APPL proteins modulate DNA repair and radiation survival of pancreatic carcinoma cells by regulating ATM

Cell Death and Disease

Volumn 5, Issue 4, 2014, Pages

  Hennig, J ^a   McShane, M P ^b   Cordes, N ^a   Eke, I ^a  

^a UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

APPL; ATM; DNA repair; Pancreatic cancer; Radioresistance

Indexed keywords

ADAPTOR PROTEIN; ATM PROTEIN; DNA; LEUCINE ZIPPER PROTEIN; PHOSPHOTYROSINE; PLECKSTRIN; SMALL INTERFERING RNA; APPL1 PROTEIN, HUMAN; APPL2 PROTEIN, HUMAN; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; BASIC LEUCINE ZIPPER MOTIF; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; HUMAN; HUMAN CELL; IRRADIATION; PANCREAS ADENOCARCINOMA; PANCREAS CARCINOMA; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; WESTERN BLOTTING; X RAY; DOUBLE STRANDED DNA BREAK; ENDOSOME; ENZYME ACTIVATION; GENE SILENCING; METABOLISM; PANCREAS TUMOR; PATHOLOGY; PHOSPHORYLATION; RADIATION DOSE; RADIATION RESPONSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL SURVIVAL; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; ENDOSOMES; ENZYME ACTIVATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; PANCREATIC NEOPLASMS; PHOSPHORYLATION; PROTEIN BINDING; RADIATION TOLERANCE; X-RAYS;

EID: 84901045038     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.167     Document Type: Article

References (47)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics. CA Cancer J Clin 2012; 62: 10-29.
2. Hariharan D, Saied A, Kocher HM. Analysis of mortality rates for pancreatic cancer across the world. HPB (Oxford) 2008; 10: 58-62.
3. Penchev VR, Rasheed ZA, Maitra A, Matsui W. Heterogeneity and targeting of pancreatic cancer stem cells. Clin Cancer Res 2012; 18: 4277-4284.
4. Hehlgans S, Eke I, Storch K, Haase M, Baretton GB, Cordes N. Caveolin-1 mediated radioresistance of 3D grown pancreatic cancer cells. Radiother Oncol 2009; 92: 362-370.
5. Eke I, Koch U, Hehlgans S, Sandfort V, Stanchi F, Zips D et al. PINCH1 regulates Akt1 activation and enhances radioresistance by inhibiting PP1alpha. J Clin Invest 2010; 120: 2516-2527.
6. Eke I, Deuse Y, Hehlgans S, Gurtner K, Krause M, Baumann M et al. beta(1)Integrin/FAK/ cortactin signaling is essential for human head and neck cancer resistance to radiotherapy. J Clin Invest 2012; 122: 1529-1540.
7. Morgan MA, Parsels LA, Kollar LE, Normolle DP, Maybaum J, Lawrence TS. The combination of epidermal growth factor receptor inhibitors with gemcitabine and radiation in pancreatic cancer. Clin Cancer Res 2008; 14: 5142-5149.
8. Eke I, Storch K, Krause M, Cordes N. Cetuximab attenuates its cytotoxic and radiosensitizing potential by inducing fibronectin biosynthesis. Cancer Res 2013; 73: 5869-5879.
9. Cordes N, Frick S, Brunner TB, Pilarsky C, Grutzmann R, Sipos B et al. Human pancreatic tumor cells are sensitized to ionizing radiation by knockdown of caveolin-1. Oncogene 2007; 26: 6851-6862.
10. Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B et al. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 2004; 116: 445-456.
11. Hupalowska A, Pyrzynska B, Miaczynska M. APPL1 regulates basal NF-kappaB activity by stabilizing NIK. J Cell Sci 2012; 125: 4090-4102.
12. Schenck A, Goto-Silva L, Collinet C, Rhinn M, Giner A, Habermann B et al. The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 2008; 133: 486-497.
13. Lee JR, Hahn HS, Kim YH, Nguyen HH, Yang JM, Kang JS et al. Adaptor protein containing PH domain, PTB domain and leucine zipper (APPL1) regulates the protein level of EGFR by modulating its trafficking. Biochem Biophys Res Commun 2011; 415: 206-211.
14. Mitsuuchi Y, Johnson SW, Sonoda G, Tanno S, Golemis EA, Testa JR. Identification of a chromosome 3p14.3-21.1 gene, APPL, encoding an adaptor molecule that interacts with the oncoprotein-serine/threonine kinase AKT2. Oncogene 1999; 18: 4891-4898.
15. Deng R, Tang J, Ma JG, Chen SP, Xia LP, Zhou WJ et al. PKB/Akt promotes DSB repair in cancer cells through upregulating Mre11 expression following ionizing radiation. Oncogene 2010; 30: 944-955.
16. Cheng KK, Lam KS, Wu D, Wang Y, Sweeney G, Hoo RL et al. APPL1 potentiates insulin secretion in pancreatic beta cells by enhancing protein kinase Akt-dependent expression of SNARE proteins in mice. Proc Natl Acad Sci USA 2012; 109: 8919-8924.
17. Rashid S, Pilecka I, Torun A, Olchowik M, Bielinska B, Miaczynska M. Endosomal adaptor proteins APPL1 and APPL2 are novel activators of beta-catenin/TCF-mediated transcription. J Biol Chem 2009; 284: 18115-18128.
18. Storch K, Eke I, Borgmann K, Krause M, Richter C, Becker K et al. Three-dimensional cell growth confers radioresistance by chromatin density modification. Cancer Res 2010; 70: 3925-3934.
19. Watson RL, Spalding AC, Zielske SP, Morgan M, Kim AC, Bommer GT et al. GSK3beta and beta-catenin modulate radiation cytotoxicity in pancreatic cancer. Neoplasia 2010; 12: 357-365.
20. Bolden JE, Shi W, Jankowski K, Kan CY, Cluse L, Martin BP et al. HDAC inhibitors induce tumor-cell-selective pro-apoptotic transcriptional responses. Cell Death Dis 2013; 4: e519.
21. Abu-Baker A, Laganiere J, Gaudet R, Rochefort D, Brais B, Neri C et al. Lithium chloride attenuates cell death in oculopharyngeal muscular dystrophy by perturbing Wnt/betacatenin pathway. Cell Death Dis 2013; 4: e821.
22. Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet 2001; 27: 247-254.
23. Noon AT, Goodarzi AA. 53BP1-mediated DNA double strand break repair: insert bad pun here. DNA Repair (Amst) 2011; 10: 1071-1076.
24. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421: 499-506.
25. Chaturvedi P, Eng WK, Zhu Y, Mattern MR, Mishra R, Hurle MR et al. Mammalian Chk2 is a downstream effector of the ATM-dependent DNA damage checkpoint pathway. Oncogene 1999; 18: 4047-4054.
26. Sinha S, Ghildiyal R, Mehta VS, Sen E. ATM-NFkappaB axis-driven TIGAR regulates sensitivity of glioma cells to radiomimetics in the presence of TNFalpha. Cell Death Dis 2013; 4: e615.
27. Williams RS, Williams JS, Tainer JA. Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template. Biochem Cell Biol 2007; 85: 509-520.
28. Watters D, Khanna KK, Beamish H, Birrell G, Spring K, Kedar P et al. Cellular localisation of the ataxia-telangiectasia (ATM) gene product and discrimination between mutated and normal forms. Oncogene 1997; 14: 1911-1921.
29. Lim DS, Kirsch DG, Canman CE, Ahn JH, Ziv Y, Newman LS et al. ATM binds to beta-adaptin in cytoplasmic vesicles. Proc Natl Acad Sci USA 1998; 95: 10146-10151.
30. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 2001; 276: 42462-42467.
31. Pyrzynska B, Banach-Orlowska M, Teperek-Tkacz M, Miekus K, Drabik G, Majka M et al. Multifunctional protein APPL2 contributes to survival of human glioma cells. Mol Oncol 2013; 7: 67-84.
32. Meyer C, Liu Y, Kaul A, Peipe I, Dooley S. Caveolin-1 abrogates TGF-beta mediated hepatocyte apoptosis. Cell Death Dis 2013; 4: e466.
33. Zhang Y, Yu S, Zhuang L, Zheng Z, Chao T, Fu Q. Caveolin-1 is involved in radiationinduced ERBB2 nuclear transport in breast cancer cells. J Huazhong Univ Sci Technolog Med Sci 2012; 32: 888-892.
34. Dittmann K, Mayer C, Kehlbach R, Rodemann HP. Radiation-induced caveolin-1 associated EGFR internalization is linked with nuclear EGFR transport and activation of DNA-PK. Mol Cancer 2008; 7: 69.
35. Pilch DR, Sedelnikova OA, Redon C, Celeste A, Nussenzweig A, Bonner WM. Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem Cell Biol 2003; 81: 123-129.
36. Matsuoka S, Ballif BA, Smogorzewska A, McDonald 3rd ER, Hurov KE, Luo J et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007; 316: 1160-1166.
37. Jeggo PA, Lobrich M. DNA double-strand breaks: their cellular and clinical impact? Oncogene 2007; 26: 7717-7719.
38. Berrozpe G, Schaeffer J, Peinado MA, Real FX, Perucho M. Comparative analysis of mutations in the p53 and K-ras genes in pancreatic cancer. Int J Cancer 1994; 58: 185-191.
39. Song H, Hollstein M, Xu Y. p53 gain-of-function cancer mutants induce genetic instability by inactivating ATM. Nat Cell Biol 2007; 9: 573-580.
40. Mavrou A, Tsangaris GT, Roma E, Kolialexi A. The ATM gene and ataxia telangiectasia. Anticancer Res 2008; 28: 401-405.
41. Ziv Y, Bar-Shira A, Pecker I, Russell P, Jorgensen TJ, Tsarfati I et al. Recombinant ATM protein complements the cellular A-T phenotype. Oncogene 1997; 15: 159-167.
42. Lundholm L, Haag P, Zong D, Juntti T, Mork B, Lewensohn R et al. Resistance to DNAdamaging treatment in non-small cell lung cancer tumor-initiating cells involves reduced DNA-PK/ATM activation and diminished cell cycle arrest. Cell Death Dis 2013; 4: e478.
43. Eke I, Schneider L, Forster C, Zips D, Kunz-Schughart LA, Cordes N. EGFR/JIP-4/JNK2 Signaling Attenuates Cetuximab-Mediated Radiosensitization of Squamous Cell Carcinoma Cells. Cancer Res 2013; 73: 297-306.
44. Eke I, Leonhardt F, Storch K, Hehlgans S, Cordes N. The small molecule inhibitor QLT0267 Radiosensitizes squamous cell carcinoma cells of the head and neck. PLoS One 2009; 4: e6434.
45. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005; 122: 735-749.
46. Collinet C, Stoter M, Bradshaw CR, Samusik N, Rink JC, Kenski D et al. Systems survey of endocytosis by multiparametric image analysis. Nature 2010; 464: 243-249.
47. Bolte S, Cordelières FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 2006; 224: 213-232.