Arctic Stress: Mechanisms and Experimental Models

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Abstract

Human’s stay in the Polar regions results in the development of stress caused by a combination of factors such as low air temperature, hypodynamia, hypoxia, and disruption of the daylight cycle. All this strongly indicates the increased requirements for health protection and prevention of morbidity in the population of the Arctic. The problem is topical of search for optimal biological models of Arctic stress intended for preclinical testing of pharmacological and dietary correction of its consequences. Aim — analysis of literature data on the pathophysiological mechanisms of polar stress, existing methods for its modeling in the experiment, informative biomarkers and prospects for dietary correction. Selection by keywords and analysis of literary sources using PubMed, Web of Science and Scopus online resources for the period, mainly, 2010–2022. The reaction to adverse environmental conditions in the Arctic is based on universal mechanisms associated with the excitation of midbrain centers (primarily the hypothalamus) with the development of a subsequent hormonal response from peptide hormones, corticosteroids, catecholamines, and thyroid hormones. The secondary targets of these effects are muscle tissue, endothelium, white and brown adipose tissue, cells of the immune system, in which changes occur aimed at neutralizing external adverse effects. A number of laboratory animal models have been developed to reproduce conditions associated with polar stress, including various types of acute, subacute and chronic cold exposure, as well as its combination with forced physical activity and additional stress factors. Sensitive biomarkers that allow monitoring the severity of polar stress are, firstly, the content of corticosteroids, catecholamines, neuropeptides, micro-RNA (miR-210) in blood plasma, organs and compartments of the brain, expression levels of uncoupling proteins (UCP) in brown adipose tissue, indicators of oxidative stress (lipoperoxide and malondialdehyde content, activity of antioxidant defense enzymes — GPX, GR, SOD, catalase and others), levels of bioantioxidants (vitamin E, ascorbic acid, carotenoids, GSH), cytokines and chemokines, including IL-1β, IL-6, IL-10, IL-17, IL-33, RANTES, FGF21 and various forms of their receptors, gene expression of signaling molecules (proteinkinases). In the issue of dietary correction of disorders caused by polar stress, the main place is given to the use of dietary antioxidant factors (vitamins E and C, selenium, zinc, coenzyme Q10, cinnamic acids and bioflavonoids). The data available in the world literature form the basis for further study of the molecular mechanisms of polar stress and pathogenetically substantiated methods of its dietary correction.

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.V. Gmoshinski 1, D.B. Nikityuk 1,2

1Federal Research Centre of Nutrition, Biotechnology and Food Safety, 109240, Moscow,Russian Federation

2Federal State Autonomous Educational Institution of Higher Education I.M. Sechenov First Moscow State Medical University under the Ministry of Health of the Russian Federation (Sechenov University), 119991, Moscow, Russian Federation

ARCTIC STRESS: MECHANISMS AND EXPERIMENTAL MODELS

Abstract

Background. Human’s stay in the Polar regions leads to the development of stress caused by a combination of factors such as low air temperature, hypodynamia, hypoxia, and disruption of the daylight cycle. All this strongly indicates the increased requirements for health protection and prevention of morbidity in the population of the Arctic. The problem is topical of search for optimal biological models of "polar stress" intended for preclinical testing of pharmacological and dietary correction of its consequences . Aim: analysis of literature data on the pathophysiological mechanisms of "polar stress", existing methods for its modeling in the experiment, informative biomarkers and prospects for dietary correction. Methods. Selection by keywords and analysis of literary sources using PubMed, Web of Science and Scopus online resources for the period, mainly, 2010-2022. Results. The reaction to adverse environmental conditions in the Arctic is based on universal mechanisms associated with the excitation of midbrain centers (primarily the hypothalamus) with the development of a subsequent hormonal response from peptide hormones, corticosteroids, catecholamines, and thyroid hormones. The secondary targets of these effects are muscle tissue, endothelium, white and brown adipose tissue, cells of the immune system, in which changes occur aimed at neutralizing external adverse effects. A number of laboratory animal models have been developed to reproduce conditions associated with "polar stress", including various types of acute, subacute and chronic cold exposure, as well as its combination with forced physical activity and additional stress factors. Sensitive biomarkers that allow monitoring the severity of “polar stress” are, firstly, the content of corticosteroids, catecholamines, neuropeptides, micro-RNA (miR-210) in blood plasma, organs and compartments of the brain, expression levels of uncoupling proteins (UCP) in brown adipose tissue, indicators of oxidative stress (lipoperoxide and malondialdehyde content, activity of antioxidant defense enzymes - GPX, GR, SOD, catalase and others), levels of bioantioxidants (vitamin E, ascorbic acid, carotenoids, GSH), cytokines and chemokines, including Il-1b, IL-6, IL-10, IL-17, IL-33, RANTES, FGF21 and various forms of their receptors, gene expression of signaling molecules (proteinkinases). In the issue of dietary correction of disorders caused by polar stress, the main place is given to the use of dietary antioxidant factors (vitamins E and C, selenium, zinc, coenzyme Q10, cinnamic acids and bioflavonoids). Conclusion. The data available in the world literature form the basis for further study of the molecular mechanisms of "polar stress" and pathogenetically substantiated methods of its dietary correction.

Keywords: Arctic, low temperatures, cold-stress reaction, biomarkers, diet therapy.

 

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About the authors

Ivan V. Gmoshinski

Federal Research Centre of Nutrition, Biotechnology and Food Safety

Author for correspondence.
Email: gmosh@ion.ru
ORCID iD: 0000-0002-3671-6508

PhD in Biology

Россия, 2/14, Ust’insky proezd, 109240, Moscow

Dmitry B. Nikityuk

Federal Research Centre of Nutrition, Biotechnology and Food Safety; I.M. Sechenov First Moscow State Medical University (Sechenov University)

Email: mailbox@ion.ru
ORCID iD: 0000-0002-4968-4517
SPIN-code: 1236-8210

MD, PhD, Professor, Academician of the RAS

Россия, 2/14, Ust’insky proezd, 109240, Moscow; Moscow

References

  1. Хаснулин В.И. Введение в полярную медицину. — Новосибирск: СО РАМН, 1998. — 337 с. [Khasnulin VI. Introduction to polar medicine. Novosibirsk: SO RAMN; 1998. 337 p. (In Russ.)]
  2. Sharma A, Verma HK, Joshi S, et al. A link between cold environment and cancer. Tumour Biol. 2015;36(8):5953–5964. doi: https://doi.org/10.1007/s13277-015-3270-0
  3. Bandyopadhayaya S, Ford B, Mandal CC. Cold-hearted: A case for cold stress in cancer risk. J Therm Biol. 2020;91:102608. doi: https://doi.org/10.1016/j.jtherbio.2020.102608
  4. Okimura K, Nakane Y, Nishiwaki-Ohkawa T, et al. Photoperiodic regulation of dopamine signaling regulates seasonal changes in retinal photosensitivity in mice. Sci Rep. 2021;11(1):1843. doi: https://doi.org/10.1038/s41598-021-81540-w
  5. Srivastava KK, Kumar R. Human nutrition in cold and high terrestrial altitudes. Int J Biometeorol. 1992;36(1):10–13. doi: https://doi.org/10.1007/BF01208728
  6. Glanz K, Bishop DB. The role of behavioral science theory in development and implementation of public health interventions. Annu Rev Public Health. 2010;31:399–418. doi: https://doi.org/10.1146/annurev.publhealth.012809.103604
  7. Salim S. Oxidative stress: a potential link between emotional wellbeing and immune response. Curr Opin Pharmacol. 2016;29:70–76. doi: https://doi.org/10.1016/j.coph.2016.06.006
  8. Okumoto K, Tamura S, Honsho M, et al. Peroxisome: Metabolic functions and biogenesis. Adv Exp Med Biol. 2020;1299:3–17. doi: https://doi.org/10.1007/978-3-030-60204-8_1
  9. Venditti P, Di Stefano L, Di Meo S. Oxidative stress in cold-induced hyperthyroid state. J Exp Biol. 2010;213(Pt 17):2899–2911. doi: https://doi.org/10.1242/jeb.043307
  10. Dzietko M, Boos V, Sifringer M, et al. A critical role for Fas/CD-95 dependent signaling pathways in the pathogenesis of hyperoxia-induced brain injury. Ann Neurol. 2008;64(6):664–673. doi: https://doi.org/10.1002/ana.21516
  11. Förstermann U, Xia N, Li H. Roles of vascular oxidative stress and nitric oxide in the pathogenesis of atherosclerosis. Circ Res. 2017;120(4):713–735. doi: https://doi.org/10.1161/CIRCRESAHA.116.309326
  12. Коденцова В.М., Вржесинская О.А., Мазо В.К. Витамины и окислительный стресс // Вопросы питания. — 2013. — Т. 82. — № 3. — С. 11–18. [Kodentsova VM, Vrzhesinskaya OA, Mazo VK. Vitamins and oxidative stress. Voprosy pitanya. 2013;82(3):11–18. (In Russ.)]
  13. Arreaza-Gil V, Escobar-Martínez I, Suárez M, et al. Gut seasons: photoperiod effects on fecal microbiota in healthy and cafeteria-induced obese Fisher 344 rats. Nutrients. 2022;14(3):722. doi: https://doi.org/10.3390/nu14030722
  14. Wee NKY, Nguyen AD, Enriquez RF, et al. Neuropeptide Y regulation of energy partitioning and bone mass during cold exposure. Calcif Tissue Int. 2020;107(5):510–523. doi: https://doi.org/10.1007/s00223-020-00745-9
  15. Shi SY, Zhang W, Luk CT, et al. JAK2 promotes brown adipose tissue function and is required for diet- and cold-induced thermogenesis in mice. Diabetologia. 2016;59(1):187–196. doi: https://doi.org/10.1007/s00125-015-3786-2
  16. Yang J, Zhang M, Zhou Y. Effects of selenium-enriched Bacillus sp. compounds on growth performance, antioxidant status, and lipid parameters breast meat quality of Chinese Huainan partridge chicks in winter cold stress. Lipids Health Dis. 2019;18(1):63. doi: https://doi.org/10.1186/s12944-019-1015-6
  17. Cui Y-M, Wang J, Zhang H-J, et al. Effects of photoperiod on performance, ovarian morphology, reproductive hormone level, and hormone receptor mRNA expression in laying ducks. Poult Sci. 2021;100(4):100979. doi: https://doi.org/10.1016/j.psj.2021.01.002
  18. Xu Q, Wang YC, Liu R, et al. Differential gene expression in the peripheral blood of Chinese Sanhe cattle exposed to severe cold stress. Genet Mol Res. 2017;16(2). doi: https://doi.org/10.4238/gmr16029593
  19. Ohsaka Y, Ohgiya S, Hoshino T, et al. Phosphorylation of c-Jun N-terminal kinase in human hepatoblastoma cells is transiently increased by cold exposure and further enhanced by subsequent warm incubation of the cells. Cell Physiol Biochem. 2002;12(2–3):111–118. doi: https://doi.org/10.1159/000063787
  20. Chang JC, Durinck S, Chen MZ, et al. Adaptive adipose tissue stromal plasticity in response to cold stress and antibody-based metabolic therapy. Sci Rep. 2019;9(1):8833. doi: https://doi.org/10.1038/s41598-019-45354-1
  21. Kuperman Y, Weiss M, Dine J, et al. CRFR1 in AgRP neurons modulates sympathetic nervous system activity to adapt to cold stress and fasting. Cell Metab. 2016;23(6):1185–1199. doi: https://doi.org/10.1016/j.cmet.2016.04.017
  22. Guo W-J, Lian S, Guo J-R, et al. Biological function prediction of mir-210 in the liver of acute cold stress rat. Sheng Li Xue Bao. 2016;68(2):165–170.
  23. Miyamoto T, Funakami Y, Kawashita E, et al. Enhanced hyperthermic responses to lipopolysaccharide in mice exposed to repeated cold stress. Pharmacology. 2017;99(3–4):172–178. doi: https://doi.org/10.1159/000454815
  24. Joo S-Y, Park M-J, Kim K-H, et al. Cold stress aggravates inflammatory responses in an LPS-induced mouse model of acute lung injury. Int J Biometeorol. 2016;60(8):1217–1225. doi: https://doi.org/10.1007/s00484-015-1116-5
  25. Asha Devi S, Manjula KR, Subramanyam MVV. Protective role of vitamins E and C against oxidative stress caused by intermittent cold exposure in aging rat’s frontoparietal cortex. Neurosci Lett. 2012;529(2):155–160. doi: https://doi.org/10.1016/j.neulet.2012.09.041
  26. Robertson CE, McClelland GB. Ancestral and developmental cold alter brown adipose tissue function and adult thermal acclimation in Peromyscus. J Comp Physiol B. 2021;191(3):589–601. doi: https://doi.org/10.1007/s00360-021-01355-z
  27. Kalaz EB, Evran B, Develi-İş S, et al. Effect of carnosine on prooxidant-antioxidant balance in several tissues of rats exposed to chronic cold plus immobilization stress. J Pharmacol Sci. 2012;120(2):98–104. doi: https://doi.org/10.1254/jphs.12107fp
  28. Syamsunarno MR, Iso T, Yamaguchi A, et al. Fatty acid binding protein 4 and 5 play a crucial role in thermogenesis under the conditions of fasting and cold stress. PLoS One. 2014;9(6):e90825. doi: https://doi.org/10.1371/journal.pone.0090825
  29. Liu Y-L, Bi H, Fan R, et al. Effect of compound nutrients on acute immobilization and cold water-immersion stress-induced changes of Th1/Th2 cytokines. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi. 2012;28(6):601–603.
  30. Авакян А.Р., Бровкина И.Л., Лазарев А.И., и др. Иммуномодулирующее действие препаратов жирорастворимых витаминов после интенсивных физических нагрузок, выполняемых при низкой температуре окружающей среды // Патологическая физиология и экспериментальная терапия. — 2002. — Т. 3. — С. 26–29. [Avakyan AR, Brovkina IL, Lazarev AI, et al. Immunomodulatory effect of fat-soluble vitamin preparations after intense physical exertion performed at low ambient temperatures. Patologicheskaya fisiologiya i eksperimentalnaya terapiya. 2002;3:26–29. (In Russ.)]
  31. Zhu P, Zhang Z-H, Huang X-F, et al. Cold exposure promotes obesity and impairs glucose homeostasis in mice subjected to a high-fat diet. Mol Med Rep. 2018;18(4):3923–3931. doi: https://doi.org/10.3892/mmr.2018.9382
  32. Пешков М.Н., Шарова Е.И., Клабуков И.Д. Использование постгеномных технологий для диагностики онкологических заболеваний на примере рака предстательной железы // Российский онкологический журнал. — 2015. — Т. 20. — № 2. — С. 29–32. [Peshkov MN, Sharova EI, Klabukov ID. The use of post-genomic technologies for the diagnosis of oncological diseases on the example of prostate cancer. Rossiyskiy onkologicheskiy zhurnal. 2015;20(2):29–32. (In Russ.)]
  33. Dutheil S, Ota KT, Wohleb ES, et al. High-fat diet induced anxiety and anhedonia: impact on brain homeostasis and inflammation. Neuropsychopharmacology. 2016;41(7):1874–1887. doi: https://doi.org/10.1038/npp.2015.357
  34. Zinder R, Cooley R, Vlad LG, et al. Vitamin A and wound healing. Nutr Clin Pract. 2019;34(6):839–849. doi: https://doi.org/10.1002/ncp.10420
  35. Camargo A, Dalmagro AP, Rikel L, et al. Cholecalciferol counteracts depressive-like behavior and oxidative stress induced by repeated corticosterone treatment in mice. Eur J Pharmacol. 2018;833:451–461. doi: https://doi.org/10.1016/j.ejphar.2018.07.002
  36. Opperhuizen AL, van Kerkhof LW, Proper KI, et al. Rodent models to study the metabolic effects of shiftwork in humans. Front Pharmacol. 2015;6:50. doi: https://doi.org/10.3389/fphar.2015.00050
  37. Eimonte M, Paulauskas H, Daniuseviciute L, et al. Residual effects of short-term whole-body cold-water immersion on the cytokine profile, white blood cell count, and blood markers of stress. Int J Hyperthermia. 2021;38(1):696–707. doi: https://doi.org/10.1080/02656736.2021.1915504
  38. Mahoney CR, Castellani J, Kramer FM, et al. Tyrosine supplementation mitigates working memory decrements during cold exposure. Physiol Behav. 2007;92(4):575–582. doi: https://doi.org/10.1016/j.physbeh.2007.05.003
  39. Liu J-Q, Hu T-Y, Diao K-Y, et al. Cold stress promotes IL-33 expression in intestinal epithelial cells to facilitate food allergy development. Cytokine. 2020;136:155295. doi: https://doi.org/10.1016/j.cyto.2020.155295
  40. Xu B, Lang L-M, Li S-Z, et al. Cortisol excess-mediated mitochondrial damage induced hippocampal neuronal apoptosis in mice following cold exposure. Cells. 2019;8(6):612. doi: https://doi.org/10.3390/cells8060612
  41. Sahin E, Gumuslu S. Cold-stress-induced modulation of antioxidant defence: role of stressed conditions in tissue injury followed by protein oxidation and lipid peroxidation. Int J Biometeorol. 2004;48(4):165–171. doi: https://doi.org/10.1007/s00484-004-0205-7
  42. Shu L, Hoo RL, Wu X, et al. A-FABP mediates adaptive thermogenesis by promoting intracellular activation of thyroid hormones in brown adipocytes. Nat Commun. 2017;8:14147. doi: https://doi.org/10.1038/ncomms14147
  43. Belay T, Woart A, Graffeo V. Effect of cold water-induced stress on immune response, pathology and fertility in mice during Chlamydia muridarum genital infection. Pathog Dis. 2017;75(5):ftx045. doi: https://doi.org/10.1093/femspd/ftx045
  44. Liu Y-Z, Guo J-R, Peng M-L, et al. Screening differentially expressed plasma proteins in cold stress rats based on iTRAQ combined with mass spectrometry technology. Zhongguo Ying Yong Sheng Li Xue Za Zhi. 2015;31(5):392–395,400.
  45. Pernes G, Morgan PK, Huynh K, et al. Characterization of the circulating and tissue-specific alterations to the lipidome in response to moderate and major cold stress in mice. Am J Physiol Regul Integr Comp Physiol. 2021;320(2):R95–R104. doi: https://doi.org/10.1152/ajpregu.00112.2020
  46. Guo W-J, Lian S, Guo J-R, et al. Biological function prediction of mir-210 in the liver of acute cold stress rat. Sheng Li Xue Bao. 2016;68(2):165–170.
  47. Guo W, Lian S, Zhen L, et al. The favored mechanism for coping with acute cold stress: upregulation of miR-210 in rats. Cell Physiol Biochem. 2018;46(5):2090–2102. doi: https://doi.org/10.1159/000489449
  48. Xu B, Lian S, Guo J-R, et al. Activation of the MAPK signaling pathway induces upregulation of pro-apoptotic proteins in the hippocampi of cold stressed adolescent mice. Neurosci Lett. 2019;699:97–102. doi: https://doi.org/10.1016/j.neulet.2018.12.028
  49. Dempersmier J, Sambeat A, Gulyaeva O, et al. Cold-inducible Zfp516 activates UCP1 transcription to promote browning of white fat and development of brown fat. Mol Cell. 2015;57(2):235–246. doi: https://doi.org/10.1016/j.molcel.2014.12.005
  50. Fan G, Li Y, Ma F, et al. Zinc-α2-glycoprotein promotes skeletal muscle lipid metabolism in cold-stressed mice. Endocr J. 2021;68(1):53–62. doi: https://doi.org/10.1507/endocrj.EJ20-0179
  51. Weiner J, Rohde K, Krause K, et al. Brown adipose tissue (BAT) specific vaspin expression is increased after obesogenic diets and cold exposure and linked to acute changes in DNA-methylation. Mol Metab. 2017;6(6):482–493. doi: https://doi.org/10.1016/j.molmet.2017.03.004
  52. Putri M, Syamsunarno MR, Iso T, et al. CD36 is indispensable for thermogenesis under conditions of fasting and cold stress. Biochem Biophys Res Commun. 2015;457(4):520–525. doi: https://doi.org/10.1016/j.bbrc.2014.12.124
  53. Martarelli D, Cocchioni M, Scuri S, et al. Cold exposure increases exercise-induced oxidative stress. J Sports Med Phys Fitness. 2011;51(2):299–304.
  54. Гейн С.В., Шаравьева И.Л. Влияние холодового стресса на функциональную активность перитонеальных макрофагов мыши в условиях блокады опиатных рецепторов // Российский физиологический журнал им. И.М.Сеченова. — 2016. — Т. 102. — № 2. — С. 188–194. [Gein SV, Sharav’eva IL. The effect of cold stress on the functional activity of mouse peritoneal macrophages under conditions of blockade of opiate receptors. Rossiyskiy fiziologicheskiy zhurnal im. I.M.Sechenova. 2016;102(2):188–194. (In Russ.)]
  55. Yildirim NC, Yurekli M. The effect of adrenomedullin and cold stress on interleukin-6 levels in some rat tissues. Clin Exp Immunol. 2010;161(1):171–175. doi: https://doi.org/10.1111/j.1365-2249.2010.04156.x
  56. Xu B, Lang L-M, Lian S, et al. Neuroinflammation induced by secretion of acetylated HMGB1 from activated microglia in hippocampi of mice following chronic cold exposure. Brain Res. 2020;1726:146495. doi: https://doi.org/10.1016/j.brainres.2019.146495
  57. LaVoy EC, McFarlin BK, Simpson RJ. Immune responses to exercising in a cold environment. Wilderness Environ Med. 2011;22(4):343–351. doi: https://doi.org/10.1016/j.wem.2011.08.005
  58. Chan P-C, Hung L-M, Huang J-P, et al. Augmented CCL5/ CCR5 signaling in brown adipose tissue inhibits adaptive thermogenesis and worsens insulin resistance in obesity. Clin Sci (Lond). 2022;136(1):121–137. doi: https://doi.org/10.1042/CS20210959
  59. Piao Z, Zhai B, Jiang X, et al. Reduced adiposity by compensatory WAT browning upon iBAT removal in mice. Biochem Biophys Res Commun. 2018;501(3):807–813. doi: https://doi.org/10.1016/j.bbrc.2018.05.089
  60. Pandit C, Sai Latha S, Usha Rani T, et al. Pepper and cinnamon improve cold induced cognitive impairment via increasing non-shivering thermogenesis; a study. Int J Hyperthermia. 2018;35(1):518–527. doi: https://doi.org/10.1080/02656736.2018.1511835
  61. Jones DM, Bailey SP, De Pauw K, et al. Evaluation of cognitive performance and neurophysiological function during repeated immersion in cold water. Brain Res. 2019;1718:1–9. doi: https://doi.org/10.1016/j.brainres.2019.04.032
  62. Torki M, Akbari M, Kaviani K. Single and combined effects of zinc and cinnamon essential oil in diet on productive performance, egg quality traits, and blood parameters of laying hens reared under cold stress condition. Int J Biometeorol. 2015;59(9):1169–1177. doi: https://doi.org/10.1007/s00484-014-0928-z
  63. Murad N, Takiuchi K, Lopes AC, et al. Coenzyme Q10 exogenous administration attenuates cold stress cardiac injury. Jpn Heart J. 2001;42(3):327–338. doi: https://doi.org/10.1536/jhj.42.327
  64. Kolosova ON, Kershengolts BM. Stabilization of homeostasis in rats during cold exposure with ethanol. Bull Exp Biol Med. 2016;160(3):300–303. doi: https://doi.org/10.1007/s10517-016-3156-1

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