Death-associated protein kinase: A molecule with functional antagonistic duality and a potential role in inflammatory bowel disease (Review)
- Authors:
- Sara Steinmann
- Kristina Scheibe
- Katharina Erlenbach-Wuensch
- Clemens Neufert
- Regine Schneider-Stock
-
Affiliations: Experimental Tumorpathology, Institute of Pathology, FAU Erlangen-Nürnberg, 91054 Erlangen, Germany, Department of Medicine 1, University Hospital Erlangen, FAU Erlangen-Nürnberg, Kussmaul Campus for Medical Research, 91052 Erlangen, Germany, Institute of Pathology, FAU Erlangen-Nürnberg, 91054 Erlangen, Germany - Published online on: May 11, 2015 https://doi.org/10.3892/ijo.2015.2998
- Pages: 5-15
-
Copyright: © Steinmann et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 3.0].
This article is mentioned in:
Abstract
Schneider-Stock R: Death-associated kinase (DAPK): a cancer ‘gene chameleon’. Apoptosis. 19:2852014. View Article : Google Scholar | |
Ivanovska J, Tregubova A, Mahadevan V, Chakilam S, Gandesiri M, Benderska N, Ettle B, Hartmann A, Söder S, Ziesché E, et al: Identification of DAPK as a scaffold protein for the LIMK/cofilin complex in TNF-induced apoptosis. Int J Biochem Cell Biol. 45:1720–1729. 2013. View Article : Google Scholar : PubMed/NCBI | |
Cohen O, Inbal B, Kissil JL, Raveh T, Berissi H, Spivak-Kroizaman T, Feinstein E and Kimchi A: DAP-kinase participates in TNF-alpha- and Fas-induced apoptosis and its function requires the death domain. J Cell Biol. 146:141–148. 1999. View Article : Google Scholar : PubMed/NCBI | |
Bialik S and Kimchi A: The death-associated protein kinases: Structure, function, and beyond. Annu Rev Biochem. 75:189–210. 2006. View Article : Google Scholar : PubMed/NCBI | |
Gautel M: Cytoskeletal protein kinases: Titin and its relations in mechanosensing. Pflugers Arch. 462:119–134. 2011. View Article : Google Scholar : PubMed/NCBI | |
Brenner H, Kloor M and Pox CP: Colorectal cancer. Lancet. 383:1490–1502. 2014. View Article : Google Scholar | |
Wu WK, Wang XJ, Cheng AS, Luo MX, Ng SS, To KF, Chan FK, Cho CH, Sung JJ and Yu J: Dysregulation and crosstalk of cellular signaling pathways in colon carcinogenesis. Crit Rev Oncol Hematol. 86:251–277. 2013. View Article : Google Scholar : PubMed/NCBI | |
Jass JR: Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology. 50:113–130. 2007. View Article : Google Scholar : PubMed/NCBI | |
Draht MX, Riedl RR, Niessen H, Carvalho B, Meijer GA, Herman JG, van Engeland M, Melotte V and Smits KM: Promoter CpG island methylation markers in colorectal cancer: The road ahead. Epigenomics. 4:179–194. 2012. View Article : Google Scholar : PubMed/NCBI | |
Feagins LA, Souza RF and Spechler SJ: Carcinogenesis in IBD: Potential targets for the prevention of colorectal cancer. Nat Rev Gastroenterol Hepatol. 6:297–305. 2009. View Article : Google Scholar : PubMed/NCBI | |
Itzkowitz SH and Yio X: Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: The role of inflammation. Am J Physiol Gastrointest Liver Physiol. 287:G7–G17. 2004. View Article : Google Scholar : PubMed/NCBI | |
Mittag F, Kuester D, Vieth M, Peters B, Stolte B, Roessner A and Schneider-Stock R: DAPK promotor methylation is an early event in colorectal carcinogenesis. Cancer Lett. 240:69–75. 2006. View Article : Google Scholar | |
Chen HY, Lee YR and Chen RH: The functions and regulations of DAPK in cancer metastasis. Apoptosis. 19:364–370. 2014. View Article : Google Scholar | |
Bajbouj K, Poehlmann A, Kuester D, Drewes T, Haase K, Hartig R, Teller A, Kliche S, Walluscheck D, Ivanovska J, et al: Identification of phosphorylated p38 as a novel DAPK-interacting partner during TNFalpha-induced apoptosis in colorectal tumor cells. Am J Pathol. 175:557–570. 2009. View Article : Google Scholar : PubMed/NCBI | |
Kuester D, Guenther T, Biesold S, Hartmann A, Bataille F, Ruemmele P, Peters B, Meyer F, Schubert D, Bohr UR, et al: Aberrant methylation of DAPK in long-standing ulcerative colitis and ulcerative colitis-associated carcinoma. Pathol Res Pract. 206:616–624. 2010. View Article : Google Scholar : PubMed/NCBI | |
Chakilam S, Gandesiri M, Rau TT, Agaimy A, Vijayalakshmi M, Ivanovska J, Wirtz RM, Schulze-Luehrmann J, Benderska N, Wittkopf N, et al: Death-associated protein kinase controls STAT3 activity in intestinal epithelial cells. Am J Pathol. 182:1005–1020. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kawai T, Matsumoto M, Takeda K, Sanjo H and Akira S: ZIP kinase, a novel serine/threonine kinase which mediates apoptosis. Mol Cell Biol. 18:1642–1651. 1998.PubMed/NCBI | |
Kögel D, Plöttner O, Landsberg G, Christian S and Scheidtmann KH: Cloning and characterization of Dlk, a novel serine/threonine kinase that is tightly associated with chromatin and phosphorylates core histones. Oncogene. 17:2645–2654. 1998. View Article : Google Scholar : PubMed/NCBI | |
Inbal B, Shani G, Cohen O, Kissil JL and Kimchi A: Death-associated protein kinase-related protein 1, a novel serine/threonine kinase involved in apoptosis. Mol Cell Biol. 20:1044–1054. 2000. View Article : Google Scholar : PubMed/NCBI | |
Kawai T, Nomura F, Hoshino K, Copeland NG, Gilbert DJ, Jenkins NA and Akira S: Death-associated protein kinase 2 is a new calcium/calmodulin-dependent protein kinase that signals apoptosis through its catalytic activity. Oncogene. 18:3471–3480. 1999. View Article : Google Scholar : PubMed/NCBI | |
Benderska N and Schneider-Stock R: Transcription control of DAPK. Apoptosis. 19:298–305. 2014. View Article : Google Scholar | |
Dagher R, Peng S, Gioria S, Fève M, Zeniou M, Zimmermann M, Pigault C, Haiech J and Kilhoffer MC: 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. 1813.1059–1067. 2011. | |
de Diego I, Kuper J, Bakalova N, Kursula P and Wilmanns M: Molecular basis of the death-associated protein kinase-calcium/calmodulin regulator complex. Sci Signal. 3:ra62010. View Article : Google Scholar : PubMed/NCBI | |
Wang WJ, Kuo JC, Ku W, Lee YR, Lin FC, Chang YL, Lin YM, Chen CH, Huang YP, Chiang MJ, et al: The tumor suppressor DAPK is reciprocally regulated by tyrosine kinase Src and phosphatase LAR. Mol Cell. 27:701–716. 2007. View Article : Google Scholar : PubMed/NCBI | |
Bialik S and Kimchi A: Biochemical and functional characterization of the ROC domain of DAPK establishes a new paradigm of GTP regulation in ROCO proteins. Biochem Soc Trans. 40:1052–1057. 2012. View Article : Google Scholar : PubMed/NCBI | |
Carlessi R, Levin-Salomon V, Ciprut S, Bialik S, Berissi H, Albeck S, Peleg Y and Kimchi A: GTP binding to the ROC domain of DAP-kinase regulates its function through intra-molecular signalling. EMBO Rep. 12:917–923. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kim BM, You MH, Chen CH, Lee S, Hong Y, Hong Y, Kimchi A, Zhou XZ and Lee TH: Death-associated protein kinase 1 has a critical role in aberrant tau protein regulation and function. Cell Death Dis. 5:e12372014. View Article : Google Scholar : PubMed/NCBI | |
Stevens C, Lin Y, Harrison B, Burch L, Ridgway RA, Sansom O and Hupp T: 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. 284:334–344. 2009. View Article : Google Scholar | |
Kissil JL, Feinstein E, Cohen O, Jones PA, Tsai YC, Knowles MA, Eydmann ME and Kimchi A: DAP-kinase loss of expression in various carcinoma and B-cell lymphoma cell lines: Possible implications for role as tumor suppressor gene. Oncogene. 15:403–407. 1997. View Article : Google Scholar : PubMed/NCBI | |
Leung RC, Liu SS, Chan KY, Tam KF, Chan KL, Wong LC and Ngan HY: Promoter methylation of death-associated protein kinase and its role in irradiation response in cervical cancer. Oncol Rep. 19:1339–1345. 2008.PubMed/NCBI | |
Shanmugam R, Gade P, Wilson-Weekes A, Sayar H, Suvannasankha A, Goswami C, Li L, Gupta S, Cardoso AA, Al Baghdadi T, et al: A noncanonical Flt3ITD/NF-κB signaling pathway represses DAPK1 in acute myeloid leukemia. Clin Cancer Res. 18:360–369. 2012. View Article : Google Scholar | |
Hayakawa J, Mittal S, Wang Y, Korkmaz KS, Adamson E, English C, Ohmichi M, McClelland M and Mercola D: Identification of promoters bound by c-Jun/ATF2 during rapid large-scale gene activation following genotoxic stress. Mol Cell. 16:521–535. 2004. View Article : Google Scholar : PubMed/NCBI | |
Martoriati A, Doumont G, Alcalay M, Bellefroid E, Pelicci PG and Marine JC: dapk1, encoding an activator of a p19ARF-p53-mediated apoptotic checkpoint, is a transcription target of p53. Oncogene. 24:1461–1466. 2005. View Article : Google Scholar | |
Gade P, Roy SK, Li H, Nallar SC and Kalvakolanu DV: Critical role for transcription factor C/EBP-beta in regulating the expression of death-associated protein kinase 1. Mol Cell Biol. 28:2528–2548. 2008. View Article : Google Scholar : PubMed/NCBI | |
Benderska N, Ivanovska J, Rau TT, Schulze-Luehrmann J, Mohan S, Chakilam S, Gandesiri M, Ziesché E, Fischer T, Söder S, et al: DAPK-HSF1 interaction as a new positive feedback loop for TNF-induced apoptosis in colorectal cancer cells. J Cell Sci. 127:5273–5287. 2014. View Article : Google Scholar : PubMed/NCBI | |
Massagué J, Seoane J and Wotton D: Smad transcription factors. Genes Dev. 19:2783–2810. 2005. View Article : Google Scholar : PubMed/NCBI | |
Gandesiri M, Chakilam S, Ivanovska J, Benderska N, Ocker M, Di Fazio P, Feoktistova M, Gali-Muhtasib H, Rave-Fränk M, Prante O, et al: DAPK plays an important role in panobinostat-induced autophagy and commits cells to apoptosis under autophagy deficient conditions. Apoptosis. 17:1300–1315. 2012. View Article : Google Scholar : PubMed/NCBI | |
Jin Y and Gallagher PJ: Antisense depletion of death-associated protein kinase promotes apoptosis. J Biol Chem. 278:51587–51593. 2003. View Article : Google Scholar : PubMed/NCBI | |
Zhang L, Nephew KP and Gallagher PJ: Regulation of death-associated protein kinase. Stabilization by HSP90 hetero-complexes. J Biol Chem. 282:11795–11804. 2007. View Article : Google Scholar : PubMed/NCBI | |
Jin Y, Blue EK, Dixon S, Shao Z and Gallagher PJ: 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. 277:46980–46986. 2002. View Article : Google Scholar : PubMed/NCBI | |
Lee YR, Yuan WC, Ho HC, Chen CH, Shih HM and Chen RH: The Cullin 3 substrate adaptor KLHL20 mediates DAPK ubiquitination to control interferon responses. EMBO J. 29:1748–1761. 2010. View Article : Google Scholar : PubMed/NCBI | |
Gallagher PJ and Blue EK: Post-translational regulation of the cellular levels of DAPK. Apoptosis. 19:306–315. 2014. View Article : Google Scholar | |
Lin Y, Stevens C and Hupp T: Identification of a dominant negative functional domain on DAPK-1 that degrades DAPK-1 protein and stimulates TNFR-1-mediated apoptosis. J Biol Chem. 282:16792–16802. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lin Y, Hupp TR and Stevens C: Death-associated protein kinase (DAPK) and signal transduction: Additional roles beyond cell death. FEBS J. 277:48–57. 2010. View Article : Google Scholar | |
Benderska N, Chakilam S, Hugle M, Ivanovska J, Gandesiri M, Schulze-Luhrmann J, Bajbouj K, Croner R and Schneider-Stock R: Apoptosis signalling activated by TNF in the lower gastrointestinal tract--review. Curr Pharm Biotechnol. 13:2248–2258. 2012. View Article : Google Scholar | |
Henshall DC, Araki T, Schindler CK, Shinoda S, Lan JQ and Simon RP: Expression of death-associated protein kinase and recruitment to the tumor necrosis factor signaling pathway following brief seizures. J Neurochem. 86:1260–1270. 2003. View Article : Google Scholar : PubMed/NCBI | |
Zalckvar E, Berissi H, Mizrachy L, Idelchuk Y, Koren I, Eisenstein M, Sabanay H, Pinkas-Kramarski R and Kimchi A: DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO Rep. 10:285–292. 2009. View Article : Google Scholar : PubMed/NCBI | |
Chen CH, Wang WJ, Kuo JC, Tsai HC, Lin JR, Chang ZF and Chen RH: Bidirectional signals transduced by DAPK-ERK interaction promote the apoptotic effect of DAPK. EMBO J. 24:294–304. 2005. View Article : Google Scholar : | |
Anjum R, Roux PP, Ballif BA, Gygi SP and Blenis J: The tumor suppressor DAP kinase is a target of RSK-mediated survival signaling. Curr Biol. 15:1762–1767. 2005. View Article : Google Scholar : PubMed/NCBI | |
Eisenberg-Lerner A and Kimchi A: DAP kinase regulates JNK signaling by binding and activating protein kinase D under oxidative stress. Cell Death Differ. 14:1908–1915. 2007. View Article : Google Scholar : PubMed/NCBI | |
Shani G, Marash L, Gozuacik D, Bialik S, Teitelbaum L, Shohat G and Kimchi A: Death-associated protein kinase phosphorylates ZIP kinase, forming a unique kinase hierarchy to activate its cell death functions. Mol Cell Biol. 24:8611–8626. 2004. View Article : Google Scholar : PubMed/NCBI | |
Kuo JC, Lin JR, Staddon JM, Hosoya H and Chen RH: Uncoordinated regulation of stress fibers and focal adhesions by DAP kinase. J Cell Sci. 116:4777–4790. 2003. View Article : Google Scholar : PubMed/NCBI | |
Houle F, Poirier A, Dumaresq J and Huot J: DAP kinase mediates the phosphorylation of tropomyosin-1 downstream of the ERK pathway, which regulates the formation of stress fibers in response to oxidative stress. J Cell Sci. 120:3666–3677. 2007. View Article : Google Scholar : PubMed/NCBI | |
Bialik S, Berissi H and Kimchi A: A high throughput proteomics screen identifies novel substrates of death-associated protein kinase. Mol Cell Proteomics. 7:1089–1098. 2008. View Article : Google Scholar : PubMed/NCBI | |
Schumacher AM, Schavocky JP, Velentza AV, Mirzoeva S and Watterson DM: A calmodulin-regulated protein kinase linked to neuron survival is a substrate for the calmodulin-regulated death-associated protein kinase. Biochemistry. 43:8116–8124. 2004. View Article : Google Scholar : PubMed/NCBI | |
Fraser JA and Hupp TR: Chemical genetics approach to identify peptide ligands that selectively stimulate DAPK-1 kinase activity. Biochemistry. 46:2655–2673. 2007. View Article : Google Scholar : PubMed/NCBI | |
Schumacher AM, Velentza AV, Watterson DM and Dresios J: Death-associated protein kinase phosphorylates mammalian ribosomal protein S6 and reduces protein synthesis. Biochemistry. 45:13614–13621. 2006. View Article : Google Scholar : PubMed/NCBI | |
Tian JH, Das S and Sheng ZH: Ca2+-dependent phosphorylation of syntaxin-1A by the death-associated protein (DAP) kinase regulates its interaction with Munc18. J Biol Chem. 278:26265–26274. 2003. View Article : Google Scholar : PubMed/NCBI | |
Danese S and Fiocchi C: Ulcerative colitis. N Engl J Med. 365:1713–1725. 2011. View Article : Google Scholar : PubMed/NCBI | |
Baumgart DC and Sandborn WJ: Crohn’s disease. Lancet. 380:1590–1605. 2012. View Article : Google Scholar : PubMed/NCBI | |
Atreya R and Neurath MF: IBD pathogenesis in 2014: Molecular pathways controlling barrier function in IBD. Nat Rev Gastroenterol Hepatol. 12:67–68. 2014. View Article : Google Scholar : PubMed/NCBI | |
Strober W, Fuss I and Mannon P: The fundamental basis of inflammatory bowel disease. J Clin Invest. 117:514–521. 2007. View Article : Google Scholar : PubMed/NCBI | |
Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA, et al: International IBD Genetics Consortium (IIBDGC): Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 491:119–124. 2012. View Article : Google Scholar : PubMed/NCBI | |
Neurath MF: Cytokines in inflammatory bowel disease. Nat Rev Immunol. 14:329–342. 2014. View Article : Google Scholar : PubMed/NCBI | |
Feagan BG, Rutgeerts P, Sands BE, Hanauer S, Colombel JF, Sandborn WJ, Van Assche G, Axler J, Kim HJ, Danese S, et al: GEMINI 1 Study Group: Vedolizumab as induction and maintenance therapy for ulcerative colitis. N Engl J Med. 369:699–710. 2013. View Article : Google Scholar : PubMed/NCBI | |
Sandborn WJ, Feagan BG, Rutgeerts P, Hanauer S, Colombel JF, Sands BE, Lukas M, Fedorak RN, Lee S, Bressler B, et al: GEMINI 2 Study Group: Vedolizumab as induction and maintenance therapy for Crohn’s disease. N Engl J Med. 369:711–721. 2013. View Article : Google Scholar : PubMed/NCBI | |
Atreya R, Zimmer M, Bartsch B, Waldner MJ, Atreya I, Neumann H, Hildner K, Hoffman A, Kiesslich R, Rink AD, et al: Antibodies against tumor necrosis factor (TNF) induce T-cell apoptosis in patients with inflammatory bowel diseases via TNF receptor 2 and intestinal CD14+ macrophages. Gastroenterology. 141:2026–2038. 2011. View Article : Google Scholar : PubMed/NCBI | |
Lai MZ and Chen RH: Regulation of inflammation by DAPK. Apoptosis. 19:357–363. 2014. View Article : Google Scholar | |
Backert I, Koralov SB, Wirtz S, Kitowski V, Billmeier U, Martini E, Hofmann K, Hildner K, Wittkopf N, Brecht K, et al: STAT3 activation in Th17 and Th22 cells controls IL-22-mediated epithelial host defense during infectious colitis. J Immunol. 193:3779–3791. 2014. View Article : Google Scholar : PubMed/NCBI | |
Pickert G, Neufert C, Leppkes M, Zheng Y, Wittkopf N, Warntjen M, Lehr HA, Hirth S, Weigmann B, Wirtz S, et al: STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J Exp Med. 206:1465–1472. 2009. View Article : Google Scholar : PubMed/NCBI | |
Atreya R, Neumann H, Neufert C, Waldner MJ, Billmeier U, Zopf Y, Willma M, App C, Münster T, Kessler H, et al: In vivo imaging using fluorescent antibodies to tumor necrosis factor predicts therapeutic response in Crohn’s disease. Nat Med. 20:313–318. 2014. View Article : Google Scholar : PubMed/NCBI | |
Jin Y, Blue EK and Gallagher PJ: Control of death-associated protein kinase (DAPK) activity by phosphorylation and proteasomal degradation. J Biol Chem. 281:39033–39040. 2006. View Article : Google Scholar : PubMed/NCBI | |
Yoo HJ, Byun HJ, Kim BR, Lee KH, Park SY and Rho SB: DAPk1 inhibits NF-κB activation through TNF-α and INF-γ-induced apoptosis. Cell Signal. 24:1471–1477. 2012. View Article : Google Scholar : PubMed/NCBI | |
Chuang YT, Fang LW, Lin-Feng MH, Chen RH and Lai MZ: The tumor suppressor death-associated protein kinase targets to TCR-stimulated NF-kappa B activation. J Immunol. 180:3238–3249. 2008. View Article : Google Scholar : PubMed/NCBI | |
Chuang YT, Lin YC, Lin KH, Chou TF, Kuo WC, Yang KT, Wu PR, Chen RH, Kimchi A and Lai MZ: Tumor suppressor death-associated protein kinase is required for full IL-1β production. Blood. 117:960–970. 2011. View Article : Google Scholar | |
Turner-Brannen E, Choi KY, Arsenault R, El-Gabalawy H, Napper S and Mookherjee N: Inflammatory cytokines IL-32 and IL-17 have common signaling intermediates despite differential dependence on TNF-receptor 1. J Immunol. 186:7127–7135. 2011. View Article : Google Scholar : PubMed/NCBI | |
Nakav S, Cohen S, Feigelson SW, Bialik S, Shoseyov D, Kimchi A and Alon R: Tumor suppressor death-associated protein kinase attenuates inflammatory responses in the lung. Am J Respir Cell Mol Biol. 46:313–322. 2012. View Article : Google Scholar | |
Bauer C, Duewell P, Mayer C, Lehr HA, Fitzgerald KA, Dauer M, Tschopp J, Endres S, Latz E and Schnurr M: Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut. 59:1192–1199. 2010. View Article : Google Scholar : PubMed/NCBI | |
Schoultz I, Verma D, Halfvarsson J, Törkvist L, Fredrikson M, Sjöqvist U, Lördal M, Tysk C, Lerm M, Söderkvist P, et al: Combined polymorphisms in genes encoding the inflammasome components NALP3 and CARD8 confer susceptibility to Crohn’s disease in Swedish men. Am J Gastroenterol. 104:1180–1188. 2009. View Article : Google Scholar : PubMed/NCBI | |
Fantini MC, Rizzo A, Fina D, Caruso R, Sarra M, Stolfi C, Becker C, Macdonald TT, Pallone F, Neurath MF and Monteleone G: Smad7 controls resistance of colitogenic T cells to regulatory T cell-mediated suppression. Gastroenterology. 136:1308–1316. e1–3. 2009. View Article : Google Scholar : PubMed/NCBI | |
Monteleone G, Fantini MC, Onali S, Zorzi F, Sancesario G, Bernardini S, Calabrese E, Viti F, Monteleone I, Biancone L and Pallone F: Phase I clinical trial of Smad7 knockdown using antisense oligonucleotide in patients with active Crohn’s disease. Mol Ther. 20:870–876. 2012. View Article : Google Scholar : PubMed/NCBI | |
Jang CW, Chen CH, Chen CC, Chen JY, Su YH and Chen RH: TGF-beta induces apoptosis through Smad-mediated expression of DAP-kinase. Nat Cell Biol. 4:51–58. 2002. View Article : Google Scholar | |
MacDonald TT, Monteleone I, Fantini MC and Monteleone G: Regulation of homeostasis and inflammation in the intestine. Gastroenterology. 140:1768–1775. 2011. View Article : Google Scholar : PubMed/NCBI | |
Shiloh R, Bialik S and Kimchi A: The DAPK family: a structure-function analysis. Apoptosis. 19:286–297. 2014. View Article : Google Scholar | |
Ekbom A, Helmick C, Zack M and Adami HO: Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med. 323:1228–1233. 1990. View Article : Google Scholar : PubMed/NCBI | |
Mathy C, Schneider K, Chen YY, Varma M, Terdiman JP and Mahadevan U: Gross versus microscopic pancolitis and the occurrence of neoplasia in ulcerative colitis. Inflamm Bowel Dis. 9:351–355. 2003. View Article : Google Scholar : PubMed/NCBI | |
Rutter M, Saunders B, Wilkinson K, Rumbles S, Schofield G, Kamm M, Williams C, Price A, Talbot I and Forbes A: Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology. 126:451–459. 2004. View Article : Google Scholar : PubMed/NCBI | |
Broomé U, Lindberg G and Löfberg R: Primary sclerosing cholangitis in ulcerative colitis - a risk factor for the development of dysplasia and DNA aneuploidy? Gastroenterology. 102:1877–1880. 1992. | |
Van Assche G, Dignass A, Bokemeyer B, Danese S, Gionchetti P, Moser G, Beaugerie L, Gomollón F, Häuser W, Herrlinger K, et al: European Crohn’s and Colitis Organisation: Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 3: Special situations. J Crohn’s Colitis. 7:1–33. 2013. View Article : Google Scholar | |
Ullman TA and Itzkowitz SH: Intestinal inflammation and cancer. Gastroenterology. 140:1807–1816. 2011. View Article : Google Scholar : PubMed/NCBI | |
Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, Nakamura Y, White R, Smits AM and Bos JL: Genetic alterations during colorectal-tumor development. N Engl J Med. 319:525–532. 1988. View Article : Google Scholar : PubMed/NCBI | |
Fearon ER: Molecular genetics of colorectal cancer. Annu Rev Pathol. 6:479–507. 2011. View Article : Google Scholar | |
Hussain SP, Amstad P, Raja K, Ambs S, Nagashima M, Bennett WP, Shields PG, Ham AJ, Swenberg JA, Marrogi AJ, et al: Increased p53 mutation load in noncancerous colon tissue from ulcerative colitis: A cancer-prone chronic inflammatory disease. Cancer Res. 60:3333–3337. 2000.PubMed/NCBI | |
Redston MS, Papadopoulos N, Caldas C, Kinzler KW and Kern SE: Common occurrence of APC and K-ras gene mutations in the spectrum of colitis-associated neoplasias. Gastroenterology. 108:383–392. 1995. View Article : Google Scholar : PubMed/NCBI | |
Michie AM, McCaig AM, Nakagawa R and Vukovic M: Death-associated protein kinase (DAPK) and signal transduction: Regulation in cancer. FEBS J. 277:74–80. 2010. View Article : Google Scholar | |
Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, Vallabhapurapu S, Scheller J, Rose-John S, Cheroutre H, Eckmann L, et al: IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell. 15:103–113. 2009. View Article : Google Scholar : PubMed/NCBI | |
Neufert C, Becker C, Türeci Ö, Waldner MJ, Backert I, Floh K, Atreya I, Leppkes M, Jefremow A, Vieth M, et al: Tumor fibroblast-derived epiregulin promotes growth of colitis-associated neoplasms through ERK. J Clin Invest. 123:1428–1443. 2013. View Article : Google Scholar : PubMed/NCBI | |
Salcedo R, Worschech A, Cardone M, Jones Y, Gyulai Z, Dai RM, Wang E, Ma W, Haines D, O’hUigin C, et al: MyD88-mediated signaling prevents development of adenocarcinomas of the colon: Role of interleukin 18. J Exp Med. 207:1625–1636. 2010. View Article : Google Scholar : PubMed/NCBI | |
Popivanova BK, Kitamura K, Wu Y, Kondo T, Kagaya T, Kaneko S, Oshima M, Fujii C and Mukaida N: Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest. 118:560–570. 2008.PubMed/NCBI | |
D’Incà R, Cardin R, Benazzato L, Angriman I, Martines D and Sturniolo GC: Oxidative DNA damage in the mucosa of ulcerative colitis increases with disease duration and dysplasia. Inflamm Bowel Dis. 10:23–27. 2004. View Article : Google Scholar | |
Goel A and Boland CR: Epigenetics of colorectal cancer. Gastroenterology. 143:1442–1460. e12012. View Article : Google Scholar : PubMed/NCBI | |
Schneider-Stock R, Kuester D, Ullrich O, Mittag F, Habold C, Boltze C, Peters B, Krueger S, Hintze C, Meyer F, et al: Close localization of DAP-kinase positive tumour-associated macrophages and apoptotic colorectal cancer cells. J Pathol. 209:95–105. 2006. View Article : Google Scholar : PubMed/NCBI | |
Mukhopadhyay R, Ray PS, Arif A, Brady AK, Kinter M and Fox PL: DAPK-ZIPK-L13a axis constitutes a negative-feedback module regulating inflammatory gene expression. Mol Cell. 32:371–382. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kamal M, Pawlak A, BenMohamed F, Valanciuté A, Dahan K, Candelier M, Lang P, Guellaën G and Sahali D: C-mip interacts with the p85 subunit of PI3 kinase and exerts a dual effect on ERK signaling via the recruitment of Dip1 and DAP kinase. FEBS Lett. 584:500–506. 2010. View Article : Google Scholar |