Activation of Wnt/β-catenin protein signaling induces mitochondria-mediated apoptosis in hematopoietic progenitor cells

Journal of Biological Chemistry

Volumn 287, Issue 27, 2012, Pages 22683-22690

  Ming, Ming ^a   Wang, Sheng ^a   Wu, Wenshu ^c   Senyuk, Vitalyi ^a   Le Beau, Michelle M ^b   Nucifora, Giuseppina ^a   Qian, Zhijian ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC PATHWAYS; BONE MARROW TRANSPLANTATION; CASPASES; CATENIN SIGNALING; CELL SURVIVAL; CONDITIONAL EXPRESSIONS; DOWN-REGULATION; HEMATOPOIETIC PROGENITOR CELLS; HEMATOPOIETIC STEM/PROGENITOR CELLS; IN-VITRO; IN-VIVO; MITOCHONDRIAL MEMBRANE POTENTIAL; PROTEIN SIGNALING; TRANSGENE; TUMORIGENESIS;

MITOCHONDRIA; STEM CELLS;

CELL DEATH;

BETA CATENIN; CASPASE 3; CASPASE 9; PROTEIN BCL 2; WNT PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSGENE;

ANIMALS; APOPTOSIS; BETA CATENIN; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL SURVIVAL; CELLS, CULTURED; HEMATOPOIETIC STEM CELLS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; PROTO-ONCOGENE PROTEINS C-BCL-2; WNT SIGNALING PATHWAY;

EID: 84863327580     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.342089     Document Type: Article

References (34)

1. Cobas, M., Wilson, A., Ernst, B., Mancini, S. J., MacDonald, H. R., Kemler, R., and Radtke, F. (2004) β-Catenin is dispensable for hematopoiesis and lymphopoiesis. J. Exp. Med. 199, 221-229
2. Jeannet, G., Scheller, M., Scarpellino, L., Duboux, S., Gardiol, N., Back, J., Kuttler, F., Malanchi, I., Birchmeier, W., Leutz, A., Huelsken, J., and Held, W. (2008) Long-term, multilineage hematopoiesis occurs in the combined absence of β-catenin and γ-catenin. Blood 111, 142-149
3. Zhao, C., Blum, J., Chen, A., Kwon, H. Y., Jung, S. H., Cook, J. M., Lagoo, A., and Reya, T. (2007) Loss of β-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell 12, 528-541 (Pubitemid 350199070)
4. Reya, T., Duncan, A. W., Ailles, L., Domen, J., Scherer, D. C., Willert, K., Hintz, L., Nusse, R., and Weissman, I. L. (2003) A role for Wnt signaling in self-renewal of hematopoietic stem cells. Nature 423, 409-414 (Pubitemid 36626987)
5. Willert, K., Brown, J. D., Danenberg, E., Duncan, A. W., Weissman, I. L., Reya, T., Yates, J. R., 3rd, and Nusse, R. (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448-452 (Pubitemid 36626997)
6. Trowbridge, J. J., Xenocostas, A., Moon, R. T., and Bhatia, M. (2006) Glycogen synthase kinase-3 is an in vivo regulator of hematopoietic stem cell repopulation. Nat. Med. 12, 89-98 (Pubitemid 43050082)
7. Baba, Y., Garrett, K. P., and Kincade, P. W. (2005) Constitutively active β-catenin confers multilineage differentiation potential on lymphoid and myeloid progenitors. Immunity 23, 599-609 (Pubitemid 41779482)
8. Baba, Y., Yokota, T., Spits, H., Garrett, K. P., Hayashi, S., and Kincade, P. W. (2006) Constitutively active β-catenin promotes expansion of multipotent hematopoietic progenitors in culture. J. Immunol. 177, 2294-2303 (Pubitemid 44200989)
9. Kirstetter, P., Anderson, K., Porse, B. T., Jacobsen, S. E., and 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 (Pubitemid 44420649)
10. Scheller, M., Huelsken, J., Rosenbauer, F., Taketo, M. M., Birchmeier, W., Tenen, D. G., and Leutz, A. (2006) Hematopoietic stem cell and multilineage defects generated by constitutive β-catenin activation. Nat. Immunol. 7, 1037-1047 (Pubitemid 44420648)
11. He, T. C., Sparks, A. B., Rago, C., Hermeking, H., Zawel, L., da Costa, L. T., Morin, P. J., Vogelstein, B., and Kinzler, K. W. (1998) Identification of c-MYC as a target of the APC pathway. Science 281, 1509-1512 (Pubitemid 28425575)
12. Tetsu, O., and McCormick, F. (1999) β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398, 422-426 (Pubitemid 29180374)
13. Wong, M. H., Rubinfeld, B., and Gordon, J. I. (1998) Effects of forced expression of an NH2-terminal truncated β-catenin on mouse intestinal epithelial homeostasis. J. Cell Biol. 141, 765-777 (Pubitemid 28217920)
14. Kim, K., Pang, K. M., Evans, M., and Hay, E. D. (2000) Overexpression of β-catenin induces apoptosis independent of its transactivation function with LEF-1 or the involvement of major G1 cell cycle regulators. Mol. Biol. Cell 11, 3509-3523
15. Raab, M. S., Breitkreutz, I., Tonon, G., Zhang, J., Hayden, P. J., Nguyen, T., Fruehauf, J. H., Lin, B. K., Chauhan, D., Hideshima, T., Munshi, N. C., Anderson, K. C., and Podar, K. (2009) Targeting PKC: a novel role for β-catenin in ER stress and apoptotic signaling. Blood 113, 1513-1521
16. Harada, N., Tamai, Y., Ishikawa, T., Sauer, B., Takaku, K., Oshima, M., and Taketo, M. M. (1999) Intestinal polyposis in mice with a dominant stable mutation of the β-catenin gene. EMBO J. 18, 5931-5942 (Pubitemid 29515670)
17. Qian, Z., Mao, L., Fernald, A. A., Yu, H., Luo, R., Jiang, Y., Anastasi, J., Valk, P. J., Delwel, R., and Le Beau, M. M. (2009) Enhanced expression of FHL2 leads to abnormal myelopoiesis in vivo. Leukemia 23, 1650-1657
18. Lavau, C., Szilvassy, S. J., Slany, R., and Cleary, M. L. (1997) Immortalization and leukemic transformation of a myelomonocytic precursor by retrovirally transduced HRX-ENL. EMBO J. 16, 4226-4237 (Pubitemid 27298175)
19. Qian, Z., Chen, L., Fernald, A. A., Williams, B. O., and Le Beau, M. M. (2008) A critical role for Apc in hematopoietic stem and progenitor cellsurvival. J. Exp. Med. 205, 2163-2175
20. Zhang, J., Grindley, J. C., Yin, T., Jayasinghe, S., He, X. C., Ross, J. T., Haug, J. S., Rupp, D., Porter-Westpfahl, K. S., Wiedemann, L. M., Wu, H., and Li, L. (2006) PTEN maintains hematopoietic stem cells and acts in lineage choice and leukemia prevention. Nature 441, 518-522 (Pubitemid 44050154)
21. Qian, Z., Okuhara, D., Abe, M. K., and Rosner, M. R. (1999) Molecular cloning and characterization of a mitogen-activated protein kinase-associated intracellular chloride channel. J. Biol. Chem. 274, 1621-1627
22. Goessling, W., North, T. E., Loewer, S., Lord, A. M., Lee, S., Stoick-Cooper, C. L., Weidinger, G., Puder, M., Daley, G. Q., Moon, R. T., and Zon, L. I. (2009) Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration. Cell 136, 1136-1147
23. Brault, V., Moore, R., Kutsch, S., Ishibashi, M., Rowitch, D. H., McMahon, A. P., Sommer, L., Boussadia, O., and Kemler, R. (2001) Inactivation of the β-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264 (Pubitemid 32409648)
24. Ogilvy, S., Metcalf, D., Print, C. G., Bath, M. L., Harris, A. W., and Adams, J. M. (1999) Constitutive Bcl-2 expression throughout the hematopoietic compartment affects multiple lineages and enhances progenitor cell survival. Proc. Natl. Acad. Sci. U.S.A. 96, 14943-14948 (Pubitemid 30019744)
25. Perry, J. M., He, X. C., Sugimura, R., Grindley, J. C., Haug, J. S., Ding, S., and Li, L. (2011) Cooperation between both Wnt/β-catenin and PTEN/PI3K/Akt signaling promotes primitive hematopoietic stem cell self-renewal and expansion. Genes Dev. 25, 1928-1942
26. Domen, J., and Weissman, I. L. (2000) Hematopoietic stem cells need two signals to prevent apoptosis; BCL-2 can provide one of these, Kitl/c-Kit signaling the other. J. Exp. Med. 192, 1707-1718 (Pubitemid 32049764)
27. Porter, A. G., and Jänicke, R. U. (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 6, 99-104 (Pubitemid 29082297)
28. Fodde, R., Smits, R., and Clevers, H. (2001) APC, signal transduction, and genetic instability in colorectal cancer. Nat. Rev. Cancer 1, 55-67 (Pubitemid 33741881)
29. Luis, T. C., Naber, B. A., Roozen, P. P., Brugman, M. H., de Haas, E. F., Ghazvini, M., Fibbe, W. E., van Dongen, J. J., Fodde, R., and Staal, F. J. (2011) Canonical Wnt signaling regulates hematopoiesis in a dosage-dependent fashion. Cell Stem Cell 9, 345-356
30. Chung, E. J., Hwang, S. G., Nguyen, P., Lee, S., Kim, J. S., Kim, J. W., Henkart, P. A., Bottaro, D. P., Soon, L., Bonvini, P., Lee, S. J., Karp, J. E., Oh, H. J., Rubin, J. S., and Trepel, J. B. (2002) Regulation of leukemic cell adhesion, proliferation, and survival by β-catenin. Blood 100, 982-990 (Pubitemid 34832627)
31. Simon, M., Grandage, V. L., Linch, D. C., and Khwaja, A. (2005) Constitutive activation of the Wnt/β-catenin signaling pathway in acute myeloid leukemia. Oncogene 24, 2410-2420 (Pubitemid 40546699)
32. Tickenbrock, L., Schwäble, J., Wiedehage, M., Steffen, B., Sargin, B., Choudhary, C., Brandts, C., Berdel, W. E., Müller-Tidow, C., and Serve, H. (2005) Flt3 tandem duplication mutations cooperate with Wnt signaling in leukemic signal transduction. Blood 105, 3699-3706 (Pubitemid 40628219)
33. Ysebaert, L., Chicanne, G., Demur, C., De Toni, F., Prade-Houdellier, N., Ruidavets, J. B., Mansat-De Mas, V., Rigal-Huguet, F., Laurent, G., Payrastre, B., Manenti, S., and Racaud-Sultan, C. (2006) Expression of β-catenin by acute myeloid leukemia cells predicts enhanced clonogenic capacities and poor prognosis. Leukemia 20, 1211-1216 (Pubitemid 43905823)
34. Del Principe, M. I., Del Poeta, G., Venditti, A., Buccisano, F., Maurillo, L., Mazzone, C., Bruno, A., Neri, B., Irno Consalvo, M., Lo Coco, F., and Amadori, S. (2005) Apoptosis and immaturity in acute myeloid leukemia. Hematology 10, 25-34 (Pubitemid 41093585)