The DAPK family: A structure-function analysis

Apoptosis

Volumn 19, Issue 2, 2014, Pages 286-297

  Shiloh, Ruth ^a   Bialik, Shani ^a   Kimchi, Adi ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Autophagy; Ca 2+ calmodulin; DAP kinase; DRP 1; Programmed cell death; ZIP kinase

Indexed keywords

ANIMALS; APOPTOSIS; DEATH-ASSOCIATED PROTEIN KINASES; HUMANS; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84894996077     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-013-0924-5     Document Type: Review

References (77)

1. Deiss LP, Feinstein E, Berissi H, Cohen O, Kimchi A (1995) Identification of a novel serine/threonine kinase and a novel 15-kD protein as potential mediators of the gamma interferon-induced cell death. Genes Dev 9(1):15-30
2. Bialik S, Kimchi A (2006) The death-associated protein kinases: structure, function, and beyond. Annu Rev Biochem 75:189-210. doi: 10.1146/annurev.biochem.75.103004.142615
3. Kawai T, Matsumoto M, Takeda K, Sanjo H, Akira S (1998) ZIP kinase, a novel serine/threonine kinase which mediates apoptosis. Mol Cell Biol 18(3):1642-1651
4. Kogel D, Plottner O, Landsberg G, Christian S, Scheidtmann KH (1998) Cloning and characterization of Dlk, a novel serine/threonine kinase that is tightly associated with chromatin and phosphorylates core histones. Oncogene 17(20):2645-2654
5. Inbal B, Shani G, Cohen O, Kissil JL, Kimchi A (2000) Death-associated protein kinase-related protein 1, a novel serine/threonine kinase involved in apoptosis. Mol Cell Biol 20(3):1044-1054
6. Kawai T, Nomura F, Hoshino K, Copeland NG, Gilbert DJ, Jenkins NA, Akira S (1999) Death-associated protein kinase 2 is a new calcium/calmodulin-dependent protein kinase that signals apoptosis through its catalytic activity. Oncogene 18(23):3471-3480
7. Sanjo H, Kawai T, Akira S (1998) DRAKs, novel serine/threonine kinases related to death-associated protein kinase that trigger apoptosis. J Biol Chem 273(44):29066-29071
8. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298(5600):1912-1934. doi: 10.1126/science.1075762
9. 2+/calmodulin-dependent, cytoskeletal-associated protein kinase, with cell death-inducing functions that depend on its catalytic activity. EMBO J 16(5):998-1008
10. Inbal B, Bialik S, Sabanay I, Shani G, Kimchi A (2002) DAP kinase and DRP-1 mediate membrane blebbing and the formation of autophagic vesicles during programmed cell death. J Cell Biol 157(3):455-468
11. Zalckvar E, Berissi H, Eisenstein M, Kimchi A (2009) Phosphorylation of Beclin 1 by DAP-kinase promotes autophagy by weakening its interactions with Bcl-2 and Bcl-XL. Autophagy 5(5):720-722
12. Gozuacik D, Kimchi A (2006) DAPk protein family and cancer. Autophagy 2(2):74-79
13. Kissil JL, Feinstein E, Cohen O, Jones PA, Tsai YC, Knowles MA, Eydmann ME, Kimchi A (1997) DAP-kinase loss of expression in various carcinoma and B-cell lymphoma cell lines: possible implications for role as tumor suppressor gene. Oncogene 15(4):403-407
14. Raveh T, Droguett G, Horwitz MS, DePinho RA, Kimchi A (2001) DAP kinase activates a p19ARF/p53-mediated apoptotic checkpoint to suppress oncogenic transformation. Nat Cell Biol 3(1):1-7
15. Inbal B, Cohen O, Polak-Charcon S, Kopolovic J, Vadai E, Eisenbach L, Kimchi A (1997) DAP kinase links the control of apoptosis to metastasis. Nature 390(6656):180-184
16. Kuo JC, Wang WJ, Yao CC, Wu PR, Chen RH (2006) The tumor suppressor DAPK inhibits cell motility by blocking the integrin-mediated polarity pathway. J Cell Biol 172(4):619-631. doi: 10.1083/jcb.200505138
17. Wang WJ, Kuo JC, Yao CC, Chen RH (2002) DAP-kinase induces apoptosis by suppressing integrin activity and disrupting matrix survival signals. J Cell Biol 159(1):169-179
18. Bialik S, Bresnick AR, Kimchi A (2004) DAP-kinase-mediated morphological changes are localization dependent and involve myosin-II phosphorylation. Cell Death Differ 11(6):631-644. doi: 10.1038/sj.cdd.4401386
19. Kuo JC, Lin JR, Staddon JM, Hosoya H, Chen RH (2003) Uncoordinated regulation of stress fibers and focal adhesions by DAP kinase. J Cell Sci 116(Pt 23):4777-4790
20. Shamloo M, Soriano L, Wieloch T, Nikolich K, Urfer R, Oksenberg D (2005) Death-associated protein kinase is activated by dephosphorylation in response to cerebral ischemia. J Biol Chem 280(51):42290-42299. doi: 10.1074/jbc.M505804200
21. Li Y, Grupe A, Rowland C, Nowotny P, Kauwe JS, Smemo S, Hinrichs A, Tacey K, Toombs TA, Kwok S, Catanese J, White TJ, Maxwell TJ, Hollingworth P, Abraham R, Rubinsztein DC, Brayne C, Wavrant-De Vrieze F, Hardy J, O'Donovan M, Lovestone S, Morris JC, Thal LJ, Owen M, Williams J, Goate A (2006) DAPK1 variants are associated with Alzheimer's disease and allele-specific expression. Hum Mol Genet 15(17):2560-2568. doi: 10.1093/hmg/ddl178
22. Tu W, Xu X, Peng L, Zhong X, Zhang W, Soundarapandian MM, Balel C, Wang M, Jia N, Lew F, Chan SL, Chen Y, Lu Y (2010) DAPK1 interaction with NMDA receptor NR2B subunits mediates brain damage in stroke. Cell 140(2):222-234. doi: 10.1016/j.cell.2009.12.055
23. Chuang YT, Fang LW, Lin-Feng MH, Chen RH, Lai MZ (2008) The tumor suppressor death-associated protein kinase targets to TCR-stimulated NF-kappa B activation. J Immunol 180(5):3238-3249. doi: 180/5/3238
24. Chuang YT, Lin YC, Lin KH, Chou TF, Kuo WC, Yang KT, Wu PR, Chen RH, Kimchi A, Lai MZ (2011) Tumor suppressor death-associated protein kinase is required for full IL-1beta production. Blood 117(3):960-970. doi: 10.1182/blood-2010-08-303115
25. Mukhopadhyay R, Ray PS, Arif A, Brady AK, Kinter M, Fox PL (2008) DAPK-ZIPK-L13a axis constitutes a negative-feedback module regulating inflammatory gene expression. Mol Cell 32(3):371-382. doi: 10.1016/j.molcel. 2008.09.019
26. Nakav S, Cohen S, Feigelson SW, Bialik S, Shoseyov D, Kimchi A, Alon R (2012) Tumor suppressor death-associated protein kinase attenuates inflammatory responses in the lung. Am J Respir Cell Mol Biol 46(3):313-322. doi: 10.1165/rcmb.2011-0181OC
27. Bialik S, Kimchi A (2013) The DAP-kinase interactome. Apoptosis. doi: 10.1007/s10495-013-0926-3
28. Kogel D, Reimertz C, Mech P, Poppe M, Fruhwald MC, Engemann H, Scheidtmann KH, Prehn JH (2001) Dlk/ZIP kinase-induced apoptosis in human medulloblastoma cells: requirement of the mitochondrial apoptosis pathway. Br J Cancer 85(11):1801-1808
29. Tang HW, Wang YB, Wang SL, Wu MH, Lin SY, Chen GC (2011) Atg1-mediated myosin II activation regulates autophagosome formation during starvation-induced autophagy. EMBO J 30(4):636-651. doi: 10.1038/emboj.2010.338
30. Brognard J, Zhang YW, Puto LA, Hunter T (2011) Cancer-associated loss-of-function mutations implicate DAPK3 as a tumor-suppressing kinase. Cancer Res 71(8):3152-3161. doi: 10.1158/0008-5472.CAN-10-3543
31. Murata-Hori M, Suizu F, Iwasaki T, Kikuchi A, Hosoya H (1999) ZIP kinase identified as a novel myosin regulatory light chain kinase in HeLa cells. FEBS Lett 451(1):81-84
32. Murata-Hori M, Fukuta Y, Ueda K, Iwasaki T, Hosoya H (2001) HeLa ZIP kinase induces diphosphorylation of myosin II regulatory light chain and reorganization of actin filaments in nonmuscle cells. Oncogene 20(57):8175-8183
33. Haystead TA (2005) ZIP kinase, a key regulator of myosin protein phosphatase 1. Cell Signal 17(11):1313-1322. doi: 10.1016/j.cellsig.2005.05.008
34. Sato N, Kawai T, Sugiyama K, Muromoto R, Imoto S, Sekine Y, Ishida M, Akira S, Matsuda T (2005) Physical and functional interactions between STAT3 and ZIP kinase. Int Immunol 17(12):1543-1552. doi: 10.1093/intimm/dxh331
35. Usui T, Okada M, Yamawaki H (2013) Zipper interacting protein kinase (ZIPK): function and signaling. Apoptosis. doi: 10.1007/s10495-013-0934-3
36. Fang J, Menon M, Zhang D, Torbett B, Oxburgh L, Tschan M, Houde E, Wojchowski DM (2008) Attenuation of EPO-dependent erythroblast formation by death-associated protein kinase-2. Blood 112(3):886-890. doi: 10.1182/blood-2008-02-138909
37. Rizzi M, Tschan MP, Britschgi C, Britschgi A, Hugli B, Grob TJ, Leupin N, Mueller BU, Simon HU, Ziemiecki A, Torbett BE, Fey MF, Tobler A (2007) The death-associated protein kinase 2 is up-regulated during normal myeloid differentiation and enhances neutrophil maturation in myeloid leukemic cells. J Leukoc Biol 81(6):1599-1608. doi: 10.1189/jlb.0606400
38. Tur MK, Neef I, Jost E, Galm O, Jager G, Stocker M, Ribbert M, Osieka R, Klinge U, Barth S (2009) Targeted restoration of down-regulated DAPK2 tumor suppressor activity induces apoptosis in Hodgkin lymphoma cells. J Immunother 32(5):431-441. doi: 10.1097/CJI.0b013e31819f1cb6
39. Li H, Ray G, Yoo BH, Erdogan M, Rosen KV (2009) Down-regulation of death-associated protein kinase-2 is required for beta-catenin-induced anoikis resistance of malignant epithelial cells. J Biol Chem 284(4):2012-2022. doi: 10.1074/jbc.M805612200
40. Tereshko V, Teplova M, Brunzelle J, Watterson DM, Egli M (2001) Crystal structures of the catalytic domain of human protein kinase associated with apoptosis and tumor suppression. Nat Struct Biol 8(10):899-907
41. Zimmermann M, Atmanene C, Xu Q, Fouillen L, Van Dorsselaer A, Bonnet D, Marsol C, Hibert M, Sanglier-Cianferani S, Pigault C, McNamara LK, Watterson DM, Haiech J, Kilhoffer MC (2010) Homodimerization of the death-associated protein kinase catalytic domain: development of a new small molecule fluorescent reporter. PLoS One 5(11):e14120. doi: 10.1371/journal.pone.0014120
42. Patel AK, Yadav RP, Majava V, Kursula I, Kursula P (2011) Structure of the dimeric autoinhibited conformation of DAPK2, a pro-apoptotic protein kinase. J Mol Biol 409(3):369-383. doi: 10.1016/j.jmb.2011.03.065
43. Velentza AV, Schumacher AM, Weiss C, Egli M, Watterson DM (2001) A protein kinase associated with apoptosis and tumor suppression: structure, activity, and discovery of peptide substrates. J Biol Chem 276(42):38956-38965
44. Shani G, Marash L, Gozuacik D, Bialik S, Teitelbaum L, Shohat G, Kimchi A (2004) Death-associated protein kinase phosphorylates ZIP kinase, forming a unique kinase hierarchy to activate its cell death functions. Mol Cell Biol 24(19):8611-8626
45. Pike AC, Rellos P, Niesen FH, Turnbull A, Oliver AW, Parker SA, Turk BE, Pearl LH, Knapp S (2008) Activation segment dimerization: a mechanism for kinase autophosphorylation of non-consensus sites. EMBO J 27(4):704-714. doi: 10.1038/emboj.2008.8
46. Nolen B, Taylor S, Ghosh G (2004) Regulation of protein kinases; controlling activity through activation segment conformation. Mol Cell 15(5):661-675
47. Graves PR, Winkfield KM, Haystead TA (2005) Regulation of zipper-interacting protein kinase activity in vitro and in vivo by multisite phosphorylation. J Biol Chem 280(10):9363-9374
48. Temmerman K, Simon B, Wilmanns M (2013) Structural and functional diversity in the activity and regulation of DAPK-related protein kinases. FEBS J. doi: 10.1111/febs.12384
49. Citri A, Harari D, Shohat G, Ramakrishnan P, Gan J, Lavi S, Eisenstein M, Kimchi A, Wallach D, Pietrokovski S, Yarden Y (2006) Hsp90 recognizes a common surface on client kinases. J Biol Chem 281(20):14361-14369. doi: 10.1074/jbc.M512613200
50. de Diego I, Kuper J, Bakalova N, Kursula P, Wilmanns M (2010) Molecular basis of the death-associated protein kinase-calcium/calmodulin regulator complex. Sci Signal 3(106):ra6. doi: 10.1126/scisignal.2000552
51. Anjum R, Roux PP, Ballif BA, Gygi SP, Blenis J (2005) The tumor suppressor DAP kinase is a target of RSK-mediated survival signaling. Curr Biol 15(19):1762-1767. doi: 10.1016/j.cub.2005.08.050
52. Shani G, Henis-Korenblit S, Jona G, Gileadi O, Eisenstein M, Ziv T, Admon A, Kimchi A (2001) Autophosphorylation restrains the apoptotic activity of DRP-1 kinase by controlling dimerization and calmodulin binding. EMBO J 20(5):1099-1113
53. Shohat G, Spivak-Kroizman T, Cohen O, Bialik S, Shani G, Berrisi H, Eisenstein M, Kimchi A (2001) The pro-apoptotic function of death-associated protein kinase is controlled by a unique inhibitory autophosphorylation-based mechanism. J Biol Chem 276(50):47460-47467
54. Carlessi R, Levin-Salomon V, Ciprut S, Bialik S, Berissi H, Albeck S, Peleg Y, Kimchi A (2011) GTP binding to the ROC domain of DAP-kinase regulates its function through intramolecular signalling. EMBO Rep 12(9):917-923. doi: 10.1038/embor.2011.126
55. Gozuacik D, Bialik S, Raveh T, Mitou G, Shohat G, Sabanay H, Mizushima N, Yoshimori T, Kimchi A (2008) DAP-kinase is a mediator of endoplasmic reticulum stress-induced caspase activation and autophagic cell death. Cell Death Differ 15(12):1875-1886. doi: 10.1038/cdd.2008.121
56. Guenebeaud C, Goldschneider D, Castets M, Guix C, Chazot G, Delloye-Bourgeois C, Eisenberg-Lerner A, Shohat G, Zhang M, Laudet V, Kimchi A, Bernet A, Mehlen P (2010) The dependence receptor UNC5H2/B triggers apoptosis via PP2A-mediated dephosphorylation of DAP kinase. Mol Cell 40(6):863-876. doi: 10.1016/j.molcel.2010.11.021
57. Widau RC, Jin Y, Dixon SA, Wadzinski BE, Gallagher PJ (2010) Protein phosphatase 2A (PP2A) holoenzymes regulate death-associated protein kinase (DAPK) in ceramide-induced anoikis. J Biol Chem 285(18):13827-13838. doi: 10.1074/jbc.M109.085076
58. Dagher R, Peng S, Gioria S, Feve M, Zeniou M, Zimmermann M, Pigault C, Haiech J (1813) Kilhoffer MC (2011) A general strategy to characterize calmodulin-calcium complexes involved in CaM-target recognition: DAPK and EGFR calmodulin binding domains interact with different calmodulin-calcium complexes. Biochim Biophys Acta 5:1059-1067. doi: 10.1016/j.bbamcr.2010.11.004
59. Raveh T, Berissi H, Eisenstein M, Spivak T, Kimchi A (2000) A functional genetic screen identifies regions at the C-terminal tail and death-domain of death-associated protein kinase that are critical for its proapoptotic activity. Proc Natl Acad Sci USA 97(4):1572-1577
60. Jin Y, Blue EK, Dixon S, Shao Z, Gallagher PJ (2002) A death-associated protein kinase (DAPK)-interacting protein, DIP-1, is an E3 ubiquitin ligase that promotes tumor necrosis factor-induced apoptosis and regulates the cellular levels of DAPK. J Biol Chem 277(49):46980-46986
61. Capoccia BJ, Jin RU, Kong YY, Peek RM Jr, Fassan M, Rugge M, Mills JC (2013) The ubiquitin ligase Mindbomb 1 coordinates gastrointestinal secretory cell maturation. J Clin Invest 123(4):1475-1491. doi: 10.1172/JCI65703
62. Wang WJ, Kuo JC, Ku W, Lee YR, Lin FC, Chang YL, Lin YM, Chen CH, Huang YP, Chiang MJ, Yeh SW, Wu PR, Shen CH, Wu CT, Chen RH (2007) The tumor suppressor DAPK is reciprocally regulated by tyrosine kinase Src and phosphatase LAR. Mol Cell 27(5):701-716. doi: 10.1016/j.molcel.2007.06.037
63. Klein CL, Rovelli G, Springer W, Schall C, Gasser T, Kahle PJ (2009) Homo- and heterodimerization of ROCO kinases: LRRK2 kinase inhibition by the LRRK2 ROCO fragment. J Neurochem 111(3):703-715. doi: 10.1111/j.1471-4159.2009. 06358.x
64. Lee TH, Chen C-H, Suizu F, Huang P, Schiene-Fischer C, Daum S, Zhang YJ, Goate A, Chen R-H, Zhou XZ, Lu KP (2011) Death-associated protein kinase 1 phosphorylates pin1 and inhibits its prolyl isomerase activity and cellular function. Mol Cell 42(2):147-159
65. Cohen O, Inbal B, Kissil JL, Raveh T, Berissi H, Spivak-Kroizaman T, Feinstein E, Kimchi A (1999) DAP-kinase participates in TNF-alpha- and Fas-induced apoptosis and its function requires the death domain. J Cell Biol 146(1):141-148
66. Chen CH, Wang WJ, Kuo JC, Tsai HC, Lin JR, Chang ZF, Chen RH (2005) Bidirectional signals transduced by DAPK-ERK interaction promote the apoptotic effect of DAPK. EMBO J 24(2):294-304
67. Llambi F, Lourenco FC, Gozuacik D, Guix C, Pays L, Del Rio G, Kimchi A, Mehlen P (2005) The dependence receptor UNC5H2 mediates apoptosis through DAP-kinase. EMBO J 24(6):1192-1201
68. Lee YR, Yuan WC, Ho HC, Chen CH, Shih HM, Chen RH (2010) The Cullin 3 substrate adaptor KLHL20 mediates DAPK ubiquitination to control interferon responses. EMBO J 29(10):1748-1761. doi: 10.1038/emboj.2010.62
69. Wu PR, Tsai PI, Chen GC, Chou HJ, Huang YP, Chen YH, Lin MY, Kimchi A, Chien CT, Chen RH (2011) DAPK activates MARK1/2 to regulate microtubule assembly, neuronal differentiation, and tau toxicity. Cell Death Differ 18(9):1507-1520. doi: 10.1038/cdd.2011.2
70. Mor I, Carlessi R, Ast T, Feinstein E, Kimchi A (2011) Death-associated protein kinase increases glycolytic rate through binding and activation of pyruvate kinase. Oncogene 31(6):683-693. doi: 10.1038/onc.2011.264
71. Stevens C, Lin Y, Harrison B, Burch L, Ridgway RA, Sansom O, Hupp T (2009) Peptide combinatorial libraries identify TSC2 as a death-associated protein kinase (DAPK) death domain-binding protein and reveal a stimulatory role for DAPK in mTORC1 signaling. J Biol Chem 284(1):334-344. doi: 10.1074/jbc.M805165200
72. Kogel D, Bierbaum H, Preuss U, Scheidtmann KH (1999) C-terminal truncation of Dlk/ZIP kinase leads to abrogation of nuclear transport and high apoptotic activity. Oncogene 18(51):7212-7218
73. Shoval Y, Pietrokovski S, Kimchi A (2007) ZIPK: a unique case of murine-specific divergence of a conserved vertebrate gene. PLoS Genet 3(10):1884-1893. doi: 10.1371/journal.pgen.0030180
74. Page G, Kogel D, Rangnekar V, Scheidtmann KH (1999) Interaction partners of Dlk/ZIP kinase: co-expression of Dlk/ZIP kinase and Par-4 results in cytoplasmic retention and apoptosis. Oncogene 18(51):7265-7273
75. Vetterkind S, Illenberger S, Kubicek J, Boosen M, Appel S, Naim HY, Scheidtmann KH, Preuss U (2005) Binding of Par-4 to the actin cytoskeleton is essential for Par-4/Dlk-mediated apoptosis. Exp Cell Res 305(2):392-408
76. Nehru V, Almeida FN, Aspenstrom P (2013) Interaction of RhoD and ZIP kinase modulates actin filament assembly and focal adhesion dynamics. Biochem Biophys Res Commun 433(2):163-169. doi: 10.1016/j.bbrc.2013.02.046
77. Shoval Y, Berissi H, Kimchi A, Pietrokovski S (2011) New modularity of DAP-kinases: alternative splicing of the DRP-1 gene produces a ZIPk-like isoform. PLoS One 6(2):e17344