Effects of calorie restriction and diet-induced obesity on murine colon carcinogenesis, growth and inflammatory factors, and MicroRNA expression

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Olivo Marston, Susan E ^a,b   Hursting, Stephen D ^c,d   Perkins, Susan N ^a   Schetter, Aaron ^a   Khan, Mohammed ^a   Croce, Carlo ^e   Harris, Curtis C ^a   Lavigne, Jackie ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c The University of Texas at Austin   (United States)

^d UNIVERSITY OF TEXAS   (United States)

^e THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GROWTH FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MICRORNA; MICRORNA 138; MICRORNA 150; MICRORNA 155; MICRORNA 16; MICRORNA 196; MICRORNA 34; MICRORNA 351; MICRORNA 425; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOAVAILABILITY; BODY COMPOSITION; BODY WEIGHT; CALORIC RESTRICTION; CARCINOGENESIS; CELL PROLIFERATION; COLON CANCER; CONTROLLED STUDY; CORRELATION ANALYSIS; DUAL ENERGY X RAY ABSORPTIOMETRY; ENERGY BALANCE; GENE EXPRESSION; GLUCOSE TOLERANCE TEST; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; COLON TUMOR; COMPLICATION; DIET; GENE EXPRESSION REGULATION; INFLAMMATION; METABOLISM; PATHOLOGY; RANDOMIZATION; RISK FACTOR;

ADIPOKINES; ANIMALS; APOPTOSIS; BODY COMPOSITION; BODY WEIGHT; CALORIC RESTRICTION; CARCINOGENESIS; CELL PROLIFERATION; COLONIC NEOPLASMS; CYTOKINES; DIET; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE TOLERANCE TEST; INFLAMMATION; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; MICRORNAS; OBESITY; RANDOM ALLOCATION; RISK FACTORS;

EID: 84899630749     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094765     Document Type: Article

References (54)

1. Slattery ML, Potter J, Caan B, Edwards S, Coates A, et al. (1997) Energy Balance and Colon Cancer - beyond Physical Activity. Cancer Research 57: 75-80. (Pubitemid 27020333)
2. Giovannucci E, Colditz GA, Stampfer MJ, Willett WC (1996) Physical activity, obesity, and risk of colorectal adenoma in women (United States). Cancer Causes Control 7: 253-263. (Pubitemid 26155463)
3. Giovannucci E, Ascherio A, Rimm E, Colditz G, Stampfer M, et al. (1995) Physical activity, obesity, and risk for colon cancer and adenoma in men. Ann Intern Med 122: 327-334.
4. Giovannucci E, Pollak M, Platz EA, Willett WC, Stampfer MJ, et al. (2000) Insulin-like growth factor I (IGF-I), IGF-binding protein-3 and the risk of colorectal adenoma and cancer in the Nurses' Health Study. Growth HormIGFRes 10 Suppl A: S30-S31. (Pubitemid 30641925)
5. Tannenbaum A (1947) Effects of varying caloric intake upon tumor incidence and tumor growth. Ann Acad Sci 49: 5-18.
6. Hursting SD, Lavigne JA, Berrigan D, Perkins SN, Barrett JC (2003) Calorie restriction, aging, and cancer prevention: mechanisms of action and applicability to humans. AnnuRevMed 54: 131-152. (Pubitemid 37386388)
7. Reddy BS, Wang C-X, Maruyama H (1987) Effect of Restricted Caloric Intake on Azoxymethane-induced Colon Tumor Incidence in Male F344 Rats. Cancer Research 47: 1226-1228. (Pubitemid 17023185)
8. Kumar SP, Roy SJ, Tokumo K, Reddy BS (1990) Effect of Different Levels of Calorie Restriction on Azoxymethane-induced Colon Carcinogenesis in Male F344 Rats. Cancer Research 50: 5761-5766. (Pubitemid 20331373)
9. Mai V, Colbert LH, Berrigan D, Perkins SN, Pfeiffer R, et al. (2003) Calorie restriction and diet composition modulate spontaneous intestinal tumorigenesis in Apc(Min) mice through different mechanisms. Cancer Res 63: 1752-1755. (Pubitemid 36460832)
10. Rondini EA, Harvey AE, Steibel JP, Hursting SD, Fenton JI (2011) Energy balance modulates colon tumor growth: Interactive roles of insulin and estrogen. Molecular Carcinogenesis 50: 370-382.
11. Klurfeld DM, Weber MM, Kritchevsky D (1987) Inhibition of Chemically Induced Mammary and Colon Tumor Promotion by Caloric Restriction in Rats Fed Increased Dietary Fat. Cancer Research 47: 2759-2762. (Pubitemid 17113410)
12. Giovanella BC, Shepard RC, Stehlin JS, Venditti JM, Abbott BJ (1982) Calorie restriction: effect on growth of human tumors heterotransplanted in nude mice. J Natl Cancer Inst 68: 249-257. (Pubitemid 12136129)
13. Raju J, Bird RP (2003) Energy restriction reduces the number of advanced aberrant crypt foci and attenuates the expression of colonic transforming growth factor beta and cyclooxygenase isoforms in Zucker obese (fa/fa) rats. Cancer Res 63: 6595-6601. (Pubitemid 37322937)
14. Albanes D (1987) Caloric intake, body weight, and cancer: a review. NutrCancer 9: 199-217. (Pubitemid 17079340)
15. Macrae FA (1993) Fat and Calories in Colon and Breast Cancer: From Animal Studies to Controlled Clinical Trials. Preventive Medicine 22: 750-766. (Pubitemid 23311558)
16. Weber RV, Stein DE, Scholes J, Kral JG (2000) Obesity potentiates AOMinduced colon cancer. Dig Dis Sci 45: 890-895. (Pubitemid 30238248)
17. Yakar S, Nunez NP, Pennisi P, Brodt P, Sun H, et al. (2006) Increased Tumor Growth in Mice with Diet-Induced Obesity: Impact of Ovarian Hormones. Endocrinology 147: 5826-5834. (Pubitemid 44833499)
18. Wheatley KE, Williams EA, Smith NCP, Dillard A, Park EY, et al. (2007) Low-Carbohydrate Diet Versus Caloric Restriction: Effects on Weight Loss, Hormones, and Colon Tumor Growth in Obese Mice. Nutrition and Cancer 60: 61-68. (Pubitemid 351192917)
19. Giovannucci E (2001) Insulin, insulin-like growth factors and colon cancer: a review of the evidence. JNutr 131: 3109S-3120S. (Pubitemid 33070788)
20. Giovannucci E, Pollak MN, Platz EA, Willett WC, Stampfer MJ, et al. (2000) A prospective study of plasma insulin-like growth factor-1 and binding protein-3 and risk of colorectal neoplasia in women. Cancer EpidemiolBiomarkers Prev 9: 345-349. (Pubitemid 30265776)
21. Palmqvist R, Hallmans G, Rinaldi S, Biessy C, Stenling R, et al. (2002) Plasma insulin-like growth factor 1, insulin-like growth factor binding protein 3, and risk of colorectal cancer: a prospective study in northern Sweden. Gut 50: 642-646. (Pubitemid 34407490)
22. Fenton JI, Hord NG, Lavigne JA, Perkins SN, Hursting SD (2005) Leptin, insulin-like growth factor-1, and insulin-like growth factor-2 are mitogens in ApcMin/+ but not Apc+/+ colonic epithelial cell lines. Cancer EpidemiolBiomarkers Prev 14: 1646-1652. (Pubitemid 40995074)
23. Hursting SD, Lashinger LM, Colbert LH, Rogers CJ, Wheatley KW, et al. (2007) Energy balance and carcinogenesis: underlying pathways and targets for intervention. Curr Cancer Drug Targets 7: 484-491. (Pubitemid 47196208)
24. Koenuma M, Yamori T, Tsuruo T (1989) Insulin and insulin-like growth factor 1 stimulate proliferation of metastatic variants of colon carcinoma 26. JpnJCancer Res 80: 51-58. (Pubitemid 20027198)
25. Ruhl CE, Harris TB, Ding J, Goodpaster BH, Kanaya AM, et al. (2007) Body mass index and serum leptin concentration independently estimate percentage body fat in older adults. The American Journal of Clinical Nutrition 85: 1121-1126. (Pubitemid 46557930)
26. Hardwick JC, Van Den Brink GR, Offerhaus GJ, Van Deventer SJ, Peppelenbosch MP (2001) Leptin is a growth factor for colonic epithelial cells. Gastroenterology 121: 79-90. (Pubitemid 32591517)
27. Otake S, Takeda H, Fujishima S, Fukui T, Orii T, et al. (2010) Decreased levels of plasma adiponectin associated with increased risk of colorectal cancer. World J Gastroenterol 16: 1252-1257.
28. Otake S, Takeda H, Suzuki Y, Fukui T, Watanabe S, et al. (2005) Association of Visceral Fat Accumulation and Plasma Adiponectin with Colorectal Adenoma: Evidence for Participation of Insulin Resistance. Clinical Cancer Research 11: 3642-3646. (Pubitemid 40685579)
29. Wei EK, Giovannucci E, Fuchs CS, Willett WC, Mantzoros CS (2005) Low Plasma Adiponectin Levels and Risk of Colorectal Cancer in Men: A Prospective Study. Journal of the National Cancer Institute 97: 1688-1694. (Pubitemid 41672235)
30. Olivo-Marston SE, Hursting SD, Lavigne J, Perkins SN, Maarouf RS, et al. (2009) Genetic reduction of circulating insulin-like growth factor-1 inhibits azoxymethane-induced colon tumorigenesis in mice. Mol Carcinog 48: 1071-1076.
31. Olivo SE, Hilakivi-Clarke L (2005) Opposing effects of prepubertal low-and high-fat n-3 polyunsaturated fatty acid diets on rat mammary tumorigenesis. Carcinogenesis 26: 1563-1572. (Pubitemid 41236049)
32. Liu C-G, Calin GA, Meloon B, Gamliel N, Sevignani C, et al. (2004) An oligonucleotide microchip for genome-wide microRNA profiling in human and mouse tissues. Proceedings of the National Academy of Sciences of the United States of America 101: 9740-9744. (Pubitemid 38869306)
33. StataCorp (2009) Stata Statistical Software: Release 11. 11 ed. College Station: StataCorp LP.
34. Ealey KN, Lu S, Archer MC (2008) Development of aberrant crypt foci in the colons of ob/ob and db/db mice: Evidence that leptin is not a promoter. Molecular Carcinogenesis 47: 667-677.
35. Bobe G, Barrett KG, Mentor-Marcel RA, Saffiotti U, Young MR, et al. (2008) Dietary Cooked Navy Beans and Their Fractions Attenuate Colon Carcinogenesis in Azoxymethane-Induced Ob/Ob Mice. Nutrition and Cancer 60: 373-381. (Pubitemid 351601375)
36. Mentor-Marcel RA, Bobe G, Barrett KG, Young MR, Albert PS, et al. (2009) Inflammation-Associated Serum and Colon Markers as Indicators of Dietary Attenuation of Colon Carcinogenesis in ob/ob Mice. Cancer Prevention Research 2: 60-69.
37. Padidar S, Farquharson AJ, Williams LM, Kelaiditi E, Hoggard N, et al. (2011) Leptin up-regulates pro-inflammatory cytokines in discrete cells within mouse colon. Journal of Cellular Physiology 226: 2123-2130.
38. Liu Z, Brooks RS, Ciappio ED, Kim SJ, Crott JW, et al. Diet-induced obesity elevates colonic TNF-á in mice and is accompanied by an activation of Wnt signaling: a mechanism for obesity-associated colorectal cancer. The Journal of Nutritional Biochemistry.
39. Zeng H, Lazarova DL (2011) Obesity-related colon cancer: dietary factors and their mechanisms of anticancer action. Clinical and Experimental Pharmacology and Physiology: no-no.
40. Karin M, Greten FR (2005) NF-[kappa]B: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 5: 749-759. (Pubitemid 41400849)
41. Fenton JI, Nuñez NP, Yakar S, Perkins SN, Hord NG, et al. (2009) Diet-induced adiposity alters the serum profile of inflammation in C57BL/6N mice as measured by antibody array. Diabetes, Obesity and Metabolism 11: 343-354.
42. Abolhassani M, Aloulou N, Chaumette MT, Aparicio T, Martin-Garcia N, et al. (2008) Leptin Receptor-Related Immune Response in Colorectal Tumors: The Role of Colonocytes and Interleukin-8. Cancer Research 68: 9423-9432.
43. Farquharson A, Steele R, Carey F, Drew J, Novel multiplex method to assess insulin, leptin and adiponectin regulation of inflammatory cytokines associated with colon cancer. Molecular Biology Reports: 1-10.
44. Barb D, Pazaitou-Panayiotou K, Mantzoros CS (2006) Adiponectin: a link between obesity and cancer. Expert Opin Investig Drugs 15: 917-931.
45. Huang XF, Chen J (2009) Adiponectin and signal pathways in obesity-induced colon cancer. Gut 58: 1169; author reply 1169-1170.
46. Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, et al. (2008) Epigenetic Silencing of MicroRNA-34b/c and B-Cell Translocation Gene 4 Is Associated with CpG Island Methylation in Colorectal Cancer. Cancer Research 68: 4123-4132.
47. Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, et al. (2008) MicroRNA Expression Profiles Associated With Prognosis and Therapeutic Outcome in Colon Adenocarcinoma. JAMA: The Journal of the American Medical Association 299: 425-436. (Pubitemid 351185951)
48. Watanabe A, Tagawa H, Yamashita J, Teshima K, Nara M, et al. (2011) The role of microRNA-150 as a tumor suppressor in malignant lymphoma. Leukemia 25: 1324-1334.
49. Volinia S, Calin GA, Liu C-G, Ambs S, Cimmino A, et al. (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proceedings of the National Academy of Sciences of the United States of America 103: 2257-2261. (Pubitemid 43271657)
50. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, et al. (2006) Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9: 189-198. (Pubitemid 43357945)
51. Takagi T, Naito Y, Mizushima K, Hirata I, Yagi N, et al. (2010) Increased expression of microRNA in the inflamed colonic mucosa of patients with active ulcerative colitis. Journal of Gastroenterology and Hepatology 25: S129-S133.
52. Schimanski CC, Frerichs K., Rahman F., Berger M., Lang H., Galle P.R., Moehler M., Gockel I. (2009) High miR-196a levels promote the oncogenic phenotype of colorectal cancer cells. World J Gastroenterol 15: 2089-2096.
53. Lashinger LM, Malone LM, Brown GW, Daniels EA, Goldberg JA, et al. (2011) Rapamycin Partially Mimics the Anticancer Effects of Calorie Restriction in a Murine Model of Pancreatic Cancer. Cancer Prevention Research 4: 1041-1051.
54. Moore T, Beltran L, Carbajal S, Strom S, Traag J, et al. (2008) Dietary Energy Balance Modulates Signaling through the Akt/Mammalian Target of Rapamycin Pathways in Multiple Epithelial Tissues. Cancer Prevention Research 1: 65-76.