Hypoxia, lipids, and cancer: Surviving the harsh tumor microenvironment

Trends in Cell Biology

Volumn 24, Issue 8, 2014, Pages 472-478

  Ackerman, Daniel ^a   Simon, M Celeste ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

ER stress; Hypoxia; Metabolism; SCD1; Unsaturated lipids

Indexed keywords

MEMBRANE LIPID; PROTEIN IRE1; UNSATURATED FATTY ACID; LIPID;

CANCER CELL; CELL METABOLISM; ENDOPLASMIC RETICULUM STRESS; FATTY ACID DESATURATION; HYPOXIA; IN VITRO STUDY; LIPOGENESIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; TUMOR MICROENVIRONMENT; ANIMAL; CELL HYPOXIA; CHEMISTRY; DIET; HUMAN; METABOLISM; NEOPLASM; PATHOLOGY;

ANIMALS; CELL HYPOXIA; DIET; ENDOPLASMIC RETICULUM STRESS; HUMANS; LIPIDS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84904732950     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2014.06.001     Document Type: Review

References (72)

1. Balkwill F.R., et al. The tumor microenvironment at a glance. J. Cell Sci. 2012, 125:5591-5596.
2. Goel S., et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol. Rev. 2011, 91:1071-1121.
3. Vaupel P. Metabolic microenvironment of tumor cells: a key factor in malignant progression. Exp. Oncol. 2010, 32:125-127.
4. Brown J.M., Giaccia A.J. The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res. 1998, 58:1408-1416.
5. Cairns R.A., et al. Regulation of cancer cell metabolism. Nat. Rev. Cancer 2011, 11:85-95.
6. Zaidi N., et al. Lipogenesis and lipolysis: the pathways exploited by the cancer cells to acquire fatty acids. Prog. Lipid Res. 2013, 52:585-589.
7. Menendez J.A., Lupu R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat. Rev. Cancer 2007, 7:763-777.
8. 18F]fluorodeoxyglucose for positron emission tomography of androgen dependent and androgen independent prostate cancer. J. Urol. 2002, 168:273-280.
9. Liu Y., et al. Dominant uptake of fatty acid over glucose by prostate cells: a potential new diagnostic and therapeutic approach. Anticancer Res. 2010, 30:369-374.
10. Zha S., et al. Peroxisomal branched chain fatty acid beta-oxidation pathway is upregulated in prostate cancer. Prostate 2005, 63:316-323.
11. Kuemmerle N.B., et al. Lipoprotein lipase links dietary fat to solid tumor cell proliferation. Mol. Cancer Ther. 2011, 10:427-436.
12. Currie E., et al. Cellular fatty acid metabolism and cancer. Cell Metab. 2013, 18:153-161.
13. Menon S., Manning B.D. Common corruption of the mTOR signaling network in human tumors. Oncogene 2008, 27(Suppl. 2):S43-S51.
14. Duvel K., et al. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol. Cell 2010, 39:171-183.
15. Laplante M., Sabatini D.M. Regulation of mTORC1 and its impact on gene expression at a glance. J. Cell Sci. 2013, 126:1713-1719.
16. Ozcan U., et al. Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis. Mol. Cell 2008, 29:541-551.
17. Young R.M., et al. Dysregulated mTORC1 renders cells critically dependent on desaturated lipids for survival under tumor-like stress. Genes Dev. 2013, 27:1115-1131.
18. Griffiths B., et al. Sterol regulatory element binding protein-dependent regulation of lipid synthesis supports cell survival and tumor growth. Cancer Metab. 2013, 1:3.
19. Guo D., et al. EGFR signaling through an Akt-SREBP-1-dependent, rapamycin-resistant pathway sensitizes glioblastomas to antilipogenic therapy. Sci. Signal. 2009, 2:ra82.
20. Porstmann T., et al. SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab. 2008, 8:224-236.
21. Williams K.J., et al. An essential requirement for the SCAP/SREBP signaling axis to protect cancer cells from lipotoxicity. Cancer Res. 2013, 73:2850-2862.
22. Kamphorst J.J., et al. Hypoxic and Ras-transformed cells support growth by scavenging unsaturated fatty acids from lysophospholipids. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:8882-8887.
23. Feng B., et al. The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat. Cell Biol. 2003, 5:781-792.
24. Cunha D.A., et al. Initiation and execution of lipotoxic ER stress in pancreatic beta-cells. J. Cell Sci. 2008, 121:2308-2318.
25. Fu S., et al. Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature 2011, 473:528-531.
26. Leamy A.K., et al. Molecular mechanisms and the role of saturated fatty acids in the progression of non-alcoholic fatty liver disease. Prog. Lipid Res. 2013, 52:165-174.
27. Muoio D.M., Newgard C.B. Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and beta-cell failure in type 2 diabetes. Nat. Rev. Mol. Cell Biol. 2008, 9:193-205.
28. Giacca A., et al. Lipid-induced pancreatic beta-cell dysfunction: focus on in vivo studies. Am. J. Physiol. Endocrinol. Metab. 2011, 300:E255-E262.
29. Borradaile N.M., et al. Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J. Lipid Res. 2006, 47:2726-2737.
30. Ariyama H., et al. Decrease in membrane phospholipid unsaturation induces unfolded protein response. J. Biol. Chem. 2010, 285:22027-22035.
31. Peng G., et al. Oleate blocks palmitate-induced abnormal lipid distribution, endoplasmic reticulum expansion and stress, and insulin resistance in skeletal muscle. Endocrinology 2011, 152:2206-2218.
32. 2-terminal kinase activation and elevated proapoptotic Bax. J. Nutr. 2008, 138:1866-1871.
33. Wang D., et al. Saturated fatty acids promote endoplasmic reticulum stress and liver injury in rats with hepatic steatosis. Endocrinology 2006, 147:943-951.
34. Zhang W., et al. ER stress potentiates insulin resistance through PERK-mediated FOXO phosphorylation. Genes Dev. 2013, 27:441-449.
35. Coll T., et al. Oleate reverses palmitate-induced insulin resistance and inflammation in skeletal muscle cells. J. Biol. Chem. 2008, 283:11107-11116.
36. Nakamura S., et al. Palmitate induces insulin resistance in H4IIEC3 hepatocytes through reactive oxygen species produced by mitochondria. J. Biol. Chem. 2009, 284:14809-14818.
37. Ryan M., et al. Diabetes and the Mediterranean diet: a beneficial effect of oleic acid on insulin sensitivity, adipocyte glucose transport and endothelium-dependent vasoreactivity. QJM 2000, 93:85-91.
38. Serra-Majem L., et al. Scientific evidence of interventions using the Mediterranean diet: a systematic review. Nutr. Rev. 2006, 64:S27-S47.
39. Vessby B., et al. Substituting dietary saturated for monounsaturated fat impairs insulin sensitivity in healthy men and women: the KANWU Study. Diabetologia 2001, 44:312-319.
40. Rong X., et al. LXRs regulate ER stress and inflammation through dynamic modulation of membrane phospholipid composition. Cell Metab. 2013, 18:685-697.
41. 2-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol. Cell 2002, 10:983-994.
42. Kitai Y., et al. Membrane lipid saturation activates IRE1alpha without inducing clustering. Genes Cells 2013, 18:798-809.
43. Promlek T., et al. Membrane aberrancy and unfolded proteins activate the endoplasmic reticulum stress sensor Ire1 in different ways. Mol. Biol. Cell 2011, 22:3520-3532.
44. Volmer R., et al. Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:4628-4633.
45. 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.
46. Nieman K.M., et al. Adipose tissue and adipocytes support tumorigenesis and metastasis. Biochim. Biophys. Acta 2013, 1831:1533-1541.
47. Carter J.C., Church F.C. Mature breast adipocytes promote breast cancer cell motility. Exp. Mol. Pathol. 2012, 92:312-317.
48. Nieman K.M., et al. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat. Med. 2011, 17:1498-1503.
49. Donohoe C.L., et al. Cancer cachexia: mechanisms and clinical implications. Gastroenterol. Res. Pract. 2011, 2011:601434.
50. Islam-Ali B., et al. Modulation of adipocyte G-protein expression in cancer cachexia by a lipid-mobilizing factor (LMF). Br. J. Cancer 2001, 85:758-763.
51. Agustsson T., et al. Mechanism of increased lipolysis in cancer cachexia. Cancer Res. 2007, 67:5531-5537.
52. Arner P. Medicine. Lipases in cachexia. Science 2011, 333:163-164.
53. Das S.K., et al. Adipose triglyceride lipase contributes to cancer-associated cachexia. Science 2011, 333:233-238.
54. Renehan A.G., et al. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet 2008, 371:569-578.
55. Reeves G.K., et al. Cancer incidence and mortality in relation to body mass index in the Million Women Study: cohort study. BMJ 2007, 335:1134.
56. Friedenreich C.M., et al. Case-control study of the metabolic syndrome and metabolic risk factors for endometrial cancer. Cancer Epidemiol. Biomarkers Prev. 2011, 20:2384-2395.
57. Yahagi N., et al. Co-ordinate activation of lipogenic enzymes in hepatocellular carcinoma. Eur. J. Cancer 2005, 41:1316-1322.
58. Li J., et al. Partial characterization of a cDNA for human stearoyl-CoA desaturase and changes in its mRNA expression in some normal and malignant tissues. Int. J. Cancer 1994, 57:348-352.
59. von Roemeling C.A., et al. Stearoyl-CoA desaturase 1 is a novel molecular therapeutic target for clear cell renal cell carcinoma. Clin. Cancer Res. 2013, 19:2368-2380.
60. Leung J.Y., Kim W.Y. Stearoyl Co-A desaturase 1 as a ccRCC therapeutic target: death by stress. Clin. Cancer Res. 2013, 19:3111-3113.
61. Roongta U.V., et al. Cancer cell dependence on unsaturated fatty acids implicates stearoyl-CoA desaturase as a target for cancer therapy. Mol. Cancer Res. 2011, 9:1551-1561.
62. Mason P., et al. SCD1 inhibition causes cancer cell death by depleting mono-unsaturated fatty acids. PLoS ONE 2012, 7:e33823.
63. Hess D., et al. Inhibition of stearoylCoA desaturase activity blocks cell cycle progression and induces programmed cell death in lung cancer cells. PLoS ONE 2010, 5:e11394.
64. Commisso C., et al. Macropinocytosis of protein is an amino acid supply route in Ras-transformed cells. Nature 2013, 497:633-637.
65. Hollien J., Weissman J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 2006, 313:104-107.
66. Yoshida H., et al. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001, 107:881-891.
67. Upton J.P., et al. IRE1alpha cleaves select microRNAs during ER stress to derepress translation of proapoptotic Caspase-2. Science 2012, 338:818-822.
68. Lerner A.G., et al. IRE1alpha induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab. 2012, 16:250-264.
69. Walter P., Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334:1081-1086.
70. Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 2012, 13:89-102.
71. Tabas I., Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 2011, 13:184-190.
72. Sovolyova N., et al. Stressed to death - mechanisms of ER stress-induced cell death. Biol. Chem. 2014, 395:1-13.