The effect of aerobic exercise on the oxidative stress of brown adipose tissue
الموضوعات :
Nazanin Rahmannezhad
1
,
Mohammad Ali Azarbayjani
2
,
Saleh Rahmati Ahmadabad
3
,
Maghsoud Peeri
4
,
Hoseyn fatolahi
5
1 - Department of Exercise Physiology, Central Tehran Branch, Islamic Azad University, Tehran, Iran
2 - Department of Sport Physiology, Central Tehran Branch, Islamic Azad University, Tehran, Iran
3 - Department of Physical Education, Pardis Branch, Islamic Azad University, Pardis, Iran
4 - Department of Sports Physiology, Central Tehran Branch, Islamic Azad University, Tehran, Iran
5 - Department of Physical Education, Pardis Branch, Islamic Azad University, Pardis, Iran
الکلمات المفتاحية: Aerobic exercise, brown adipose tissue, Nrf-2 and SIRT3,
ملخص المقالة :
Brown adipose tissue (BAT) plays a very critical role in controlling obesity and metabolic complications due to thermogenesis (fatty acid conversion into heat). Just as this tissue's natural activity prevents obesity, obesity can also disrupt its function through several mechanisms. This is especially due to the increase in oxidative stress. Many studies have shown that aerobic exercise improves the thermogenic function of BAT and exert an anti-obesity effect. However, aerobic exercise not only improves brown fat tissue function, but also protects it from oxidative damage by increasing its antioxidant defense capacity. Since aerobic exercise with moderate intensity can cause a physiological increase in reactive oxygen species (ROS), molecular studies have shown that ROS produced following aerobic exercise can enhance the expression of HSP72, Nrf-2 and SIRT3, and following It enhances the expression of antioxidant enzymes such as SOD, CAT, GPX and hemooxygenase in BAT. Considering that these enzymes (as enzymatic antioxidant defense) inhibit and neutralize all kinds of ROS, BAT's antioxidant defense capacity is increased and disruption of its biological functions is prevented.
1. Mota de Sá P, Richard AJ, Hang H, Stephens JM. Transcriptional Regulation of Adipogenesis. Compr Physiol. 2017 Mar 16;7(2):635-674. doi: 10.1002/cphy.c160022. PMID: 28333384.
2. White U. Adipose tissue expansion in obesity, health, and disease. Front Cell Dev Biol. 2023 Apr 26; 11:1188844.
3. Takhti M, Riyahi Malayeri S, Behdari R. Comparison of two methods of concurrent training and ginger intake on visfatin and metabolic syndrome in overweight women. Razi Journal of Medical Sciences. 2020;27(9):98-111.
4. Avgerinos KI, Spyrou N, Mantzoros CS, Dalamaga M. Obesity and cancer risk: Emerging biological mechanisms and perspectives. Metabolism. 2019 Mar;92:121-135. doi: 10.1016/j.metabol.2018.11.001. Epub 2018 Nov 13. PMID: 30445141.
5. Hedayati S, Riyahi Malayeri S, Hoseini M. The Effect of Eight Weeks of High and Moderate Intensity Interval Training Along with Aloe Vera Consumption on Serum Levels of Chemerin, Glucose and Insulin in Streptozotocin-induced Diabetic Rats: An Experimental Study. JRUMS. 2018; 17 (9) :801-814. URL: http://journal.rums.ac.ir/article-1-4209-fa.html.
6. Harvey I, Boudreau A, Stephens JM. Adipose tissue in health and disease. Open Biol. 2020 Dec;10(12):200291. doi: 10.1098/rsob.200291. Epub 2020 Dec 9. PMID: 33292104; PMCID: PMC7776562.
7. Ghesmati Z, Rashid M, Fayezi S, Gieseler F, Alizadeh E, Darabi M. An update on the secretory functions of brown, white, and beige adipose tissue: Towards therapeutic applications. Rev Endocr Metab Disord. 2024 Apr;25(2):279-308. doi: 10.1007/s11154-023-09850-0. Epub 2023 Dec 5. PMID: 38051471; PMCID: PMC10942928.
8. McNeill BT, Suchacki KJ, Stimson RH. MECHANISMS IN ENDOCRINOLOGY: Human brown adipose tissue as a therapeutic target: warming up or cooling down? Eur J Endocrinol. 2021 May 4;184(6):R243-R259. doi: 10.1530/EJE-20-1439. PMID: 33729178; PMCID: PMC8111330.
9. Kajimura S, Saito M. A new era in brown adipose tissue biology: molecular control of brown fat development and energy homeostasis. Annu Rev Physiol. 2014;76:225-49. doi: 10.1146/annurev-physiol-021113-170252. Epub 2013 Nov 4. PMID: 24188710; PMCID: PMC4090362.
10. Maharjan BR, Martinez-Huenchullan SF, Mclennan SV, Twigg SM, Williams PF. Exercise induces favorable metabolic changes in white adipose tissue preventing high-fat diet obesity. Physiol Rep. 2021 Aug;9(16):e14929. doi: 10.14814/phy2.14929. PMID: 34405572; PMCID: PMC8371352.
11. Meng Q, Su CH. The Impact of Physical Exercise on Oxidative and Nitrosative Stress: Balancing the Benefits and Risks. Antioxidants (Basel). 2024 May 7;13(5):573. doi: 10.3390/antiox13050573. PMID: 38790678; PMCID: PMC11118032.
12. Luo B, Xiang D, Ji X, Chen X, Li R, Zhang S, Meng Y, Nieman DC, Chen P. The anti-inflammatory effects of exercise on autoimmune diseases: A 20-year systematic review. J Sport Health Sci. 2024 May;13(3):353-367. doi: 10.1016/j.jshs.2024.02.002. Epub 2024 Feb 9. PMID: 38341137; PMCID: PMC11117003.
13. Sies H. Oxidative stress: a concept in redox biology and medicine. Redox Biol. 2015;4:180-3. doi: 10.1016/j.redox.2015.01.002. Epub 2015 Jan 3. PMID: 25588755; PMCID: PMC4309861.
14. Jones DP. Radical-free biology of oxidative stress. Am J Physiol Cell Physiol. 2008 Oct;295(4):C849-68. doi: 10.1152/ajpcell.00283.2008. Epub 2008 Aug 6. PMID: 18684987; PMCID: PMC2575825.
15. Shimizu I, Aprahamian T, Kikuchi R, Shimizu A, Papanicolaou KN, MacLauchlan S, Maruyama S, Walsh K. Vascular rarefaction mediates whitening of brown fat in obesity. J Clin Invest. 2014 May;124(5):2099-112. doi: 10.1172/JCI71643. Epub 2014 Apr 8. PMID: 24713652; PMCID: PMC4001539.
16. Graja A, Schulz TJ. Mechanisms of aging-related impairment of brown adipocyte development and function. Gerontology. 2015;61(3):211-7. doi: 10.1159/000366557. Epub 2014 Dec 20. PMID: 25531079.
17. Ro SH, Nam M, Jang I, Park HW, Park H, Semple IA, Kim M, Kim JS, Park H, Einat P, Damari G, Golikov M, Feinstein E, Lee JH. Sestrin2 inhibits uncoupling protein 1 expression through suppressing reactive oxygen species. Proc Natl Acad Sci U S A. 2014 May 27;111(21):7849-54. doi: 10.1073/pnas.1401787111. Epub 2014 May 13. PMID: 24825887; PMCID: PMC4040599.
26. Narasimhan M, Hong J, Atieno N, Muthusamy VR, Davidson CJ, Abu-Rmaileh N, Richardson RS, Gomes AV, Hoidal JR, Rajasekaran NS. Nrf2 deficiency promotes apoptosis and impairs PAX7/MyoD expression in aging skeletal muscle cells. Free Radic Biol Med. 2014 Jun;71:402-414. doi: 10.1016/j.freeradbiomed.2014.02.023. Epub 2014 Mar 6. PMID: 24613379; PMCID: PMC4493911.
27. Priestley JR, Kautenburg KE, Casati MC, Endres BT, Geurts AM, Lombard JH. The NRF2 knockout rat: a new animal model to study endothelial dysfunction, oxidant stress, and microvascular rarefaction. Am J Physiol Heart Circ Physiol. 2016 Feb 15;310(4):H478-87. doi: 10.1152/ajpheart.00586.2015. Epub 2015 Dec 4. PMID: 26637559; PMCID: PMC4796617.
28. Jin Y, Miao W, Lin X, Pan X, Ye Y, Xu M, Fu Z. Acute exposure to 3-methylcholanthrene induces hepatic oxidative stress via activation of the Nrf2/ARE signaling pathway in mice. Environ Toxicol. 2014 Dec;29(12):1399-408. doi: 10.1002/tox.21870. Epub 2013 May 27. PMID: 23712962.
29. Periyasamy P, Shinohara T. Age-related cataracts: Role of unfolded protein response, Ca2+ mobilization, epigenetic DNA modifications, and loss of Nrf2/Keap1 dependent cytoprotection. Prog Retin Eye Res. 2017 Sep;60:1-19. doi: 10.1016/j.preteyeres.2017.08.003. Epub 2017 Aug 31. PMID: 28864287; PMCID: PMC5600869.
30. Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, Talalay P, Kensler TW. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3410-5. doi: 10.1073/pnas.051618798. PMID: 11248092; PMCID: PMC30667.
31. Kang, J.S., Kim, D.J., Kim, GY. et al. Ethanol extract of Prunus mume fruit attenuates hydrogen peroxide-induced oxidative stress and apoptosis involving Nrf2/HO-l activation in C2C12 myoblasts. Revista Brasileira de Farmacognosia 26, 184–190 (2016). https://doi.org/10.1016/j.bjp.2015.06.012.
32. Xu Y., Liu F., Xu Z., Liu Z., Zhang J. Soyasaponins protects against physical fatigue and improves exercise performance in mice. International Journal of Clinical and Experimental Medicine. 2017;10(8):11856–11865.
18. Lee JH, Budanov AV, Talukdar S, Park EJ, Park HL, Park HW, Bandyopadhyay G, Li N, Aghajan M, Jang I, Wolfe AM, Perkins GA, Ellisman MH, Bier E, Scadeng M, Foretz M, Viollet B, Olefsky J, Karin M. Maintenance of metabolic homeostasis by Sestrin2 and Sestrin3. Cell Metab. 2012 Sep 5;16(3):311-21. doi: 10.1016/j.cmet.2012.08.004. PMID: 22958918; PMCID: PMC3687365.
19. Pan R, Chen Y. Management of Oxidative Stress: Crosstalk Between Brown/Beige Adipose Tissues and Skeletal Muscles. Front Physiol. 2021 Sep 16;12:712372. doi: 10.3389/fphys.2021.712372. PMID: 34603076; PMCID: PMC8481590.
20. Alcalá M, Calderon-Dominguez M, Bustos E, Ramos P, Casals N, Serra D, Viana M, Herrero L. Increased inflammation, oxidative stress and mitochondrial respiration in brown adipose tissue from obese mice. Sci Rep. 2017 Nov 22;7(1):16082. doi: 10.1038/s41598-017-16463-6. PMID: 29167565; PMCID: PMC5700117.
21. Tsuzuki T, Yoshihara T, Ichinoseki-Sekine N, Kobayashi H, Negishi T, Yukawa K, Naito H. Exercise training improves obesity-induced inflammatory signaling in rat brown adipose tissue. Biochem Biophys Rep. 2022 Nov 28;32:101398. doi: 10.1016/j.bbrep.2022.101398. PMID: 36467545; PMCID: PMC9713272.
22. de Lemos ET, Oliveira J, Pinheiro JP, Reis F. Regular physical exercise as a strategy to improve antioxidant and anti-inflammatory status: benefits in type 2 diabetes mellitus. Oxid Med Cell Longev. 2012;2012:741545. doi: 10.1155/2012/741545. Epub 2012 Aug 13. PMID: 22928086; PMCID: PMC3425959.
23. Park HS, Lee JS, Huh SH, Seo JS, Choi EJ. Hsp72 functions as a natural inhibitory protein of c-Jun N-terminal kinase. EMBO J. 2001 Feb 1;20(3):446-56. doi: 10.1093/emboj/20.3.446. PMID: 11157751; PMCID: PMC133486.
24. Ostrom EL, Traustadóttir T. Aerobic exercise training partially reverses the impairment of Nrf2 activation in older humans. Free Radic Biol Med. 2020 Nov 20;160:418-432. doi: 10.1016/j.freeradbiomed.2020.08.016. Epub 2020 Aug 28. PMID: 32866619; PMCID: PMC7704731.
25. Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol. 2007;47:89-116. doi: 10.1146/annurev.pharmtox.46.120604.141046. PMID: 16968214.
26. Narasimhan M, Hong J, Atieno N, Muthusamy VR, Davidson CJ, Abu-Rmaileh N, Richardson RS, Gomes AV, Hoidal JR, Rajasekaran NS. Nrf2 deficiency promotes apoptosis and impairs PAX7/MyoD expression in aging skeletal muscle cells. Free Radic Biol Med. 2014 Jun;71:402-414. doi: 10.1016/j.freeradbiomed.2014.02.023. Epub 2014 Mar 6. PMID: 24613379; PMCID: PMC4493911.
27. Priestley JR, Kautenburg KE, Casati MC, Endres BT, Geurts AM, Lombard JH. The NRF2 knockout rat: a new animal model to study endothelial dysfunction, oxidant stress, and microvascular rarefaction. Am J Physiol Heart Circ Physiol. 2016 Feb 15;310(4):H478-87. doi: 10.1152/ajpheart.00586.2015. Epub 2015 Dec 4. PMID: 26637559; PMCID: PMC4796617.
28. Jin Y, Miao W, Lin X, Pan X, Ye Y, Xu M, Fu Z. Acute exposure to 3-methylcholanthrene induces hepatic oxidative stress via activation of the Nrf2/ARE signaling pathway in mice. Environ Toxicol. 2014 Dec;29(12):1399-408. doi: 10.1002/tox.21870. Epub 2013 May 27. PMID: 23712962.
29. Periyasamy P, Shinohara T. Age-related cataracts: Role of unfolded protein response, Ca2+ mobilization, epigenetic DNA modifications, and loss of Nrf2/Keap1 dependent cytoprotection. Prog Retin Eye Res. 2017 Sep;60:1-19. doi: 10.1016/j.preteyeres.2017.08.003. Epub 2017 Aug 31. PMID: 28864287; PMCID: PMC5600869.
30. Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, Talalay P, Kensler TW. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3410-5. doi: 10.1073/pnas.051618798. PMID: 11248092; PMCID: PMC30667.
31. Kang, J.S., Kim, D.J., Kim, GY. et al. Ethanol extract of Prunus mume fruit attenuates hydrogen peroxide-induced oxidative stress and apoptosis involving Nrf2/HO-l activation in C2C12 myoblasts. Revista Brasileira de Farmacognosia 26, 184–190 (2016). https://doi.org/10.1016/j.bjp.2015.06.012.
32. Xu Y., Liu F., Xu Z., Liu Z., Zhang J. Soyasaponins protects against physical fatigue and improves exercise performance in mice. International Journal of Clinical and Experimental Medicine. 2017;10(8):11856–11865.
33. Long M, Li X, Li L, Dodson M, Zhang DD, Zheng H. Multifunctional p62 Effects Underlie Diverse Metabolic Diseases. Trends Endocrinol Metab. 2017 Nov;28(11):818-830. doi: 10.1016/j.tem.2017.09.001. Epub 2017 Sep 28. PMID: 28966079.
34. Tsai YC, Wang CW, Wen BY, Hsieh PS, Lee YM, Yen MH, Cheng PY. Involvement of the p62/Nrf2/HO-1 pathway in the browning effect of irisin in 3T3-L1 adipocytes. Mol Cell Endocrinol. 2020 Aug 20;514:110915. doi: 10.1016/j.mce.2020.110915. Epub 2020 Jun 12. PMID: 32540261.
35. Tebay LE, Robertson H, Durant ST, Vitale SR, Penning TM, Dinkova-Kostova AT, Hayes JD. Mechanisms of activation of the transcription factor Nrf2 by redox stressors, nutrient cues, and energy status and the pathways through which it attenuates degenerative disease. Free Radic Biol Med. 2015 Nov;88(Pt B):108-146. doi: 10.1016/j.freeradbiomed.2015.06.021. Epub 2015 Jun 27. PMID: 26122708; PMCID: PMC4659505.
36. Suh JH, Shenvi SV, Dixon BM, Liu H, Jaiswal AK, Liu RM, Hagen TM. Decline in transcriptional activity of Nrf2 causes age-related loss of glutathione synthesis, which is reversible with lipoic acid. Proc Natl Acad Sci U S A. 2004 Mar 9;101(10):3381-6. doi: 10.1073/pnas.0400282101. Epub 2004 Feb 25. PMID: 14985508; PMCID: PMC373470.
37. Asghar M, George L, Lokhandwala MF. Exercise decreases oxidative stress and inflammation and restores renal dopamine D1 receptor function in old rats. Am J Physiol Renal Physiol. 2007 Sep;293(3):F914-9. doi: 10.1152/ajprenal.00272.2007. Epub 2007 Jul 18. PMID: 17634393.
38. Yu M, Zhang H, Wang B, Zhang Y, Zheng X, Shao B, Zhuge Q, Jin K. Key Signaling Pathways in Aging and Potential Interventions for Healthy Aging. Cells. 2021 Mar 16;10(3):660. doi: 10.3390/cells10030660. PMID: 33809718; PMCID: PMC8002281.
39. Yu Q, Xia Z, Liong EC, Tipoe GL. Chronic aerobic exercise improves insulin sensitivity and modulates Nrf2 and NF κB/IκBα pathways in the skeletal muscle of rats fed with a high fat diet. Mol Med Rep. 2019 Dec;20(6):4963-4972. doi: 10.3892/mmr.2019.10787. Epub 2019 Oct 31. PMID: 31702809; PMCID: PMC6854540.
40. Ahmed SM, Luo L, Namani A, Wang XJ, Tang X. Nrf2 signaling pathway: Pivotal roles in inflammation. Biochim Biophys Acta Mol Basis Dis. 2017 Feb;1863(2):585-597. doi: 10.1016/j.bbadis.2016.11.005. Epub 2016 Nov 4. PMID: 27825853.
41. Liu GH, Qu J, Shen X. NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK. Biochim Biophys Acta. 2008 May;1783(5):713-27. doi: 10.1016/j.bbamcr.2008.01.002. Epub 2008 Jan 12. PMID: 18241676.
42. Jiang T, Tian F, Zheng H, Whitman SA, Lin Y, Zhang Z, Zhang N, Zhang DD. Nrf2 suppresses lupus nephritis through inhibition of oxidative injury and the NF-κB-mediated inflammatory response. Kidney Int. 2014 Feb;85(2):333-343. doi: 10.1038/ki.2013.343. Epub 2013 Sep 11. PMID: 24025640; PMCID: PMC3992978.
43. Chowdhry S, Nazmy MH, Meakin PJ, Dinkova-Kostova AT, Walsh SV, Tsujita T, Dillon JF, Ashford ML, Hayes JD. Loss of Nrf2 markedly exacerbates nonalcoholic steatohepatitis. Free Radic Biol Med. 2010 Jan 15;48(2):357-71. doi: 10.1016/j.freeradbiomed.2009.11.007. Epub 2009 Nov 13. PMID: 19914374.
44. Liu Z, Dou W, Ni Z, Wen Q, Zhang R, Qin M, Wang X, Tang H, Cao Y, Wang J, Zhao S. Deletion of Nrf2 leads to hepatic insulin resistance via the activation of NF-κB in mice fed a high-fat diet. Mol Med Rep. 2016 Aug;14(2):1323-31. doi: 10.3892/mmr.2016.5393. Epub 2016 Jun 10. PMID: 27315552.
45. Vatner DE, Oydanich M, Zhang J, Campbell SC, Vatner SF. Exercise enhancement by RGS14 disruption is mediated by brown adipose tissue. Aging Cell. 2023 Apr;22(4):e13791. doi: 10.1111/acel.13791. Epub 2023 Mar 10. PMID: 36905127; PMCID: PMC10086526.
46. Sebaa R, Johnson J, Pileggi C, Norgren M, Xuan J, Sai Y, Tong Q, Krystkowiak I, Bondy-Chorney E, Davey NE, Krogan N, Downey M, Harper ME. SIRT3 controls brown fat thermogenesis by deacetylation regulation of pathways upstream of UCP1. Mol Metab. 2019 Jul;25:35-49. doi: 10.1016/j.molmet.2019.04.008. Epub 2019 Apr 17. PMID: 31060926; PMCID: PMC6601363.
: PMC6092475.
47. Koltai E, Bori Z, Osvath P, Ihasz F, Peter S, Toth G, Degens H, Rittweger J, Boldogh I, Radak Z. Master athletes have higher miR-7, SIRT3 and SOD2 expression in skeletal muscle than age-matched sedentary controls. Redox Biol. 2018 Oct;19:46-51. doi: 10.1016/j.redox.2018.07.022. Epub 2018 Aug 7. PMID: 30107294; PMCID: PMC6092475.
48. Cheng A, Yang Y, Zhou Y, Maharana C, Lu D, Peng W, Liu Y, Wan R, Marosi K, Misiak M, Bohr VA, Mattson MP. Mitochondrial SIRT3 Mediates Adaptive Responses of Neurons to Exercise and Metabolic and Excitatory Challenges. Cell Metab. 2016 Jan 12;23(1):128-42. doi: 10.1016/j.cmet.2015.10.013. Epub 2015 Nov 19. PMID: 26698917; PMCID: PMC5141613.
49. Lin L, Chen K, Abdel Khalek W, Ward JL 3rd, Yang H, Chabi B, Wrutniak-Cabello C, Tong Q. Regulation of skeletal muscle oxidative capacity and muscle mass by SIRT3. PLoS One. 2014 Jan 15;9(1):e85636. doi: 10.1371/journal.pone.0085636. PMID: 24454908; PMCID: PMC3893254.
50. Qiu X, Brown K, Hirschey MD, Verdin E, Chen D. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab. 2010 Dec 1;12(6):662-7. doi: 10.1016/j.cmet.2010.11.015. PMID: 21109198.
51, Chen Y, Zhang J, Lin Y, Lei Q, Guan KL, Zhao S, Xiong Y. Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep. 2011 Jun;12(6):534-41. doi: 10.1038/embor.2011.65. Epub 2011 May 13. PMID: 21566644; PMCID: PMC3128277.
52. Cho SY, Chung YS, Yoon HK, Roh HT. Impact of Exercise Intensity on Systemic Oxidative Stress, Inflammatory Responses, and Sirtuin Levels in Healthy Male Volunteers. Int J Environ Res Public Health. 2022 Sep 8;19(18):11292. doi: 10.3390/ijerph191811292. PMID: 36141561; PMCID: PMC9516970.
53. Zhou L, Pinho R, Gu Y, Radak Z. The Role of SIRT3 in Exercise and Aging. Cells. 2022 Aug 20;11(16):2596. doi: 10.3390/cells11162596. PMID: 36010672; PMCID: PMC9406297.
