Dietary energy balance modulates signaling through the Akt/mammalian target of rapamycin pathways in multiple epithelial tissues

Cancer Prevention Research

Volumn 1, Issue 1, 2008, Pages 65-76

  Moore, Tricia ^a,b   Beltran, Linda ^a   Carbajal, Steve ^a   Strom, Sara ^c   Traag, Jeanine ^a   Hursting, Stephen D ^a,b   DiGiovanni, John ^a,b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; ONCOPROTEIN; PROTEIN KINASE; SOMATOMEDIN C;

ANIMAL; ARTICLE; BODY FAT DISTRIBUTION; BODY WEIGHT; C57BL MOUSE; DIET; EATING; ENERGY METABOLISM; EPITHELIUM; FEMALE; HOMEOSTASIS; INSTITUTE FOR CANCER RESEARCH MOUSE; MALE; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BODY FAT DISTRIBUTION; BODY WEIGHT; DIET; EATING; ENERGY METABOLISM; EPITHELIUM; FEMALE; HOMEOSTASIS; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; ONCOGENE PROTEIN V-AKT; PROTEIN KINASES; SIGNAL TRANSDUCTION;

EID: 56549109059     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-08-0022     Document Type: Article

References (77)

1. Hedley AA, Ogden CL, Johnson CL, Carroll MD, Curtin LR, Flegal KM. Prevalence of overweight and obesity among US children, adolescents, and adults, 1999-2002. JAMA 2004;291:2847-50.
2. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U S. adults. N Engl J Med 2003;348:1625-38.
3. Hursting SD, Lavigne JA, Berrigan D, Perkins SN, Barrett JC. Calorie restriction, aging, and cancer prevention: mechanisms of action and applicability to humans. Annu Rev Med 2003;54:131-52.
4. Patel AC, Nunez NP, Perkins SN, Barrett JC, Hursting SD. Effects of energy balance on cancer in genetically altered mice. J Nutr 2004;134:3394S-8S.
5. Yakar S, Nunez NP, Pennisi P, et al. Increased tumor growth in mice with diet-induced obesity: impact of ovarian hormones. Endocrinology 2006.
6. Birt DF, Pelling JC, White LT, Dimitroff K, Barnett T. Influence of diet and calorie restriction on the initiation and promotion of skin carcinogenesis in the SENCAR mouse model. Cancer Res 1991;51: 1851-4.
7. Birt DF, Pinch HJ, Barnett T, Phan A, Dimitroff K. Inhibition of skin tumor promotion by restriction of fat and carbohydrate calories in SENCAR mice. Cancer Res 1993;53:27-31.
8. Gillette CA, ZhuZ, Westerlind KC, Melby CL, Wolfe P, Thompson HJ. Energy availability and mammary carcinogenesis: effects of calorie restriction and exercise. Carcinogenesis 1997;18:1183-8.
9. Weber RV, Stein DE, Scholes J, Kral JG. Obesity potentiates AOM-induced colon cancer. Dig Dis Sci 2000;45:890-5.
10. Hirose Y, Hata K, Kuno T, et al. Enhancement of development of azoxymethane-induced colonic premalignant lesions in C57BL/KsJ-db/db mice. Carcinogenesis 2004;25:821-5.
11. Dogan S, HuX, Zhang Y, Maihle NJ, Grande JP, Cleary MP. Effects of high fat diet and/or body weight on mammary tumor leptin and apoptosis signaling pathways in MMTV-TGF-α mice. Breast Cancer Res 2007;9:R91.
12. Hursting SD, Lashinger LM, Colbert LH, et al. Energy balance and carcinogenesis: underlying pathways and targets for intervention. Curr Cancer Drug Targets 2007;7:484-91.
13. ZhuZ, Jiang W, McGinley J, Wolfe P, Thompson HJ. Effects of dietary energy repletion and IGF-1 infusion on the inhibition of mammary carcinogenesis by dietary energy restriction. Mol Carcinog 2005; 42:170-6.
14. Dunn SE, Kari FW, French J, et al. Dietary restriction reduces insulin-like growth factor I levels, which modulates apoptosis, cell proliferation, and tumor progression in p53-deficient mice. Cancer Res 1997;57:4667-72.
15. Hursting SD, Switzer BR, French JE, Kari FW. The growth hormone: insulin-like growth factor 1 axis is a mediator of diet restriction-induced inhibition of mononuclear cell leukemia in Fischer rats. Cancer Res 1993;53:2750-7.
16. Nunez NP, Oh WJ, Rozenberg J, et al. Accelerated tumor formation in a fatless mouse with type 2 diabetes and inflammation. Cancer Res 2006;66: 5469-76.
17. LeRoith D, Baserga R, Helman L, Roberts CT, Jr. Insulin-like growth factors and cancer. Ann Intern Med 1995;122:54-9.
18. Macaulay VM. Insulin-like growth factors and cancer. Br J Cancer 1992;65:311-20.
19. Yee D, Paik S, Lebovic GS, et al. Analysis of insulin-like growth factor I gene expression in malignancy: evidence for a paracrine role in human breast cancer. Mol Endocrinol 1989;3:509-17.
20. Tricoli JV, Rall LB, Karakousis CP, et al. Enhanced levels of insulin-like growth factor mRNA in human colon carcinomas and liposarcomas. Cancer Res 1986;46:6169-73.
21. Minuto F, Del Monte P, Barreca A, et al. Evidence for an increased somatomedin-C/insulin-like growth factor I content in primary human lung tumors. Cancer Res 1986;46:985-8.
22. Chan JM, Stampfer MJ, Giovannucci E, et al. Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 1998; 279:563-6.
23. Hankinson SE, Willett WC, Colditz GA, et al. Circulating concentrations of insulin-like growth factor-I and risk of breast cancer. Lancet 1998;351: 1393-6.
24. Adams TE, Epa VC, Garrett TP, Ward CW. Structure and function of the type 1 insulin-like growth factor receptor. Cell Mol Life Sci 2000; 57:1050-93.
25. Grimberg A, Cohen P. Role of insulin-like growth factors and their binding proteins in growth control and carcinogenesis. J Cell Physiol 2000;183:1-9.
26. DiGiovanni J, Bol DK, Wilker E, et al. Constitutive expression of insulin-like growth factor-1 in epidermal basal cells of transgenic mice leads to spontaneous tumor promotion. Cancer Res 2000;60: 1561-70.
27. Taniguchi CM, Emanuelli B, Kahn CR. Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 2006;7:85-96.
28. Wilker E, LuJ, Rho O, Carbajal S, Beltran L, Di-Giovanni J. Role of PI3K/Akt signaling in insulin-like growth factor-1 (IGF-1) skin tumor promotion. Mol Carcinog 2005;44:137-45.
29. Liscovitch M, Cantley LC. Lipid second messengers. Cell 1994;77:329-34.
30. Engelman JA, Luo J, Cantley LC. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 2006;7: 606-19.
31. Luo J, Manning BD, Cantley LC. Targeting the PI3K-Akt pathway in human cancer: rationale and promise. Cancer Cell 2003;4:257-62.
32. Shaw RJ, Cantley LC. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 2006; 441:424-30.
33. Vivanco I, Sawyers CL. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2002;2:489-501.
34. Wilker E, Bol D, Kiguchi K, Rupp T, Beltran L, Di-Giovanni J. Enhancement of susceptibility to diverse skin tumor promoters by activation of the insulin-like growth factor-1 receptor in the epidermis of transgenic mice. Mol Carcinog 1999;25: 122-31.
35. Segrelles C, Ruiz S, Perez P, et al. Functional roles of Akt signaling in mouse skin tumorigenesis. Oncogene 2002;21:53-64.
36. Segrelles C, LuJ, Hammann B, et al. Deregulated activity of Akt in basal cells of stratified epithelia induces spontaneous tumors and heightened sensitivity to skin carcinogenesis. Cancer Res 2007;67: 10879-88.
37. Lindsley JE, Rutter J. Nutrient sensing and metabolic decisions. Comp Biochem Physiol B Biochem Mol Biol 2004;139:543-59.
38. Martin TL, Alquier T, Asakura K, Furukawa N, Preitner F, Kahn BB. Diet-induced obesity alters AMP kinase activity in hypothalamus and skeletal muscle. J Biol Chem 2006;281:18933-41.
39. Hawley SA, Boudeau J, Reid JL, et al. Complexes between the LKB1 tumor suppressor, STRADα/β and MO25α/β are upstream kinases in the AMP-activated protein kinase cascade. J Biol 2003;2:28.
40. Hawley SA, Pan DA, Mustard KJ, et al. Calmodulin-dependent protein kinase kinase-β is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2005;2:9-19.
41. 2+/calmodulindependent protein kinase kinases are AMP-activated protein kinase kinases. J Biol Chem 2005; 280:29060-6.
42. Kahn BB, Alquier T, Carling D, Hardie DG. AMPactivated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 2005;1:15-25.
43. 2+/calmodulin- dependent protein kinase kinase-β acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2005;2:21-33.
44. Woods A, Johnstone SR, Dickerson K, et al. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 2003;13:2004-8.
45. Nunez N, Carpenter C, Berrigan D, et al. Extreme obesity reduces bone density in the absence of ovarian hormones: complimentary evidence from mice and women. Obesity 2007;15:1980-7.
46. Parekh PI, Petro AE, Tiller JM, Feinglos MN, Surwit RS. Reversal of diet-induced obesity and diabetes in C57BL/6J mice. Metabolism 1998;47: 1089-96.
47. Petro AE, Cotter J, Cooper DA, Peters JC, Surwit SJ, Surwit RS. Fat, carbohydrate, and calories in the development of diabetes and obesity in the C57BL/6J mouse. Metabolism 2004;53:454-7.
48. Van Heek M, Compton DS, France CF, et al. Dietinduced obese mice develop peripheral, but not central, resistance to leptin. J Clin Invest 1997;99: 385-90.
49. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-5.
50. WuY, Yakar S, Zhao L, Hennighausen L, LeRoith D. Circulating insulin-like growth factor-I levels regulate colon cancer growth and metastasis. Cancer Res 2002;62:1030-5.
51. Moore T, Carbajal S, Beltran L, et al. Reduced susceptibility to two-stage skin carcinogenesis in mice with low circulating IGF-1 levels. Cancer Res. In press 2008.
52. Wu Y, Cui K, Miyoshi K, et al. Reduced circulating insulin-like growth factor I levels delay the onset of chemically and genetically induced mammary tumors. Cancer Res 2003;63:4384-8.
53. Yakar S, LiuJL, Stannard B, et al. Normal growth and development in the absence of hepatic insulinlike growth factor I. Proc Natl Acad Sci U S A 1999; 96:7324-9.
54. Jiang W, ZhuZ, Bhatia N, Agarwal R, Thompson HJ. Mechanisms of energy restriction: effects of corticosterone on cell growth, cell cycle machinery, and apoptosis. Cancer Res 2002;62:5280-7.
55. ZhuZ, Jiang W, Thompson HJ. Effect of energy restriction on the expression of cyclin D1 and p27 during premalignant and malignant stages of chemically induced mammary carcinogenesis. Mol Carcinog 1999;24:241-5.
56. Gao N, Zhang Z, Jiang BH, Shi X. Role of PI3K/AKT/mTOR signaling in the cell cycle progression of human prostate cancer. Biochem Biophys Res Commun 2003;310:1124-32.
57. Gera JF, Mellinghoff IK, Shi Y, et al. AKT activity determines sensitivity to mammalian target of rapamycin (mTOR) inhibitors by regulating cyclin D1 and c-myc expression. J Biol Chem 2004;279:2737-46.
58. Averous J, Fonseca BD, Proud CG. Regulation of cyclin D1 expression by mTORC1 signaling requires eukaryotic initiation factor 4E-binding protein 1. Oncogene 2008;27:1106-13.
59. Fatrai S, Elghazi L, Balcazar N, et al. Akt induces β-cell proliferation by regulating cyclin D1, cyclin D2, and p21 levels and cyclin-dependent kinase-4 activity. Diabetes 2006;55:318-25.
60. Roberts PJ, Der CJ. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007;26:3291-310.
61. Scaltriti M, Baselga J. The epidermal growth factor receptor pathway: a model for targeted therapy. Clin Cancer Res 2006;12:5268-72.
62. Summy JM, Gallick GE. Treatment for advanced tumors: SRC reclaims center stage. Clin Cancer Res 2006;12:1398-401.
63. Yamamoto H, Ochiya T, Takeshita F, et al. Enhanced skin carcinogenesis in cyclin D1-conditional transgenic mice: cyclin D1 alters keratinocyte response to calcium-induced terminal differentiation. Cancer Res 2002;62:1641-7.
64. Robles AI, Larcher F, Whalin RB, et al. Expression of cyclin D1 in epithelial tissues of transgenic mice results in epidermal hyperproliferation and severe thymic hyperplasia. Proc Natl Acad Sci U S A 1996;93:7634-8.
65. Rodriguez-Puebla ML, LaCava M, Conti CJ. Cyclin D1 overexpression in mouse epidermis increases cyclin-dependent kinase activity and cell proliferation in vivo but does not affect skin tumor development. Cell Growth Differ 1999;10: 467-72.
66. Robles AI, Rodriguez-Puebla ML, Glick AB, et al. Reduced skin tumor development in cyclin D1-deficient mice highlights the oncogenic ras pathway in vivo. Genes Dev 1998;12:2469-74.
67. Gonzalez AA, Kumar R, Mulligan JD, Davis AJ, Weindruch R, Saupe KW. Metabolic adaptations to fasting and chronic caloric restriction in heart, muscle, and liver do not include changes in AMPK activity. Am J Physiol Endocrinol Metab 2004;287: E1032-7.
68. Bol DK, Kiguchi K, Gimenez-Conti I, Rupp T, DiGiovanni J. Overexpression of insulin-like growth factor-1 induces hyperplasia, dermal abnormalities, and spontaneous tumor formation in transgenic mice. Oncogene 1997;14: 1725-34.
69. Burgaud JL, Baserga R. Intracellular transactivation of the insulin-like growth factor I receptor by an epidermal growth factor receptor. Exp Cell Res 1996;223:412-9.
70. Desbois-Mouthon C, Cacheux W, Blivet-Van Eggelpoel MJ, et al. Impact of IGF-1R/EGFR cross-talks on hepatoma cell sensitivity to gefitinib. Int J Cancer 2006;119:2557-66.
71. El-Shewy HM, Kelly FL, Barki-Harrington L, Luttrell LM. Ectodomain shedding-dependent transactivation of epidermal growth factor receptors in response to insulin-like growth factor type I. Mol Endocrinol 2004;18:2727-39.
72. Krane JF, Murphy DP, Carter DM, Krueger JG. Synergistic effects of epidermal growth factor (EGF) and insulin-like growth factor I/somatomedin C (IGF-I) on keratinocyte proliferation may be mediated by IGF-I transmodulation of the EGF receptor. J Invest Dermatol 1991;96:419-24.
73. Roudabush FL, Pierce KL, Maudsley S, Khan KD, Luttrell LM. Transactivation of the EGF receptor mediates IGF-1-stimulated shc phosphorylation and ERK1/2 activation in COS-7 cells. J Biol Chem 2000;275:22583-9.
74. Birt DF, Yaktine A, Duysen E. Glucocorticoid mediation of dietary energy restriction inhibition of mouse skin carcinogenesis. J Nutr 1999;129: 571S-4S.
75. Birt DF, Przybyszewski J, Wang W, Stewart J, Liu Y. Identification of molecular targets for dietary energy restriction prevention of skin carcinogenesis: an idea cultivated by Edward Bresnick. J Cell Biochem 2004;91:258-64.
76. LiuY, Duysen E, Yaktine AL, AuA, Wang W, Birt DF. Dietary energy restriction inhibits ERK but not JNK or p38 activity in the epidermis of SENCAR mice. Carcinogenesis 2001;22: 607-12.
77. Xie L, Jiang Y, Ouyang P, et al. Effects of dietary calorie restriction or exercise on the PI3K and Ras signaling pathways in the skin of mice. J Biol Chem 2007;282:28025-35.