Mitochondrial p53 phosphorylation induces Bak-mediated and caspase-independent cell death

Oncotarget

Volumn 6, Issue 19, 2015, Pages 17192-17205

  Wang, Jinjing ^a   Guo, Wenhao ^a   Zhou, Hang ^b   Luo, Na ^c   Nie, Chunlai ^a   Zhao, Xinyu ^a   Yuan, Zhu ^a   Liu, Xinyu ^a   Wei, Yuquan ^a  

^a SICHUAN UNIVERSITY   (China)

^b SICHUAN CANCER HOSPITAL   (China)

^c NANKAI UNIVERSITY   (China)

Author keywords

Akt; Bak; Caspase independent; p53

Indexed keywords

CASPASE; PLUMBAGIN; PROTEIN BAK; PROTEIN KINASE B; PROTEIN P53; SHORT HAIRPIN RNA; ANTINEOPLASTIC AGENT; BAK1 PROTEIN, HUMAN; NAPHTHOQUINONE; PROTEIN BAX; SMALL INTERFERING RNA; TP53 PROTEIN, HUMAN;

ARTICLE; ATTENUATION; CANCER RESISTANCE; CELL DEATH; CELL TRANSFER; DRUG EFFICACY; HCT116 CELL LINE; MCF 7 CELL LINE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; WILD TYPE; APOPTOSIS; DRUG EFFECTS; DRUG RESISTANCE; FLUORESCENT ANTIBODY TECHNIQUE; GENE INACTIVATION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; METABOLISM; MITOCHONDRION; PHOSPHORYLATION; PHYSIOLOGY; TUMOR CELL LINE; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CASPASES; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCKDOWN TECHNIQUES; GENE KNOCKOUT TECHNIQUES; HUMANS; MITOCHONDRIA; NAPHTHOQUINONES; PHOSPHORYLATION; RNA, SMALL INTERFERING; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84938222624     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3780     Document Type: Article

References (47)

1. Vardiman JW, Thiele J, Arber DA, Brunning RD, Borowitz MJ, Porwit A, Harris NL, Le Beau MM, Hellstrom-Lindberg E, Tefferi A, Bloomfield CD. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood. 2009; 114:937-951.
2. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61:69-90.
3. Yang X, Fraser M, Moll UM, Basak A, Tsang BK. Akt-mediated cisplatin resistance in ovarian cancer: modulation of p53 action on caspase-dependent mitochondrial death pathway. Cancer Res. 2006; 66:3126-3136.
4. Fraser M, Leung BM, Yan X, Dan HC, Cheng JQ, Tsang BK. p53 is a determinant of X-linked inhibitor of apoptosis protein/Akt-mediated chemoresistance in human ovarian cancer cells. Cancer Res. 2003; 63:7081-7088.
5. Liu J, Uematsu H, Tsuchida N, Ikeda MA. Essential role of caspase-8 in p53/p73-dependent apoptosis induced by etoposide in head and neck carcinoma cells. Mol Cancer. 2011; 10:95.
6. Devarajan E, Sahin AA, Chen JS, Krishnamurthy RR, Aggarwal N, Brun AM, Sapino A, Zhang F, Sharma D, Yang XH, Tora AD, Mehta K. Down-regulation of caspase 3 in breast cancer: a possible mechanism for chemoresistance. Oncogene. 2002; 21:8843-8851.
7. Tsujimoto Y. Cell death regulation by the Bcl-2 protein family in the mitochondria. J Cell Physiol. 2003; 195:158-167.
8. Yuan Z, Wang F, Zhao Z, Zhao X, Qiu J, Nie C, Wei Y. BIM-Mediated AKT Phosphorylation Is a Key Modulator of Arsenic Trioxide-Induced Apoptosis in Cisplatin-Sensitive and -Resistant Ovarian Cancer Cells. PLoS One. 2011; 6:e20586.
9. Hu W, Wang F, Tang J, Liu X, Yuan Z, Nie C, Wei Y. Proapoptotic protein Smac mediates apoptosis in cisplatin-resistant ovarian cancer cells when treated with the anti-tumor agent AT101. J Biol Chem. 2012; 287:68-80.
10. Arnoult D, Gaume B, Karbowski M, Sharpe JC, Cecconi F, Youle RJ. Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. EMBO J. 2003; 22:4385-4399.
11. Zhao Z, Wang J, Tang J, Liu X, Zhong Q, Wang F, Hu W, Yuan Z, Nie C, Wei Y. JNK- and Akt-mediated Puma expression in the apoptosis of cisplatin-resistant ovarian cancer cells. Biochem J. 2012; 444:291-301.
12. Cregan SP, Dawson VL, Slack RS. Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene. 2004; 23:2785-2796.
13. Cregan SP, Fortin A, MacLaurin JG, Callaghan SM, Cecconi F, Yu SW, Dawson TM, Dawson VL, Park DS, Kroemer G, Slack RS. Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J Cell Biol. 2002; 158:507-517.
14. Hemmati PG, Guner D, Gillissen B, Wendt J, von Haefen C, Chinnadurai G, Dorken B, Daniel PT. Bak functionally complements for loss of Bax during p14ARF-induced mitochondrial apoptosis in human cancer cells. Oncogene. 2006; 25:6582-6594.
15. Li LY, Luo X, Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature. 2001; 412:95-99.
16. Chandra D, Choy G, Daniel PT, Tang DG. Bax-dependent regulation of Bak by voltage-dependent anion channel 2.J Biol Chem. 2005; 280:19051-19061.
17. Leu JI, Dumont P, Hafey M, Murphy ME, George DL. Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat Cell Biol. 2004; 6:443-450.
18. Saleem A, Hood DA. Acute exercise induces tumour suppressor protein p53 translocation to the mitochondria and promotes a p53-Tfam-mitochondrial DNA complex in skeletal muscle. J Physiol. 2013; 591:3625-3636.
19. Nieminen AI, Eskelinen VM, Haikala HM, Tervonen TA, Yan Y, Partanen JI, Klefstrom J. Myc-induced AMPK-phospho p53 pathway activates Bak to sensitize mitochondrial apoptosis. Proc Natl Acad Sci U S A. 2013; 110:E1839-1848.
20. Barlev NA, Liu L, Chehab NH, Mansfield K, Harris KG, Halazonetis TD, Berger SL. Acetylation of p53 activates transcription through recruitment of coactivators/histone acetyltransferases. Mol Cell. 2001; 8:1243-1254.
21. Fraser M, Bai T, Tsang BK. Akt promotes cisplatin resistance in human ovarian cancer cells through inhibition of p53 phosphorylation and nuclear function. Int J Cancer. 2008; 122:534-546.
22. Vivanco I, Sawyers CL. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer. 2002; 2:489-501.
23. Ahmad A, Banerjee S, Wang Z, Kong D, Sarkar FH. Plumbagin-induced apoptosis of human breast cancer cells is mediated by inactivation of NF-kappaB and Bcl-2. J Cell Biochem. 2008; 105:1461-1471.
24. Aziz MH, Dreckschmidt NE, Verma AK. Plumbagin, a medicinal plant-derived naphthoquinone, is a novel inhibitor of the growth and invasion of hormone-refractory prostate cancer. Cancer Res. 2008; 68:9024-9032.
25. Sandur SK, Ichikawa H, Sethi G, Ahn KS, Aggarwal BB. Plumbagin (5-hydroxy-2-methyl-1,4-naphthoquinone) suppresses NF-kappaB activation and NF-kappaB-regulated gene products through modulation of p65 and IkappaBalpha kinase activation, leading to potentiation of apoptosis induced by cytokine and chemotherapeutic agents. J Biol Chem. 2006; 281:17023-17033.
26. Kuo PL, Hsu YL, Cho CY. Plumbagin induces G2-M arrest and autophagy by inhibiting the AKT/mammalian target of rapamycin pathway in breast cancer cells. Mol Cancer Ther. 2006; 5:3209-3221.
27. Asselin E, Mills GB, Tsang BK. XIAP regulates Akt activity and caspase-3-dependent cleavage during cisplatin-induced apoptosis in human ovarian epithelial cancer cells. Cancer Res. 2001; 61:1862-1868.
28. Blanc C, Deveraux QL, Krajewski S, Janicke RU, Porter AG, Reed JC, Jaggi R, Marti A. Caspase-3 is essential for procaspase-9 processing and cisplatin-induced apoptosis of MCF-7 breast cancer cells. Cancer Res. 2000; 60:4386-4390.
29. Kim HS, Lee JW, Soung YH, Park WS, Kim SY, Lee JH, Park JY, Cho YG, Kim CJ, Jeong SW, Nam SW, Kim SH, Lee JY, Yoo NJ, Lee SH. Inactivating mutations of caspase-8 gene in colorectal carcinomas. Gastroenterology. 2003; 125:708-715.
30. Catchpoole DR, Lock RB. The potential tumour suppressor role for caspase-9 (CASP9) in the childhood malignancy, neuroblastoma. Eur J Cancer. 2001; 37:2217-2221.
31. Terry MR, Arya R, Mukhopadhyay A, Berrett KC, Clair PM, Witt B, Salama ME, Bhutkar A, Oliver TG. Caspase-2 impacts lung tumorigenesis and chemotherapy response in vivo. Cell Death Differ. 2014.
32. Nie C, Tian C, Zhao L, Petit PX, Mehrpour M, Chen Q. Cysteine 62 of Bax is critical for its conformational activation and its proapoptotic activity in response to H2O2-induced apoptosis. J Biol Chem. 2008; 283:15359-15369.
33. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M, Thompson CB, Korsmeyer SJ. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 2000; 14:2060-2071.
34. Kandasamy K, Srinivasula SM, Alnemri ES, Thompson CB, Korsmeyer SJ, Bryant JL, Srivastava RK. Involvement of proapoptotic molecules Bax and Bak in tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced mitochondrial disruption and apoptosis: differential regulation of cytochrome c and Smac/DIABLO release. Cancer Res. 2003; 63:1712-1721.
35. Vaseva AV, Moll UM. The mitochondrial p53 pathway. Biochim Biophys Acta. 2009; 5:414-420.
36. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science. 2004; 303:1010-1014.
37. Wang F, Liu J, Robbins D, Morris K, Sit A, Liu YY, Zhao Y. Mutant p53 exhibits trivial effects on mitochondrial functions which can be reactivated by ellipticine in lymphoma cells. Apoptosis. 2011; 16:301-310.
38. Ravichandran LV, Chen H, Li Y, Quon MJ. Phosphorylation of PTP1B at Ser(50) by Akt impairs its ability to dephosphorylate the insulin receptor. Mol Endocrinol. 2001; 15:1768-1780.
39. Ahmad F, Cong LN, Stenson Holst L, Wang LM, Rahn Landstrom T, Pierce JH, Quon MJ, Degerman E, Manganiello VC. Cyclic nucleotide phosphodiesterase 3B is a downstream target of protein kinase B and may be involved in regulation of effects of protein kinase B on thymidine incorporation in FDCP2 cells. J Immunol. 2000; 164:4678-4688.
40. Tai YT, Podar K, Mitsiades N, Lin B, Mitsiades C, Gupta D, Akiyama M, Catley L, Hideshima T, Munshi NC, Treon SP, Anderson KC. CD40 induces human multiple myeloma cell migration via phosphatidylinositol 3-kinase/AKT/NF-kappa B signaling. Blood. 2003; 101:2762-2769.
41. Chen KF, Yeh PY, Yeh KH, Lu YS, Huang SY, Cheng AL. Down-regulation of phospho-Akt is a major molecular determinant of bortezomib-induced apoptosis in hepatocellular carcinoma cells. Cancer Res. 2008; 68:6698-6707.
42. Nie C, Luo Y, Zhao X, Luo N, Tong A, Liu X, Yuan Z, Wang C, Wei Y. Caspase-9 mediates Puma activation in UCN-01-induced apoptosis. Cell Death Dis. 2014; 5:e1495.
43. Vaseva AV, Marchenko ND, Ji K, Tsirka SE, Holzmann S, Moll UM. p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell. 2012; 149:1536-1548.
44. Ming L, Wang P, Bank A, Yu J, Zhang L. PUMA Dissociates Bax and Bcl-X(L) to induce apoptosis in colon cancer cells. J Biol Chem. 2006; 281:16034-16042.
45. Dittmann K, Mayer C, Fehrenbacher B, Schaller M, Raju U, Milas L, Chen DJ, Kehlbach R, Rodemann HP. Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase. J Biol Chem. 2005; 280:31182-31189.
46. Chen S, Dai Y, Pei XY, Grant S. Bim upregulation by histone deacetylase inhibitors mediates interactions with the Bcl-2 antagonist ABT-737: evidence for distinct roles for Bcl-2, Bcl-xL, and Mcl-1. Mol Cell Biol. 2009; 29:6149-6169.
47. Stros M, Ozaki T, Bacikova A, Kageyama H, Nakagawara A. HMGB1 and HMGB2 cell-specifically down-regulate the p53- and p73-dependent sequence-specific transactivation from the human Bax gene promoter. J Biol Chem. 2002; 277:7157-7164.