Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 50, 2011, Pages 20012-20017

  Pang, Wendy W ^a   Price, Elizabeth A ^b   Sahoo, Debashis ^a   Beerman, Isabel ^c   Maloney, William J ^b   Rossi, Derrick J ^c   Schrier, Stanley L ^b   Weissman, Irving L ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Hematopoiesis; Leukemia; Lineage potential; Microarray

Indexed keywords

AGED; AGING; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW; CELL CYCLE; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE EXPRESSION PROFILING; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

ADULT; AGED; AGED, 80 AND OVER; AGING; ANIMALS; BONE MARROW CELLS; CELL COUNT; CELL DIFFERENTIATION; CELL LINEAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MIDDLE AGED; MYELOID CELLS; YOUNG ADULT;

EID: 84055200841     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1116110108     Document Type: Article

References (45)

1. Bryder D, Rossi DJ, Weissman IL (2006) Hematopoietic stem cells: The paradigmatic tissue-specific stem cell. Am J Pathol 169:338-346. (Pubitemid 44156296)
2. Chambers SM, et al. (2007) Aging hematopoietic stem cells decline in function and exhibit epigenetic dysregulation. PLoS Biol 5:e201.
3. 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. (Pubitemid 36706601)
4. Morrison SJ, Wandycz AM, Akashi K, Globerson A, Weissman IL (1996) The aging of hematopoietic stem cells. Nat Med 2:1011-1016. (Pubitemid 26306840)
5. 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. (Pubitemid 46572578)
6. Rossi DJ, et al. (2005) Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci USA 102:9194-9199. (Pubitemid 40923540)
7. Sudo K, Ema H, Morita Y, Nakauchi H (2000) Age-associated characteristics of murine hematopoietic stem cells. J Exp Med 192:1273-1280.
8. Cho RH, Sieburg HB, Muller-Sieburg CE (2008) A new mechanism for the aging of hematopoietic stem cells: Aging changes the clonal composition of the stem cell compartment but not individual stem cells. Blood 111:5553-5561.
9. Muller-Sieburg CE, Cho RH, Karlsson L, Huang JF, Sieburg HB (2004) Myeloid-biased hematopoietic stem cells have extensive self-renewal capacity but generate diminished lymphoid progeny with impaired IL-7 responsiveness. Blood 103:4111-4118. (Pubitemid 38685351)
10. Dykstra B, et al. (2007) Long-term propagation of distinct hematopoietic differentiation programs in vivo. Cell Stem Cell 1:218-229. (Pubitemid 47215588)
11. Beerman I, 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.
12. Challen GA, Boles NC, Chambers SM, Goodell MA (2010) Distinct hematopoietic stem cell subtypes are differentially regulated by TGF-beta1. Cell Stem Cell 6:265-278.
13. Morita Y, Ema H, Nakauchi H (2010) Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment. J Exp Med 207:1173-1182.
14. Ogawa T, Kitagawa M, Hirokawa K (2000) Age-related changes of human bone marrow: A histometric estimation of proliferative cells, apoptotic cells, T cells, B cells and macrophages. Mech Ageing Dev 117(1-3):57-68. (Pubitemid 30665793)
15. Linton PJ, Dorshkind K (2004) Age-related changes in lymphocyte development and function. Nat Immunol 5(2):133-139. (Pubitemid 38208354)
16. Miller JP, Allman D (2003) The decline in B lymphopoiesis in aged mice reflects loss of very early B-lineage precursors. J Immunol 171:2326-2330. (Pubitemid 37025538)
17. Guralnik JM, Eisenstaedt RS, Ferrucci L, Klein HG, Woodman RC (2004) Prevalence of anemia in persons 65 years and older in the United States: Evidence for a high rate of unexplained anemia. Blood 104:2263-2268. (Pubitemid 39331821)
18. Lichtman MA, Rowe JM (2004) The relationship of patient age to the pathobiology of the clonal myeloid diseases. Semin Oncol 31(2):185-197. (Pubitemid 38488832)
19. Bhatia M, Wang JC, Kapp U, Bonnet D, Dick JE (1997) Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci USA 94:5320-5325. (Pubitemid 27214781)
20. Baum CM, Weissman IL, Tsukamoto AS, Buckle AM, Peault B (1992) Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci USA 89:2804-2808.
21. Péault B, Weissman IL, Buckle AM, Tsukamoto A, Baum C (1993) Thy-1-expressing CD34+ human cells express multiple hematopoietic potentialities in vitro and in SCID-hu mice. Nouv Rev Fr Hematol 35(1):91-93. (Pubitemid 23140733)
22. McCune JM, et al. (1988) The SCID-hu mouse: Murine model for the analysis of human hematolymphoid differentiation and function. Science 241:1632-1639.
23. Negrin RS, et al. (2000) Transplantation of highly purified CD34+Thy-1+ hematopoietic stem cells in patients with metastatic breast cancer. Biol Blood Marrow Transplant 6:262-271.
24. Murray L, et al. (1994) Analysis of human hematopoietic stem cell populations. Blood Cells 20:364-369, discussion 369-370.
25. Lansdorp PM, Dragowska W, Mayani H (1993) Ontogeny-related changes in proliferative potential of human hematopoietic cells. J Exp Med 178:787-791. (Pubitemid 23260416)
26. Gale RE, Fielding AK, Harrison CN, Linch DC (1997) Acquired skewing of X-chromosome inactivation patterns in myeloid cells of the elderly suggests stochastic clonal loss with age. Br J Haematol 98:512-519. (Pubitemid 27386528)
27. Marley SB, et al. (1999) Evidence for a continuous decline in haemopoietic cell function from birth: Application to evaluating bone marrow failure in children. Br J Haematol 106(1):162-166. (Pubitemid 29343544)
28. Lipschitz DA, Mitchell CO, Thompson C (1981) The anemia of senescence. Am J Hematol 11(1):47-54. (Pubitemid 11052362)
29. Kollman C, et al. (2001) Donor characteristics as risk factors in recipients after transplantation of bone marrow from unrelated donors: The effect of donor age. Blood 98:2043-2051.
30. Waterstrat A, et al. (2008) Telomeres and Telomerase in Ageing, Disease, and Cancer, ed Rudolph KL (Springer, Berlin), pp 111-140.
31. Taraldsrud E, et al. (2009) Age and stress related phenotypical changes in bone marrow CD34+ cells. Scand J Clin Lab Invest 69(1):79-84.
32. Beerman I, Maloney WJ, Weissmann IL, Rossi DJ (2010) Stem cells and the aging hematopoietic system. Curr Opin Immunol 22:500-506.
33. Majeti R, Park CY, Weissman IL (2007) Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood. Cell Stem Cell 1:635-645. (Pubitemid 350215330)
34. Manz MG, Miyamoto T, Akashi K, Weissman IL (2002) Prospective isolation of human clonogenic common myeloid progenitors. Proc Natl Acad Sci USA 99:11872-11877. (Pubitemid 34994491)
35. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116-5121. (Pubitemid 32397092)
36. Chambers SM, et al. (2007) Hematopoietic fingerprints: An expression database of stem cells and their progeny. Cell Stem Cell 1:578-591. (Pubitemid 350056409)
37. Nalapareddy K, Jiang H, Guachalla Gutierrez LM, Rudolph KL (2008) Determining the influence of telomere dysfunction and DNA damage on stem and progenitor cell aging: What markers can we use? Exp Gerontol 43:998-1004.
38. Weissman IL (2005) Normal and neoplastic stem cells. Novartis Found Symp 265:35-50; discussion 50-54, 92-97.
39. Lieber MR, Karanjawala ZE (2004) Ageing, repetitive genomes and DNA damage. Nat Rev Mol Cell Biol 5(1):69-75. (Pubitemid 38089843)
40. Nijnik A, et al. (2007) DNA repair is limiting for haematopoietic stem cells during ageing. Nature 447:686-690. (Pubitemid 46889732)
41. Rossi DJ, et al. (2007) Hematopoietic stem cell quiescence attenuates DNA damage response and permits DNA damage accumulation during aging. Cell Cycle 6:2371-2376. (Pubitemid 350058690)
42. Whitlock CA, Tidmarsh GF, Muller-Sieburg C, Weissman IL (1987) Bone marrow stromal cell lines with lymphopoietic activity express high levels of a pre-B neoplasiaassociated molecule. Cell 48:1009-1021.
43. Ishikawa F, et al. (2005) Development of functional human blood and immune systems in NOD/SCID/IL2 receptor gamma chain(null) mice. Blood 106:1565-1573. (Pubitemid 41208567)
44. Sahoo D, et al. (2010) MiDReG: A method of mining developmentally regulated genes using Boolean implications. Proc Natl Acad Sci USA 107:5732-5737.
45. Sahoo D, Dill DL, Gentles AJ, Tibshirani R, Plevritis SK (2008) Boolean implication networks derived from large scale, whole genome microarray datasets. Genome Biol 9:R157.1-R157.17.