CC BY 4.0 · Journal of Health and Allied Sciences NU 2024; 14(01): 071-077
DOI: 10.1055/s-0043-1762581
Original Article

Aerobic Exercise Modulates Visceral Adipose Tissue of Estrogen Deprived Rats in an Experimental Model of Dyslipidemia

Walkyria Villegas Magalhães
1   Laboratory of Morphological and Immunohistochemical Studies, Department of Physical Education, São Judas Tadeu University located at Rua Taquari, Mooca, São Paulo, Brazil
,
Kemily Loren Barros Chucata
1   Laboratory of Morphological and Immunohistochemical Studies, Department of Physical Education, São Judas Tadeu University located at Rua Taquari, Mooca, São Paulo, Brazil
,
Nuha Ahmad Dsouki
2   Department of Morphology and Physiology of the ABC District Medical School located at Av. Lauro Gomes, Vila Sacadura Cabral, Santo André, Brazil
,
1   Laboratory of Morphological and Immunohistochemical Studies, Department of Physical Education, São Judas Tadeu University located at Rua Taquari, Mooca, São Paulo, Brazil
3   Department of Pathology, University of São Paulo Medical School located at Av. Dr. Arnaldo, Cerqueira César, São Paulo, Brazil
,
4   Department of Morphology of Oswaldo Cruz School located at Rua Brigadeiro Galvão, Barra Funda, São Paulo, Brazil
,
Fernando Luiz Affonso Fonseca
5   Laboratory of Clinical Analysis of the ABC District Medical School located at Av. Lauro Gomes, Vila Sacadura Cabral, Santo André, Brazil
6   Department of Pharmaceutical Sciences of the Federal University of São Paulo (UNIFESP) located at Rua Sena Madureira, Vila Clementino, São Paulo, Brazil
,
5   Laboratory of Clinical Analysis of the ABC District Medical School located at Av. Lauro Gomes, Vila Sacadura Cabral, Santo André, Brazil
7   Dante Pazzanese Institute of Cardiology located at Av. Dr. Dante Pazzanese, Vila Mariana, São Paulo, Brazil
› Author Affiliations
Funding None.

Abstract

Introduction Menopausal women have an increase deposition of body fat and changes in the lipid profile, being especially susceptible to cardiovascular diseases, and type 2 diabetes. However, physical activity can mitigate this situation. Thus, the aim of the present study is to evaluate the effects of moderate aerobic exercise on visceral adipose tissue (VAT) of female LDL-receptor knockout ovariectomized mice. Methods We used 48 animals, divided into six groups (n = 8/per group): sedentary control (SC), sedentary ovariectomized control (SCO), trained ovariectomized control (TCO), sedentary non-ovariectomized LDL-receptor knockout (KS), sedentary ovariectomized LDL-receptor knockout (KOS), and trained LDL-receptor knockout ovariectomized (KOT). We analyzed the VAT through morphometric and stereological parameters in hematoxylin and eosin stained sections. Additionally, we evaluated biochemical parameters as glucose, triglycerides, and total cholesterol. Finally, immunohistochemical techniques for matrix remodeling, inflammation, apoptosis, and oxidative stress were evaluated. Results We observed that menopause is related to increased visceral adiposity, inflammation, oxidative stress, macrophages activity, serum levels of glucose, triglycerides, and total cholesterol. However, exercise was effective in reducing these parameters, as well as being associated with increased vascularization of VAT and interstitial volume density. Conclusions Moderate exercise is a key factor in mitigating the effects of dyslipidemia in estrogen deprivation. However, further studies are needed to corroborate with our findings.

Availability of Data and Materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.


Authors' contributions

W.V.M. Investigation, writing-review and editing.


K.L.B.C. Investigation, writing-review and editing.


N.A.D. Investigation, writing-review and editing.


R.A.B.N. Data curation, formal analysis, visualization, writing-review and editing.


A.G.B.V. Investigation, writing-review and editing.


F.L.A.F. Resources, supervision, validation, writing-original draft.


L.B.M.M. Conceptualization, methodology, project administration, writing-original draft.




Publication History

Article published online:
14 April 2023

© 2023. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

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  • References

  • 1 Brianezi L, Marques M, Cardoso CG, Miranda MLdJ, Fonseca FLA, Maifrino LB. Effects of physical training on the myocardium of female ldl knockout ovariectomized mice. Rev Bras Med Esp 2017; 23 (06) 441-445
  • 2 Burns RA, French D, Luszcz M, Kendig HL, Anstey KJ. Heterogeneity in the health and functional capacity of adults aged 85+ as risk for mortality. J Am Geriatr Soc 2019; 67 (05) 1036-1042
  • 3 Naser B, Castelo-Branco C, Meden H. et al. Weight gain in menopause: systematic review of adverse events in women treated with black cohosh. Climacteric 2022; 25 (03) 220-227
  • 4 Alvarez MS, Fernandez-Alvarez A, Cucarella C, Casado M. Stable SREBP-1a knockdown decreases the cell proliferation rate in human preadipocyte cells without inducing senescence. Biochem Biophys Res Commun 2014; 447 (01) 51-56
  • 5 Schaffer JE. Lipotoxicity: many roads to cell dysfunction and cell death: introduction to a thematic review series. J Lipid Res 2016; 57 (08) 1327-1328
  • 6 Yoon H, Shaw JL, Haigis MC, Greka A. Lipid metabolism in sickness and in health: Emerging regulators of lipotoxicity. Mol Cell 2021; 81 (18) 3708-3730
  • 7 Crewe C, An YA, Scherer PE. The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. J Clin Invest 2017; 127 (01) 74-82
  • 8 Larabee CM, Neely OC, Domingos AI. Obesity: a neuroimmunometabolic perspective. Nat Rev Endocrinol 2020; 16 (01) 30-43
  • 9 Park HJ, Kim J, Bak S, Lee M. High salt intake induces adipogenesis by the modulation of MAPK/ERK1/2 pathway in both 3T3-L1 adipocytes and co-culture with macrophages. FASEB J 2017; 31: 947.2
  • 10 Cury JCS, Encinas JA, Nucci RAB. et al. Effects of different diet intake and resistance training on left ventricle remodeling in ovariectomized rats. Comp Clin Pathol 2019; 28 (06) 1797-1803
  • 11 Maifrino LBM, Lima NEA, Marques MR. et al. Evaluation of collagen fibers, MMP2, MMP9, 8-OHdG and apoptosis in the aorta of ovariectomized LDL knockout mice submitted to aerobic exercise. Arq Bras Cardiol 2019; 112 (02) 180-188
  • 12 Marchon C, de Marco Ornelas E, da Silva Viegas KA. et al. Effects of moderate exercise on the biochemical, physiological, morphological and functional parameters of the aorta in the presence of estrogen deprivation and dyslipidemia: an experimental model. Cell Physiol Biochem 2015; 35 (01) 397-405
  • 13 Brianezi L, Ornelas E, Gehrke FS. et al. Effects of physical training on the myocardium of oxariectomized LDLr knockout mice: MMP 2/9, collagen I/III, inflammation and oxidative stress. Arq Bras Cardiol 2020; 114 (01) 100-105
  • 14 Mandarim-de-Lacerda CA. Stereological tools in biomedical research. An Acad Bras Cienc 2003; 75 (04) 469-486
  • 15 Novelle MG, Vázquez MJ, Peinado JR. et al. Sequential exposure to obesogenic factors in females rats: from physiological changes to lipid metabolism in liver and mesenteric adipose tissue. Sci Rep 2017; 7: 46194
  • 16 Sutjarit N, Sueajai J, Boonmuen N. et al. Curcuma comosa reduces visceral adipose tissue and improves dyslipidemia in ovariectomized rats. J Ethnopharmacol 2018; 215: 167-175
  • 17 Fatima LA, Campello RS, Barreto-Andrade JN. et al. Estradiol stimulates adipogenesis and Slc2a4/GLUT4 expression via ESR1-mediated activation of CEBPA. Mol Cell Endocrinol 2019; 498: 110447
  • 18 Stanford KI, Goodyear LJ. Exercise regulation of adipose tissue. Adipocyte 2016; 5 (02) 153-162
  • 19 Pagnotti GM, Styner M, Uzer G. et al. Combating osteoporosis and obesity with exercise: leveraging cell mechanosensitivity. Nat Rev Endocrinol 2019; 15 (06) 339-355
  • 20 Stanford KI, Middelbeek RJ, Goodyear LJ. Exercise effects on white adipose tissue: beiging and metabolic adaptations. Diabetes 2015; 64 (07) 2361-2368
  • 21 Medeiros CS, de Sousa Neto IV, Silva KKS. et al. The effects of high-protein diet and resistance training on glucose control and inflammatory profile of visceral adipose tissue in rats. Nutrients 2021; 13 (06) 1969
  • 22 Rodrigues MFC, Ferreira FC, Silva-Magosso NS. et al. Effects of resistance training and estrogen replacement on adipose tissue inflammation in ovariectomized rats. Appl Physiol Nutr Metab 2017; 42 (06) 605-612
  • 23 Alfonso L, Mendizabal JA. Caracterización de la distribución del tamaño de los adipocitos para el estudio del tejido adiposo en producción animal. ITEA 2016; 112 (02) 147-161
  • 24 Ghaben AL, Scherer PE. Adipogenesis and metabolic health. Nat Rev Mol Cell Biol 2019; 20 (04) 242-258
  • 25 Murphy J, Moullec G, Santosa S. Factors associated with adipocyte size reduction after weight loss interventions for overweight and obesity: a systematic review and meta-regression. Metabolism 2017; 67: 31-40
  • 26 Ibáñez CA, Vázquez-Martínez M, León-Contreras JC. et al. Different statistical approaches to characterization of adipocyte size in offspring of obese rats: effects of maternal or offspring exercise intervention. Front Physiol 2018; 9: 1571
  • 27 Jung UJ, Choi MS. Obesity and its metabolic complications: the role of adipokines and the relationship between obesity, inflammation, insulin resistance, dyslipidemia and nonalcoholic fatty liver disease. Int J Mol Sci 2014; 15 (04) 6184-6223
  • 28 Welte MA. Expanding roles for lipid droplets. Curr Biol 2015; 25 (11) R470-R481
  • 29 Sharma M, Schlegel M, Brown EJ. et al. Netrin-1 alters adipose tissue macrophage fate and function in obesity. Immunometabolism 2019; 1 (02) e190010
  • 30 Majdoubi A, Kishta OA, Thibodeau J. Role of antigen presentation in the production of pro-inflammatory cytokines in obese adipose tissue. Cytokine 2016; 82: 112-121
  • 31 Virtue S, Masoodi M, de Weijer BAM. et al. Prostaglandin profiling reveals a role for haematopoietic prostaglandin D synthase in adipose tissue macrophage polarisation in mice and humans. Int J Obes 2015; 39 (07) 1151-1160
  • 32 Walsh NP, Gleeson M, Shephard RJ. et al. Position statement. Part one: Immune function and exercise. Exerc Immunol Rev 2011; 17: 6-63