UDC

[612.79+612.882](045)

DOI

10.17238/issn2542-1298.2019.7.1.92

Authors

Aleksey A. Medvedev*, Lyudmila V. Sokolova*
*Northern (Arctic) Federal University named after M.V. Lomonosov (Arkhangelsk, Russian Federation)

Abstract

Thermoreceptor function of the human body helps to maintain optimal body temperature, which is highly important for the normal course of all physiological processes. The key element in the system of temperature perception are receptors located in the skin and internal organs and responding to changes in the temperature of the environment. This article covers the development of the ideas about the work of the human thermosensory system: from the moment of its discovery and morphological description to the study of its molecular structure. In addition, the paper describes the mechanisms beyond the activity of temperature receptors forming polymodal receptive fields in different areas of the skin surface. Further, the physiological role of receptors located in different parts of the body is shown. The authors emphasize that modern classification of thermoreceptors is based not only on the sensitivity to changes in temperature, but also on the differences in their molecular structure; in particular, this applies to receptors of TRPA, TRPV and TRPM families. The paper provides data obtained by Russian and foreign authors on the functioning of receptors under different environmental conditions: at low and elevated temperatures, in normobaric hypoxia, as well as under the influence of various internal physiological factors such as sex, age, and others. It is shown that a change in temperature can directly affect the conformation and structure of biological macromolecules, e.g. proteins that are part of cell membranes and cause their permeability to various ions forming membrane potential. Further, the article dwells on the studies into the genetic aspects of functioning of thermoreceptors. It is assumed that encoding of information about the structure of ion channels is determined by different polymorphic gene variants. The authors emphasize the importance of studying the genetic basis of temperature sensitivity in different human populations that are initially adapted to different temperatures. New insights into this issue could significantly deepen our understanding of the mechanisms triggering human adaptation to changes in temperature.

Keywords

temperature sensitivity, thermoreceptors, ion channels, receptor adaptation, receptive fields

References

1. Filingeri D. Neurophysiology of Skin Thermal Sensations. Compr. Physiol., 2016, vol. 6, no. 3, pp. 1279–1294.
2. Zotterman Y. Special Senses: Thermal Receptors. Annu. Rev. Physiol., 1953, no. 15, pp. 357–372.
3. Cain D.M., Khasabov S.G., Simone D.A. Response Properties of Mechanoreceptors and Nociceptors in Mouse Glabrous Skin: An in vivo Study. J. Neurophysiol., 2001, vol. 85, no. 4, pp. 1561–1574.
4. Mano H., Yoshida W., Shibata K., Zhang S., Koltzenburg M., Kawato M., Seymour B. Thermosensory Perceptual Learning Is Associated with Structural Brain Changes in Parietal-Opercular (SII) Cortex. J. Neurosci., 2017, vol. 37, no. 39, pp. 9380 –9388.
5. Ulashchik V.S. Retseptory kozhi i lechebnye fizicheskie faktory [Skin Receptors and Therapeutic Physical Factors]. Voprosy kurortologii, fizioterapii i lechebnoy fizicheskoy kul’tury, 2017, vol. 94, no. 5, pp. 48–57.
6. Digel I. Primary Thermosensory Events in Cells. Adv. Exp. Med. Biol., 2011, vol. 704, pp. 451–468.
7. Mickle A.D., Shepherd A.J., Mohapatra D.P. Sensory TRP Channels: The Key Transducers of Nociception and Pain. Prog. Mol. Biol. Transl. Sci., 2015, vol. 131, pp. 73–118.
8. Borodin E.A., Borodin P.E. TRP-retseptory. Bioinformaticheskaya kharakteristika [TRP Receptors. Bioinformatics Characteristics]. Kolosov V.P. (ed.). Sistemnyy analiz v meditsine (SAM 2016) [Systems Analysis in Medicine (CAM 2016)]. Blagoveshchensk, 2016, pp. 28–30.
9. Bertin S., Raz E. Transient Receptor Potential (TRP) Channels in T Cells. Semin. Immunopathol., 2016, vol. 38, no. 3, pp. 309–319.
10. Kozyreva T.V., Voronova I.P. Vovlechenie neyrogenomnogo urovnya regulyatsii v protsessy podderzhaniya temperaturnogo gomeostaza organizma na kholode [Involvement of Neurogenomic Regulation in the Maintenance of Temperature Homeostasis in the Cold]. Vavilovskiy zhurnal genetiki i selektsii, 2014, vol. 18, no. 4/3, pp. 1100–1109.
11. Schäfer K., Braun H.A., Hensel H. Static and Dynamic Activity of Cold Receptors at Various Calcium Levels. J. Neurophysiol., 1982, vol. 47, no. 6, pp. 1017–1028.
12. Glossary of Terms for Thermal Physiology. Jpn. J. Physiol., 2001, vol. 51, no. 2, pp. 245–280. 13. Zhang X. Molecular Sensors and Modulators of Thermoreception. Channels (Austin), 2015, vol. 9, no. 2, pp. 73–81.
14. Babenko V.N., Isakova Zh.T., Talaybekova E.T., Asambaeva D.A., Kobzev V.F., Potapova T.A., Voevoda M.I., Aldashev A.A. Polimorfizm gena TRPM8 v kyrgyzskoy populyatsii: vozmozhnaya svyaz’ s vysokogornoy adaptatsiey [Polymorphism in the TRPM8 Gene in Kyrgyz Population: Putative Association with Highland Adaptation]. Vavilovskiy zhurnal genetiki i selektsii, 2015, vol. 19, no. 5, pp. 630–637.
15. Kozyreva T.V., Tkachenko E.Ya., Potapova T.A., Romashchenko A.G., Voevoda M.I. Single-Nucleotide Polymorphism rs11562975 of the Thermosensitive Ion Channel TRPM8 Gene and Human Sensitivity to Cold and Menthol. Hum. Physiol., 2011, vol. 37, no. 2, pp. 188–192.
16. Sabnis A.S., Shadid M., Yost G.S., Reilly C.A. Human Lung Epithelial Cells Express a Functional Cold-Sensing TRPM8 Variant. Am. J. Respir. Cell Mol. Biol., 2008, vol. 39, no. 4, pp. 466–474.
17. Hensel H., Schäfer K. Thermoreception and Temperature Regulation in Man. Ring E.F.J., Phillips B. (eds.). Recent Advances in Medical Thermology. Boston, 1984, pp. 51−64.
18. Yarmolinsky D.A., Peng Y., Pogorzala L.A., Rutlin M., Hoon M.A., Zuker C.S. Coding and Plasticity in the Mammalian Thermosensory System. Neuron, 2016, vol. 92, no. 5, pp. 1079–1092.
19. Bocharov M.I. Termoregulyatsiya organizma pri kholodovykh vozdeystviyakh (obzor). Soobshchenie I [Thermoregulation in Cold Environments (Review). Report I]. Vestnik Severnogo (Arkticheskogo) federal’nogo universiteta. Ser.: Mediko-biologicheskie nauki, 2015, no. 1, pp. 5–15.
20. Kozyreva T.V., Verkhoglyad L.A. Funktsional’noe znachenie dinamicheskoy aktivnosti kholodovykh retseptorov kozhi [Functional Role of the Dynamic Activity of Cold Skin Receptors]. Fiziologicheskiy zhurnal SSSR im. I.M. Sechenova, 1989, vol. 75, no. 1, pp. 117–123.
21. Baytinger V.F., Nikulin A.A. Funktsional’nye metody issledovaniya chuvstvitel’nosti pal’tsev kisti [Functional Research Methods of Hand Fingers’ Sensitivity]. Voprosy rekonstruktivnoy i plasticheskoy khirurgii, 2013, vol. 16, no. 1, pp. 42–45.
22. Huang J., Zhang X., McNaughton P.A. Modulation of Temperature-Sensitive TRP Channels. Semin. Cell Dev. Biol., 2006, vol. 17, no. 6, pp. 638–645.
23. Kenshalo R. Correlations of Temperature Sensation and Neural Activity: A Second Approximation. Bligh J., Voigt K., Braun H.A., Brück K., Heldmaier G. (eds.). Thermoreception and Thermoregulation. Berlin, 1990, pp. 67–88.
24. Mitrukhina O., Minlebaev M., Khazipov R. Geneticheskie i epigeneticheskie mekhanizmy formirovaniya somatosensornykh kart v kore golovnogo mozga [Genetic and Epigenetic Mechanisms of Sensory Maps Development]. Geny & Kletki, 2015, vol. 10, no. 3, pp. 6–11.
25. Darian-Smith I., Johnson K.O. Thermal Sensibility and Thermal Receptors. J. Investig. Dermatol., 1977, vol. 69, no. 1, pp. 146–153.
26. Hensel H., Schäfer K. Static and Dynamic Activity of Cold Receptors in Cats After Long-Term Exposure to Various Temperatures. Pflugers Arch., 1982, vol. 392, no. 3, pp. 291−294.
27. Sinitskaya E.Yu., Prokopchuk N.N. Temperaturnaya chuvstvitel’nost’ u studentov-severyan s raznym urovnem trevozhnosti [Thermal Sensitivity of Northern Students with Different Anxiety Levels]. Vestnik Severnogo (Arkticheskogo) federal’nogo universiteta. Ser.: Mediko-biologicheskie nauki, 2013, no. 2, pp. 64–70.
28. Divert V.E. The Influence of the Rate of Stimulus Temperature Rise on Local Skin Thermal Thresholds. Hum. Physiol., 2002, vol. 28, no. 5, pp. 575–580.
29. Parsons K. Human Thermal Environments: The Effects of Hot, Moderate and Cold on Human Health, Comfort and Performance. London, 2001. 527 p.
30. Green B.G. Temperature Perception and Nociception. J. Neurobiol., 2004, vol. 61, no. 1, pp. 13–29.
31. Zhang H., Huizenga C., Arens E., Wang D. Thermal Sensation and Comfort in Transient Non-Uniform Thermal Environments. Eur. J. Appl. Physiol., 2004, vol. 92, no. 6, pp. 728–733.
32. Silina E.V., Strokov I.A., Akhmedzhanova L.T., Shalygin V.S., Drokonova O.O., Suslova E.Yu., Shagbazyan A.E. Neyrofiziologiya temperaturnoy chuvstvitel’nosti [Thermal Sense Neurophysiology]. Vestnik nevrologii, psikhiatrii i neyrokhirurgii, 2015, no. 11–12, pp. 71–80.
33. Alamri A.S., Wood R.J., Ivanusic J.J., Brock J.A. The Neurochemistry and Morphology of Functionally Identified Corneal Polymodal Nociceptors and Cold Thermoreceptors. PLoS One, 2018, vol. 13, no. 3. Art. no. e0195108.
34. Arens E., Zhang H., Huizenga C. Partial- and Whole-Body Thermal Sensation and Comfort – Part I: Uniform Environmental Conditions. J. Therm. Biol., 2006, vol. 31, no. 1–2, pp. 53–59.
35. Burgess K.R., Whitelaw W.A. Effects of Nasal Cold Receptors on Pattern of Breathing. J. Appl. Physiol., 1988, vol. 64, no. 1, pp. 371–376.
36. Pellerin N., Deschuyteneer A., Candas V. Local Thermal Unpleasantness and Discomfort Prediction in the Vicinity of Thermoneutrality. Eur. J. Appl. Physiol., 2004, vol. 92, no. 6, pp. 717–720.
37. Divert V.E. Vliyanie mestnykh barometricheskikh vozdeystviy na porogi kozhnykh termooshchushcheniy [Local Barometric Influences on Thresholds of Skin Thermal Sensations]. Sensornye sistemy, 2004, vol. 18, no. 1, pp. 56–64.
38. Mglinets V.A. Geneticheskie osnovy kozhnoy chuvstvitel’nosti [Genetic Basis of Skin Sensitivity]. Uspekhi sovremennoy biologii, 2014, vol. 134, no. 6, pp. 531–544.
39. Divert V.E. Vliyanie blokady NO-sintazy na temperaturnuyu chuvstvitel’nost’ i kozhnyy krovotok [The Influence of NO-Synthase Blockade on Thermal Sensitivity and Skin Blood Flow]. Sensornye sistemy, 2011, vol. 25, no. 2, pp. 165–173.
40. Divert V.E. Temperaturnaya chuvstvitel’nost’ kozhi pri gipoksii [Thermal Sensitivity of the Skin in Hypoxia]. Rossiyskiy fiziologicheskiy zhurnal im. I.M. Sechenova, 2004, vol. 90, no. 8, p. 40.
41. Schellen L., Van Marken Lichtenbelt W.D., Loomans M.G.L.C., Toftum J., De Wit M.H. Differences Between Young Adults and Elderly in Thermal Comfort, Productivity, and Thermal Physiology in Response to a Moderate Temperature Drift and a Steady-State Condition. Indoor Air, 2010, vol. 20, no. 4, pp. 273–283.
42. Skedung L., El Rawadi C., Arvidsson M., Farcet C., Luengo G.S., Breton L., Rutland M.W. Mechanisms of Tactile Sensory Deterioration Amongst the Elderly. Sci. Rep., 2018, vol. 8, no. 1. Art. no. 5303.
43. Sychev V.S., Davydova S.S. Kozhnaya chuvstvitel’nost’ pal’tsev u yunoshey i devushek s raznym profilem manual’noy asimmetrii [Skin Sensitivity of Fingers in Boys and Girls with Different Profiles of Manual Asymmetry]. Neyronauka dlya meditsiny i psikhologii [Neuroscience for Medicine and Psychology]. Moscow, 2017, p. 399.
44. Shchurova E.N., Tropina E.Yu. Osobennosti negativnykh izmeneniy temperaturno-bolevoy chuvstvitel’nosti u bol’nykh s poyasnichnym osteokhondrozom pozvonochnika [Peculiarities of Negative Temperature-Pain Susceptibility Changes in Patients with Lumbar Spinal Osteochondrosis]. Permskiy meditsinskiy zhurnal, 2012, vol. 29, no. 2, pp. 5–12.
45. Divert V.E. Perifericheskaya termoretseptsiya pri razlichnykh funktsional’nykh sostoyaniyakh organizma [Peripheral Thermoreception in Different Functional States of the Body: Diss. Abs.]. Novosibirsk, 2008. 32 p.
46. Orlov G.A. Khronicheskoe porazhenie kholodom [Chronic Cold Injury]. Leningrad, 1978. 168 p.
47. Levina G.Yu., Bykov Yu.N., Borisov A.S. Diagnostika i lechenie perifericheskoy neyropaticheskoy boli (obzor literatury) [Diagnostics and Therapy of Peripheral Neuropathy (Literature Review)]. Byulleten’ VSNTs SO RAMN, 2015, no. 1, pp. 72–76.
48. Kozyreva T.V., Evtushenko A.A., Voronova I.P., Khramova G.M., Kozaruk V.P. Vliyanie ostrogo okhlazhdeniya na ekspressiyu genov termochuvstvitel’nykh TRP ionnykh kanalov v gipotalamuse [Effect of Acute Cooling on the Expression of the Thermosensitive TRP Ion Channel Genes in Hypothalamus]. Rossiyskiy fiziologicheskiy zhurnal im. I.M. Sechenova, 2017, vol. 103, no. 11, pp. 1260–1269.
49. Wadood A., Ur Rehman A., Shams S., Khan М., Ur Rahman T., Jamal S.B., Khan A., Ahmad A., Ali F. Homology Modeling, Molecular Dynamic Simulation and Phylogenetic Analysis of Human Transient Receptor Potential Melastatin 1 (TRPM1). Int. J. Comput. Bioinfo. In Silico Model., 2014, vol. 3, no. 3, pp. 381–387.
50. Medvedev A.A. Kholodovaya chuvstvitel’nost’ kozhi yuzhnoaziatskikh studentov v nachal’nyy period adaptatsii k usloviyam Evropeyskogo Severa [Skin Sensitivity to Cold in South Asian Students During the Initial Period of Adaptation to the Conditions of the European North]. Arkticheskie issledovaniya: ot ekstensivnogo osvoeniya k kompleksnomu razvitiyu [Arctic Research: From Extensive Exploration to Integrated Development]. Arkhangelsk, 2018. Vol. 1, pp. 197–200.
51. Panchenko L.S. Izuchenie dinamiki fiziologicheskoy adaptatsii inostrannykh studentov k rezko kontinental’nomu klimatu Rossii [Studying the Dynamics of Physiological Adaptation of Foreign Students to Russia’s Severe Continental Climate]. Rol’ nauki v razvitii sotsiuma: teoreticheskie i prakticheskie aspekty [The Role of Science in the Development of Society: Theoretical and Practical Aspects]. St. Petersburg, 2018, pp. 21–23.