Mechanisms linking obesity, inflammation and altered metabolism to colon carcinogenesis

Obesity Reviews

Volumn 13, Issue 12, 2012, Pages 1083-1095

  Yehuda Shnaidman, E ^a   Schwartz, B ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Adipokines; Inflammation; Inflammatory colon cancer; Obesity

Indexed keywords

FATTY ACID; HYPOXIA INDUCIBLE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; TOLL LIKE RECEPTOR 4;

ADIPOSE TISSUE; CANCER GROWTH; COLON CARCINOGENESIS; COLORECTAL CANCER; DIABETES MELLITUS; ENDOPLASMIC RETICULUM STRESS; HUMAN; INFLAMMATION; MACROPHAGE; METABOLIC DISORDER; OBESITY; REVIEW;

ADIPOSE TISSUE; CHRONIC DISEASE; COLONIC NEOPLASMS; COMORBIDITY; ENERGY METABOLISM; HUMANS; INFLAMMATION; MACROPHAGES; OBESITY;

EID: 84868529715     PISSN: 14677881     EISSN: 1467789X     Source Type: Journal    
DOI: 10.1111/j.1467-789X.2012.01024.x     Document Type: Review

References (106)

1. Braun S, Bitton-Worms K, Leroith D. The link between the metabolic syndrome and cancer. Int J Biol Sci 2011; 7: 1003-1015.
2. Ibrahim MM. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev 2010; 11: 11-18.
3. Kursawe R, Eszlinger M, Narayan D etal. Cellularity and adipogenic profile of the abdominal subcutaneous adipose tissue from obese adolescents: association with insulin resistance and hepatic steatosis. Diabetes 2010; 59: 2288-2296.
4. Kershaw EE, Flier JS. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 2004; 89: 2548-2556.
5. Dalmas E, Clement K, Guerre-Millo M. Defining macrophage phenotype and function in adipose tissue. Trends Immunol 2011; 32: 307-314.
6. Osborn O, Olefsky JM. The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 2012; 18: 363-374.
7. Chawla A, Nguyen KD, Goh YP. Macrophage-mediated inflammation in metabolic disease. Nat Rev Immunol 2011; 11: 738-749.
8. Codoner-Franch P, Valls-Belles V, Arilla-Codoner A, Alonso-Iglesias E. Oxidant mechanisms in childhood obesity: the link between inflammation and oxidative stress. Transl Res 2011; 158: 369-384.
9. Bondia-Pons I, Ryan L, Martinez JA. Oxidative stress and inflammation interactions in human obesity. J Physiol Biochem 2012 Feb 17. [Epub ahead of print].
10. Aljada A, Mohanty P, Ghanim H etal. Increase in intranuclear nuclear factor kappaB and decrease in inhibitor kappaB in mononuclear cells after a mixed meal: evidence for a proinflammatory effect. Am J Clin Nutr 2004; 79: 682-690.
11. Bhargava P, Lee CH. Role and function of macrophages in the metabolic syndrome. Biochem J 2012; 442: 253-262.
12. Suganami T, Tanimoto-Koyama K, Nishida J etal. Role of the Toll-like receptor 4/NF-kappaB pathway in saturated fatty acid-induced inflammatory changes in the interaction between adipocytes and macrophages. Arterioscler Thromb Vasc Biol 2007; 27: 84-91.
13. Bjorkbacka H, Kunjathoor VV, Moore KJ etal. Reduced atherosclerosis in MyD88-null mice links elevated serum cholesterol levels to activation of innate immunity signaling pathways. Nat Med 2004; 10: 416-421.
14. Schaeffler A, Gross P, Buettner R etal. Fatty acid-induced induction of Toll-like receptor-4/nuclear factor-kappaB pathway in adipocytes links nutritional signalling with innate immunity. Immunology 2009; 126: 233-245.
15. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 2006; 116: 3015-3025.
16. Lee KY, Gesta S, Boucher J, Wang XL, Kahn CR. The differential role of Hif1beta/Arnt and the hypoxic response in adipose function, fibrosis, and inflammation. Cell Metab 2011; 14: 491-503.
17. Ronti T, Lupattelli G, Mannarino E. The endocrine function of adipose tissue: an update. Clin Endocrinol (Oxf) 2006; 64: 355-365.
18. Anubhuti AS. Leptin and its metabolic interactions: an update. Diabetes Obes Metab 2008; 10: 973-993.
19. de Heredia FP, Gomez-Martinez S, Marcos A. Obesity, inflammation and the immune system. Proc Nutr Soc 2012; 71: 332-338.
20. Singla P, Bardoloi A, Parkash AA. Metabolic effects of obesity: a review. World J Diabetes 2010; 1: 76-88.
21. Harvey AE, Lashinger LM, Hursting SD. The growing challenge of obesity and cancer: an inflammatory issue. Ann N Y Acad Sci 2011; 1229: 45-52.
22. Drevon CA. Fatty acids and expression of adipokines. Biochim Biophys Acta 2005; 1740: 287-292.
23. Laharrague P, Oppert JM, Brousset P etal. High concentration of leptin stimulates myeloid differentiation from human bone marrow CD34+ progenitors: potential involvement in leukocytosis of obese subjects. Int J Obes Relat Metab Disord 2000; 24: 1212-1216.
24. Balogh Z, Foris G, Konya G etal. Obesity abrogates the concentration-dependent effect of leptin on endogenous cholesterol synthesis in human monocytes. Immunobiology 2011; 216: 431-435.
25. Kopp A, Buechler C, Neumeier M etal. Innate immunity and adipocyte function: ligand-specific activation of multiple Toll-like receptors modulates cytokine, adipokine, and chemokine secretion in adipocytes. Obesity (Silver Spring) 2009; 17: 648-656.
26. Tiaka EK, Manolakis AC, Kapsoritakis AN, Potamianos SP. The implication of adiponectin and resistin in gastrointestinal diseases. Cytokine Growth Factor Rev 2011; 22: 109-119.
27. Xu Y, Zhang C, Wang N etal. Adiponectin inhibits lymphotoxin-beta receptor-mediated NF-kappaB signaling in human umbilical vein endothelial cells. Biochem Biophys Res Commun 2011; 404: 1060-1064.
28. Fantuzzi G. Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol 2005; 115: 911-919. Quiz 920.
29. Ohman MK, Wright AP, Wickenheiser KJ, Luo W, Russo HM, Eitzman DT. Monocyte chemoattractant protein-1 deficiency protects against visceral fat-induced atherosclerosis. Arterioscler Thromb Vasc Biol 2010; 30: 1151-1158.
30. Sartipy P, Loskutoff DJ. Monocyte chemoattractant protein 1 in obesity and insulin resistance. Proc Natl Acad Sci U S A 2003; 100: 7265-7270.
31. Kalupahana NS, Claycombe KJ, Moustaid-Moussa N. (n-3) Fatty acids alleviate adipose tissue inflammation and insulin resistance: mechanistic insights. Adv Nutr 2011; 2: 304-316.
32. Iannone F, Lapadula G. Obesity and inflammation - targets for OA therapy. Curr Drug Targets 2010; 11: 586-598.
33. Suganami T, Ogawa Y. Adipose tissue macrophages: their role in adipose tissue remodeling. J Leukoc Biol 2010; 88: 33-39.
34. Fujisaka S, Usui I, Bukhari A etal. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes 2009; 58: 2574-2582.
35. Patsouris D, Li PP, Thapar D, Chapman J, Olefsky JM, Neels JG. Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals. Cell Metab 2008; 8: 301-309.
36. Zeyda M, Stulnig TM. Adipose tissue macrophages. Immunol Lett 2007; 112: 61-67.
37. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010; 60: 277-300.
38. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009; 59: 225-249.
39. Merrill RM, Anderson AE. Risk-adjusted colon and rectal cancer incidence rates in the United States. Dis Colon Rectum 2011; 54: 1301-1306.
40. Kant P, Hull MA. Excess body weight and obesity - the link with gastrointestinal and hepatobiliary cancer. Nat Rev Gastroenterol Hepatol 2011; 8: 224-238.
41. Donohoe CL, Pidgeon GP, Lysaght J, Reynolds JV. Obesity and gastrointestinal cancer. Br J Surg 2010; 97: 628-642.
42. Pais R, Silaghi H, Silaghi AC, Rusu ML, Dumitrascu DL. Metabolic syndrome and risk of subsequent colorectal cancer. World J Gastroenterol 2009; 15: 5141-5148.
43. Sung MK, Yeon JY, Park SY, Park JH, Choi MS. Obesity-induced metabolic stresses in breast and colon cancer. Ann N Y Acad Sci 2011; 1229: 61-68.
44. Gunter MJ, Leitzmann MF. Obesity and colorectal cancer: epidemiology, mechanisms and candidate genes. J Nutr Biochem 2006; 17: 145-156.
45. Poullis A, Foster R, Shetty A, Fagerhol MK, Mendall MA. Bowel inflammation as measured by fecal calprotectin: a link between lifestyle factors and colorectal cancer risk. Cancer Epidemiol Biomarkers Prev 2004; 13: 279-284.
46. Rutter M, Saunders B, Wilkinson K etal. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology 2004; 126: 451-459.
47. Westbrook AM, Szakmary A, Schiestl RH. Mechanisms of intestinal inflammation and development of associated cancers: lessons learned from mouse models. Mutat Res 2010; 705: 40-59.
48. Liu Z, Brooks RS, Ciappio ED etal. Diet-induced obesity elevates colonic TNF-alpha in mice and is accompanied by an activation of Wnt signaling: a mechanism for obesity-associated colorectal cancer. J Nutr Biochem 2011 Dec 29. [Epub ahead of print].
49. Kaler P, Augenlicht L, Klampfer L. Macrophage-derived IL-1beta stimulates Wnt signaling and growth of colon cancer cells: a crosstalk interrupted by vitamin D3. Oncogene 2009; 28: 3892-3902.
50. Liu J, Lam JB, Chow KH etal. Adiponectin stimulates Wnt inhibitory factor-1 expression through epigenetic regulations involving the transcription factor specificity protein 1. Carcinogenesis 2008; 29: 2195-2202.
51. Bremer AA, Devaraj S, Afify A, Jialal I. Adipose tissue dysregulation in patients with metabolic syndrome. J Clin Endocrinol Metab 2011; 96: E1782-E1788.
52. Vykoukal D, Davies MG. Vascular biology of metabolic syndrome. J Vasc Surg 2011; 54: 819-831.
53. Lysaght J, van der Stok EP, Allott EH etal. Pro-inflammatory and tumour proliferative properties of excess visceral adipose tissue. Cancer Lett 2011; 312: 62-72.
54. Le Marchand L, Wang H, Rinaldi S etal. Associations of plasma C-peptide and IGFBP-1 levels with risk of colorectal adenoma in a multiethnic population. Cancer Epidemiol Biomarkers Prev 2010; 19: 1471-1477.
55. Eddi R, Karki A, Shah A, Debari VA, Depasquale JR. Association of type 2 diabetes and colon adenomas. J Gastrointest Cancer 2012; 43: 87-92.
56. Gallagher EJ, LeRoith D. Minireview: IGF, insulin, and cancer. Endocrinology 2011; 152: 2546-2551.
57. Frystyk J, Vestbo E, Skjaerbaek C, Mogensen CE, Orskov H. Free insulin-like growth factors in human obesity. Metabolism 1995; 44: 37-44.
58. Chen J. Multiple signal pathways in obesity-associated cancer. Obes Rev 2011; 12: 1063-1070.
59. Kashyap AS, Hollier BG, Manton KJ, Satyamoorthy K, Leavesley DI, Upton Z. Insulin-like growth factor-I: vitronectin complex-induced changes in gene expression effect breast cell survival and migration. Endocrinology 2011; 152: 1388-1401.
60. Frasca F, Pandini G, Sciacca L etal. The role of insulin receptors and IGF-I receptors in cancer and other diseases. Arch Physiol Biochem 2008; 114: 23-37.
61. Bellacosa A, de Feo D, Godwin AK etal. Molecular alterations of the AKT2 oncogene in ovarian and breast carcinomas. Int J Cancer 1995; 64: 280-285.
62. Fiume R, Ramazzotti G, Faenza I etal. Nuclear PLCs affect insulin secretion by targeting PPARgamma in pancreatic beta cells. FASEB J 2012; 26: 203-210.
63. Sala G, Dituri F, Raimondi C etal. Phospholipase Cgamma1 is required for metastasis development and progression. Cancer Res 2008; 68: 10187-10196.
64. Park SY, Kim JS, Seo YR, Sung MK. Effects of diet-induced obesity on colitis-associated colon tumor formation in A/J mice. Int J Obes (Lond) 2012; 36: 273-280.
65. Algamas-Dimantov A, Davidovsky D, Ben-Ari J etal. Amelioration of diabesity-induced colorectal ontogenesis by omega-3 fatty acids in mice. J Lipid Res 2012; 53: 1056-1070.
66. Lund EK, Belshaw NJ, Elliott GO, Johnson IT. Recent advances in understanding the role of diet and obesity in the development of colorectal cancer. Proc Nutr Soc 2011; 70: 194-204.
67. Jaffe T, Schwartz B. Leptin promotes motility and invasiveness in human colon cancer cells by activating multiple signal-transduction pathways. Int J Cancer 2008; 123: 2543-2556.
68. Popivanova BK, Kitamura K, Wu Y etal. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest 2008; 118: 560-570.
69. Mutoh M, Niho N, Komiya M etal. Plasminogen activator inhibitor-1 (Pai-1) blockers suppress intestinal polyp formation in Min mice. Carcinogenesis 2008; 29: 824-829.
70. Mutoh M, Teraoka N, Takasu S etal. Loss of adiponectin promotes intestinal carcinogenesis in Min and wild-type mice. Gastroenterology 2011; 140: 2000-2008.
71. Otake S, Takeda H, Fujishima S etal. Decreased levels of plasma adiponectin associated with increased risk of colorectal cancer. World J Gastroenterol 2010; 16: 1252-1257.
72. Byeon JS, Jeong JY, Kim MJ etal. Adiponectin and adiponectin receptor in relation to colorectal cancer progression. Int J Cancer 2010; 127: 2758-2767.
73. Nkondjock A, Shatenstein B, Maisonneuve P, Ghadirian P. Specific fatty acids and human colorectal cancer: an overview. Cancer Detect Prev 2003; 27: 55-66.
74. Schwartz B, Algamas-Dimantov A, Hertz R etal. Inhibition of colorectal cancer by targeting hepatocyte nuclear factor-4alpha. Int J Cancer 2009; 124: 1081-1089.
75. Gravaghi C, Bo J, Laperle KM etal. Obesity enhances gastrointestinal tumorigenesis in Apc-mutant mice. Int J Obes (Lond) 2008; 32: 1716-1719.
76. Mutoh M, Komiya M, Teraoka N etal. Overexpression of low-density lipoprotein receptor and lipid accumulation in intestinal polyps in Min mice. Int J Cancer 2009; 125: 2505-2510.
77. Antico Arciuch VG, Elguero ME, Poderoso JJ, Carreras MC. Mitochondrial regulation of cell cycle and proliferation. Antioxid Redox Signal 2012; 16: 1150-1180.
78. Kaaman M, Sparks LM, van Harmelen V etal. Strong association between mitochondrial DNA copy number and lipogenesis in human white adipose tissue. Diabetologia 2007; 50: 2526-2533.
79. Gauthier MS, Miyoshi H, Souza SC etal. AMP-activated protein kinase is activated as a consequence of lipolysis in the adipocyte: potential mechanism and physiological relevance. J Biol Chem 2008; 283: 16514-16524.
80. Kopecky J, Rossmeisl M, Flachs P, Bardova K, Brauner P. Mitochondrial uncoupling and lipid metabolism in adipocytes. Biochem Soc Trans 2001; 29: 791-797.
81. Subauste AR, Burant CF. Role of FoxO1 in FFA-induced oxidative stress in adipocytes. Am J Physiol Endocrinol Metab 2007; 293: E159-E164.
82. Harper JA, Dickinson K, Brand MD. Mitochondrial uncoupling as a target for drug development for the treatment of obesity. Obes Rev 2001; 2: 255-265.
83. Daiber A. Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim Biophys Acta 2010; 1797: 897-906.
84. Yehuda-Shnaidman E, Buehrer B, Pi J, Kumar N, Collins S. Acute stimulation of white adipocyte respiration by PKA-induced lipolysis. Diabetes 2010; 59: 2474-2483.
85. Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 1999; 79: 1127-1155.
86. Wieckowski MR, Brdiczka D, Wojtczak L. Long-chain fatty acids promote opening of the reconstituted mitochondrial permeability transition pore. FEBS Lett 2000; 484: 61-64.
87. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 1999; 341(Pt 2): 233-249.
88. Jacobson J, Duchen MR. Mitochondrial oxidative stress and cell death in astrocytes - requirement for stored Ca2+ and sustained opening of the permeability transition pore. J Cell Sci 2002; 115: 1175-1188.
89. Samovski D, Kalderon B, Yehuda-Shnaidman E, Bar-Tana J. Gating of the mitochondrial permeability transition pore by long chain fatty acyl analogs in vivo. J Biol Chem 2010; 285: 6879-6890.
90. Yehuda-Shnaidman E, Kalderon B, Bar-Tana J. Modulation of mitochondrial transition pore components by thyroid hormone. Endocrinology 2005; 146: 2462-2472.
91. Klein S, Fontana L, Young VL etal. Absence of an effect of liposuction on insulin action and risk factors for coronary heart disease. N Engl J Med 2004; 350: 2549-2557.
92. Pories WJ. Bariatric surgery: risks and rewards. J Clin Endocrinol Metab 2008; 93: S89-S96.
93. Stienstra R, Duval C, Muller M, Kersten S. PPARs, obesity, and inflammation. PPAR Res 2007; 2007: 95974.
94. Westerink J, Visseren FL. Pharmacological and non-pharmacological interventions to influence adipose tissue function. Cardiovasc Diabetol 2011; 10: 13.
95. Lee JE, Baba Y, Ng K etal. Statin use and colorectal cancer risk according to molecular subtypes in two large prospective cohort studies. Cancer Prev Res (Phila) 2011; 4: 1808-1815.
96. Lawson LD, Hughes BG. Human absorption of fish oil fatty acids as triacylglycerols, free acids, or ethyl esters. Biochem Biophys Res Commun 1988; 152: 328-335.
97. Courtney ED, Matthews S, Finlayson C etal. Eicosapentaenoic acid (EPA) reduces crypt cell proliferation and increases apoptosis in normal colonic mucosa in subjects with a history of colorectal adenomas. Int J Colorectal Dis 2007; 22: 765-776.
98. Fini L, Piazzi G, Ceccarelli C etal. Highly purified eicosapentaenoic acid as free fatty acids strongly suppresses polyps in Apc(Min/+) mice. Clin Cancer Res 2010; 16: 5703-5711.
99. West NJ, Clark SK, Phillips RK etal. Eicosapentaenoic acid reduces rectal polyp number and size in familial adenomatous polyposis. Gut 2010; 59: 918-925.
100. Kus V, Flachs P, Kuda O etal. Unmasking differential effects of rosiglitazone and pioglitazone in the combination treatment with n-3 fatty acids in mice fed a high-fat diet. Plos ONE 2011; 6: e27126.
101. Buckley JD, Howe PR. Long-chain omega-3 polyunsaturated fatty acids may be beneficial for reducing obesity-a review. Nutrients 2010; 2: 1212-1230.
102. Ruzickova J, Rossmeisl M, Prazak T etal. Omega-3 PUFA of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue. Lipids 2004; 39: 1177-1185.
103. Huang XF, Xin X, McLennan P, Storlien L. Role of fat amount and type in ameliorating diet-induced obesity: insights at the level of hypothalamic arcuate nucleus leptin receptor, neuropeptide Y and pro-opiomelanocortin mRNA expression. Diabetes Obes Metab 2004; 6: 35-44.
104. Garaulet M, Perez-Llamas F, Perez-Ayala M etal. Site-specific differences in the fatty acid composition of abdominal adipose tissue in an obese population from a Mediterranean area: relation with dietary fatty acids, plasma lipid profile, serum insulin, and central obesity. Am J Clin Nutr 2001; 74: 585-591.
105. Garaulet M, Hernandez-Morante JJ, Lujan J, Tebar FJ, Zamora S. Relationship between fat cell size and number and fatty acid composition in adipose tissue from different fat depots in overweight/obese humans. Int J Obes (Lond) 2006; 30: 899-905.
106. Micallef M, Munro I, Phang M, Garg M. Plasma n-3 polyunsaturated fatty acids are negatively associated with obesity. Br J Nutr 2009; 102: 1370-1374.