Estrogen protects against obesity-induced mammary gland inflammation in mice

Cancer Prevention Research

Volumn 8, Issue 8, 2015, Pages 751-759

  Bhardwaj, Priya ^a   Du, Baoheng ^a   Zhou, Kathy Xi ^a   Sue, Erika ^a   Giri, Dilip ^b   Harbus, Michael D ^a   Falcone, Domenick J ^a   Hudis, Clifford A ^a,b   Subbaramaiah, Kotha ^a   Dannenberg, Andrew J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; CYCLOOXYGENASE 2; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; FAT; INTERLEUKIN 1BETA; PLACEBO; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET INDUCED OBESITY; ESTROGEN THERAPY; FEMALE; HORMONAL THERAPY; LIPID DIET; MAMMARY GLAND; MASTITIS; MEDIATOR; MOUSE; NONHUMAN; OVARIECTOMY; OVARY; POSTMENOPAUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; WEIGHT GAIN; WEIGHT REDUCTION; WHITE ADIPOSE TISSUE; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; COMPLICATION; DRUG EFFECTS; GENETICS; METABOLISM; OBESITY; PATHOLOGY; PATHOPHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UDDER;

ANIMALS; DIET, HIGH-FAT; ESTROGENS; FEMALE; INFLAMMATION MEDIATORS; MAMMARY GLANDS, ANIMAL; MASTITIS; MICE; MICE, INBRED C57BL; OBESITY; OVARIECTOMY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; WEIGHT GAIN;

EID: 84942017434     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-15-0082     Document Type: Article

References (38)

1. Cleary MP, Grossmann ME. Minireview: obesity and breast cancer: the estrogen connection. Endocrinology 2009;150:2537-42.
2. van Kruijsdijk RC, van der Wall E, Visseren FL. Obesity and cancer: the role of dysfunctional adipose tissue. Cancer Epidemiol Biomarkers Prev 2009;18:2569-78.
3. 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.
4. Ewertz M, Jensen MB, Gunnarsdottir KA, Hojris I, Jakobsen EH, Nielsen D, et al. Effect of obesity on prognosis after early-stage breast cancer. J Clin Oncol 2011;29:25-31.
5. Rose DP, Vona-Davis L. Influence of obesity on breast cancer receptor status and prognosis. Expert Rev Anticancer Ther 2009;9:1091-101.
6. Lorincz AM, Sukumar S. Molecular links between obesity and breast cancer. Endocr Relat Cancer 2006;13:279-92.
7. Bulun SE, Lin Z, Imir G, Amin S, Demura M, Yilmaz B, et al. Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol Rev 2005;57:359-83.
8. Goss PE, Ingle JN, Ales-Martinez JE, Cheung AM, Chlebowski RT, Wactawski-Wende J, et al. Exemestane for breast-cancer prevention in postmenopausal women. N Engl J Med 2011;364:2381-91.
9. Key TJ, Appleby PN, Reeves GK, Roddam A, Dorgan JF, Longcope C, et al. Body mass index, serum sex hormones, and breast cancer risk in postmenopausal women. J Natl Cancer Inst 2003;95:1218-26.
10. LaCroix AZ, Chlebowski RT, Manson JE, Aragaki AK, Johnson KC, Martin L, et al. Health outcomes after stopping conjugated equine estrogens among postmenopausal women with prior hysterectomy: a randomized controlled trial. JAMA 2011;305:1305-14.
11. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E, et al. Adipocyte death defines macrophage localization and function inadipose tissue of obese mice and humans. J Lipid Res 2005;46:2347-55.
12. Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 2010;72:219-46.
13. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003;112:1796-808.
14. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, Kitazawa R, et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 2006;116:1494-505.
15. Amano SU, Cohen JL, Vangala P, Tencerova M, Nicoloro SM, Yawe JC, et al. Local proliferation of macrophages contributes to obesity-associated adipose tissue inflammation. Cell Metab 2014;19:162-71.
16. Subbaramaiah K, Howe LR, Bhardwaj P, Du B, Gravaghi C, Yantiss RK, et al. Obesity is associated with inflammation and elevated aromatase expression in the mouse mammary gland. Cancer Prev Res 2011;4:329-46.
17. Morris PG, Hudis CA, Giri D, Morrow M, Falcone DJ, Zhou XK, et al. Inflammation and increased aromatase expression occur in the breast tissue of obese women with breast cancer. Cancer Prev Res 2011;4:1021-9.
18. Subbaramaiah K, Morris PG, Zhou XK, Morrow M, Du B, Giri D, et al. Increased levels of COX-2 and prostaglandin E2 contribute to elevated aromatase expression in inflamed breast tissue of obese women. Cancer Discov 2012;2:356-65.
19. Iyengar NM, Morris PG, Zhou XK, Gucalp A, Giri D, Harbus MD, et al. Menopause is a determinant of breast adipose inflammation. Cancer Prev Res 2015;8:349-58.
20. Wing RR, Matthews KA, Kuller LH, Meilahn EN, Plantinga PL. Weight gain at the time of menopause. Arch Intern Med 1991;151:97-102.
21. Stubbins RE, Holcomb VB, Hong J, Nunez NP. Estrogen modulates abdominal adiposity and protects female mice from obesity and impaired glucose tolerance. Eur J Nutr 2012;51:861-70.
22. Bhardwaj P, Du B, Zhou XK, Sue E, Harbus MD, Falcone DJ, et al. Caloric restriction reverses obesity-induced mammary gland inflammation in mice. Cancer Prev Res 2013;6:282-9.
23. Subbaramaiah K, Hudis C, Chang SH, Hla T, Dannenberg AJ. EP2 and EP4 receptors regulate aromatase expression in human adipocytes and breast cancer cells. Evidence of a BRCA1 and p300 exchange. J Biol Chem 2008;283:3433-44.
24. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-75.
25. Karin M, Greten FR. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 2005;5:749-59.
26. Yonezawa R, Wada T, Matsumoto N, Morita M, Sawakawa K, Ishii Y, et al. Central versus peripheral impact of estradiol on the impaired glucose metabolism in ovariectomized mice on a high-fat diet. Am J Physiol Endocrinol Metab 2012;303:E445-56.
27. Stubbins RE, Najjar K, Holcomb VB, Hong J, Nunez NP. Oestrogen alters adipocyte biology and protects female mice from adipocyte inflammation and insulin resistance. Diabetes Obes Metab 2012;14:58-66.
28. Lovejoy JC, Champagne CM, de Jonge L, Xie H, Smith SR. Increased visceral fat and decreased energy expenditure during the menopausal transition. Int J Obes 2008;32:949-58.
29. Vegeto E, Ghisletti S, Meda C, Etteri S, Belcredito S, Maggi A. Regulation of the lipopolysaccharide signal transduction pathway by 17beta-estradiol in macrophage cells. J Steroid Biochem Mol Biol 2004;91:59-66.
30. Straub RH. The complex role of estrogens in inflammation. Endocr Rev 2007;28:521-74.
31. Ghisletti S, Meda C, Maggi A, Vegeto E. 17beta-estradiol inhibits inflammatory gene expression by controlling NF-kappaB intracellular localization. Mol Cell Biol 2005;25:2957-68.
32. Levin ER. Extranuclear estrogen receptor's roles in physiology: lessons from mouse models. Am J Physiol Endocrinol Metab 2014;307:E133-40.
33. Rogers NH, Perfield JW II, Strissel KJ, Obin MS, Greenberg AS. Reduced energy expenditure and increased inflammation are early events in the development of ovariectomy-induced obesity. Endocrinology 2009;150:2161-8.
34. Brown LM, Clegg DJ. Central effects of estradiol in the regulation of food intake, body weight, and adiposity. J Steroid Biochem Mol Biol 2010;122:65-73.
35. Barros RP, Gustafsson JA. Estrogen receptors and the metabolic network. Cell Metab 2011;14:289-99.
36. Musatov S, Chen W, Pfaff DW, Mobbs CV, Yang XJ, Clegg DJ, et al. Silencing of estrogen receptor alpha in the ventromedial nucleus of hypothalamus leads to metabolic syndrome. Proc Natl Acad Sci U S A 2007;104:2501-6.
37. Finan B, Yang B, Ottaway N, Stemmer K, Muller TD, Yi CX, et al. Targeted estrogen delivery reverses the metabolic syndrome. Nat Med 2012;18:1847-56.
38. Howe LR, Subbaramaiah K, Hudis CA, Dannenberg AJ. Molecular pathways: adipose inflammation as a mediator of obesity-associated cancer. Clin Cancer Res 2013;19:6074-83.