P38MAPK is a major determinant of the balance between apoptosis and autophagy triggered by 5-fluorouracil: Implication in resistance

Oncogene

Volumn 31, Issue 9, 2012, Pages 1073-1085

  De La Cruz Morcillo, M A ^a   Valero, M L L ^a   Callejas Valera, J L ^a   Arias Gonzalez L ^a   Melgar Rojas, P ^a   Galan Moya E M ^a   Garcia Gil E ^a   Garcia Cano J ^a   Sanchez Prieto R ^a  

^a University of Castilla La Mancha   (Spain)

Author keywords

5 fluorouracil; apoptosis; autophagy; p38MAPK; p53; resistance

Indexed keywords

FLUOROURACIL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 6; MITOGEN ACTIVATED PROTEIN KINASE P38;

APOPTOSIS; ARTICLE; AUTOPHAGY; DRUG EFFECT; DRUG MECHANISM; DRUG RESPONSE; ENZYME ACTIVATION; ENZYME ACTIVITY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; AUTOPHAGY; CELL CYCLE PROTEINS; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DNA-BINDING PROTEINS; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; FLUOROURACIL; HCT116 CELLS; HT29 CELLS; HUMANS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA;

EID: 84857782869     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.321     Document Type: Article

References (74)

1. Ariumi Y, Turelli P, Masutani M, Trono D. (2005). DNA damage sensors ATM, ATR, DNA-PKcs, and PARP-1 are dispensable for human immunodeficiency virus type 1 integration. J Virol 79: 2973-2978.
2. Bensaad K, Cheung EC, Vousden KH. (2009). Modulation of intracellular ROS levels by TIGAR controls autophagy. EMBO J 28: 3015-3026.
3. Brancho D, Tanaka N, Jaeschke A, Ventura JJ, Kelkar N, Tanaka Y et al. (2003). Mechanism of p38 MAP kinase activation in vivo. Genes Dev 17: 1969-1978.
4. Bulavin DV, Saito S, Hollander MC, Sakaguchi K, Anderson CW, Appella E et al. (1999). Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J 18: 6845-6854.
5. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP et al. (1998). Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282: 1497-1501.
6. Bunz F, Hwang PM, Torrance C, Waldman T, Zhang Y, Dillehay L et al. (1999). Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J Clin Invest 104: 263-269.
7. Callejas-Valera JL, Guinea-Viniegra J, Ramirez-Castillejo C, Recio JA, Galan-Moya E, Martinez N et al. (2008). E1a gene expression blocks the ERK1/2 signaling pathway by promoting nuclear localization and MKP up-regulation: implication in v-H-Rasinduced senescence. J Biol Chem 283: 13450-13458.
8. Chan A, Verrill M. (2009). Capecitabine and vinorelbine in metastatic breast cancer. Eur J Cancer 45: 2253-2265.
9. Chen S, Rehman SK, Zhang W, Wen A, Yao L, Zhang J. (2010). Autophagy is a therapeutic target in anticancer drug resistance. Biochim Biophys Acta 1806: 220-229.
10. Comes F, Matrone A, Lastella P, Nico B, Susca FC, Bagnulo R et al. (2007). A novel cell type-specific role of p38alpha in the control of autophagy and cell death in colorectal cancer cells. Cell Death Differ 14: 693-702.
11. Cortez D, Guntuku S, Qin J, Elledge SJ. (2001). ATR and ATRIP: partners in checkpoint signaling. Science 294: 1713-1716.
12. Crighton D, O'Prey J, Bell HS, Ryan KM. (2007). p73 regulates DRAM-independent autophagy that does not contribute to programmed cell death. Cell Death Differ 14: 1071-1079.
13. Crighton D, Wilkinson S, O'Prey J, Syed N, Smith P, Harrison PR et al. (2006). DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126: 121-134.
14. Cuadrado A, Lafarga V, Cheung PC, Dolado I, Llanos S, Cohen P et al. (2007). A new p38 MAP kinase-regulated transcriptionalcoactivator that stimulates p53-dependent apoptosis. EMBO J 26: 2115-2126.
15. Cuadrado A, Nebreda AR. (2010). Mechanisms and functions of p38 MAPK signalling. Biochem J 429: 403-417.
16. Dai C, Gu W. (2010). p53 post-translational modification: deregulated in tumorigenesis. Trends Mol Med 16: 528-536.
17. Elsea CR, Roberts DA, Druker BJ, Wood LJ. (2008). Inhibition of p38 MAPK suppresses inflammatory cytokine induction by etoposide, 5-fluorouracil, and doxorubicin without affecting tumoricidal activity. PLoS One 3: e2355.
18. Ewald B, Sampath D, Plunkett W. (2008a). ATM and the Mre11-Rad50-Nbs1 complex respond to nucleoside analogue-induced stalled replication forks and contribute to drug resistance. Cancer Res 68: 7947-7955.
19. Ewald B, Sampath D, Plunkett W. (2008b). Nucleoside analogs: molecular mechanisms signaling cell death. Oncogene 27: 6522-6537.
20. Fedier A, Schlamminger M, Schwarz VA, Haller U, Howell SB, Fink D. (2003). Loss of atm sensitises p53-deficient cells to topoisomerase poisons and antimetabolites. Ann Oncol 14: 938-945.
21. Galan-Moya EM, Hernandez-Losa J, Ceves Luquero CI, de la Cruz-Morcillo MA, Ramirez-Castillejo C, Callejas-Valera JL et al. (2008). c-Abl activates p38MAPK independently of its tyrosine kinase activity: implications in cisplatin-based therapy. Int J Cancer 122: 289-297.
22. Goedert M, Cuenda A, Craxton M, Jakes R, Cohen P. (1997). Activation of the novel stress-activated protein kinase SAPK4 by cytokines and cellular stresses is mediated by SKK3 (MKK6); comparison of its substrate specificity with that of other SAP kinases. EMBO J 16: 3563-3571.
23. Green DR, Kroemer G. (2009). Cytoplasmic functions of the tumour suppressor p53. Nature 458: 1127-1130.
24. Habiro A, Tanno S, Koizumi K, Izawa T, Nakano Y, Osanai M et al. (2004). Involvement of p38 mitogen-activated protein kinase in gemcitabine-induced apoptosis in human pancreatic cancer cells. Biochem Biophys Res Commun 316: 71-77.
25. Hector S, Prehn JH. (2009). Apoptosis signaling proteins as prognostic biomarkers in colorectal cancer: a review. Biochim Biophys Acta 1795: 117-129.
26. Im JS, Lee JK. (2008). ATR-dependent activation of p38 MAP kinase is responsible for apoptotic cell death in cells depleted of Cdc7. J Biol Chem 283: 25171-25177.
27. Jardim MJ, Wang Q, Furumai R, Wakeman T, Goodman BK, Wang XF. (2009). Reduced ATR or Chk1 expression leads to chromosome instability and chemosensitization of mismatch repair-deficient colorectal cancer cells. Mol Biol Cell 20: 3801-3809.
28. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T et al. (2000). LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728.
29. Kaeser MD, Pebernard S, Iggo RD. (2004). Regulation of p53 stability and function in HCT116 colon cancer cells. J Biol Chem 279: 7598-7605.
30. Kennedy AS, Harrison GH, Mansfield CM, Zhou XJ, Xu JF, Balcer-Kubiczek EK. (2000). Survival of colorectal cancer cell lines treated with paclitaxel, radiation, and 5-FU: effect of TP53 or hMLH1 deficiency. Int J Cancer 90: 175-185.
31. Koizumi K, Tanno S, Nakano Y, Habiro A, Izawa T, Mizukami Y et al. (2005). Activation of p38 mitogen-activated protein kinase is necessary for gemcitabine-induced cytotoxicity in human pancreatic cancer cells. Anticancer Res 25: 3347-3353.
32. Kroemer G, Marino G, Levine B. (2010). Autophagy and the integrated stress response. Mol Cell 40: 280-293.
33. Lafarga V, Cuadrado A, Lopez dS I, Bengoechea R, Fernandez-Capetillo O, Nebreda AR. (2009). p38 Mitogen-activated protein kinase-and HuR-dependent stabilization of p21(Cip1) mRNA mediates the G(1)/S checkpoint. Mol Cell Biol 29: 4341-4351.
34. Lau A, Swinbank KM, Ahmed PS, Taylor DL, Jackson SP, Smith GC et al. (2005). Suppression of HIV-1 infection by a small molecule inhibitor of the ATM kinase. Nat Cell Biol 7: 493-500.
35. Li J, Hou N, Faried A, Tsutsumi S, Kuwano H. (2010). Inhibition of autophagy augments 5-fluorouracil chemotherapy in human colon cancer in vitro and in vivo model. Eur J Cancer 46: 1900-1909.
36. Li J, Hou N, Faried A, Tsutsumi S, Takeuchi T, Kuwano H. (2009). Inhibition of autophagy by 3-MA enhances the effect of 5-FUinduced apoptosis in colon cancer cells. Ann Surg Oncol 16: 761-771.
37. Li Y, Yang DQ. (2010). The ATM inhibitor KU-55933 suppresses cell proliferation and induces apoptosis by blocking Akt in cancer cells with overactivated Akt. Mol Cancer Ther 9: 113-125.
38. Liu A, Yoshioka K, Salerno V, Hsieh P. (2008). The mismatch repairmediated cell cycle checkpoint response to fluorodeoxyuridine. J Cell Biochem 105: 245-254.
39. Longley DB, Boyer J, Allen WL, Latif T, Ferguson PR, Maxwell PJ et al. (2002). The role of thymidylate synthase induction in modulating p53-regulated gene expression in response to 5-fluorouracil and antifolates. Cancer Res 62: 2644-2649.
40. Longley DB, Harkin DP, Johnston PG. (2003). 5-fluorouracil: mechanisms of action and clinical strategies. Nat Rev Cancer 3: 330-338.
41. Losa JH, Parada CC, Viniegra JG, Sanchez-Arevalo LV, Cajal S, Sanchez-Prieto R. (2003). Role of the p38 MAPK pathway in cisplatin-based therapy. Oncogene 22: 3998-4006.
42. Lowe SW, Ruley HE, Jacks T, Housman DE. (1993). p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74: 957-967.
43. Maiuri MC, Galluzzi L, Morselli E, Kepp O, Malik SA, Kroemer G. (2010). Autophagy regulation by p53. Curr Opin Cell Biol 22: 181-185.
44. Maiuri MC, Malik SA, Morselli E, Kepp O, Criollo A, Mouchel PL et al. (2009). Stimulation of autophagy by the p53 target gene Sestrin2. Cell Cycle 8: 1571-1576.
45. Mariadason JM, Arango D, Shi Q, Wilson AJ, Corner GA, Nicholas C et al. (2003). Gene expression profiling-based prediction of response of colon carcinoma cells to 5-fluorouracil and camptothecin. Cancer Res 63: 8791-8812.
46. McClung JM, Judge AR, Powers SK, Yan Z. (2010). p38 MAPK links oxidative stress to autophagy-related gene expression in cachectic muscle wasting. Am J Physiol Cell Physiol 298: C542-C549.
47. McDonald GT, Sullivan R, Pare GC, Graham CH. (2010). Inhibition of phosphatidylinositol 3-kinase promotes tumor cell resistance to chemotherapeutic agents via a mechanism involving delay in cell cycle progression. Exp Cell Res 316: 3197-3206.
48. Mizushima N, Levine B. (2010). Autophagy in mammalian development and differentiation. Nat Cell Biol 12: 823-830.
49. Nabeya Y, Loganzo Jr| F, Maslak P, Lai L, de Oliveira AR, Schwartz GK et al. (1995). The mutational status of p53 protein in gastric and esophageal adenocarcinoma cell lines predicts sensitivity to chemotherapeutic agents. Int J Cancer 64: 37-46.
50. O'Connor PM, Jackman J, Bae I, Myers TG, Fan S, Mutoh M et al, 1997, Characterization of the p53 tumor suppressor pathway in cell lines of the National Cancer Institute anticancer drug screen and correlations with the growth-inhibitory potency of 123 anticancer agents. Cancer Res, 57, 4285-4300.
51. O'Donovan TR, O'Sullivan GC, McKenna S. (2011). Induction of autophagy by drug-resistant esophageal cancer cells promotes their survival and recovery following treatment with chemotherapeutics. Autophagy 7: 509-524.
52. Olson JM, Hallahan AR. (2004). p38 MAP kinase: a convergence point in cancer therapy. Trends Mol Med 10: 125-129.
53. Perfettini JL, Nardacci R, Bourouba M, Subra F, Gros L, Seror C et al. (2008). Critical involvement of the ATM-dependent DNA damage response in the apoptotic demise of HIV-1-elicited syncytia. PLoS One 3: e2458.
54. Peters GJ, Backus HH, Freemantle S, van TB, Codacci-Pisanelli G, van der Wilt CL et al. (2002). Induction of thymidylate synthase as a 5-fluorouracil resistance mechanism. Biochim Biophys Acta 1587: 194-205.
55. Raftery L, Sanoff HK, Goldberg R. (2008). Colon cancer in older adults. Semin Oncol 35: 561-568.
56. Reinhardt HC, Aslanian AS, Lees JA, Yaffe MB. (2007). p53-deficient cells rely on ATM-and ATR-mediated checkpoint signalingthrough the p38MAPK/MK2 pathway for survival after DNA damage. Cancer Cell 11: 175-189.
57. Reinhardt HC, Hasskamp P, Schmedding I, Morandell S, van Vugt MA, Wang X et al. (2010). DNA damage activates a spatially distinct late cytoplasmic cell-cycle checkpoint network controlled by MK2-mediated RNA stabilization. Mol Cell 40: 34-49.
58. Sanchez-Arevalo LV, Ceves Luquero CI, Varez-Vallina L, Tipping AJ, Viniegra JG, Hernandez LJ et al. (2005). Modulation of the p38 MAPK (mitogen-activated protein kinase) pathway through Bcr/Abl: implications in the cellular response to Ara-C. Biochem J 387: 231-238.
59. Sanchez-Prieto R, Rojas JM, Taya Y, Gutkind JS. (2000). A role for the p38 mitogen-acitvated protein kinase pathway in the transcriptional activation of p53 on genotoxic stress by chemotherapeutic agents. Cancer Res 60: 2464-2472.
60. Sanchez-Prieto R, Sanchez-Arevalo VJ, Servitja JM, Gutkind JS. (2002). Regulation of p73 by c-Abl through the p38 MAP kinase pathway. Oncogene 21: 974-979.
61. Specenier P, Vermorken JB. (2010). Advances in the systemic treatment of head and neck cancers. Curr Opin Oncol 22: 200-205.
62. Tanida I, Yamaji T, Ueno T, Ishiura S, Kominami E, Hanada K. (2008). Consideration about negative controls for LC3 and expression vectors for four colored fluorescent protein-LC3 negative controls. Autophagy 4: 131-134.
63. Tasdemir E, Chiara MM, Morselli E, Criollo A, D'Amelio M, Djavaheri-MergnyMet al. (2008a). A dual role of p53 in the control of autophagy. Autophagy 4: 810-814.
64. Tasdemir E, Maiuri MC, Galluzzi L, Vitale I, Djavaheri-Mergny M, D0AmelioMet al. (2008b). Regulation of autophagy by cytoplasmic p53. Nat Cell Biol 10: 676-687.
65. Tominaga T, Iwahashi M, Takifuji K, Hotta T, Yokoyama S, Matsuda K et al. (2010). Combination of p53 codon 72 polymorphism and inactive p53 mutation predicts chemosensitivity to 5-fluorouracil in colorectal cancer. Int J Cancer 126: 1691-1701.
66. Viniegra JG, Martinez N, Modirassari P, Losa JH, Parada CC, Lobo VJ et al. (2005). Full activation of PKB/Akt in response to insulin or ionizing radiation is mediated through ATM. J Biol Chem 280: 4029-4036.
67. Wagner EF, Nebreda AR. (2009). Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 9: 537-549.
68. Webber JL, Tooze SA. (2010). Coordinated regulation of autophagy by p38alpha MAPK through mAtg9 and p38IP. EMBO J 29: 27-40.
69. Wilsker D, Bunz F. (2007). Loss of ataxia telangiectasia mutated-and Rad3-related function potentiates the effects of chemotherapeutic drugs on cancer cell survival. Mol Cancer Ther 6: 1406-1413.
70. Wyatt MD, Wilson III DM. (2009). Participation of DNA repair in the response to 5-fluorouracil. Cell Mol Life Sci 66: 788-799.
71. Xiong HY, Guo XL, Bu XX, Zhang SS, Ma NN, Song JR et al. (2010). Autophagic cell death induced by 5-FU in Bax or PUMA deficient human colon cancer cell. Cancer Lett 288: 68-74.
72. Zeng X, Kinsella TJ. (2010). BNIP3 is essential for mediating 6-thioguanine-and 5-fluorouracil-induced autophagy following DNA mismatch repair processing. Cell Res 20: 665-675.
73. Zhao HY, Ooyama A, Yamamoto M, Ikeda R, Haraguchi M, Tabata S et al. (2008). Molecular basis for the induction of an angiogenesis inhibitor, thrombospondin-1, by 5-fluorouracil. Cancer Res 68: 7035-7041.
74. Zheng M, Wang H, Zhang H, Ou Q, Shen B, Li N et al. (1999). The influence of the p53 gene on the in vitro chemosensitivity of colorectal cancer cells. J Cancer Res Clin Oncol 125: 357-360.