A plant alkaloid, veratridine, potentiates cancer chemosensitivity by UBXN2A-dependent inhibition of an oncoprotein, mortalin-2

Oncotarget

Volumn 6, Issue 27, 2015, Pages 23561-23581

  Abdullah, Ammara ^a   Sane, Sanam ^a   Branick, Kate A ^a   Freeling, Jessica L ^a   Wang, Hongmin ^a   Zhang, Dong ^b   Rezvani, Khosrow ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

^b NEW YORK INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Chemotherapy; Mortalin 2; P53; UBXN2A; Veratridine

Indexed keywords

ETOPOSIDE; FLUOROURACIL; HERMES ANTIGEN; MORTALIN 2; ONCOPROTEIN; PROTEIN UBXN2A; UNCLASSIFIED DRUG; VERATRIDINE; ANTINEOPLASTIC AGENT; CD44 PROTEIN, HUMAN; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 70; HSPA9 PROTEIN, HUMAN; MITOCHONDRIAL PROTEIN; PLANT EXTRACT; PROTEIN P53; TP53 PROTEIN, HUMAN; UBIQUITIN; UBXN2A PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER CELL LINE; CANCER INHIBITION; COLON CANCER; COLON CANCER CELL LINE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; DRUG MECHANISM; DRUG POTENTIATION; DRUG RESPONSE; DRUG TARGETING; FEMALE; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; BREAST NEOPLASMS; CANCER TRANSPLANTATION; CHEMISTRY; COLON TUMOR; DISEASE COURSE; DRUG EFFECTS; ENHANCER REGION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HCT 116 CELL LINE; METABOLISM; NUDE MOUSE; PROTEIN MICROARRAY; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD44; ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; COLONIC NEOPLASMS; CYTOPLASM; DISEASE PROGRESSION; ENHANCER ELEMENTS, GENETIC; ETOPOSIDE; FEMALE; FLUOROURACIL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GREEN FLUORESCENT PROTEINS; HCT116 CELLS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MICE; MICE, NUDE; MITOCHONDRIAL PROTEINS; NEOPLASM TRANSPLANTATION; PLANT EXTRACTS; PROTEIN ARRAY ANALYSIS; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN; UBIQUITINS; VERATRIDINE;

EID: 84943422058     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4452     Document Type: Article

References (73)

1. Kaul SC, Aida S, Yaguchi T, Kaur K, Wadhwa R. Activation of wild type p53 function by its mortalinbinding, cytoplasmically localizing carboxyl terminus peptides. J Biol Chem. 2005;280:39373-39379.
2. Lu WJ, Lee NP, Kaul SC, Lan F, Poon RT, Wadhwa R, Luk JM. Mortalin-p53 interaction in cancer cells is stress dependent and constitutes a selective target for cancer therapy. Cell Death Differ. 2011;6:1046-1056.
3. Wadhwa R, Takano S, Robert M, Yoshida A, Nomura H, Reddel RR, Mitsui Y, Kaul SC. Inactivation of tumor suppressor p53 by mot-2, a hsp70 family member. J Biol Chem. 1998;273:29586-29591.
4. Sane S, Abdullah A, Boudreau DA, Autenried RK, Gupta BK, Wang X, Wang H, Schlenker EH, Zhang D, Telleria C, Huang L, Chauhan SC, Rezvani K. Ubiquitin-like (UBX)-domain-containing protein, UBXN2A, promotes cell death by interfering with the p53-Mortalin interactions in colon cancer cells. Cell Death Dis. 2014;5:e1118.
5. Burbulla LF, Schelling C, Kato H, Rapaport D, Woitalla D, Schiesling C, Schulte C, Sharma M, Illig T, Bauer P, Jung S, Nordheim A, Schols L, Riess O, Kruger R. Dissecting the role of the mitochondrial chaperone mortalin in Parkinson's disease:functional impact of disease-related variants on mitochondrial homeostasis. Hum Mol Genet. 2010;19:4437-4452.
6. Grover A, Priyandoko D, Gao R, Shandilya A, Widodo N, Bisaria VS, Kaul SC, Wadhwa R, Sundar D. Withanone binds to mortalin and abrogates mortalin-p53 complex: computational and experimental evidence. Int J Biochem Cell Biol. 2012;44:496-504.
7. Wadhwa R, Sugihara T, Yoshida A, Nomura H, Reddel RR, Simpson R, Maruta H, Kaul SC. Selective toxicity of MKT-077 to cancer cells is mediated by its binding to the hsp70 family protein mot-2 and reactivation of p53 function. Cancer Res. 2000;60:6818-6821.
8. Koya K, Li Y, Wang H, Ukai T, Tatsuta N, Kawakami M, Shishido , Chen LB. MKT-077, a novel rhodacyanine dye in clinical trials, exhibits anticarcinoma activity in preclinical studies based on selective mitochondrial accumulation. Cancer Res. 1996;56:538-543.
9. Dundas SR, Lawrie LC, Rooney PH, Murray GI. Mortalin is over-expressed by colorectal adenocarcinomas and correlates with poor survival. J Pathol. 2005;205:74-81.
10. Ando K, Oki E, Zhao Y, Ikawa-Yoshida A, Kitao H, Saeki H, Kimura Y, Ida S, Morita M, Kusumoto T, Maehara Y. Mortalin is a prognostic factor of gastric cancer with normal p53 function. Gastric Cancer. 2014;17:255-262.
11. Chen J, Liu WB, Jia WD, Xu GL, Ma JL, Huang M, Deng YR, Li JS. Overexpression of Mortalin in hepatocellular carcinoma and its relationship with angiogenesis and epithelial to mesenchymal transition. Int J Oncol. 2014; 44:247-255.
12. Takano S, Wadhwa R, Yoshii Y, Nose T, Kaul SC, Mitsui Y. Elevated levels of mortalin expression in human brain tumors. Exp Cell Res. 1997;237:38-45.
13. Gao RN, Neutel CI, Wai E. Gender differences in colorectal cancer incidence, mortality, hospitalizations and surgical procedures in Canada. J Public Health (Oxf). 2008; 30:194-201.
14. Boyle P, Leon ME. Epidemiology of colorectal cancer. Br Med Bull. 2002;64:1-25.
15. Warren RS, Atreya CE, Niedzwiecki D, Weinberg VK, Donner DB, Mayer RJ, Goldberg RM, Compton CC, Zuraek MB, Ye C, Saltz LB, Bertagnolli MM. Association of TP53 mutational status and gender with survival after adjuvant treatment for stage III colon cancer:results of CALGB 89803. Clin Cancer Res. 2013;19:5777-5787.
16. Vaziri SA, Krumroy LM, Elson P, Budd GT, Darlington G, Myles J, Tubbs RR, Casey G. Breast tumor immunophenotype of BRCA1-mutation carriers is influenced by age at diagnosis. Clin Cancer Res. 2001;7:1937-1945.
17. Sutandyo N, Suzanna E, Haryono SJ, Reksodiputro AH. Signaling pathways in early onset sporadic breast cancer of patients in Indonesia. Acta Med Indones. 2008; 40:139-145.
18. Lee JJ, Kim YM, Jeong J, Bae DS, Lee KJ. UbiquitinAssociated (UBA) Domain in Human Fas Associated Factor 1 Inhibits Tumor Formation by Promoting Hsp70 Degradation. PLoS One. 2012;7:e40361.
19. Phan VT, Ding VW, Li F, Chalkley RJ, Burlingame A, McCormick F. The RasGAP proteins Ira2 and neurofibromin are negatively regulated by Gpb1 in yeast and ETEA in humans. Mol Cell Biol. 2010;30:2264-2279.
20. Wu-Baer F, Ludwig T, Baer R. The UBXN1 protein associates with autoubiquitinated forms of the BRCA1 tumor suppressor and inhibits its enzymatic function. Mol Cell Biol. 2010;11:2787-2798.
21. Brotherick I, Shenton BK, Cowan WK, Angus B, Horne CH, Higgs MJ, Lennard TW. p53 expression measured by flow cytometry. A comparison of three monoclonal antibodies and the relationship with grade and DNA ploidy in breast cancer. Cancer Immunol Immunother. 1995; 41:146-150.
22. Wu PK, Hong SK, Veeranki S, Karkhanis M, Starenki D, Plaza JA, Park JI. A mortalin/HSPA9-mediated switch in tumor-suppressive signaling of Raf/MEK/extracellular signal-regulated kinase. Mol Cell Biol. 2013;33:4051-4067.
23. Zhang J, Wang C, Ke N, Bliesath J, Chionis J, He QS, Li QX, Chatterton JE, Wong-Staal F, Zhou D. A more efficient RNAi inducible system for tight regulation of gene expression in mammalian cells and xenograft animals. RNA. 2007;13:1375-1383.
24. Hensley H, Devarajan K, Johnson JR, Piwnica-Worms D, Godwin AK, von Mehren M, Rink L. Evaluating new therapies in gastrointestinal stromal tumor using in vivo molecular optical imaging. Cancer Biol Ther. 2014;15:911-918.
25. Lu WJ, Lee NP, Kaul SC, Lan F, Poon RT, Wadhwa R, Luk JM. Induction of mutant p53-dependent apoptosis in human hepatocellular carcinoma by targeting stress protein mortalin. Int J Cancer. 2011;129:1806-1814.
26. Windham TC, Parikh NU, Siwak DR, Summy JM, McConkey DJ, Kraker AJ, Gallick GE. Src activation regulates anoikis in human colon tumor cell lines. Oncogene. 2002;21:7797-7807.
27. Zhang H, Hoang T, Saeed B, Ng SC. Induction of apoptosis in prostatic tumor cell line DU145 by staurosporine, a potent inhibitor of protein kinases. Prostate. 1996; 29:69-76.
28. Short DM, Heron ID, Birse-Archbold JL, Kerr LE, Sharkey J, McCulloch J. Apoptosis induced by staurosporine alters chaperone and endoplasmic reticulum proteins: Identification by quantitative proteomics. Proteomics. 2007; 7:3085-3096.
29. Rezvani K, Teng Y, Pan Y, Dani JA, Lindstrom J, Garcia Gras EA, McIntosh JM, De Biasi M. UBXD4, a UBXcontaining protein, regulates the cell surface number and stability of alpha3-containing nicotinic acetylcholine receptors. J Neurosci. 2009;29:6883-6896.
30. Bourin M, Chenu F, Hascoet M. Topiramate and phenytoin anti-immobility effect in the mice forced swimming test is reversed by veratrine:Implication for bipolar depression treatment. Behav Brain Res. 2009;205:421-425.
31. Benforado JM. The veratrum alkaloids. Physiological pharmacology. 1967.
32. Hare JD. Purification and Quantitative Analysis of Veratridine and Cevadine by HPLC. Journal of Agricultural and Food Chemistry. 1996;44:149-152.
33. Loizzo MR, Tundis R, Menichini F, Statti GA. Hypotensive natural products:current status. Mini Rev Med Chem. 2008; 8:828-855.
34. Fraser SP, Grimes JA, Djamgoz MB. Effects of voltagegated ion channel modulators on rat prostatic cancer cell proliferation:comparison of strongly and weakly metastatic cell lines. Prostate. 2000;44:61-76.
35. Fraser SP, Salvador V, Manning EA, Mizal J, Altun S, Raza M, Berridge RJ, Djamgoz MB. Contribution of functional voltage-gated Na+ channel expression to cell behaviors involved in the metastatic cascade in rat prostate cancer: I. Lateral motility. J Cell Physiol. 2003;195:479-487.
36. Jordan J, Galindo MF, Calvo S, Gonzalez-Garcia C, Cena V. Veratridine induces apoptotic death in bovine chromaffin cells through superoxide production. Br J Pharmacol. 2000;130:1496-1504.
37. Jordan J, Galindo MF, Tornero D, Benavides A, Gonzalez C, Agapito MT, Gonzalez-Garcia C, Cena V. Superoxide anions mediate veratridine-induced cytochrome c release and caspase activity in bovine chromaffin cells. Br J Pharmacol. 2002;137:993-1000.
38. Gomez-Lazaro M, Galindo MF, Fernandez-Gomez FJ, Prehn JH, Jordan J. Activation of p53 and the pro-apoptotic p53 target gene PUMA during depolarization-induced apoptosis of chromaffin cells. Exp Neurol. 2005;196:96-103.
39. Sui X, Kong N, Wang X, Fang Y, Hu X, Xu Y, Chen W, Wang K, Li D, Jin W, Lou F, Zheng Y, Hu H, Gong L, Zhou X, Pan H, et al. JNK confers 5-fluorouracil resistance in p53-deficient and mutant p53-expressing colon cancer cells by inducing survival autophagy. Sci Rep. 2014;4:4694.
40. Kaul Z, Yaguchi T, Kaul SC, Hirano T, Wadhwa R, Taira K. Mortalin imaging in normal and cancer cells with quantum dot immuno-conjugates. Cell Res. 2003; 13:503-507.
41. Widodo N, Deocaris CC, Kaur K, Hasan K, Yaguchi T, Yamasaki K, Sugihara T, Ishii T, Wadhwa R, Kaul SC. Stress chaperones, mortalin, and pex19p mediate 5-aza-2' deoxycytidine-induced senescence of cancer cells by DNA methylation-independent pathway. J Gerontol A Biol Sci Med Sci. 2007;62:246-255.
42. Green DR, Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature. 2009;458:1127-1130.
43. Hermanson D, Addo SN, Bajer AA, Marchant JS, Das SG, Srinivasan B, Al-Mousa F, Michelangeli F, Thomas DD, Lebien TW, Xing C. Dual mechanisms of sHA 14-1 in inducing cell death through endoplasmic reticulum and mitochondria. Mol Pharmacol. 2009;76:667-678.
44. Harwood FG, Frazier MW, Krajewski S, Reed JC, Houghton JA. Acute and delayed apoptosis induced by thymidine deprivation correlates with expression of p53 and p53-regulated genes in colon carcinoma cells. Oncogene. 1996;12:2057-2067.
45. Violette S, Poulain L, Dussaulx E, Pepin D, Faussat AM, Chambaz J, Lacorte JM, Staedel C, Lesuffleur T. Resistance of colon cancer cells to long-term 5-fluorouracil exposure is correlated to the relative level of Bcl-2 and Bcl-X(L) in addition to Bax and p53 status. Int J Cancer. 2002;98:498-504.
46. Parmar N, Nichole Wetton, Shelley Alvarado, Shane Kennedy. Profiling of human normal and cancer cell lines using phenotype microarray analysis. The FASEB Journal. 2014;28:613-615.
47. Hondroulis E, Zhang R, Zhang C, Chen C, Ino K, Matsue T, Li CZ. Immuno nanoparticles integrated electrical control of targeted cancer cell development using whole cell bioelectronic device. Theranostics. 2014;4:919-930.
48. Taherian A, Li X, Liu Y, Haas TA. Differences in integrin expression and signaling within human breast cancer cells. BMC Cancer. 2011;11:293.
49. Lowe SW, Cepero E, Evan G. Intrinsic tumour suppression. Nature. 2004;432:307-315.
50. Gajate C, An F, Mollinedo F. Differential cytostatic and apoptotic effects of ecteinascidin-743 in cancer cells. Transcription-dependent cell cycle arrest and transcriptionindependent JNK and mitochondrial mediated apoptosis. J Biol Chem. 2002;277:41580-41589.
51. Deeb KK, Trump DL, Johnson CS. Vitamin D signalling pathways in cancer:potential for anticancer therapeutics. Nat Rev Cancer. 2007;7:684-700.
52. Yang MH, Kim J, Khan IA, Walker LA, Khan SI. Nonsteroidal anti-inflammatory drug activated gene-1 (NAG-1) modulators from natural products as anti-cancer agents. Life Sci. 2014;100:75-84.
53. Chan JY, Phoo MS, Clement MV, Pervaiz S, Lee SC. Resveratrol displays converse dose-related effects on 5-fluorouracil-evoked colon cancer cell apoptosis:the roles of caspase-6 and p53. Cancer Biol Ther. 2008; 7:1305-1312.
54. Kozovska Z, Gabrisova V, Kucerova L. Colon cancer: cancer stem cells markers, drug resistance and treatment. Biomed Pharmacother. 2014;68:911-916.
55. Schmoll HJ, Buchele T, Grothey A, Dempke W. Where do we stand with 5-fluorouracil?. Semin Oncol. 1999; 26:589-605.
56. Rao GH, Liu HM, Li BW, Hao JJ, Yang YL, Wang MR, Wang XH, Wang J, Jin HJ, Du L, Chen Q. Establishment of a human colorectal cancer cell line P6C with stem cell properties and resistance to chemotherapeutic drugs. Acta Pharmacol Sin. 2013;34:793-804.
57. Kurashina K, Yamashita Y, Ueno T, Koinuma K, Ohashi J, Horie H, Miyakura Y, Hamada T, Haruta H, Hatanaka H, Soda M, Choi YL, Takada S, Yasuda Y, Nagai H, Mano H. Chromosome copy number analysis in screening for prognosis-related genomic regions in colorectal carcinoma. Cancer Sci. 2008;99:1835-1840.
58. Hsu TI, Wang MC, Chen SY, Yeh YM, Su WC, Chang WC, Hung JJ. Sp1 expression regulates lung tumor progression. Oncogene. 2012;31:3973-3988.
59. Yang B, Cao L, Liu J, Xu Y, Milne G, Chan W, Heys SD, McCaig CD, Pu J. Low expression of chloride channel accessory 1 predicts a poor prognosis in colorectal cancer. Cancer. 2015;121:1570-1580.
60. Braun MS, Richman SD, Quirke P, Daly C, Adlard JW, Elliott F, Barrett JH, Selby P, Meade AM, Stephens RJ, Parmar MK, Seymour MT. Predictive biomarkers of chemotherapy efficacy in colorectal cancer:results from the UK MRC FOCUS trial. J Clin Oncol. 2008;26:2690-2698.
61. Shao RG, Cao CX, Nieves-Neira W, Dimanche-Boitrel MT, Solary E, Pommier Y. Activation of the Fas pathway independently of Fas ligand during apoptosis induced by camptothecin in p53 mutant human colon carcinoma cells. Oncogene. 2001;20:1852-1859.
62. Upreti M, Lyle CS, Skaug B, Du L, Chambers TC. Vinblastine-induced apoptosis is mediated by discrete alterations in subcellular location, oligomeric structure, and activation status of specific Bcl-2 family members. J Biol Chem. 2006;281:15941-15950.
63. Urra FA, Cordova-Delgado M, Pessoa-Mahana H, Ramirez-Rodriguez O, Weiss-Lopez B, Ferreira J, ArayaMaturana R. Mitochondria:a promising target for anticancer alkaloids. Curr Top Med Chem. 2013;13:2171-2183.
64. Yang L, Guo W, Zhang Q, Li H, Liu X, Yang Y, Zuo J, Liu W. Crosstalk between Raf/MEK/ERK and PI3K/AKT in suppression of Bax conformational change by Grp75 under glucose deprivation conditions. J Mol Biol. 2011; 414:654-666.
65. Guo W, Yan L, Yang L, Liu X, Qiukai E, Gao P, Ye X, Liu W, Zuo J. Targeting GRP75 improves HSP90 inhibitor efficacy by enhancing p53-mediated apoptosis in hepatocellular carcinoma. PLoS One. 2014;9:e85766.
66. Saar Ray M, Moskovich O, Iosefson O, Fishelson Z. Mortalin/Grp75 Binds to Complement C9 and Plays a Role in Resistance to Complement-Dependent Cytotoxicity. J Biol Chem. 2014;289:15014-15022.
67. Ryu J, Kaul Z, Yoon AR, Liu Y, Yaguchi T, Na Y, Ahn HM, Gao R, Choi IK, Yun CO, Kaul SC, Wadhwa R. Identification and functional characterization of nuclear mortalin in human carcinogenesis. J Biol Chem. 2014; 289:24832-24844.
68. Yoo JY, Ryu J, Gao R, Yaguchi T, Kaul SC, Wadhwa R, Yun CO. Tumor suppression by apoptotic and antiangiogenic effects of mortalin-targeting adeno-oncolytic virus. J Gene Med. 2010;12:586-595.
69. Vidal SJ, Rodriguez-Bravo V, Galsky M, Cordon-Cardo C, Domingo-Domenech J. Targeting cancer stem cells to suppress acquired chemotherapy resistance. Oncogene. 2014;33:4451-4463.
70. Tai-Nagara I, Matsuoka S, Ariga H, Suda T. Mortalin and DJ-1 coordinately regulate hematopoietic stem cell function through the control of oxidative stress. Blood. 2014; 123:41-50.
71. Kanwar SS, Yu Y, Nautiyal J, Patel BB, Padhye S, Sarkar FH, Majumdar AP. Difluorinated-curcumin (CDF):a novel curcumin analog is a potent inhibitor of colon cancer stem-like cells. Pharm Res. 2011; 28:827-838.
72. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ, Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007; 1:313-323.
73. Witney TH, Kettunen MI, Hu DE, Gallagher FA, Bohndiek SE, Napolitano R, Brindle KM. Detecting treatment response in a model of human breast adenocarcinoma using hyperpolarised [1-13C]pyruvate and [1,4-13C2]fumarate. Br J Cancer. 2010;103:1400-1406.