Regulation of hematopoietic stem cells in the niche

Science China Life Sciences

Volumn 58, Issue 12, 2015, Pages 1209-1215

  Zhao, Meng ^a   Li, LinHeng ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

hematopoietic stem cells; niche; regeneration

Indexed keywords

ANIMAL; BONE MARROW CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; STEM CELL NICHE;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; SIGNAL TRANSDUCTION; STEM CELL NICHE;

EID: 84949313491     PISSN: 16747305     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11427-015-4960-y     Document Type: Review

References (81)

1. 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
2. Siminovitch L, McCulloch EA, Till JE. The distribution of colony-forming cells among spleen colonies. J Cell Physiol, 1963, 62: 327–336
3. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells, 1978, 4: 7–25
4. Dexter TM, Allen TD, Lajtha LG. Conditions controlling the proliferation of haemopoietic stem cells in vitro. J Cell Physiol, 1977, 91: 335–344
5. Taichman RS, Emerson SG. Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med, 1994, 179: 1677–1682
6. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, Milner LA, Kronenberg HM, Scadden DT. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature, 2003, 425: 841–846
7. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, Harris S, Wiedemann LM, Mishina Y, Li L. Identification of the haematopoietic stem cell niche and control of the niche size. Nature, 2003, 425: 836–841
8. Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ. Slam family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell, 2005, 121: 1109–1121
9. Morrison SJ, Scadden DT. The bone marrow niche for haematopoietic stem cells. Nature, 2014, 505: 327–334
10. Mendez-Ferrer S, Scadden DT, Sanchez-Aguilera A. Bone marrow stem cells: current and emerging concepts. Ann N Y Acad Sci, 2015, 1335: 32–44
11. Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W, Jaworski M, Offner S, Dunant CF, Eshkind L, Bockamp E, Lio P, Macdonald HR, Trumpp A. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell, 2008, 135: 1118–1129
12. Cheng T, Rodrigues N, Shen H, Yang Y, Dombkowski D, Sykes M, Scadden DT. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science, 2000, 287: 1804–1808
13. Ogawa M. Differentiation and proliferation of hematopoietic stem cells. Blood, 1993, 81: 2844–2853
14. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh GY, Suda T. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell, 2004, 118: 149–161
15. Sugimura R, He XC, Venkatraman A, Arai F, Box A, Semerad C, Haug JS, Peng L, Zhong XB, Suda T, Li L. Noncanonical wnt signaling maintains hematopoietic stem cells in the niche. Cell, 2012, 150: 351–365
16. Foudi A, Hochedlinger K, Van Buren D, Schindler JW, Jaenisch R, Carey V, Hock H. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol, 2008, 27: 84–90
17. Sprent J, Tough DF. Lymphocyte life-span and memory. Science, 1994, 265: 1395–1400
18. Xie Y, Yin T, Wiegraebe W, He XC, Miller D, Stark D, Perko K, Alexander R, Schwartz J, Grindley JC, Park J, Haug JS, Wunderlich JP, Li H, Zhang S, Johnson T, Feldman RA, Li L. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature, 2009, 457: 97–101
19. Lo Celso C, Fleming HE, Wu JW, Zhao CX, Miake-Lye S, Fujisaki J, Cote D, Rowe DW, Lin CP, Scadden DT. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature, 2009, 457: 92–96
20. Nombela-Arrieta C, Pivarnik G, Winkel B, Canty KJ, Harley B, Mahoney JE, Park SY, Lu J, Protopopov A, Silberstein LE. Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat Cell Biol, 2013, 15: 533–543
21. Weksberg DC, Chambers SM, Boles NC, Goodell MA. Cd150-side population cells represent a functionally distinct population of long-term hematopoietic stem cells. Blood, 2008, 111: 2444–2451
22. Kunisaki Y, Bruns I, Scheiermann C, Ahmed J, Pinho S, Zhang D, Mizoguchi T, Wei Q, Lucas D, Ito K, Mar JC, Bergman A, Frenette PS. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature, 2013, 502: 637–643
23. Bruns I, Lucas D, Pinho S, Ahmed J, Lambert MP, Kunisaki Y, Scheiermann C, Schiff L, Poncz M, Bergman A, Frenette PS. Megakaryocytes regulate hematopoietic stem cell quiescence through CXCL4 secretion. Nat Med, 2014, 20: 1315–1320
24. Zhao M, Perry JM, Marshall H, Venkatraman A, Qian P, He XC, Ahamed J, Li L. Megakaryocytes maintain homeostatic quiescence and promote post-injury regeneration of hematopoietic stem cells. Nat Med, 2014, 20: 1321–1326
25. Scadden DT. The stem-cell niche as an entity of action. Nature, 2006, 441: 1075–1079
26. Wilson A, Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol, 2006, 6: 93–106
27. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, Tesio M, Samstein RM, Goichberg P, Spiegel A, Elson A, Lapidot T. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med, 2006, 12: 657–664
28. Yoshihara H, Arai F, Hosokawa K, Hagiwara T, Takubo K, Nakamura Y, Gomei Y, Iwasaki H, Matsuoka S, Miyamoto K, Miyazaki H, Takahashi T, Suda T. Thrombopoietin/mpl signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell, 2007, 1: 685–697
29. Kent D, Copley M, Benz C, Dykstra B, Bowie M, Eaves C. Regulation of hematopoietic stem cells by the steel factor/kit signaling pathway. Clin Cancer Res, 2008, 14: 1926–1930
30. Broudy VC. Stem cell factor and hematopoiesis. Blood, 1997, 90: 1345–1364
31. Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature, 2012, 481: 457–462
32. Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, Bronson RT, Springer TA. Impaired b-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4-and SDF-1-deficient mice. Proc Natl Acad Sci USA, 1998, 95: 9448–9453
33. Levesque JP, Hendy J, Takamatsu Y, Simmons PJ, Bendall LJ. Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest, 2003, 111: 187–196
34. 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: 977–988
35. 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: 536–540
36. Ding L, Morrison SJ. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature, 2013, 495: 231–235
37. Greenbaum A, Hsu YM, Day RB, Schuettpelz LG, Christopher MJ, Borgerding JN, Nagasawa T, Link DC. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature, 2013, 495: 227–230
38. Massague J. TGFbeta signalling in context. Nat Rev, 2012, 13: 616–630
39. Yamazaki S, Iwama A, Takayanagi S, Eto K, Ema H, Nakauchi H. TGF-beta as a candidate bone marrow niche signal to induce hematopoietic stem cell hibernation. Blood, 2009, 113: 1250–1256
40. Larsson J, Blank U, Helgadottir H, Bjornsson JM, Ehinger M, Goumans MJ, Fan X, Leveen P, Karlsson S. TGF-beta signaling-deficient hematopoietic stem cells have normal self-renewal and regenerative ability in vivo despite increased proliferative capacity in vitro. Blood, 2003, 102: 3129–3135
41. Yamazaki S, Ema H, Karlsson G, Yamaguchi T, Miyoshi H, Shioda S, Taketo MM, Karlsson S, Iwama A, Nakauchi H. Nonmyelinating schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell, 2011, 147: 1146–1158
42. Zhao M, Li L. Osteoblast ablation burns out functional stem cells. Blood, 2015, 125: 2590–2591
43. Bowers M, Zhang B, Ho Y, Agarwal P, Chen CC, Bhatia R. Osteoblast ablation reduces normal long-term hematopoietic stem cell self-renewal but accelerates leukemia development. Blood, 2015, 125: 2678–2688
44. Guezguez B, Campbell CJ, Boyd AL, Karanu F, Casado FL, Di Cresce C, Collins TJ, Shapovalova Z, Xenocostas A, Bhatia M. Regional localization within the bone marrow influences the functional capacity of human HSCs. Cell Stem Cell, 2013, 13: 175–189
45. Zhou BO, Ding L, Morrison SJ. Hematopoietic stem and progenitor cells regulate the regeneration of their niche by secreting angiopoietin-1. ELife, 2015, 4: e05521
46. Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, Scadden DT, Ma’ayan A, Enikolopov GN, Frenette PS. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature, 2010, 466: 829–834
47. Zhou BO, Yue R, Murphy MM, Peyer JG, Morrison SJ. Leptin-receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow. Cell Stem Cell, 2014, 15: 154–168
48. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, Hintz L, Nusse R, Weissman IL. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature, 2003, 423: 409–414
49. Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, Yates JR, Nusse R. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature, 2003, 423: 448–452
50. Perry JM, He XC, Sugimura R, Grindley JC, Haug JS, Ding S, Li L. Cooperation between both Wnt/ta-catenin and pten/pi3k/akt signaling promotes primitive hematopoietic stem cell self-renewal and expansion. Genes Dev, 2011, 25: 1928–1942
51. Koch U, Wilson A, Cobas M, Kemler R, Macdonald HR, Radtke F. Simultaneous loss of beta-and gamma-catenin does not perturb hematopoiesis or lymphopoiesis. Blood, 2008, 111: 160–164
52. Jeannet G, Scheller M, Scarpellino L, Duboux S, Gardiol N, Back J, Kuttler F, Malanchi I, Birchmeier W, Leutz A, Huelsken J, Held W. Long-term, multilineage hematopoiesis occurs in the combined absence of {beta}-catenin and {gamma}-catenin. Blood, 2008, 111: 142–149
53. Cobas M, Wilson A, Ernst B, Mancini SJ, MacDonald HR, Kemler R, Radtke F. Beta-catenin is dispensable for hematopoiesis and lymphopoiesis. J Exp Med, 2004, 199: 221–229
54. Nemeth MJ, Topol L, Anderson SM, Yang Y, Bodine DM. Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation. Proc Natl Acad Sci USA, 2007, 104: 15436–15441
55. Lento W, Ito T, Zhao C, Harris JR, Huang W, Jiang C, Owzar K, Piryani S, Racioppi L, Chao N, Reya T. Loss of beta-catenin triggers oxidative stress and impairs hematopoietic regeneration. Genes Dev, 2014, 28: 995–1004
56. de Haan G, Weersing E, Dontje B, van Os R, Bystrykh LV, Vellenga E, Miller G. In vitro generation of long-term repopulating hematopoietic stem cells by fibroblast growth factor-1. Dev Cell, 2003, 4: 241–251
57. Zhang CC, Lodish HF. Murine hematopoietic stem cells change their surface phenotype during ex vivo expansion. Blood, 2005, 105: 4314–4320
58. Zhao M, Ross JT, Itkin T, Perry JM, Venkatraman A, Haug JS, Hembree MJ, Deng CX, Lapidot T, He XC, Li L. FGF signaling facilitates postinjury recovery of mouse hematopoietic system. Blood, 2012, 120: 1831–1842
59. Itkin T, Ludin A, Gradus B, Gur-Cohen S, Kalinkovich A, Schajnovitz A, Ovadya Y, Kollet O, Canaani J, Shezen E, Coffin DJ, Enikolopov GN, Berg T, Piacibello W, Hornstein E, Lapidot T. FGF-2 expands murine hematopoietic stem and progenitor cells via proliferation of stromal cells, c-kit activation, and CXCL12 down-regulation. Blood, 2012, 120: 1843–1855
60. Doan PL, Himburg HA, Helms K, Russell JL, Fixsen E, Quarmyne M, Harris JR, Deoliviera D, Sullivan JM, Chao NJ, Kirsch DG, Chute JP. Epidermal growth factor regulates hematopoietic regeneration after radiation injury. Nat Med, 2013, 19: 295–304
61. Winkler IG, Barbier V, Nowlan B, Jacobsen RN, Forristal CE, Patton JT, Magnani JL, Levesque JP. Vascular niche e-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat Med, 2012, 18: 1651–1657
62. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci USA, 2007, 104: 5431–5436
63. Simsek T, Kocabas F, Zheng J, Deberardinis RJ, Mahmoud AI, Olson EN, Schneider JW, Zhang CC, Sadek HA. The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell, 2010, 7: 380–390
64. Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, Shima H, Johnson RS, Hirao A, Suematsu M, Suda T. Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell, 2010, 7: 391–402
65. Spencer JA, Ferraro F, Roussakis E, Klein A, Wu J, Runnels JM, Zaher W, Mortensen LJ, Alt C, Turcotte R, Yusuf R, Cote D, Vinogradov SA, Scadden DT, Lin CP. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature, 2014, 508: 269–273
66. Nakamura-Ishizu A, Takubo K, Fujioka M, Suda T. Megakaryocytes are essential for HSC quiescence through the production of thrombopoietin. Biochem Biophys Res Commun, 2014, 454: 353–357
67. Heazlewood SY, Neaves RJ, Williams B, Haylock DN, Adams TE, Nilsson SK. Megakaryocytes co-localise with hemopoietic stem cells and release cytokines that up-regulate stem cell proliferation. Stem Cell Res, 2013, 11: 782–792
68. Blank U, Karlsson S. TGF-beta signaling in the control of hematopoietic stem cells. Blood, 2015, 125: 3542–3550
69. Schepers K, Campbell TB, Passegue E. Normal and leukemic stem cell niches: insights and therapeutic opportunities. Cell Stem Cell, 2015, 16: 254–267
70. Wang JF, Liu ZY, Groopman JE. The alpha-chemokine receptor CXCR4 is expressed on the megakaryocytic lineage from progenitor to platelets and modulates migration and adhesion. Blood, 1998, 92: 756–764
71. Hamada T, Mohle R, Hesselgesser J, Hoxie J, Nachman RL, Moore MA, Rafii S. Transendothelial migration of megakaryocytes in response to stromal cell-derived factor 1 (SDF-1) enhances platelet formation. J Exp Med, 1998, 188: 539–548
72. Avecilla ST, Hattori K, Heissig B, Tejada R, Liao F, Shido K, Jin DK, Dias S, Zhang F, Hartman TE, Hackett NR, Crystal RG, Witte L, Hicklin DJ, Bohlen P, Eaton D, Lyden D, de Sauvage F, Rafii S. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med, 2004, 10: 64–71
73. Mohle R, Green D, Moore MA, Nachman RL, Rafii S. Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets. Proc Natl Acad Sci USA, 1997, 94: 663–668
74. Varner JA. The sticky truth about angiogenesis and thrombospondins. J Clin Invest, 2006, 116: 3111–3113
75. Kopp HG, Hooper AT, Broekman MJ, Avecilla ST, Petit I, Luo M, Milde T, Ramos CA, Zhang F, Kopp T, Bornstein P, Jin DK, Marcus AJ, Rafii S. Thrombospondins deployed by thrombopoietic cells determine angiogenic switch and extent of revascularization. J Clin Invest, 2006, 116: 3277–3291
76. Hooper AT, Butler JM, Nolan DJ, Kranz A, Iida K, Kobayashi M, Kopp HG, Shido K, Petit I, Yanger K, James D, Witte L, Zhu Z, Wu Y, Pytowski B, Rosenwaks Z, Mittal V, Sato TN, Rafii S. Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells. Cell Stem Cell, 2009, 4: 263–274
77. Jiang Y, Bonig H, Ulyanova T, Chang K, Papayannopoulou T. On the adaptation of endosteal stem cell niche function in response to stress. Blood, 2009, 114: 3773–3782
78. Ciovacco WA, Cheng YH, Horowitz MC, Kacena MA. Immature and mature megakaryocytes enhance osteoblast proliferation and inhibit osteoclast formation. J Cell Biochem, 2010, 109: 774–781
79. Beeton CA, Bord S, Ireland D, Compston JE. Osteoclast formation and bone resorption are inhibited by megakaryocytes. Bone, 2006, 39: 985–990
80. Olson TS, Caselli A, Otsuru S, Hofmann TJ, Williams R, Paolucci P, Dominici M, Horwitz EM. Megakaryocytes promote murine osteoblastic hsc niche expansion and stem cell engraftment after radioablative conditioning. Blood, 2013, 121: 5238–5249
81. Dominici M, Rasini V, Bussolari R, Chen X, Hofmann TJ, Spano C, Bernabei D, Veronesi E, Bertoni F, Paolucci P, Conte P, Horwitz EM. Restoration and reversible expansion of the osteoblastic hematopoietic stem cell niche after marrow radioablation. Blood, 2009, 114: 2333–2343