Mitochondrial dysfunction-mediated apoptosis resistance associates with defective heat shock protein response in African-American men with prostate cancer

British Journal of Cancer

Volumn 114, Issue 10, 2016, Pages 1090-1100

  Chaudhary, Ajay K ^a   Bhat, Tariq A ^a   Kumar, Sandeep ^a   Kumar, Anil ^b   Kumar, Rahul ^a   Underwood, Willie ^a   Koochekpour, Shahriar ^a   Shourideh, Mojgan ^a   Yadav, Neelu ^a   Dhar, Shanta ^b   Chandra, Dhyan ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

apoptosis; dichloroacetate; mitochondrial dysfunction; oxidative phosphorylation; reactive oxygen species

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; CHAPERONIN 60; DICHLOROACETIC ACID; DOXORUBICIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 90; PACLITAXEL; REACTIVE OXYGEN METABOLITE;

AFRICAN AMERICAN; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER PATIENT; CANCER RESISTANCE; CELL CYCLE; CELL INVASION; CELL MIGRATION ASSAY; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; CLONOGENIC ASSAY; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MALE; METASTASIS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; ZYMOGRAPHY; CELL MOTION; DRUG EFFECTS; ETHNOLOGY; GENE EXPRESSION REGULATION; METABOLISM; PROSTATE TUMOR; TUMOR CELL LINE; UNITED STATES;

AFRICAN AMERICANS; APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; DICHLOROACETIC ACID; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAT-SHOCK PROTEINS; HUMANS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PROSTATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; UNITED STATES;

EID: 84967261775     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2016.88     Document Type: Article

References (54)

1. Aldridge JE, Horibe T, Hoogenraad NJ. (2007). Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR), and cognate promoter elements. PloS One. 2(9): e874.
2. Alirol E, Martinou JC. (2006). Mitochondria, and cancer: is there a morphological connection?. Oncogene. 25(34): 4706-4716.
3. Altieri DC. (2011). Mitochondrial compartmentalized protein folding, and tumor cell survival. Oncotarget. 2(4): 347-351.
4. Altieri DC. (2013). Hsp90 regulation of mitochondrial protein folding: from organelle integrity to cellular homeostasis. Cell Mol Life Sci. 70(14): 2463-2472.
5. Bonnet S, Archer SL, Allalunis-Turner J, Haromy A, Beaulieu C, Thompson R, Lee CT, Lopaschuk GD, Puttagunta L, Bonnet S, Harry G, Hashimoto K, Porter CJ, Andrade MA, Thebaud B, Michelakis ED. (2007) A mitochondria-K+ channel axis is suppressed in cancer, and its normalization promotes apoptosis, and inhibits cancer growth. Cancer Cell. 111: 37-51.
6. Cao W, Yacoub S, Shiverick KT, Namiki K, Sakai Y, Porvasnik S, Urbanek C, Rosser CJ. (2008). Dichloroacetate (DCA) sensitizes both wild-Type, and over expressing Bcl-2 prostate cancer cells in vitro to radiation. Prostate. 68(11): 1223-1231.
7. Chatterjee A, Mambo E, Sidransky D. (2006). Mitochondrial DNA mutations in human cancer. Oncogene. 25(34): 4663-4674.
8. Chen G, Wang F, Trachootham D, Huang P. (2010). Preferential killing of cancer cells with mitochondrial dysfunction by natural compounds. Mitochondrion. 10(6): 614-625.
9. Chornokur G, Dalton K, Borysova ME, Kumar NB. (2011). Disparities at presentation, diagnosis, treatment, and survival in African American men, affected by prostate cancer. Prostate. 71(9): 985-997.
10. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. (2005). Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 65(23): 10946-10951.
11. Coulonval K, Bockstaele L, Paternot S, Roger PP. (2003). Phosphorylations of cyclin-dependent kinase 2 revisited using two-dimensional gel electrophoresis. J Biol Chem. 278(52): 52052-52060.
12. Dey R, Moraes CT. (2000). Lack of oxidative phosphorylation, and low mitochondrial membrane potential decrease susceptibility to apoptosis, and do not modulate the protective effect of Bcl-x(L) in osteosarcoma cells. J Biol Chem. 275(10): 7087-7094.
13. Evan GI, Brown L, Whyte M, Harrington E. (1995). Apoptosis, and the cell cycle. Curr Opin Cell Biol. 76: 825-834.
14. Fantin VR, St-Pierre J, Leder P. (2006). Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell. 96: 425-434.
15. Fischer U, Schulze-Osthoff K. (2005). New approaches, and therapeutics targeting apoptosis in disease. Pharmacol Rev. 57(2): 187-215.
16. Godley PA, Schenck AP, Amamoo MA, Schoenbach VJ, Peacock S, Manning M, Symons M, Talcott JA. (2003). Racial differences in mortality among Medicare recipients after treatment for localized prostate cancer. J Natl Cancer Inst. 95(22): 1702-1710.
17. Green DR, Reed JC. (1998). Mitochondria, and apoptosis. Science. 281(5381): 1309-1312.
18. Grossfeld GD, Latini DM, Downs T, Lubeck DP, Mehta SS, Carroll PR. (2002). Is ethnicity an independent predictor of prostate cancer recurrence after radical prostatectomy?. J Urol. 168(6): 2510-2515.
19. Hayn MH, Orom H, Shavers VL, Sanda MG, Glasgow M, Mohler JL, Underwood 3rd W. (2011). Racial/ethnic differences in receipt of pelvic lymph node dissection among men with localized/regional prostate cancer. Cancer. 117(20): 4651-4658.
20. Haynes CM, Ron D. (2010). The mitochondrial UPR- protecting organelle protein homeostasis. J Cell Sci 123(Pt 22): 3849-3855.
21. Haynes CM, Yang Y, Blais SP, Neubert TA, Ron D. (2010). The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C elegans. Mol Cell. 374: 529-540.
22. Huang Q, Li F, Liu X, Li W, Shi W, Liu FF, OSullivan B, He Z, Peng Y, Tan AC, Zhou L, Shen J, Han G, Wang XJ, Thorburn J, Thorburn A, Jimeno A, Raben D, Bedford JS, Li CY. (2011). Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy. Nat Med. 17(7): 860-866.
23. Indran IR, Tufo G, Pervaiz S, Brenner C. (2011). Recent advances in apoptosis, mitochondria, and drug resistance in cancer cells. Biochim Biophys Acta 1807(6): 735-745.
24. Koochekpour S, Maresh GA, Katner A, Parker-Johnson K, Lee TJ, Hebert FE, Kao YS, Skinner J, Rayford W. (2004). Establishment, and characterization of a primary androgen-responsive African-American prostate cancer cell line, E006AA. Prostate. 60(2): 141-152.
25. Koochekpour S, Marlowe T, Singh KK, Attwood K, Chandra D. (2013). Reduced mitochondrial DNA content associates with poor prognosis of prostate cancer in African American men. PloS One. 8(9): e74688.
26. Koochekpour S, Willard SS, Shourideh M, Ali S, Liu C, Azabdaftari G, Saleem M, Attwood K. (2014). Establishment, and characterization of a highly tumorigenic african american prostate cancer cell line, E006AA-hT. Int J Biol Sci. 10(8): 834-845.
27. Latini DM, Elkin EP, Cooperberg MR, Sadetsky N, Duchane J, Carroll PR. (2006). Differences in clinical characteristics, and disease-free survival for Latino, African American, and non-Latino white men with localized prostate cancer: data from CaPSURE. Cancer. 106(4): 789-795.
28. Majmundar AJ, Wong WJ, Simon MC. (2010). Hypoxia-inducible factors, and the response to hypoxic stress. Mol Cell. 40(2): 294-309.
29. McIntosh H. (1997). Why do African-American men suffer more prostate cancer?. J Natl Cancer Inst. 89(3): 188-189.
30. Michelakis ED, Webster L, Mackey JR. (2008). Dichloroacetate (DCA) as a potential metabolic-Targeting therapy for cancer. Br J Cancer. 99(7): 989-994.
31. Pathak RK, Marrache S, Harn DA, Dhar S. (2014). Mito-DCA: a mitochondria targeted molecular scaffold for efficacious delivery of metabolic modulator dichloroacetate. ACS Chem Biol. 95: 1178-1187.
32. Pecqueur C, Oliver L, Oizel K, Lalier L, Vallette FM. (2013). Targeting metabolism to induce cell death in cancer cells, and cancer stem cells. Int J Cell Biol. 2013: 805975.
33. Pelicano H, Xu RH, Du M, Feng L, Sasaki R, Carew JS, Hu Y, Ramdas L, Hu L, Keating MJ, Zhang W, Plunkett W, Huang P. (2006). Mitochondrial respiration defects in cancer cells cause activation of Akt survival pathway through a redox-mediated mechanism. J Cell Biol. 1756: 913-923.
34. Pellegrino MW, Nargund AM, Haynes CM. (2013). Signaling the mitochondrial unfolded protein response. Biochim Biophys Acta 1833(2): 410-416.
35. Ponnala S, Chetty C, Veeravalli KK, Dinh DH, Klopfenstein JD, Rao JS. (2012). Metabolic remodeling precedes mitochondrial outer membrane permeabilization in human glioma xenograft cells. Int J Oncol. 40(2): 509-518.
36. Powell IJ, Banerjee M, Novallo M, Sakr W, Grignon D, Wood DP, Pontes JE. (2000). Prostate cancer biochemical recurrence stage for stage is more frequent among African-American than white men with locally advanced but not organ-confined disease. Urology. 55(2): 246-251.
37. Powell IJ, Heilbrun LK, Sakr W, Grignon D, Montie J, Novallo M, Smith D, Pontes JE. (1997). The predictive value of race as a clinical prognostic factor among patients with clinically localized prostate cancer: a multivariate analysis of positive surgical margins. Urology. 49(5): 726-731.
38. Pucci B, Kasten M, Giordano A. (2000). Cell cycle, and apoptosis. Neoplasia. 2(4): 291-299.
39. Schieber M, Chandel NS. (2014). ROS function in redox signaling, and oxidative stress. Curr Biol. 24(10): R453-R462.
40. Sebastian B, Kakizuka A, Hunter T. (1993). Cdc25M2 activation of cyclindependent kinases by dephosphorylation of threonine-14, and tyrosine-15. Proc Natl Acad Sci USA. 90(8): 3521-3524.
41. Seliger C, Leukel P, Moeckel S, Jachnik B, Lottaz C, Kreutz M, Brawanski A, Proescholdt M, Bogdahn U, Bosserhoff AK, Vollmann-Zwerenz A, Hau P. (2013). Lactate-modulated induction of THBS-1 activates transforming growth factor (TGF)-beta2, and migration of glioma cells in vitro. PloS One. 8(11): e78935.
42. Semenas J, Allegrucci C, Boorjian SA, Mongan NP, Persson JL. (2012). Overcoming drug resistance, and treating advanced prostate cancer. Curr Drug Targets. 13(10): 1308-1323.
43. Simon HU, Haj-Yehia A, Levi-Schaffer F. (2000). Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis. 5(5): 415-418.
44. Srivastava P, Yadav N, Lella R, Schneider A, Jones A, Marlowe T, Lovett G, OLoughlin K, Minderman H, Gogada R, Chandra D. (2012). Neem oil limonoids induces p53-independent apoptosis, and autophagy. Carcinogenesis. 33(11): 2199-2207.
45. Tait SW, Ichim G, Green DR. (2014). Die another way-non-Apoptotic mechanisms of cell death. J Cell Sci 127(Pt 10): 2135-2144.
46. Underwood W, De Monner S, Ubel P, Fagerlin A, Sanda MG, Wei JT. (2004). Racial/ethnic disparities in the treatment of localized/regional prostate cancer. J Urol. 171(4): 1504-1507.
47. Warburg O. (1956). On respiratory impairment in cancer cells. Science. 124(3215): 269-270.
48. Yadav N, Kumar S, Kumar R, Srivastava P, Sun L, Rapali P, Marlowe T, Schneider A, Inigo JR, OMalley J, Londonkar R, Gogada R, Chaudhary AK, Yadava N, Chandra D. (2016). Mechanism of neem limonoids-induced cell death in cancer: role of oxidative phosphorylation. Free Radic Biol Med. 90: 261-271.
49. Yadav N, Kumar S, Marlowe T, Chaudhary AK, Kumar R, Wang J, OMalley J, Boland PM, Jayanthi S, Kumar TK, Yadava N, Chandra D. (2015). Oxidative phosphorylation-dependent regulation of cancer cell apoptosis in response to anticancer agents. Cell Death Dis 6: e1969.
50. Yadav N, Pliss A, Kuzmin A, Rapali P, Sun L, Prasad P, Chandra D. (2014). Transformations of the macromolecular landscape at mitochondria during DNA-damage-induced apoptotic cell death. Cell Death Dis 5: e1453.
51. Yu M. (2012). Somatic mitochondrial DNA mutations in human cancers. Adv Clin Chem. 57: 99-138.
52. Yu M, Zhou Y, Shi Y, Ning L, Yang Y, Wei X, Zhang N, Hao X, Niu R. (2007). Reduced mitochondrial DNA copy number is correlated with tumor progression, and prognosis in Chinese breast cancer patients. IUBMB Life. 597: 450-457.
53. Zhao Q, Wang J, Levichkin, Stasinopoulos S, Ryan MT, Hoogenraad NJ. (2002) A mitochondrial specific stress response in mammalian cells. EMBO J. 21(17): 4411-4419.
54. Zhao Y, Butler EB, Tan M. (2013). Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis 4: e532.