PubMed  Google Scholar 

  • Sutherland HJ, Eaves CJ, Eaves AC, Dragowska W, Lansdorp PM . Characterization and partial purification of human marrow cells capable of initiating long-term hematopoiesis in vitro Blood 1989 74: 1563–1570

    Article  CAS  PubMed  Google Scholar 

  • Bhatia M, Wang JC, Kapp U, Bonnet D, Dick JE . Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice Proc Natl Acad Sci USA 1997 94: 5320–5325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orlic D, Bodine D . What defines a pluripotent hematopoietic stem cell (PHSC): will the real PHSC please stand up! Blood 1994 84: 3991–3994

    Article  CAS  PubMed  Google Scholar 

  • Spangrude GJ, Heimfeld S, Weissman IL . Purification and characterization of mouse hematopoietic stem cells Science 1988 241: 58–62

    Article  CAS  PubMed  Google Scholar 

  • Uchida N, Weissman IL . Searching for hematopoietic stem cells: evidence that Thy-1.1lo Lin− Sca-1+ cells are the only stem cells in C57BL/Ka-Thy-1.1 bone marrow J Exp Med 1992 175: 175–184

    Article  CAS  PubMed  Google Scholar 

  • Okada S, Nakachi H, Nagayoshi K, Nagayishi K, Nishikawa S, Miura Y, Suda T . In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells Blood 1992 80: 3044–3050

    Article  CAS  PubMed  Google Scholar 

  • Ikuta K, Weissman IL . Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation Proc Natl Acad Sci USA 1992 89: 1502–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szilvassy SJ, Lansdorp PM, Humphries RK, Eaves AC, Eaves CJ . Isolation in a single step of highly enriched murine hematopoietic stem cell population with competitive long-term repopulating ability Blood 1989 74: 930–939

    Article  CAS  PubMed  Google Scholar 

  • Morel F, Szilvassy SJ, Travis M, Chen B, Galy A . Primitive hematopoietic cells in murine bone marrow express the CD34 antigen Blood 1996 88: 3774–3784

    Article  CAS  PubMed  Google Scholar 

  • Krause DS, Ito T, Fackler MJ, Smith OM, Collector MI, Sharkis SJ, May WS . Characterization of murine CD34, a marker for hematopoietic progenitor and stem cells Blood 1994 84: 691–901

    Article  CAS  PubMed  Google Scholar 

  • Gallacher L, Murdoch B, Wu DM, Karanu FN, Keeney M, Bhatia M . Isolation and characterization of human CD34(−)Lin(−) and CD34(+)Lin(−) hematopoietic stem cells using cell surface markers AC133 and CD7 Blood 2000 95: 2813–2820

    Article  CAS  PubMed  Google Scholar 

  • Civin CI, Almeida-Porada G, Lee MJ, Olweus J, Terstappen LWMM . Sustained, retransplantable, multilineage engraftment of highly purified adult human bone marrow stem cells in vivo Blood 1996 88: 4102–4109

    Article  CAS  PubMed  Google Scholar 

  • Link H, Arseniev L, BΩhre O, Kadar JG, Diedrich H, Poliwoda H . Transplantation of allogeneic CD34+ blood cells Blood 1996 87: 4903–4909

    Article  CAS  PubMed  Google Scholar 

  • Urbano-Ispizua A, Rozman C, Martinaez C, Marin P, Briones J, Rovira M, Feliz P, Viguria MC, Merino A, Sierra J, Mazzara R, Caaeras E, Montserrat E . Rapid engraftment without significant graft-versus-host disease after allogeneic transplantation of CD34+ selected cells from peripheral blood Blood 1997 89: 3967–3973

    Article  CAS  PubMed  Google Scholar 

  • Engelhardt M, Bertz H, Afting M, Waller CF, Finke J . High- versus standard-dose filgrastim (rhG-CSF) for mobilization of peripheral-blood progenitor cells from allogeneic donors and CD34+ immunoselection J Clin Oncol 1999 17: 2160–2172

    Article  CAS  PubMed  Google Scholar 

  • Engelhardt M, Bertz H, WΩsch R, Finke J . Analysis of stem cell apheresis products using intermediate-dose filgrastim plus large volume apheresis for allogeneic transplantation Ann Hematol 2001 80: 201–208

    Article  CAS  PubMed  Google Scholar 

  • Engelhardt M, Douville J, Behringer D, Jähne A, Smith A, Henschler R, Lange W . Hematopoietic recovery of ex vivo perfusion culture expanded bone marrow and unexpanded peripheral blood progenitors after myeloablative chemotherapy Bone Marrow Transplant 2001 27: 249–259

    Article  CAS  PubMed  Google Scholar 

  • Baum CM, Weissman IL, Tsukamoto AS, Buckle AM, Peault B . Isolation of a candidate human hematopoietic stem-cell population Proc Natl Acad Sci USA 1992 89: 2804–2808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berardi AC, Wang A, Levine JD, Lopez P, Scadden DT . Functional isolation and characterization of human hematopoietic stem cells Science 1995 267: 104–108

    Article  CAS  PubMed  Google Scholar 

  • Petzer AL, Hogge DE, Lansdorp PM, Reid DS, Eaves CJ . Self-renewal of primitive human hematopoietic cells (long-term-culture-initiating cells) in vitro and their expansion in define medium Proc Natl Acad Sci USA 1996 93: 1470–1474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Civin CI, Trischmann T, Kadan NS, Davis J, Noga S, Cohen K, Duffy B, Gronewegen I, Wiley J, Law P, Hardwick A, Oldham F, Gee A . Highly purified CD34-positive cells reconstitute hematopoiesis J Clin Oncol 1996 14: 2224–2233

    Article  CAS  PubMed  Google Scholar 

  • Larochelle A, Vormoor J, Hanenberg H, Wang JC, Bhatia M, Lapidot T, Murdoch B, Xiao XL, Kato I, Williams DA, Dick JE . Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: implication for gene therapy Nat Med 1996 2: 1329–1337

    Article  CAS  PubMed  Google Scholar 

  • Ploemacher RE, Brons NHC . Separation of CFU-S from primitive cells responsible for reconstitution of the bone marrow hemopoietic stem cell compartment following irradiation: evidence for a pre-CFU-S cell Exp Hematol 1989 17: 263–266

    CAS  PubMed  Google Scholar 

  • Testa NG, Molineux G . Haematopoiesis. A Practical Approach IRL Press at Oxford University Press: Oxford 1993

    Google Scholar 

  • Ploemacher RE, Brons NHC . Cells with marrow and spleen repopulating ability, and cells forming spleen colonies on day 16, 12 and 8 are sequentially ordered on the basis of increasing Rhodamine 123 retention J Cell Physiol 1988 136: 531–536

    Article  CAS  PubMed  Google Scholar 

  • Ploemacher RE, Van der Sluijs JP, Van Beurden CAJ, Baert MRM, Chan PL . Use of limiting dilution type long-term marrow cultures in frequency analysis of marrow-repopulating and spleen colony-forming hematopoietic stem cells in the mouse Blood 1991 78: 2527–2533

    Article  CAS  PubMed  Google Scholar 

  • Breems DA, Blokland EAW, 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

    CAS  PubMed  Google Scholar 

  • Sutherland HJ, Lansdorp PM, Henkelman DH, Eaves AC, Eaves CJ . Functional characterization of individual human hematopoietic stem cells cultured at limiting dilution on supportive marrow stromal layers Proc Natl Acad Sci USA 1990 87: 3584–3588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srour EF, Zanjani ED, Cornetta K, Traycoff CM, Flake AW, Hendrick M, Brandt JE, Leemhuis T, Hoffman R . Persistence of human multilineage, self-renewing lymphohematopoietic stem cells in chimeric sheep Blood 1993 82: 3333–3339

    Article  CAS  PubMed  Google Scholar 

  • Dick JE . Normal and leukemic human stem cells assayed in SCID mice Semin Immunol 1996 8: 197–206

    Article  CAS  PubMed  Google Scholar 

  • Glimm H, Eisterer W, Lee K, Cashman J, Holyoake TL, Nicolini F, Shultz LD, von Kalle C, Eaves CJ . Previously undetected human hematopoietic cell populations with short-term repopulating activity selectively engraft NOD/SCI-β2 microglobulin-null mice J Clin Invest 2001 107: 199–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holyoake TL, Nicolini FE, Eaves CJ . Functional differences between transplantable human hematopoietic stem cells from fetal liver, cord blood, and adult marrow Exp Hematol 1999 27: 1418–1427

    Article  CAS  PubMed  Google Scholar 

  • Bhatia M, Bonnet D, Murdoch B, Gan OL, Dick JE . A newly discovered class of human hematopoietic cells with SCID-repopulating activity Nat Med 1998 4: 1038–1045

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Ando K, Chargui J, Kawada H, Sato T, Tsuji T, Hotta T, Kato S . Ex vivo generation of CD34+ cells from CD34− hematopoietic cells Blood 1999 94: 4053–4059

    Article  CAS  PubMed  Google Scholar 

  • Zanjani ED, Almeide-Porada G, Livingston AG, Flake AW, Ogawa M . Human bone marrow CD34− cells engraft in vivo and undergo multilineage expression that includes giving rise to CD34+ cells Exp Hematol 1998 26: 353–360

    CAS  PubMed  Google Scholar 

  • Till JE, McCulloch EA . A direct measurement of the radiation sensitivity of normal mouse bone marrow cells Radiat Res 1961 14: 213–222

    Article  CAS  PubMed  Google Scholar 

  • Berenson RJ, Andrews RG, Bensinger WI, Kalamasz DF, Knitter G, Buckner CD, Bernstein ID . Antigen CD34+ marrow cells engraft lethally irradiated baboons J Clin Invest 1988 81: 951–955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Donnelly DS, Zelterman D, Sharkis S, Krause DS . Functional activity of murine CD34+ and CD34− hematopoietic stem cell populations Exp Hematol 1999 27: 788–792

    Article  CAS  PubMed  Google Scholar 

  • DiGiusto D, Chen S, Combbs J, Webb S, Namikawa R, Tsukamoto A, Chen BP, Galy AHM . Human fetal bone marrow early progenitor for T, B and myeloid cells are found exclusively in the population expression high levels of CD34 Blood 1994 84: 421–432

    Article  CAS  PubMed  Google Scholar 

  • Cashman JD, Lapidot T, Wang JCY, Doedens M, Schultz, Lansdorp P, Dick JE, Eaves C . Kinetic evidence of the regeneration of multilineage hematopoiesis from primitive cells in normal human bone marrow transplanted into immunodeficient mice Blood 1997 89: 4307–4316

    Article  CAS  PubMed  Google Scholar 

  • Hogan CJ, Shpall EJ, McNulty O, McNiece I, Dick JE, Schultz LD, Keller G . Engraftment and development of human CD34+-enriched cells from umbilical cord blood in NOD/LtSz-scid mice Blood 1997 90: 85–96

    Article  CAS  PubMed  Google Scholar 

  • Kawashima I, Zanjani E, Almaida-Porado G, Flake A, Zeng H, Ogawa M . CD34+ human marrow cells that express low levels of Kit protein are enriched for long-term marrow-engrafting cells Blood 1996 87: 4136–4142

    Article  CAS  PubMed  Google Scholar 

  • Srour E, Brandt J, Briddell R, Grigsby S, Leemhuis T, Hoffman R . Long-term generation and expression of human primitive hematopoietic progenitor cells in vitro Blood 1993 81: 661–669

    Article  CAS  PubMed  Google Scholar 

  • Sutherland D, Yeo E, Stewart A, Nayar R, DiGiusto R, Zanjani E, Hoffman R, Murray L . Identification of CD34+ subsets after glycoprotease selection: engraftment of CD34+Thy-1+Lin− stem cells in fetal sheep Exp Hematol 1996 24: 795–806

    CAS  PubMed  Google Scholar 

  • Gao Z, Fackler MJ, Leung W, Lumkul R, Ramirez M, Theobald N, Malech HL, Civin CI . Human CD34+ cell preparations contain over 100-fold greater NOD/SCID mouse engrafting capacity than do CD34− cell preparations Exp Hematol 2001 29: 910–921

    Article  CAS  PubMed  Google Scholar 

  • Goodell MA . CD34+ or CD34−: does it really matter? Blood 1999 15: 2545–2547

    Article  Google Scholar 

  • Ogawa M . Changing phenotypes of hematopoietic stem cells Exp Hematol 2002 30: 3–6

    Article  PubMed  Google Scholar 

  • Dao MA, Nolta JA . CD34: to select or not to select? That is the question Leukemia 2000 14: 773–776 (review)

    Article  CAS  PubMed  Google Scholar 

  • Andrews RG, Peterson LJ, Morris J, Potter J, Heyward S, Gough M, Bryant E, Kiem H . Differential engraftment of genetically modified CD34(+) and CD34(−) hematopoietic cell subsets in lethally irradiated baboons Exp Hematol 2000 28: 508–518

    Article  CAS  PubMed  Google Scholar 

  • Goodell MA, Brose K, Paradis G, Conner AS, Mulligan R . Isolation and function properties of murine hematopoietic stem cells that are replicating in vivo J Exp Med 1996 183: 1797–1806

    Article  CAS  PubMed  Google Scholar 

  • Goodell MA, Rosenzweig M, Kim H, Marks D, DeMaria MA, Paradis G, Grupp SA, Sieff CA, Mulligan R, Johnson RP . Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species Nat Med 1997 3: 1337–1345

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Follo M, Kaiser S, Geiger K, Kapp U, Lübbert M, Engelhardt M . Isolation of hematopoietic stem cells with efflux capacity from mice and human bone marrow, muscle tissue and various other cell sources Blood 2001 98 (Suppl.): 116b–4114

    Google Scholar 

  • Liu HJ, Verfaillie CM . Phenotypic and in vitro characterization of Hoechst 33342 side population in umbilical cord blood Blood 2000 96 (Suppl.): 664a

    Google Scholar 

  • Storms RW, Goodell MA, Fisher A, Mulligan R, Smith C . Hoechst dye efflux reveals a novel CD7+CD34− lymphoid progenitor in human umbilical cord blood Blood 2000 96: 2125–2133

    Article  CAS  PubMed  Google Scholar 

  • Pettengell R, Luft T, Henschler R, Hows JM, Dexter TM, Ryder D, Testa NK . Direct comparison by limiting dilution analysis of long-term culture-initiating cells in human bone marrow, umbilical cord blood, and blood stem cells Blood 1994 84: 3653–3659

    Article  CAS  PubMed  Google Scholar 

  • Uchida N, Fujisaki T, Eaves A, Eaves C . Transplantable hematopoietic stem cells in human fetal liver have a CD34+ side population (SP) phenotype J Clin Invest 2001 108: 1071–1077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osawa M, Hanada K, Hamada H, Nakachi H . Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cells Science 1996 273: 242–245

    Article  CAS  PubMed  Google Scholar 

  • Morel F, Galy A, Chen B, Szilvassy SJ . Equal distribution of competitive long-term repopulating stem cells in the CD34+ and CD34− fractions of Thy-1lowSca-1+ bone marrow cells Exp Hematol 1998 26: 440–448

    CAS  PubMed  Google Scholar 

  • Sato T, Laver JH, Ogawa M . Reversible expression of CD34 by murine hematopoietic stem cells Blood 1999 94: 2548–2554

    Article  CAS  PubMed  Google Scholar 

  • Tajima F, Sato T, Laver JH, Ogawa M . CD34 expression by murine hematopoietic stem cells mobilized by granulocyte colony-stimulating factor Blood 2000 96: 1989–1993

    Article  CAS  PubMed  Google Scholar 

  • Ando K, Nakamura Y, Chargui J, Matsuzawa H, Tsuji T, Kato S, Hotta T . Extensive generation of human cord blood CD34+ stem cells from Lin−CD34− cells in a long-term in vitro system Exp Hematol 2000 28: 690–699

    Article  CAS  PubMed  Google Scholar 

  • Summers YJ, Heyworth CM, De Wynter EA, Chang J, Testa NG . Cord blood G0 CD34+ cells have a thousand-fold higher capacity for generating progenitors in vitro than G1 CD34+ cells Stem Cells 2001 19: 505–513

    Article  CAS  PubMed  Google Scholar 

  • Tajima F, Deguchi T, Laver JH, Zeng H, Ogawa M . Reciprocal expression of CD38 and CD34 by adult murine hematopoietic stem cells Blood 2001 97: 2618–2624

    Article  CAS  PubMed  Google Scholar 

  • Ito T, Tajimi F, Ogawa M . Developmental changes of CD34 expression by murine hematopoietic stem cells Exp Hematol 2000 28: 1269–1273

    Article  CAS  PubMed  Google Scholar 

  • Dao MA, Nolta JA . Reversibility of CD34 expression on human stem cells that retain the capacity for secondary reconstitution Blood 2000 96 (Suppl): 581a

    Google Scholar 

  • Glimm H, Oh I-H, Eaves CJ . Human hematopoietic stem cells stimulated to proliferate in vitro lose engraftment potential during their S/G2/M transit and do not re-enter G0 Blood 2000 96: 4185–4193

    Article  CAS  PubMed  Google Scholar 

  • Verfaillie CM, Almaida-Porada G, Wissink S, Zanjani ED . Kinetics of engraftment of CD34− and CD34+ cells from mobilized blood differs from that of CD34− and CD34+ cells from bone marrow Exp Hematol 2000 28: 1071–1079

    Article  CAS  PubMed  Google Scholar 

  • Morrison SJ, Weissman IL . The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype Immunity 1994 1: 6611–6673

    Article  Google Scholar 

  • Magli MC, Iscove NN, Odartchenko N . Transient nature of early hematopoietic spleen colonies Nature 1982 295: 527–529

    Article  CAS  PubMed  Google Scholar 

  • Kondo M, Weissman IL, Akashi K . Identification of clonogenic common lymphoid progenitors in mouse bone marrow Cell 1997 91: 661–672

    Article  CAS  PubMed  Google Scholar 

  • Akashi K, Traver D, Miyamoto T, Weissmann IL . A clonogenic common myeloid progenitor that gives rise to all myeloid lineages Nature 2000 404: 193–197

    Article  CAS  PubMed  Google Scholar 

  • Eaves AC, Eaves CJ . Growth control in leukemia Prog Clin Biol Res 1990 354: 223–236

    Google Scholar 

  • Jackson KA, Mi T, Goodell MA . Hematopoietic potential of stem cells isolated from murine skeletal muscle Proc Natl Acad Sci USA 1999 96: 14482–14486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodell MA . Stem cells: is there a future in plastics? Curr Opin Cell Biol 2001 13: 662–665

    Article  CAS  PubMed  Google Scholar 

  • Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WWK, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pyeritz RE, Brenner MK . Transplantibility and therapeutic effects of bone marrow derived mesenchymal cells in children with osteogenesis imperfecta Nat Med 1999 5: 309–313

    Article  CAS  PubMed  Google Scholar 

  • Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS, Goff JP . Bone marrow as a potential source of hepatic oval cells Science 1999 284: 1168–1170

    Article  CAS  PubMed  Google Scholar 

  • Makino S, Fukuda K, Miyoshi S, Konishi F, Kodama H, Pan J, Sno M, Takahashi T, Hori S, Abe H, Hata J, Umezawa A, Ogawa S . Cardiomyocytes can be generated from bone marrow cells in vitro J Clin Invest 1999 103: 697–705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Brazelton TR, Rossi FM, Keshet GI, Blau HM . From marrow to brain: expression of neuronal phenotypes in adult mice Science 2000 290: 1775–1779

    Article  CAS  PubMed  Google Scholar 

  • Bjornson CRR, Rietze RL, Reynolds BA, Magli MC, Vescovi AL . Turning brain into blood: a hematopoietic fate adopted by adult neuronal stem cells in vivo Science 1999 283: 534–537

    Article  CAS  PubMed  Google Scholar