Effects of estrogen on calcium signaling in molecular pathways of pain; Importance of TRPV1 cation channels
Estrogen and TRPV1 in pain pathways
DOI:
https://doi.org/10.5281/zenodo.11652969Anahtar Kelimeler:
TRPV1 channels; Estrogen; Calcium; Pain; NociceptorsÖz
Pain is an unpleasant and uncomfortable sensation that informs us that something is wrong and overrides other neuronal signals. Nociceptive pain is an unconscious response of sensory receptors to noxious stimuli. Transient Receptor Potential (TRP) channels are a family of non-selective cation channels located at nociceptive sensory nerve endings that respond to thermal, mechanical, or chemical stimuli with threatening/irritating potential. Depending on the type and intensity of the stimulus, different TRP proteins alter calcium ion permeability and modulate cellular response patterns. TRP Vanilloid Receptor-1 (TRPV1), which has the most crucial role in the activation of pain transmission pathways in this family, is sensitive to vanilloid-like chemicals, temperature (>430C), and low pH.
Recent studies indicate that gonadal hormones are actively involved not only in reproductive behavior and sex determination but also in all physiological systems. Current literature shows that gonadal hormones play active roles not only in reproductive behavior and sex determination but also in all physiological systems. Estrogen, the most potent of these hormones, has been the subject of numerous studies due to its vital effects on the nervous system, such as neuronal viability, excitability, and perception of somatosensory stimuli. Although the literature shows that estrogen has essential roles in the modulation of pain, there is insufficient evidence regarding the molecular pathways of its effect. This review aims to investigate the importance of calcium signaling in the molecular pathways of pain and the effects of estrogen on TRPV1 cation channels that alter the calcium ion permeability of nociceptors.
İndirmeler
Referanslar
Guyton AC, Hall JE. Textbook of Medical Physiology. Elsevier Inc. 2006;11th ed.
Kim E, M. Susan, Scott B, Heddwen L. Ganong’un Review of Medical Physiology. New York McGraw-Hill. 2011;23th Ed:416-18.
Kumar RS, Goyal N. Estrogens as regulator of hematopoietic stem cell, immune cells and bone biology. Life Sci. 2021;269:119091. doi: 10.1016/j.lfs.2021.119091
Beato M, Klug J. Steroid hormone receptors: an update. Human reproduction update. 2000;6(3):225-36. doi: 10.1093/humupd/6.3.225
Vrtačnik P, Ostanek B, Mencej-Bedrač S, Marc J. The many faces of estrogen signaling. Biochem Med (Zagreb). 2014;24(3):329-42. doi: 10.11613/BM.2014.035.
Faltas CL, LeBron KA, Holz MK. Unconventional estrogen signaling in health and disease. Endocrinology. 2020;161(4):1–7. doi: 10.1210/endocr/bqaa030
Craft RM. Modulation of pain by estrogens. Pain. 2007;132 Suppl 1:S3-12. doi: 10.1016/j.pain.2007.09.028
Shaw ND, Histed SN, Srouji SS, Yang J, Lee H, JE. H. Estrogen negative feedback on gonadotropin secretion: evidence for a direct pituitary effect in women. The Journal of clinical endocrinology and metabolism. 2010;95(4):1955-61. doi: 10.1210/jc.2009-2108
Genazzani AR BF. Estrogen effects on neuroendocrine function: the new challenge of pulsed therapy. Climacteric. 2002;5(Suppl 2):50-6.
Berridge MJ BM, Roderick HL. . Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev. Mol Cell Biol. 2003;4(7):517-29. doi: 10.1038/nrm1155
Amandusson A, Blomqvist A. Estrogenic influences in pain processing. Frontiers in neuroendocrinology. 2013;34(4):329-49. doi: 10.1016/j.yfrne.2013.06.001
Chen P, Li B, Ou-Yang L. Role of estrogen receptors in health and disease. Front Endocrinol (Lausanne). 2022;13:839005. doi: 10.3389/fendo.2022.839005.
Bayer U, Hausmann M. Estrogen treatment affects brain functioning after menopause. Menopause Int. 2011;17(4):148-52. doi: 10.1258/mi.2011.011105.
Brann DW, Lu Y, Wang J, Sareddy GR, Pratap UP, Zhang Q, Tekmal RR, Vadlamudi RK. Neuron-Derived Estrogen-A Key Neuromodulator in Synaptic Function and Memory. Int J Mol Sci. 2021;22(24):13242. doi: 10.3390/ijms222413242. doi: 10.3390/ijms222413242
Guvenal T, Durna A, Erden O, Guvenal F, Cetin M, Cetin A. Effects of different postmenopausal hormone therapy regimens on cerebral blood flow and cognitive functions. Adv Ther. 2009;(8):805-11. doi: 10.1007/s12325-009-0058-x.
Wan L, Huang RJ, Luo ZH, Gong JE, Pan A, Manavis J, Yan XX, Xiao B. Reproduction-Associated Hormones and Adult Hippocampal Neurogenesis. Neural Plast. 2021;10;2021:3651735. doi: 10.1155/2021/3651735.
Yankova M, Hart SA, Woolley CS. Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electron-microscopic study. Proceedings of the National Academy of Sciences of the United States of America. 2001;98(6):3525-30. doi: 10.1073/pnas.051624598.
Wang L, Andersson S, Warner M, Gustafsson JA. Estrogen receptor (ER)beta knockout mice reveal a role for ERbeta in migration of cortical neurons in the developing brain. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(2):703-8.
McEwen BS, Akama KT, Spencer-Segal JL, Milner TA, Waters EM. Estrogen effects on the brain: actions beyond the hypothalamus via novel mechanisms. Behavioral neuroscience. 2012;126(1):4-16. doi: 10.1037/a0026708
Kow LM, Pfaff DW. Effects of estrogen treatment on the size of receptive field and response threshold of pudendal nerve in the female rat. Neuroendocrinology. 1973;13(4):299-313. doi: 10.1159/000122214
Martin VT, Behbehani M. Ovarian hormones and migraine headache: understanding mechanisms and pathogenesis--part I. Headache. 2006;46(1):3-23. doi: 10.1111/j.1526-4610.2006.00309.x.
Craft RM, Ulibarri C, Leitl MD, Sumner JE. Dose- and time-dependent estradiol modulation of morphine antinociception in adult female rats. European journal of pain. 2008;12(4):472-9. doi: 10.1016/j.ejpain.2007.07.014
Souza Monteiro de Araujo D, Nassini R, Geppetti P, De Logu F. TRPA1 as a therapeutic target for nociceptive pain. Expert Opin Ther Targets. 2020;24(10):997-1008. doi: 10.1080/14728222.2020.1815191.
Lee DT, Chai YG, Lee EB, Kim KW, Nah SY, Oh TH, et al. 17b-Estradiol inhibits high-voltage-activated calcium channel Currents in rat sensory neurons via a non-genomic mechanism. Life sciences. 2002;70:2047-59. doi: 10.1016/s0024-3205(01)01534-x
Papka RE, Storey-Workley M. Estrogen receptor-alpha and -beta coexist in a subpopulation of sensory neurons of female rat dorsal root ganglia. Neurosci Lett. 2002;319(2):71-4. doi: 10.1016/s0304-3940(01)02562-9.
Matthews J, Gustafsson JA. Estrogen signaling: a subtle balance between ER alpha and ER beta. Molecular interventions. 2003;3(5):281-92. doi: 10.1124/mi.3.5.281
Matthews J, Wihlen B, Heldring N, MacPherson L, Helguero L, Treuter E, et al. Co-planar 3,3',4,4',5-pentachlorinated biphenyl and non-co-planar 2,2',4,6,6'-pentachlorinated biphenyl differentially induce recruitment of oestrogen receptor alpha to aryl hydrocarbon receptor target genes. The Biochemical journal. 2007;406(2):343-53. doi: 10.1042/BJ20070585
Murphy AZ, Suckow SK, Johns M, Traub RJ. Sex differences in the activation of the spinoparabrachial circuit by visceral pain. Physiology & behavior. 2009;97(2):205-12. doi: 10.1016/j.physbeh.2009.02.037
Gintzler AR, Liu NJ. Importance of sex to pain and its amelioration; relevance of spinal estrogens and its membrane receptors. Frontiers in neuroendocrinology. 2012;33(4):412-24. doi: 10.1016/j.yfrne.2012.09.004
Sarlani E, Farooq N, Greenspan JD. Gender and laterality differences in thermosensation throughout the perceptible range. Pain. 2003;106(1-2):9-18. doi: 10.1016/s0304-3959(03)00211-2
Chesterton LS, Barlas P, Foster NE, Baxter GD, Wright CC. Gender differences in pressure pain threshold in healthy humans. Pain. 2003;101(3):259-66. doi: 10.1016/S0304-3959(02)00330-5
Sanoja R, Cervero F. Estrogen modulation of ovariectomy-induced hyperalgesia in adult mice. European journal of pain. 2008;12(5):573-81. doi: 10.1016/j.ejpain.2007.09.003
Sanoja R, Cervero F. Estrogen-dependent abdominal hyperalgesia induced by ovariectomy in adult mice: a model of functional abdominal pain. Pain. 2005;118(1-2):243-53. doi: 10.1016/j.pain.2005.08.021
Fischer L, Torres-Chavez KE, Clemente-Napimoga JT, Jorge D, Arsati F, de Arruda Veiga MC, et al. The influence of sex and ovarian hormones on temporomandibular joint nociception in rats. The journal of pain : official journal of the American Pain Society. 2008;9(7):630-8. doi: 10.1016/j.jpain.2008.02.006
Mannino CA, South SM, Quinones-Jenab V, Inturrisi CE. Estradiol replacement in ovariectomized rats is antihyperalgesic in the formalin test. The journal of pain : official journal of the American Pain Society. 2007;8(4):334-42. doi: 10.1016/j.jpain.2006.10.002
Forman LJ, Tingle V, Estilow S, Cater J. The response to analgesia testing is affected by gonadal steroids in the rat. Life sciences. 1989;45(5):447-54. doi: 10.1016/0024-3205(89)90631-0
Beatty WW, Fessler RG. Gonadectomy and sensitivity to electric shock in the rat. Physiology & behavior. 1977;19(1):1-6. doi: 10.1016/0031-9384(77)90149-4
Gaumond I, Arsenault P, Marchand S. The role of sex hormones on formalin-induced nociceptive responses. Brain research. 2002;958(1):139-45. doi: 10.1016/s0006-8993(02)03661-2.
Chen SC, Liu BC, Chen CW, Wu FS. Intradermal pregnenolone sulfate attenuates capsaicin-induced nociception in rats. Biochemical and biophysical research communications. 2006;349(2):626-33. doi: 10.1016/j.bbrc.2006.08.076
Lu YC, Chen CW, Wang SY, Wu FS. 17Beta-estradiol mediates the sex difference in capsaicin-induced nociception in rats. The Journal of pharmacology and experimental therapeutics. 2009;331(3):1104-10. doi: 10.1124/jpet.109.158402
Lee CW, Ho IK. Sex differences in opioid analgesia and addiction: interactions among opioid receptors and estrogen receptors. Mol Pain. 2013;9:45. doi: 10.1186/1744-8069-9-45.
Ji Y, Murphy AZ, Traub RJ. Estrogen modulation of morphine analgesia of visceral pain in female rats is supraspinally and peripherally mediated. The journal of pain : official journal of the American Pain Society. 2007;8(6):494-502. doi: 10.1016/j.jpain.2007.01.006
Loyd DR, Morgan MM, Murphy AZ. Morphine preferentially activates the periaqueductal gray-rostral ventromedial medullary pathway in the male rat: a potential mechanism for sex differences in antinociception. Neuroscience. 2007;147(2):456-68. doi: 10.1016/j.neuroscience.2007.03.053
Wang X, Traub RJ, Murphy AZ. Persistent pain model reveals sex difference in morphine potency. American journal of physiology Regulatory, integrative and comparative physiology. 2006;291(2):R300-6. doi: 10.1152/ajpregu.00022.2006
Craft RM, Kandasamy R, Davis SM. Sex differences in anti-allodynic, anti-hyperalgesic and anti-edema effects of Delta(9)-tetrahydrocannabinol in the rat. Pain. 2013;154(9):1709-17. doi: 10.1016/j.pain.2013.05.017
Toner BB, Akman D. Gender role and irritable bowel syndrome: literature review and hypothesis. The American journal of gastroenterology. 2000;95(1):11-6. doi: 10.1111/j.1572-0241.2000.01698.x
Vuong C, Van Uum SH, O'Dell LE, Lutfy K, Friedman TC. The effects of opioids and opioid analogs on animal and human endocrine systems. Endocrine reviews. 2010;31(1):98-132.
Paredes S, Cantillo S, Candido KD, Knezevic NN. An Association of Serotonin with Pain Disorders and Its Modulation by Estrogens. Int J Mol Sci. 2019;20(22):5729. doi: 10.3390/ijms20225729. doi: 10.3390/ijms20225729
Kaur S, McDonald H, Tongkhuya S, Lopez CMC, Ananth S, Hickman TM, Averitt DL. Estrogen exacerbates the nociceptive effects of peripheral serotonin on rat trigeminal sensory neurons. Neurobiol Pain. 2021;10:100073. doi: 10.1016/j.ynpai.2021.100073.
MacGregor EA. Estrogen replacement and migraine. Maturitas. 2009;63(1):51-5. doi: 10.1016/j.maturitas.2009.03.016.
Artero-Morales M, González-Rodríguez S, Ferrer-Montiel A. TRP Channels as Potential Targets for Sex-Related Differences in Migraine Pain. Front Mol Biosci. 2018;5:73. doi: 10.3389/fmolb.2018.00073.
Zhao X, Yu B, Wang L, Liu J, Xie W, Xu J. Ovariotomy and persistent pain affect long-term Fos expression in spinal cord. Neuroscience letters. 2005;375(3):165-9. doi: 10.1016/j.neulet.2004.11.006
Kou XX, Wu YW, Ding Y, Hao T, Bi RY, Gan YH, et al. 17beta-estradiol aggravates temporomandibular joint inflammation through the NF-kappaB pathway in ovariectomized rats. Arthritis and rheumatism. 2011;63(7):1888-97. doi: 10.1002/art.30334
Shen W, Shen L, Chen G, Wang F, Li C, Lin F, et al. Ovariectomy modulation of morphine analgesia of neuropathic pain is associated with the change of K-Cl cotransporter 2 protein level in spinal dorsal horn. International journal of clinical and experimental medicine. 2014;7(10):3467-72.
Tang B, Ji Y, Traub RJ. Estrogen alters spinal NMDA receptor activity via a PKA signaling pathway in a visceral pain model in the rat. Pain. 2008;137(3):540-9. doi: 10.1016/j.pain.2007.10.017
Vodo S, Arcelli D, Fiorenzani P, Meriggiola MC, Butkevich I, Di Canio C, et al. Gonadal ER alpha/beta, AR and TRPV1 gene expression: Modulation by pain and morphine. treatment in male and female rats. Physiology & behavior. 2013;110:80-6. doi: 10.1016/j.physbeh.2012.12.014
Smith YR, Stohler CS, Nichols TE, Bueller JA, Koeppe RA, Zubieta JK. Pronociceptive and antinociceptive effects of estradiol through endogenous opioid neurotransmission in women. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2006;26(21):5777-85. doi: 10.1523/JNEUROSCI.5223-05.2006
Sarajari S, Oblinger MM. Estrogen effects on pain sensitivity and neuropeptide expression in rat sensory neurons. Experimental neurology. 2010;224(1):163-9. doi: 10.1016/j.expneurol.2010.03.006
Ceccarelli I, Fiorenzani P, Massafra C, Aloisi AM. Long-term ovariectomy changes formalin-induced licking in female rats: the role of estrogens. Reproductive biology and endocrinology:RB&E. 2003;1:24. doi: 10.1186/1477-7827-1-24
Ma B, Yu LH, Fan J, Cong B, He P, Ni X, et al. Estrogen modulation of peripheral pain signal transduction: involvement of P2X(3) receptors. Purinergic signalling. 2011;7(1):73-83. doi: 10.1007/s11302-010-9212-9
Wu YW, Bi YP, Kou XX, Xu W, Ma LQ, Wang KW, et al. 17-Beta-estradiol enhanced allodynia of inflammatory temporomandibular joint through upregulation of hippocampal TRPV1 in ovariectomized rats. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2010;30(26):8710-9. doi: 10.1523/JNEUROSCI.6323-09.2010
Martin VT, Lee J, Behbehani MM. Sensitization of the trigeminal sensory system during different stages of the rat estrous cycle: implications for menstrual migraine. Headache. 2007;47(4):552-63. doi: 10.1111/j.1526-4610.2007.00714.x
Stening K, Eriksson O, Wahren L, Berg G, Hammar M, Blomqvist A. Pain sensations to the cold pressor test in normally menstruating women: comparison with men and relation to menstrual phase and serum sex steroid levels. American journal of physiology Regulatory, integrative and comparative physiology. 2007;293(4):R1711-6. doi: 10.1152/ajpregu.00127.2007
Li L, Fan X, Warner M, Xu XJ, Gustafsson JA, Wiesenfeld-Hallin Z. Ablation of estrogen receptor alpha or beta eliminates sex differences in mechanical pain threshold in normal and inflamed mice. Pain. 2009;143(1-2):37-40. doi: 10.1016/j.pain.2009.01.005
Hucho TB, Dina OA, Kuhn J, Levine JD. Estrogen controls PKCepsilon-dependent mechanical hyperalgesia through direct action on nociceptive neurons. The European journal of neuroscience. 2006;24(2):527-34. doi: 10.1111/j.1460-9568.2006.04913.x
Tong C, Conklin D, Clyne BB, Stanislaus JD, Eisenach JC. Uterine cervical afferents in thoracolumbar dorsal root ganglia express transient receptor potential vanilloid type 1 channel and calcitonin gene-related peptide, but not P2X3 receptor and somatostatin. Anesthesiology. 2006;104(4):651-7. doi: 10.1097/00000542-200604000-00007
Fillingim RB, King CD, Ribeiro-Dasilva MC, Rahim-Williams B, Riley JL, 3rd. Sex, gender, and pain: a review of recent clinical and experimental findings. The journal of pain : official journal of the American Pain Society. 2009;10(5):447-85. doi: 10.1016/j.jpain.2008.12.001
Balemans D, Boeckxstaens GE, Talavera K, Wouters MM. Transient receptor potential ion channel function in sensory transduction and cellular signaling cascades underlying visceral hypersensitivity. Am J Physiol Gastrointest Liver Physiol. 2017;312(6):G635-G648. doi: 10.1152/ajpgi.00401.2016.
Clapham DE. TRP channels as cellular sensors. Nature. 2003;426(6966):517-24. doi: 10.1038/nature02196
Minke B, Cook B. TRP channel proteins and signal transduction. Physiological reviews. 2002;82(2):429-72. doi: 10.1152/physrev.00001.2002
Montell C. The TRP superfamily of cation channels. Science's STKE : signal transduction knowledge environment. 2005;2005(272):re3. doi: 10.1126/stke.2722005re3
Naziroglu M. TRPM2 cation channels, oxidative stress and neurological diseases: where are we now? Neurochemical research. 2011;36(3):355-66. doi: 10.1007/s11064-010-0347-4
Ozgül C, Naziroglu M. Role of TRPM2 cation channels on molecular pathways in neurological cells. Journal of Experimental and Clinical Medicine. 2010;27,144-151.
Feng Z, Pearce LV, Xu X, Yang X, Yang P, Blumberg PM, et al. Structural Insight into Tetrameric hTRPV1 from Homology Modeling, Molecular Docking, Molecular Dynamics Simulation, Virtual Screening, and Bioassay Validations. Journal of chemical information and modeling. 2015;55(3):572-88. doi: 10.1021/ci5007189
Hofmann T, Schaefer M, Schultz G, Gudermann T. Subunit composition of mammalian transient receptor potential channels in living cells. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(11):7461-6. doi: 10.1073/pnas.102596199
Dietrich A, Chubanov V, Kalwa H, Rost BR, Gudermann T. Cation channels of the transient receptor potential superfamily: their role in physiological and pathophysiological processes of smooth muscle cells. Pharmacology & therapeutics. 2006;112(3):744-60. doi: 10.1016/j.pharmthera.2006.05.013
Gunthorpe MJ, Benham CD, Randall A, Davis JB. The diversity in the vanilloid (TRPV) receptor family of ion channels. Trends in pharmacological sciences. 2002;23(4):183-91. doi: 10.1016/s0165-6147(02)01999-5
Benham CD, Davis JB, Randall AD. Vanilloid and TRP channels: a family of lipid-gated cation channels. Neuropharmacology. 2002;42(7):873-88. doi: 10.1016/s0028-3908(02)00047-3
Pedersen SF, Owsianik G, Nilius B. TRP channels: an overview. Cell Calcium. 2005;38(3-4):233-52. doi: 10.1016/j.ceca.2005.06.028
Beech DJ, Muraki K, Flemming R. Non-selective cationic channels of smooth muscle and the mammalian homologues of Drosophila TRP. The Journal of physiology. 2004;559(Pt3):685-706. doi: 10.1113/jphysiol.2004.068734
Iwata Y, Katanosaka Y, Arai Y, Komamura K, Miyatake K, Shigekawa M. A novel mechanism of myocyte degeneration involving the Ca2+-permeable growth factor-regulated channel. The Journal of cell biology. 2003;161(5):957-67. doi: 10.1083/jcb.200301101
O'Neil RG, Heller S. The mechanosensitive nature of TRPV channels. Pflugers Archiv : European journal of physiology. 2005;451(1):193-203. doi: 10.1007/s00424-005-1424-4
Nilius B, Vriens J, Prenen J, Droogmans G, Voets T. TRPV4 calcium entry channel: a paradigm for gating diversity. American journal of physiology Cell physiology. 2004;286(2):C195-205. doi: 10.1152/ajpcell.00365.2003
Nilius B, Voets T. TRP channels: a TR(I)P through a world of multifunctional cation channels. Pflugers Archiv : European journal of physiology. 2005;451(1):1-10. doi: 10.1007/s00424-005-1462-y
den Dekker E, Hoenderop JG, Nilius B, Bindels RJ. The epithelial calcium channels, TRPV5 & TRPV6: from identification towards regulation. Cell Calcium. 2003;33(5-6):497-507. doi: 10.1016/s0143-4160(03)00065-4
Zhang Y, Xiang B, Li YM, Wang Y, Wang X, Wang YN, et al. Expression and characteristics of vanilloid receptor 1 in the rabbit submandibular gland. Biochemical and biophysical research communications. 2006;345(1):467-73. doi: 10.1016/j.bbrc.2006.04.106
McIntyre P, McLatchie LM, Chambers A, Phillips E, Clarke M, Savidge J, et al. Pharmacological differences between the human and rat vanilloid receptor 1 (VR1). Br J Pharmacol. 2001;132(5):1084-94. doi: 10.1038/sj.bjp.0703918
Karai LJ, Russell JT, Iadarola MJ, Olah Z. Vanilloid receptor 1 regulates multiple calcium compartments and contributes to Ca2+-induced Ca2+ release in sensory neurons. The Journal of biological chemistry. 2004;279(16):16377-87. doi: 10.1074/jbc.M310891200
Marshall IC, Owen DE, Cripps TV, Davis JB, McNulty S, Smart D. Activation of vanilloid receptor 1 by resiniferatoxin mobilizes calcium from inositol 1,4,5-trisphosphate-sensitive stores. Br J Pharmacol. 2003;138(1):172-6. doi: 10.1038/sj.bjp.0705003
Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science. 2000;288(5464):306-13. doi: 10.1126/science.288.5464.306
Szallasi A. Vanilloid receptor ligands: hopes and realities for the future. Drugs & aging. 2001;18(8):561-73. doi: 10.2165/00002512-200118080-00001
Szallasi A, Blumberg PM. Resiniferatoxin and its analogs provide novel insights into the pharmacology of the vanilloid (capsaicin) receptor. Life sciences. 1990;47(16):1399-408. doi: 10.1016/0024-3205(90)90518-v
Adcock JJ. TRPV1 receptors in sensitisation of cough and pain reflexes. Pulmonary pharmacology & therapeutics. 2009;22(2):65-70. doi: 10.1016/j.pupt.2008.12.014
Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 1998;21(3):531-43. doi: 10.1016/s0896-6273(00)80564-4
Caterina MJ, Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annual review of neuroscience. 2001;24:487-517. doi: 10.1146/annurev.neuro.24.1.487
Cui M, Honore P, Zhong C, Gauvin D, Mikusa J, Hernandez G, et al. TRPV1 receptors in the CNS play a key role in broad-spectrum analgesia of TRPV1 antagonists. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2006;26(37):9385-93. doi: 10.1523/JNEUROSCI.1246-06.2006
Szallasi A, Szabo T, Biro T, Modarres S, Blumberg PM, Krause JE, et al. Resiniferatoxin-type phorboid vanilloids display capsaicin-like selectivity at native vanilloid receptors on rat DRG neurons and at the cloned vanilloid receptor VR1. Br J Pharmacol. 1999;128(2):428-34. doi: 10.1038/sj.bjp.0702810
Ferreira J, da Silva GL, Calixto JB. Contribution of vanilloid receptors to the overt nociception induced by B2 kinin receptor activation in mice. Br J Pharmacol. 2004;141(5):787-94. doi: 10.1038/sj.bjp.0705546
Honore P, Wismer CT, Mikusa J, Zhu CZ, Zhong C, Gauvin DM, et al. A-425619 [1-isoquinolin-5-yl-3-(4-trifluoromethyl-benzyl)-urea], a novel transient receptor potential type V1 receptor antagonist, relieves pathophysiological pain associated with inflammation and tissue injury in rats. The Journal of pharmacology and experimental therapeutics. 2005;314(1):410-21. doi: 10.1124/jpet.105.083915
Gavva NR. Body-temperature maintenance as the predominant function of the vanilloid receptor TRPV1. Trends in pharmacological sciences. 2008;29(11):550-7. doi: 10.1016/j.tips.2008.08.003
Xu S, Cheng Y, Keast JR, Osborne PB. 17beta-estradiol activates estrogen receptor beta-signalling and inhibits transient receptor potential vanilloid receptor 1 activation by capsaicin in adult rat nociceptor neurons. Endocrinology. 2008;149(11):5540-8. doi: 10.1210/en.2008-0278.
Martonosi AN, Pikula S. The network of calcium regulation in muscle. Acta biochimica Polonica. 2003;50(1):1-30.
Berridge MJ. The versatility and complexity of calcium signalling. Novartis Foundation symposium. 2001;239:52-64; discussion -7, 150-9.
Saygin M, Naziroğlu M. Role of TRPM cation channels on molecular Ca2+ signaling pathways in heart. Journal of Experimental and Clinical Medicine. 2011;29:83-90.
Targos B, Baranska J, Pomorski P. Store-operated calcium entry in physiology and pathology of mammalian cells. Acta biochimica Polonica. 2005;52(2):397-409. doi: 10.18388/abp.2005_3452
Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling. Nature reviews Molecular cell biology. 2000;1(1):11-21. doi: 10.1038/35036035
Rossier MF. T channels and steroid biosynthesis: in search of a link with mitochondria. Cell calcium. 2006;40(2):155-64. doi: 10.1016/j.ceca.2006.04.020
Kumar A, Kumari S, Majhi RK, Swain N, Yadav M, Goswami C. Regulation of TRP channels by steroids: Implications in physiology and diseases. General and comparative endocrinology. 2014. doi: 10.1016/j.ygcen.2014.10.004
Méndez-Reséndiz KA, Enciso-Pablo Ó, González-Ramírez R, Juárez-Contreras R, Rosenbaum T, Morales-Lázaro SL. Steroids and TRP Channels: A Close Relationship. Int J Mol Sci. 2020;21(11):3819. doi: 10.3390/ijms21113819.