Heterogeneity in hematopoietic stem cell populations: Implications for transplantation

Current Opinion in Hematology

Volumn 20, Issue 4, 2013, Pages 257-264

  Miller, Paul H ^a   Knapp, David J H F ^a   Eaves, Connie J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Expansion; Hematopoietic; Heterogeneity; Stem cell; Transplantation

Indexed keywords

CELL HETEROGENEITY; CELL POPULATION; CELL RENEWAL; EX VIVO STUDY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; INOCULATION; NEUTROPHIL; PRIORITY JOURNAL; REVIEW;

CELL LINEAGE; CELL PROLIFERATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; SIGNAL TRANSDUCTION;

EID: 84880232664     PISSN: 10656251     EISSN: 15317048     Source Type: Journal    
DOI: 10.1097/MOH.0b013e328360aaf6     Document Type: Review

References (68)

1. Goldman JM, Gale RP, Horowitz MM, et al. Bone marrow transplantation for chronic myelogenous leukemia in chronic phase. Increased risk for relapse associated with T-cell depletion. Ann Intern Med 1988; 108:806-814.
2. Doulatov S, Notta F, Laurenti E, Dick JE. Hematopoiesis: a human perspective. Cell Stem Cell 2012; 10:120-136.
3. Lemischka IR. Clonal, in vivo behavior of the totipotent hematopoietic stem cell. Semin Immunol 1991; 3:349-355.
4. Bystrykh LV, Verovskaya E, Zwart E, et al. Counting stem cells: methodological constraints. Nat Methods 2012; 9:567-574.
5. Copley MR, Beer PA, Eaves CJ. Hematopoietic stem cell heterogeneity takes center stage. Cell Stem Cell 2012; 10:690-697.
6. Muller-Sieburg CE, Sieburg HB, Bernitz JM, Cattarossi G. Stem cell heterogeneity: implications for aging and regenerative medicine. Blood 2012; 119:3900-3907.
7. Yeager AM, Kaizer H, Santos GW, et al. Autologous bone marrow transplantation in patients with acute nonlymphocytic leukemia, using ex vivo marrow treatment with 4-hydroperoxycyclophosphamide. N Engl J Med 1986; 315:141-147.
8. Udomsakdi C, Lansdorp PM, Hogge DE, et al. Characterization of primitive hematopoietic cells in normal human peripheral blood. Blood 1992; 80:2513-2521.
9. Kamel-Reid S, Dick JE. Engraftment of immune-deficient mice with human hematopoietic stem cells. Science 2013; 242:1706-1709.
10. Shultz LD, Brehm MA, Garcia-Martinez JV, Greiner DL. Humanized mice for immune system investigation: progress, promise and challenges. Nat Rev Immunol 2012; 12:786-798.
11. Glimm H, Eisterer W, Lee K, et al. Previously undetected human hematopoietic cell populations with short-term repopulating activity selectively engraft NOD/SCID-beta2 microglobulin-null mice. J Clin Invest 2001; 107:199-206.
12. Cheung AM, Leung D, Rostamirad S, et al. Distinct but phenotypically heterogeneous human cell populations produce rapid recovery of platelets and neutrophils after transplantation. Blood 2012; 119:3431-3439.
13. Miller PH, Cheung AM, Beer PA, et al. Enhanced normal short-term human myelopoiesis in mice engineered to express human-specific myeloid growth factors. Blood 2013; 121:e1-e4.
14. Christ O, Lucke K, Imren S, et al. Improved purification of hematopoietic stem cells based on their elevated aldehyde dehydrogenase activity. Haematologica 2007; 92:1165-1172.
15. Hu Z, Yang YG. Full reconstitution of human platelets in humanized mice after macrophage depletion. Blood 2012; 120:1713-1716.
16. Anasetti C, Logan BR, Lee SJ, et al. Peripheral-blood stem cells versus bone marrow from unrelated donors. N Engl J Med 2012; 367:1487-1496.
17. Cavazzana-Calvo M, Payen E, Negre O, et al. Transfusion independence and HMGA2 activation after gene therapy of human beta-thalassaemia. Nature 2010; 467:318-322.
18. Payen E, Leboulch P. Advances in stem cell transplantation and gene therapy in the beta-hemoglobinopathies. Hematology Am Soc Hematol Educ Program 2012; 2012:276-283.
19. Adair JE, Beard BC, Trobridge GD, et al. Extended survival of glioblastoma patients after chemoprotective HSC gene therapy. Sci Transl Med 2012; 4:133ra57.
20. Kim HJ, Tisdale JF, Wu T, et al. Many multipotential gene-marked progenitor or stem cell clones contribute to hematopoiesis in nonhuman primates. Blood 2000; 96:1-8.
21. Glimm H, Schmidt M, Fischer M, et al. Efficient marking of human cells with rapid but transient repopulating activity in autografted recipients. Blood 2005; 106:893-898.
22. Wang GP, Berry CC, Malani N, et al. Dynamics of gene-modified progenitor cells analyzed by tracking retroviral integration sites in a human SCID-X1 gene therapy trial. Blood 2010; 115:4356-4366.
23. Mathioudakis G, Storb R, McSweeney PA, et al. Polyclonal hematopoiesis with variable telomere shortening in human long-term allogeneic marrow graft recipients. Blood 2000; 96:3991-3994.
24. Gluckman E, Ruggeri A, Volt F, et al. Milestones in umbilical cord blood transplantation. Br J Haematol 2011; 154:441-447.
25. Majeti R, Park CY, Weissman IL. Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood. Cell Stem Cell 2007; 1:635-645.
26. Notta F, Doulatov S, Laurenti E, et al. Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science 2011; 333:218-221.
27. Benveniste P, Frelin C, Janmohamed S, et al. Intermediate-term hematopoietic stem cells with extended but time-limited reconstitution potential. Cell Stem Cell 2010; 6:48-58.
28. Dykstra B, Kent D, Bowie M, et al. Long-term propagation of distinct hematopoietic differentiation programs in vivo. Cell Stem Cell 2007; 1:218-229.
29. Kent DG, Copley MR, Benz C, et al. Prospective isolation and molecular characterization of hematopoietic stem cells with durable self-renewal potential. Blood 2009; 113:6342-6350.
30. Benz C, Copley MR, Kent DG, et al. Hematopoietic stem cell subtypes expand differentially during development and display distinct lymphopoietic programs. Cell Stem Cell 2012; 10:273-283.
31. Morita Y, Ema H, Nakauchi H. Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment. J Exp Med 2010; 207:1173-1182.
32. Civin CI, Almeida-Porada G, Lee MJ, et al. Sustained, retransplantable, multilineage engraftment of highly purified adult human bone marrow stem cells in vivo. Blood 1996; 88:4102-4109.
33. Bowie MB, Kent DG, Dykstra B, et al. Identification of a new intrinsically timed developmental checkpoint that reprograms key hematopoietic stem cell properties. Proc Natl Acad Sci USA 2007; 104:5878-5882.
34. Dykstra B, Olthof S, Schreuder J, et al. Clonal analysis reveals multiple functional defects of aged murine hematopoietic stem cells. J Exp Med 2011; 208:2691-2703.
35. Pang WW,Price EA, Sahoo D, et al. Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age. Proc Natl Acad Sci USA 2011; 108:20012-20017.
36. Cavazzana-Calvo M, Fischer A, Bushman FD, et al. Is normal hematopoiesis maintained solely by long-term multipotent stem cells? Blood 2011; 117: 4420-4424.
37. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126:663-676.
38. Zon LI. Intrinsic and extrinsic control of haematopoietic stem-cell self-renewal. Nature 2008; 453:306-313.
39. Yuan J, Nguyen CK, Liu X, et al. Lin28b reprograms adult bone marrow hematopoietic progenitors to mediate fetal-like lymphopoiesis. Science 2012; 335:1195-1200.
40. Lechman ER, Gentner B, van Galen P, et al. Attenuation of miR-126 activity expands HSC in vivo without exhaustion. Cell Stem Cell 2012; 11:799-811
41. Ergen AV, Boles NC, Goodell MA. Rantes/Ccl5 influences hematopoietic stem cell subtypes and causes myeloid skewing. Blood 2012; 119:2500-2509.
42. Florian MC, Dorr K, Niebel A, et al. Cdc42 activity regulates hematopoietic stem cell aging and rejuvenation. Cell Stem Cell 2012; 10:520-530.
43. Ito K, Carracedo A, Weiss D, et al. A PML-PPAR-delta pathway for fatty acid oxidation regulates hematopoietic stem cell maintenance. Nat Med 2012; 18:1350-1358.
44. Huang J, Nguyen-McCarty M, Hexner EO, et al. Maintenance of hematopoietic stem cells through regulation of Wnt and mTOR pathways. Nat Med 2012; 18:1778-1785.
45. Wang J, Sun Q, Morita Y, et al. A differentiation checkpoint limits hematopoietic stem cell self-renewal in response to DNA damage. Cell 2012; 148:1001-1014.
46. Chen X, Skutt-Kakaria K, Davison J, et al. G9a/GLP-dependent histone H3K9me2 patterning during human hematopoietic stem cell lineage commitment. Genes Dev 2012; 26:2499-2511. This article presents new insights into epigenetic state changes that accompany the differentiation of human HSCs.
47. Gibbs KD Jr, Gilbert PM, Sachs K, et al. Single-cell phospho-specific flow cytometric analysis demonstrates biochemical and functional heterogeneity in human hematopoietic stem and progenitor compartments. Blood 2011; 117:4226-4233.
48. Sloma I, Imren S, Beer PA, et al. Ex vivo expansion of normal and chronic myeloid leukemic stem cells without functional alteration using a NUP98HOXA10homeodomain fusion gene. Leukemia 2013; 27:159-169.
49. Kent DG, Dykstra BJ, Cheyne J, et al. Steel factor coordinately regulates the molecular signature and biologic function of hematopoietic stem cells. Blood 2008; 112:560-567.
50. Dykstra B, Ramunas J, Kent D, et al. High-resolution video monitoring of hematopoietic stem cells cultured in single-cell arrays identifies new features of self-renewal. Proc Natl Acad Sci USA 2006; 103:8185-8190.
51. Lecault V, Vaninsberghe M, Sekulovic S, et al. High-throughput analysis of single hematopoietic stem cell proliferation in microfluidic cell culture arrays. Nat Methods 2011; 8:581-586.
52. Petzer AL, Zandstra PW, Piret JM, Eaves CJ. Differential cytokine effects on primitive (CD34ÃCD38-) human hematopoietic cells: novel responses to Flt3-ligand and thrombopoietin. J Exp Med 1996; 183:2551-2558.
53. Watts KL, Zhang X, Beard BC, et al. Differential effects of HOXB4 and NUP98-HOXA10hd on hematopoietic repopulating cells in a nonhuman primate model. Hum Gene Ther 2011; 22:1475-1482.
54. Csaszar E, Kirouac DC, Yu M, et al. Rapid expansion of human hematopoietic stem cells by automated control of inhibitory feedback signaling. Cell Stem Cell 2012; 10:218-229
55. Carbonaro DA, Jin X, Wang X, et al. Gene therapy/bone marrow transplantation in ADA-deficient mice: roles of enzyme-replacement therapy and cytoreduction. Blood 2012; 120:3677-3687.
56. Candotti F, Shaw KL, Muul L, et al. Gene therapy for adenosine deaminasedeficient severe combined immune deficiency: clinical comparison of retroviral vectors and treatment plans. Blood 2012; 120:3635-3646.
57. Czechowicz A, Kraft D, Weissman IL, Bhattacharya D. Efficient transplantation via antibody-based clearance of hematopoietic stem cell niches. Science 2007; 318:1296-1299.
58. Ahmed F, Ings SJ, Pizzey AR, et al. Impaired bone marrow homing of cytokineactivated CD34Ã cells in the NOD/SCID model. Blood 2004; 103:2079-2087.
59. Rebel VI, Tanaka M, Lee JS, et al. One-day ex vivo culture allows effective gene transfer into human nonobese diabetic/severe combined immune-deficient repopulating cells using high-titer vesicular stomatitis virus G protein pseudotyped retrovirus. Blood 1999; 93:2217-2224.
60. Szilvassy SJ, Bass MJ, Van Zant G,Grimes B. Organ-selective homing defines engraftment kinetics of murine hematopoietic stem cells and is compromised by ex vivo expansion. Blood 1999; 93:1557-1566.
61. Guenechea G, Segovia JC, Albella B, et al. Delayed engraftment of nonobese diabetic/severe combined immunodeficient mice transplanted with ex vivoexpanded human CD34(Ã) cord blood cells. Blood 1999; 93:1097-1105.
62. Mazurier F, Gan OI, McKenzie JL, et al. Lentivector-mediated clonal tracking reveals intrinsic heterogeneity in the human hematopoietic stem cell compartment and culture-induced stem cell impairment. Blood 2004; 103:545-552.
63. Kallinikou K, Anjos-Afonso F, Blundell MP, et al. Engraftment defect of cytokine-cultured adult human mobilized CD34(Ã) cells is related to reduced adhesion to bone marrowniche elements. Br J Haematol 2012; 158:778-787.
64. Takenaka K, Prasolava TK, Wang JC, et al. Polymorphism in Sirpa modulates engraftment of human hematopoietic stem cells. Nat Immunol 2007; 8:1313-1323.
65. Takagi S, Saito Y, Hijikata A, et al. Membrane-bound human SCF/KL promotes in vivo human hematopoietic engraftment and myeloid differentiation. Blood 2012; 119:2768-2777.
66. Rongvaux A, Willinger T, Takizawa H, et al. Human thrombopoietin knockin mice efficiently support human hematopoiesis in vivo. Proc Natl Acad Sci USA 2011; 108:2378-2383.
67. Landel CP, Dunlap J, Patton JB, Manser T. A germline-competent embryonic stem cell line from NOD.Cg-Prkdc (scid) Il2rg (tm1Wjl)/SzJ (NSG) mice. Transgenic Res 2013; 22:179-185.
68. Bendall SC, Simonds EF, Qiu P, et al. Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science 2011; 332:687-696.