Caveolin-1 regulates cancer cell metabolism via scavenging Nrf2 and suppressing MnSOD-driven glycolysis

Oncotarget

Volumn 7, Issue 1, 2016, Pages 308-322

  Hart, Peter C ^a   Ratti, Bianca A ^a,c   Mao, Mao ^a   Ansenberger Fricano, Kristine ^a   Shajahan Haq, Ayesha N ^b   Tyner, Angela L ^a   Minshall, Richard D ^a   Bonini, Marcelo G ^a,c  

^a UNIVERSITY OF ILLINOIS   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c STATE UNIVERSITY OF MARINGÁ   (Brazil)

Author keywords

Breast cancer; Caveolin 1; MnSOD; Nrf2; Tumor progression

Indexed keywords

CAVEOLIN 1; HYDROGEN PEROXIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MANGANESE SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2; KEAP1 PROTEIN, HUMAN; KELCH LIKE ECH ASSOCIATED PROTEIN 1; NFE2L2 PROTEIN, HUMAN; PROTEIN BINDING; SIGNAL PEPTIDE; SUPEROXIDE DISMUTASE;

ARTICLE; BREAST CANCER; BREAST CARCINOMA; CANCER CELL; CANCER PROGNOSIS; CELL METABOLISM; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; GLYCOLYSIS; HUMAN; HUMAN TISSUE; MALIGNANT TRANSFORMATION; MCF-7 CELL LINE; PROTEIN EXPRESSION; SURVIVAL RATE; UPREGULATION; ANIMAL; BREAST TUMOR; CELL LINE; CONFOCAL MICROSCOPY; EXPERIMENTAL MAMMARY NEOPLASM; GENETICS; METABOLISM; MOUSE; PATHOLOGY; PROGNOSIS; RNA INTERFERENCE; SURVIVAL ANALYSIS; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BREAST NEOPLASMS; CAVEOLIN 1; CELL LINE; GLYCOLYSIS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KELCH-LIKE ECH-ASSOCIATED PROTEIN 1; MAMMARY NEOPLASMS, ANIMAL; MCF-7 CELLS; MICE; MICROSCOPY, CONFOCAL; NF-E2-RELATED FACTOR 2; PROGNOSIS; PROTEIN BINDING; RNA INTERFERENCE; SUPEROXIDE DISMUTASE; SURVIVAL ANALYSIS;

EID: 84997344872     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/ONCOTARGET.5687     Document Type: Article

References (40)

1. Lisanti MP, Scherer PE, Vidugiriene J, Tang Z, Hermanowski-Vosatka A, Tu YH, Cook RF and Sargiacomo M. Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease. J Cell Biol. 1994; 126:111-126
2. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR and Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell. 1992; 68:673-682
3. Lisanti MP, Scherer PE, Tang Z and Sargiacomo M. Caveolae, caveolin and caveolin-rich membrane domains: a signalling hypothesis. Trends Cell Biol. 1994; 4:231-235
4. Schnitzer JE, Liu J and Oh P. Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSF, SNAP, annexins, and GTPases. J Biol Chem. 1995; 270:14399-14404
5. Sargiacomo M, Scherer PE, Tang Z, Kubler E, Song KS, Sanders MC and Lisanti MP. Oligomeric structure of caveolin: implications for caveolae membrane organization. Proc Natl Acad Sci U S A. 1995; 92:9407-9411
6. Liu J, Oh P, Horner T, Rogers RA and Schnitzer JE. Organized endothelial cell surface signal transduction in caveolae distinct from glycosylphosphatidylinositol-anchored protein microdomains. J Biol Chem. 1997; 272:7211-7222
7. Lu ML, Schneider MC, Zheng Y, Zhang X and Richie JP. Caveolin-1 interacts with androgen receptor. A positive modulator of androgen receptor mediated transactivation. J Biol Chem. 2001; 276:13442-13451
8. Volonte D, Liu Z, Musille PM, Stoppani E, Wakabayashi N, Di YP, Lisanti MP, Kensler TW and Galbiati F. Inhibition of nuclear factor-erythroid 2-related factor (Nrf2) by caveolin-1 promotes stress-induced premature senescence. Molecular biology of the cell. 2013; 24:1852-1862
9. Schlegel A, Wang C, Katzenellenbogen BS, Pestell RG and Lisanti MP. Caveolin-1 potentiates estrogen receptor alpha (ERalpha) signaling. caveolin-1 drives ligand-independent nuclear translocation and activation of ERalpha. J Biol Chem. 1999; 274:33551-33556
10. Brouet A, Sonveaux P, Dessy C, Moniotte S, Balligand JL and Feron O. Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins. Circ Res. 2001; 89:866-873
11. Mao M, Varadarajan S, Fukai T, Bakhshi FR, Chernaya O, Dudley SC, Jr., Minshall RD and Bonini MG. Nitroglycerin tolerance in caveolin-1 deficient mice. PLoS One. 2014; 9:e104101
12. Lim EJ, Smart EJ, Toborek M and Hennig B. The role of caveolin-1 in PCB77-induced eNOS phosphorylation in human-derived endothelial cells. Am J Physiol Heart Circ Physiol. 2007; 293:H3340-3347
13. Majkova Z, Toborek M and Hennig B. The role of caveolae in endothelial cell dysfunction with a focus on nutrition and environmental toxicants. J Cell Mol Med. 2010; 14:2359-2370
14. Isshiki M, Ando J, Yamamoto K, Fujita T, Ying Y and Anderson RG. Sites of Ca(2+) wave initiation move with caveolae to the trailing edge of migrating cells. J Cell Sci. 2002; 115:475-484
15. Grande-Garcia A, Echarri A, de Rooij J, Alderson NB, Waterman-Storer CM, Valdivielso JM and del Pozo MA. Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J Cell Biol. 2007; 177:683-694
16. Bakhshi FR, Mao M, Shajahan AN, Piegeler T, Chen Z, Chernaya O, Sharma T, Elliott WM, Szulcek R, Bogaard HJ, Comhair S, Erzurum S, van Nieuw Amerongen GP, et al. Nitrosation-dependent caveolin 1 phosphorylation, ubiquitination, and degradation and its association with idiopathic pulmonary arterial hypertension. Pulm Circ. 2013; 3:816-830
17. Yang KC, Rutledge CA, Mao M, Bakhshi FR, Xie A, Liu H, Bonini MG, Patel HH, Minshall RD and Dudley SC, Jr. Caveolin-1 modulates cardiac gap junction homeostasis and arrhythmogenecity by regulating cSrc tyrosine kinase. Circ Arrhythm Electrophysiol. 2014; 7:701-710
18. Bitar MS, Abdel-Halim SM and Al-Mulla F. Caveolin-1/PTRF upregulation constitutes a mechanism for mediating p53-induced cellular senescence: implications for evidencebased therapy of delayed wound healing in diabetes. Am J Physiol Endocrinol Metab. 2013; 305:E951-963
19. Pavlides S, Tsirigos A, Vera I, Flomenberg N, Frank PG, Casimiro MC, Wang C, Fortina P, Addya S, Pestell RG, Martinez-Outschoorn UE, Sotgia F and Lisanti MP. Loss of stromal caveolin-1 leads to oxidative stress, mimics hypoxia and drives inflammation in the tumor microenvironment, conferring the "reverse Warburg effect": a transcriptional informatics analysis with validation. Cell Cycle. 2010; 9:2201-2219
20. Chanvorachote P and Chunhacha P. Caveolin-1 regulates endothelial adhesion of lung cancer cells via reactive oxygen species-dependent mechanism. PLoS One. 2013; 8:e57466
21. Simpkins SA, Hanby AM, Holliday DL and Speirs V. Clinical and functional significance of loss of caveolin-1 expression in breast cancer-associated fibroblasts. J Pathol. 2012; 227:490-498
22. Pavlides S, Whitaker-Menezes D, Castello-Cros R, Flomenberg N, Witkiewicz AK, Frank PG, Casimiro MC, Wang C, Fortina P, Addya S, Pestell RG, Martinez-Outschoorn UE, Sotgia F, et al. The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell Cycle. 2009; 8:3984-4001
23. Cerezo A, Guadamillas MC, Goetz JG, Sanchez-Perales S, Klein E, Assoian RK and del Pozo MA. The absence of caveolin-1 increases proliferation and anchorage-independent growth by a Rac-dependent, Erk-independent mechanism. Mol Cell Biol. 2009; 29:5046-5059
24. Hulit J, Bash T, Fu M, Galbiati F, Albanese C, Sage DR, Schlegel A, Zhurinsky J, Shtutman M, Ben-Ze'ev A, Lisanti MP and Pestell RG. The cyclin D1 gene is transcriptionally repressed by caveolin-1. J Biol Chem. 2000; 275:21203-21209
25. Burgermeister E, Friedrich T, Hitkova I, Regel I, Einwachter H, Zimmermann W, Rocken C, Perren A, Wright MB, Schmid RM, Seger R and Ebert MP. The Ras inhibitors caveolin-1 and docking protein 1 activate peroxisome proliferator-activated receptor gamma through spatial relocalization at helix 7 of its ligand-binding domain. Mol Cell Biol. 2011; 31:3497-3510
26. Hart PC, Mao, M., Abreu, A.L., Ansenberger-Fricano, K., Ekou, D.N., Ganini, D., Kajdacsy-Balla, A., Diamond, A.M., Minshall, R.D., Consolaro, M.E., Santos, J.H., Bonini, M.G. MnSOD upregulation sustains the Warburg effect via mitochondrial ROS and AMPK-dependent signalling in cancer. Nat Commun. 2015; 6:6053
27. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A. 2001; 98:10869-10874
28. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, Speed D, Lynch AG, Samarajiwa S, Yuan Y, Graf S, Ha G, Haffari G, et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature. 2012; 486:346-352
29. Kao KJ, Chang KM, Hsu HC and Huang AT. Correlation of microarray-based breast cancer molecular subtypes and clinical outcomes: implications for treatment optimization. BMC Cancer. 2011; 11:143
30. Li W, Liu H, Zhou JS, Cao JF, Zhou XB, Choi AM, Chen ZH and Shen HH. Caveolin-1 inhibits expression of antioxidant enzymes through direct interaction with nuclear erythroid 2 p45-related factor-2 (Nrf2). The Journal of biological chemistry. 2012; 287:20922-20930
31. Kansanen E, Kuosmanen SM, Leinonen H and Levonen AL. The Keap1-Nrf2 pathway: Mechanisms of activation and dysregulation in cancer. Redox Biol. 2013; 1:45-49
32. Iliopoulos D, Hirsch HA and Struhl K. An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell. 2009; 139:693-706
33. Peng M, Ball-Kell SM, Franks RR, Xie H and Tyner AL. Protein tyrosine kinase 6 regulates mammary gland tumorigenesis in mouse models. Oncogenesis. 2013; 2:e81
34. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD and Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999; 13:76-86
35. Dhakshinamoorthy S and Jaiswal AK. Functional characterization and role of INrf2 in antioxidant response element-mediated expression and antioxidant induction of NAD(P)H:quinone oxidoreductase1 gene. Oncogene. 2001; 20:3906-3917
36. Fourquet S, Guerois R, Biard D and Toledano MB. Activation of NRF2 by nitrosative agents and H2O2 involves KEAP1 disulfide formation. J Biol Chem. 2010; 285:8463-8471
37. Shajahan AN, Dobbin ZC, Hickman FE, Dakshanamurthy S and Clarke R. Tyrosine-phosphorylated caveolin-1 (Tyr-14) increases sensitivity to paclitaxel by inhibiting BCL2 and BCLxL proteins via c-Jun N-terminal kinase (JNK). J Biol Chem. 2012; 287:17682-17692
38. Hirsch HA, Iliopoulos D, Joshi A, Zhang Y, Jaeger SA, Bulyk M, Tsichlis PN, Shirley Liu X and Struhl K. A transcriptional signature and common gene networks link cancer with lipid metabolism and diverse human diseases. Cancer Cell. 2010; 17:348-361
39. Rodriguez AM, Carrico PM, Mazurkiewicz JE and Melendez JA. Mitochondrial or cytosolic catalase reverses the MnSOD-dependent inhibition of proliferation by enhancing respiratory chain activity, net ATP production, and decreasing the steady state levels of H(2)O(2). Free Radic Biol Med. 2000; 29:801-813
40. Burgess A, Vigneron S, Brioudes E, Labbe JC, Lorca T and Castro A. Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/PP2A balance. Proc Natl Acad Sci U S A. 2010; 107:12564-12569