Advertisement

Molecular Biology Reports

, Volume 46, Issue 1, pp 1499–1510 | Cite as

Immune aspects of the bi-directional neuroimmune facilitator TRPV1

  • Yan-Ruide LiEmail author
  • Puneet GuptaEmail author
Review

Abstract

A rapidly growing area of interest in biomedical science involves the reciprocal crosstalk between the sensory nervous and immune systems. Both of these systems are highly integrated, detecting potential environmental harms and restoring homeostasis. Many different cytokines, receptors, neuropeptides, and other proteins are involved in this bidirectional communication that are common to both systems. One such family of proteins includes the transient receptor potential vanilloid (TRPV) proteins. Though much progress has been made in understanding TRPV proteins in the nervous system, their functions in the immune system are not well elucidated. Hence, further understanding their role in the peripheral immune system and as regulators of neuroimmunity is critical for evaluating their potential as therapeutic targets for numerous inflammatory disorders, cancers, and other disease states. Here, we focus on the latest advancements in understanding TRPV1 and TRPV2’s roles in the immune system, TRPV1 in neuroimmunity, and TRPV1’s potential involvement in anti-tumor therapy.

Keywords

TRPV1 TRPV2 Neuroimmunity Anti-tumor therapy Capsaicin 

Notes

Acknowledgements

The authors express gratitude to Zhihua Li and Mingye Yan in their support of this project.

Author contributions

Y-RL and PG conceived and authored the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the review.

References

  1. 1.
    Amachi R, Hiasa M, Teramachi J, Harada T, Oda A, Nakamura S, Abe M et al (2016) A vicious cycle between acid sensing and survival signaling in myeloma cells: acid-induced epigenetic alteration. Oncotarget.  https://doi.org/10.18632/oncotarget.11927 Google Scholar
  2. 2.
    Amantini C, Mosca M, Nabissi M, Lucciarini R, Caprodossi S, Arcella A, Santoni G et al (2007) Capsaicin-induced apoptosis of glioma cells is mediated by TRPV1 vanilloid receptor and requires p38 MAPK activation. J Neurochem 102(3):977–990.  https://doi.org/10.1111/j.1471-4159.2007.04582.x Google Scholar
  3. 3.
    Assas BM, Wakid MH, Zakai HA, Miyan JA, Pennock JL (2016) Transient receptor potential vanilloid 1 expression and function in splenic dendritic cells: a potential role in immune homeostasis. Immunology 147(3):292–304.  https://doi.org/10.1111/imm.12562 Google Scholar
  4. 4.
    Bailey TW, Jin Y-HH, Doyle MW, Andresen MC (2002) Vanilloid-sensitive afferents activate neurons with prominent A-type potassium currents in nucleus tractus solitarius. The Journal of Neuroscience 22(18):8230–8237.  https://doi.org/10.1523/JNEUROSCI.22-18-08230.2002 Google Scholar
  5. 5.
    Basu S, Srivastava P (2005) Immunological role of neuronal receptor vanilloid receptor 1 expressed on dendritic cells. Proc Natl Acad Sci USA 102(14):5120–5125.  https://doi.org/10.1073/pnas.0407780102 Google Scholar
  6. 6.
    Bertin S, Aoki-Nonaka Y, De Jong PR, Nohara LL, Xu H, Stanwood SR, Raz E et al (2014) The ion channel TRPV1 regulates the activation and proinflammatory properties of CD4+ T cells. Nat Immunol 15(11):1055–1063.  https://doi.org/10.1038/ni.3009 Google Scholar
  7. 7.
    Bertin S, Aoki-Nonaka Y, Lee J, De Jong PR, Kim P, Han T, Raz E et al (2017) The TRPA1 ion channel is expressed in CD4+ t cells and restrains T-cell-mediated colitis through inhibition of TRPV1. Gut 66(9):1584–1596.  https://doi.org/10.1136/gutjnl-2015-310710 Google Scholar
  8. 8.
    Bertin S, De Jong PR, Jefferies WA, Raz E (2014) Novel immune function for the TRPV1 channel in T lymphocytes. Channels.  https://doi.org/10.4161/19336950.2014.991640 Google Scholar
  9. 9.
    Bode AM, Dong Z (2011) The two faces of capsaicin. Can Res.  https://doi.org/10.1158/0008-5472.CAN-10-3756 Google Scholar
  10. 10.
    Borbély É, Botz B, Bölcskei K, Kenyér T, Kereskai L, Kiss T, Szolcsányi J, Pintér E, Csepregi JZ, Mócsai A, Helyes Z (2015) Capsaicin-sensitive sensory nerves exert complex regulatory functions in the serum-transfer mouse model of autoimmune arthritis. Brain Behav Immun 45:50–59Google Scholar
  11. 11.
    Boyd RS, Jukes-Jones R, Walewska R, Brown D, Dyer MJS, Cain K (2009) Protein profiling of plasma membranes defines aberrant signaling pathways in mantle cell lymphoma. Mol Cell Proteom 8(7):1501–1515.  https://doi.org/10.1074/mcp.M800515-MCP200 Google Scholar
  12. 12.
    Caprodossi S, Amantini C, Nabissi M, Morelli MB, Farfariello V, Santoni M, Santoni G et al (2011) Capsaicin promotes a more aggressive gene expression phenotype and invasiveness in null-TRPV1 urothelial cancer cells. Carcinogenesis 32(5):686–694.  https://doi.org/10.1093/carcin/bgr025 Google Scholar
  13. 13.
    Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398(6726):436–441.  https://doi.org/10.1038/18906 Google Scholar
  14. 14.
    Cavanaugh DJ, Chesler AT, Jackson AC, Sigal YM, Yamanaka H, Grant R, Basbaum AI et al (2011) Trpv1 reporter mice reveal highly restricted brain distribution and functional expression in arteriolar smooth muscle cells. J Neurosci 31(13):5067–5077Google Scholar
  15. 15.
    Cevikbas F, Wang X, Akiyama T, Kempkes C, Savinko T, Antal A, Steinhoff M et al (2014) A sensory neuron-expressed IL-31 receptor mediates T helper cell-dependent itch: involvement of TRPV1 and TRPA1. J Allergy Clin Immunol.  https://doi.org/10.1016/j.jaci.2013.10.048 Google Scholar
  16. 16.
    Cheung CKY, Lan LL, Kyaw M, Mak ADP, Chan A, Chan Y, Wu JCY (2018) Up-regulation of transient receptor potential vanilloid (TRPV) and down-regulation of brain-derived neurotrophic factor (BDNF) expression in patients with functional dyspepsia (FD). Neurogastroenterol Motil 30(2):e13176.  https://doi.org/10.1111/nmo.13176 Google Scholar
  17. 17.
    Chora AA, Fontoura P, Cunha A, Pais TF, Cardoso S, Ho PP, Lee LY, Sobel RA, Steinman L, Soares MP et al (2007) Heme oxygenase-1 and carbon monoxide suppress autoimmune neuroinflammation. J Clin Investig 117(2):438–447Google Scholar
  18. 18.
    Dai Y (2004) Proteinase-activated receptor 2-mediated potentiation of transient receptor potential vanilloid subfamily 1 activity reveals a mechanism for proteinase-induced inflammatory pain. J Neurosci 24(18):4293–4299.  https://doi.org/10.1523/JNEUROSCI.0454-04.2004 Google Scholar
  19. 19.
    Devesa I, Planells-Cases R, Fernandez-Ballester G, Gonzalez-Ros JM, Ferrer-Montiel A, Fernandez-Carvajal A (2011) Role of the transient receptor potential vanilloid 1 in inflammation and sepsis. J Inflamm Res 4:67–81.  https://doi.org/10.2147/JIR.S12978 Google Scholar
  20. 20.
    Doyle MW, Bailey TW, Jin Y-H, Andresen MC (2002) Vanilloid receptors presynaptically modulate cranial visceral afferent synaptic transmission in nucleus tractus solitarius. J Neurosci 22(18):8222–8229.  https://doi.org/10.1523/JNEUROSCI.22-18-08222.2002 Google Scholar
  21. 21.
    Duzen IV, Yavuz F, Vuruskan E, Saracoglu E, Poyraz F, Goksuluk H, Demiryurek S et al (2017) Leukocyte TRP channel gene expressions in patients with non-valvular atrial fibrillation. Sci Rep 7(1):9272.  https://doi.org/10.1038/s41598-017-10039-0 Google Scholar
  22. 22.
    Earley S (2010) Vanilloid and melastatin transient receptor potential channels in vascular smooth muscle. Microcirculation.  https://doi.org/10.1111/j.1549-8719.2010.00026.x Google Scholar
  23. 23.
    Entin-Meer M, Cohen L, Hertzberg-Bigelman E, Levy R, Ben-Shoshan J, Keren G (2017) TRPV2 knockout mice demonstrate an improved cardiac performance following myocardial infarction due to attenuated activity of peri-infarct macrophages. PLoS ONE.  https://doi.org/10.1371/journal.pone.0177132 Google Scholar
  24. 24.
    Entin-Meer M, Levy R, Goryainov P, Landa N, Barshack I, Avivi C, Keren G et al (2014) The transient receptor potential vanilloid 2 cation channel is abundant in macrophages accumulating at the peri-infarct zone and may enhance their migration capacity towards injured cardiomyocytes following myocardial infarction. PLoS ONE.  https://doi.org/10.1371/journal.pone.0105055 Google Scholar
  25. 25.
    Fagone P, Mangano K, Coco M, Perciavalle V, Garotta G, Romao CC, Nicoletti F (2012) Therapeutic potential of carbon monoxide in multiple sclerosis. Clin Exp Immunol 167(2):179–187Google Scholar
  26. 26.
    Fagone P, Mangano K, Quattrocchi C, Motterlini R, Di Marco R, Magro G, Penacho N, Romao CC, Nicoletti F (2011) Prevention of clinical and histological signs of proteolipid protein (PLP)-induced experimental allergic encephalomyelitis (EAE) in mice by the water-soluble carbon monoxide-releasing molecule (CORM)-A1. Clin Exp Immunol 163(3):368–374Google Scholar
  27. 27.
    Fagone P, Mazzon E, Bramanti P, Bendtzen K, Nicoletti F (2018) Gasotransmitters and the immune system: mode of action and novel therapeutic targets. Eur J Pharmacol 834:92–102Google Scholar
  28. 28.
    Fernandes ES, Liang L, Smillie S-J, Kaiser F, Purcell R, Rivett DW, Brain SD et al (2012) TRPV1 deletion enhances local inflammation and accelerates the onset of systemic inflammatory response syndrome. J Immunol 188(11):5741–5751.  https://doi.org/10.4049/jimmunol.1102147 Google Scholar
  29. 29.
    Gibson HE, Edwards JG, Page RS, Van Hook MJ, Kauer JA (2008) TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Neuron 57(5):746–759.  https://doi.org/10.1016/j.neuron.2007.12.027 Google Scholar
  30. 30.
    Goswami C, Schmidt H, Hucho F (2007) TRPV1 at nerve endings regulates growth cone morphology and movement through cytoskeleton reorganization. FEBS J 274(3):760–772.  https://doi.org/10.1111/j.1742-4658.2006.05621.x Google Scholar
  31. 31.
    Hassan S, Eldeeb K, Millns PJ, Bennett AJ, Alexander SPH, Kendall DA (2014) Cannabidiol enhances microglial phagocytosis via transient receptor potential (TRP) channel activation. Br J Pharmacol 171(9):2426–2439.  https://doi.org/10.1111/bph.12615 Google Scholar
  32. 32.
    Hdud IM, El-Shafei AA, Loughna P, Barrett-Jolley R, Mobasheri A (2012) Expression of transient receptor potential vanilloid (TRPV) channels in different passages of articular chondrocytes. Int J Mol Sci 13(4):4433–4445.  https://doi.org/10.3390/ijms13044433 Google Scholar
  33. 33.
    Heiner I, Eisfeld J, Halaszovich CR, Wehage E, Jüngling E, Zitt C, Lückhoff A (2003) Expression profile of the transient receptor potential (TRP) family in neutrophil granulocytes: evidence for currents through long TRP channel 2 induced by ADP-ribose and NAD. Biochem J 371(Pt 3):1045–1053.  https://doi.org/10.1042/BJ20021975 Google Scholar
  34. 34.
    Heiner I, Eisfeld J, Lückhoff A (2003) Role and regulation of TRP channels in neutrophil granulocytes. Cell Calcium 33(5–6):533–540.  https://doi.org/10.1016/S0143-4160(03)00058-7 Google Scholar
  35. 35.
    Helyes Z, Szabó A, Németh J, Jakab B, Pintér E, Bánvölgyi A, Kereskai L, Kéri G, Szolcsányi J (2004) Antiinflammatory and analgesic effects of somatostatin released from capsaicin-sensitive sensory nerve terminals in a Freund’s adjuvant-induced chronic arthritis model in the rat. Arthritis Rheum 50(5):1677–1685Google Scholar
  36. 36.
    Ho KW, Lambert WS, Calkins DJ (2014) Activation of the TRPV1 cation channel contributes to stress-induced astrocyte migration. GLIA 62(9):1435–1451.  https://doi.org/10.1002/glia.22691 Google Scholar
  37. 37.
    Jara-Oseguera A, Simon SA, Rosenbaum T (2008) TRPV1: on the road to pain relief. Curr Mol Pharmacol 1(3):255–269.  https://doi.org/10.2174/1874467210801030255 Google Scholar
  38. 38.
    Járomi P, Garab D, Hartmann P, Bodnár D, Nyíri S, Sántha P, Szabó A et al (2018) Capsaicin-induced rapid neutrophil leukocyte activation in the rat urinary bladder microcirculatory bed. Neurourol Urodyn 37(2):690–698.  https://doi.org/10.1002/nau.23376 Google Scholar
  39. 39.
    Kim HS, Kwon HJ, Kim GE, Cho MH, Yoon SY, Davies AJ, Kim YK et al (2014) Attenuation of natural killer cell functions by capsaicin through a direct and TRPV1-independent mechanism: capsaicin-induced NK cell dysfunction. Carcinogenesis.  https://doi.org/10.1093/carcin/bgu091 Google Scholar
  40. 40.
    Lai JP, Douglas SD, Ho WZ (1998) Human lymphocytes express substance P and its receptor. J Neuroimmunol 86(1):80–86.  https://doi.org/10.1016/S0165-5728(98)00025-3 Google Scholar
  41. 41.
    Lévêque M, Penna A, Le Trionnaire S, Belleguic C, Desrues B, Brinchault G, Martin-Chouly C et al (2018) Phagocytosis depends on TRPV2-mediated calcium influx and requires TRPV2 in lipids rafts: alteration in macrophages from patients with cystic fibrosis. Sci Rep 8:4310.  https://doi.org/10.1038/s41598-018-22558-5 Google Scholar
  42. 42.
    Liapi A, Wood JN (2005) Extensive co-localization and heteromultimer formation of the vanilloid receptor-like protein TRPV2 and the capsaicin receptor TRPV1 in the adult rat cerebral cortex. Eur J Neurosci 22(4):825–834.  https://doi.org/10.1111/j.1460-9568.2005.04270.x Google Scholar
  43. 43.
    Link TM, Park U, Vonakis BM, Raben DM, Soloski MJ, Caterina MJ (2010) TRPV2 has a pivotal role in macrophage particle binding and phagocytosis. Nat Immunol 11(3):232–239.  https://doi.org/10.1038/ni.1842 Google Scholar
  44. 44.
    Liu B, Qin F (2016) Use dependence of heat sensitivity of vanilloid receptor TRPV2. Biophys J 110(7):1523–1537.  https://doi.org/10.1016/j.bpj.2016.03.005 Google Scholar
  45. 45.
    Magierowska K, Wojcik D, Chmura A, Bakalarz D, Wierdak M, Kwiecien S, Sliwowski Z, Brzozowski T, Magierowski M et al (2018) Alterations in gastric mucosal expression of calcitonin gene-related peptides, vanilloid receptors, and heme oxygenase-1 mediate gastroprotective action of carbon monoxide against ethanol-induced gastric mucosal lesions. Int J Mol Sci 19(10):2960.  https://doi.org/10.3390/ijms19102960 Google Scholar
  46. 46.
    Majhi RK, Sahoo SS, Yadav M, Pratheek BM, Chattopadhyay S, Goswami C (2015) Functional expression of TRPV channels in T cells and their implications in immune regulation. FEBS J 282(14):2661–2681.  https://doi.org/10.1111/febs.13306 Google Scholar
  47. 47.
    Marinelli S, Pascucci T, Bernardi G, Puglisi-Allegra S, Mercuri NB (2005) Activation of TRPVI in the VTA excites dopaminergic neurons and increases chemical- and noxious-induced dopamine release in the nucleus accumbens. Neuropsychopharmacology 30(5):864–870.  https://doi.org/10.1038/sj.npp.1300615 Google Scholar
  48. 48.
    Marsch R, Foeller E, Rammes G, Bunck M, Kossl M, Holsboer F, Wotjak CT et al (2007) Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice. J Neurosci 27(4):832–839.  https://doi.org/10.1523/JNEUROSCI.3303-06.2007 Google Scholar
  49. 49.
    Mazzone SB, Geraghty DP (2000) Respiratory actions of tachykinins in the nucleus of the solitary tract: effect of neonatal capsaicin pretreatment. Br J Pharmacol 129(6):1132–1139Google Scholar
  50. 50.
    McNamara FN, Randall A, Gunthorpe MJ (2005) Effects of piperine, the pungent component of black pepper, at the human vanilloid receptor (TRPV1). Br J Pharmacol 144(6):781–790.  https://doi.org/10.1038/sj.bjp.0706040 Google Scholar
  51. 51.
    Medvedeva YV, Kim M-S, Usachev YM (2008) Mechanisms of prolonged presynaptic Ca2+ signaling and glutamate release induced by TRPV1 activation in rat sensory neurons. J Neurosci 28(20):5295–5311.  https://doi.org/10.1523/JNEUROSCI.4810-07.2008 Google Scholar
  52. 52.
    Mikami N, Matsushita H, Kato T, Kawasaki R, Sawazaki T, Kishimoto T, Tsujikawa K et al (2011) Calcitonin gene-related peptide is an important regulator of cutaneous immunity: effect on dendritic cell and T cell functions. J Immunol 186(12):6886–6893.  https://doi.org/10.4049/jimmunol.1100028 Google Scholar
  53. 53.
    Miyake T, Shirakawa H, Nakagawa T, Kaneko S (2015) Activation of mitochondrial transient receptor potential vanilloid 1 channel contributes to microglial migration. GLIA 63(10):1870–1882.  https://doi.org/10.1002/glia.22854 Google Scholar
  54. 54.
    Mohammed M, Madden CJ, Andresen MC, Morrison SF (2018) Activation of TRPV1 in nucleus tractus solitarius reduces brown adipose tissue thermogenesis, arterial pressure and heart rate. Am J Physiol-Regul Integr Comp Physiol.  https://doi.org/10.1152/ajpregu.00049.2018 Google Scholar
  55. 55.
    Murai M, Tsuji F, Nose M, Seki I, Oki K, Setoguchi C, Aono H et al (2008) SA13353 (1-[2-(1-Adamantyl)ethyl]-1-pentyl-3-[3-(4-pyridyl)propyl]urea) inhibits TNF-α production through the activation of capsaicin-sensitive afferent neurons mediated via transient receptor potential vanilloid 1 in vivo. Eur J Pharmacol 588(2–3):309–315.  https://doi.org/10.1016/j.ejphar.2008.04.037 Google Scholar
  56. 56.
    Nagasawa M, Nakagawa Y, Tanaka S, Kojima I (2007) Chemotactic peptide fMetLeuPhe induces translocation of the TRPV2 channel in macrophages. J Cell Physiol 210(3):692–702.  https://doi.org/10.1002/jcp.20883 Google Scholar
  57. 57.
    Nam JH, Park ES, Won SY, Lee YA, Kim KI, Jeong JY, Jin BK et al (2015) TRPV1 on astrocytes rescues nigral dopamine neurons in Parkinson’s disease via CNTF. Brain 138(12):3610–3622.  https://doi.org/10.1093/brain/awv297 Google Scholar
  58. 58.
    Nathan C (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol.  https://doi.org/10.1038/nri1785 Google Scholar
  59. 59.
    Nevius E, Srivastava PK, Basu S (2011) Oral ingestion of capsaicin, the pungent component of chili pepper, enhances a discreet population of macrophages and confers protection from autoimmune diabetes. Mucosal Immunol 5(1):76–86.  https://doi.org/10.1038/mi.2011.50 Google Scholar
  60. 60.
    Nicoletti F, Mancuso G, Cusumano V, Marco RD, Zaccone P, Bendtzen K, Teti G (1997) Prevention of endotoxin-induced lethality in neonatal mice by interleukin-13. Eur J Immunol 27(6):1580–1583.  https://doi.org/10.1002/eji.1830270639 Google Scholar
  61. 61.
    Nikolic I, Saksida T, Mangano K, Vujicic M, Stojanovic I, Nicoletti F, Stosic-Grujicic S (2014) Pharmacological application of carbon monoxide ameliorates islet-directed autoimmunity in mice via anti-inflammatory and anti-apoptotic effects. Diabetologia 57(5):980–990.  https://doi.org/10.1007/s00125-014-3170-7 Google Scholar
  62. 62.
    Ninomiya Y, Tanuma SI, Tsukimoto M (2017) Differences in the effects of four TRPV1 channel antagonists on lipopolysaccharide-induced cytokine production and COX-2 expression in murine macrophages. Biochem Biophys Res Commun 484(3):668–674.  https://doi.org/10.1016/j.bbrc.2017.01.173 Google Scholar
  63. 63.
    Omari SA, Adams MJ, Geraghty DP (2017) TRPV1 channels in immune cells and hematological malignancies. Adv Pharmacol 79:173–198.  https://doi.org/10.1016/bs.apha.2017.01.002 Google Scholar
  64. 64.
    Parenti A, De Logu F, Geppetti P, Benemei S (2016) What is the evidence for the role of TRP channels in inflammatory and immune cells? Br J Pharmacol 173(6):953–969.  https://doi.org/10.1111/bph.13392 Google Scholar
  65. 65.
    Park KS, Pang B, Park SJ, Lee Y-G, Bae J-Y, Park S, Kim SJ et al (2011) Identification and functional characterization of ion channels in CD34+ hematopoietic stem cells from human peripheral blood. Mol Cells 32(2):181–188.  https://doi.org/10.1007/s10059-011-0068-9 Google Scholar
  66. 66.
    Perálvarez-Marín A, Doñate-Macian P, Gaudet R (2013) What do we know about the transient receptor potential vanilloid 2 (TRPV2) ion channel? FEBS J 280:5471–5487.  https://doi.org/10.1111/febs.12302 Google Scholar
  67. 67.
    Ray A, Vasudevan S, Sengupta S (2015) 6-Shogaol inhibits breast cancer cells and stem cell-like spheroids by modulation of notch signaling pathway and induction of autophagic cell death. PLoS ONE 10(9):e0137614.  https://doi.org/10.1371/journal.pone.0137614 Google Scholar
  68. 68.
    Rehman R, Bhat YA, Panda L, Mabalirajan U (2013) TRPV1 inhibition attenuates IL-13 mediated asthma features in mice by reducing airway epithelial injury. Int Immunopharmacol 15(3):597–605.  https://doi.org/10.1016/j.intimp.2013.02.010 Google Scholar
  69. 69.
    Roberts JC, Davis JB, Benham CD (2004) [3H]Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Brain Res 995(2):176–183.  https://doi.org/10.1016/j.brainres.2003.10.001 Google Scholar
  70. 70.
    Rochlitzer S, Veres TZ, Kühne K, Prenzler F, Pilzner C, Knothe S, Braun A et al (2011) The neuropeptide calcitonin gene-related peptide affects allergic airway inflammation by modulating dendritic cell function. Clin Exp Allergy 41(11):1609–1621.  https://doi.org/10.1111/j.1365-2222.2011.03822.x Google Scholar
  71. 71.
    Rodrigues T, Sieglitz F, Bernardes GJL (2016) Natural product modulators of transient receptor potential (TRP) channels as potential anti-cancer agents. Chem Soc Rev 45(22):6130–6137.  https://doi.org/10.1039/C5CS00916B Google Scholar
  72. 72.
    Samivel R, Kim DW, Son HR, Rhee YH, Kim EH, Kim JH, Mo JH et al (2016) The role of TRPV1 in the CD4+ T cell-mediated inflammatory response of allergic rhinitis. Oncotarget 7(1):148–160.  https://doi.org/10.18632/oncotarget.6653 Google Scholar
  73. 73.
    Santoni G, Farfariello V, Liberati S, Morelli MB, Nabissi M, Santoni M, Amantini C (2013) The role of transient receptor potential vanilloid type-2 ion channels in innate and adaptive immune responses. Front Immunol 4:34.  https://doi.org/10.3389/fimmu.2013.00034 Google Scholar
  74. 74.
    Sauer K, Jegla TJ (2006) Methods for identifying T cell activation modulating compoundsGoogle Scholar
  75. 75.
    Saunders CI, Kunde DA, Crawford A, Geraghty DP (2007) Expression of transient receptor potential vanilloid 1 (TRPV1) and 2 (TRPV2) in human peripheral blood. Mol Immunol 44(6):1429–1435.  https://doi.org/10.1016/j.molimm.2006.04.027 Google Scholar
  76. 76.
    Schain AJ, Melo-Carrillo A, Borsook D, Grutzendler J, Strassman AM, Burstein R (2018) Activation of pial and dural macrophages and dendritic cells by cortical spreading depression. Ann Neurol 83(3):508–521.  https://doi.org/10.1002/ana.25169 Google Scholar
  77. 77.
    Schraml BU, Reis e Sousa C (2015) Defining dendritic cells. Curr Opin Immunol 32:13–20.  https://doi.org/10.1016/j.coi.2014.11.001 Google Scholar
  78. 78.
    Shibasaki K, Ishizaki Y, Mandadi S (2013) Astrocytes express functional TRPV2 ion channels. Biochem Biophys Res Commun 441(2):327–332.  https://doi.org/10.1016/j.bbrc.2013.10.046 Google Scholar
  79. 79.
    Shibasaki K, Murayama N, Ono K, Ishizaki Y, Tominaga M (2010) TRPV2 enhances axon outgrowth through its activation by membrane stretch in developing sensory and motor neurons. J Neurosci 30(13):4601–4612.  https://doi.org/10.1523/JNEUROSCI.5830-09.2010 Google Scholar
  80. 80.
    Shimosato G, Amaya F, Ueda M, Tanaka Y, Decosterd I, Tanaka M (2005) Peripheral inflammation induces up-regulation of TRPV2 expression in rat DRG. Pain 119(1–3):225–232.  https://doi.org/10.1016/j.pain.2005.10.002 Google Scholar
  81. 81.
    Simeoli R, Montague K, Jones HR, Castaldi L, Chambers D, Kelleher JH, Malcangio M et al (2017) Exosomal cargo including microRNA regulates sensory neuron to macrophage communication after nerve trauma. Nat Commun.  https://doi.org/10.1038/s41467-017-01841-5 Google Scholar
  82. 82.
    Singer EM, Shin DB, Nattkemper LA, Benoit BM, Klein RS, Didigu CA, Rook AH et al (2013) IL-31 is produced by the malignant T-Cell population in cutaneous T-Cell lymphoma and correlates with CTCL Pruritus. J Investig Dermatol 133(12):2783–2785.  https://doi.org/10.1038/jid.2013.227 Google Scholar
  83. 83.
    Solís-López A, Kriebs U, Marx A, Mannebach S, Liedtke WB, Caterina MJ, Tsvilovskyy VV et al (2017) Analysis of TRPV channel activation by stimulation of FCεRI and MRGPR receptors in mouse peritoneal mast cells. PLoS ONE.  https://doi.org/10.1371/journal.pone.0171366 Google Scholar
  84. 84.
    Stock K, Garthe A, De Almeida Sassi F, Glass R, Wolf SA, Kettenmann H (2014) The capsaicin receptor TRPV1 as a novel modulator of neural precursor cell proliferation. Stem Cells 32(12):3183–3195.  https://doi.org/10.1002/stem.1805 Google Scholar
  85. 85.
    Szöllősi AG, Oláh A, Tóth IB, Papp F, Czifra G, Panyi G, Bíró T (2013) Transient receptor potential vanilloid-2 mediates the effects of transient heat shock on endocytosis of human monocyte-derived dendritic cells. FEBS Lett 587(9):1440–1445.  https://doi.org/10.1016/j.febslet.2013.03.027 Google Scholar
  86. 86.
    Takayama Y, Uta D, Furue H, Tominaga M (2015) Pain-enhancing mechanism through interaction between TRPV1 and anoctamin 1 in sensory neurons. Proc Natl Acad Sci 112(16):5213–5218.  https://doi.org/10.1073/pnas.1421507112 Google Scholar
  87. 87.
    Talbot S, Foster SL, Woolf CJ (2016) Neuroimmunity: physiology and pathology. Annu Rev Immunol 34(1):421–447.  https://doi.org/10.1146/annurev-immunol-041015-055340 Google Scholar
  88. 88.
    Tóth BI, Benkő S, Szöllősi AG, Kovács L, Rajnavölgyi É, Bíró T (2009) Transient receptor potential vanilloid-1 signaling inhibits differentiation and activation of human dendritic cells. FEBS Lett 583(10):1619–1624.  https://doi.org/10.1016/j.febslet.2009.04.031 Google Scholar
  89. 89.
    Tsou M-F, Lu H-F, Chen S-C, Wu L-T, Chen Y-S, Kuo H-M, Chung J-G et al (2006) Involvement of Bax, Bcl-2, Ca2+ and caspase-3 in capsaicin-induced apoptosis of human leukemia HL-60 cells. Anticancer Res 26(3A):1965–1971Google Scholar
  90. 90.
    Tsuji F, Murai M, Oki K, Seki I, Ueda K, Inoue H, Aono H et al (2010) Transient receptor potential vanilloid 1 agonists as candidates for anti-inflammatory and immunomodulatory agents. Eur J Pharmacol 627(1–3):332–339.  https://doi.org/10.1016/j.ejphar.2009.10.044 Google Scholar
  91. 91.
    Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76(1):387–417.  https://doi.org/10.1146/annurev.biochem.75.103004.142819 Google Scholar
  92. 92.
    Voedisch S, Rochlitzer S, Veres TZ, Spies E, Braun A (2012) Neuropeptides control the dynamic behavior of airway mucosal dendritic cells. PLoS ONE 7(9):e45951.  https://doi.org/10.1371/journal.pone.0045951 Google Scholar
  93. 93.
    Wainger BJ, Buttermore ED, Oliveira JT, Mellin C, Lee S, Saber WA, Woolf CJ et al (2015) Modeling pain in vitro using nociceptor neurons reprogrammed from fibroblasts. Nat Neurosci 18(1):17–24.  https://doi.org/10.1038/nn.3886 Google Scholar
  94. 94.
    Walpole CSJ, Wrigglesworth R (1993) Structural requirements for capsaicin agonists and antagonists. In: Wood JN (ed) Capsaicin in the study of pain. Academic Press, London, pp 63–81Google Scholar
  95. 95.
    Wang SE, Ko SY, Kim Y-S, Jo S, Lee SH, Jung SJ, Son H (2018) Capsaicin upregulates HDAC2 via TRPV1 and impairs neuronal maturation in mice. Exp Mol Med 50(3):e455.  https://doi.org/10.1038/emm.2017.289 Google Scholar
  96. 96.
    Wu TTL, Peters AA, Tan PT, Roberts-Thomson SJ, Monteith GR (2014) Consequences of activating the calcium-permeable ion channel TRPV1 in breast cancer cells with regulated TRPV1 expression. Cell Calcium 56(2):59–67.  https://doi.org/10.1016/j.ceca.2014.04.006 Google Scholar
  97. 97.
    Yaffe PB, Coombs PMR, Doucette CD, Walsh M, Hoskin DW (2015) Piperine, an alkaloid from black pepper, inhibits growth of human colon cancer cells via G1 arrest and apoptosis triggered by endoplasmic reticulum stress. Mol Carcinog 54(10):1070–1085.  https://doi.org/10.1002/mc.22176 Google Scholar
  98. 98.
    Yamashiro K, Sasano T, Tojo K, Namekata I, Kurokawa J, Sawada N, Furukawa T et al (2010) Role of transient receptor potential vanilloid 2 in LPS-induced cytokine production in macrophages. Biochem Biophys Res Commun 398(2):284–289Google Scholar
  99. 99.
    Yang F, Zheng J (2017) Understand spiciness: mechanism of TRPV1 channel activation by capsaicin. Protein Cell 8(3):169–177.  https://doi.org/10.1007/s13238-016-0353-7 Google Scholar
  100. 100.
    Zhang D, Spielmann A, Wang L, Ding G, Huang F, Gu Q, Schwarz W (2012) Mast-cell degranulation induced by physical stimuli involves the activation of transient-receptor-potential channel TRPV2. Physiol Res 61(1):113–124Google Scholar
  101. 101.
    Zhang H, Xiao J, Hu Z, Xie M, Wang W, He D (2016) Blocking transient receptor potential vanilloid 2 channel in astrocytes enhances astrocyte-mediated neuroprotection after oxygen–glucose deprivation and reoxygenation. Eur J Neurosci 44(7):2493–2503.  https://doi.org/10.1111/ejn.13352 Google Scholar
  102. 102.
    Zhao J, Gover TD, Muralidharan S, Auston DA, Weinreich D, Kao JPY (2006) Caged vanilloid ligands for activation of TRPV1 receptors by 1- and 2-photon excitation. Biochemistry 45(15):4915–4926.  https://doi.org/10.1021/bi052082f Google Scholar
  103. 103.
    Zhen X, Xie C, Jiang Y, Ai X, Xing B, Pu K (2018) Semiconducting photothermal nanoagonist for remote-controlled specific cancer therapy. Nano Lett 18(2):1498–1505.  https://doi.org/10.1021/acs.nanolett.7b05292 Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.College of Life SciencesZhejiang UniversityHangzhouChina
  2. 2.Department of Microbiology, Immunology & Molecular GeneticsUniversity of CaliforniaLos AngelesUSA
  3. 3.School of Arts and SciencesSt. Bonaventure UniversityNew YorkUSA
  4. 4.School of Medicine and Health SciencesThe George Washington UniversityWashingtonUSA

Personalised recommendations