Aging of the hematopoietic stem cells niche

International Journal of Hematology

Volumn 100, Issue 4, 2014, Pages 317-325

  Nakamura Ishizu, Ayako ^a   Suda, Toshio ^a  

^a KEIO UNIVERSITY   (Japan)

Author keywords

Aging; Bone marrow; Hematopoietic stem cells; Niche

Indexed keywords

CRE RECOMBINASE;

AGE; AGING; CELL AGING; ENDOTHELIUM CELL; HEMATOLOGIC MALIGNANCY; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC SYSTEM; HOMEOSTASIS; HUMAN; MOLECULAR MECHANICS; NONHUMAN; OSTEOBLAST; OSTEOCYTE; PHENOTYPE; REVIEW; STEM CELL MOBILIZATION; STEM CELL NICHE; STROMA CELL; ANIMAL; BONE MARROW; KNOCKOUT MOUSE; METABOLISM; MOUSE;

AGING; ANIMALS; BONE MARROW; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, KNOCKOUT; STEM CELL NICHE;

EID: 84927170343     PISSN: 09255710     EISSN: 18653774     Source Type: Journal    
DOI: 10.1007/s12185-014-1641-8     Document Type: Review

References (103)

1. Weissman IL. Stem cells. Cell. 2000;100:157–68.
2. Till JE, McCulloch EA, Siminovitch L. A stochastic model of stem cell proliferation, based on the growth of spleen colony-forming cells. Proc Natl Acad Sci USA. 1964;51:29–36.
3. Beerman I, Bhattacharya D, Zandi S, Sigvardsson M, Weissman IL, Bryder D, et al. Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proc Natl Acad Sci USA. 2010;107:5465–70.
4. Morrison SJ, Wandycz AM, Akashi K, Globerson A, Weissman IL. The aging of hematopoietic stem cells. Nat Med. 1996;2:1011–6.
5. Xing Z, Ryan MA, Daria D, Nattamai KJ, Van Zant G, Wang L, et al. Increased hematopoietic stem cell mobilization in aged mice. Blood. 2006;108:2190–7.
6. Chambers SM, Shaw CA, Gatza C, Fisk CJ, Donehower LA, Goodell MA. Aging hematopoietic stem cells decline in function and exhibit epigenetic dysregulation. PLoS Biol. 2007;5:e201.
7. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells. 1978;4:7–25.
8. Zhang J, Niu C, Ye L, Huang H, He X, Tong W-G, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425:836–41.
9. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, et al. Tie2/Angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 2004;118:149–61.
10. Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature. 2012;481:457–62.
11. Butler JM, Nolan DJ, Vertes EL, Varnum-Finney B, Kobayashi H, Hooper AT, et al. Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. Cell Stem Cell. 2010;6:251–64.
12. Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity. 2006;25:977.
13. Méndez-Ferrer S, Michurina VT, Ferraro F, Macarthur BD, Lira SA, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2010;466:829–34.
14. Katayama Y, Battista M, Kao W-M, Hidalgo A, Peired AJ, Thomas SA, et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell. 2006;124:407.
15. Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, Daley GQ. Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature. 2009;460:259–63.
16. Yamazaki S, Ema H, Karlsson G, Yamaguchi T, Miyoshi H, Shioda S, et al. Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell. 2011;147:1146–58.
17. Chow A, Lucas D, Hidalgo A, Méndez-Ferrer S, Hashimoto D, Scheiermann C, et al. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J Exp Med. 2011;208:261–71.
18. Fujisaki J, Wu J, Carlson AL, Silberstein L, Putheti P, Larocca R, et al. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature. 2011;474:216–9.
19. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, et al. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med. 2006;12:657–64.
20. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 2004;118:149–61.
21. Yoshihara H, Arai F, Hosokawa K, Hagiwara T, Takubo K, Nakamura Y, et al. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell. 2007;1:685–97.
22. Nilsson SK, Johnston HM, Whitty GA, Williams B, Webb RJ, Denhardt DT, et al. Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood. 2005;106:1232–9.
23. Nakamura-Ishizu A, Okuno Y, Omatsu Y, Okabe K, Morimoto J, Uede T, et al. Extracellular matrix protein Tenascin-C is required in the bone marrow microenvironment primed for hematopoietic regeneration. Blood. 2012;119(23):5429–37.
24. Hosokawa K, Arai F, Yoshihara H, Iwasaki H, Nakamura Y, Gomei Y, et al. Knockdown of N-cadherin suppresses the long-term engraftment of hematopoietic stem cells. Blood. 2010;116:554–63.
25. Constien R, Forde A, Liliensiek B, Gröne HJ, Nawroth P, Hämmerling G, et al. Characterization of a novel EGFP reporter mouse to monitor Cre recombination as demonstrated by a Tie2 Cre mouse line. Genesis. 2001;30:36–44.
26. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol. 2001;230:230–42.
27. Alva JA, Zovein AC, Monvoisin A, Murphy T, Salazar A, Harvey NL, et al. VE-Cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells. Dev Dyn. 2006;235:759–67.
28. Monvoisin A, Alva JA, Hofmann JJ, Zovein AC, Lane TF, Iruela-Arispe ML. VE-cadherin-CreERT2 transgenic mouse: a model for inducible recombination in the endothelium. Dev Dyn. 2006;235:3413–22.
29. Sun JF, Phung T, Shiojima I, Felske T, Upalakalin JN, Feng D, et al. Microvascular patterning is controlled by fine-tuning the Akt signal. Proc Natl Acad Sci USA. 2005;102:128–33.
30. Sörensen I, Adams RH, Gossler A. DLL1-mediated Notch activation regulates endothelial identity in mouse fetal arteries. Blood. 2009;113:5680–8.
31. Logan M, Martin JF, Nagy A, Lobe C, Olson EN, Tabin CJ. Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis. 2002;33:77–80.
32. Trumpp A, Depew MJ, Rubenstein JLR, Bishop JM, Martin GR. Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev. 1999;13:3136–48.
33. Yeo H, Beck LH, Thompson SR, Farach-Carson MC, McDonald JM, Clemens TL, et al. Conditional disruption of calcineurin B1 in osteoblasts increases bone formation and reduces bone resorption. J Biol Chem. 2007;282:35318–27.
34. Dacquin R, Starbuck M, Schinke T, Karsenty G. Mouse alpha1(I)-collagen promoter is the best known promoter to drive efficient Cre recombinase expression in osteoblast. Dev Dyn. 2002;224:245–51.
35. Liu F, Woitge HW, Braut A, Kronenberg MS, Lichtler AC, Mina M, et al. Expression and activity of osteoblast-targeted Cre recombinase transgenes in murine skeletal tissues. J Dev Biol. 2004;48:645–53.
36. Rodda SJ, McMahon AP. Distinct roles for hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development. 2006;133:3231–44.
37. Maes C, Kobayashi T, Kronenberg HM. A novel transgenic mouse model to study the osteoblast lineage in vivo. Ann N Y Acad Sci. 2007;1116:149–64.
38. Kalajzic I, Braut A, Guo D, Jiang X, Kronenberg MS, Mina M, et al. Dentin matrix protein 1 expression during osteoblastic differentiation, generation of an osteocyte GFP-transgene. Bone. 2004;35:74–82.
39. Lu Y, Xie Y, Zhang S, Dusevich V, Bonewald LF, Feng JQ. DMP1-targeted Cre expression in odontoblasts and osteocytes. J Dent Res. 2007;86:320–5.
40. Kühn R, Schwenk F, Aguet M, Rajewsky K. Inducible gene targeting in mice. Science. 1995;269:1427–9.
41. Georgiades P, Ogilvy S, Duval H, Licence DR, Charnock-Jones DS, Smith SK, et al. VavCre transgenic mice: a tool for mutagenesis in hematopoietic and endothelial lineages. Genesis. 2002;34:251–6.
42. de Boer J, Williams A, Skavdis G, Harker N, Coles M, Tolaini M, et al. Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur J Immunol. 2003;33:314–25.
43. Croker BA, Metcalf D, Robb L, Wei W, Mifsud S, DiRago L, et al. SOCS3 is a critical physiological negative regulator of G-CSF signaling and emergency granulopoiesis. Immunity. 2004;20:153–65.
44. Göthert JR, Gustin SE, Hall MA, Green AR, Göttgens B, Izon DJ, et al. In vivo fate-tracing studies using the Scl stem cell enhancer: embryonic hematopoietic stem cells significantly contribute to adult hematopoiesis. Blood. 2005;105:2724–32.
45. d hematopoietic progenitors are deficient in situ. Exp Hematol. 1994;22:174–7.
46. Tokoyoda K, Egawa T, Sugiyama T, Choi B-I, Nagasawa T. Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity. 2004;20:707–18.
47. Nagasawa T, Omatsu Y, Sugiyama T. Control of hematopoietic stem cells by the bone marrow stromal niche: the role of reticular cells. Trends Immunol. 2011;32(7):315–20.
48. Ding L, Morrison SJ. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature. 2013;495(7440):231–5.
49. Greenbaum A, Hsu Y-MS, Day RB, Schuettpelz LG, Christopher MJ, Borgerding JN, et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature. 2013;495:227–30.
50. Decotto E, Spradling AC. The Drosophila ovarian and testis stem cell niches: similar somatic stem cells and signals. Dev Cell. 2005;9:501–10.
51. Pan L, Chen S, Weng C, Call G, Zhu D, Tang H, et al. Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell Stem Cell. 2007;1:458–69.
52. Boyle M, Wong C, Rocha M, Jones DL. Decline in self-renewal factors contributes to aging of the stem cell niche in the Drosophila testis. Cell Stem Cell. 2007;1:470–8.
53. de Cuevas M, Matunis EL. The stem cell niche: lessons from the Drosophila testis. Development. 2011;138:2861–9.
54. Toledano H, D’Alterio C, Czech B, Levine E, Jones DL. The let-7-Imp axis regulates ageing of the Drosophila testis stem-cell niche. Nature. 2012;485:605–10.
55. Boyle M, Wong C, Rocha M, Jones DL. Decline in self-renewal factors contributes to aging of the stem cell niche in the Drosophila testis. Cell Stem Cell. 2007;1:470–8.
56. Doetsch F. A niche for adult neural stem cells. Curr Opin Genet Dev. 2003;13:543–50.
57. Ramírez-Castillejo C, Sánchez-Sánchez F, Andreu-Agulló C, Ferrón SR, Aroca-Aguilar JD, Sánchez P, et al. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci. 2006;9:331–9.
58. Sii-Felice K, Etienne O, Hoffschir F, Mathieu C, Riou L, Barroca V, et al. Fanconi DNA repair pathway is required for survival and long-term maintenance of neural progenitors. EMBO J. 2008;27:770–81.
59. Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci. 2004;24:8354–65.
60. Pineda JR, Daynac M, Chicheportiche A, Cebrian-Silla A, Sii K, Felice, Garcia-Verdugo JM, et al. Vascular-derived TGF-β increases in the stem cell niche and perturbs neurogenesis during aging and following irradiation in the adult mouse brain. EMBO Mol Med. 2013;5:548–62.
61. I.M. Conboy, M.J. Conboy, G.M. Smythe, T.A. Rando, Notch-mediated restoration of regenerative potential to aged muscle., Science (New York, N.Y.). 302 (2003) 1575–7.
62. Carlson ME, Conboy MJ, Hsu M, Barchas L, Jeong J, Agrawal A, et al. Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell. 2009;8:676–89.
63. Conboy MJ, Conboy IM, Rando TA, Service N, Alto P. Heterochromatic parabiosis: historical perspective and methodological considerations for studies of aging and longevity. Aging Cell. 2013;12(3):525–30.
64. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature. 2005;433:760–4.
65. Carlson ME, Conboy IM. Loss of stem cell regenerative capacity within aged niches. Aging Cell. 2007;6:371–82.
66. Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M, Bieri G, et al. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature. 2011;477:90–4.
67. Ruckh JM, Zhao J-W, Shadrach JL, van Wijngaarden P, Rao TN, Wagers AJ, et al. Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell. 2012;10:96–103.
68. Wagner W, Horn P, Bork S, Ho AD. Aging of hematopoietic stem cells is regulated by the stem cell niche. Exp Gerontol. 2008;43:974–80.
69. Tokalov SV, Grüner S, Schindler S, Wolf G, Baumann M, Abolmaali N. Age-related changes in the frequency of mesenchymal stem cells in the bone marrow of rats. Stem Cells Dev. 2007;16:439–46.
70. Bellantuono I, Aldahmash A, Kassem M. Aging of marrow stromal (skeletal) stem cells and their contribution to age-related bone loss. Biochim Biophys Acta. 2009;1792:364–70.
71. Stenderup K. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone. 2003;33:919–26.
72. Yvan-Charvet L, Pagler T, Gautier EL, Avagyan S, Siry RL, Han S, et al. ATP-binding cassette transporters and HDL suppress hematopoietic stem cell proliferation. Science. 2010;328:1689–93.
73. Omatsu Y, Seike M, Sugiyama T, Kume T, Nagasawa T. Foxc1 is a critical regulator of haematopoietic stem/progenitor cell niche formation. Nature. 2014;508(7497):536–40.
74. Hotta T, Hirabayashi N, Utsumi M, Murate T, Yamada H. Age-related changes in the function of hemopoietic stroma in mice. Exp Hematol. 1980;8:933–6.
75. Liang Y, Van Zant G, Szilvassy SJ. Effects of aging on the homing and engraftment of murine hematopoietic stem and progenitor cells. Blood. 2005;106:1479–87.
76. Rossi DJ, Bryder D, Zahn JM, Ahlenius H, Sonu R, Wagers AJ, et al. Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci USA. 2005;102:9194–9.
77. Li F, Jin F, Freitas A, Szabo P, Weksler ME. Impaired regeneration of the peripheral B cell repertoire from bone marrow following lymphopenia in old mice. Eur J Immunol. 2001;31:500–5.
78. Zhu X, Gui J, Dohkan J, Cheng L, Barnes PF, Su D-M. Lymphohematopoietic progenitors do not have a synchronized defect with age-related thymic involution. Aging Cell. 2007;6:663–72.
79. Miller PH, Knapp DJHF, Eaves CJ. Heterogeneity in hematopoietic stem cell populations: implications for transplantation. Curr Opin Hematol. 2013;20:257–64.
80. Köhler A, Schmithorst V, Filippi M-D, Ryan MA, Daria D, Gunzer M, et al. Altered cellular dynamics and endosteal location of aged early hematopoietic progenitor cells revealed by time-lapse intravital imaging in long bones. Blood. 2009;114:290–8.
81. Florian MC, Dörr K, Niebel A, Daria D, Schrezenmeier H, Rojewski M, et al. Cdc42 activity regulates hematopoietic stem cell aging and rejuvenation. Cell Stem Cell. 2012;10:520–30.
82. Baxter MA, Wynn RF, Jowitt SN, Wraith JE, Fairbairn LJ, Bellantuono I. Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells. 2004;22:675–82.
83. Ju Z, Jiang H, Jaworski M, Rathinam C, Gompf A, Klein C, et al. Telomere dysfunction induces environmental alterations limiting hematopoietic stem cell function and engraftment. Nat Med. 2007;13:742–7.
84. Geiger H, Koehler A, Gunzer M. Stem cells, aging, niche, adhesion and Cdc42: a model for changes in cell–cell interactions and hematopoietic stem cell aging. Cell Cycle. 2007;6:884–7.
85. Wang L, Yang L, Debidda M, Witte D, Zheng Y. Cdc42 GTPase-activating protein deficiency promotes genomic instability and premature aging-like phenotypes. Proc Natl Acad Sci USA. 2007;104:1248–53.
86. Stolzing A, Jones E, McGonagle D, Scutt A. Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev. 2008;129:163–73.
87. Pattappa G, Thorpe SD, Jegard NC, Heywood HK, de Bruijn JD, Lee DA. Continuous and uninterrupted oxygen tension influences the colony formation and oxidative metabolism of human mesenchymal stem cells. Tissue Eng Part C Methods. 2013;19:68–79.
88. Pozotrigo M, Adel N, Landau H, Lesokhin A, Lendvai N, Chung DJ, et al. Factors impacting stem cell mobilization failure rate and efficiency in multiple myeloma in the era of novel therapies: experience at Memorial Sloan Kettering Cancer Center. Bone Marrow Transpl. 2013;48:1033–9.
89. Morris CL, Siegel E, Barlogie B, Cottler-Fox M, Lin P, Fassas A, et al. Mobilization of CD34+ cells in elderly patients (>/= 70 years) with multiple myeloma: influence of age, prior therapy, platelet count and mobilization regimen. Br J Haematol. 2003;120:413–23.
90. Verovskaya E, Broekhuis MJC, Zwart E, Weersing E, Ritsema M, Bosman LJ, et al. Asymmetry in skeletal distribution of mouse hematopoietic stem cell clones and their equilibration by mobilizing cytokines. J Exp Med. 2014;211:487–97.
91. Huntly BJP, Gilliland DG. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat Rev Cancer. 2005;5:311–21.
92. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367:645–8.
93. Lane SW, Scadden DT, Gilliland DG. The leukemic stem cell niche: current concepts and therapeutic opportunities. Blood. 2009;114:1150–7.
94. Walkley CR, Olsen GH, Dworkin S, Fabb SA, Swann J, McArthur GA, et al. A microenvironment-induced myeloproliferative syndrome caused by retinoic acid receptor gamma deficiency. Cell. 2007;129:1097–110.
95. Walkley CR, Shea JM, Sims NA, Purton LE, Orkin SH. Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell. 2007;129:1081–95.
96. Raaijmakers MHGP, Mukherjee S, Guo S, Zhang S, Kobayashi T, Schoonmaker JA, et al. Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature. 2010;464:852–7.
97. Raaijmakers MH. Myelodysplastic syndromes: revisiting the role of the bone marrow microenvironment in disease pathogenesis. Int J Hematol. 2012;95:17–25.
98. Kode A, Manavalan JS, Mosialou I, Bhagat G, Rathinam CV, Luo N, et al. Leukaemogenesis induced by an activating β-catenin mutation in osteoblasts. Nature. 2014;506:240–4.
99. Schepers K, Pietras EM, Reynaud D, Flach J, Binnewies M, Garg T, et al. Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell Stem Cell. 2013;13:285–99.
100. Hamaker ME, Prins MC, Stauder R. The relevance of a geriatric assessment for elderly patients with a haematological malignancy––a systematic review. Leuk Res. 2014;38:275–83.
101. Rossi DJ, Bryder D, Seita J, Nussenzweig A, Hoeijmakers J, Weissman IL. Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature. 2007;447:725–9.
102. Vas V, Senger K, Dörr K, Niebel A, Geiger H. Aging of the microenvironment influences clonality in hematopoiesis. PLoS ONE. 2012;7:e42080.
103. Vas V, Wandhoff C, Dörr K, Niebel A, Geiger H. Contribution of an aged microenvironment to aging-associated myeloproliferative disease. PLoS ONE. 2012;7:e31523.