Daxx mediates activation-induced cell death in microglia by triggering MST1 signalling

EMBO Journal

Volumn 30, Issue 12, 2011, Pages 2465-2476

  Yun, Hee Jae ^a   Yoon, Je Hyun ^a   Lee, Jae Keun ^a   Noh, Kyung Tae ^a   Yoon, Kyoung Wan ^a   Oh, Sang Phil ^b   Oh, Hyun Jung ^b   Chae, Ji Soo ^a   Hwang, Sang Gil ^a   Kim, Eun Hee ^c   Maul, Gerd G ^d   Lim, Dae Sik ^b   Choi, Eui Ju ^a  

^a Korea University   (South Korea)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^c Chungnam National University   (South Korea)

^d WISTAR INSTITUTE   (United States)

Author keywords

cell death; Daxx; interferon g; microglia; MST1

Indexed keywords

DAXX PROTEIN; GAMMA INTERFERON; MAMMALIAN STE20 LIKE KINASE 1; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; CARRIER PROTEINS; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; FIBROBLASTS; HEK293 CELLS; HELA CELLS; HEPATOCYTE GROWTH FACTOR; HUMANS; INFLAMMATION MEDIATORS; INTERFERON-GAMMA; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; MICROGLIA; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

MAMMALIA; MUS; RATTUS;

EID: 79958845426     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.152     Document Type: Article

References (53)

1. Block ML, Hong JS (2005) Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol 76: 77-98 (Pubitemid 41242883)
2. Block ML, Zecca L, Hong JS (2007) Microglia-mediated neurotoxi-city: uncovering the molecular mechanisms. Nat Rev Neurosci 8: 57-69 (Pubitemid 46011999)
3. Callus BA, Verhagen AM, Vaux DL (2006) Association of mammalian sterile twenty kinases, Mst1 and Mst2, with hSalvador via C-terminal coiled-coil domains, leads to its stabilization and phos-phorylation. FEBS J 273: 4264-4276 (Pubitemid 44326506)
4. Chan EH, Nousiainen M, Chalamalasetty RB, Schafer A, Nigg EA, Sillje HH (2005) The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 24: 2076-2086 (Pubitemid 40516201)
5. Cheung WL, Ajiro K, Samejima K, Kloc M, Cheung P, Mizzen CA, Beeser A, Etkin LD, Chernoff J, Earnshaw WC, Allis CD (2003) Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113: 507-517 (Pubitemid 36603322)
6. Cho SG, Kim JW, Lee YH, Hwang HS, Kim MS, Ryoo K, Kim MJ, Noh KT, Kim EK, Cho JH, Yoon KW, Cho EG, Park HS, Chi SW, Lee MJ, Kang SS, Ichijo H, Choi EJ (2003) Identification of a novel antiapoptotic protein that antagonizes ASK1 and CAD activities. J Cell Biol 163: 71-81 (Pubitemid 37271435)
7. Creasy CL, Ambrose DM, Chernoff J (1996) The Ste20-like protein kinase, Mst1, dimerizes and contains an inhibitory domain. J Biol Chem 271: 21049-21053 (Pubitemid 26292952)
8. Dan I, Watanabe NM, Kusumi A (2001) The Ste20 group kinases as regulators of MAP kinase cascades. Trends Cell Biol 11 : 220-230 (Pubitemid 32367879)
9. de Souza PM, Lindsay MA (2004) Mammalian Sterile20-like kinase 1 and the regulation of apoptosis. Biochem Soc Trans 32: 485-488 (Pubitemid 38813544)
10. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, Gayyed MF, Anders RA, Maitra A, Pan D (2007) Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130: 1120-1133 (Pubitemid 47410268)
11. Glantschnig H, Rodan GA, Reszka AA (2002) Mapping of MST1 kinase sites of phosphorylation. Activation and autophosphoryla-tion. J Biol Chem 277: 42987-42996 (Pubitemid 35285678)
12. Graves JD, Draves KE, Gotoh Y, Krebs EG, Clark EA (2001) Both phosphorylation and caspase-mediated cleavage contribute to regulation of the Ste20-like protein kinase Mst1 during CD95/ Fas-induced apoptosis. J Biol Chem 276: 14909-14915
13. Graves JD, Gotoh Y, Draves KE, Ambrose D, Han DK, Wright M, Chernoff J, Clark EA, Krebs EG (1998) Caspase-mediated activation and induction of apoptosis by the mammalian Ste20-like kinase Mst1. EMBO J 17: 2224-2234 (Pubitemid 28171908)
14. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394 (Pubitemid 350014685)
15. Hao Y, Chun A, Cheung K, Rashidi B, Yang X (2008) Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem 283: 5496-5509
16. Huang J, Wu S, Barrera J, Matthews K, Pan D (2005) The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122: 421-434 (Pubitemid 41127143)
17. Ishov AM, Sotnikov AG, Negorev D, Vladimirova OV, Neff N, Kamitani T, Yeh ET, Strauss III JF, Maul GG (1999) PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J Cell Biol 147: 221-234
18. Justice RW, Zilian O, Woods DF, Noll M, Bryant PJ (1995) The Drosophila tumor suppressor gene warts encodes a homolog of human myotonic dystrophy kinase and is required for the control of cell shape and proliferation. Genes Dev 9: 534-546
19. Kennedy PS, Goyal RK, Hersh T (1972) Hereditary angioneurotic edema. A case with recurring abdominal pain. Am J Dig Dis 17: 435-438
20. Khazaei MR, Habibi-Rezaei M, Karimzadeh F, Moosavi-Movahedi AA, Sarrafnejhad AA, Sabouni F, Bakhti M (2008) Microglial cell death induced by glycated bovine serum albumin: nitric oxide involvement. J Biochem 144: 197-206
21. Khokhlatchev A, Rabizadeh S, Xavier R, Nedwidek M, Chen T, Zhang XF, Seed B, Avruch J (2002) Identification of a novel Ras-regulated proapoptotic pathway. Curr Biol 12: 253-265 (Pubitemid 34161469)
22. Lee J, Hur J, Lee P, Kim JY, Cho N, Kim SY, Kim H, Lee MS, Suk K (2001a) Dual role of inflammatory stimuli in activation-induced cell death of mouse microglial cells. Initiation of two separate apoptotic pathways via induction of interferon regulatory factor-1 and caspase-11. J Biol Chem 276: 32956-32965
23. Lee JH, Kim TS, Yang TH, Koo BK, Oh SP, Lee KP, Oh HJ, Lee SH, Kong YY, Kim JM, Lim DS (2008) A crucial role of WW45 in developing epithelial tissues in the mouse. EMBO J 27: 1231-1242
24. Lee P, Lee J, Kim S, Lee MS, Yagita H, Kim SY, Kim H, Suk K (2001b) NO as an autocrine mediator in the apoptosis of activated microglial cells: correlation between activation and apoptosis of microglial cells. Brain Res 892: 380-385 (Pubitemid 32141226)
25. Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villen J, Becker EB, DiBacco S, de la Iglesia N, Gygi S, Blackwell TK, Bonni A (2006) A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125: 987-1001 (Pubitemid 43795191)
26. Lin DY, Fang HI, Ma AH, Huang YS, Pu YS, Jenster G, Kung HJ, Shih HM (2004) Negative modulation of androgen receptor transcrip-tional activity by Daxx. Mol Cell Biol 24: 10529-10541 (Pubitemid 39603115)
27. Liu B, Hong JS (2003) Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J Pharmacol Exp Ther 304: 1-7 (Pubitemid 36008905)
28. Liu B, Wang K, Gao HM, Mandavilli B, Wang JY, Hong JS (2001) Molecular consequences of activated microglia in the brain: overactivation induces apoptosis. J Neurochem 77: 182-189 (Pubitemid 32245092)
29. Mayo L, Jacob-Hirsch J, Amariglio N, Rechavi G, Moutin MJ, Lund FE, Stein R (2008) Dual role of CD38 in microglial activation and activation-induced cell death. J Immunol 181: 92-103
30. Mayo L, Stein R (2007) Characterization of LPS and interferon-gamma triggered activation-induced cell death in N9 and primary microglial cells: induction of the mitochondrial gateway by nitric oxide. Cell Death Differ 14: 183-186 (Pubitemid 44911905)
31. Meydan N, Grunberger T, Dadi H, Shahar M, Arpaia E, Lapidot Z, Leeder JS, Freedman M, Cohen A, Gazit A, Levitzki A, Roifman CM (1996) Inhibition of acute lymphoblastic leukaemia by a Jak-2 inhibitor. Nature 379: 645-648 (Pubitemid 26053453)
32. Neumann H (2001) Control of glial immune function by neurons. Glia 36: 191-199 (Pubitemid 33055907)
33. Oh H, Irvine KD (2009) In vivo analysis of Yorkie phosphorylation sites. Oncogene 28: 1916-1927
34. Oh HJ, Lee KK, Song SJ, Jin MS, Song MS, Lee JH, Im CR, Lee JO, Yonehara S, Lim DS (2006) Role of the tumor suppressor RASSF1A in Mst1-mediated apoptosis. Cancer Res 66: 2562-2569
35. Oh S, Lee D, Kim T, Kim TS, Oh HJ, Hwang CY, Kong YY, Kwon KS, Lim DS (2009) Crucial role for Mst1 and Mst2 kinases in early embryonic development of the mouse. Mol Cell Biol 29: 6309-6320
36. Park HS, Lee JS, Huh SH, Seo JS, Choi EJ (2001) Hsp72 functions as a natural inhibitory protein of c-Jun N-terminal kinase. EMBO J 20: 446-456
37. Pocock JM, Kettenmann H (2007) Neurotransmitter receptors on microglia. Trends Neurosci 30: 527-535 (Pubitemid 47513237)
38. Praskova M, Xia F, Avruch J (2008) MOBKL1A/MOBKL1B phos-phorylation by MST1 and MST2 inhibits cell proliferation. Curr Biol 18: 311-321
39. Radu M, Chernoff J (2009) The DeMSTification of mammalian Ste20 kinases. Curr Biol 19: R421-R425
40. Rogers J, Mastroeni D, Leonard B, Joyce J, Grover A (2007) Neuroinflammation in Alzheimer's disease and Parkinson's disease: are microglia pathogenic in either disorder? Int Rev Neurobiol 82: 235-246
41. Ryoo K, Huh SH, Lee YH, Yoon KW, Cho SG, Choi EJ (2004) Negative regulation of MEKK1-induced signaling by glutathione S-transferase Mu. J Biol Chem 279: 43589-43594 (Pubitemid 39390661)
42. Scheel H, Hofmann K (2003) A novel interaction motif, SARAH, connects three classes of tumor suppressor. Curr Biol 13: R899-R900 (Pubitemid 37502506)
43. Song JJ, Lee YJ (2003) Role of the ASK1-SEK1-JNK1-HIPK1 signal in Daxx trafficking and ASK1 oligomerization. J Biol Chem 278: 47245-47252 (Pubitemid 37452312)
44. Strano S, Munarriz E, Rossi M, Castagnoli L, Shaul Y, Sacchi A, Oren M, Sudol M, Cesareni G, Blandino G (2001) Physical interaction with Yes-associated protein enhances p73 transcriptional activity. J Biol Chem 276: 15164-15173
45. Streit WJ, Walter SA, Pennell NA (1999) Reactive microgliosis. Prog Neurobiol 57: 563-581 (Pubitemid 29148415)
46. Takeuchi H, Wang J, Kawanokuchi J, Mitsuma N, Mizuno T, Suzumura A (2006) Interferon-gamma induces microglial-activa-tion-induced cell death: a hypothetical mechanism of relapse and remission in multiple sclerosis. Neurobiol Dis 22: 33-39
47. Ura S, Masuyama N, Graves JD, Gotoh Y (2001a) Caspase cleavage of MST1 promotes nuclear translocation and chromatin condensation. Proc Natl Acad Sci USA 98: 10148-10153 (Pubitemid 32802989)
48. Ura S, Masuyama N, Graves JD, Gotoh Y (2001b) MST1-JNK promotes apoptosis via caspase-dependent and independent pathways. Genes Cells 6: 519-530 (Pubitemid 32655384)
49. Vichalkovski A, Gresko E, Cornils H, Hergovich A, Schmitz D, Hemmings BA (2008) NDR kinase is activated by RASSF1A/ MST1 in response to Fas receptor stimulation and promotes apoptosis. Curr Biol 18: 1889-1895
50. Xu T, Wang W, Zhang S, Stewart RA, Yu W (1995) Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 121: 1053-1063
51. Yagi R, Chen LF, Shigesada K, Murakami Y, Ito Y (1999) A WW domain-containing yes-associated protein (YAP) is a novel tran-scriptional co-activator. EMBO J 18: 2551-2562 (Pubitemid 29213286)
52. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, Zheng P, Ye K, Chinnaiyan A, Halder G, Lai ZC, Guan KL (2007) Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 21: 2747-2761 (Pubitemid 350070721)
53. Zhong S, Salomoni P, Ronchetti S, Guo A, Ruggero D, Pandolfi PP (2000) Promyelocytic leukemia protein (PML) and Daxx participate in a novel nuclear pathway for apoptosis. J Exp Med 191: 631-640