Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Manuscript
  • Published:

Normal Hemopoiesis and Stemcellology

NOD/SCID repopulating cells but not LTC-IC are enriched in human CD34+ cells expressing the CCR1 chemokine receptor

Leukemia volume 15, pages 1092–1101 (2001)Cite this article

Abstract

Human haemopoietic stem and progenitor cells may be distinguished by the pattern of cell surface markers they display. The cells defined as ‘stem’ cells are heterogeneous and lack specific markers for their detection. However, they may be identified in in vitro assays such as the long-term culture initiating cell (LTC-IC) and in transplant assays involving immunosuppressed NOD/SCID mice. It is still not clear to what extent, if any, these cell populations overlap. The chemokine macrophage inflammatory protein-1α (MIP-1α) prolongs survival of LTC-IC in suspension cultures and we now show that in long-term bone marrow cultures (LTBMC) maintenance of haemopoiesis was significantly better from the CD34+ cells which possess MIP-1α receptors (P < 0.006). We examined one MIP-1α receptor, CCR1, which is present on CD34+ cells from haemopoietic tissues. In LTBMC the production of GM-CFC from CD34+CCR1−cells was significantly higher (P < 0.02) than that from CD34+CCR1+ cultures and the incidence of LTC-IC was 3- to 6-fold higher in the CD34+CCR1− cell fraction. In contrast, the cells responsible for high levels of engraftment in NOD/SCID mice were contained in the CD34+CCR1+ cell fraction. The CD34+CCR1+ cells engrafted to high levels in NOD/SCID and generated large numbers of progenitor cells. Therefore, we conclude that LTC-IC and SRC may be distinguished on the basis of expression of the chemokine receptor CCR1.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Similar content being viewed by others

References

  1. Sutherland H, Eaves C, Eaves A . Characterisation and partial purification of human marrow cells capable of initiating long-term hematopoiesis in vitro Blood 1989 74: 1563–1569

    CAS  PubMed  Google Scholar 

  2. 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 

  3. McNiece IK, Stewart FM, Deacon DM, Zsebo KM, Clark SC, Quesenberry PJ . Detection of human CFC with a high proliferative potential Blood 1989 74: 609–612

    CAS  PubMed  Google Scholar 

  4. Bradley TR, Hodgson GS . Detection of primitive macrophage progenitor cells in mouse bone marrow Blood 1979 54: 1446–1450

    CAS  PubMed  Google Scholar 

  5. Larochelle A, Vormoor J, Hanenberg H . Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: implications for gene therapy Nat Med 1996 2: 1329–1337

    Article  CAS  PubMed  Google Scholar 

  6. Kamel-Reid S, Dick JE . Engraftment of immune-deficient mice with human hematopoietic stem cells Science 1988 242: 1706–1709

    Article  CAS  PubMed  Google Scholar 

  7. Ploemacher RE, van der Sluijs JP, van Beurden AJ, 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

    CAS  PubMed  Google Scholar 

  8. 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: 9836–9841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wang JCY, Doedens M, Dick JE . Primitive human hematopoietic cells are enriched in cord blood compared with adult bone marrow or mobilised peripheral blood as measured by the quantitative in vivo SCID-repopulating cell assay Blood 1997 89: 3919–3924

    CAS  PubMed  Google Scholar 

  10. 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 

  11. Broxmeyer HE, Sherry B, Lu L, Cooper S, Oh K-O, Tekamp-Olson P, Kwon BS, Cerami A . Enhancing and suppressing effects of recombinant murine macrophage inflammatory proteins on colony formation in vitro by bone marrow myeloid progenitor cells Blood 1990 76: 1110–1116

    CAS  PubMed  Google Scholar 

  12. Bonnet D, Lemoine FM, Najman A, Guigon M . Comparison of the inhibitory effect of ACSDKP, TNF-α, TGF-β, and MIP-1α on marrow purified CD34+ progenitors Exp Hematol 1995 23: 551–556

    CAS  PubMed  Google Scholar 

  13. Clements JM, Craig S, Gearing AJ, Hunter MG, Heyworth CM, Dexter TM, Lord, BI . Biological and structural properties of MIP-1 alpha expressed in yeast Cytokine 1992 4: 76–82

    Article  CAS  PubMed  Google Scholar 

  14. Cooper S, Mantel C, Broxmeyer HE . Myelosuppressive effects in vivo with very low dosages of monomeric recombinant murine macrophage inflammatory protein-1 alpha Exp Hematol 1994 22: 186–193

    CAS  PubMed  Google Scholar 

  15. Dunlop DJ, Wright EG, Lorimore S, Graham GJ, Holyoake T, Kerr DJ, Wolpe SD, Pragnell IB . Demonstration of stem cell inhibition and myeloprotective effects of SCI/rhMIP1 alpha in vivo Blood 1992 79: 2221–2225

    CAS  PubMed  Google Scholar 

  16. Graham GJ, Wright EG, Hewick R, Wolpe SD, Wilkie NM, Donaldson D, Lorimore, S, Pragnell, IB . Identification and characterization of an inhibitor of haemopoietic stem cell proliferation Nature 1990 344: 442–444

    Article  CAS  PubMed  Google Scholar 

  17. Lord BI, Dexter TM, Clements JM, Hunter MA, Gearing AJ . Macrophage-inflammatory protein protects multipotent hematopoietic cells from the cytotoxic effects of hydroxyurea in vivo Blood 1992 79: 2605–2609

    CAS  PubMed  Google Scholar 

  18. Verfaillie CM, Catanzarro PM, Li WN . Macrophage Inflammatory protein 1α, interleukin 3 and diffusible marrow stromal factors maintain human hematopoietic stem cells for at least eight weeks in vitro J Exp Med 1994 179: 643–649

    Article  CAS  PubMed  Google Scholar 

  19. Verfaillie CM, Miller JS . CD34+/CD33− cells reselected from macrophage inflammatroy protein 1α + interleukin 3-supplemented ‘stroma-noncontact’ cultures are highly enriched for long-term bone marrow culture initiating cells Blood 1994 84: 1442–1449

    CAS  PubMed  Google Scholar 

  20. Gupta P, Oegema TH Jr, Brazil JJ, Dudek AZ, Slungaard A, Verfaillie CM . Human LTC-IC can be maintained for at least 5 weeks in vitro when interleukin-3 and a single chemokine are combined with O-sulphated heparan sulfates: requirement for optimal binding interactions of heparan sulfate with early-acting cytokines and matrix proteins Blood 2000 95: 147–155

    CAS  PubMed  Google Scholar 

  21. Miller JS, McCullar V, Verfaillie CM . Ex vivo culture of CD34+/Lin−/DR− cells in stroma-derived soluble factors, interleukin-3, and macrophage inflammatory protein-1alpha maintains not only myeloid but also lymphoid progenitors in a novel switch culture assay Blood 1998 91: 4516–4522

    CAS  PubMed  Google Scholar 

  22. Cashman JD, Eaves AC, Wolpe S, Eaves CJ . Regulatory activity of endogenous MIP-1α in long-term culture of human marrow Prog Clin Biol Res 1994 389: 261–268

    CAS  PubMed  Google Scholar 

  23. Otsuka T, Eaves CJ, Humphries RK, Hogge DE, Eaves AC . Lack of evidence for abnormal autocrine or paracrine mechanisms underlying the uncontrolled proliferation of primitive chronic myeloid leukemia progenitor cells Leukemia 1991 5: 861–868

    CAS  PubMed  Google Scholar 

  24. Lu L, Xiao M, Grigsby S, Wang WX, Wu B, Shen R-N, Broxmeyer HE . Comparative effects of suppressive cytokines on isolated single CD34+++ stem/progenitor cells from human bone marrow and umbilical cord blood plated with and without serum Exp Hematol 1993 21: 1442–1446

    CAS  PubMed  Google Scholar 

  25. Keller JR, Bartelmez SH, Sitnicka E, Ruscetti FW, Ortiz M, Gooya JM, Jacobsen, SE . Distinct and overlapping direct effects of macrophage inflammatory protein-1α and transforming growth factor β on hematopoietic progenitor/stem cell growth Blood 1994 84: 2175–2181

    CAS  PubMed  Google Scholar 

  26. Avalos BR, Bartynski KJ, Elder PJ, Kotur MS, Burton WG, Wilkie NM . The active monomeric form of macrophage inflammatory protein-1 alpha interacts with high- and low-affinity classes of receptors on human hematopoietic cells Blood 1994 84: 1790–1801

    CAS  PubMed  Google Scholar 

  27. Chasty RC, Lucas GS, Owen Lynch PJ, Pierce A, Whetton AD . Macrophage inflammatory protein-1 alpha receptors are present on cells enriched for CD34 expression from patients with chronic myeloid leukemia Blood 1995 86: 4270–4277

    CAS  PubMed  Google Scholar 

  28. de Wynter EA, Durig J, Cross MA, Heyworth CM, Testa NG . Differential response of CD34+ cells isolated from cord blood and bone marrow to MIP-1α and the expression of MIP-1α receptors on these immature cells Stem Cells 1998 16: 349–356

    Article  CAS  PubMed  Google Scholar 

  29. Durig J, de Wynter EA, Kasper C, Cross MA, Chang J, Testa NG, Heyworth CM . Expression of macrophage inflammatory protein-1α receptors in human CD34+ hematopoietic cells and their modulation by tumor necrosis factor-α and interferon-γ Blood 1998 92: 3073–3081

    CAS  PubMed  Google Scholar 

  30. Pease JE, Wang G, Ponath PD, Murphy PM . The N-terminal extracellular segments of the chemokine receptors CCR1 and CCR3 are determinants for MIP-1 alpha and eotaxin binding, respectively, but a second domain is essential for efficient receptor activation J Biol Chem 1998 273: 19972–19976

    Article  CAS  PubMed  Google Scholar 

  31. Imai T, Baba M, Nishimura M, Kakizaki M, Takagi S, Yoshie O . The T cell directed CC chemokine TARC is a highly specific biological ligand for CC chemokine receptor 4 J Biol Chem 1997 272: 15036–15042

    Article  CAS  PubMed  Google Scholar 

  32. Su S, Mukaida N, Wang J, Zhang Y, Takami A, Nakao S, Matsushima K . Inhibition of immature erythroid progenitor cell proliferation by macrophage inflammatory protein-1alpha by interacting mainly with a C-C chemokine receptor, CCR1 Blood 1997 90: 605–611

    CAS  PubMed  Google Scholar 

  33. Su SB, Mukaida N, Wang J, Nomura H, Matsushima K . Preparation of specific polyclonal antibodies to a C-C chemokine receptor, CCR1, and determination of CCR1 expression on various types of leukocytes J Leuk Biol 1996 60: 658–666

    Article  CAS  Google Scholar 

  34. Coutinho LH, Gilleece MH, de Wynter EA, Will A, Testa NG . Clonal and long-term cultures using human bone marrow. In: Testa NG, Molineux G (eds) Haemopoiesis: A Practical Approach Oxford University Press: Oxford 1993 pp 75–106

    Google Scholar 

  35. Weaver A, Ryder D, Crowther D, Dexter TM, Testa NG . Increased numbers of long-term culture initiating cells in the apheresis product of patients randomised to receive increasing doses of stem cell factor administered in combination with chemotherapy and a standard dose of granulocyte colony-stimulating factor Blood 1996 88: 3323–3328

    CAS  PubMed  Google Scholar 

  36. Weaver A, Ryder WD, Testa NG . Measurement of long-term culture initiating cells (LTC-ICs) using limiting dilution: comparison of endpoints and stromal support Exp Hematol 1997 25: 1333–1338

    CAS  PubMed  Google Scholar 

  37. de Wynter EA, Buck D, Hart C, Heywood R, Coutinho LH, Clayton A, Rafferty JA, Burt D, Guenechea G, Bueren JA, Gagen D, Fairbairn LJ, Lord BI, 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 Stem Cells 1998 16: 387–396

    Article  CAS  PubMed  Google Scholar 

  38. Durig J, Testa NG, Lord BI, Kasper C, Chang J, Telford N, Dexter TM, Heyworth CM . Characterization of the differential response of normal and CML haemopoietic progenitor cells to macrophage inflammatory protein-1α Leukemia 1999 13: 2012–2022

    Article  CAS  PubMed  Google Scholar 

  39. de Wynter EA, Heyworth CM, Chang J, Mukaida N, Matsushima K, Testa NG . Expression of MIP-1α receptors on primitive haemopoietic cells Exp Hematol 1999 27: 99

    Article  Google Scholar 

  40. Pettengell R, Luft T, Henschler R, Hows JM, Dexter TM, Ryder D, Testa NG . 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

    CAS  PubMed  Google Scholar 

  41. Lapidot T, Pflumio F, Doedens M, Murdoch B, Williams DE, Dick JE . Cytokine stimulation of multi lineage hematopoiesis from immature human cells engrafted in SCID mice Science 1992 255: 1137–1141

    Article  CAS  PubMed  Google Scholar 

  42. Cashman JD, Lapidot T, Wang JC, Doedens M, Shultz LD, Lansdorp P, Dick JE, Eaves CJ . 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

    CAS  PubMed  Google Scholar 

  43. Sutherland HJ, Eaves CJ, Lansdorp PM, Thacker JD, Hogge DE . Differential regulation of primitive human hematopoietic cells in long-term cultures maintained on genetically engineered murine stromal cells Blood 1991 78: 666–672

    CAS  PubMed  Google Scholar 

  44. Udomsakdi C, Lansdorp PM, Hogge DE, Reid DS, Eaves AC, Eaves CJ . Characterization of primitive hematopoietic cells in normal human peripheral blood Blood 1992 80: 2513–2521

    CAS  PubMed  Google Scholar 

  45. Verfaillie CM, Miller JS . A novel single-cell proliferation assay shows that long-term culture initiating cell (LTC-IC) maintenance over time results from the extensive proliferation of a small fraction of LTC-IC Blood 1995 86: 2137–2145

    CAS  PubMed  Google Scholar 

  46. de Wynter EA, Nadali G, Coutinho LH, Testa NG . Extensive amplification of single cells from CD34+ subpopulations in umbilical cord blood and identification of long-term culture-initiating cells present in two subsets Stem Cells 1996 14: 566–576

    Article  CAS  PubMed  Google Scholar 

  47. Hao QL, Shah AJ, Thiemann FT, Smogorzewska EM, Crooks GM . A functional comparison of CD34+CD38− cells in cord blood and bone marrow Blood 1995 86: 3745–3753

    CAS  PubMed  Google Scholar 

  48. Hao QL, Smogorzewska EM, Barsky LW, Crooks GM . In vitro identification of single CD34+CD38− cells with both lymphoid and myeloid potential Blood 1998 91: 4145–4151

    CAS  PubMed  Google Scholar 

  49. Miller JS, McCullar V, Punzel M, Lemischka IR, Moore KA . Single adult human CD34(+)/Lin−/CD38(−) progenitors give rise to natural killer cells, B-lineage cells, dendritic cells, and myeloid cells Blood 1999 93: 96–106

    CAS  PubMed  Google Scholar 

  50. Punzel M, Moore KA, Lemischka IR, Verfaillie CM . The type of stromal feeder used in limiting dilution assays influences frequency and maintenance assessment of human long-term culture initiating cells Leukemia 1999 13: 92–97

    Article  CAS  PubMed  Google Scholar 

  51. Sakabe H, Yahata N, Kimura T, Zeng ZZ, Minamiguchi H, Kaneko H, Mori KJ, Ohyashiki K, Ohyashiki JH, Toyama K, Abe T, Sonoda Y . Human cord blood-derived primitive progenitors are enriched in CD34+c-kit− cells: correlation between long-term culture-initiating cells and telomerase expression Leukemia 1998 12: 728–734

    Article  CAS  PubMed  Google Scholar 

  52. Chang J, Geary CG, Testa NG . Long-term bone marrow damage after chemotherapy for acute myeloid leukaemia does not improve with time Br J Haematol 1990 75: 68–72

    Article  CAS  PubMed  Google Scholar 

  53. Alkhatib G, Combadiere C, Broder CC, Feng Y, Kennedy PE, Murphy PM, Berger EA . CC CKR5: a RANTES, MIP-1 alpha, MIP-1 beta receptor as a fusion cofactor for macrophage-tropic HIV-1 Science 1996 272: 1955–1958

    Article  CAS  PubMed  Google Scholar 

  54. Choe H, Farzan M, Sun Y, Sullivan N, Rollins B, Ponath PD, Wu L, Mackay CR, LaRosa G, Newman W, Gerard N, Gerard C, Sodroski J . The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates Cell 1996 85: 1135–1148

    Article  CAS  PubMed  Google Scholar 

  55. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, Di-Marzio P, Marmon S, Sutton RE, Hill CM, Davis CB, Peiper SC, Schall TJ, Littman DR, Landau NR . Identification of a major co-receptor for primary isolates of HIV-1 Nature 1996 381: 661–666

    Article  CAS  PubMed  Google Scholar 

  56. Doranz BJ, Rucker J, Yi Y, Smyth RJ, Samson M, Peiper SC, Parmentier M, Collman RG, Doms RW . A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3 and CKR-2b as fusion cofactors Cell 1996 85: 1149–1158

    Article  CAS  PubMed  Google Scholar 

  57. Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, Nagashima KA, Cayanan C, Maddon PJ, Koup RA, Moore JP, Paxton WA . HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5 Nature 1996 381: 667–673

    Article  CAS  PubMed  Google Scholar 

  58. Deichmann M, Kronenwett R, Hass R . Expression of the human immunodeficiency virus type-1 coreceptors CXCR-4 (fusin, LESTR) and CKR-5 in CD34+ hematopoietic progenitor cells Blood 1997 89: 3522–3528

    CAS  PubMed  Google Scholar 

  59. Liu R, Paxton WA, Choe S, Ceradini D, Martin SR, Horuk R, MacDonald ME, Stuhlmann H, Koup RA, Landau NR . Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection Cell 1996 86: 367–377

    Article  CAS  PubMed  Google Scholar 

  60. Rana S, Besson G, Cook DG, Rucker J, Smyth RJ, Yi Y, Turner JD, Guo HH, Du JG, Peiper SC, Lavi E, Samson M, Libert F, Liesnard C, Vassart G, Doms RW, Parmentier M, Collman RG . Role of CCR5 in infection of primary macrophages and lymphocytes by M-tropic strains of HIV: resistance to patient-derived and prototype isolates resulting from the Δccr5 mutation J Virol 1997 71: 3219–3227

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, Farber CM, Saragosti S, Lapoumeroulie C, Cognaux J, Forceille C, Muyldermans G, Verhofstede C, Burtonboy G, Georges M, Imai T, Rana S, Yi Y, Smyth RJ, Collman RG, Doms RW, Vassart G, Parmentier M . Resistance to HIV-1 infection of Caucasian individuals bearing mutant alleles of the CCR5 chemokine receptor gene Nature 1996 382: 722–725

    Article  CAS  PubMed  Google Scholar 

  62. 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

    Article  CAS  PubMed  Google Scholar 

  63. Graham GJ, Wilkinson PC, Nibbs RJ, Lowe S, Kolset SO, Parker A, Freshney MG, Tsang ML, Pragnell IB . Uncoupling of stem cell inhibition from monocyte chemoattraction in MIP-1 alpha by mutagenesis of the proteoglycan binding site EMBO J 1996 15: 6506–6515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Colantonio L, Iellem A, Clissi B, Pardi R, Rogge L, Sinigaglia F, D'Ambrosio D . Upregulation of integrin α6/β1 and chemokine receptor CCR1 by interleukin-12 promotes the migration of human type 1 helper T cells Blood 1999 94: 2981–2989

    CAS  PubMed  Google Scholar 

  65. Gao JL, Wynn TA, Chang Y, Lee EJ, Broxmeyer HE, Cooper S, Tiffany HL, Westphal H, Kwon-Chung J, Murphy PM . Impaired host defense, hematopoiesis, granulomatous inflammation and type 1-type 2 cytokine balance in mice lacking CC chemokine receptor 1 J Exp Med 1997 185: 1959–1968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Van Hennick PB, de Koning A, Ploemacher RE . Seeding efficiency of primitive human hematopoietic cells in nonobese diabetic/severe combined immune deficiency mice: implications for stem cell frequency assessment Blood 1999 94: 3055–3061

    Google Scholar 

Download references

Acknowledgements

This work was supported by the Cancer Research Campaign and the authors would like to thank Jeff Barry and Mike Hughes for flow cytometry; Clare Hart and Dorothy Gagen for excellent technical assistance.

Author information

Authors and Affiliations

  1. CRC Experimental Haematology Group, Paterson Institute for Cancer Research, Manchester, UK

    EA de Wynter, CM Heyworth & NG Testa

  2. Department of Molecular Oncology, Cancer Research Institute, Kanazawa University, Japan

    N Mukaida

  3. Department of Molecular Preventive Medicine and CREST, School of Medicine, The University of Tokyo, Japan

    K Matsushima

Authors
  1. EA de Wynter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. CM Heyworth
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N Mukaida
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K Matsushima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. NG Testa
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Wynter, E., Heyworth, C., Mukaida, N. et al. NOD/SCID repopulating cells but not LTC-IC are enriched in human CD34+ cells expressing the CCR1 chemokine receptor. Leukemia 15, 1092–1101 (2001). https://doi.org/10.1038/sj.leu.2402146

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.leu.2402146

Keywords

Search

Advanced search

Quick links