Physical Activity and Exercise Promote Peroxisome Proliferator-Activated Receptor Gamma Expression in Adipose Tissues of Obese Adults
-
Maryam Zarkesh
,
Zahra Nozhat
,
Mahdi Akbarzadeh
,
Maryam S Daneshpour
,
Behnaz Mahmoodi
,
Golaleh Asghari
,
Mehdi Hedayati
,
Afsoon Daneshafrooz
,
Rani Fedoruk
,
Emad Yuzbashian
,
Parvin Mirmiran
,
Alireza Khalaj
Abstract
Background: Peroxisome proliferator-activated receptor gamma (PPARγ) has recently been studied for its potential influence on the functional response of the human body to exercise. We aimed to investigate the association of habitual physical activity (PA) with PPARγ mRNA level in the visceral and subcutaneous adipose tissues (VAT and SAT) in non-obese and obese non-diabetic adults.
Methods: VAT and SAT were obtained from 95 individuals, including 40 non-obese (BMI<30kg/m2) and 55 obese (BMI≥30kg/m2) who underwent elective abdominal surgery (Tehran, Iran, 2012-2015). The assessment of habitual PA was performed by a valid and reliable International PA Questionnaire-long form, and the metabolic equivalent of task (MET) was evaluated. Real-time quantitative reverse transcriptase-PCR evaluated the PPARγ expression in VAT and SAT.
Results: PPARγ expression in both VAT (1.18 vs. 0.37 fold change, P<0.001) and SAT (2.07 vs. 0.29 fold change, P=0.004) among obese subjects was higher than the non-obese group. After controlling for age, sex, and total energy intake, a positive association was found between total METs and PPARγ expression in both VAT and SAT among obese participants (β=0.22, P=0.007 and β=0.12, P<0.001, respectively). Among obese participants, there was a direct association between leisure time-related METs with VAT PPARγ expression (β=0.05, P=0.026). Moreover, in this group, an association was observed between occupation-related METs with PPARγ in both fat tissues (β=0.11, P=0.002 and β=0.17, P=0.013, respectively), and household work-related METs with SAT PPARγ (β=0.21, P=0.011).
Conclusion: High PA as an indispensable part of a healthy lifestyle may exert its beneficial effect by regulating PPARγ expression.
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17. Ekelund U, Franks PW, Sharp S, Brage S, Wareham NJ (2007). Increase in physical activity energy expenditure is associated with reduced metabolic risk independent of change in fatness and fitness. Diabetes Care, 30 (8): 2101-6.
18. Yuzbashian E, Asghari G, Hedayati M, Zarkesh M, Mirmiran P, Khalaj A (2019). The association of dietary carbohydrate with FTO gene expression in visceral and subcutaneous adipose tissue of adults without diabetes. Nutrition, 63-64: 92-7.
19. Vasheghani-Farahani A, Tahmasbi M, Ash-eri H, Ashraf H, Nedjat S, Kordi R (2011). The Persian, last 7-day, long form of the International Physical Activity Questionnaire: translation and validation study. Asian J Sports Med, 2 (2): 106-16.
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21. Asghari G, Rezazadeh A, Hosseini-Esfahani F, Mehrabi Y, Mirmiran P, Azizi F (2012). Reliability, comparative validity and stabil-ity of dietary patterns derived from an FFQ in the Tehran Lipid and Glucose Study. Br J Nutr, 108 (6): 1109-17.
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23. Roy D, Tomo S, Modi A, Purohit P, Sharma P (2020). Optimising total RNA quality and quantity by phenol-chloroform ex-traction method from human visceral ad-ipose tissue: A standardisation study. MethodsX, 7:101113.
24. Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods, 25 (4): 402-8.
25. Jeong S-H (2012). Regulation of PPAR and SREBP-1C through Exercise in White Adipose Tissue of Female C57BL/6J Mice. J Exp Biomed Sci, 18 (3): 227-36.
26. Mattevi VS, Zembrzuski VM, Hutz MH (2007). Effects of a PPARG gene variant on obesity characteristics in Brazil. Braz J Med Biol Res, 40 (7): 927-32.
27. Ruschke K, Fishbein L, Dietrich A, et al (2010). Gene expression of PPARγ and PGC-1α in human omental and subcuta-neous adipose tissues is related to insulin resistance markers and mediates benefi-cial effects of physical training. Eur J En-docrinol, 162 (3): 515-23.
28. Kato H, Shibahara T, Rahman N, Takakura H, Ohira Y, Izawa T (2018). Effect of a 9-week exercise training regimen on ex-pression of developmental genes related to growth-dependent fat expansion in ju-venile rats. Physiol Rep, 6 (19): e13880.
29. Kawamura T, Yoshida K, Sugawara A, et al (2004). Regulation of skeletal muscle pe-roxisome proliferator-activated receptor gamma expression by exercise and angio-tensin-converting enzyme inhibition in fructose-fed hypertensive rats. Hypertens Res, 27 (1): 61-70.
30. Hallal PC, Victora CG, Wells JC, Lima RC (2003). Physical inactivity: prevalence and associated variables in Brazilian adults. Med Sci Sports Exerc, 35 (11): 1894-900.
31. Madsen MS, Siersbæk R, Boergesen M, Nielsen R, Mandrup S (2014). Peroxi-some proliferator-activated receptor γ and C/EBPα synergistically activate key metabolic adipocyte genes by assisted loading. Mol Cell Biol, 34 (6): 939-54.
32. Sugii S, Olson P, Sears DD, et al (2009). PPARgamma activation in adipocytes is sufficient for systemic insulin sensitiza-tion. Proc Natl Acad Sci U S A, 106 (52): 22504-9.
33. Castellano-Castillo D, Denechaud P-D, Fa-jas L, et al (2019). Human adipose tissue H3K4me3 histone mark in adipogenic, lipid metabolism and inflammatory genes is positively associated with BMI and HOMA-IR. PLoS One, 14 (4): e0215083.
34. Hammes TO, dos Santos Costa C, Rohden F, et al (2012). Parallel down-regulation of FOXO1, PPARγ and adiponectin mRNA expression in visceral adipose tissue of class III obese individuals. Obes Facts, 5 (3): 452-9.
35. Bortolotto JW, Margis R, Ferreira ÂCB, Pa-doin AV, Mottin CC, Guaragna RM (2007). Adipose tissue distribution and quantification of PPARβ/δ and PPARγ1-3 mRNAS: discordant gene expression in subcutaneous, retroperitoneal and visceral adipose tissue of morbidly obese pa-tients. Obes Surg, 17 (7): 934-40.
36. Maddison R, Mhurchu CN, Jiang Y, et al (2007). International physical activity questionnaire (IPAQ) and New Zealand physical activity questionnaire (NZPAQ): a doubly labelled water validation. Int J Behav Nutr Phys Act, 4: 62.
37. Afzal N, Hassan M, Fatima S, Tariq S, Qa-yum I (2016). Expression of Peroxisome-Proliferator Activated Receptors-γ In Di-abetics, Obese and Normal Subjects. J Ayub Med Coll Abbottabad, 28 (1): 130-4.
38. Montague CT, Prins JB, Sanders L, et al (1998). Depot-related gene expression in human subcutaneous and omental adipo-cytes. Diabetes, 47 (9): 1384-91.
2. Castro AVB, Kolka CM, Kim SP, Bergman RN (2014). Obesity, insulin resistance and comorbidities? Mechanisms of associa-tion. Arq Bras Endocrinol Metabol, 58 (6): 600-9.
3. Romieu I, Dossus L, Barquera S, et al (2017). Energy balance and obesity: what are the main drivers? Cancer Causes Control, 28 (3): 247-58.
4. Agurs-Collins T, Bouchard C (2008). Gene-nutrition and gene-physical activity inter-actions in the etiology of obesity. Obesity (Silver Spring), 16 Suppl 3(Suppl 3): S2-4.
5. Rostami H, Samadi M, Yuzbashian E, et al (2017). Habitual dietary intake of fatty ac-ids are associated with leptin gene ex-pression in subcutaneous and visceral ad-ipose tissue of patients without diabetes. Prostaglandins Leukot Essent Fatty Acids, 126: 49-54.
6. Goossens GH (2008). The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol Behav, 94 (2): 206-18.
7. Nosrati-Oskouie M, Yuzbashian E, Zarkesh M, et al (2021). Association of plasma fat-ty acids pattern with omentin gene ex-pression in human adipose tissues: A cross-sectional study. Nutr Metab Cardio-vasc Dis, 31 (3): 894-901.
8. Zareie R, Yuzbashian E, Rahimi H, et al (2021). Dietary fat content and adipose triglyceride lipase and hormone-sensitive lipase gene expressions in adults’ subcu-taneous and visceral fat tissues. Prostaglan-dins Leukot Essent Fatty Acids, 165: 102244.
9. Sokkar S, El-Sharnouby JA, Helmy A, et al (2009). Role of Peroxisome Proliferator-Activated Receptor gamma2 (PPAR-γ2) Gene Polymorphism in Type 2 Diabetes Mellitus. Eur J Gen Med, 6 (2): 78-86.
10. Adams KF, Schatzkin A, Harris TB, et al (2006). Overweight, obesity, and mortality in a large prospective cohort of persons 50 to 71 years old. N Engl J Med, 355 (8): 763-78.
11. Motawi T, Shaker O, Ismail M, Sayed N (2017). Peroxisome proliferator-activated receptor gamma in obesity and colorectal cancer: the role of epigenetics. Sci Rep, 7 (1): 10714.
12. Leońska-Duniec A, Ahmetov I, Zmijewski P (2016). Genetic variants influencing effec-tiveness of exercise training programmes in obesity–an overview of human studies. Biol Sport, 33 (3): 207-14.
13. Thomas AW, Davies NA, Moir H, et al (2012). Exercise-associated generation of PPARγ ligands activates PPARγ signaling events and upregulates genes related to lipid metabolism. J Appl Physiol(1985), 112 (5): 806-15.
14. Iemitsu M, Miyauchi T, Maeda S, et al (2002). Aging-induced decrease in the PPAR-α level in hearts is improved by exercise training. Am J Physiol Heart Circ Physiol, 283 (5): H1750-60.
15. Li M, Bai Y, Jianfei C, Xiaodong X, Yuanyuan D, Jing Z (2014). [Effects of different exercise intensity on PPARγ and relative index in adolescent obesity rats]. Wei Sheng Yan Jiu, 43 (5): 732-7.
16. Mahmoodi B, Shemshaki A, Zarkesh M, Hedayati M, Mirmiran P (2019). Habitual Physical Activity is Associated with Rela-tive Apelin Gene Expression in Adipose Tissues Among Non-Diabetic Adults. Int J Pept Res Ther, 25 (4): 1573-9.
17. Ekelund U, Franks PW, Sharp S, Brage S, Wareham NJ (2007). Increase in physical activity energy expenditure is associated with reduced metabolic risk independent of change in fatness and fitness. Diabetes Care, 30 (8): 2101-6.
18. Yuzbashian E, Asghari G, Hedayati M, Zarkesh M, Mirmiran P, Khalaj A (2019). The association of dietary carbohydrate with FTO gene expression in visceral and subcutaneous adipose tissue of adults without diabetes. Nutrition, 63-64: 92-7.
19. Vasheghani-Farahani A, Tahmasbi M, Ash-eri H, Ashraf H, Nedjat S, Kordi R (2011). The Persian, last 7-day, long form of the International Physical Activity Questionnaire: translation and validation study. Asian J Sports Med, 2 (2): 106-16.
20. Forde C (2018). Scoring the international physical activity questionnaire (IPAQ). University of Dublin. 3.
21. Asghari G, Rezazadeh A, Hosseini-Esfahani F, Mehrabi Y, Mirmiran P, Azizi F (2012). Reliability, comparative validity and stabil-ity of dietary patterns derived from an FFQ in the Tehran Lipid and Glucose Study. Br J Nutr, 108 (6): 1109-17.
22. Yuzbashian E, Asghari G, Hedayati M, Zarkesh M, Mirmiran P, Khalaj A (2019). Determinants of vitamin D receptor gene expression in visceral and subcutaneous adipose tissue in non-obese, obese, and morbidly obese subjects. J Steroid Biochem Mol Biol, 187: 82-7.
23. Roy D, Tomo S, Modi A, Purohit P, Sharma P (2020). Optimising total RNA quality and quantity by phenol-chloroform ex-traction method from human visceral ad-ipose tissue: A standardisation study. MethodsX, 7:101113.
24. Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods, 25 (4): 402-8.
25. Jeong S-H (2012). Regulation of PPAR and SREBP-1C through Exercise in White Adipose Tissue of Female C57BL/6J Mice. J Exp Biomed Sci, 18 (3): 227-36.
26. Mattevi VS, Zembrzuski VM, Hutz MH (2007). Effects of a PPARG gene variant on obesity characteristics in Brazil. Braz J Med Biol Res, 40 (7): 927-32.
27. Ruschke K, Fishbein L, Dietrich A, et al (2010). Gene expression of PPARγ and PGC-1α in human omental and subcuta-neous adipose tissues is related to insulin resistance markers and mediates benefi-cial effects of physical training. Eur J En-docrinol, 162 (3): 515-23.
28. Kato H, Shibahara T, Rahman N, Takakura H, Ohira Y, Izawa T (2018). Effect of a 9-week exercise training regimen on ex-pression of developmental genes related to growth-dependent fat expansion in ju-venile rats. Physiol Rep, 6 (19): e13880.
29. Kawamura T, Yoshida K, Sugawara A, et al (2004). Regulation of skeletal muscle pe-roxisome proliferator-activated receptor gamma expression by exercise and angio-tensin-converting enzyme inhibition in fructose-fed hypertensive rats. Hypertens Res, 27 (1): 61-70.
30. Hallal PC, Victora CG, Wells JC, Lima RC (2003). Physical inactivity: prevalence and associated variables in Brazilian adults. Med Sci Sports Exerc, 35 (11): 1894-900.
31. Madsen MS, Siersbæk R, Boergesen M, Nielsen R, Mandrup S (2014). Peroxi-some proliferator-activated receptor γ and C/EBPα synergistically activate key metabolic adipocyte genes by assisted loading. Mol Cell Biol, 34 (6): 939-54.
32. Sugii S, Olson P, Sears DD, et al (2009). PPARgamma activation in adipocytes is sufficient for systemic insulin sensitiza-tion. Proc Natl Acad Sci U S A, 106 (52): 22504-9.
33. Castellano-Castillo D, Denechaud P-D, Fa-jas L, et al (2019). Human adipose tissue H3K4me3 histone mark in adipogenic, lipid metabolism and inflammatory genes is positively associated with BMI and HOMA-IR. PLoS One, 14 (4): e0215083.
34. Hammes TO, dos Santos Costa C, Rohden F, et al (2012). Parallel down-regulation of FOXO1, PPARγ and adiponectin mRNA expression in visceral adipose tissue of class III obese individuals. Obes Facts, 5 (3): 452-9.
35. Bortolotto JW, Margis R, Ferreira ÂCB, Pa-doin AV, Mottin CC, Guaragna RM (2007). Adipose tissue distribution and quantification of PPARβ/δ and PPARγ1-3 mRNAS: discordant gene expression in subcutaneous, retroperitoneal and visceral adipose tissue of morbidly obese pa-tients. Obes Surg, 17 (7): 934-40.
36. Maddison R, Mhurchu CN, Jiang Y, et al (2007). International physical activity questionnaire (IPAQ) and New Zealand physical activity questionnaire (NZPAQ): a doubly labelled water validation. Int J Behav Nutr Phys Act, 4: 62.
37. Afzal N, Hassan M, Fatima S, Tariq S, Qa-yum I (2016). Expression of Peroxisome-Proliferator Activated Receptors-γ In Di-abetics, Obese and Normal Subjects. J Ayub Med Coll Abbottabad, 28 (1): 130-4.
38. Montague CT, Prins JB, Sanders L, et al (1998). Depot-related gene expression in human subcutaneous and omental adipo-cytes. Diabetes, 47 (9): 1384-91.
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| Issue | Vol 51 No 11 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v51i11.11181 | |
| Keywords | ||
| Adipose tissue Exercise Non-diabetic | ||
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How to Cite
1.
Zarkesh M, Nozhat Z, Akbarzadeh M, Daneshpour MS, Mahmoodi B, Asghari G, Hedayati M, Daneshafrooz A, Fedoruk R, Yuzbashian E, Mirmiran P, Khalaj A. Physical Activity and Exercise Promote Peroxisome Proliferator-Activated Receptor Gamma Expression in Adipose Tissues of Obese Adults. Iran J Public Health. 2022;51(11):2619-2628.
