Cooperation between both Wnt/β-catenin and PTEN/PI3k/Akt signaling promotes primitive hematopoietic stem cell self-renewal and expansion

Genes and Development

Volumn 25, Issue 18, 2011, Pages 1928-1942

  Perry, John M ^a   He, Xi C ^a   Sugimura, Ryohichi ^a   Grindley, Justin C ^a,d   Haug, Jeffrey S ^a   Ding, Sheng ^b   Li, Linheng ^a,c  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

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

^d PFIZER INC   (United States)

Author keywords

catenin; Ex vivo expansion; Hematopoietic stem cells; PTEN; Self renewal

Indexed keywords

BETA CATENIN; INHIBITOR OF DIFFERENTIATION 2; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN MCL 1; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; GENE ACTIVATION; GENE DELETION; GENE LOSS; GENETIC MODEL; HEMATOPOIETIC STEM CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; UPREGULATION;

ANIMALS; APOPTOSIS; BETA CATENIN; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CELLS, CULTURED; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; MICE; MUTATION; PHENOTYPE; PHOSPHATIDYLINOSITOL 3-KINASES; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION; WNT PROTEINS;

MUS;

EID: 80052983495     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.17421911     Document Type: Article

References (69)

1. Akashi K, Traver D, Miyamoto T, Weissman IL. 2000. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404: 193-197.
2. Akashi K, He X, Chen J, Iwasaki H, Niu C, Steenhard B, Zhang J, Haug J, Li L. 2003. Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood 101: 383-389.
3. Antonchuk J, Sauvageau G, Humphries RK. 2002. HOXB4- induced expansion of adult hematopoietic stem cells ex vivo. Cell 109: 39-45.
4. Baba Y, Garrett KP, Kincade PW. 2005. Constitutively active β-catenin confers multilineage differentiation potential on lymphoid and myeloid progenitors. Immunity 23: 599-609.
5. Blanpain C, Fuchs E. 2009. Epidermal homeostasis: a balancing act of stem cells in the skin. Natl Rev 10: 207-217.
6. Boitano AE, Wang J, Romeo R, Bouchez LC, Parker AE, Sutton SE, Walker JR, Flaveny CA, Perdew GH, Denison MS, et al. 2010. Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science 329: 1347-1348.
7. Borowitz MJ, Guenther KL, Shults KE, Stelzer GT. 1993. Immunophenotyping of acute leukemia by flow cytometric analysis. Am J Clin Pathol 100: 534-540.
8. Butler JM, Nolan DJ, Vertes EL, Varnum-Finney B, Kobayashi H, Hooper AT, Seandel M, Shido K, White IA, Kobayashi M, et al. 2010. Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. Cell Stem Cell 6: 251-264.
9. Chou S, Chu P, Hwang W, Lodish H. 2010. Expansion of human cord blood hematopoietic stem cells for transplantation. Cell Stem Cell 7: 427-428.
10. Christensen JL, Weissman IL. 2001. Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc Natl Acad Sci 98: 14541-14546.
11. Cobas M, Wilson A, Ernst B, Mancini SJ, MacDonald HR, Kemler R, Radtke F. 2004. β-Catenin is dispensable for hematopoiesis and lymphopoiesis. J Exp Med 199: 221-229.
12. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-241.
13. Delaney C, Heimfeld S, Brashem-Stein C, Voorhies H, Manger RL, Bernstein ID. 2010. Notch-mediated expansion of human cord blood progenitor cells capable of rapid myeloid reconstitution. Nat Med 16: 232-236.
14. Doulatov S, Notta F, Rice KL, Howell L, Zelent A, Licht JD, Dick JE. 2009. PLZF is a regulator of homeostatic and cytokine-induced myeloid development. Genes Dev 23: 2076-2087.
15. Enver T, Greaves M. 1998. Loops, lineage, and leukemia. Cell 94: 9-12.
16. Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, Trumpp A. 2009. IFNα activates dormant haematopoietic stem cells in vivo. Nature 458: 904-908.
17. Fleming HE, Janzen V, Lo Celso C, Guo J, Leahy KM, Kronenberg HM, Scadden DT. 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.
18. Goessling W, North TE, Loewer S, Lord AM, Lee S, Stoick-Cooper CL, Weidinger G, Puder M, Daley GQ, Moon RT, et al. 2009. Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration. Cell 136: 1136-1147.
19. Gothert JR, Gustin SE, Hall MA, Green AR, Gottgens B, Izon DJ, Begley CG. 2005. In vivo fate-tracing studies using the Scl stem cell enhancer: embryonic hematopoietic stem cells significantly contribute to adult hematopoiesis. Blood 105: 2724-2732.
20. Guo W, Lasky JL, Chang CJ, Mosessian S, Lewis X, Xiao Y, Yeh JE, Chen JY, Iruela-Arispe ML, Varella-Garcia M, et al. 2008. Multi-genetic events collaboratively contribute to Pten-null leukaemia stem-cell formation. Nature 453: 529-533.
21. Harada N, Tamai Y, Ishikawa T, Sauer B, Takaku K, Oshima M, Taketo MM. 1999. Intestinal polyposis in mice with a dominant stable mutation of the β-catenin gene. EMBO J 18: 5931-5942.
22. He XC, Yin T, Grindley JC, Tian Q, Sato T, Tao WA, Dirisina R, Porter-Westpfahl KS, Hembree M, Johnson T, et al. 2007. PTEN-deficient intestinal stem cells initiate intestinal polyposis. Nat Genet 39: 189-198.
23. Himburg HA, Muramoto GG, Daher P, Meadows SK, Russell JL, Doan P, Chi J-T, Salter AB, Lento WE, Reya T, et al. 2010. Pleiotrophin regulates the expansion and regeneration of hematopoietic stem cells. Nat Med 16: 475-482.
24. Hu M, Krause D, Greaves M, Sharkis S, Dexter M, Heyworth C, Enver T. 1997. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev 11: 774-785.
25. Huang J, Zhang Y, Bersenev A, O'Brien WT, Tong W, Emerson SG, Klein PS. 2009. Pivotal role for glycogen synthase kinase- 3 in hematopoietic stem cell homeostasis in mice. J Clin Invest 119: 3519-3529.
26. Jeannet G, Scheller M, Scarpellino L, Duboux S, Gardiol N, Back J, Kuttler F, Malanchi I, Birchmeier W, Leutz A, et al. 2008. Long-term, multilineage hematopoiesis occurs in the combined absence of β-catenin and γ-catenin. Blood 111: 142-149.
27. Ji M, Li H, Suh HC, Klarmann KD, Yokota Y, Keller JR. 2008. Id2 intrinsically regulates lymphoid and erythroid development via interaction with different target proteins. Blood 112: 1068-1077.
28. Kirstetter P, Anderson K, Porse BT, Jacobsen SE, Nerlov C. 2006. Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multilineage differentiation block. Nat Immunol 7: 1048-1056.
29. Koch U, Wilson A, Cobas M, Kemler R, Macdonald HR, Radtke F. 2008. Simultaneous loss of β- and γ-catenin does not perturb hematopoiesis or lymphopoiesis. Blood 111: 160-164.
30. Kondo M, Weissman IL, Akashi K. 1997. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91: 661-672.
31. Lesche R, Groszer M, Gao J, Wang Y, Messing A, Sun H, Liu X, Wu H. 2002. Cre/loxP-mediated inactivation of the murine Pten tumor suppressor gene. Genesis 32: 148-149.
32. Li J, Sarosi I, Cattley RC, Pretorius J, Asuncion F, Grisanti M, Morony S, Adamu S, Geng Z, Qiu W, et al. 2006. Dkk1- mediated inhibition of Wnt signaling in bone results in osteopenia. Bone 39: 754-766.
33. Li H, Ji M, Klarmann KD, Keller JR. 2010. Repression of Id2 expression by Gfi-1 is required for B-cell and myeloid development. Blood 116: 1060-1069.
34. Maira SM, Stauffer F, Brueggen J, Furet P, Schnell C, Fritsch C, Brachmann S, Chene P, De Pover A, Schoemaker K, et al. 2008. Identification and characterization of NVP-BEZ235, a new orally available dual phosphatidylinositol 3-kinase/ mammalian target of rapamycin inhibitor with potent in vivo antitumor activity. Mol Cancer Ther 7: 1851-1863.
35. Malhotra S, Kincade PW. 2009. Wnt-related molecules and signaling pathway equilibrium in hematopoiesis. Cell Stem Cell 4: 27-36.
36. Miller CL, Eaves CJ. 1997. Expansion in vitro of adult murine hematopoietic stem cells with transplantable lympho-myeloid reconstituting ability. Proc Natl Acad Sci 94: 13648-13653.
37. Miyamoto T, Iwasaki H, Reizis B, Ye M, Graf T, Weissman IL, Akashi K. 2002. Myeloid or lymphoid promiscuity as a critical step for hematopoietic lineage commitment. Dev Cell 3: 137-147.
38. Morrison SJ, Kimble J. 2006. Asymmetric and symmetric stemcell divisions in development and cancer. Nature 441: 1068-1074.
39. Murdoch B, Chadwick K, Martin M, Shojaei F, Shah KV, Gallacher L, Moon RT, Bhatia M. 2003. Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc Natl Acad Sci 100: 3422-3427.
40. Na Nakorn T, Traver D, Weissman IL, Akashi K. 2002. Myeloerythroid-restricted progenitors are sufficient to confer radioprotection and provide the majority of day 8 CFU-S. J Clin Invest 109: 1579-1585.
41. Nemeth MJ, Topol L, Anderson SM, Yang Y, Bodine DM. 2007. Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation. Proc Natl Acad Sci 104: 15436-15441.
42. North TE, Goessling W. 2010. Previews. NOTCHing an arrow at cord blood: translating stem cell knowledge into clinical practice. Cell Stem Cell 6: 186-187.
43. North TE, Goessling W, Walkley CR, Lengerke C, Kopani KR, Lord AM, Weber GJ, Bowman TV, Jang IH, Grosser T, et al. 2007. Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 447: 1007-1011.
44. Novak A, Guo C, Yang W, Nagy A, Lobe CG. 2000. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28: 147-155.
45. Opferman JT, Iwasaki H, Ong CC, Suh H, Mizuno S, Akashi K, Korsmeyer SJ. 2005. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307: 1101-1104.
46. Orkin SH. 2000. Diversification of haematopoietic stem cells to specific lineages. Nat Rev Genet 1: 57-64.
47. Orkin SH, Zon LI. 2008. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132: 631-644.
48. Osawa M, Hanada K, Hamada H, Nakauchi H. 1996. Long-term lymphohematopoietic reconstitution by a single CD34-low/ negative hematopoietic stem cell. Science 273: 242-245.
49. Purton LE, Scadden DT. 2007. Limiting factors in murine hematopoietic stem cell assays. Cell Stem Cell 1: 263-270.
50. Reya T, Morrison SJ, Clarke MF, Weissman IL. 2001. Stem cells, cancer, and cancer stem cells. Nature 414: 105-111.
51. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, Hintz L, Nusse R, Weissman IL. 2003. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423: 409-414.
52. Rossi DJ, Weissman IL. 2006. Pten, tumorigenesis, and stem cell self-renewal. Cell 125: 229-231.
53. Salmena L, Carracedo A, Pandolfi PP. 2008. Tenets of PTEN tumor suppression. Cell 133: 403-414.
54. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH. 2004. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10: 55-63.
55. Sauvageau G, Thorsteinsdottir U, Eaves CJ, Lawrence HJ, Largman C, Lansdorp PM, Humphries RK. 1995. Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes Dev 9: 1753-1765.
56. Scadden DT. 2006. The stem-cell niche as an entity of action. Nature 441: 1075-1079.
57. Scheller M, Huelsken J, Rosenbauer F, Taketo MM, Birchmeier W, Tenen DG, Leutz A. 2006. Hematopoietic stem cell and multilineage defects generated by constitutive b-catenin activation. Nat Immunol 7: 1037-1047.
58. Trowbridge JJ, Xenocostas A, Moon RT, Bhatia M. 2006. Glycogen synthase kinase-3 is an in vivo regulator of hematopoietic stem cell repopulation. Nat Med 12: 89-98.
59. van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A, van der Horn K, Batlle E, Coudreuse D, Haramis AP, et al. 2002. The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111: 241-250.
60. Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, Yates JR 3rd, Nusse R. 2003. Wnt proteins are lipidmodified and can act as stem cell growth factors. Nature 423: 448-452.
61. Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W, Jaworski M, Offner S, Dunant CF, Eshkind L, Bockamp E, et al. 2008. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135: 1118-1129.
62. Xie Y, Yin T, Wiegraebe W, He XC, Miller D, Stark D, Perko K, Alexander R, Schwartz J, Grindley JC, et al. 2009. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 457: 97-101.
63. Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, Wu H, Morrison SJ. 2006. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441: 475-482.
64. Ying Q-L, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P, Smith A. 2008. The ground state of embryonic stem cell self-renewal. Nature 453: 519-523.
65. Zhang J, Li L. 2005. BMP signaling and stem cell regulation. Dev Biol 284: 1-11.
66. Zhang CC, Lodish HF. 2005. Murine hematopoietic stem cells change their surface phenotype during ex vivo expansion. Blood 105: 4314-4320.
67. Zhang CC, Kaba M, Ge G, Xie K, Tong W, Hug C, Lodish HF. 2006. Angiopoietin-like proteins stimulate ex vivo expansion of hematopoietic stem cells. Nat Med 12: 240-245.
68. Zhang J, Grindley JC, Yin T, Jayasinghe S, He XC, Ross JT, Haug JS, Rupp D, Porter-Westpfahl KS, Wiedemann LM, et al. 2006. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 441: 518-522.
69. Zhao C, Blum J, Chen A, Kwon HY, Jung SH, Cook JM, Lagoo A, Reya T. 2007. Loss of β-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell 12: 528-541.