Comprehensive hematopoietic stem cell isolation methods

Methods in Molecular Biology

Volumn 976, Issue , 2013, Pages 1-15

  Rector, Kyle ^a   Liu, Yi ^a   Van Zant, Gary ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Hematopoietic stem cells; Isolation methods; Lineage bias; Phenotypic markers

Indexed keywords

CELL MARKER;

ARTICLE; BONE MARROW; CELL ISOLATION; CELL LINEAGE; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL; HUMAN; NONHUMAN; ONTOGENY; PHENOTYPE; PRIORITY JOURNAL; ADULT; ANIMAL; CELL SEPARATION; METHODOLOGY; REVIEW;

ADULT; ANIMALS; CELL SEPARATION; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELLS; HUMANS;

MLCS; MLOWN;

EID: 84880606877     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-62703-317-6_1     Document Type: Article

References (68)

1. Siminovitch L, McCulloch EA, Till JE (1963) The distribution of colony-forming cells among spleen colonies. J Cell Physiol 62: 327-336
2. Snippert HJ, Clevers H (2011) Tracking adult stem cells. EMBO Rep 12: 113-122
3. Yin T, Li L (2006) The stem cell niches in bone. J Clin Invest 116: 1195-1201
4. Notta F, Doulatov S, Laurenti E, Poeppl A, Jurisica I et al (2011) Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science 333: 218-221
5. Spangrude GJ, Heimfeld S, Weissman IL (1988) Purification and characterization of mouse hematopoietic stem cells. Science 241: 58-62
6. Ogawa M, Matsuzaki Y, Nishikawa S, Hayashi S, Kunisada T et al (1991) Expression and function of c-kit in hemopoietic progenitor cells. J Exp Med 174: 63-71
7. Okada S, Nakauchi H, Nagayoshi K, Nishikawa S, Miura Y et al (1992) In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells. Blood 80: 3044-3050
8. Boswell HS, Wade PM Jr, Quesenberry PJ (1984) Thy-1 antigen expression by murine high-proliferative capacity hematopoietic progenitor cells. I. Relation between sensitivity to depletion by Thy-1 antibody and stem cell generation potential. J Immunol 133: 2940-2949
9. Berman JW, Basch RS (1985) Thy-1 antigen expression by murine hematopoietic precursor cells. Exp Hematol 13: 1152-1156
10. Williams DE, Boswell HS, Floyd AD, Broxmeyer HE (1985) Pluripotential hematopoietic stem cells in post-5-fluorouracil murine bone marrow express the Thy-1 antigen. J Immunol 135: 1004-1011
11. Szilvassy SJ, Lansdorp PM, Humphries RK, Eaves AC, Eaves CJ (1989) Isolation in a single step of a highly enriched murine hematopoietic stem cell population with competitive longterm repopulating ability. Blood 74: 930-939
12. Ikuta K, Weissman IL (1992) Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc Natl Acad Sci USA 89: 1502-1506
13. Uchida N, Weissman IL (1992) 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 175: 175-184
14. Spangrude GJ, Brooks DM (1992) Phenotypic analysis of mouse hematopoietic stem cells shows a Thy-1-negative subset. Blood 80: 1957-1964
15. Morrison SJ, Weissman IL (1994) The longterm repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1: 661-673
16. Osawa M, Hanada K, Hamada H, Nakauchi H (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273: 242-245
17. Adolfsson J, Borge OJ, Bryder D, Theilgaard- Monch K, Astrand-Grundstrom I et al (2001) Upregulation of Flt3 expression within the bone marrow Lin(-)Sca1(+)c-kit(+) stem cell compartment is accompanied by loss of selfrenewal capacity. Immunity 15: 659-669
18. Christensen JL, Weissman IL (2001) Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc Natl Acad Sci USA 98: 14541-14546
19. Yang L, Bryder D, Adolfsson J, Nygren J, Mansson R et al (2005) Identification of Lin(-)Sca1(+) kit(+)CD34(+)Flt3- short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients. Blood 105: 2717-2723
20. Sitnicka E, Bryder D, Theilgaard-Monch K, Buza-Vidas N, Adolfsson J et al (2002) Key role offlt3 ligand in regulation of the common lymphoid progenitor but not in maintenance of the hematopoietic stem cell pool. Immunity 17: 463-472
21. Adolfsson J, Mansson R, Buza-Vidas N, Hultquist A, Liuba K et al (2005) Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 121: 295-306
22. Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ (2005) SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121: 1109-1121
23. Balazs AB, Fabian AJ, Esmon CT, Mulligan RC (2006) Endothelial protein C receptor (CD201) explicitly identifies hematopoietic stem cells in murine bone marrow. Blood 107: 2317-2321
24. Kent DG, Copley MR, Benz C, Wohrer S, Dykstra BJ et al (2009) Prospective isolation and molecular characterization of hematopoietic stem cells with durable self-renewal potential. Blood 113: 6342-6350
25. Cheshier SH, Morrison SJ, Liao X, Weissman IL (1999) In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc Natl Acad Sci USA 96: 3120-3125
26. Foudi A, Hochedlinger K, Van Buren D, Schindler JW, Jaenisch R et al (2009) Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol 27: 84-90
27. Ploemacher RE, Brons NH (1988) Cells with marrow and spleen repopulating ability and forming spleen colonies on day 16, 12, and 8 are sequentially ordered on the basis of increasing rhodamine 123 retention. J Cell Physiol 136: 531-536
28. Ploemacher RE, Brons NH (1988) In vivo proliferative and differential properties of murine bone marrow cells separated on the basis of rhodamine-123 retention. Exp Hematol 16: 903-907
29. Zijlmans JM, Visser JW, Kleiverda K, Kluin PM, Willemze R et al (1995) Modification of rhodamine staining allows identification of hematopoietic stem cells with preferential short-term or long-term bone marrowrepopulating ability. Proc Natl Acad Sci USA 92: 8901-8905
30. Peng K, Visser AJ, van Hoek A, Wolfs CJ, Sanders JC et al (1990) Analysis of timeresolvedfluorescence anisotropy in lipid-protein systems. I. Application to the lipid probe octadecyl rhodamine B in interaction with bacteriophage M13 coat protein incorporated in phospholipid bilayers. Eur Biophys J 18: 277-283
31. Visser JW, de Vries P (1988) Isolation of spleen-colony forming cells (CFU-s) using wheat germ agglutinin and rhodamine 123 labeling. Blood Cells 14: 369-384
32. Mulder AH, Visser JW (1987) Separation and functional analysis of bone marrow cells separated by rhodamine-123fluorescence. Exp Hematol 15: 99-104
33. Kim M, Cooper DD, Hayes SF, Spangrude GJ (1998) Rhodamine-123 staining in hematopoietic stem cells of young mice indicates mitochondrial activation rather than dye efflux. Blood 91: 4106-4117
34. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183: 1797-1806
35. Goodell MA (2005) Stem cell identification and sorting using the Hoechst 33342 side population (SP). Curr Protoc Cytom, Chapter 9: Unit9 18
36. Morrison SJ, Hemmati HD, Wandycz AM, Weissman IL (1995) The purification and characterization of fetal liver hematopoietic stem cells. Proc Natl Acad Sci USA 92: 10302-10306
37. Harrison DE, Zhong RK, Jordan CT, Lemischka IR, Astle CM (1997) Relative to adult marrow, fetal liver repopulates nearlyfive times more effectively long-term than shortterm. Exp Hematol 25: 293-297
38. Jordan CT, McKearn JP, Lemischka IR (1990) Cellular and developmental properties of fetal hematopoietic stem cells. Cell 61: 953-963
39. Jordan CT, Astle CM, Zawadzki J, Mackarehtschian K, Lemischka IR et al (1995) Long-term repopulating abilities of enriched fetal liver stem cells measured by competitive repopulation. Exp Hematol 23: 1011-1015
40. Orlic D, Fischer R, Nishikawa S, Nienhuis AW, Bodine DM (1993) Purification and characterization of heterogeneous pluripotent hematopoietic stem cell populations expressing high levels of c-kit receptor. Blood 82: 762-770
41. Sanchez MJ, Holmes A, Miles C, Dzierzak E (1996) Characterization of thefirst definitive hematopoietic stem cells in the AGM and liver of the mouse embryo. Immunity 5: 513-525
42. Yoder MC, Hiatt K, Dutt P, Mukherjee P, Bodine DM et al (1997) Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity 7: 335-344
43. Ito T, Tajima F, Ogawa M (2000) Developmental changes of CD34 expression by murine hematopoietic stem cells. Exp Hematol 28: 1269-1273
44. Matsuoka S, Ebihara Y, Xu M, Ishii T, Sugiyama D et al (2001) CD34 expression on long-term repopulating hematopoietic stem cells changes during developmental stages. Blood 97: 419-425
45. Uchida N, Dykstra B, Lyons K, Leung F, Kristiansen M et al (2004) ABC transporter activities of murine hematopoietic stem cells vary according to their developmental and activation status. Blood 103: 4487-4495
46. Kim I, He S, Yilmaz OH, Kiel MJ, Morrison SJ (2006) Enhanced purification of fetal liver hematopoietic stem cells using SLAM family receptors. Blood 108: 737-744
47. Randall TD, Weissman IL (1997) Phenotypic and functional changes induced at the clonal level in hematopoietic stem cells after 5-fluorouracil treatment. Blood 89: 3596-3606
48. Sato T, Laver JH, Ogawa M (1999) Reversible expression of CD34 by murine hematopoietic stem cells. Blood 94: 2548-2554
49. Higuchi Y, Zeng H, Ogawa M (2003) CD38 expression by hematopoietic stem cells of newborn and juvenile mice. Leukemia 17: 171-174
50. Spangrude GJ, Brooks DM, Tumas DB (1995) Long-term repopulation of irradiated mice with limiting numbers of purified hematopoietic stem cells: in vivo expansion of stem cell phenotype but not function. Blood 85: 1006-1016
51. Morrison SJ, Wandycz AM, Akashi K, Globerson A, Weissman IL (1996) The aging of hematopoietic stem cells. Nat Med 2: 1011-1016
52. Pearce DJ, Anjos-Afonso F, Ridler CM, Eddaoudi A, Bonnet D (2007) Age-dependent increase in side population distribution within hematopoiesis: implications for our understanding of the mechanism of aging. Stem Cells 25: 828-835
53. Yilmaz OH, Kiel MJ, Morrison SJ (2006) SLAM family markers are conserved among hematopoietic stem cells from old and reconstituted mice and markedly increase their purity. Blood 107: 924-930
54. Sudo K, Ema H, Morita Y, Nakauchi H (2000) Age-associated characteristics of murine hematopoietic stem cells. J Exp Med 192: 1273-1280
55. Kim M, Moon HB, Spangrude GJ (2003) Major age-related changes of mouse hematopoietic stem/progenitor cells. Ann N Y Acad Sci 996: 195-208
56. Li CL, Johnson GR (1992) Rhodamine123 reveals heterogeneity within murine Lin-, Sca- 1+ hemopoietic stem cells. J Exp Med 175: 1443-1447
57. Sieburg HB, Cho RH, Dykstra B, Uchida N, Eaves CJ et al (2006) The hematopoietic stem compartment consists of a limited number of discrete stem cell subsets. Blood 107: 2311-2316
58. Muller-Sieburg CE, Cho RH, Karlsson L, Huang JF, Sieburg HB (2004) Myeloid-biased hematopoietic stem cells have extensive selfrenewal capacity but generate diminished lymphoid progeny with impaired IL-7 responsiveness. Blood 103: 4111-4118
59. Muller-Sieburg CE, Cho RH, Thoman M, Adkins B, Sieburg HB (2002) Deterministic regulation of hematopoietic stem cell selfrenewal and differentiation. Blood 100: 1302-1309
60. Sieburg HB, Rezner BD, Muller-Sieburg CE (2011) Predicting clonal self-renewal and extinction of hematopoietic stem cells. Proc Natl Acad Sci USA 108: 4370-4375
61. Beerman I, Bhattacharya D, Zandi S, Sigvardsson M, Weissman IL et al (2010) Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proc Natl Acad Sci USA 107: 5465-5470
62. Challen GA, Boles NC, Chambers SM, Goodell MA (2010) Distinct hematopoietic stem cell subtypes are differentially regulated by TGFbeta1. Cell Stem Cell 6: 265-278
63. Morita Y, Ema H, Nakauchi H (2010) Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment. J Exp Med 207: 1173-1182
64. Matsuzaki Y, Kinjo K, Mulligan RC, Okano H (2004) Unexpectedly efficient homing capacity of purified murine hematopoietic stem cells. Immunity 20: 87-93
65. Robinson SN, Seina SM, Gohr JC, Kuszynski CA, Sharp JG (2005) Evidence for a qualitative hierarchy within the Hoechst-33342 'side population' (SP) of murine bone marrow cells. Bone Marrow Transplant 35: 807-818
66. Kiel MJ, Yilmaz OH, Morrison SJ (2008) CD150- cells are transiently reconstituting multipotent progenitors with little or no stem cell activity. Blood 111:4413-4414, author reply 4414-4415
67. Weksberg DC, Chambers SM, Boles NC, Goodell MA (2008) CD150- side population cells represent a functionally distinct population of long-term hematopoietic stem cells. Blood 111: 2444-2451
68. Benveniste P, Frelin C, Janmohamed S, Barbara M, Herrington R et al (2010) Intermediateterm hematopoietic stem cells with extended but time-limited reconstitution potential. Cell Stem Cell 6: 48-58