Sex differences in obesity-induced hypertension and vascular dysfunction: A protective role for estrogen in adipose tissue inflammation?

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 311, Issue 4, 2016, Pages R714-R720

  Taylor, Lia E ^a   Sullivan, Jennifer C ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Adipose tissue; Fat; Females; Hypertension; Obesity; Vascular dysfunction

Indexed keywords

CYTOKINE; ESTROGEN;

ADIPOCYTE; ADIPOSE TISSUE; FAT INTAKE; HUMAN; HYPERTENSION; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INFLAMMATION; LIPID DIET; MACROPHAGE; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; T LYMPHOCYTE; VASCULAR DISEASE; ANIMAL; COMPLICATION; IMMUNOLOGY; PANNICULITIS; VASCULAR DISEASES;

ADIPOSE TISSUE; ANIMALS; ESTROGENS; HUMANS; HYPERTENSION; OBESITY; PANNICULITIS; SEX FACTORS; VASCULAR DISEASES;

EID: 84990909750     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00202.2016     Document Type: Review

References (64)

1. Amengual-Cladera E, Llado I, Gianotti M, Proenza AM. Sex differences in the effect of high-fat diet feeding on rat white adipose tissue mitochondrial function and insulin sensitivity. Metabolism 61: 1108-1117, 2012
2. Bhattacharya I, Dragert K, Albert V, Contassot E, Damjanovic M, Hagiwara A, Zimmerli L, Humar R, Hall MN, Battegay EJ, Haas E. Rictor in perivascular adipose tissue controls vascular function by regulating inflammatory molecule expression. Arterioscler Thromb 33: 2105-2111, 2013
3. Bolego C, Cignarella A, Staels B, Chinetti-Gbaguidi G. Macrophage function and polarization in cardiovascular disease: a role of estrogen signaling? Arterioscler Thromb Vasc Biol 33: 1127-1134, 2013
4. Bottner A, Kratzsch J, Muller G, Kapellen TM, Bluher S, Keller E, Bluher M, Kiess W. Gender differences of adiponectin levels develop during the progression of puberty and are related to serum androgen levels. J Clin Endocrinol Metab 89: 4053-4061, 2004
5. Brinson KN, Rafikova O, Sullivan JC. Female sex hormones protect against salt-sensitive hypertension but not essential hypertension. Am J Physiol Regul Integr Comp Physiol 307: R149-R157, 2014
6. Britton KA, Fox CS. Ectopic fat depots and cardiovascular disease. Circulation 124: e837-e841, 2011
7. Chatterjee TK, Stoll LL, Denning GM, Harrelson A, Blomkalns AL, Idelman G, Rothenberg FG, Neltner B, Romig-Martin SA, Dickson EW, Rudich S, Weintraub NL. Proinflammatory phenotype of perivascular adipocytes influence of high-fat feeding. Circ Res 104: 541-U237, 2009
8. Dalpiaz PL, Lamas AZ, Caliman IF, Ribeiro RF Jr. Abreu GR, Moyses MR, Andrade TU, Gouvea SA, Alves MF, Carmona AK, Bissoli NS. Sex hormones promote opposite effects on ACE and ACE2 activity, hypertrophy and cardiac contractility in spontaneously hypertensive rats. Plos One 10: e0127515, 2015
9. Davis KE, MDN, Sun K, WMS, JDB, JAZ, Zeve D, LDH, DWC, LMG, Xu Y, ZVW, SAK, Clegg DJ. The sexually dimorphic role of adipose and adipocyte estrogen receptors in modulating adipose tissue expansion, inflammation, and fibrosis. Mol Metab 2: 227-242, 2013
10. Davis SK, Gebreab SY, Xu RH, Riestra P, Khan RJ, Sumner AE, Hickson D, Bidulescu A. Association of adiponectin with type 2 diabetes and hypertension in African American men and women: the Jackson Heart Study. BMC Cardiovasc Disord 15: 13, 2015
11. De Ciuceis C, Amiri F, Brassard P, Endemann DH, Touyz RM, Schiffrin EL. Reduced vascular remodeling, endothelial dysfunction, and oxidative stress in resistance arteries of angiotensin II-infused macrophage colony-stimulating factor-deficient mice. Evidence for a role in inflammation in angiotensin-induced vascular injury. Arterioscler Thromb Vasc Biol 25: 2106-2113, 2005
12. Dinh QN, Drummond GR, Sobey CG, Chrissobolis S. Roles of inflammation, oxidative stress, and vascular dysfunction in hypertension. Biomed Res Int 2014: 406960, 2014
13. Durand JL, Nawrocki AR, Scherer PE, Jelicks LA. Gender differences in adiponectin modulation of cardiac remodeling in mice deficient in endothelial nitric oxide synthase. J Cell Biochem 113: 3276-3287, 2012
14. El Akoum S, Lamontagne V, Cloutier I, Tanguay JF. Nature of fatty acids in high fat diets differentially delineates obesity-linked metabolic syndrome components in male and female C57BL/6J mice. Diabetol Metab Syndr 3: 34, 2011
15. Elmarakby AA, Quigley JE, Pollock DM, Imig JD. Tumor necrosis factor alpha blockade increases renal cyp2c23 expression and slows the progression of renal damage in salt-sensitive hypertension. Hypertension 47: 557-562, 2006
16. Ferrer B, Navia B, Giralt M, Comes G, Carrasco J, Molinero A, Quintana A, Senaris RM, Hidalgo J. Muscle-specific interleukin-6 deletion influences body weight and body fat in a sex-dependent manner. Brain Behav Immun 40: 121-130, 2014
17. Ganz M, Csak T, Szabo G. High-fat diet feeding results in gender specific steatohepatitis and inflammasome activation. World J Gastroenterol 20: 8525-8534, 2014
18. Gorres BK, Bomhoff GL, Gupte AA, Geiger PC. Altered estrogen receptor expression in skeletal muscle and adipose tissue of female rats fed a high-fat diet. J Appl Physiol 110: 1046-1053, 2011
19. Greenstein AS, Khavandi K, Withers SB, Sonoyama K, Clancy O, Jeziorska M, Laing I, Yates AP, Pemberton PW, Malik RA, Heagerty AM. Local inflammation and hypoxia abolish the protective anticontractile properties of perivascular fat in obese patients. Circulation 119: 1661-U1166, 2009
20. Gui Y, Silha JV, Murphy LJ. Sexual dimorphism and regulation of resistin, adiponectin, and leptin expression in the mouse. Obes Res 12: 1481-1491, 2004
21. Gupte M, Thatcher SE, Boustany-Kari CM, Shoemaker R, Yiannikouris F, Zhang X, Karounos M, Cassis LA. Angiotensin-converting enzyme 2 contributes to sex differences in the development of obesity hypertension in C57BL/6 mice. Arterioscler Thromb Vasc Biol 32: 1392-1399, 2012
22. Gurgen D, Kusch A, Klewitz R, Hoff U, Catar R, Hegner B, Kintscher U, Luft FC, Dragun D. Sex-specific mTOR signaling determines sexual dimorphism in myocardial adaptation in normotensive DOCA-salt model. Hypertension 61: 730-736, 2013
23. Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, Goronzy J, Weyand C, Harrison DG. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 204: 2449-2460, 2007
24. Hall JE, do Carmo JM, da Silva AA, Wang Z, Hall ME. Obesityinduced hypertension interaction of neurohumoral and renal mechanisms. Circ Res 116: 991-1006, 2015
25. Ji H, Zheng W, Li X, Liu J, Wu X, Zhang MA, Umans JG, Hay M, Speth RC, Dunn SE, Sandberg K. Sex-specific T-cell regulation of angiotensin II-dependent hypertension. Hypertension 64: 573-582, 2014
26. Kamari Y, Peleg E, Leibowitz A, Grossman E. Blunted blood pressure response and elevated plasma adiponectin levels in female SpragueDawley rats. Am J Hypertens 25: 612-619, 2012
27. Khan D, Ahmed SA. The immune system is a natural target for estrogen action: opposing effects of estrogen in two prototypical autoimmune diseases. Front Immunol 6, 635, 2016
28. Khera A, Vega GL, Das SR, Ayers C, McGuire DK, Grundy SM, de Lemos JA. Sex differences in the relationship between C-reactive protein and body fat. J Clin Endocrinol Metab 94: 3251-3258, 2009
29. Ko EA, Amiri F, Pandey NR, Javeshghani D, Leibovitz E, Touyz RM, Schiffrin EL. Resistance artery remodeling in deoxycorticosterone acetate-salt hypertension is dependent on vascular inflammation: evidence from m-CSF-deficient mice. Am J Physiol Heart Circ Physiol 292: H1789-H1795, 2007
30. Lakoski SG, Cushman M, Siscovick D, Blumenthal RS, Burke G, Palmas W, Herrington D. The relationship between inflammation, obesity, and risk for hypertension in the Multi-Ethnic Study of Atherosclerosis (MESA). Circulation 116: 801-801, 2007
31. Litwak SA, Wilson JL, Chen WY, Garcia-Rudaz C, Khaksari M, Cowley MA, Enriori PJ. Estradiol prevents fat accumulation and overcomes leptin resistance in female high-fat diet mice. Endocrinology 155: 4447-4460, 2014
32. Luckheeram RV, Zhou R, Verma AD, Xia B. CD4()T cells: differentiation and functions. Clin Dev Immunol 2012: 925135, 2012
33. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117: 175-184, 2007
34. Ma LQ, Ma ST, He HB, Yang DC, Chen XP, Luo ZD, Liu DY, Zhu ZM. Perivascular fat-mediated vascular dysfunction and remodeling through the AMPK/mTOR pathway in high-fat diet-induced obese rats. Hypertens Res 33: 446-453, 2010
35. Miller CN, Brown LM, Rayalam S, Della-Fera MA, Baile CA. Estrogens, inflammation and obesity: an overview. Front Biol 7: 40-47, 2012
36. Mozaffarian D. Heart disease and stroke statistics-2015 update: a report from the American Heart Association (vol 131, pg e29, 2015). Circulation 131: E535-E535, 2015
37. Mraz M, Haluzik M. The role of adipose tissue immune cells in obesity and low-grade inflammation. J Endocrinol 222: R113-R127, 2014
38. Navia B, Ferrer B, Giralt M, Comes G, Carrasco J, Molinero A, Quintana A, Leclerc J, Viollet B, Senaris RM, Hidalgo J. Interleukin-6 deletion in mice driven by aP2-Cre-ERT2 prevents against high-fat dietinduced gain weight and adiposity in female mice. Acta Physiol (Oxf) 211: 585-596, 2014
39. Nguyen NT, Magno CP, Lane KT, Hinojosa MW, Lane JS. Association of hypertension, diabetes, dyslipidemia, and metabolic syndrome with obesity: findings from the National Health and Nutrition Examination Survey, 1999 to 2004. J Am Coll Surg 207: 928-934, 2008
40. Nishimura S., Manabe I., Nagasaki M., Eto K., Yamashita H., Ohsugi M., Otsu M, Hara K, Ueki K, Sugiura S, Yoshimura K, Kadowaki T, Nagai R. CD8 effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 15: 914-U116, 2009
41. Ogden CL, Carroll MD, Fryar CD, Flegal KM. Prevalence of obesity among adults and youth: United States, 2011-2014. NCHS Data Brief 1-8, 2015
42. Ohashi K, Kihara S, Ouchi N, Kumada M, Fujita K, Hiuge A, Hibuse T, Ryo M, Nishizawa H, Maeda N, Maeda K, Shibata R, Walsh K, Funahashi T, Shimomura I. Adiponectin replenishment ameliorates obesity-related hypertension. Hypertension 47: 1108-1116, 2006
43. Passos-Silva DG, Verano-Braga T, Santos RA. Angiotensin-(1-7): beyond the cardio-renal actions. Clin Sci (Lond) 124: 443-456, 2013
44. Pausova Z, Mahboubi A, Abrahamowicz M, Leonard GT, Perron M, Richer L, Veillette S, Gaudet D, Paus T. Sex differences in the contributions of visceral and total body fat to blood pressure in adolescence. Hypertension 59: 572-U113, 2012
45. Pettersson US, Walden TB, Carlsson PO, Jansson L, Phillipson M. Female mice are protected against high-fat diet induced metabolic syndrome and increase the regulatory T cell population in adipose tissue. Plos One 7, 2012
46. Pitsavos C, Chrysohoou C, Panagiotakos DB, Lentzas Y, Stefanadis C. Abdominal obesity and inflammation predicts hypertension among prehypertensive men and women: the ATTICA Study. Heart Vessels 23: 96-103, 2008
47. Ribot J, Rodriguez AM, Rodriguez E, Palou A. Adiponectin and resistin response in the onset of obesity in male and female rats. Obesity (Silver Spring) 16: 723-730, 2008
48. Schiffrin EL. Immune mechanisms in hypertension and vascular injury. Clin Sci (Lond) 126: 267-274, 2014
49. Shen M, Kumar SP, Shi H. Estradiol regulates insulin signaling and inflammation in adipose tissue. Horm Mol Biol Clin Invest 17: 99-107, 2014
50. Shim IK, Cho KI, Kim HS, Heo JH, Cha TJ. Impact of gender on the association of epicardial fat thickness, obesity, and circadian blood pressure pattern in hypertensive patients. J Diabetes Res 924539, 10 pages, 2015
51. Spradley FT, De Miguel C, Hobbs J, Pollock DM, Pollock JS. Mycophenolate mofetil prevents high-fat diet-induced hypertension and renal glomerular injury in Dahl SS rats. Physiol Rep 1: e00137, 2013
52. Sullivan JC, Bhatia K, Yamamoto T, Elmarakby AA. Angiotensin (1-7) receptor antagonism equalizes angiotensin II-induced hypertension in male and female spontaneously hypertensive rats. Hypertension 56: 658-666, 2010
53. Sullivan JC, Semprun-Prieto L, Boesen EI, Pollock DM, Pollock JS. Sex and sex hormones influence the development of albuminuria and renal macrophage infiltration in spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 293: R1573-R1579, 2007
54. Szasz T, Webb RC. Perivascular adipose tissue: more than just structural support. Clin Sci 122: 1-12, 2012
55. Thomas-Moya E, Gianotti M, Proenza AM, Llado I. Paraoxonase 1 response to a high-fat diet: gender differences in the factors involved. Mol Med 13: 203-209, 2007
56. Tipton AJ, Baban B, Sullivan JC. Female spontaneously hypertensive rats have a compensatory increase in renal regulatory T cells in response to elevations in blood pressure. Hypertension 64: 557-564, 2014
57. Tipton AJ, Sullivan JC. Sex differences in T cells in hypertension. Clin Ther 36: 1882-1900, 2014
58. Venegas-Pont M, Manigrasso MB, Grifoni SC, LaMarca BB, Maric C, Racusen LC, Glover PH, Jones AV, Drummond HA, Ryan MJ. Tumor necrosis factorantagonist etanercept decreases blood pressure and protects the kidney in a mouse model of systemic lupus erythematosus. Hypertension 56: 643-649, 2010
59. Wang D, Wang C, Wu X, Zheng W, Sandberg K, Ji H, Welch WJ, Wilcox CS. Endothelial dysfunction and enhanced contractility in microvessels from ovariectomized rats roles of oxidative stress and perivascular adipose tissue. Hypertension 63: 1063-1069, 2014
60. Wang Y, Shoemaker R, Thatcher SE, Batifoulier-Yiannikouris F, English VL, Cassis LA. Administration of 17-estradiol to ovariectomized obese female mice reverses obesity-hypertension through an ACE2dependent mechanism. Am J Physiol Endocrinol Metab 308: E1066-E1075, 2015
61. Wang ZV, Scherer PE. Adiponectin, cardiovascular function, and hypertension. Hypertension 51: 8-14, 2008
62. Winer S, Chan Y, Paltser G, Truong D, Tsui H, Bahrami J, Dorfman R, Wang YQ, Zielenski J, Mastronardi F, Maezawa Y, Drucker DJ, Engleman E, Winer D, Dosch HM. Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 15: 921-U126, 2009
63. Xu JM, Shi GP. Emerging role of mast cells and macrophages in cardiovascular and metabolic diseases. Endocr Rev 33: 71-108, 2012
64. Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K, Mori Y, Ide T, Murakami K, Tsuboyama-Kasaoka N, Ezaki O, Akanuma Y, Gavrilova O, Vinson C, Reitman ML, Kagechika H, Shudo K, Yoda M, Nakano Y, Tobe K, Nagai R, Kimura S, Tomita M, Froguel P, Kadowaki T. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med 7: 941-946, 2001