TAK1 is Required for the Survival of Hematopoietic Cells and Hepatocytes in Mice

Overview

Journal J Exp Med

Specialties Allergy & Immunology
General Medicine

Date 2008 Jun 25

PMID 18573910

Citations 66

Authors

Minghui Tang

Xudong Wei

Yinshi Guo

Peter Breslin

Shubin Zhang

Shanshan Zhang

Wei Wei

Zhenbiao Xia

Manuel Diaz

Shizuo Akira

Jiwang Zhang

Affiliations

Soon will be listed here.

Abstract

Transforming growth factor beta-activated kinase 1 (TAK1), a member of the MAPKKK family, is a key mediator of proinflammatory and stress signals. Activation of TAK1 by proinflammatory cytokines and T and B cell receptors induces the nuclear localization of nuclear factor kappaB (NF-kappaB) and the activation of c-Jun N-terminal kinase (JNK)/AP1 and P38, which play important roles in mediating inflammation, immune responses, T and B cell activation, and epithelial cell survival. Here, we report that TAK1 is critical for the survival of both hematopoietic cells and hepatocytes. Deletion of TAK1 results in bone marrow (BM) and liver failure in mice due to the massive apoptotic death of hematopoietic cells and hepatocytes. Hematopoietic stem cells and progenitors were among those hematopoietic cells affected by TAK1 deletion-induced cell death. This apoptotic cell death is autonomous, as demonstrated by reciprocal BM transplantation. Deletion of TAK1 resulted in the inactivation of both JNK and NF-kappaB signaling, as well as the down-regulation of expression of prosurvival genes.

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References

Pearl-Yafe M, Stein J, Yolcu E, Farkas D, Shirwan H, Yaniv I . Fas transduces dual apoptotic and trophic signals in hematopoietic progenitors. Stem Cells. 2007; 25(12):3194-203. DOI: 10.1634/stemcells.2007-0402. View

Brandt J, Bhalla K, Hoffman R . Effects of interleukin-3 and c-kit ligand on the survival of various classes of human hematopoietic progenitor cells. Blood. 1994; 83(6):1507-14. View

Shim J, Xiao C, Paschal A, Bailey S, Rao P, Hayden M . TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 2005; 19(22):2668-81. PMC: 1283960. DOI: 10.1101/gad.1360605. View

Kimura S, Roberts A, Metcalf D, Alexander W . Hematopoietic stem cell deficiencies in mice lacking c-Mpl, the receptor for thrombopoietin. Proc Natl Acad Sci U S A. 1998; 95(3):1195-200. PMC: 18717. DOI: 10.1073/pnas.95.3.1195. View

Blume-Jensen P, Janknecht R, Hunter T . The kit receptor promotes cell survival via activation of PI 3-kinase and subsequent Akt-mediated phosphorylation of Bad on Ser136. Curr Biol. 1998; 8(13):779-82. DOI: 10.1016/s0960-9822(98)70302-1. View

Wan Y, Chi H, Xie M, Schneider M, Flavell R . The kinase TAK1 integrates antigen and cytokine receptor signaling for T cell development, survival and function. Nat Immunol. 2006; 7(8):851-8. DOI: 10.1038/ni1355. View

Sato S, Sanjo H, Takeda K, Ninomiya-Tsuji J, Yamamoto M, Kawai T . Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol. 2005; 6(11):1087-95. DOI: 10.1038/ni1255. View

Kuhn R, Schwenk F, Aguet M, Rajewsky K . Inducible gene targeting in mice. Science. 1995; 269(5229):1427-9. DOI: 10.1126/science.7660125. View

Dufour C, Corcione A, Svahn J, Haupt R, Poggi V, Bekassy A . TNF-alpha and IFN-gamma are overexpressed in the bone marrow of Fanconi anemia patients and TNF-alpha suppresses erythropoiesis in vitro. Blood. 2003; 102(6):2053-9. DOI: 10.1182/blood-2003-01-0114. View

10.

Jadrich J, OConnor M, Coucouvanis E . The TGF beta activated kinase TAK1 regulates vascular development in vivo. Development. 2006; 133(8):1529-41. DOI: 10.1242/dev.02333. View

11.

Yamaguchi K, Shirakabe K, Shibuya H, Irie K, Oishi I, Ueno N . Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science. 1995; 270(5244):2008-11. DOI: 10.1126/science.270.5244.2008. View

12.

Geisler F, Algul H, Paxian S, Schmid R . Genetic inactivation of RelA/p65 sensitizes adult mouse hepatocytes to TNF-induced apoptosis in vivo and in vitro. Gastroenterology. 2007; 132(7):2489-503. DOI: 10.1053/j.gastro.2007.03.033. View

13.

Kerzic P, Pyatt D, Zheng J, Gross S, Le A, Irons R . Inhibition of NF-kappaB by hydroquinone sensitizes human bone marrow progenitor cells to TNF-alpha-induced apoptosis. Toxicology. 2003; 187(2-3):127-37. DOI: 10.1016/s0300-483x(03)00064-7. View

14.

Sakurai H, Miyoshi H, Mizukami J, Sugita T . Phosphorylation-dependent activation of TAK1 mitogen-activated protein kinase kinase kinase by TAB1. FEBS Lett. 2000; 474(2-3):141-5. DOI: 10.1016/s0014-5793(00)01588-x. View

15.

Zhang J, Niu C, Ye L, Huang H, He X, Tong W . Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003; 425(6960):836-41. DOI: 10.1038/nature02041. View

16.

Motoyama N, Wang F, Roth K, Sawa H, Nakayama K, Negishi I . Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science. 1995; 267(5203):1506-10. DOI: 10.1126/science.7878471. View

17.

Liu J, Lin A . Role of JNK activation in apoptosis: a double-edged sword. Cell Res. 2005; 15(1):36-42. DOI: 10.1038/sj.cr.7290262. View

18.

Omori E, Matsumoto K, Sanjo H, Sato S, Akira S, Smart R . TAK1 is a master regulator of epidermal homeostasis involving skin inflammation and apoptosis. J Biol Chem. 2006; 281(28):19610-7. PMC: 1797070. DOI: 10.1074/jbc.M603384200. View

19.

Wallach D . Cell death induction by TNF: a matter of self control. Trends Biochem Sci. 1997; 22(4):107-9. DOI: 10.1016/s0968-0004(97)01015-3. View

20.

Horwitz B, Scott M, Cherry S, Bronson R, Baltimore D . Failure of lymphopoiesis after adoptive transfer of NF-kappaB-deficient fetal liver cells. Immunity. 1997; 6(6):765-72. DOI: 10.1016/s1074-7613(00)80451-3. View