Caveolin-1 in the regulation of cell metabolism: A cancer perspective

Molecular Cancer

Volumn 15, Issue 1, 2016, Pages

  Nwosu, Zeribe Chike ^a   Ebert, Matthias Philip ^a   Dooley, Steven ^a   Meyer, Christoph ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Autophagy; CAV1; Fatty acid metabolism; Glutaminolysis; Glycolysis; Metabolic targets; Mitochondrion

Indexed keywords

ACETYL COENZYME A ACYLTRANSFERASE; ADIPOCYTOKINE; ALPHA ENOLASE; CARNITINE PALMITOYLTRANSFERASE; CAVEOLIN 1; FATTY ACID SYNTHASE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUCOSE 6 PHOSPHATASE; GLUCOSE TRANSPORTER 3; GLUCOSE TRANSPORTER 4; HEXOKINASE; HEXOKINASE 2; HYPOXIA INDUCIBLE FACTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; PHOSPHOGLYCERATE KINASE; PHOSPHOGLYCERATE KINASE 1; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN C RECEPTOR; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; FATTY ACID; GLUTAMINE;

AMINO ACID METABOLISM; ANCHORAGE INDEPENDENT GROWTH; APOPTOSIS; AUTOPHAGY; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER SURVIVAL; CELL METABOLISM; CELLULAR DISTRIBUTION; COLON CANCER; DOWN REGULATION; ENZYME ACTIVITY; FATTY ACID METABOLISM; GENE SILENCING; GLUCOSE TRANSPORT; GLUTAMINOLYSIS; GLYCOLYSIS; HUMAN; INSULIN RESISTANCE; LIPID METABOLISM; METABOLIC REGULATION; MITOCHONDRIAL BIOGENESIS; NON SMALL CELL LUNG CANCER; NONHUMAN; OBESITY; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; UPREGULATION; ANIMAL; CHEMISTRY; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRION; NEOPLASM;

ANIMALS; AUTOPHAGY; CAVEOLIN 1; ENERGY METABOLISM; FATTY ACIDS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUTAMINE; GLYCOLYSIS; HUMANS; INSULIN RESISTANCE; METABOLIC NETWORKS AND PATHWAYS; MITOCHONDRIA; NEOPLASMS; OBESITY;

EID: 84997355381     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/s12943-016-0558-7     Document Type: Review

References (115)

1. Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer. 2011;11:85-95.
2. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-74.
3. Warburg O. On the origin of cancer cells. Science. 1956;123(3191):309-14.
4. Hsu PP, Sabatini DM. Cancer cell metabolism: Warburg and beyond. Cell. 2008;134(5):703-7.
5. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324(5930):1029-33.
6. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M, Wehrli S, Thompson CB. Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci U S A. 2007;104(49):19345-50.
7. Samudio I, Harmancey R, Fiegl M, Kantarjian H, Konopleva M, Korchin B, et al. Pharmacologic inhibition of fatty acid oxidation sensitizes human leukemia cells to apoptosis induction. J Clin Invest. 2010;120(1):142-56.
8. Sun RC, Denko NC. Hypoxic regulation of glutamine metabolism through HIF1 and SIAH2 supports lipid synthesis that is necessary for tumor growth. Cell Metab. 2014;19(2):285-92.
9. Maddocks OD, Berkers CR, Mason SM, Zheng L, Blyth K, Gottlieb E, Vousden KH. Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells. Nature. 2013;493(7433):542-6.
10. Kamphorst JJ, Nofal M, Commisso C, Hackett SR, Lu W, Grabocka E, et al. Human pancreatic cancer tumors are nutrient poor and tumor cells actively scavenge extracellular protein. Cancer Res. 2015;75(3):544-53.
11. Sousa CM, Biancur DE, Wang X, Halbrook CJ, Sherman MH, Zhang L, et al. Pancreatic stellate cells support tumour metabolism through autophagic alanine secretion. Nature. 2016;536(7617):479-83.
12. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, Bartrons R, et al. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell. 2006;126(1):107-20.
13. Lu X, Kang Y. Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin Cancer Res. 2010;16(24):5928-35.
14. Dang CV. MYC, metabolism, cell growth, and tumorigenesis. Cold Spring Harb Perspect Med. 2013;3(8):a014217.
15. Weljie AM, Jirik FR. Hypoxia-induced metabolic shifts in cancer cells: moving beyond the Warburg effect. Int J Biochem Cell Biol. 2011;43(7):981-9.
16. Bieging KT, Mello SS, Attardi LD. Unravelling mechanisms of p53-mediated tumour suppression. Nat Rev Cancer. 2014;14(5):359-70.
17. Zhao Y, Butler EB, Tan M. Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis. 2013;4:e532.
18. Martinez-Outschoorn UE, Prisco M, Ertel A, Tsirigos A, Lin Z, Pavlides S, et al. Ketones and lactate increase cancer cell "stemness," driving recurrence, metastasis and poor clinical outcome in breast cancer: achieving personalized medicine via Metabolo-Genomics. Cell Cycle. 2011;10(8):1271-86.
19. Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim SH, et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of α-ketoglutarate-dependent dioxygenases. Cancer Cell. 2011;19(1):17-30.
20. Nowicki S, Gottlieb E. Oncometabolites: tailoring our genes. FEBS J. 2015;282(15):2796-805.
21. Cairns RA, Mak TW. Oncogenic isocitrate dehydrogenase mutations: mechanisms, models, and clinical opportunities. Cancer Discov. 2013;3(7):730-41.
22. Sullivan LB, Martinez-Garcia E, Nguyen H, Mullen AR, Dufour E, Sudarshan S, et al. The proto-oncometabolite fumarate binds glutathione to amplify ROS-dependent signaling. Mol Cell. 2013;51(2):236-48.
23. Gupta R, Toufaily C, Annabi B. Caveolin and cavin family members: dual roles in cancer. Biochimie. 2014;107(Pt B):188-202.
24. Meyer C, Liu Y, Dooley S. Caveolin and TGF-β entanglements. J Cell Physiol. 2013;228(11):2097-102.
25. Liu P, Rudick M, Anderson RG. Multiple functions of caveolin-1. J Biol Chem. 2002;277(44):41295-8.
26. Parton RG, del Pozo MA. Caveolae as plasma membrane sensors, protectors and organizers. Nat Rev Mol Cell Biol. 2013;14(2):98-112.
27. Razani B, Combs TP, Wang XB, Frank PG, Park DS, Russell RG, et al. Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J Biol Chem. 2002;277(10):8635-47.
28. Navarro A, Anand-Apte B, Parat MO. A role for caveolae in cell migration. FASEB J. 2004;18(15):1801-11.
29. Burgermeister E, Liscovitch M, Röcken C, Schmid RM, Ebert MP. Caveats of caveolin-1 in cancer progression. Cancer Lett. 2008;268(2):187-201.
30. Patani N, Martin LA, Reis-Filho JS, Dowsett M. The role of caveolin-1 in human breast cancer. Breast Cancer Res Treat. 2012;131(1):1-15.
31. Meyer C, Liu Y, Kaul A, Peipe I, Dooley S. Caveolin-1 abrogates TGF-β mediated hepatocyte apoptosis. Cell Death Dis. 2013;4:e466.
32. Nunez-Wehinger S, Ortiz RJ, Diaz N, Diaz J, Lobos-Gonzalez L, Quest AF. Caveolin-1 in cell migration and metastasis. Curr Mol Med. 2014;14(2):255-74.
33. Wang Z, Wang N, Liu P, Peng F, Tang H, Chen Q, et al. Caveolin-1, a stress-related oncotarget, in drug resistance. Oncotarget. 2015;6(35):37135-50.
34. Savage K, Lambros MB, Robertson D, Jones RL, Jones C, Mackay A, et al. Caveolin 1 is overexpressed and amplified in a subset of basal-like and metaplastic breast carcinomas: a morphologic, ultrastructural, immunohistochemical, and in situ hybridization analysis. Clin Cancer Res. 2007;13(1):90-101.
35. Goetz JG, Lajoie P, Wiseman SM, Nabi IR. Caveolin-1 in tumor progression: the good, the bad and the ugly. Cancer Metastasis Rev. 2008;27(4):715-35.
36. Ho CC, Kuo SH, Huang PH, Huang HY, Yang CH, Yang PC. Caveolin-1 expression is significantly associated with drug resistance and poor prognosis in advanced non-small cell lung cancer patients treated with gemcitabine-based chemotherapy. Lung Cancer. 2008;59(1):105-10.
37. Tang Y, Zeng X, He F, Liao Y, Qian N, Toi M. Caveolin-1 is related to invasion, survival, and poor prognosis in hepatocellular cancer. Med Oncol. 2012;29(2):977-84.
38. Tse EY, Ko FC, Tung EK, Chan LK, Lee TK, Ngan ES, Man K, Wong AS, Ng IO, Yam JW. Caveolin-1 overexpression is associated with hepatocellular carcinoma tumourigenesis and metastasis. J Pathol. 2012;226(4):645-53.
39. Faggi F, Chiarelli N, Colombi M, Mitola S, Ronca R, Madaro L, et al. Cavin-1 and Caveolin-1 are both required to support cell proliferation, migration and anchorage-independent cell growth in rhabdomyosarcoma. Lab Invest. 2015;95(6):585-602.
40. Carver LA, Schnitzer JE. Caveolae: mining little caves for new cancer targets. Nat Rev Cancer. 2003;3(8):571-81.
41. Pavlides S, Whitaker-Menezes D, Castello-Cros R, Flomenberg N, Witkiewicz AK, Frank PG, et al. The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell Cycle. 2009;8(23):3984-4001.
42. Yang SF, Yang JY, Huang CH, Wang SN, Lu CP, Tsai CJ, et al. Increased caveolin-1 expression associated with prolonged overall survival rate in hepatocellular carcinoma. Pathology. 2010;42(5):438-45.
43. Rimessi A, Marchi S, Patergnani S, Pinton P. H-Ras-driven tumoral maintenance is sustained through caveolin-1-dependent alterations in calcium signaling. Oncogene. 2014;33(18):2329-40.
44. Friedrich T, Richter B, Gaiser T, Weiss C, Janssen KP, Einwächter H, Schmid RM, Ebert MP, Burgermeister E. Deficiency of caveolin-1 in Apc(min/+) mice promotes colorectal tumorigenesis. Carcinogenesis. 2013;34(9):2109-18.
45. Sotgia F, Martinez-Outschoorn UE, Howell A, Pestell RG, Pavlides S, Lisanti MP. Caveolin-1 and cancer metabolism in the tumor microenvironment: markers, models, and mechanisms. Annu Rev Pathol. 2012;7:423-67.
46. Ng KL, Morais C, Bernard A, Saunders N, Samaratunga H, Gobe G, Wood S. A systematic review and meta-analysis of immunohistochemical biomarkers that differentiate chromophobe renal cell carcinoma from renal oncocytoma. J Clin Pathol. 2016;69:661-71.
47. Kawaraguchi Y, Horikawa YT, Murphy AN, Murray F, Miyanohara A, Ali SS, et al. Volatile anesthetics protect cancer cells against tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis via caveolins. Anesthesiology. 2011;115(3):499-508.
48. Ha TK, Her NG, Lee MG, Ryu BK, Lee JH, Han J, et al. Caveolin-1 increases aerobic glycolysis in colorectal cancers by stimulating HMGA1-mediated GLUT3 transcription. Cancer Res. 2012;72(16):4097-109.
49. Tahir SA, Yang G, Goltsov A, Song KD, Ren C, Wang J, et al. Caveolin-1-LRP6 signaling module stimulates aerobic glycolysis in prostate cancer. Cancer Res. 2013;73(6):1900-11.
50. Salani B, Maffioli S, Hamoudane M, Parodi A, Ravera S, Passalacqua M, et al. Caveolin-1 is essential for metformin inhibitory effect on IGF1 action in non-small-cell lung cancer cells. FASEB J. 2012;26(2):788-98.
51. Raikar LS, Vallejo J, Lloyd PG, Hardin CD. Overexpression of caveolin-1 results in increased plasma membrane targeting of glycolytic enzymes: the structural basis for a membrane associated metabolic compartment. J Cell Biochem. 2006;98(4):861-71.
52. Shiroto T, Romero N, Sugiyama T, Sartoretto JL, Kalwa H, Yan Z, et al. Caveolin-1 is a critical determinant of autophagy, metabolic switching, and oxidative stress in vascular endothelium. PLoS One. 2014;9(2):e87871.
53. Keith B, Johnson RS, Simon MC. HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer. 2011;12(1):9-22.
54. Wang Y, Roche O, Xu C, Moriyama EH, Heir P, Chung J, et al. Hypoxia promotes ligand-independent EGF receptor signaling via hypoxia-inducible factor-mediated upregulation of caveolin-1. Proc Natl Acad Sci U S A. 2012;109(13):4892-7.
55. Chiavarina B, Whitaker-Menezes D, Migneco G, Martinez-Outschoorn UE, Pavlides S, Howell A, et al. HIF1-alpha functions as a tumor promoter in cancer associated fibroblasts, and as a tumor suppressor in breast cancer cells: Autophagy drives compartment-specific oncogenesis. Cell Cycle. 2010;9(17):3534-51.
56. Hart PC, Ratti BA, Mao M, Ansenberger-Fricano K, Shajahan-Haq AN, Tyner AL, et al. Caveolin-1 regulates cancer cell metabolism via scavenging Nrf2 and suppressing MnSOD-driven glycolysis. Oncotarget. 2016;7(1):308-22.
57. Asterholm IW, Mundy DI, Weng J, Anderson RG, Scherer PE. Altered mitochondrial function and metabolic inflexibility associated with loss of caveolin-1. Cell Metab. 2012;15(2):171-85.
58. Fernández-Rojo MA, Restall C, Ferguson C, Martel N, Martin S, Bosch M, et al. Caveolin-1 orchestrates the balance between glucose and lipid-dependent energy metabolism: implications for liver regeneration. Hepatology. 2012;55(5):1574-84.
59. Chen Y-H, Lin W-W, Liu C-S, Hsu L-S, Lin Y-M, et al. Caveolin-1 Provides Palliation for Adverse Hepatic Reactions in Hypercholesterolemic Rabbits. PLoS One. 2014;9(1):e71862.
60. Niesman IR, Zemke N, Fridolfsson HN, Haushalter KJ, Levy K, Grove A, et al. Caveolin isoform switching as a molecular, structural, and metabolic regulator of microglia. Mol Cell Neurosci. 2013;56:283-97.
61. Fridolfsson HN, Kawaraguchi Y, Ali SS, Panneerselvam M, Niesman IR, Finley JC, et al. Mitochondria-localized caveolin in adaptation to cellular stress and injury. FASEB J. 2012;26(11):4637-49.
62. Bosch M, Marí M, Herms A, Fernández A, Fajardo A, Kassan A, et al. Caveolin-1 deficiency causes cholesterol-dependent mitochondrial dysfunction and apoptotic susceptibility. Curr Biol. 2011;21(8):681-6.
63. Hensley CT, Wasti AT, DeBerardinis RJ. Glutamine and cancer: cell biology, physiology, and clinical opportunities. J Clin Invest. 2013;123(9):3678-84.
64. Ko YH, Lin Z, Flomenberg N, Pestell RG, Howell A, Sotgia F, et al. 61: implications for preventing chemotherapy resistance. Cancer Biol Ther. 2011;12(12):1085-97.
65. Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T, et al. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature. 2009;458:762-5.
66. Timme TL, Goltsov A, Tahir S, Li L, Wang J, Ren C, Johnston RN, Thompson TC. Caveolin-1 is regulated by c-myc and suppresses c-myc-induced apoptosis. Oncogene. 2000;19(29):3256-65.
67. Park DS, Razani B, Lasorella A, Schreiber-Agus N, Pestell RG, Iavarone A, Lisanti MP. Evidence that Myc isoforms transcriptionally repress caveolin-1 gene expression via an INR-dependent mechanism. Biochemistry. 2001;40(11):3354-62.
68. Roy UK, Henkhaus RS, Ignatenko NA, Mora J, Fultz KE, Gerner EW. Wild-type APC regulates caveolin-1 expression in human colon adenocarcinoma cell lines via FOXO1a and C-myc. Mol Carcinog. 2008;47(12):947-55.
69. Yang G, Goltsov AA, Ren C, Kurosaka S, Edamura K, Logothetis R, et al. Caveolin-1 upregulation contributes to c-Myc-induced high-grade prostatic intraepithelial neoplasia and prostate cancer. Mol Cancer Res. 2012;10(2):218-29.
70. Balkrishna S, Bröer A, Kingsland A, Bröer S. Rapid downregulation of the rat glutamine transporter SNAT3 by a caveolin-dependent trafficking mechanism in Xenopus laevis oocytes. Am J Physiol Cell Physiol. 2010;299(5):C1047-57.
71. Ganapathy V, Thangaraju M, Prasad PD. Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol Ther. 2009;121(1):29-40.
72. McCracken AN, Edinger AL. Nutrient transporters: the Achilles' heel of anabolism. Trends Endocrinol Metab. 2013;24(4):200-8.
73. Menendez JA, Lupu R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat Rev Cancer. 2007;7(10):763-77.
74. Swierczynski J, Hebanowska A, Sledzinski T. Role of abnormal lipid metabolism in development, progression, diagnosis and therapy of pancreatic cancer. World J Gastroenterol. 2014;20(9):2279-303.
75. Zaytseva YY, Elliott VA, Rychahou P, Mustain WC, Kim JT, Valentino J, et al. Cancer cell-associated fatty acid synthase activates endothelial cells and promotes angiogenesis in colorectal cancer. Carcinogenesis. 2014;35(6):1341-51.
76. Di Vizio D, Adam RM, Kim J, Kim R, Sotgia F, Williams T, et al. Caveolin-1 interacts with a lipid raft-associated population of fatty acid synthase. Cell Cycle. 2008;7(14):2257-67.
77. Witkiewicz AK, Nguyen KH, Dasgupta A, Kennedy EP, Yeo CJ, Lisanti MP, Brody JR. Co-expression of fatty acid synthase and caveolin-1 in pancreatic ductal adenocarcinoma: implications for tumor progression and clinical outcome. Cell Cycle. 2008;7(19):3021-5.
78. Pandey V, Vijayakumar MV, Ajay AK, Malvi P, Bhat MK. Diet-induced obesity increases melanoma progression: involvement of Cav-1 and FASN. Int J Cancer. 2012;130(3):497-508.
79. Salaun C, Greaves J, Chamberlain LH. The intracellular dynamic of protein palmitoylation. J Cell Biol. 2010;191(7):1229-38.
80. Blaskovic S, Blanc M, van der Goot FG. What does S-palmitoylation do to membrane proteins? FEBS J. 2013;280(12):2766-74.
81. Fernández-Real JM, Catalán V, Moreno-Navarrete JM, Gómez-Ambrosi J, Ortega FJ, Rodriguez-Hermosa JI, et al. Study of caveolin-1 gene expression in whole adipose tissue and its subfractions and during differentiation of human adipocytes. Nutr Metab (Lond). 2010;7:20.
82. Fernández-Rojo MA, Gongora M, Fitzsimmons RL, Martel N, Martin SD, Nixon SJ, et al. Caveolin-1 is necessary for hepatic oxidative lipid metabolism: evidence for crosstalk between caveolin-1 and bile acid signaling. Cell Rep. 2013;4(2):238-47.
83. Kagawa Y, Yasumoto Y, Sharifi K, Ebrahimi M, Islam A, Miyazaki H, et al. Fatty acid-binding protein 7 regulates function of caveolae in astrocytes through expression of caveolin-1. Glia. 2015;63(5):780-94.
84. Azrad M, Turgeon C, Demark-Wahnefried W. Current evidence linking polyunsaturated fatty acids with cancer risk and progression. Front Oncol. 2013;3:224.
85. Vaughan VC, Hassing MR, Lewandowski PA. Marine polyunsaturated fatty acids and cancer therapy. Br J Cancer. 2013;108(3):486-92.
86. Lee EJ, Yun UJ, Koo KH, Sung JY, Shim J, Ye SK, et al. Down-regulation of lipid raft-associated onco-proteins via cholesterol-dependent lipid raft internalization in docosahexaenoic acid-induced apoptosis. Biochim Biophys Acta. 2014;1841(1):190-203.
87. Wehinger S, Ortiz R, Díaz MI, Aguirre A, Valenzuela M, Llanos P, et al. Phosphorylation of caveolin-1 on tyrosine-14 induced by ROS enhances palmitate-induced death of beta-pancreatic cells. Biochim Biophys Acta. 2015;1852(5):693-708.
88. Pei Z, Sun P, Huang P, Lal B, Laterra J, Watkins PA. Acyl-CoA synthetase VL3 knockdown inhibits human glioma cell proliferation and tumorigenicity. Cancer Res. 2009;69(24):9175-82.
89. Zaugg K, Yao Y, Reilly PT, Kannan K, Kiarash R, Mason J, et al. Carnitine palmitoyltransferase 1C promotes cell survival and tumor growth under conditions of metabolic stress. Genes Dev. 2011;25(10):1041-51.
90. Pacilli A, Calienni M, Margarucci S, D'Apolito M, Petillo O, Rocchi L, et al. Carnitine-acyltransferase system inhibition, cancer cell death, and prevention of myc-induced lymphomagenesis. J Natl Cancer Inst. 2013;105(7):489-98.
91. van Dieren S, Beulens JW, van der Schouw YT, Grobbee DE, Neal B. The global burden of diabetes and its complications: an emerging pandemic. Eur J Cardiovasc Prev Rehabil. 2010;17 Suppl 1:S3-8.
92. Lauby-Secretan B, Scoccianti C, Loomis D, Grosse Y, Bianchini F, Straif K, International Agency for Research on Cancer Handbook Working Group. Body Fatness and Cancer--Viewpoint of the IARC Working Group. N Engl J Med. 2016;375(8):794-8.
93. Giovannucci E, Harlan DM, Archer MC, Bergenstal RM, Gapstur SM, Habel LA, et al. Diabetes and Cancer. Diabetes Care. 2010;33(7):1674-85.
94. Méndez-Giménez L, Rodríguez A, Balaguer I, Frühbeck G. Role of aquaglyceroporins and caveolins in energy and metabolic homeostasis. Mol Cell Endocrinol. 2014;397(1-2):78-92.
95. Palacios-Ortega S, Varela-Guruceaga M, Milagro FI, Martínez JA, de Miguel C. Expression of Caveolin 1 is enhanced by DNA demethylation during adipocyte differentiation. status of insulin signaling. PLoS One. 2014;9(4):e95100.
96. Catalán V, Gómez-Ambrosi J, Rodríguez A, Silva C, Rotellar F, Gil MJ, et al. Expression of caveolin-1 in human adipose tissue is upregulated in obesity and obesity-associated type 2 diabetes mellitus and related to inflammation. Clin Endocrinol (Oxf). 2008;68(2):213-9.
97. Malvi P, Chaube B, Pandey V, Vijayakumar MV, Boreddy PR, Mohammad N, et al. Obesity induced rapid melanoma progression is reversed by orlistat treatment and dietary intervention: role of adipokines. Mol Oncol. 2015;9(3):689-703.
98. Rabinowitz JD, White E. Autophagy and metabolism. Science. 2010;330(6009):1344-8.
99. Altman BJ, Rathmell JC. Metabolic stress in autophagy and cell death pathways. Cold Spring Harb Perspect Biol. 2012;4(9):a008763.
100. Kondo Y, Kanzawa T, Sawaya R, Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer. 2005;5(9):726-34.
101. Coker-Gurkan A, Arisan ED, Obakan P, Guvenir E, Unsal NP. Inhibition of autophagy by 3-MA potentiates purvalanol-induced apoptosis in Bax deficient HCT 116 colon cancer cells. Exp Cell Res. 2014;328(1):87-98.
102. Yang A, Kimmelman AC. Inhibition of autophagy attenuates pancreatic cancer growth independent of TP53/TRP53 status. Autophagy. 2014;10(9):1683-4.
103. Martinez-Outschoorn UE, Sotgia F, Lisanti MP. Caveolae and signalling in cancer. Nat Rev Cancer. 2015;15:225-37.
104. Liu WR, Jin L, Tian MX, Jiang XF, Yang LX, Ding ZB, et al. Caveolin-1 promotes tumor growth and metastasis via autophagy inhibition in hepatocellular carcinoma. Clin Res Hepatol Gastroenterol. 2016;40(2):169-78.
105. Barth S, Glick D, Macleod KF. Autophagy: assays and artifacts. J Pathol. 2010;221(2):117-24.
106. Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12(1):1-222.
107. Shi Y, Tan SH, Ng S, Zhou J, Yang ND, Koo GB, et al. Critical role of CAV1/caveolin-1 in cell stress responses in human breast cancer cells via modulation of lysosomal function and autophagy. Autophagy. 2015;11(5):769-84.
108. Martinez-Outschoorn UE, Trimmer C, Lin Z, Whitaker-Menezes D, Chiavarina B, Zhou J, et al. Autophagy in cancer associated fibroblasts promotes tumor cell survival: Role of hypoxia, HIF1 induction and NFΚB activation in the tumor stromal microenvironment. Cell Cycle. 2010;9(17):3515-33.
109. Wang R, He W, Li Z, Chang W, Xin Y, Huang T. Caveolin-1 functions as a key regulator of 17β-estradiol-mediated autophagy and apoptosis in BT474 breast cancer cells. Int J Mol Med. 2014;34(3):822-7.
110. Chen ZH, Cao JF, Zhou JS, Liu H, Che LQ, Mizumura K, et al. Interaction of caveolin-1 with ATG12-ATG5 system suppresses autophagy in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2014;306(11):L1016-25.
111. Hall DP, Cost NG, Hegde S, Kellner E, Mikhaylova O, Stratton Y, et al. TRPM3 and miR-204 establish a regulatory circuit that controls oncogenic autophagy in clear cell renal cell carcinoma. Cancer Cell. 2014;26(5):738-53.
112. Cabrera S, Maciel M, Herrera I, Nava T, Vergara F, Gaxiola M, López-Otín C, Selman M, Pardo A. Essential role for the ATG4B protease and autophagy in bleomycin-induced pulmonary fibrosis. Autophagy. 2015;11(4):670-84.
113. Zhang J, Ma K, Qi T, Wei X, Zhang Q, Li G, Chiu JF. P62 regulates resveratrol-mediated Fas/Cav-1 complex formation and transition from autophagy to apoptosis. Oncotarget. 2015;6(2):789-801.
114. Galluzzi L, Kepp O, Vander Heiden MG, Kroemer G. Metabolic targets for cancer therapy. Nat Rev Drug Discov. 2013;12(11):829-46.
115. Xie H, Hanai J, Ren JG, Kats L, Burgess K, Bhargava P, et al. Targeting lactate dehydrogenase--a inhibits tumorigenesis and tumor progression in mouse models of lung cancer and impacts tumor-initiating cells. Cell Metab. 2014;19(5):795-809.