Abstract
Recent advances have increased the purity of hematopoietic stem cells (HSCs) isolated from young mouse bone marrow. However, little attention has been paid to the purity of HSCs from other contexts. Although Thy-1 low Sca-1+ Lineage- c-kit+ cells from young bone marrow are highly enriched for HSCs (1 in 5 cells gives long-term multilineage reconstitution after transplantation into irradiated mice), the same population from old, reconstituted, or cytokine-mobilized mice engrafts much less efficiently (1 in 78 to 1 in 185 cells gives long-term multilineage reconstitution). To test whether we could increase the purity of HSCs isolated from these contexts, we examined the SLAM family markers CD150 and CD48. All detectable HSCs from old, reconstituted, and cyclophosphamide/G-CSF-mobilized mice were CD150+ CD48-, just as in normal young bone marrow. Thy-1 low Sca-1+ Lineage- c-kit+ cells from old, reconstituted, or mobilized mice included mainly CD48+ and/or CD150- cells that lacked reconstituting ability. CD150+ CD48- Sca-1+ Lineage- c-kit+ cells from old, reconstituted, or mobilized mice were much more highly enriched for HSCs, with 1 in 3 to 1 in 7 cells giving long-term multilineage reconstitution. SLAM family receptor expression is conserved among HSCs from diverse contexts, and HSCs from old, reconstituted, and mobilized mice engraft relatively efficiently after transplantation when contaminating cells are eliminated.
MeSH Terms
Aging/metabolism
Animals
Antigens, CD/metabolism
Antigens, Ly
Antineoplastic Agents, Alkylating/administration & dosage
CD48 Antigen
Cell Separation
Cyclophosphamide/administration & dosage
Glycoproteins/metabolism
Graft Survival/radiation effects
Granulocyte Colony-Stimulating Factor/administration & dosage
Hematopoietic Stem Cell Mobilization/methods
Hematopoietic Stem Cell Transplantation
Hematopoietic Stem Cells/metabolism
Immunoglobulins/metabolism
Membrane Proteins
Mice
Proto-Oncogene Proteins c-kit
Receptors, Cell Surface
Signaling Lymphocytic Activation Molecule Family Member 1
Thy-1 Antigens
Whole-Body Irradiation
Chemicals
Antigens, CD
Antigens, Ly
Antineoplastic Agents, Alkylating
CD48 Antigen
Cd48 protein, mouse
Glycoproteins
Immunoglobulins
Ly6a protein, mouse
Membrane Proteins
Receptors, Cell Surface
Thy-1 Antigens
Granulocyte Colony-Stimulating Factor
Signaling Lymphocytic Activation Molecule Family Member 1
Cyclophosphamide
Proto-Oncogene Proteins c-kit
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Yilmaz Omer H
Howard Hughes Medical Institute, Department of Internal Medicine, Ann Arbor, MI, USA.
Kiel Mark J
Morrison Sean J
References (29)
29 references, click to expand
-
Translating stem and progenitor cell biology to the clinic: barriers and opportunities.
Science. 2000 Feb 25;287(5457):1442-6
PMID: 10688785
-
The endoglin(positive) sca-1(positive) rhodamine(low) phenotype defines a near-homogeneous population of long-term repopulating hematopoietic stem cells.
Immunity. 2003 Oct;19(4):525-33
PMID: 14563317
-
Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells.
Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14541-6
PMID: 11724967
-
Changes in integrin expression are associated with altered homing properties of Lin(-/lo)Thy1.1(lo)Sca-1(+)c-kit(+) hematopoietic stem cells following mobilization by cyclophosphamide/granulocyte colony-stimulating factor.
Exp Hematol. 2002 Feb;30(2):176-85
PMID: 11823053
-
Different in vivo repopulating activities of purified hematopoietic stem cells before and after being stimulated to divide in vitro with the same kinetics.
Exp Hematol. 2003 Dec;31(12):1338-47
PMID: 14662343
-
"Homing to Niche," a new criterion for hematopoietic stem cells?
Immunity. 2004 Jan;20(1):1-2
PMID: 14738758
-
Unexpectedly efficient homing capacity of purified murine hematopoietic stem cells.
Immunity. 2004 Jan;20(1):87-93
PMID: 14738767
-
Asymmetric division and lineage commitment at the level of hematopoietic stem cells: inference from differentiation in daughter cell and granddaughter cell pairs.
J Exp Med. 2004 Feb 2;199(3):295-302
PMID: 14744992
-
Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche.
Cell. 2004 Jul 23;118(2):149-61
PMID: 15260986
-
Molecular signatures of proliferation and quiescence in hematopoietic stem cells.
PLoS Biol. 2004 Oct;2(10):e301
PMID: 15459755
-
Clonal analysis of hematopoietic stem-cell differentiation in vivo.
Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2788-92
PMID: 1672767
-
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 Jan 1;175(1):175-84
PMID: 1346154
-
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. 1995 Feb 15;85(4):1006-16
PMID: 7849289
-
The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype.
Immunity. 1994 Nov;1(8):661-73
PMID: 7541305
-
The purification and characterization of fetal liver hematopoietic stem cells.
Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10302-6
PMID: 7479772
-
The biology of hematopoietic stem cells.
Annu Rev Cell Dev Biol. 1995;11:35-71
PMID: 8689561
-
Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell.
Science. 1996 Jul 12;273(5272):242-5
PMID: 8662508
-
Bone marrow collected 14 days after in vivo administration of granulocyte colony-stimulating factor and stem cell factor to mice has 10-fold more repopulating ability than untreated bone marrow.
Blood. 1996 Jul 1;88(1):89-97
PMID: 8704206
-
Little evidence for developmental plasticity of adult hematopoietic stem cells.
Science. 2002 Sep 27;297(5590):2256-9
PMID: 12215650
-
The aging of hematopoietic stem cells.
Nat Med. 1996 Sep;2(9):1011-6
PMID: 8782459
-
Cyclophosphamide/granulocyte colony-stimulating factor induces hematopoietic stem cells to proliferate prior to mobilization.
Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):1908-13
PMID: 9050878
-
Mouse strain-dependent changes in frequency and proliferation of hematopoietic stem cells during aging: correlation between lifespan and cycling activity.
Blood. 1997 Mar 1;89(5):1543-50
PMID: 9057635
-
Phenotypic and functional changes induced at the clonal level in hematopoietic stem cells after 5-fluorouracil treatment.
Blood. 1997 May 15;89(10):3596-606
PMID: 9160664
-
Identification of a lineage of multipotent hematopoietic progenitors.
Development. 1997 May;124(10):1929-39
PMID: 9169840
-
SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells.
Cell. 2005 Jul 1;121(7):1109-21
PMID: 15989959
-
CD144 (VE-cadherin) is transiently expressed by fetal liver hematopoietic stem cells.
Blood. 2005 Aug 1;106(3):903-5
PMID: 15831702
-
Effects of aging on the homing and engraftment of murine hematopoietic stem and progenitor cells.
Blood. 2005 Aug 15;106(4):1479-87
PMID: 15827136
-
Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo.
Blood. 2003 Jan 15;101(2):508-16
PMID: 12393529
-
Age-associated characteristics of murine hematopoietic stem cells.
J Exp Med. 2000 Nov 6;192(9):1273-80
PMID: 11067876