A novel class of mitochondria-targeted soft electrophiles modifies mitochondrial proteins and inhibits mitochondrial metabolism in breast cancer cells through redox mechanisms

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Vayalil, Praveen K ^a,b   Oh, Joo Yeun ^a,b   Zhou, Fen ^a,b   Diers, Anne R ^a,b,f   Smith, M Ryan ^a,b   Golzarian, Hafez ^b   Oliver, Patsy G ^c   Smith, Robin A J ^d   Murphy, Michael P ^e   Velu, Sadanandan E ^b   Landar, Aimee ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c The University of Alabama at Birmingham   (United States)

^d UNIVERSITY OF OTAGO   (New Zealand)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f Berg Biosystems   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

10 CARBON IODOPROPYL TRIPHENYLPHOSPHONIUM; 3, 4, 6, 8 IODOPROPYL TRIPHENYLPHOSPHONIUM; ELECTROPHILE; IODOBUTYL TRIPHENYLPHOSPHONIUM; IODODECYL TRIPHENYLPHOSPHONIUM; IODOHEXYL TRIPHENYLPHOSPHONIUM; IODOOCTYL TRIPHENYLPHOSPHONIUM; MITOCHONDRIA TARGETED SOFT ELECTROPHILE; MITOCHONDRIAL PROTEIN; UNCLASSIFIED DRUG; (4-IODOBUTYL)TRIPHENYLPHOSPHONIUM; ORGANOPHOSPHORUS COMPOUND;

ALKYLATION; ARTICLE; BIOENERGY; BREAST CANCER; BREAST CANCER CELL LINE; CARBON NUCLEAR MAGNETIC RESONANCE; CELL ADHESION; CELL FRACTIONATION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL STRESS; CHEMICAL STRUCTURE; GLYCOLYSIS; HUMAN; IMMUNOBLOTTING; IN VITRO STUDY; MITOCHONDRIA TARGETED SOFT ELECTROPHILES; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTON NUCLEAR MAGNETIC RESONANCE; BREAST TUMOR; CELL MOTION; DRUG EFFECTS; ELECTRON TRANSPORT; ENERGY METABOLISM; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; ELECTRON TRANSPORT; ENERGY METABOLISM; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; ORGANOPHOSPHORUS COMPOUNDS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84925707456     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120460     Document Type: Article

References (56)

1. Warburg O. On respiratory impairment in cancer cells. Science. 1956; 124:269-70. PMID: 13351639
2. Cheng G, Zielonka J, McAllister DM, Mackinnon AC Jr., Joseph J, Dwinell MB, et al. Mitochondria-targeted vitamin E analogs inhibit breast cancer cell energy metabolism and promote cell death. BMC Cancer. 2013; 13:285. doi: 10.1186/1471-2407-13-285 PMID: 23764021
3. Diers AR, Vayalil PK, Oliva CR, Griguer CE, Darley-Usmar V, Hurst DR, et al. Mitochondrial bioenergetics of metastatic breast cancer cells in response to dynamic changes in oxygen tension: effects of HIF-1alpha. PLoS One. 2013; 8:e68348. doi: 10.1371/journal.pone.0068348 PMID: 23840849
4. Li Z, Lopez M, Hardy M, McAllister DM, Kalyanaraman B, Zhao M. A (99m)Tc-labeled triphenylphosphonium derivative for the early detection of breast tumors. Cancer Biother Radiopharm. 2009; 24:579-87. doi: 10.1089/cbr.2008.0606 PMID: 19877888
5. Griguer CE, Oliva CR. Bioenergetics pathways and therapeutic resistance in gliomas: emerging role of mitochondria. Curr Pharm Des. 2011; 17:2421-7. PMID: 21827418
6. Griguer CE, Oliva CR, Gillespie GY. Glucose metabolism heterogeneity in human and mouse malignant glioma cell lines. J Neurooncol. 2005; 74:123-33. PMID: 16193382
7. Cheng G, Zielonka J, Dranka BP, McAllister D, Mackinnon AC Jr., Joseph J, et al. Mitochondria-targeted drugs synergize with 2-deoxyglucose to trigger breast cancer cell death. Cancer Res. 2012; 72:2634-44. doi: 10.1158/0008-5472.CAN-11-3928 PMID: 22431711
8. Millard M, Gallagher JD, Olenyuk BZ, Neamati N. A selective mitochondrial-targeted chlorambucil with remarkable cytotoxicity in breast and pancreatic cancers. J Med Chem. 2013; 56:9170-9. doi: 10.1021/jm4012438 PMID: 24147900
9. Reily C, Mitchell T, Chacko BK, Benavides G, Murphy MP, Darley-Usmar V. Mitochondrially targeted compounds and their impact on cellular bioenergetics. Redox Biol. 2013; 1:86-93. PMID: 23667828
10. Diers AR, Higdon AN, Ricart KC, Johnson MS, Agarwal A, Kalyanaraman B, et al. Mitochondrial targeting of the electrophilic lipid 15-deoxy-Delta12,14-prostaglandin J2 increases apoptotic efficacy via redox cell signalling mechanisms. Biochem J. 2010; 426:31-41. doi: 10.1042/BJ20091293 PMID: 19916962
11. Lopachin RM, Gavin T, Decaprio A, Barber DS. Application of the Hard and Soft, Acids and Bases (HSAB) theory to toxicant - target interactions. Chem Res Toxicol. 2012; 25:239-51. doi: 10.1021/tx2003257 PMID: 22053936
12. Schopfer FJ, Cipollina C, Freeman BA. Formation and signaling actions of electrophilic lipids. Chem Rev. 2011; 111:5997-6021. doi: 10.1021/cr200131e PMID: 21928855
13. Baker LM, Baker PR, Golin-Bisello F, Schopfer FJ, Fink M, Woodcock SR, et al. Nitro-fatty acid reaction with glutathione and cysteine. Kinetic analysis of thiol alkylation by a Michael addition reaction. J Biol Chem. 2007; 282:31085-93. PMID: 17720974
14. Ahn YH, Hwang Y, Liu H, Wang XJ, Zhang Y, Stephenson KK, et al. Electrophilic tuning of the chemoprotective natural product sulforaphane. Proc Natl Acad Sci U S A. 2010; 107:9590-5. doi: 10.1073/pnas.1004104107 PMID: 20439747
15. Roberts DW, Aptula AO, Patlewicz GY. Chemistry-based risk assessment for skin sensitization: quantitative mechanistic modeling for the S(N)Ar domain. Chem Res Toxicol. 2011; 24:1003-11. doi: 10.1021/tx100420w PMID: 21671633
16. Wall SB, Oh JY, Diers AR, Landar A. Oxidative modification of proteins: an emerging mechanism of cell signaling. Front Physiol. 2012; 3:369. doi: 10.3389/fphys.2012.00369 PMID: 23049513
17. Forman HJ, Davies KJ, Ursini F. How do nutritional antioxidants really work: nucleophilic tone and para-hormesis versus free radical scavenging in vivo. Free Radic Biol Med. 2014; 66:24-35. doi: 10.1016/j.freeradbiomed.2013.05.045 PMID: 23747930
18. Oh JY, Giles N, Landar A, Darley-Usmar V. Accumulation of 15-deoxy-delta(12,14)-prostaglandin J2 adduct formation with Keap1 over time: effects on potency for intracellular antioxidant defence induction. Biochem J. 2008; 411:297-306. doi: 10.1042/bj20071189 PMID: 18237271
19. Sanchez-Gomez FJ, Cernuda-Morollon E, Stamatakis K, Perez-Sala D. Protein thiol modification by 15-deoxy-Delta12,14-prostaglandin J2 addition in mesangial cells: role in the inhibition of pro-inflammatory genes. Mol Pharmacol. 2004; 66:1349-58. PMID: 15317873
20. Lu J, Holmgren A. Selenoproteins. J Biol Chem. 2009; 284:723-7. doi: 10.1074/jbc.R800045200 PMID: 18757362
21. LoPachin RM, Gavin T, Geohagen BC, Das S. Neurotoxic mechanisms of electrophilic type-2 alkenes: soft soft interactions described by quantum mechanical parameters. Toxicol Sci. 2007; 98:561-70. PMID: 17519395
22. Landar A, Oh JY, Giles NM, Isom A, Kirk M, Barnes S, et al. A sensitive method for the quantitative measurement of protein thiol modification in response to oxidative stress. Free Radic Biol Med. 2006; 40:459-68. PMID: 16443161
23. Cooper CE, Patel RP, Brookes PS, Darley-Usmar VM. Nanotransducers in cellular redox signaling: modification of thiols by reactive oxygen and nitrogen species. Trends Biochem Sci. 2002; 27:489-92. PMID: 12368076
24. Hansen JM, Go YM, Jones DP. Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling. Annu Rev Pharmacol Toxicol. 2006; 46:215-34. PMID: 16402904
25. Nulton-Persson AC, Starke DW, Mieyal JJ, Szweda LI. Reversible inactivation of alpha-ketoglutarate dehydrogenase in response to alterations in the mitochondrial glutathione status. Biochemistry. 2003; 42:4235-42. PMID: 12680778
26. Kil IS, Park JW. Regulation of mitochondrial NADP+-dependent isocitrate dehydrogenase activity by glutathionylation. J Biol Chem. 2005; 280:10846-54. PMID: 15653693
27. Venkatraman A, Landar A, Davis AJ, Ulasova E, Page G, Murphy MP, et al. Oxidative modification of hepatic mitochondria protein thiols: effect of chronic alcohol consumption. Am J Physiol Gastrointest Liver Physiol. 2004; 286:G521-7. PMID: 14670822
28. Taylor ER, Hurrell F, Shannon RJ, Lin TK, Hirst J, Murphy MP. Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J Biol Chem. 2003; 278:19603-10. PMID: 12649289
29. Chen YR, Chen CL, Pfeiffer DR, Zweier JL. Mitochondrial complex II in the post-ischemic heart: oxidative injury and the role of protein S-glutathionylation. J Biol Chem. 2007; 282:32640-54. PMID: 17848555
30. Lin TK, Hughes G, Muratovska A, Blaikie FH, Brookes PS, Darley-Usmar V, et al. Specific modification of mitochondrial protein thiols in response to oxidative stress: a proteomics approach. J Biol Chem. 2002; 277:17048-56. PMID: 11861642
31. Lin TK, Hughes G, Muratovska A, Blaikie FH, Brookes PS, Darley-Usmar V, et al. Specific modification of mitochondrial protein thiols in response to oxidative stress: a proteomics approach. The Journal of biological chemistry. 2002; 277:17048-56. PMID: 11861642
32. Ferrick DA, Neilson A, Beeson C. Advances in measuring cellular bioenergetics using extracellular flux. Drug Discov Today. 2008; 13:268-74. doi: 10.1016/j.drudis.2007.12.008 PMID: 18342804
33. Wu M, Neilson A, Swift AL, Moran R, Tamagnine J, Parslow D, et al. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am J Physiol Cell Physiol. 2007; 292:C125-36. PMID: 16971499
34. Dranka BP, Benavides GA, Diers AR, Giordano S, Zelickson BR, Reily C, et al. Assessing bioenergetic function in response to oxidative stress by metabolic profiling. Free Radic Biol Med. 2011; 51:1621-35. doi: 10.1016/j.freeradbiomed.2011.08.005 PMID: 21872656
35. Hill BG, Dranka BP, Zou L, Chatham JC, Darley-Usmar VM. Importance of the bioenergetic reserve capacity in response to cardiomyocyte stress induced by 4-hydroxynonenal. Biochem J. 2009; 424:99-107. doi: 10.1042/BJ20090934 PMID: 19740075
36. Wu M, Neilson A, Swift AL, Moran R, Tamagnine J, Parslow D, et al. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. American journal of physiology Cell physiology. 2007; 292:C125-36. PMID: 16971499
37. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 2007; 13:4429-34. PMID: 17671126
38. Lin NU, Claus E, Sohl J, Razzak AR, Arnaout A, Winer EP. Sites of distant recurrence and clinical outcomes in patients with metastatic triple-negative breast cancer: high incidence of central nervous system metastases. Cancer. 2008; 113:2638-45. doi: 10.1002/cncr.23930 PMID: 18833576
39. McCleland ML, Adler AS, Shang Y, Hunsaker T, Truong T, Peterson D, et al. An integrated genomic screen identifies LDHB as an essential gene for triple-negative breast cancer. Cancer Res. 2012; 72:5812-23. doi: 10.1158/0008-5472.CAN-12-1098 PMID: 23139210
40. Oliva CR, Nozell SE, Diers A, McClugage SG 3rd, Sarkaria JN, Markert JM, et al. Acquisition of temozolomide chemoresistance in gliomas leads to remodeling of mitochondrial electron transport chain. J Biol Chem. 2010; 285:39759-67. doi: 10.1074/jbc.M110.147504 PMID: 20870728
41. Astuti D, Latif F, Dallol A, Dahia PL, Douglas F, George E, et al. Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am J Hum Genet. 2001; 69:49-54. PMID: 11404820
42. Tomlinson IP, Alam NA, Rowan AJ, Barclay E, Jaeger EE, Kelsell D, et al. Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer. Nat Genet. 2002; 30:406-10. PMID: 11865300
43. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med. 2009; 360:765-73. doi: 10.1056/NEJMoa0808710 PMID: 19228619
44. Marin-Valencia I, Yang C, Mashimo T, Cho S, Baek H, Yang XL, et al. Analysis of tumor metabolism reveals mitochondrial glucose oxidation in genetically diverse human glioblastomas in the mouse brain in vivo. Cell Metab. 2012; 15:827-37. doi: 10.1016/j.cmet.2012.05.001 PMID: 22682223
45. Whitaker-Menezes D, Martinez-Outschoorn UE, Flomenberg N, Birbe RC, Witkiewicz AK, Howell A, et al. Hyperactivation of oxidative mitochondrial metabolism in epithelial cancer cells in situ: visualizing the therapeutic effects of metformin in tumor tissue. Cell Cycle. 2011; 10:4047-64. doi: 10.4161/cc.10.23.18151 PMID: 22134189
46. Ricart KC, Bolisetty S, Johnson MS, Perez J, Agarwal A, Murphy MP, et al. The permissive role of mitochondria in the induction of haem oxygenase-1 in endothelial cells. Biochem J. 2009; 419:427-36. doi: 10.1042/BJ20081350 PMID: 19161347
47. Ross MF, Da Ros T, Blaikie FH, Prime TA, Porteous CM, Severina II, et al. Accumulation of lipophilic dications by mitochondria and cells. Biochem J. 2006; 400:199-208. PMID: 16948637
48. Marley K, Mooney DT, Clark-Scannell G, Tong TT, Watson J, Hagen TM, et al. Mass tagging approach for mitochondrial thiol proteins. J Proteome Res. 2005; 4:1403-12. PMID: 16083293
49. Diers AR, Dranka BP, Ricart KC, Oh JY, Johnson MS, Zhou F, et al. Modulation of mammary cancer cell migration by 15-deoxy-delta(12,14)-prostaglandin J(2): implications for anti-metastatic therapy. Biochem J. 2010; 430:69-78. doi: 10.1042/BJ20091193 PMID: 20536428
50. Porporato PE, Payen VL, Perez-Escuredo J, De Saedeleer CJ, Danhier P, Copetti T, et al. A mitochondrial switch promotes tumor metastasis. Cell Rep. 2014; 8:754-66. doi: 10.1016/j.celrep.2014.06.043 PMID: 25066121
51. Zhao J, Zhang J, Yu M, Xie Y, Huang Y, Wolff DW, et al. Mitochondrial dynamics regulates migration and invasion of breast cancer cells. Oncogene. 2013; 32:4814-24. doi: 10.1038/onc.2012.494 PMID: 23128392
52. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol. 2004; 287:C817-33. PMID: 15355853
53. Kowaltowski AJ, Seetharaman S, Paucek P, Garlid KD. Bioenergetic consequences of opening the ATP-sensitive K(+) channel of heart mitochondria. Am J Physiol Heart Circ Physiol. 2001; 280:H649-57. PMID: 11158963
54. Costa AD, Jakob R, Costa CL, Andrukhiv K, West IC, Garlid KD. The mechanism by which the mitochondrial ATP-sensitive K+ channel opening and H2O2 inhibit the mitochondrial permeability transition. J Biol Chem. 2006; 281:20801-8. PMID: 16720572
55. Wall SB, Smith MR, Ricart K, Zhou F, Vayalil PK, Oh JY, et al. Detection of electrophile-sensitive proteins. Biochim Biophys Acta. 2014; 1840:913-22. doi: 10.1016/j.bbagen.2013.09.003 PMID: 24021887
56. Costa AD, Garlid KD. Intramitochondrial signaling: interactions among mitoKATP, PKCepsilon, ROS, and MPT. Am J Physiol Heart Circ Physiol. 2008; 295:H874-82. doi: 10.1152/ajpheart.01189.2007 PMID: 18586884