Age-associated changes in human hematopoietic stem cells

Seminars in Hematology

Volumn 54, Issue 1, 2017, Pages 39-42

  Pang, Wendy W ^a,b   Schrier, Stanley L ^b   Weissman, Irving L ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Aging Clonal selection; Hematopoietic stem cell; Myeloid bias

Indexed keywords

ACUTE MYELOID LEUKEMIA; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; CANCER REGRESSION; CELL AGING; CELL DIFFERENTIATION; CELL POPULATION; CHRONIC MYELOID LEUKEMIA; CLONAL HEMATOPOIESIS; EPIGENETICS; HEMATOPOIESIS; HUMAN; IMMUNOPHENOTYPING; MOLECULAR CLONING; MYELODYSPLASTIC SYNDROME; MYELOPROLIFERATIVE DISORDER; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR MICROENVIRONMENT; UPREGULATION; X CHROMOSOME INACTIVATION; ANIMAL; CYTOLOGY; GENETICS; HEMATOPOIETIC STEM CELL; METABOLISM; MOUSE;

ANIMALS; CELL AGING; CELL DIFFERENTIATION; HEMATOPOIETIC STEM CELLS; HUMANS; MICE;

EID: 85006721611     PISSN: 00371963     EISSN: 15328686     Source Type: Journal    
DOI: 10.1053/j.seminhematol.2016.10.004     Document Type: Review

References (66)

1. [1] Pang, W.W., Schrier, S.L., Anemia in the elderly. Curr Opin Hematol 19:3 (2012), 133–140.
2. [2] Guralnik, J.M., Eisenstaedt, R.S., Ferrucci, L., Klein, H.G., Woodman, R.C., Prevalence of anemia in persons 65 years and older in the United States: evidence for a high rate of unexplained anemia. Blood 104:8 (2004), 2263–2268.
3. [3] Shaw, A.C., Goldstein, D.R., Montgomery, R.R., Age-dependent dysregulation of innate immunity. Nat Rev Immunol 13:12 (2013), 875–887.
4. [4] Kogut, I., Scholz, J.L., Cancro, M.P., Cambier, J.C., B cell maintenance and function in aging. Semin Immunol 24:5 (2012), 342–349.
5. [5] Nikolich- ugich, J., Aging of the T cell compartment in mice and humans: from no naive expectations to foggy memories. J Immunol 193:6 (2014), 2622–2629.
6. [6] Montecino-Rodriguez, E., Berent-Maoz, B., Dorshkind, K., et al. Causes, consequences, and reversal of immune system aging. J Clin Invest 123:3 (2013), 958–965.
7. [7] Goronzy, J.J., Fang, F., Cavanagh, M.M., Qi, Q., Weyand, C.M., Naive T cell maintenance and function in human aging. J Immunol 194:9 (2015), 4073–4080.
8. [8] Lichtman, M.A., Rowe, J.M., The relationship of patient age to the pathobiology of the clonal myeloid diseases. Semin Oncol 31:2 (2004), 185–197.
9. [9] Kyle, R.A., Gertz, M.A., Witzig, T.E., et al. Review of 1027 patients with newly diagnosed multiple myeloma. Mayo Clin Proc 78:1 (2003), 21–33.
10. [10] Morton, L.M., Wang, S.S., Devesa, S.S., et al. Lymphoma incidence patterns by WHO subtype in the United States, 1992-2001. Blood 107:1 (2006), 265–276.
11. [11] Bryder, D., Rossi, D.J., Weissman, I.L., Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. Am J Pathol 169:2 (2006), 338–346.
12. [12] Negrin, R.S., Atkinson, K., Leemhuis, T., et al. Transplantation of highly purified CD34+Thy-1+ hematopoietic stem cells in patients with metastatic breast cancer. Biol Blood Marrow Transplant 6:3 (2000), 262–271.
13. [13] Baum, C.M., Weissman, I.L., Tsukamoto, A.S., Buckle, A.M., Peault, B., Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci U S A 89:7 (1992), 2804–2808.
14. [14] Murray, L., DiGiusto, D., Chen, B., et al. Analysis of human hematopoietic stem cell populations. Blood Cells 20:2-3 (1994), 364–369.
15. [15] Majeti, R., Park, C.Y., Weissman, I.L., Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood. Cell Stem Cell 1:6 (2007), 635–645.
16. [16] Bhatia, M., Wang, J.C., Kapp, U., Bonnet, D., Dick, J.E., Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci U S A 94:10 (1997), 5320–5325.
17. [17] Ogawa, T., Kitagawa, M., Hirokawa, K., 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 (2000), 57–68.
18. [18] Muschler, G.F., Nitto, H., Boehm, C.A., Easley, K.A., Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J Orthop Res 19:1 (2001), 117–125.
19. [19] Pang, W.W., Price, E.A., Sahoo, D., et al. Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age. Proc Natl Acad Sci U S A 108:50 (2011), 20012–20017.
20. [20] Woolthuis, C.M., Mariani, N., Verkaik-Schakel, R.N., et al. Aging impairs long-term hematopoietic regeneration after autologous stem cell transplantation. Biol Blood Marrow Transplant 20:6 (2014), 865–871.
21. [21] Kollman, C., Spellman, S.R., Zhang, M.-J., et al. The effect of donor characteristics on survival after unrelated donor transplantation for hematologic malignancy. Blood 127:2 (2016), 260–267.
22. [22] Kollman, C., Howe, C.W., Anasetti, C., et al. Donor characteristics as risk factors in recipients after transplantation of bone marrow from unrelated donors: the effect of donor age. Blood 98:7 (2001), 2043–2051.
23. [23] Finke, J., Schmoor, C., Bethge, W.A., et al. Prognostic factors affecting outcome after allogeneic transplantation for hematological malignancies from unrelated donors: results from a randomized trial. Biol Blood Marrow Transplant 18:11 (2012), 1716–1726.
24. [24] Rezvani, A.R., Storer, B.E., Guthrie, K.A., et al. Impact of donor age on outcome after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant 21:1 (2015), 105–112.
25. [25] Yahata, T., Takanashi, T., Muguruma, Y., et al. Accumulation of oxidative DNA damage restricts the self-renewal capacity of human hematopoietic stem cells. Blood 118:11 (2011), 2941–2950.
26. [26] Kuranda, K., Vargaftig, J., de la Rochere, P., et al. Age-related changes in human hematopoietic stem/progenitor cells. Aging Cell 10:3 (2011), 542–546.
27. [27] Morrison, S.J., Wandycz, A.M., Akashi, K., Globerson, A., Weissman, I.L., The aging of hematopoietic stem cells. Nat Med 2:9 (1996), 1011–1016.
28. [28] Wright, D.E., Bowman, E.P., Wagers, A.J., Butcher, E.C., Weissman, I.L., Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J Exp Med 195:9 (2002), 1145–1154.
29. [29] Signer, R.A.J., Montecino-Rodriguez, E., Witte, O.N., et al. Age-related defects in B lymphopoiesis underlie the myeloid dominance of adult leukemia. Blood 110:6 (2007), 1831–1839.
30. [30] Miyamoto, T., Weissman, I.L., Akashi, K., AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc Natl Acad Sci U S A 97:13 (2000), 7521–7526.
31. [31] Corces-Zimmerman, M.R., Hong, W.-J., Weissman, I.L., Medeiros, B.C., Majeti, R., Preleukemic mutations in human acute myeloid leukemia affect epigenetic regulators and persist in remission. Proc Natl Acad Sci U S A 111:7 (2014), 2548–2553.
32. [32] Jan, M., Snyder, T.M., Corces-Zimmerman, M.R., et al. Clonal evolution of preleukemic hematopoietic stem cells precedes human acute myeloid leukemia. Sci Transl Med, 4(149), 2012 149ra118.
33. [33] Shlush, L.I., Zandi, S., Mitchell, A., et al. Identification of pre-leukaemic haematopoietic stem cells in acute leukaemia. Nature 506:7488 (2014), 328–333.
34. [34] Cho, R.H., Sieburg, H.B., Muller-Sieburg, C.E., 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 111:12 (2008), 5553–5561.
35. [35] Beerman, I., Bhattacharya, D., Zandi, S., et al. Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proc Natl Acad Sci U S A 107:12 (2010), 5465–5470.
36. [36] Dykstra, B., Olthof, S., Schreuder, J., Ritsema, M., de Haan, G., Clonal analysis reveals multiple functional defects of aged murine hematopoietic stem cells. J Exp Med 208:13 (2011), 2691–2703.
37. [37] Challen, G.A., Boles, N.C., Chambers, S.M., Goodell, M.A., Distinct hematopoietic stem cell subtypes are differentially regulated by TGF-β1. Cell Stem Cell 6:3 (2010), 265–278.
38. [38] Busque, L., Mio, R., Mattioli, J., et al. Nonrandom X-inactivation patterns in normal females: lyonization ratios vary with age. Blood 88:1 (1996), 59–65.
39. [39] El Kassar, N., Hetet, G., Brière, J., Grandchamp, B., X-chromosome inactivation in healthy females: incidence of excessive lyonization with age and comparison of assays involving DNA methylation and transcript polymorphisms. Clin Chem 44:1 (1998), 61–67.
40. [40] Genovese, G., Kähler, A.K., Handsaker, R.E., et al. Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence. N Engl J Med 371:26 (2014), 2477–2487.
41. [41] Jaiswal, S., Fontanillas, P., Flannick, J., et al. Age-related clonal hematopoiesis associated with adverse outcomes. N Engl J Med 371:26 (2014), 2488–2498.
42. [42] Xie, M., Lu, C., Wang, J., et al. Age-related mutations associated with clonal hematopoietic expansion and malignancies. Nat Med 20:12 (2014), 1472–1478.
43. [43] McKerrell, T., Park, N., Moreno, T., et al. Leukemia-associated somatic mutations drive distinct patterns of age-related clonal hemopoiesis. Cell Rep 10:8 (2015), 1239–1245.
44. [44] Holstege, H., Pfeiffer, W., Sie, D., et al. Somatic mutations found in the healthy blood compartment of a 115-yr-old woman demonstrate oligoclonal hematopoiesis. Genome Res 24:5 (2014), 733–742.
45. [45] Pang, W.W., Pluvinage, J.V., Price, E., et al. Hematopoietic stem cell and progenitor cell mechanisms in myelodysplastic syndromes. Proc Natl Acad Sci U S A 110:8 (2013), 3011–3016.
46. [46] Will, B., Zhou, L., Vogler, T.O., et al. Stem and progenitor cells in myelodysplastic syndromes show aberrant stage-specific expansion and harbor genetic and epigenetic alterations. Blood 120:10 (2012), 2076–2086.
47. [47] Woll, P.S., Kjällquist, U., Chowdhury, O., et al. Myelodysplastic syndromes are propagated by rare and distinct human cancer stem cells in vivo. Cancer Cell 25:6 (2014), 794–808.
48. [48] Mian, S.A., Rouault-Pierre, K., Smith, A.E., et al. SF3B1 mutant MDS-initiating cells may arise from the haematopoietic stem cell compartment. Nat Commun, 6, 2015, 10004.
49. [49] Tehranchi, R., Woll, P.S., Anderson, K., et al. Persistent malignant stem cells in del(5q) myelodysplasia in remission. N Engl J Med 363:11 (2010), 1025–1037.
50. [50] Nilsson, L., Åstrand-Grundström, I., Anderson, K., et al. Involvement and functional impairment of the CD34+CD38-Thy-1+ hematopoietic stem cell pool in myelodysplastic syndromes with trisomy 8. Blood 100:1 (2002), 259–267.
51. [51] Nilsson, L., Astrand-Grundström, I., Arvidsson, I., et al. Isolation and characterization of hematopoietic progenitor/stem cells in 5q-deleted myelodysplastic syndromes: evidence for involvement at the hematopoietic stem cell level. Blood 96:6 (2000), 2012–2021.
52. [52] Jamieson, C.H.M., Gotlib, J., Durocher, J.A., et al. The JAK2 V617F mutation occurs in hematopoietic stem cells in polycythemia vera and predisposes toward erythroid differentiation. Proc Natl Acad Sci U S A 103:16 (2006), 6224–6229.
53. [53] Jamieson, C.H.M., Ailles, L.E., Dylla, S.J., et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 351:7 (2004), 657–667.
54. [54] Abrahamsson, A.E., Geron, I., Gotlib, J., et al. Glycogen synthase kinase 3beta missplicing contributes to leukemia stem cell generation. Proc Natl Acad Sci U S A 106:10 (2009), 3925–3929.
55. [55] Jiang, Q., Crews, L.A., Barrett, C.L., et al. ADAR1 promotes malignant progenitor reprogramming in chronic myeloid leukemia. Proc Natl Acad Sci U S A 110:3 (2013), 1041–1046.
56. [56] Figueroa, M.E., Abdel-Wahab, O., Lu, C., et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 18:6 (2010), 553–567.
57. [57] Bröske, A.-M., Vockentanz, L., Kharazi, S., et al. DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction. Nat Genet 41:11 (2009), 1207–1215.
58. [58] Trowbridge, J.J., Snow, J.W., Kim, J., Orkin, S.H., DNA Methyltransferase 1 Is essential for and uniquely regulates hematopoietic stem and progenitor cells. Cell Stem Cell 5:4 (2009), 442–449.
59. [59] Tanaka, S., Miyagi, S., Sashida, G., et al. Ezh2 augments leukemogenicity by reinforcing differentiation blockage in acute myeloid leukemia. Blood 120:5 (2012), 1107–1117.
60. [60] Challen, G.A., Sun, D., Jeong, M., et al. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat. Genet 44:1 (2012), 23–31.
61. [61] Moran-Crusio, K., Reavie, L., Shih, A., et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 20:1 (2011), 11–24.
62. [62] Abdel-Wahab, O., Adli, M., LaFave, L.M., et al. ASXL1 mutations promote myeloid transformation through loss of PRC2-mediated gene repression. Cancer Cell 22:2 (2012), 180–193.
63. [63] Griffith, J.F., Yeung, D.K.W., Ma, H.T., et al. Bone marrow fat content in the elderly: a reversal of sex difference seen in younger subjects. J Magn Reson Imaging 36:1 (2012), 225–230.
64. [64] Tuljapurkar, S.R., McGuire, T.R., Brusnahan, S.K., et al. Changes in human bone marrow fat content associated with changes in hematopoietic stem cell numbers and cytokine levels with aging. J Anat 219:5 (2011), 574–581.
65. [65] Reinisch, A., Etchart, N., Thomas, D., et al. Epigenetic and in vivo comparison of diverse MSC sources reveals an endochondral signature for human hematopoietic niche formation. Blood 125:2 (2015), 249–260.
66. [66] Kode, A., Manavalan, J.S., Mosialou, I., et al. Leukaemogenesis induced by an activating β-catenin mutation in osteoblasts. Nature 506:7487 (2014), 240–244.