Calorie restriction decreases murine and human pancreatic tumor cell growth, nuclear factor-κB activation, and inflammation-related gene expression in an insulin-like growth factor-1 - Dependent manner

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Harvey, Alison E ^a   Lashinger, Laura M ^a   Hays, Drew ^a   Harrison, Lauren M ^a   Lewis, Kimberly ^a   Fischer, Susan M ^b   Hursting, Stephen D ^a,b  

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

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALGRANULIN B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; SOMATOMEDIN C; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL MONITORING; BIRC5 GENE; C57BL 6 MOUSE; CALORIC RESTRICTION; CANCER CELL; CANCER INHIBITION; CANCER SIZE; CCDN1 GENE; CELL NUCLEUS; CELL STRAIN; CELL STRAIN MIAPACA 2; CELL STRAIN PANC02; CONTROLLED STUDY; DIETARY INTAKE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; INTRACELLULAR TRANSPORT; MACROPHAGE; MALE; MOUSE; NONHUMAN; PANCREAS CANCER; PROTEIN BLOOD LEVEL; PROTEIN DNA BINDING; PROTEIN TRANSPORT; PTGS2 GENE; SOMATOMEDIN C BLOOD LEVEL; TRANSCRIPTION INITIATION; VEGF GENE; ANIMAL; BLOOD; C57BL MOUSE; METABOLISM; PANCREAS TUMOR;

ANIMALS; CALORIC RESTRICTION; HUMANS; INFLAMMATION; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; MICE, INBRED C57BL; NF-KAPPA B; PANCREATIC NEOPLASMS;

EID: 84900523546     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094151     Document Type: Article

References (48)

1. Siegel R, Naishadham D, Jemal A (2012) Cancer statistics, 2012. CA: a cancer journal for clinicians 62: 10-29.
2. Shaib YH, Davila JA, El-Serag HB (2006) The epidemiology of pancreatic cancer in the United States: changes below the surface. Aliment Pharmacol Ther 24: 87-94. (Pubitemid 43894008)
3. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ (2003) Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 348: 1625-1638. (Pubitemid 36459468)
4. Giovannucci E, Michaud D (2007) The role of obesity and related metabolic disturbances in cancers of the colon, prostate, and pancreas. Gastroenterology 132: 2208-2225. (Pubitemid 46693749)
5. Hursting SD, Dunlap SM (2012) Obesity, metabolic dysregulation, and cancer: a growing concern and an inflammatory (and microenvironmental) issue. Annals of the New York Academy of Sciences 1271: 82-87.
6. Sica A, Allavena P, Mantovani A (2008) Cancer related inflammation: the macrophage connection. Cancer Lett 267: 204-215.
7. Lowenfels AB, Maisonneuve P, Cavallini G, Ammann RW, Lankisch PG, et al. (1993) Pancreatitis and the risk of pancreatic cancer. International Pancreatitis Study Group. N Engl J Med 328: 1433-1437. (Pubitemid 23143844)
8. Goecke H, Forssmann U, Uguccioni M, Friess H, Conejo-Garcia JR, et al. (2000) Macrophages infiltrating the tissue in chronic pancreatitis express the chemokine receptor CCR5. Surgery 128: 806-814.
9. Bellone G, Smirne C, Mauri FA, Tonel E, Carbone A, et al. (2006) Cytokine expression profile in human pancreatic carcinoma cells and in surgical specimens: implications for survival. Cancer Immunol Immunother 55: 684-698.
10. Kokawa A, Kondo H, Gotoda T, Ono H, Saito D, et al. (2001) Increased expression of cyclooxygenase-2 in human pancreatic neoplasms and potential for chemoprevention by cyclooxygenase inhibitors. Cancer 91: 333-338. (Pubitemid 32099234)
11. Monti P, Leone BE, Marchesi F, Balzano G, Zerbi A, et al. (2003) The CC chemokine MCP-1/CCL2 in pancreatic cancer progression: regulation of expression and potential mechanisms of antimalignant activity. Cancer Res 63: 7451-7461. (Pubitemid 37413488)
12. Balkwill F, Coussens LM (2004) Cancer: an inflammatory link. Nature 431: 405-406. (Pubitemid 39329565)
13. Wang W, Abbruzzese JL, Evans DB, Larry L, Cleary KR, et al. (1999) The nuclear factor-kappa B RelA transcription factor is constitutively activated in human pancreatic adenocarcinoma cells. Clinical cancer research: an official journal of the American Association for Cancer Research 5: 119-127.
14. Maier HJ, Schmidt-Strassburger U, Huber MA, Wiedemann EM, Beug H, et al. (2010) NF-kappaB promotes epithelial-mesenchymal transition, migration and invasion of pancreatic carcinoma cells. Cancer letters 295: 214-228.
15. Xiong HQ, Abbruzzese JL (2004) Adjuvant therapy for pancreatic cancer: current status and future directions. Surgical oncology clinics of North America 13: 737-749, xi. (Pubitemid 39209350)
16. Yebra M, Filardo EJ, Bayna EM, Kawahara E, Becker JC, et al. (1995) Induction of carcinoma cell migration on vitronectin by NF-kappa B-dependent gene expression. Molecular biology of the cell 6: 841-850.
17. Harvey AE, Lashinger LM, Hursting SD (2011) The growing challenge of obesity and cancer: an inflammatory issue. Annals of the New York Academy of Sciences 1229: 45-52.
18. Adachi Y, Yamamoto H, Ohashi H, Endo T, Carbone DP, et al. (2010) A candidate targeting molecule of insulin-like growth factor-I receptor for gastrointestinal cancers. World J Gastroenterol 16: 5779-5789.
19. Dolcet X, Llobet D, Pallares J, Matias-Guiu X (2005) NF-kB in development and progression of human cancer. Virchows Arch 446: 475-482. (Pubitemid 40884279)
20. Basseres DS, Baldwin AS (2006) Nuclear factor-kappaB and inhibitor of kappaB kinase pathways in oncogenic initiation and progression. Oncogene 25: 6817-6830. (Pubitemid 44657854)
21. Bhattacharya A, Chandrasekar B, Rahman MM, Banu J, Kang JX, et al. (2006) Inhibition of inflammatory response in transgenic fat-1 mice on a calorie-restricted diet. Biochem Biophys Res Commun 349: 925-930. (Pubitemid 44380189)
22. Wheatley KE, Williams EA, Smith NC, Dillard A, Park EY, et al. (2008) Low-carbohydrate diet versus caloric restriction: effects on weight loss, hormones, and colon tumor growth in obese mice. Nutr Cancer 60: 61-68. (Pubitemid 351192917)
23. Hursting SD, Berger NA (2010) Energy balance, host-related factors, and cancer progression. J Clin Oncol 28: 4058-4065.
24. Roebuck BD, Baumgartner KJ, MacMillan DL (1993) Caloric restriction and intervention in pancreatic carcinogenesis in the rat. Cancer research 53: 46-52. (Pubitemid 23019375)
25. Lashinger LM, Harrison LM, Rasmussen AJ, Logsdon CD, Fischer SM, et al. (2013) Dietary Energy Balance Modulation of Kras- and Ink4a/Arf+/ - Driven Pancreatic Cancer: The Role of Insulin-like Growth Factor-I. Cancer prevention research 6: 1046-1055.
26. 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.
27. Lashinger LM, Malone LM, McArthur MJ, Goldberg JA, Daniels EA, et al. (2011) Genetic reduction of insulin-like growth factor-1 mimics the anticancer effects of calorie restriction on cyclooxygenase-2-driven pancreatic neoplasia. Cancer prevention research 4: 1030-1040.
28. Harvey AE, Lashinger LM, Otto G, Nunez NP, Hursting SD (2012) Decreased systemic IGF-1 in response to calorie restriction modulates murine tumor cell growth, nuclear factor-kappaB activation, and inflammation-related gene expression. Molecular carcinogenesis.
29. Lashinger LM, Ford NA, Hursting SD (2014) Interacting inflammatory and growth factor signals underlie the obesity-cancer link. The Journal of nutrition 144: 109-113.
30. Kim DH, Kim JY, Yu BP, Chung HY (2008) The activation of NF-kappaB through Akt-induced FOXO1 phosphorylation during aging and its modulation by calorie restriction. Biogerontology 9: 33-47.
31. Kim HJ, Yu BP, Chung HY (2002) Molecular exploration of age-related NF-kappaB/IKK downregulation by calorie restriction in rat kidney. Free Radic Biol Med 32: 991-1005.
32. Bhattacharya A, Chandrasekar B, Rahman MM, Banu J, Kang JX, et al. (2006) Inhibition of inflammatory response in transgenic fat-1 mice on a calorie-restricted diet. Biochemical and biophysical research communications 349: 925-930. (Pubitemid 44380189)
33. 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. Molecular carcinogenesis 48: 1071-1076.
34. Corbett TH, Roberts BJ, Leopold WR, Peckham JC, Wilkoff LJ, et al. (1984) Induction and chemotherapeutic response of two transplantable ductal adenocarcinomas of the pancreas in C57BL/6 mice. Cancer research 44: 717-726. (Pubitemid 14184610)
35. Ford NA, Nunez NP, Holcomb VB, Hursting SD (2013) IGF1 dependence of dietary energy balance effects on murine Met1 mammary tumor progression, epithelial-to-mesenchymal transition, and chemokine expression. Endocrine-related cancer 20: 39-51.
36. Nunez NP, Perkins SN, Smith NC, Berrigan D, Berendes DM, et al. (2008) Obesity accelerates mouse mammary tumor growth in the absence of ovarian hormones. Nutrition and cancer 60: 534-541. (Pubitemid 351918549)
37. Fenton JI, Nunez 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 & metabolism 11: 343-354.
38. Roebuck BD, Yager JD, Longnecker DS (1981) Dietary Modulation of Azaserine-induced Pancreatic Carcinogenesis in the Rat. Cancer Res 41: 888-893. (Pubitemid 11136331)
39. Craven-Giles T, Tagliaferro AR, Ronan AM, Baumgartner KJ, Roebuck BD (1994) Dietary modulation of pancreatic carcinogenesis: calories and energy expenditure. Cancer research 54: 1964s-1968s. (Pubitemid 24132157)
40. 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.
41. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, et al. (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118: 285-296. (Pubitemid 39061110)
42. Karin M (2005) Inflammation and cancer: the long reach of Ras. Nat Med 11: 20-21.
43. Mancino A, Lawrence T (2010) Nuclear Factor-κB and Tumor-Associated Macrophages. Clinical Cancer Research 16: 784-789.
44. Luedde T, Beraza N, Trautwein C (2006) Evaluation of the role of nuclear factor-κB signaling in liver injury using genetic animal models. J Gastroenterol Hepatol 21: S43-S46. (Pubitemid 44266549)
45. Rouet-Benzineb P, Aparicio T, Guilmeau S, Pouzet C, Descatoire V, et al. (2004) Leptin counteracts sodium butyrate-induced apoptosis in human colon cancer HT-29 cells via NF-kappaB signaling. J Biol Chem 279: 16495-16502. (Pubitemid 38509348)
46. Ma J, Sawai H, Matsuo Y, Ochi N, Yasuda A, et al. (2010) IGF-1 Mediates PTEN Suppression and Enhances Cell Invasion and Proliferation via Activation of the IGF-1/PI3K/Akt Signaling Pathway in Pancreatic Cancer Cells. J Surg Res 160: 90-101.
47. Lin Y, Tamakoshi A, Kikuchi S, Yagyu K, Obata Y, et al. (2004) Serum insulin-like growth factor-I, insulin-like growth factor binding protein-3, and the risk of pancreatic cancer death. Int J Cancer 110: 584-588. (Pubitemid 38658024)
48. Karna E, Surazynski A, Orlowski K, Laszkiewicz J, Puchalski Z, et al. (2002) Serum and tissue level of insulin-like growth factor-I (IGF-I) and IGF-I binding proteins as an index of pancreatitis and pancreatic cancer. Int J Exp Pathol 83: 239-245. (Pubitemid 36321742)