Molecular mechanisms of heat shock protein 27 under physical exertion and its role in cardiovascular disease prevention

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Abstract

Cardiovascular diseases (CVDs) pose a serious threat to public health in the Russian Federation and remain the leading cause of mortality. In 2016, the economic burden of CVDs amounted to 2.7 trillion rubles, representing 3.2% of the country’s gross domestic product. Major risk factors for CVDs, such as physical inactivity, smoking, alcohol consumption, unhealthy diet, and obesity, are directly associated with deterioration of cardiovascular system condition. Circulating heat shock protein 27 (HSP27) exhibits numerous beneficial properties, including involvement in inflammatory regulation, antioxidant, anti-apoptotic, and anti-atherogenic processes. Acting as a signaling molecule in the blood, it helps the body cope with various types of stress. Studies show that HSP27 levels decline with age and during menopause, potentially contributing to the development of atherosclerosis, which is a key factor in the development of many CVDs. Physical exercise exerts a positive influence on the body by increasing plasma HSP27 levels. This elevation may have an immunomodulatory effect on various immune cells, including monocytes. Through this mechanism, physical activity supports the body in managing inflammation and reducing the risk of CVDs. Thus, understanding the role of HSP27 in the context of physical exertion offers new opportunities for the prevention and treatment of CVDs. Further research may lead to innovative therapeutic strategies aimed at enhancing HSP27 levels and lowering the risk of atherosclerosis and other CVDs.

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About the authors

Aleksandr A. Rachkov

Rostov State Medical University

Author for correspondence.
Email: motoredj2@rambler.ru
ORCID iD: 0009-0002-8654-0229
Russian Federation, 29 Nakhichevan aly, Rostov-on-Don, 344022

Alina S. Oleynikova

Rostov State Medical University

Email: a_vinyukova@list.ru
ORCID iD: 0009-0000-4740-0755
Russian Federation, 29 Nakhichevan aly, Rostov-on-Don, 344022

Alena I. Borolisova

Rostov State Medical University

Email: alena-dits@mail.ru
ORCID iD: 0009-0003-2145-3041
Russian Federation, 29 Nakhichevan aly, Rostov-on-Don, 344022

Ikbol I. Mirzosharipov

Bashkir State Medical University

Email: ikbol.ikromi@bk.ru
ORCID iD: 0009-0000-7655-661X
Russian Federation, Ufa

Ruslan R. Makhyanov

Bashkir State Medical University

Email: ruslanmakhyanov0608@gmail.com
ORCID iD: 0009-0001-0437-1744
Russian Federation, Ufa

Sofia A. Kadochnikova

Kazan Federal University

Email: skadochnikovaa@mail.ru
ORCID iD: 0009-0002-1901-830X
Russian Federation, Kazan

Liliya A. Khairullina

City Polyclinic N. 21

Email: lily_2205khai@mail.ru
ORCID iD: 0009-0009-5342-269X
Russian Federation, Kazan

Khabibat B. Abutalimova

Dagestan State Medical University

Email: habibat408@gmail.com
ORCID iD: 0009-0001-3702-3965
Russian Federation, Makhachkala

Ruslan O. Zimin

Krasnoyarsk State Medical University

Email: Zimin.ruslan99@mail.ru
ORCID iD: 0009-0003-0792-2307
Russian Federation, Krasnoyarsk

Nazira F. Merdalieva

Russian University of Medicine

Email: merdalieva6@gmail.com
ORCID iD: 0009-0006-5411-0813
Russian Federation, Moscow

Kirill B. Pokidov

Voronezh State Medical University

Email: pokidov.kiril@yandex.ru
ORCID iD: 0009-0005-0438-7569
Russian Federation, Voronezh

Diana A. Nelyubina

Voronezh State Medical University

Email: di709@yandex.ru
ORCID iD: 0000-0002-6279-9300
Russian Federation, Voronezh

Darya O. Boiko

Rostov State Medical University

Email: cuttheworld57@gmail.com
ORCID iD: 0009-0006-9493-1763
Russian Federation, 29 Nakhichevan aly, Rostov-on-Don, 344022

Sofya A. Kharchenko

Rostov State Medical University

Email: Sofiaivanova79@mail.ru
ORCID iD: 0000-0001-7635-7418
Russian Federation, 29 Nakhichevan aly, Rostov-on-Don, 344022

References

  1. Kontsevaya AV, Mukaneeva DK, Ignatieva VI, et al. Economics of cardiovascular prevention in the Russian Federation. Russian Journal of Cardiology. 2023;28(9):5521. doi: 10.15829/1560-4071-2023-5521 EDN: KNLBZO
  2. Benjamin EJ, Muntner P, Alonso A, et al. Disease and stroke statistics-2019 update: a report from the American heart association. Circulation. 2019;139(10):e56–e528. doi: 10.1161/CIR.0000000000000659
  3. Zimakova EI, Orlova YaA, Begrambekova YuL. Prevalence and promising directions for correction of behavioral risk factors for cardiovascular diseases associated with unhealthy diet and low physical activity in young people. South Russian Journal of Therapeutic Practice. 2024;5(3):6–13. doi: 10.21886/2712-8156-2024-5-3-6-13 EDN: HFDCWE
  4. Maksimovich NYe, Bon EI. Heat shock proteins. Properties. Role in adaptation. Methodological approaches to definition. Journal Biomed. 2020;(2):60–67. doi: 10.33647/2074-5982-16-2-60-67 EDN: JDHMWC
  5. Zou Y, Shi H, Liu N, et al. Mechanistic insights into heat shock protein 27, a potential therapeutic target for cardiovascular diseases. Front Cardiovasc Med. 2023;10:1195464. doi: 10.3389/fcvm.2023.1195464 EDN: VZUGOH
  6. Batulan Z, Pulakazhi Venu VK, Li Y, et al. Extracellular release and signaling by heat shock protein 27: role in modifying vascular inflammation. Front Immunol. 2016;7:285. doi: 10.3389/fimmu.2016.00285 EDN: WSVPFX
  7. Kardys I, Rifai N, Meilhac O, et al. Plasma concentration of heat shock protein 27 and risk of cardiovascular disease: a prospective, nested case-control study. Clin Chem. 2008;54(1):139–46. doi: 10.1373/clinchem.2007.094961
  8. Timofeev YuS, Afaunova AA, Metelskaya VA, et al. Heat shock proteins as potential biomarkers of heart failure. Cardiovascular Therapy and Prevention. 2024;23(4):3938. doi: 10.15829/1728-8800-2024-3938 EDN: HCVPTH
  9. Maarouf N, Chen YX, Shi C, et al. Unlike estrogens that increase PCSK9 levels post-menopause HSP27 vaccination lowers cholesterol levels and atherogenesis due to divergent effects on PCSK9 and LDLR. Pharmacol Res. 2020;161:105222. doi: 10.1016/j.phrs.2020.105222 EDN: BQMQSX
  10. Rayner K, Chen YX, Siebert T, O'Brien ER. Heat shock protein 27: clue to understanding estrogen-mediated atheroprotection? Trends Cardiovasc Med. 2010;20(2):54–8. doi: 10.1016/j.tcm.2010.03.008
  11. Khazova EV, Bulashova OV. Residual risk in patients with atherosclerotic cardiovascular disease. Cardiovascular Therapy and Prevention. 2023;22(1):3382. doi: 10.15829/1728-8800-2023-3382 EDN: CERZKU
  12. McCarthy M, Raval AP. The peri-menopause in a woman's life: a systemic inflammatory phase that enables later neurodegenerative disease. J Neuroinflammation. 2020;17(1):317. doi: 10.1186/s12974-020-01998-9 EDN: OQGFNB
  13. Moreau KL, Hildreth KL, Klawitter J, et al. Decline in endothelial function across the menopause transition in healthy women is related to decreased estradiol and increased oxidative stress. Geroscience. 2020;42(6):1699–1714. doi: 10.1007/s11357-020-00236-7 EDN: JRIDMH
  14. El Khoudary SR. Gaps, limitations and new insights on endogenous estrogen and follicle stimulating hormone as related to risk of cardiovascular disease in women traversing the menopause: A narrative review. Maturitas. 2017;104:44–53. doi: 10.1016/j.maturitas.2017.08.003
  15. Saner Kh. Prevention of cardiovascular diseases through physical activity and exercises: exercise stress as a medicine. Russian Journal of Cardiology and Cardiovascular Surgery. 2013;6(6):17–23. EDN: RSYZIR
  16. Gliemann L, Hellsten Y. The exercise timing hypothesis: can exercise training compensate for the reduction in blood vessel function after menopause if timed right? J Physiol. 2019;597(19):4915–4925. doi: 10.1113/JP277056
  17. Lundberg Slingsby MH, Nyberg M, Egelund J, et al. Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women. J Thromb Haemost. 2017;15(12):2419–2431. doi: 10.1111/jth.13866
  18. Mandrup CM, Egelund J, Nyberg M, et al. Effects of menopause and high-intensity training on insulin sensitivity and muscle metabolism. Menopause. 2018;25(2):165–175. doi: 10.1097/GME.0000000000000981
  19. Nyberg M, Egelund J, Mandrup CM, et al. Leg vascular and skeletal muscle mitochondrial adaptations to aerobic high-intensity exercise training are enhanced in the early postmenopausal phase. J Physiol. 2017;595(9):2969–2983. doi: 10.1113/JP273871
  20. Garber CE, Blissmer B, Deschenes MR, et al. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc. 2011;43(7):1334–59. doi: 10.1249/MSS.0b013e318213fefb
  21. Chow LS, Gerszten RE, Taylor JM, et al. Exerkines in health, resilience and disease. Nat Rev Endocrinol. 2022;18(5):273–289. doi: 10.1038/s41574-022-00641-2 EDN: POBWXT
  22. Fiuza-Luces C, Santos-Lozano A, Joyner M, et al. Exercise benefits in cardiovascular disease: beyond attenuation of traditional risk factors. Nat Rev Cardiol. 2018;15(12):731–743. doi: 10.1038/s41569-018-0065-1
  23. Magliulo L, Bondi D, Pini N, et al. The wonder exerkines-novel insights: a critical state-of-the-art review. Mol Cell Biochem. 2022;477(1):105–113. doi: 10.1007/s11010-021-04264-5 EDN: ZHJJQJ
  24. Walzik D, Wences Chirino TY, Zimmer P, Joisten N. Molecular insights of exercise therapy in disease prevention and treatment. Signal Transduct Target Ther. 2024;9(1):138. doi: 10.1038/s41392-024-01841-0 EDN: JQWUZL
  25. Whitham M, Parker BL, Friedrichsen M, et al. Extracellular vesicles provide a means for tissue crosstalk during exercise. Cell Metab. 2018;27(1):237–251.e4. doi: 10.1016/j.cmet.2017.12.001
  26. Henstridge DC, Whitham M, Febbraio MA. Chaperoning to the metabolic party: The emerging therapeutic role of heat-shock proteins in obesity and type 2 diabetes. Mol Metab. 2014;3(8):781–93. doi: 10.1016/j.molmet.2014.08.003 EDN: STWJFZ
  27. Jammes Y, Steinberg JG, Olivier M, et al. The mechanisms of the widespread production of phosphorylated HSP25 after fatiguing muscle stimulation. J Exp Biol. 2013;216(Pt 19):3620–6. doi: 10.1242/jeb.088898
  28. Murphy RM, Watt MJ, Febbraio MA. Metabolic communication during exercise. Nat Metab. 2020;2(9):805–816. doi: 10.1038/s42255-020-0258-x EDN: FPSIFB
  29. Yamada P, Amorim F, Moseley P, Schneider S. Heat shock protein 72 response to exercise in humans. Sports Med. 2008;38(9):715–33. doi: 10.2165/00007256-200838090-00002 EDN: MCBDQF
  30. Pushkina YaA, Sychev IV, Goncharova LN, et al. Pathogenetic mechanisms of atherosclerosis development in athletes. Atherosclerosis. 2020;16(4):85–92. doi: 10.15372/ATER20200411 EDN: EGXFXJ
  31. Roy P, Orecchioni M, Ley K. How the immune system shapes atherosclerosis: roles of innate and adaptive immunity. Nat Rev Immunol. 2022;22(4):251–265. doi: 10.1038/s41577-021-00584-1 EDN: TYWMZN
  32. Chinetti-Gbaguidi G, Colin S, Staels B. Macrophage subsets in atherosclerosis. Nat Rev Cardiol. 2015;12(1):10–7. doi: 10.1038/nrcardio.2014.173 EDN: UOXIFT
  33. Matzinger P. An innate sense of danger. Semin Immunol. 1998;10(5):399–415. doi: 10.1006/smim.1998.0143
  34. Vidyasagar A, Wilson NA, Djamali A. Heat shock protein 27 (HSP27): biomarker of disease and therapeutic target. Fibrogenesis Tissue Repair. 2012;5(1):7. doi: 10.1186/1755-1536-5-7 EDN: XZYWVL
  35. Calderwood SK, Repasky EA, Neckers L, Hightower LE. The IXth CSSI international symposium on heat shock proteins in biology and medicine: stress responses in health and disease: Alexandria Old Town, Alexandria, Virginia, November 10–13, 2018. Cell Stress Chaperones. 2019;24(1):1–6. doi: 10.1007/s12192-018-00966-w EDN: LAKRGR
  36. Dubrez L, Causse S, Borges Bonan N, et al. Heat-shock proteins: chaperoning DNA repair. Oncogene. 2020;39(3):516–529. doi: 10.1038/s41388-019-1016-y EDN: YEDCVQ
  37. Broere F, van der Zee R, van Eden W. Heat shock proteins are no DAMPs, rather 'DAMPERs'. Nat Rev Immunol. 2011;11(8):565; author reply 565. doi: 10.1038/nri2873-c1
  38. Gomez CR. Role of heat shock proteins in aging and chronic inflammatory diseases. Geroscience. 2021;43(5):2515–2532. doi: 10.1007/s11357-021-00394-2 EDN: QBDQYM
  39. van Eden W, Spiering R, Broere F, van der Zee R. A case of mistaken identity: HSPs are no DAMPs but DAMPERs. Cell Stress Chaperones. 2012;17(3):281–92. doi: 10.1007/s12192-011-0311-5 EDN: IHBLYP
  40. Giuliano JS Jr, Lahni PM, Wong HR, Wheeler DS. Pediatric sepsis — part V: Extracellular heat shock proteins: alarmins for the host immune system. Open Inflamm J. 2011;4:49–60. doi: 10.2174/1875041901104010049
  41. O'Brien ER, Sandhu JK. Sex differences in COVID-19 mortality: opportunity to develop HSP27 (HSPB1) immunotherapy to treat hyper-inflammation? Cell Stress Chaperones. 2020;25(5):725–729. doi: 10.1007/s12192-020-01146-5 EDN: MNXVJZ
  42. Chen YX, Shi C, Deng J, et al. HSP25 Vaccination attenuates atherogenesis via upregulation of LDLR expression, lowering of PCSK9 levels and curbing of inflammation. Arterioscler Thromb Vasc Biol. 2021;41(6):e338–e353. doi: 10.1161/ATVBAHA.121.315933 EDN: UEDQEU
  43. Cuerrier CM, Chen YX, Tremblay D, et al. Chronic over-expression of heat shock protein 27 attenuates atherogenesis and enhances plaque remodeling: a combined histological and mechanical assessment of aortic lesions. PLoS One. 2013;8(2):e55867. doi: 10.1371/journal.pone.0055867
  44. Seibert TA, Hibbert B, Chen YX, et al. Serum heat shock protein 27 levels represent a potential therapeutic target for atherosclerosis: observations from a human cohort and treatment of female mice. J Am Coll Cardiol. 2013;62(16):1446–54. doi: 10.1016/j.jacc.2013.05.041
  45. Ogbodo E, Michelangeli F, Williams JHH. Exogenous heat shock proteins HSPA1A and HSPB1 regulate TNF-α, IL-1β and IL-10 secretion from monocytic cells. FEBS Open Bio. 2023;13(10):1922–1940. doi: 10.1002/2211-5463.13695 EDN: YDBMPN
  46. Salari S, Seibert T, Chen YX, et al. Extracellular HSP27 acts as a signaling molecule to activate NF-κB in macrophages. Cell Stress Chaperones. 2013;18(1):53–63. doi: 10.1007/s12192-012-0356-0 EDN: UNKHEX
  47. Shi C, Deng J, Chiu M, et al. Heat shock protein 27 immune complex altered signaling and transport (ICAST): Novel mechanisms of attenuating inflammation. FASEB J. 2020;34(11):14287–14301. doi: 10.1096/fj.202001389RR EDN: CUVNAC
  48. Jin C, Phillips VL, Williams MJ, et al. Plasma heat shock protein 27 is associated with coronary artery disease, abdominal aortic aneurysm and peripheral artery disease. Springerplus. 2014;3:635. doi: 10.1186/2193-1801-3-635 EDN: DUCPPB
  49. Martin-Ventura JL, Duran MC, Blanco-Colio LM, et al. Identification by a differential proteomic approach of heat shock protein 27 as a potential marker of atherosclerosis. Circulation. 2004;110(15):2216–9. doi: 10.1161/01.CIR.0000136814.87170.B1
  50. Rea IM, McNerlan S, Pockley AG. Serum heat shock protein and anti-heat shock protein antibody levels in aging. Exp Gerontol. 2001;36(2):341–52. doi: 10.1016/s0531-5565(00)00215-1 EDN: AMGPXD
  51. Barna J, Csermely P, Vellai T. Roles of heat shock factor 1 beyond the heat shock response. Cell Mol Life Sci. 2018;75(16):2897–2916. doi: 10.1007/s00018-018-2836-6 EDN: VGZCGQ
  52. Trivedi R, Jurivich DA. A molecular perspective on age-dependent changes to the heat shock axis. Exp Gerontol. 2020;137:110969. doi: 10.1016/j.exger.2020.110969 EDN: DDQRUL
  53. Wang H, Alencar A, Lin M, et al. Activation of GPR30 improves exercise capacity and skeletal muscle strength in senescent female Fischer344 × Brown Norway rats. Biochem Biophys Res Commun. 2016;475(1):81–6. doi: 10.1016/j.bbrc.2016.05.040
  54. Batulan Z, Maarouf N, Shrivastava V, O'Brien E. Prophylactic salpingo-oophorectomy & surgical menopause for inherited risks of cancer: the need to identify biomarkers to assess the theoretical risk of premature coronary artery disease. Womens Midlife Health. 2018;4:7. doi: 10.1186/s40695-018-0037-y
  55. Cumming KT, Kvamme NH, Schaad L, et al. Muscular HSP70 content is higher in elderly compared to young, but is normalized after 12 weeks of strength training. Eur J Appl Physiol. 2021;121(6):1689–1699. doi: 10.1007/s00421-021-04633-4 EDN: MFMQXW
  56. Koskinen SOA, Kyröläinen H, Flink R, et al. Human skeletal muscle type 1 fibre distribution and response of stress-sensing proteins along the titin molecule after submaximal exhaustive exercise. Histochem Cell Biol. 2017;148(5):545–555. doi: 10.1007/s00418-017-1595-z EDN: YIHZCR
  57. Nielsen JL, Aagaard P, Prokhorova TA, et al. Blood flow restricted training leads to myocellular macrophage infiltration and upregulation of heat shock proteins, but no apparent muscle damage. J Physiol. 2017;595(14):4857–4873. doi: 10.1113/JP273907
  58. Cumming KT, Paulsen G, Wernbom M, et al. Acute response and subcellular movement of HSP27, αB-crystallin and HSP70 in human skeletal muscle after blood-flow-restricted low-load resistance exercise. Acta Physiol. 2014;211(4):634–46. doi: 10.1111/apha.12305 EDN: URMFAF
  59. Huey KA, McCall GE, Zhong H, Roy RR. Modulation of HSP25 and TNF-alpha during the early stages of functional overload of a rat slow and fast muscle. J Appl Physiol. 2007;102(6):2307–14. doi: 10.1152/japplphysiol.00021.2007
  60. Ishihara A, Fujino H, Nagatomo F, et al. Gene expression levels of heat shock proteins in the soleus and plantaris muscles of rats after hindlimb suspension or spaceflight. J Physiol Sci. 2008;58(6):413–7. doi: 10.2170/physiolsci.RP000808
  61. Lawler JM, Song W, Kwak HB. Differential response of heat shock proteins to hindlimb unloading and reloading in the soleus. Muscle Nerve. 2006;33(2):200–7. doi: 10.1002/mus.20454
  62. Cumming KT, Ellefsen S, Rønnestad BR, et al. Acute and long-term effects of blood flow restricted training on heat shock proteins and endogenous antioxidant systems. Scand J Med Sci Sports. 2017;27(11):1190–1201. doi: 10.1111/sms.12774
  63. Cumming KT, Raastad T, Sørstrøm A, et al. Vitamin C and E supplementation does not affect heat shock proteins or endogenous antioxidants in trained skeletal muscles during 12 weeks of strength training. BMC Nutr. 2017;3:70. doi: 10.1186/s40795-017-0185-8 EDN: FATKLX
  64. Larkins NT, Murphy RM, Lamb GD. Absolute amounts and diffusibility of HSP72, HSP25, and αB-crystallin in fast- and slow-twitch skeletal muscle fibers of rat. Am J Physiol Cell Physiol. 2012;302(1):C228–39. doi: 10.1152/ajpcell.00266.2011
  65. Sadri I, Nikookheslat SD, Karimi P, et al. Aerobic exercise training improves memory function through modulation of brain-derived neurotrophic factor and synaptic proteins in the hippocampus and prefrontal cortex of type 2 diabetic rats. J Diabetes Metab Disord. 2023;23(1):849–858. doi: 10.1007/s40200-023-01360-9 EDN: WHQBEI
  66. Brunelli A, Dimauro I, Sgrò P, et al. Acute exercise modulates BDNF and pro-BDNF protein content in immune cells. Med Sci Sports Exerc. 2012;44(10):1871–80. doi: 10.1249/MSS.0b013e31825ab69b
  67. Vardar SA, Doğanlar ZB, Kaya O, et al. Different responses of apoptotic, inflammatory and heat shock protein gene expression to a single bout of high-intensity interval exercise between physically active and inactive men. Appl Physiol Nutr Metab. 2021;46(7):743–752. doi: 10.1139/apnm-2020-0783 EDN: NJAQLR
  68. Whitham M, Halson SL, Lancaster GI, et al. Leukocyte heat shock protein expression before and after intensified training. Int J Sports Med. 2004;25(7):522–7. doi: 10.1055/s-2004-820953
  69. Hagymasi AT, Dempsey JP, Srivastava PK. Heat-shock proteins. Curr Protoc. 2022;2(11):e592. doi: 10.1002/cpz1.592 EDN: CHZQBP
  70. Grotegut P, Hoerdemann PJ, Reinehr S, et al. Heat shock protein 27 injection leads to caspase activation in the visual pathway and retinal T-cell response. Int J Mol Sci. 2021;22(2):513. doi: 10.3390/ijms22020513 EDN: FALYLN
  71. Brown J, Wang H, Hajishengallis GN, Martin M. TLR-signaling networks: an integration of adaptor molecules, kinases, and cross-talk. J Dent Res. 2011;90(4):417–27. doi: 10.1177/0022034510381264
  72. Kessler B, Rinchai D, Kewcharoenwong C, et al. Interleukin 10 inhibits pro-inflammatory cytokine responses and killing of Burkholderia pseudomallei. Sci Rep. 2017;7:42791. doi: 10.1038/srep42791
  73. Zamani F, Zare Shahneh F, Aghebati-Maleki L, Baradaran B. Induction of CD14 expression and differentiation to monocytes or mature macrophages in promyelocytic cell lines: new approach. Adv Pharm Bull. 2013;3(2):329–32. doi: 10.5681/apb.2013.053
  74. Oh ES, Na M, Rogers CJ. The association between monocyte subsets and cardiometabolic disorders/cardiovascular disease: a systematic review and meta-analysis. Front Cardiovasc Med. 2021;8:640124. doi: 10.3389/fcvm.2021.640124 EDN: WNFSPO
  75. Xiang Y, Liang B, Zhang X, Zheng F. Lower HDL-C levels are associated with higher expressions of CD16 on monocyte subsets in coronary atherosclerosis. Int J Med Sci. 2020;17(14):2171–2179. doi: 10.7150/ijms.47998 EDN: UNCFEX
  76. Grebe A, Hoss F, Latz E. NLRP3 inflammasome and the IL-1 pathway in atherosclerosis. Circ Res. 2018;122(12):1722–1740. doi: 10.1161/CIRCRESAHA.118.311362 EDN: YKPLAL
  77. Pfeiler S, Winkels H, Kelm M, Gerdes N. IL-1 family cytokines in cardiovascular disease. Cytokine. 2019;122:154215. doi: 10.1016/j.cyto.2017.11.009 EDN: NRZEUQ
  78. Hadadi E, Zhang B, Baidžajevas K, et al. Differential IL-1β secretion by monocyte subsets is regulated by Hsp27 through modulating mRNA stability. Sci Rep. 2016;6:39035. doi: 10.1038/srep39035
  79. do Brito Valente AF, Jaspers RT, Wüst RC. Regular physical exercise mediates the immune response in atherosclerosis. Exerc Immunol Rev. 2021;27:42–53.
  80. Campbell JP, Turner JE. Debunking the myth of exercise-induced immune suppression: redefining the impact of exercise on immunological health across the lifespan. Front Immunol. 2018;9:648. doi: 10.3389/fimmu.2018.00648
  81. Aw NH, Canetti E, Suzuki K, Goh J. Monocyte subsets in atherosclerosis and modification with exercise in humans. Antioxidants. 2018;7(12):196. doi: 10.3390/antiox7120196
  82. Simpson RJ, Kunz H, Agha N, Graff R. Exercise and the regulation of immune functions. Prog Mol Biol Transl Sci. 2015;135:355–80. doi: 10.1016/bs.pmbts.2015.08.001
  83. Szlezak AM, Szlezak SL, Keane J, et al. Establishing a dose-response relationship between acute resistance-exercise and the immune system: Protocol for a systematic review. Immunol Lett. 2016;180:54–65. doi: 10.1016/j.imlet.2016.10.010
  84. Durrer C, Francois M, Neudorf H, Little JP. Acute high-intensity interval exercise reduces human monocyte Toll-like receptor 2 expression in type 2 diabetes. Am J Physiol Regul Integr Comp Physiol. 2017;312(4):R529–R538. doi: 10.1152/ajpregu.00348.2016
  85. LaVoy EC, Bollard CM, Hanley PJ, et al. A single bout of dynamic exercise by healthy adults enhances the generation of monocyte-derived-dendritic cells. Cell Immunol. 2015;295(1):52–9. doi: 10.1016/j.cellimm.2015.02.007
  86. Slusher AL, Zúñiga TM, Acevedo EO. Maximal exercise alters the inflammatory phenotype and response of mononuclear cells. Med Sci Sports Exerc. 2018;50(4):675–683. doi: 10.1249/MSS.0000000000001480
  87. Rooney BV, Bigley AB, LaVoy EC, et al. Lymphocytes and monocytes egress peripheral blood within minutes after cessation of steady state exercise: A detailed temporal analysis of leukocyte extravasation. Physiol Behav. 2018;194:260–267. doi: 10.1016/j.physbeh.2018.06.008
  88. Paulsen G, Lauritzen F, Bayer ML, et al. Subcellular movement and expression of HSP27, alphaB-crystallin, and HSP70 after two bouts of eccentric exercise in humans. J Appl Physiol. 2009;107(2):570–82. doi: 10.1152/japplphysiol.00209.2009
  89. Paulsen G, Vissing K, Kalhovde JM, et al. Maximal eccentric exercise induces a rapid accumulation of small heat shock proteins on myofibrils and a delayed HSP70 response in humans. Am J Physiol Regul Integr Comp Physiol. 2007;293(2):R844–53. doi: 10.1152/ajpregu.00677.2006
  90. Thompson HS, Clarkson PM, Scordilis SP. The repeated bout effect and heat shock proteins: intramuscular HSP27 and HSP70 expression following two bouts of eccentric exercise in humans. Acta Physiol Scand. 2002;174(1):47–56. doi: 10.1046/j.1365-201x.2002.00922.x EDN: AZYQTZ
  91. Gjøvaag TF, Dahl HA. Effect of training and detraining on the expression of heat shock proteins in m. triceps brachii of untrained males and females. Eur J Appl Physiol. 2006;98(3):310–22. doi: 10.1007/s00421-006-0281-y EDN: HHJUZC
  92. Dimauro I, Grazioli E, Lisi V, et al. Systemic response of antioxidants, heat shock proteins, and inflammatory biomarkers to short-lasting exercise training in healthy male subjects. Oxid Med Cell Longev. 2021;2021:1938492. doi: 10.1155/2021/1938492 EDN: VTIEPJ
  93. Micielska K, Gmiat A, Zychowska M, et al. The beneficial effects of 15 units of high-intensity circuit training in women is modified by age, baseline insulin resistance and physical capacity. Diabetes Res Clin Pract. 2019;152:156–165. doi: 10.1016/j.diabres.2019.05.009 EDN: RYYIKH
  94. Féasson L, Stockholm D, Freyssenet D, et al. Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J Physiol. 2002;543(Pt 1):297–306. doi: 10.1113/jphysiol.2002.018689
  95. Morton JP, MacLaren DP, Cable NT, et al. Time course and differential responses of the major heat shock protein families in human skeletal muscle following acute nondamaging treadmill exercise. J Appl Physiol. 2006;101(1):176–82. doi: 10.1152/japplphysiol.00046.2006
  96. Christiansen D, Murphy RM, Bangsbo J, et al. Increased FXYD1 and PGC-1α mRNA after blood flow-restricted running is related to fibre type-specific AMPK signalling and oxidative stress in human muscle. Acta Physiol. 2018;223(2):e13045. doi: 10.1111/apha.13045 EDN: YGIGDJ
  97. Ao L, Zhai Y, Jin C, et al. Attenuated recovery of contractile function in aging hearts following global ischemia/reperfusion: Role of extracellular HSP27 and TLR4. Mol Med. 2017;23:863–872. doi: 10.2119/molmed.2016.00204 EDN: DHTITO
  98. Jin C, Cleveland JC, Ao L, et al. Human myocardium releases heat shock protein 27 (HSP27) after global ischemia: the proinflammatory effect of extracellular HSP27 through toll-like receptor (TLR)-2 and TLR4. Mol Med. 2014;20(1):280–9. doi: 10.2119/molmed.2014.00058 EDN: ADNDKI
  99. Suga T, Okita K, Morita N, et al. Intramuscular metabolism during low-intensity resistance exercise with blood flow restriction. J Appl Physiol. 2009;106(4):1119–24. doi: 10.1152/japplphysiol.90368.2008
  100. Fehrenbach E, Niess AM, Schlotz E, et al. Transcriptional and translational regulation of heat shock proteins in leukocytes of endurance runners. J Appl Physiol. 2000;89(2):704–10. doi: 10.1152/jappl.2000.89.2.704
  101. Fehrenbach E, Passek F, Niess AM, et al. HSP expression in human leukocytes is modulated by endurance exercise. Med Sci Sports Exerc. 2000;32(3):592–600. doi: 10.1097/00005768-200003000-00007
  102. Jammes Y, Steinberg JG, Delliaux S, Brégeon F. Chronic fatigue syndrome combines increased exercise-induced oxidative stress and reduced cytokine and Hsp responses. J Intern Med. 2009;266(2):196–206. doi: 10.1111/j.1365-2796.2009.02079.x
  103. Kon M, Taniguchi K, Ebi Y, Nakagaki K. Effects of high-intensity interval exercise under hyperoxia on HSP27 and oxidative stress responses. Respir Physiol Neurobiol. 2021;283:103544. doi: 10.1016/j.resp.2020.103544 EDN: FSLLNK
  104. Tan XR, Low ICC, Soong TW, Lee JKW. Pre-exercise hot water immersion increased circulatory heat shock proteins but did not alter muscle damage markers or endurance capacity after eccentric exercise. Temperature. 2024;11(2):157–169. doi: 10.1080/23328940.2024.2313954
  105. Brerro-Saby C, Delliaux S, Steinberg JG, et al. Combination of two oxidant stressors suppresses the oxidative stress and enhances the heat shock protein 27 response in healthy humans. Metabolism. 2010;59(6):879–86. doi: 10.1016/j.metabol.2009.10.006
  106. Kim JH, Jung YS, Kim JW, et al. Effects of aquatic and land-based exercises on amyloid beta, heat shock protein 27, and pulse wave velocity in elderly women. Exp Gerontol. 2018;108:62–68. doi: 10.1016/j.exger.2018.03.024
  107. Gmiat A, Micielska K, Kozłowska M, et al. The impact of a single bout of high intensity circuit training on myokines' concentrations and cognitive functions in women of different age. Physiol Behav. 2017;179:290–297. doi: 10.1016/j.physbeh.2017.07.004
  108. Périard JD, Ruell P, Caillaud C, Thompson MW. Plasma Hsp72 (HSPA1A) and Hsp27 (HSPB1) expression under heat stress: influence of exercise intensity. Cell Stress Chaperones. 2012;17(3):375–83. doi: 10.1007/s12192-011-0313-3 EDN: JFRFQO
  109. Min HJ, Min SJ, Kang H, Kim KS. Differential nasal expression of heat shock proteins 27 and 70 by aerobic exercise: a preliminary study. Int J Med Sci. 2020;17(5):640–646. doi: 10.7150/ijms.39631 EDN: YHJNBS
  110. Tezel G, Wax MB. The mechanisms of hsp27 antibody-mediated apoptosis in retinal neuronal cells. J Neurosci. 2000;20(10):3552–62. doi: 10.1523/JNEUROSCI.20-10-03552.2000 EDN: LTISNP
  111. Jia D, Tian Z, Wang R. Exercise mitigates age-related metabolic diseases by improving mitochondrial dysfunction. Ageing Res Rev. 2023;91:102087. doi: 10.1016/j.arr.2023.102087 EDN: DXSBUU
  112. Delliaux S, Brerro-Saby C, Steinberg JG, Jammes Y. Reactive oxygen species activate the group IV muscle afferents in resting and exercising muscle in rats. Pflugers Arch. 2009;459(1):143–50. doi: 10.1007/s00424-009-0713-8 EDN: ZBJQOS
  113. Murlasits Z, Cutlip RG, Geronilla KB, et al. Resistance training increases heat shock protein levels in skeletal muscle of young and old rats. Exp Gerontol. 2006;41(4):398–406. doi: 10.1016/j.exger.2006.01.005
  114. Siu PM, Alway SE. Age-related apoptotic responses to stretch-induced hypertrophy in quail slow-tonic skeletal muscle. Am J Physiol Cell Physiol. 2005;289(5):C1105–13. doi: 10.1152/ajpcell.00154.2005
  115. Ceci R, Beltran Valls MR, Duranti G, et al. Oxidative stress responses to a graded maximal exercise test in older adults following explosive-type resistance training. Redox Biol. 2014;2:65–72. doi: 10.1016/j.redox.2013.12.004
  116. Fehrenbach E, Niess AM, Voelker K, et al. Exercise intensity and duration affect blood soluble HSP72. Int J Sports Med. 2005;26(7):552–7. doi: 10.1055/s-2004-830334 EDN: LTISTJ
  117. Decherchi P, Darques JL, Jammes Y. Modifications of afferent activities from Tibialis anterior muscle in rat by tendon vibrations, increase of interstitial potassium or lactate concentration and electrically-induced fatigue. J Peripher Nerv Syst. 1998;3(4):267–76.
  118. Peterson RA, König C, Zimmermann K, et al. Effects of lactate on one class of group III (CT3) muscle afferents. Front Cell Neurosci. 2020;14:215. doi: 10.3389/fncel.2020.00215 EDN: KSHQLY

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СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
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