Metabolic obesity, adipose inflammation and elevated breast aromatase in women with normal body mass index

Cancer Prevention Research

Volumn 10, Issue 4, 2017, Pages 235-243

  Iyengar, Neil M ^a,b   Brown, Kristy A ^c,d   Zhou, Xi Kathy ^b   Gucalp, Ayca ^a,b   Subbaramaiah, Kotha ^b   Giri, Dilip D ^a   Zahid, Heba ^c,e   Bhardwaj, Priya ^b   Wendel, Nils K ^b   Falcone, Domenick J ^b   Wang, Hanhan ^b   Williams, Samantha ^a   Pollak, Michael ^f   Morrow, Monica ^a   Hudis, Clifford A ^a,b   Dannenberg, Andrew J ^b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d MONASH UNIVERSITY   (Australia)

^e TAIBAH UNIVERSITY   (Saudi Arabia)

^f MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; C REACTIVE PROTEIN; INSULIN; LEPTIN; TRIACYLGLYCEROL; CYP19A1 PROTEIN, HUMAN;

ADIPOCYTE; ADULT; ARTICLE; BLOOD SAMPLING; BODY MASS; BODY WEIGHT; BREAST; BREAST CANCER; CANCER PATIENT; CANCER SURGERY; CELL DEATH; CELL SIZE; CONTROLLED STUDY; DIET RESTRICTION; DISEASE ASSOCIATION; DISEASE SEVERITY; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; INSULIN BLOOD LEVEL; MACROPHAGE; MAJOR CLINICAL STUDY; MASTECTOMY; METABOLIC DISORDER; MIDDLE AGED; OBESITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RISK FACTOR; RISK REDUCTION; TRIACYLGLYCEROL BLOOD LEVEL; TRIPLE NEGATIVE BREAST CANCER; WHITE ADIPOSE TISSUE; BIOSYNTHESIS; BREAST TUMOR; ENZYMOLOGY; PATHOLOGY;

ADIPOSE TISSUE, WHITE; ADULT; AROMATASE; BODY MASS INDEX; BREAST NEOPLASMS; FEMALE; HUMANS; INFLAMMATION; MIDDLE AGED;

EID: 85017509727     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-16-0314     Document Type: Article

References (50)

1. Trentham-Dietz A, Newcomb PA, Storer BE, Longnecker MP, Baron J, Greenberg ER, et al. Body size and risk of breast cancer. Am J Epidemiol 1997;145:1011-9.
2. Iyengar NM, Hudis CA, Dannenberg AJ. Obesity and cancer: local and systemic mechanisms. Annu Rev Med 2015;66:297-309.
3. Calle EE, Rodriguez C, Walker-Thurmond K, ThunMJ. 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. ProtaniM, CooryM, Martin JH. Effect of obesity on survival of womenwith breast cancer: systematic review andmeta-analysis. Breast Cancer Res Treat 2010;2010:23.
6. Sparano JA, Zhao F, Martino S, Ligibel JA, Perez EA, Saphner T, et al. Longterm follow-up of the E1199 phase III trial evaluating the role of taxane and schedule in operable breast cancer. J Clin Oncol 2015;33:2353-60.
7. 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 (Phila) 2011;4:1021-9.
8. 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.
9. 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 (Phila) 2015;8:349-58.
10. Iyengar NM, Zhou XK, Gucalp A, Morris PG, Howe LR, Giri DD, et al. Systemic correlates of white adipose tissue inflammation in early-stage breast cancer. Clin Cancer Res 2016;22:2283-9.
11. Koru-Sengul T, Santander AM, Miao F, Sanchez LG, Jorda M, Gluck S, et al. Breast cancers from black women exhibit higher numbers of immunosuppressive macrophages with proliferative activity and of crown-like structures associated with lower survival compared to non-black Latinas and Caucasians. Breast Cancer Res Treat 2016;158:113-26.
12. Sun X, Casbas-Hernandez P, Bigelow C, Makowski L, Joseph Jerry D, Smith Schneider S, et al. Normal breast tissue of obese women is enriched for macrophage markers and macrophage-associated gene expression. Breast Cancer Res Treat 2012;131:1003-12.
13. Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 2010;72:219-46.
14. Rosen ED, Spiegelman BM. Whatwe talk about whenwe talk about fat. Cell 2014;156:20-44.
15. Monteiro R, Azevedo I. Chronic inflammation in obesity and the metabolic syndrome. Mediators Inflamm 2010;2010. pii: 289645.
16. Berrino F, Villarini A, Traina A, Bonanni B, Panico S, Mano MP, et al. Metabolic syndrome and breast cancer prognosis. Breast Cancer Res Treat 2014;147:159-65.
17. Goodwin PJ, Ennis M, Pritchard KI, Trudeau ME, Koo J, Madarnas Y, et al. Fasting insulin and outcome in early-stage breast cancer: results of a prospective cohort study. J Clin Oncol 2002;20:42-51.
18. Duggan C, Irwin ML, Xiao L, Henderson KD, Smith AW, Baumgartner RN, et al. Associations of insulin resistance and adiponectin with mortality in women with breast cancer. J Clin Oncol 2011;29:32-9.
19. Gunter MJ, Wang T, Cushman M, Xue X, Wassertheil-Smoller S, Strickler HD, et al. Circulating adipokines and inflammatory markers and postmenopausal breast cancer risk. J Natl Cancer Inst 2015;107. pii: djv169.
20. Gunter MJ, Xie X, Xue X, Kabat GC, Rohan TE, Wassertheil-Smoller S, et al. Breast cancer risk in metabolically healthy but overweight postmenopausal women. Cancer Res 2015;75:270-4.
21. Erickson K, Patterson RE, Flatt SW, Natarajan L, Parker BA, Heath DD, et al. Clinically defined type 2 diabetes mellitus and prognosis in early-stage breast cancer. J Clin Oncol 2011;29:54-60.
22. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: A joint interim statement of the International Diabetes federation task force on epidemiology and prevention; national heart, lung, and blood institute; american heart association; world heart federation; international atherosclerosis society; and international association for the study of obesity. Circulation 2009;120:1640-5.
23. Campbell KL, Foster-Schubert KE, Alfano CM, Wang CC, Wang CY, Duggan CR, et al. Reduced-calorie dietary weight loss, exercise, and sex hormones in postmenopausal women: randomized controlled trial. J Clin Oncol 2012;30:2314-26.
24. Demark-Wahnefried W, Morey MC, Sloane R, Snyder DC, Miller PE, Hartman TJ, et al. Reach out to enhance wellness home-based diet-exercise intervention promotes reproducible and sustainable long-term improvements in health behaviors, body weight, and physical functioning in older, overweight/obese cancer survivors. J Clin Oncol 2012;30:2354-61.
25. Chlebowski RT, Blackburn GL, Thomson CA, Nixon DW, Shapiro A, Hoy MK, et al. Dietary fat reduction and breast cancer outcome: interim efficacy results from the Women's Intervention Nutrition Study. J Natl Cancer Inst 2006;98:1767-76.
26. Pierce JP, Natarajan L, Caan BJ, Parker BA, Greenberg ER, Flatt SW, et al. Influence of a diet very high in vegetables, fruit, and fiber and low in fat on prognosis following treatment for breast cancer: The Women's Healthy Eating and Living (WHEL) randomized trial. JAMA 2007;298:289-98.
27. Garwood ER, Kumar AS, Baehner FL, Moore DH, Au A, Hylton N, et al. Fluvastatin reduces proliferation and increases apoptosis in women with high grade breast cancer. Breast Cancer Res Treat 2010;119:137-44.
28. Higgins MJ, Prowell TM, Blackford AL, Byrne C, Khouri NF, Slater SA, et al. A short-term biomarker modulation study of simvastatin in women at increased risk of a new breast cancer. Breast Cancer Res Treat 2012;131: 915-24.
29. Jiralerspong S, Palla SL, Giordano SH, Meric-Bernstam F, Liedtke C, Barnett CM, et al. Metformin and pathologic complete responses to neoadjuvant chemotherapy in diabetic patients with breast cancer. J Clin Oncol 2009;27:3297-302.
30. Goodwin PJ, Parulekar WR, Gelmon KA, Shepherd LE, Ligibel JA, Hershman DL, et al. Effect of metformin vs placebo on weight and metabolic factors in NCIC CTG MA. 32. J Natl Cancer Inst 2015;107. pii: djv006.
31. Chen S, Chen Y, Liu X, Li M, Wu B, Li Y, et al. Insulin resistance and metabolic syndrome in normal-weight individuals. Endocrine 2014;46: 496-504.
32. Deepa M, Papita M, Nazir A, Anjana RM, Ali MK, Narayan KM, et al. Lean people with dysglycemia have a worse metabolic profile than centrally obese people without dysglycemia. Diabetes Technol Ther 2014;16:91-6.
33. Ruderman N, Chisholm D, Pi-Sunyer X, Schneider S. The metabolically obese, normal-weight individual revisited. Diabetes 1998;47:699-713.
34. St-Onge MP, Janssen I, Heymsfield SB. Metabolic syndrome in normalweight Americans: new definition of the metabolically obese, normalweight individual. Diabetes Care 2004;27:2222-8.
35. Tomiyama AJ, Hunger JM, Nguyen-Cuu J, Wells C. Misclassification of cardiometabolic health when using body mass index categories in NHANES 2005-2012. Int J Obes (Lond) 2016;40:883-6.
36. NCCN. NCCN Clinical Practice Guidelines in Oncology v. 2. 2011; 2011[cited December 5, 2016]. Available from: www. nccn. org.
37. Wolff AC, HammondME, Hicks DG, Dowsett M, McShane LM, Allison KH, et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. J Clin Oncol 2013;31:3997-4013.
38. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E, et al. Adipocyte death definesmacrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 2005;46:2347-55.
39. 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.
40. Sasano H, Edwards DP, Anderson TJ, Silverberg SG, Evans DB, Santen RJ, et al. Validation of new aromatase monoclonal antibodies for immunohistochemistry: progress report. J Steroid Biochem Mol Biol 2003;86:239-44.
41. Wang X, Docanto MM, Sasano H; kConFab, Lo C, Simpson ER, et al. Prostaglandin E2 inhibits p53 in human breast adipose stromal cells: A novel mechanism for the regulation of aromatase in obesity and breast cancer. Cancer Res 2015;75:645-55.
42. Moreno-Indias I, Oliva-Olivera W, Omiste A, Castellano-Castillo D, Lhamyani S, Camargo A, et al. Adipose tissue infiltration in normalweight subjects and its impact on metabolic function. Transl Res 2016;172:6-17. e3.
43. Zhao Y, Agarwal VR, Mendelson CR, Simpson ER. Estrogen biosynthesis proximal to a breast tumor is stimulated by PGE2 via cyclic AMP, leading to activation of promoter II of the CYP19 (aromatase) gene. Endocrinology 1996;137:5739-42.
44. Brown KA, McInnes KJ, Hunger NI, Oakhill JS, Steinberg GR, Simpson ER. Subcellular localization of cyclic AMP-responsive element binding proteinregulated transcription coactivator 2 provides a link between obesity and breast cancer in postmenopausal women. Cancer Res 2009;69:5392-9.
45. Chang CC, Wu MJ, Yang JY, Camarillo IG, Chang CJ. Leptin-STAT3-G9a signaling promotes obesity-mediated breast cancer progression. Cancer Res 2015;75:2375-86.
46. Friedman JM, Halaas JL. Leptin and the regulation of body weight in mammals. Nature 1998;395:763-70.
47. Iyengar NM, Ghossein RA, Morris LG, Zhou XK, Kochhar A, Morris PG, et al. White adipose tissue inflammation and cancer-specific survival in patients with squamous cell carcinoma of the oral tongue. Cancer 2016;122:3794-802.
48. Gallagher EJ, LeRoith D. The proliferating role of insulin and insulin-like growth factors in cancer. Trends Endocrinol Metab 2010;21:610-8.
49. Belardi V, Gallagher EJ, Novosyadlyy R, LeRoith D. Insulin and IGFs in obesity-related breast cancer. J Mammary Gland Biol Neoplasia 2013; 18:277-89.
50. Novosyadlyy R, Lann DE, Vijayakumar A, Rowzee A, Lazzarino DA, Fierz Y, et al. Insulin-mediated acceleration of breast cancer development and progression in a nonobese model of type 2 diabetes. Cancer Res 2010;70:741-51.