Research progress on the role of cold-sensitive channel TRPM8 in controlling low temperature-induced bone metabolic imbalance

Yimeng Zhang; E. V Kazakova; Huijuan Chai; Ping Zhou

doi:10.2478/fzm-2023-0027

Research progress on the role of cold-sensitive channel TRPM8 in controlling low temperature-induced bone metabolic imbalance

doi: 10.2478/fzm-2023-0027

1.
Department of Geriatrics, The Second Affiliated Hospital of Harbin Medical University, Harbin 150086, China
2.
State Budgetary Health Institution "Regional Clinical Hospital No. 2", Vladivostok 690000, Russia

More Information

Corresponding author: Ping Zhou, E-mail: 541427890@qq.com

摘要

Abstract: With increasing aging population, osteoporosis has emerged as a public health problem worldwide. Epidemiological data reveal that the prevalence of osteoporosis in cold regions is high, and low temperatures may crucially affect bone mass. Recent studies have found that the transient receptor potential melastatin-8 (TRPM8) channel, a cold-sensitive ion channel, can sense cold environment, and can be activated in cold environment. It may play an antagonistic role in low temperature-induced bone mass reduction. Mechanistically, this function may be ascribed to the activation of TRPM8 channel proteins in human bone marrow mesenchymal stem cells (hBM-MSCs), which causes osteoblast differentiation and mineralization in the bone. TRPM8 channel on the surface of brown adipocytes participates in the thermogenesis in brown adipose tissue (BAT) and the regulation of whole-body energy balance to maintain bone homeostasis. TRPM8 may be involved in bone remodeling throughout life. This paper reviews recent research on the possible antagonistic mechanism of TRPM8 in signaling pathways related to low temperature-induced bone mass loss and assesses the possibility of TRPM8 as a molecular target for the prevention and treatment of low temperature-induced osteoporosis in cold regions.
- TRPM8 /
- low temperature /
- osteoporosis /
- bone mass

HTML全文

参考文献(71)

[1]	Bolamperti S, Villa I, Rubinacci A. Bone remodeling: an operational process ensuring survival and bone mechanical competence. Bone Res, 2022; 10(1): 48. doi: 10.1038/s41413-022-00219-8
[2]	Wang L, You X, Zhang L, et al. Mechanical regulation of bone remodeling. Bone Res, 2022; 10(1): 16. doi: 10.1038/s41413-022-00190-4
[3]	Zhao Q, Guo Y, Ye T, et al. Global, regional, and national burden of mortality associated with non-optimal ambient temperatures from 2000 to 2019: a three-stage modelling study. Lancet Planet Health, 2021; 5(7): e415-e425. doi: 10.1016/S2542-5196(21)00081-4
[4]	Chen R, Yin P, Wang L, et al. Association between ambient temperature and mortality risk and burden: time series study in 272 main Chinese cities. BMJ, 2018; 363: k4306.
[5]	Ebi K L, Capon A, Berry P, et al. Hot weather and heat extremes: health risks. Lancet, 2021; 398(10301): 698-708. doi: 10.1016/S0140-6736(21)01208-3
[6]	Romanello M, McGushin A, Di Napoli C, et al. The 2021 report of the Lancet Countdown on health and climate change: code red for a healthy future. Lancet, 2021; 398(10311): 1619-1662. doi: 10.1016/S0140-6736(21)01787-6
[7]	Dahl C, Madsen C, Omsland T K, et al. The Association of Cold Ambient Temperature With Fracture Risk and Mortality: National Data From Norway-A Norwegian Epidemiologic Osteoporosis Studies (NOREPOS) Study. J Bone Miner Res, 2022; 37(8): 1527-1536. doi: 10.1002/jbmr.4628
[8]	Nishimura H, Nawa N, Ogawa T, et al. Association of ambient temperature and sun exposure with hip fractures in Japan: a time-series analysis using nationwide inpatient database. Sci Total Environ, 2022; 807(Pt 1): 150774.
[9]	Johnson N A, Stirling E, Alexander M, et al. The relationship between temperature and hip and wrist fracture incidence. Ann R Coll Surg Engl, 2020; 102(5): 348-354. doi: 10.1308/rcsann.2020.0030
[10]	Johansen A, Grose C, Havelock W. Hip fractures in the winter—using the National hip Fracture Database to examine seasonal variation in incidence and mortality. Injury, 2020; 51(4): 1011-1014. doi: 10.1016/j.injury.2020.02.088
[11]	Koizia L J, Dani M, Brown H, et al. Does the weather contribute to admissions of neck of femur fractures? GeriatrOrthop Surg Rehabil, 2021; 12: 2151459320987702.
[12]	Kang T, Hong J, Radnaabaatar M, et al. Effect of meteorological factors and air pollutants on fractures: a nationwide population-based ecological study. BMJ Open, 2021; 11(6): e047000. doi: 10.1136/bmjopen-2020-047000
[13]	Watts N, Amann M, Arnell N, et al. The 2018 report of the Lancet Countdown on health and climate change: shaping the health of nations for centuries to come. Lancet, 2018; 392(10163): 2479-2514. doi: 10.1016/S0140-6736(18)32594-7
[14]	Serrat M A. Environmental temperature impact on bone and cartilage growth. ComprPhysiol, 2014; 4(2): 621-655.
[15]	Robbins A, Tom C, Cosman M N, et al. Low temperature decreases bone mass in mice: Implications for humans. Am J Phys Anthropol, 2018; 167(3): 557-568. doi: 10.1002/ajpa.23684
[16]	Serrat M A, King D, Lovejoy C O. Temperature regulates limb length in homeotherms by directly modulating cartilage growth. Proc Natl Acad Sci U S A, 2008; 105(49): 19348-19353. doi: 10.1073/pnas.0803319105
[17]	Serrat M A, Williams R M, Farnum C E. Exercise mitigates the stunting effect of cold temperature on limb elongation in mice by increasing solute delivery to the growth plate. J Appl Physiol (1985), 2010; 109(6): 1869-1879. doi: 10.1152/japplphysiol.01022.2010
[18]	Zheng J. Molecular mechanism of TRP channels. ComprPhysiol, 2013; 3(1): 221-242.
[19]	Yue L, Xu H. TRP channels in health and disease at a glance. J Cell Sci, 2021; 134(13): jcs258372. doi: 10.1242/jcs.258372
[20]	Cheng W, Zheng J. Distribution and Assembly of TRP Ion Channels. Adv Exp Med Biol, 2021; 1349: 111-138.
[21]	Naziroğlu M, Braidy N. Thermo-Sensitive TRP Channels: Novel Targets for Treating Chemotherapy-Induced Peripheral Pain. Front Physiol, 2017; 8: 1040. doi: 10.3389/fphys.2017.01040
[22]	Vay L, Gu C, McNaughton P A. The thermo-TRP ion channel family: properties and therapeutic implications. Br J Pharmacol, 2012; 165(4): 787-801. doi: 10.1111/j.1476-5381.2011.01601.x
[23]	Gees M, Owsianik G, Nilius B, et al. TRP channels. ComprPhysiol, 2012; 2(1): 563-608.
[24]	Himmel N J, Cox D N. Sensing the cold: TRP channels in thermal nociception. Channels (Austin), 2017; 11(5): 370-372. doi: 10.1080/19336950.2017.1336401
[25]	Lolignier S, Gkika D, Andersson D, et al. New Insight in Cold Pain: Role of Ion Channels, Modulation, and Clinical Perspectives. J Neurosci, 2016; 36(45): 11435-11439. doi: 10.1523/JNEUROSCI.2327-16.2016
[26]	Sakaguchi R, Mori Y. Transient receptor potential (TRP) channels: Biosensors for redox environmental stimuli and cellular status. Free Radic Biol Med, 2020; 146: 36-44. doi: 10.1016/j.freeradbiomed.2019.10.415
[27]	Kashio M, Tominaga M. TRP channels in thermosensation. CurrOpinNeurobiol, 2022; 75: 102591.
[28]	Di Donato M, Ostacolo C, Giovannelli P, et al. Therapeutic potential of TRPM8 antagonists in prostate cancer. Sci Rep, 2021; 11(1): 23232. doi: 10.1038/s41598-021-02675-4
[29]	Kaneko Y, Szallasi A. Transient receptor potential (TRP) channels: a clinical perspective. Br J Pharmacol, 2014; 171(10): 2474-2507. doi: 10.1111/bph.12414
[30]	Liu Y, Mikrani R, He Y, et al. TRPM8 channels: A review of distribution and clinical role. Eur J Pharmacol, 2020; 882: 173312. doi: 10.1016/j.ejphar.2020.173312
[31]	Basbaum A I, Bautista D M, Scherrer G, et al. Cellular and molecular mechanisms of pain. Cell, 2009; 139(2): 267-284. doi: 10.1016/j.cell.2009.09.028
[32]	Huang Y, Fliegert R, Guse A H, et al. A structural overview of the ion channels of the TRPM family. Cell Calcium, 2020; 85: 102111. doi: 10.1016/j.ceca.2019.102111
[33]	Yin Y, Le S C, Hsu A L, et al. Structural basis of cooling agent and lipid sensing by the cold-activated TRPM8 channel. Science, 2019; 363(6430): eaav9334. doi: 10.1126/science.aav9334
[34]	Dhaka A, Murray A N, Mathur J, et al. TRPM8 is required for cold sensation in mice. Neuron, 2007; 54(3): 371-378. doi: 10.1016/j.neuron.2007.02.024
[35]	Weyer-Menkhoff I, Pinter A, Schlierbach H, et al. Epidermal expression of human TRPM8, but not of TRPA1 ion channels, is associated with sensory responses to local skin cooling. Pain, 2019; 160(12): 2699-2709. doi: 10.1097/j.pain.0000000000001660
[36]	Bautista D M, Siemens J, Glazer J M, et al. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature, 2007; 448(7150): 204-208. doi: 10.1038/nature05910
[37]	Koivisto A P, Belvisi M G, Gaudet R, et al. Advances in TRP channel drug discovery: from target validation to clinical studies. Nat Rev Drug Discov, 2022; 21(1): 41-59. doi: 10.1038/s41573-021-00268-4
[38]	Liu Y, Mikrani R, He Y, et al. TRPM8 channels: A review of distribution and clinical role. Eur J Pharmacol, 2020; 882: 173312. doi: 10.1016/j.ejphar.2020.173312
[39]	Henao J C, Grismaldo A, Barreto A, et al. TRPM8 Channel Promotes the Osteogenic Differentiation in Human Bone Marrow Mesenchymal Stem Cells. Front Cell Dev Biol, 2021; 9: 592946. doi: 10.3389/fcell.2021.592946
[40]	Song L. Calcium and Bone Metabolism Indices. Adv Clin Chem, 2017; 82: 1-46.
[41]	Reid I R, Bristow S M. Calcium and Bone. Handb Exp Pharmacol, 2020; 262: 259-280.
[42]	Bristow S M, Bolland M J, Gamble G D, et al. Dietary calcium intake and change in bone mineral density in older adults: a systematic review of longitudinal cohort studies. Eur J Clin Nutr, 2022; 76(2): 196-205. doi: 10.1038/s41430-021-00957-8
[43]	Fliniaux I, Germain E, Farfariello V, et al. TRPs and Ca(2+) in cell death and survival. Cell Calcium, 2018; 69: 4-18. doi: 10.1016/j.ceca.2017.07.002
[44]	Lieben L, Carmeliet G. The Involvement of TRP Channels in Bone Homeostasis. Front Endocrinol (Lausanne), 2012; 3: 99.
[45]	Bidaux G, Borowiec A S, Gordienko D, et al. Epidermal TRPM8 channel isoform controls the balance between keratinocyte proliferation and differentiation in a cold-dependent manner. Proc Natl Acad Sci U S A, 2015; 112(26): E3345-E3354.
[46]	Lelis Carvalho A, Treyball A, Brooks D J, et al. TRPM8 modulates temperature regulation in a sex-dependent manner without affecting cold-induced bone loss. PLoS One, 2021; 16(6): e0231060. doi: 10.1371/journal.pone.0231060
[47]	Johnson N A, Stirling E, Dias J J. The effect of mean annual temperature on the incidence of distal radial fractures. J Hand Surg Eur, 2018; 43(9): 983-987. doi: 10.1177/1753193418797893
[48]	Johnson N A, Stirling E, Alexander M, et al. The relationship between temperature and hip and wrist fracture incidence. Ann R Coll Surg Engl, 2020; 102(5): 348-354. doi: 10.1308/rcsann.2020.0030
[49]	Hoff M, Torvik I A, Schei B. Forearm fractures in Central Norway, 1999-2012: incidence, time trends, and seasonal variation. Arch Osteoporos, 2016; 11: 7. doi: 10.1007/s11657-016-0257-4
[50]	Al-Azzani W, Adam MaliqMak D, Hodgson P, et al. Epidemic of fractures during a period of snow and ice: has anything changed 33 years on? BMJ Open, 2016; 6(9): e010582. doi: 10.1136/bmjopen-2015-010582
[51]	Uchida K, Dezaki K, Yoneshiro T, et al. Involvement of thermosensitive TRP channels in energy metabolism. JPS, 2017; 67(5): 549-560.
[52]	Lv J, Tang L, Zhang X, et al. Thermo-TRP channels are involved in BAT thermoregulation in cold-acclimated Brandt's voles. Comp BiochemPhysiol B Biochem Mol Biol, 2022; 263: 110794.
[53]	Reimundez A, Fernandez-Pena C, Garcia G, et al. Deletion of the cold thermoreceptor TRPM8 increases heat loss and food intake leading to reduced body temperature and obesity in mice. J Neurosci, 2018; 38(15): 3643-3656. doi: 10.1523/JNEUROSCI.3002-17.2018
[54]	Lee P, Brychta R J, Collins M T, et al. Cold-activated brown adipose tissue is an independent predictor of higher bone mineral density in women. Osteoporos Int, 2013; 24(4): 1513-1518. doi: 10.1007/s00198-012-2110-y
[55]	Bredella M A, Fazeli P K, Lecka-Czernik B, et al. IGFBP-2 is a negative predictor of cold-induced brown fat and bone mineral density in young non-obese women. Bone, 2013; 53(2): 336-339. doi: 10.1016/j.bone.2012.12.046
[56]	Devlin M J. The "Skinny" on brown fat, obesity, and bone. Am J Phys Anthropol, 2015; 156 Suppl 59: 98-115.
[57]	Lidell M E, Enerbäck S. Brown adipose tissue and bone. International journal of obesity supplements. 2015; 5(Suppl 1): S23-S27.
[58]	Motyl K J, Bishop K A, DeMambro V E, et al. Altered thermogenesis and impaired bone remodeling in Misty mice. J Bone Miner Res, 2013; 28(9): 1885-1897. doi: 10.1002/jbmr.1943
[59]	Bredella M A, Gill C M, Rosen C J, et al. Positive effects of brown adipose tissue on femoral bone structure. Bone, 2014; 58: 55-58. doi: 10.1016/j.bone.2013.10.007
[60]	Du J, He Z, Xu M, et al. Brown Adipose Tissue Rescues Bone Loss Induced by Cold Exposure. Front Endocrinol (Lausanne), 2021; 12: 778019.
[61]	Ponrartana S, Aggabao P C, Hu H H, et al. Brown adipose tissue and its relationship to bone structure in pediatric patients. J Clin Endocrinol Metab, 2012; 97(8): 2693-2698. doi: 10.1210/jc.2012-1589
[62]	Bredella M A, Fazeli P K, Freedman L M, et al. Young women with cold-activated brown adipose tissue have higher bone mineral density and lower Pref-1 than women without brown adipose tissue: a study in women with anorexia nervosa, women recovered from anorexia nervosa, and normal-weight women. J Clin Endocrinol Metab, 2012; 97(4): E584-E590. doi: 10.1210/jc.2011-2246
[63]	Du J, He Z, Cui J, et al. Osteocyte Apoptosis Contributes to Cold Exposure-induced Bone Loss. Front Bioeng Biotechnol, 2021; 9: 733582. doi: 10.3389/fbioe.2021.733582
[64]	Zhou R, Guo Q, Xiao Y, et al. Endocrine role of bone in the regulation of energy metabolism. Bone Res, 2021; 9(1): 25. doi: 10.1038/s41413-021-00142-4
[65]	Lecka-Czernik B. Diabetes, bone and glucose-lowering agents: basic biology. Diabetologia, 2017; 60(7): 1163-1169. doi: 10.1007/s00125-017-4269-4
[66]	Gupte A A, Sabek O M, Fraga D, et al. Osteocalcin protects against nonalcoholic steatohepatitis in a mouse model of metabolic syndrome. Endocrinology, 2014; 155(12): 4697-4705. doi: 10.1210/en.2014-1430
[67]	Martin S A, Philbrick K A, Wong C P, et al. Thermoneutral housing attenuates premature cancellous bone loss in male C57BL/6J mice. Endocr Connect, 2019; 8(11): 1455-1467. doi: 10.1530/EC-19-0359
[68]	Nguyen A D, Lee N J, Wee N K Y, et al. Uncoupling protein-1 is protective of bone mass under mild cold stress conditions. Bone, 2018; 106: 167-178. doi: 10.1016/j.bone.2015.05.037
[69]	Iwaniec U T, Philbrick K A, Wong C P, et al. Room temperature housing results in premature cancellous bone loss in growing female mice: implications for the mouse as a preclinical model for age-related bone loss. Osteoporos Int, 2016; 27(10): 3091-3101. doi: 10.1007/s00198-016-3634-3
[70]	Shi Y C, Lau J, Lin Z, et al. Arcuate NPY controls sympathetic output and BAT function via a relay of tyrosine hydroxylase neurons in the PVN. Cell Metab, 2013; 17(2): 236-248. doi: 10.1016/j.cmet.2013.01.006
[71]	Wee N K Y, Nguyen A D, Enriquez R F, et al. Neuropeptide Y regulation of energy partitioning and bone mass during cold exposure. Calcif Tissue Int, 2020; 107(5): 510-523. doi: 10.1007/s00223-020-00745-9