Is Reliance on Mitochondrial Respiration a "Chink in the Armor" of Therapy-Resistant Cancer?

Cancer Cell

Volumn 26, Issue 6, 2014, Pages 788-795

  Wolf, Dieter A ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 DINITROPHENOL; ANTIMYCIN A1; ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; OLIGOMYCIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PHENFORMIN; REACTIVE OXYGEN METABOLITE; ROTENONE; THENOYLTRIFLUOROACETONE; PPARGC1A PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

CANCER CELL; CANCER PATIENT; CANCER RESISTANCE; CELL CYCLE; CELL ENERGY; CHEMOSENSITIVITY; DRUG MECHANISM; HUMAN; LYMPHOMA; MELANOMA; MITOCHONDRIAL RESPIRATION; OXIDATIVE PHOSPHORYLATION; REVIEW; SENESCENCE; TREATMENT RESPONSE; UPREGULATION; ANIMAL; DRUG EFFECTS; DRUG RESISTANCE; METABOLISM; MITOCHONDRION; NEOPLASMS; OXIDATIVE STRESS;

ANIMALS; ANTINEOPLASTIC AGENTS; DRUG RESISTANCE, NEOPLASM; HUMANS; MITOCHONDRIA; NEOPLASMS; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; TRANSCRIPTION FACTORS;

EID: 84919489013     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2014.10.001     Document Type: Review

References (53)

1. Azvolinsky A. Repurposing to fight cancer: the metformin-prostate cancer connection. J.Natl. Cancer Inst. 2014, 106:dju030.
2. Brewer J.W., Hendershot L.M., Sherr C.J., Diehl J.A. Mammalian unfolded protein response inhibits cyclin D1 translation and cell-cycle progression. Proc. Natl. Acad. Sci. USA 1999, 96:8505-8510.
3. Cao S.S., Kaufman R.J. Unfolded protein response. Curr. Biol. 2012, 22:R622-R626.
4. Chien Y., Scuoppo C., Wang X., Fang X., Balgley B., Bolden J.E., Premsrirut P., Luo W., Chicas A., Lee C.S., et al. Control of the senescence-associated secretory phenotype by NF-κB promotes senescence and enhances chemosensitivity. Genes Dev. 2011, 25:2125-2136.
5. Choi W.-S., Palmiter R.D., Xia Z. Loss of mitochondrial complex I activity potentiates dopamine neuron death induced by microtubule dysfunction in a Parkinson's disease model. J.Cell. Biol. 2011, 192:873-882.
6. Coppé J.-P., Desprez P.-Y., Krtolica A., Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu. Rev. Pathol. 2010, 5:99-118.
7. Corazao-Rozas P., Guerreschi P., Jendoubi M., André F., Jonneaux A., Scalbert C., Garçon G., Malet-Martino M., Balayssac S., Rocchi S., et al. Mitochondrial oxidative stress is the Achille's heel of melanoma cells resistant to Braf-mutant inhibitor. Oncotarget 2013, 4:1986-1998.
8. Dean M., Fojo T., Bates S. Tumour stem cells and drug resistance. Nat. Rev. Cancer 2005, 5:275-284.
9. Dhomen N., Reis-Filho J.S., da Rocha Dias S., Hayward R., Savage K., Delmas V., Larue L., Pritchard C., Marais R. Oncogenic Braf induces melanocyte senescence and melanoma in mice. Cancer Cell 2009, 15:294-303.
10. Dörr J.R., Yu Y., Milanovic M., Beuster G., Zasada C., Däbritz J.H.M., Lisec J., Lenze D., Gerhardt A., Schleicher K., et al. Synthetic lethal metabolic targeting of cellular senescence in cancer therapy. Nature 2013, 501:421-425.
11. Ewald J.A., Desotelle J.A., Wilding G., Jarrard D.F. Therapy-induced senescence in cancer. J.Natl. Cancer Inst. 2010, 102:1536-1546.
12. Fang M., Shen Z., Huang S., Zhao L., Chen S., Mak T.W., Wang X. The ER UDPase ENTPD5 promotes protein N-glycosylation, the Warburg effect, and proliferation in the PTEN pathway. Cell 2010, 143:711-724.
13. Freund A., Patil C.K., Campisi J. p38MAPK is a novel DNA damage response-independent regulator of the senescence-associated secretory phenotype. EMBO J. 2011, 30:1536-1548.
14. Fulda S. Regulation of apoptosis pathways in cancer stem cells. Cancer Lett. 2013, 338:168-173.
15. Garraway L.A., Widlund H.R., Rubin M.A., Getz G., Berger A.J., Ramaswamy S., Beroukhim R., Milner D.A., Granter S.R., Du J., et al. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 2005, 436:117-122.
16. Gupta P.B., Fillmore C.M., Jiang G., Shapira S.D., Tao K., Kuperwasser C., Lander E.S. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011, 146:633-644.
17. Han J., Back S.H., Hur J., Lin Y.-H., Gildersleeve R., Shan J., Yuan C.L., Krokowski D., Wang S., Hatzoglou M., et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat. Cell Biol. 2013, 15:481-490.
18. Haq R., Shoag J., Andreu-Perez P., Yokoyama S., Edelman H., Rowe G.C., Frederick D.T., Hurley A.D., Nellore A., Kung A.L., et al. Oncogenic BRAF regulates oxidative metabolism via PGC1α and MITF. Cancer Cell 2013, 23:302-315.
19. Hirsch H.A., Iliopoulos D., Tsichlis P.N., Struhl K. Metformin selectively targets cancer stem cells, and acts together with chemotherapy to block tumor growth and prolong remission. Cancer Res. 2009, 69:7507-7511.
20. Iliopoulos D., Hirsch H.A., Struhl K. Metformin decreases the dose of chemotherapy for prolonging tumor remission in mouse xenografts involving multiple cancer cell types. Cancer Res. 2011, 71:3196-3201.
21. Kim I., Xu W., Reed J.C. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov. 2008, 7:1013-1030.
22. Kong Q., Beel J.A., Lillehei K.O. A threshold concept for cancer therapy. Med. Hypotheses 2000, 55:29-35.
23. Konieczkowski D.J., Johannessen C.M., Abudayyeh O., Kim J.W., Cooper Z.A., Piris A., Frederick D.T., Barzily-Rokni M., Straussman R., Haq R., et al. A melanoma cell state distinction influences sensitivity to MAPK pathway inhibitors. Cancer Discov. 2014, 4:816-827.
24. Lim J.-H., Luo C., Vazquez F., Puigserver P. Targeting mitochondrial oxidative metabolism in melanoma causes metabolic compensation through glucose and glutamine utilization. Cancer Res. 2014, 74:3535-3545.
25. Lunt S.Y., Vander Heiden M.G. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu. Rev. Cell Dev. Biol. 2011, 27:441-464.
26. Luo J., Solimini N.L., Elledge S.J. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 2009, 136:823-837.
27. Madesh M., Hajnóczky G. VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J.Cell Biol. 2001, 155:1003-1015.
28. Malhotra J.D., Kaufman R.J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword?. Antioxid. Redox Signal. 2007, 9:2277-2293.
29. O'Day S.J., Eggermont A.M.M., Chiarion-Sileni V., Kefford R., Grob J.J., Mortier L., Robert C., Schachter J., Testori A., Mackiewicz J., et al. Final results of phase III SYMMETRY study: randomized, double-blind trial of elesclomol plus paclitaxel versus paclitaxel alone as treatment for chemotherapy-naive patients with advanced melanoma. J.Clin. Oncol. 2013, 31:1211-1218.
30. Rico-Bautista E., Zhu W., Kitada S., Ganapathy S., Lau E., Krajewski S., Ramirez J., Bush J.A., Yuan Z., Wolf D.A. Small molecule-induced mitochondrial disruption directs prostate cancer inhibition via UPR signaling. Oncotarget 2013, 4:1212-1229.
31. Roberson R.S., Kussick S.J., Vallieres E., Chen S.-Y.J., Wu D.Y. Escape from therapy-induced accelerated cellular senescence in p53-null lung cancer cells and in human lung cancers. Cancer Res. 2005, 65:2795-2803.
32. Roesch A., Becker B., Meyer S., Wild P., Hafner C., Landthaler M., Vogt T. Retinoblastoma-binding protein 2-homolog 1: a retinoblastoma-binding protein downregulated in malignant melanomas. Mod. Pathol. 2005, 18:1249-1257.
33. Roesch A., Fukunaga-Kalabis M., Schmidt E.C., Zabierowski S.E., Brafford P.A., Vultur A., Basu D., Gimotty P., Vogt T., Herlyn M. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 2010, 141:583-594.
34. Roesch A., Vultur A., Bogeski I., Wang H., Zimmermann K.M., Speicher D., Körbel C., Laschke M.W., Gimotty P.A., Philipp S.E., et al. Overcoming intrinsic multidrug resistance in melanoma by blocking the mitochondrial respiratory chain of slow-cycling JARID1B(high) cells. Cancer Cell 2013, 23:811-825.
35. Rohlena J., Dong L.-F., Ralph S.J., Neuzil J. Anticancer drugs targeting the mitochondrial electron transport chain. Antioxid. Redox Signal. 2011, 15:2951-2974.
36. Ronai Z. The masters talk: the PGC-1α-MITF axis as a melanoma energizer. Pigment Cell Melanoma Res 2013, 26:294-295.
37. Scarpulla R.C., Vega R.B., Kelly D.P. Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol. Metab. 2012, 23:459-466.
38. Schmitt C.A., Fridman J.S., Yang M., Lee S., Baranov E., Hoffman R.M., Lowe S.W. A senescence program controlled by p53 and p16INK4a contributes to the outcome of cancer therapy. Cell 2002, 109:335-346.
39. Scholnick P., Lang D., Racker E. Regulatory mechanisms in carbohydrate metabolism. IX. Stimulation of aerobic glycolysis by energy-linked ion transport and inhibition by dextran sulfate. J.Biol. Chem. 1973, 248:5175-5182.
40. Schulze A., Harris A.L. How cancer metabolism is tuned for proliferation and vulnerable to disruption. Nature 2012, 491:364-373.
41. Sundberg T.B., Swenson L., Wahl D.R., Opipari A.W., Glick G.D. Apoptotic signaling activated by modulation of the F0F1-ATPase: Implications for selective killing of autoimmune lymphocytes. J Pharmacol. Exp. Ther. 2009, 331:437-444.
42. Tabas I., Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 2011, 13:184-190.
43. Toogood P.L. Mitochondrial drugs. Curr. Opin. Chem. Biol. 2008, 12:457-463.
44. Trachootham D., Alexandre J., Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach?. Nat. Rev. Drug Discov. 2009, 8:579-591.
45. Vander Heiden M.G., Locasale J.W., Swanson K.D., Sharfi H., Heffron G.J., Amador-Noguez D., Christofk H.R., Wagner G., Rabinowitz J.D., Asara J.M., Cantley L.C. Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science 2010, 329:1492-1499.
46. Vazquez F., Lim J.-H., Chim H., Bhalla K., Girnun G., Pierce K., Clish C.B., Granter S.R., Widlund H.R., Spiegelman B.M., Puigserver P. PGC1α expression defines a subset of human melanoma tumors with increased mitochondrial capacity and resistance to oxidative stress. Cancer Cell 2013, 23:287-301.
47. Villeneuve N.F., Lau A., Zhang D.D. Regulation of the Nrf2-Keap1 antioxidant response by the ubiquitin proteasome system: an insight into cullin-ring ubiquitin ligases. Antioxid. Redox Signal. 2010, 13:1699-1712.
48. Walter P., Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334:1081-1086.
49. Ward P.S., Thompson C.B. Metabolic reprogramming: a cancer hallmark even Warburg did not anticipate. Cancer Cell 2012, 21:297-308.
50. Watabe M., Nakaki T. ATP depletion does not account for apoptosis induced by inhibition of mitochondrial electron transport chain in human dopaminergic cells. Neuropharmacology 2007, 52:536-541.
51. Watson J. Oxidants, antioxidants and the current incurability of metastatic cancers. Open Biol. 2013, 3:120144.
52. Wondrak G.T. Redox-directed cancer therapeutics: molecular mechanisms and opportunities. Antioxid. Redox Signal. 2009, 11:3013-3069.
53. Zucker S.N., Fink E.E., Bagati A., Mannava S., Bianchi-Smiraglia A., Bogner P.N., Wawrzyniak J.A., Foley C., Leonova K.I., Grimm M.J., et al. Nrf2 amplifies oxidative stress via induction of Klf9. Mol. Cell 2014, 53:916-928.