Regulation of hematopoiesis by activators and inhibitors of Wnt signaling from the niche

Annals of the New York Academy of Sciences

Volumn 1310, Issue 1, 2014, Pages 32-43

  Schreck, Christina ^a   Bock, Franziska ^a   Grziwok, Sandra ^a   Oostendorp, Robert A J ^a   Istvánffy, Rouzanna ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Catenin; Hematopoietic stem cell; Microenvironment; Niche; Stroma; Wnt

Indexed keywords

DICKKOPF 1 PROTEIN; SECRETED FRIZZLED RELATED PROTEIN 1; WNT PROTEIN;

ARTICLE; CANCER CELL; CELL DISRUPTION; CELL FUNCTION; ENVIRONMENTAL FACTOR; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; HUMAN; LEUKEMIA; LEUKEMOGENESIS; MALIGNANT TRANSFORMATION; NONHUMAN; PROGENY; STEM CELL NICHE; STROMA CELL; WNT SIGNALING PATHWAY;

CATENIN; HEMATOPOIETIC STEM CELL; MICROENVIRONMENT; NICHE; STROMA; WNT;

ADULT; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION; HEMATOPOIESIS; HUMANS; LEUKEMIA; LIGANDS; STEM CELL NICHE; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84896300806     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/nyas.12384     Document Type: Article

References (120)

1. Ikuta, K. & I.L. Weissman. 1992. Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc. Natl. Acad. Sci. U S A 89: 1502-1506.
2. Mao, B. et al. 2002. Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signalling. Nature 417: 664-667.
3. Jamieson, C.H. et al. 2004. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N. Engl. J. Med. 351: 657-667.
4. Osawa, M. et al. 1996. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273: 242-245.
5. Christensen, J.L. & I.L. Weissman. 2001. Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc. Natl. Acad. Sci. USA 98: 14541-14546.
6. Kiel, M.J. et al. 2005. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121: 1109-1121.
7. Balazs, A.B. et al. 2006. Endothelial protein C receptor (CD201) explicitly identifies hematopoietic stem cells in murine bone marrow. Blood 107: 2317-2321.
8. Kent, D.G. et al. 2009. Prospective isolation and molecular characterization of hematopoietic stem cells with durable self-renewal potential. Blood 113: 6342-6350.
9. Morita, Y., H. Ema & H. Nakauchi. 2010. Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment. J. Exp. Med. 207: 1173-1182.
10. Dykstra, B. et al. 2007. Long-term propagation of distinct hematopoietic differentiation programs in vivo. Cell Stem. Cell 1: 218-229.
11. Benz, C. et al. 2012. Hematopoietic stem cell subtypes expand differentially during development and display distinct lymphopoietic programs. Cell Stem. Cell 10: 273-283.
12. Renstrom, J. et al. 2010. How the niche regulates hematopoietic stem cells. Chem. Biol. Interact. 184: 7-15.
13. Kondo, M., I.L. Weissman & K. Akashi. 1997. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91: 661-672.
14. Schofield, R. 1978. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4: 7-25.
15. Fuchs, E., T. Tumbar & G. Guasch. 2004. Socializing with the neighbors: stem cells and their niche. Cell 116: 769-778.
16. Morrison, S.J. & A.C. Spradling. 2008. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132: 598-611.
17. Garrett, R.W. & S.G. Emerson. 2009. Bone and blood vessels: the hard and the soft of hematopoietic stem cell niches. Cell Stem. Cell 4: 503-506.
18. Nagasawa, T., Y. Omatsu & T. Sugiyama. 2011. Control of hematopoietic stem cells by the bone marrow stromal niche: the role of reticular cells. Trends Immunol. 32: 315-320.
19. Frassoni, F., N.G. Testa & B.I. Lord. 1982. The relative spatial distribution of erythroid progenitor cells (BFUe and CFUe) in the normal mouse femur. Cell Tissue Kinet. 15: 447-455.
20. Calvi, L.M. et al. 2003. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425: 841-846.
21. Zhang, J. et al. 2003. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425: 836-841.
22. Lo Celso, C. et al. 2009. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 457: 92-96.
23. Xie, Y. et al. 2009. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 457: 97-101.
24. Kieslinger, M. et al. 2010. Early B cell factor 2 regulates hematopoietic stem cell homeostasis in a cell-nonautonomous manner. Cell Stem. Cell 7: 496-507.
25. Mendez-Ferrer, S. et al. 2010. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466: 829-834.
26. Sugiyama, T. et al. 2006. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25: 977-988.
27. Ding, L. et al. 2012. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481: 457-462.
28. Yamazaki, S. et al. 2011. Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147: 1146-1158.
29. Frenette, P.S. et al. 2013. Mesenchymal stem cell: keystone of the hematopoietic stem cell niche and a stepping-stone for regenerative medicine. Annu. Rev. Immunol. 31: 285-316.
30. Nakamura, Y. et al. 2010. Isolation and characterization of endosteal niche cell populations that regulate hematopoietic stem cells. Blood 116: 1422-1432.
31. Chan, C.K. et al. 2013. Clonal precursor of bone, cartilage, and hematopoietic niche stromal cells. Proc. Natl. Acad. Sci. USA 110: 12643-12648.
32. Morikawa, S. et al. 2009. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J. Exp. Med. 206: 2483-2496.
33. Pinho, S. et al. 2013. PDGFRalpha and CD51 mark human nestin+ sphere-forming mesenchymal stem cells capable of hematopoietic progenitor cell expansion. J. Exp. Med. 210: 1351-1367.
34. Kiel, M.J. & S.J. Morrison. 2008. Uncertainty in the niches that maintain haematopoietic stem cells. Nat. Rev. Immunol 8: 290-301.
35. Ma, Y.D. et al. 2009. Defects in osteoblast function but no changes in long-term repopulating potential of hematopoietic stem cells in a mouse chronic inflammatory arthritis model. Blood 114: 4402-4410.
36. Kiel, M.J., G.L. Radice & S.J. Morrison. 2007. Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance. Cell Stem. Cell 1: 204-217.
37. Salter, A.B. et al. 2009. Endothelial progenitor cell infusion induces hematopoietic stem cell reconstitution in vivo. Blood 113: 2104-2107.
38. Li, B. et al. 2010. Endothelial cells mediate the regeneration of hematopoietic stem cells. Stem. Cell. Res. 4: 17-24.
39. Kiel, M.J. et al. 2009. Hematopoietic stem cells do not depend on N-cadherin to regulate their maintenance. Cell Stem. Cell 4: 170-179.
40. Winkler, I.G. et al. 2012. Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat. Med. 18: 1651-1657.
41. Wilson, A. et al. 2008. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135: 1118-1129.
42. Barker, J.E. 1997. Early transplantation to a normal microenvironment prevents the development of steel hematopoietic stem cell defects. Exp. Hematol. 25: 542-547.
43. Waskow, C. et al. 2009. Hematopoietic stem cell transplantation without irradiation. Nat. Methods 6: 267-269.
44. Waskow, C. et al. 2002. Viable c-Kit(W/W) mutants reveal pivotal role for c-kit in the maintenance of lymphopoiesis. Immunity 17: 277-288.
45. Tzeng, Y.S. et al. 2011. Loss of Cxcl12/Sdf-1 in adult mice decreases the quiescent state of hematopoietic stem/progenitor cells and alters the pattern of hematopoietic regeneration after myelosuppression. Blood 117: 429-439.
46. Ma, Q. et al. 1998. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. USA 95: 9448-9453.
47. Zou, Y.R. et al. 1998. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393: 595-599.
48. Ma, Q., D. Jones & T.A. Springer. 1999. The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 10: 463-471.
49. Tsai, J.J. et al. 2013. Nrf2 regulates haematopoietic stem cell function. Nat. Cell Biol. 15: 309-316.
50. Grundler, R. et al. 2009. Dissection of PIM serine/threonine kinases in FLT3-ITD-induced leukemogenesis reveals PIM1 as regulator of CXCL12-CXCR4-mediated homing and migration. J. Exp. Med. 206: 1957-1970.
51. Goldman, D.C. et al. 2009. BMP4 regulates the hematopoietic stem cell niche. Blood 114: 4393-4401.
52. Fleming, H.E. et al. 2008. Wnt signaling in the niche enforces hematopoietic stem cell quiescence and is necessary to preserve self-renewal in vivo. Cell Stem. Cell 2: 274-283.
53. Istvanffy, R. et al. 2011. Stromal pleiotrophin regulates repopulation behavior of hematopoietic stem cells. Blood 118: 2712-2722.
54. Renstrom, J. et al. 2009. Secreted frizzled-related protein 1 extrinsically regulates cycling activity and maintenance of hematopoietic stem cells. Cell Stem. Cell 5: 157-167.
55. Qian, H. et al. 2007. Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem. Cell 1: 671-684.
56. Raaijmakers, M.H. et al. 2010. Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature 464: 852-857.
57. Hazen, A.L. et al. 2009. SHIP is required for a functional hematopoietic stem cell niche. Blood 113: 2924-2933.
58. Walkley, C.R. et al. 2007. Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell 129: 1081-1095.
59. Sesler, C.L. & M. Zayzafoon 2013. NFAT signaling in osteoblasts regulates the hematopoietic niche in the bone microenvironment. Clin. Dev. Immunol. 2013: 107321.
60. Baksh, D., G.M. Boland & R.S. Tuan. 2007. Cross-talk between Wnt signaling pathways in human mesenchymal stem cells leads to functional antagonism during osteogenic differentiation. J. Cell Biochem. 101: 1109-1124.
61. Yamane, T. et al. 2001. Wnt signaling regulates hemopoiesis through stromal cells. J. Immunol. 167: 765-772.
62. Wodarz, A. & R. Nusse. 1998. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14: 59-88.
63. Austin, T.W. et al. 1997. A role for the Wnt gene family in hematopoiesis: expansion of multilineage progenitor cells. Blood 89: 3624-3635.
64. Van Den Berg, D.J. et al. 1998. Role of members of the Wnt gene family in human hematopoiesis. Blood 92: 3189-3202.
65. MacDonald, B.T., K. Tamai & X. He. 2009. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17: 9-26.
66. Cobas, M. et al. 2004. Beta-catenin is dispensable for hematopoiesis and lymphopoiesis. J. Exp. Med. 199: 221-229.
67. Jeannet, G. et al. 2008. Long-term, multilineage hematopoiesis occurs in the combined absence of beta-catenin and gamma-catenin. Blood 111: 142-149.
68. Koch, U. et al. 2008. Simultaneous loss of beta- and gamma-catenin does not perturb hematopoiesis or lymphopoiesis. Blood 111: 160-164.
69. Kirstetter, P. et al. 2006. Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multilineage differentiation block. Nat. Immunol. 7: 1048-1056.
70. Luis, T.C. et al. 2011. Canonical wnt signaling regulates hematopoiesis in a dosage-dependent fashion. Cell Stem. Cell 9: 345-356.
71. Takada, S. et al. 1994. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes. Dev. 8: 174-189.
72. Luis, T.C. et al. 2009. Wnt3a deficiency irreversibly impairs hematopoietic stem cell self-renewal and leads to defects in progenitor cell differentiation. Blood 113: 546-554.
73. Veeman, M.T., J.D. Axelrod & R.T. Moon. 2003. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 5: 367-377.
74. Buckley, S.M. et al. 2011. Maintenance of HSC by Wnt5a secreting AGM-derived stromal cell line. Exp. Hematol. 39: 114-123 e111-e115.
75. Florian, M.C. et al. 2013. A canonical to non-canonical Wnt signalling switch in haematopoietic stem-cell ageing. Nature 503: 392-396.
76. Yamaguchi, T.P. et al. 1999. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126: 1211-1223.
77. Liang, H. et al. 2003. Wnt5a inhibits B cell proliferation and functions as a tumor suppressor in hematopoietic tissue. Cancer Cell 4: 349-360.
78. Reya, T. et al. 2000. Wnt signaling regulates B lymphocyte proliferation through a LEF-1 dependent mechanism. Immunity 13: 15-24.
79. Maeda, K. et al. 2012. Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis. Nat. Med. 18: 405-412.
80. Nemeth, M.J. et al. 2007. Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation. Proc. Natl. Acad. Sci. USA 104: 15436-15441.
81. Ghosh, M.C. et al. 2009. Activation of Wnt5A signaling is required for CXC chemokine ligand 12-mediated T-cell migration. Blood 114: 1366-1373.
82. Kuhl, M. et al. 2000. The Wnt/Ca2 +pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet. 16: 279-283.
83. Florian, M.C. et al. 2012. Cdc42 activity regulates hematopoietic stem cell aging and rejuvenation. Cell Stem. Cell 10: 520-530.
84. Halford, M.M. et al. 2013. A fully human inhibitory monoclonal antibody to the Wnt receptor RYK. PLoS One 8: e75447.
85. van Amerongen, R., A. Mikels & R. Nusse. 2008. Alternative wnt signaling is initiated by distinct receptors. Sci. Signal 1: re9.
86. Povinelli, B.J. & M.J. Nemeth. 2013. Wnt5a regulates hematopoietic stem cell proliferation and repopulation through the Ryk receptor. Stem Cells 32: 105-115.
87. Cruciat, C.M. & C. Niehrs. 2013. Secreted and transmembrane wnt inhibitors and activators. Cold Spring Harb. Perspect. Biol. 5: a015081.
88. Kawano, Y. & R. Kypta. 2003. Secreted antagonists of the Wnt signalling pathway. J. Cell Sci. 116: 2627-2634.
89. Suzuki, H. et al. 2004. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat. Genet. 36: 417-422.
90. Kele, J. et al. 2012. SFRP1 and SFRP2 dose-dependently regulate midbrain dopamine neuron development in vivo and in embryonic stem cells. Stem. Cells 30: 865-875.
91. Satoh, W. et al. 2006. Sfrp1 and Sfrp2 regulate anteroposterior axis elongation and somite segmentation during mouse embryogenesis. Development 133: 989-999.
92. Satoh, W. et al. 2008. Sfrp1, Sfrp2, and Sfrp5 regulate the Wnt/beta-catenin and the planar cell polarity pathways during early trunk formation in mouse. Genesis 46: 92-103.
93. Warr, N. et al. 2009. Sfrp1 and Sfrp2 are required for normal male sexual development in mice. Dev. Biol. 326: 273-284.
94. Roux, S. 2010. New treatment targets in osteoporosis. Joint Bone Spine 77: 222-228.
95. Nakajima, H. et al. 2009. Wnt modulators, SFRP-1, and SFRP-2 are expressed in osteoblasts and differentially regulate hematopoietic stem cells. Biochem. Biophys. Res. Commun. 390: 65-70.
96. Mao, J. et al. 2001. Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol. Cell 7: 801-809.
97. Surmann-Schmitt, C. et al. 2009. Wif-1 is expressed at cartilage-mesenchyme interfaces and impedes Wnt3a-mediated inhibition of chondrogenesis. J. Cell Sci. 122: 3627-3637.
98. Malinauskas, T. et al. 2011. Modular mechanism of Wnt signaling inhibition by Wnt inhibitory factor 1. Nat. Struct. Mol. Biol. 18: 886-893.
99. Schaniel, C. et al. 2011. Wnt-inhibitory factor 1 dysregulation of the bone marrow niche exhausts hematopoietic stem cells. Blood 118: 2420-2429.
100. Colmone, A. et al. 2008. Leukemic cells create bone marrow niches that disrupt the behavior of normal hematopoietic progenitor cells. Science 322: 1861-1865.
101. Huan, J. et al. 2013. RNA trafficking by acute myelogenous leukemia exosomes. Cancer Res. 73: 918-929.
102. Lutzny, G. et al. 2013. Protein kinase c-beta-dependent activation of NF-kappaB in stromal cells is indispensable for the survival of chronic lymphocytic leukemia B cells in vivo. Cancer Cell 23: 77-92.
103. Geyh, S. et al. 2013. Insufficient stromal support in MDS results from molecular and functional deficits of mesenchymal stromal cells. Leukemia 27: 1841-1851.
104. Frisch, B.J. et al. 2012. Functional inhibition of osteoblastic cells in an in vivo mouse model of myeloid leukemia. Blood 119: 540-550.
105. Schepers, K. et al. 2013. Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell Stem. Cell 13: 285-299.
106. Rupec, R.A. et al. 2005. Stroma-mediated dysregulation of myelopoiesis in mice lacking I kappa B alpha. Immunity 22: 479-491.
107. Tickenbrock, L. et al. 2005. Flt3 tandem duplication mutations cooperate with Wnt signaling in leukemic signal transduction. Blood 105: 3699-3706.
108. Simon, M. et al. 2005. Constitutive activation of the Wnt/beta-catenin signalling pathway in acute myeloid leukaemia. Oncogene 24: 2410-2420.
109. Wang, Y. et al. 2010. The Wnt/beta-catenin pathway is required for the development of leukemia stem cells in AML. Science 327: 1650-1653.
110. Zhao, C. et al. 2007. Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell 12: 528-541.
111. Abrahamsson, A.E. et al. 2009. Glycogen synthase kinase 3beta missplicing contributes to leukemia stem cell generation. Proc. Natl. Acad. Sci. USA 106: 3925-3929.
112. Chen, R. et al. 2013. Ubiquitin-mediated interaction of p210 BCR/ABL with beta-catenin supports disease progression in a murine model for chronic myelogenous leukemia. Blood 122: 2114-2124.
113. Wang, Y., X.X. Zhu & C.S. Zhu. 2013. [Abnormal methylation patterns of SFRP1 gene in cells of leukemia and inhibitation of arsenie trioxide on the SFRP1 gene]. Zhonghua Xue. Ye. Xue. Za. Zhi. 34: 157-159.
114. Filipovich, A. et al. 2010. Evidence for non-functional Dickkopf-1 (DKK-1) signaling in chronic lymphocytic leukemia (CLL). Eur. J. Haematol. 85: 309-313.
115. Moskalev, E.A. et al. 2012. Concurrent epigenetic silencing of wnt/beta-catenin pathway inhibitor genes in B cell chronic lymphocytic leukaemia. BMC Cancer 12: 213.
116. Hou, H.A. et al. 2011. Distinct association between aberrant methylation of Wnt inhibitors and genetic alterations in acute myeloid leukaemia. Br. J. Cancer 105: 1927-1933.
117. Cheng, C.K. et al. 2011. Secreted-frizzled related protein 1 is a transcriptional repression target of the t(8;21) fusion protein in acute myeloid leukemia. Blood 118: 6638-6648.
118. Krause, D.S. et al. 2013. Differential regulation of myeloid leukemias by the bone marrow microenvironment. Nat. Med. 19: 1513-1517.
119. Ehninger, A. & A. Trumpp. 2011. The bone marrow stem cell niche grows up: mesenchymal stem cells and macrophages move in. J. Exp. Med. 208: 421-428.
120. Kunisaki, Y. et al. 2013. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502: 637-643.