Skip to main content
Top
Published in: Seminars in Immunopathology 3/2018

Open Access 01-05-2018 | Review

A historical perspective on the role of sensory nerves in neurogenic inflammation

Authors: João Sousa-Valente, Susan D. Brain

Published in: Seminars in Immunopathology | Issue 3/2018

Login to get access

Abstract

The term ‘neurogenic inflammation’ is commonly used, especially with respect to the role of sensory nerves within inflammatory disease. However, despite over a century of research, we remain unclear about the role of these nerves in the vascular biology of inflammation, as compared with their interacting role in pain processing and of their potential for therapeutic manipulation. This chapter attempts to discuss the progress in understanding, from the initial discovery of sensory nerves until the present day. This covers pioneering findings that these nerves exist, are involved in vascular events and act as important sensors of environmental changes, including injury and infection. This is followed by discovery of the contents they release such as the established vasoactive neuropeptides substance P and CGRP as well as anti-inflammatory peptides such as the opioids and somatostatin. The more recent emergence of the importance of the transient receptor potential (TRP) channels has revealed some of the mechanisms by which these nerves sense environmental stimuli. This knowledge enables a platform from which to learn of the potential role of neurogenic inflammation in disease and in turn of novel therapeutic targets.
Literature
1.
go back to reference Ramaye A (2016) Chemical excitants of cutaneous pain. Perspectives in Basic & Applied Toxicology, ed. B. Ballantyne 13 31–41 Ramaye A (2016) Chemical excitants of cutaneous pain. Perspectives in Basic & Applied Toxicology, ed. B. Ballantyne 13 31–41
2.
go back to reference Goltz F, Freusberg A (1874) Ueber gefässerweiternde Nerven. Pflüger, Archiv für die Gesammte Physiologie des Menschen und der Thiere 9(1) 174-197 Goltz F, Freusberg A (1874) Ueber gefässerweiternde Nerven. Pflüger, Archiv für die Gesammte Physiologie des Menschen und der Thiere 9(1) 174-197
3.
go back to reference Stricker S (1876) Untersuchungen uber die Gefasserwurzeln des Ischiadicus. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften in Wien 3 173–185 Stricker S (1876) Untersuchungen uber die Gefasserwurzeln des Ischiadicus. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften in Wien 3 173–185
4.
go back to reference Sherrington CS (1893) Experiments in examination of the peripheral distribution of the fibres of the posterior roots of some spinal nerves. Philos Trans R Soc Lond B 184:641–763CrossRef Sherrington CS (1893) Experiments in examination of the peripheral distribution of the fibres of the posterior roots of some spinal nerves. Philos Trans R Soc Lond B 184:641–763CrossRef
6.
go back to reference Bayliss WM (1901) On the origin from the spinal cord of the vaso-dilator fibres of the hind-limb, and on the nature of these fibres. J Physiol 26(3–4):173–209CrossRefPubMedPubMedCentral Bayliss WM (1901) On the origin from the spinal cord of the vaso-dilator fibres of the hind-limb, and on the nature of these fibres. J Physiol 26(3–4):173–209CrossRefPubMedPubMedCentral
7.
go back to reference Oaklander AL (1999) The pathology of shingles: Head and Campbell’s 1900 monograph. Arch Neurol 56(10):1292–1294CrossRefPubMed Oaklander AL (1999) The pathology of shingles: Head and Campbell’s 1900 monograph. Arch Neurol 56(10):1292–1294CrossRefPubMed
8.
9.
go back to reference Head H, Campbell AW (1900) The pathology of herpes zoster and its bearing on sensory localisation. Brain 23(3):353–362CrossRef Head H, Campbell AW (1900) The pathology of herpes zoster and its bearing on sensory localisation. Brain 23(3):353–362CrossRef
10.
go back to reference Head H, Campbell AW, Kennedy PG (1997) The pathology of herpes zoster and its bearing on sensory localisation. Rev Med Virol 7(3):131–143CrossRefPubMed Head H, Campbell AW, Kennedy PG (1997) The pathology of herpes zoster and its bearing on sensory localisation. Rev Med Virol 7(3):131–143CrossRefPubMed
12.
go back to reference Johnson RW, Rice AS (2014) Clinical practice. Postherpetic neuralgia. N Engl J Med 371(16):1526–1533CrossRefPubMed Johnson RW, Rice AS (2014) Clinical practice. Postherpetic neuralgia. N Engl J Med 371(16):1526–1533CrossRefPubMed
13.
go back to reference Kim SR, Khan F, Ramirez-Fort MK, Downing C, Tyring SK (2014) Varicella zoster: an update on current treatment options and future perspectives. Expert Opin Pharmacother 15(1):61–71CrossRefPubMed Kim SR, Khan F, Ramirez-Fort MK, Downing C, Tyring SK (2014) Varicella zoster: an update on current treatment options and future perspectives. Expert Opin Pharmacother 15(1):61–71CrossRefPubMed
14.
go back to reference Spiess G, Die Bedeutung der Anästhesie in der Entzündungstherapie, JF Lehmann1906 Spiess G, Die Bedeutung der Anästhesie in der Entzündungstherapie, JF Lehmann1906
15.
go back to reference Jancsó G, Horváth V, Sántha P, Nagy J (2009) Sensory nerves as modulators of cutaneous inflammatory reactions in health and disease. Neuroimmune Biol 8:1–36CrossRef Jancsó G, Horváth V, Sántha P, Nagy J (2009) Sensory nerves as modulators of cutaneous inflammatory reactions in health and disease. Neuroimmune Biol 8:1–36CrossRef
16.
17.
go back to reference Breslauer F (1919) Die Pathogenese der trophischen Gewebsschäden nach der Nervenverletzung. Deutsche Zeitschrift für Chirurgie 150(1–2):50–81CrossRef Breslauer F (1919) Die Pathogenese der trophischen Gewebsschäden nach der Nervenverletzung. Deutsche Zeitschrift für Chirurgie 150(1–2):50–81CrossRef
18.
go back to reference Lewis T (1924) Vascular reactions of the skin to injury. Part 1. Reaction to stroking; urticaria factitia. Heart 11:119–140 Lewis T (1924) Vascular reactions of the skin to injury. Part 1. Reaction to stroking; urticaria factitia. Heart 11:119–140
19.
go back to reference Russell FA, King R, Smillie SJ, Kodji X, Brain SD (2014) Calcitonin gene-related peptide: physiology and pathophysiology. Physiol Rev 94(4):1099–1142CrossRefPubMedPubMedCentral Russell FA, King R, Smillie SJ, Kodji X, Brain SD (2014) Calcitonin gene-related peptide: physiology and pathophysiology. Physiol Rev 94(4):1099–1142CrossRefPubMedPubMedCentral
20.
go back to reference Jancso G, Kiraly E, Jancso-Gabor A (1977) Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. Nature 270(5639):741–743CrossRefPubMed Jancso G, Kiraly E, Jancso-Gabor A (1977) Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. Nature 270(5639):741–743CrossRefPubMed
21.
go back to reference Jancso N, Jancso-Gabor A, Szolcsanyi J (1967) Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br J Pharmacol Chemother 31(1):138–151CrossRefPubMedPubMedCentral Jancso N, Jancso-Gabor A, Szolcsanyi J (1967) Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br J Pharmacol Chemother 31(1):138–151CrossRefPubMedPubMedCentral
22.
go back to reference Kun J, Szitter I, Kemeny A, Perkecz A, Kereskai L, Pohoczky K, Vincze A, Godi S, Szabo I, Szolcsanyi J, Pinter E, Helyes Z (2014) Upregulation of the transient receptor potential ankyrin 1 ion channel in the inflamed human and mouse colon and its protective roles. PLoS One 9(9):e108164CrossRefPubMedPubMedCentral Kun J, Szitter I, Kemeny A, Perkecz A, Kereskai L, Pohoczky K, Vincze A, Godi S, Szabo I, Szolcsanyi J, Pinter E, Helyes Z (2014) Upregulation of the transient receptor potential ankyrin 1 ion channel in the inflamed human and mouse colon and its protective roles. PLoS One 9(9):e108164CrossRefPubMedPubMedCentral
23.
go back to reference Finnerup NB, Attal N, Haroutounian S, McNicol E, Baron R, Dworkin RH, Gilron I, Haanpaa M, Hansson P, Jensen TS, Kamerman PR, Lund K, Moore A, Raja SN, Rice AS, Rowbotham M, Sena E, Siddall P, Smith BH, Wallace M (2015) Pharmacotherapy for neuropathic pain in adults: a systematic review and meta-analysis. Lancet Neurol 14(2):162–173CrossRefPubMedPubMedCentral Finnerup NB, Attal N, Haroutounian S, McNicol E, Baron R, Dworkin RH, Gilron I, Haanpaa M, Hansson P, Jensen TS, Kamerman PR, Lund K, Moore A, Raja SN, Rice AS, Rowbotham M, Sena E, Siddall P, Smith BH, Wallace M (2015) Pharmacotherapy for neuropathic pain in adults: a systematic review and meta-analysis. Lancet Neurol 14(2):162–173CrossRefPubMedPubMedCentral
24.
25.
go back to reference Lembeck F, Donnerer J (2004) History of a pioneering neuropeptide: substance P. Tachykinins:1–23 Lembeck F, Donnerer J (2004) History of a pioneering neuropeptide: substance P. Tachykinins:1–23
26.
go back to reference Chang MM, Leeman SE (1970) Isolation of a sialogogic peptide from bovine hypothalamic tissue and its characterization as substance P. J Biol Chem 245(18):4784–4790PubMed Chang MM, Leeman SE (1970) Isolation of a sialogogic peptide from bovine hypothalamic tissue and its characterization as substance P. J Biol Chem 245(18):4784–4790PubMed
27.
go back to reference Gasparovic I, Hadzovic S, Hukovic S, Stern P (1964) Contribution to the theory that substance P has a transmitter role in sensitive pathway. Med Exp Int J Exp Med 10:303–306PubMed Gasparovic I, Hadzovic S, Hukovic S, Stern P (1964) Contribution to the theory that substance P has a transmitter role in sensitive pathway. Med Exp Int J Exp Med 10:303–306PubMed
28.
go back to reference Jessell TM, Iversen LL, Cuello AC (1978) Capsaicin-induced depletion of substance P from primary sensory neurones. Brain Res 152(1):183–188CrossRefPubMed Jessell TM, Iversen LL, Cuello AC (1978) Capsaicin-induced depletion of substance P from primary sensory neurones. Brain Res 152(1):183–188CrossRefPubMed
29.
go back to reference Hokfelt T, Kellerth JO, Nilsson G, Pernow B (1975) Substance p: localization in the central nervous system and in some primary sensory neurons. Science 190(4217):889–890CrossRefPubMed Hokfelt T, Kellerth JO, Nilsson G, Pernow B (1975) Substance p: localization in the central nervous system and in some primary sensory neurons. Science 190(4217):889–890CrossRefPubMed
30.
go back to reference Gamse R, Holzer P, Lembeck F (1980) Decrease of substance P in primary afferent neurones and impairment of neurogenic plasma extravasation by capsaicin. Br J Pharmacol 68(2):207–213CrossRefPubMedPubMedCentral Gamse R, Holzer P, Lembeck F (1980) Decrease of substance P in primary afferent neurones and impairment of neurogenic plasma extravasation by capsaicin. Br J Pharmacol 68(2):207–213CrossRefPubMedPubMedCentral
31.
go back to reference Lembeck F, Donnerer J (1981) Postocclusive cutaneous vasodilatation mediated by substance P. Naunyn Schmiedebergs Arch Pharmacol 316(2):165–171CrossRefPubMed Lembeck F, Donnerer J (1981) Postocclusive cutaneous vasodilatation mediated by substance P. Naunyn Schmiedebergs Arch Pharmacol 316(2):165–171CrossRefPubMed
32.
go back to reference Lembeck F, Holzer P (1979) Substance-P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn Schmiedebergs Arch Pharmacol 310(2):175–183CrossRefPubMed Lembeck F, Holzer P (1979) Substance-P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn Schmiedebergs Arch Pharmacol 310(2):175–183CrossRefPubMed
33.
go back to reference Lembeck F (1983) Sir Thomas Lewis’s nocifensor system, histamine and substance-P-containing primary afferent nerves. Trends Neurosci 6:106–108CrossRef Lembeck F (1983) Sir Thomas Lewis’s nocifensor system, histamine and substance-P-containing primary afferent nerves. Trends Neurosci 6:106–108CrossRef
34.
go back to reference Brain SD, Tippins JR, Morris HR, MacIntyre I, Williams TJ (1986) Potent vasodilator activity of calcitonin gene-related peptide in human skin. J Invest Dermatol 87(4):533–536CrossRefPubMed Brain SD, Tippins JR, Morris HR, MacIntyre I, Williams TJ (1986) Potent vasodilator activity of calcitonin gene-related peptide in human skin. J Invest Dermatol 87(4):533–536CrossRefPubMed
35.
go back to reference Erspamer V (1981) The tachykinin peptide family. Trends Neurosci 4:267–269CrossRef Erspamer V (1981) The tachykinin peptide family. Trends Neurosci 4:267–269CrossRef
37.
go back to reference Hill R (2000) NK1 (substance P) receptor antagonists—why are they not analgesic in humans? Trends Pharmacol Sci 21(7):244–246CrossRefPubMed Hill R (2000) NK1 (substance P) receptor antagonists—why are they not analgesic in humans? Trends Pharmacol Sci 21(7):244–246CrossRefPubMed
38.
go back to reference Song JS, Tawa M, Chau NG, Kupper TS, LeBoeuf NR (2017) Aprepitant for refractory cutaneous T-cell lymphoma-associated pruritus: 4 cases and a review of the literature. BMC Cancer 17(1):200CrossRefPubMedPubMedCentral Song JS, Tawa M, Chau NG, Kupper TS, LeBoeuf NR (2017) Aprepitant for refractory cutaneous T-cell lymphoma-associated pruritus: 4 cases and a review of the literature. BMC Cancer 17(1):200CrossRefPubMedPubMedCentral
39.
go back to reference Lotts T, Stander S (2014) Research in practice: substance P antagonism in chronic pruritus. J Dtsch Dermatol Ges 12(7):557–559PubMed Lotts T, Stander S (2014) Research in practice: substance P antagonism in chronic pruritus. J Dtsch Dermatol Ges 12(7):557–559PubMed
40.
go back to reference Atoyan R, Shander D, Botchkareva NV (2009) Non-neuronal expression of transient receptor potential type A1 (TRPA1) in human skin. J Invest Dermatol 129(9):2312–2315CrossRefPubMed Atoyan R, Shander D, Botchkareva NV (2009) Non-neuronal expression of transient receptor potential type A1 (TRPA1) in human skin. J Invest Dermatol 129(9):2312–2315CrossRefPubMed
41.
go back to reference Lundberg JM, Franco-Cereceda A, Hua X, Hokfelt T, Fischer JA (1985) Co-existence of substance P and calcitonin gene-related peptide-like immunoreactivities in sensory nerves in relation to cardiovascular and bronchoconstrictor effects of capsaicin. Eur J Pharmacol 108(3):315–319CrossRefPubMed Lundberg JM, Franco-Cereceda A, Hua X, Hokfelt T, Fischer JA (1985) Co-existence of substance P and calcitonin gene-related peptide-like immunoreactivities in sensory nerves in relation to cardiovascular and bronchoconstrictor effects of capsaicin. Eur J Pharmacol 108(3):315–319CrossRefPubMed
42.
go back to reference Gibbins IL, Furness JB, Costa M, MacIntyre I, Hillyard CJ, Girgis S (1985) Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs. Neurosci Lett 57(2):125–130CrossRefPubMed Gibbins IL, Furness JB, Costa M, MacIntyre I, Hillyard CJ, Girgis S (1985) Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs. Neurosci Lett 57(2):125–130CrossRefPubMed
43.
go back to reference Brain SD, Williams TJ, Tippins JR, Morris HR, MacIntyre I (1985) Calcitonin gene-related peptide is a potent vasodilator. Nature 313(5997):54–56CrossRefPubMed Brain SD, Williams TJ, Tippins JR, Morris HR, MacIntyre I (1985) Calcitonin gene-related peptide is a potent vasodilator. Nature 313(5997):54–56CrossRefPubMed
44.
go back to reference McCulloch J, Uddman R, Kingman TA, Edvinsson L (1986) Calcitonin gene-related peptide: functional role in cerebrovascular regulation. Proc Natl Acad Sci U S A 83(15):5731–5735CrossRefPubMedPubMedCentral McCulloch J, Uddman R, Kingman TA, Edvinsson L (1986) Calcitonin gene-related peptide: functional role in cerebrovascular regulation. Proc Natl Acad Sci U S A 83(15):5731–5735CrossRefPubMedPubMedCentral
45.
go back to reference Goadsby PJ, Edvinsson L, Ekman R (1988) Release of vasoactive peptides in the extracerebral circulation of humans and the cat during activation of the trigeminovascular system. Ann Neurol 23(2):193–196CrossRefPubMed Goadsby PJ, Edvinsson L, Ekman R (1988) Release of vasoactive peptides in the extracerebral circulation of humans and the cat during activation of the trigeminovascular system. Ann Neurol 23(2):193–196CrossRefPubMed
46.
go back to reference Garret C, Carruette A, Fardin V, Moussaoui S, Peyronel JF, Blanchard JC, Laduron PM (1991) Pharmacological properties of a potent and selective nonpeptide substance P antagonist. Proc Natl Acad Sci U S A 88(22):10208–10212CrossRefPubMedPubMedCentral Garret C, Carruette A, Fardin V, Moussaoui S, Peyronel JF, Blanchard JC, Laduron PM (1991) Pharmacological properties of a potent and selective nonpeptide substance P antagonist. Proc Natl Acad Sci U S A 88(22):10208–10212CrossRefPubMedPubMedCentral
47.
go back to reference McLatchie LM, Fraser NJ, Main MJ, Wise A, Brown J, Thompson N, Solari R, Lee MG, Foord SM (1998) RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393(6683):333–339CrossRefPubMed McLatchie LM, Fraser NJ, Main MJ, Wise A, Brown J, Thompson N, Solari R, Lee MG, Foord SM (1998) RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393(6683):333–339CrossRefPubMed
48.
49.
go back to reference Van der Schueren BJ, Rogiers A, Vanmolkot FH, Van Hecken A, Depre M, Kane SA, De Lepeleire I, Sinclair SR, de Hoon JN (2008) Calcitonin gene-related peptide8-37 antagonizes capsaicin-induced vasodilation in the skin: evaluation of a human in vivo pharmacodynamic model. J Pharmacol Exp Ther 325(1):248–255CrossRefPubMed Van der Schueren BJ, Rogiers A, Vanmolkot FH, Van Hecken A, Depre M, Kane SA, De Lepeleire I, Sinclair SR, de Hoon JN (2008) Calcitonin gene-related peptide8-37 antagonizes capsaicin-induced vasodilation in the skin: evaluation of a human in vivo pharmacodynamic model. J Pharmacol Exp Ther 325(1):248–255CrossRefPubMed
50.
go back to reference Escott KJ, Brain SD (1993) Effect of a calcitonin gene-related peptide antagonist (CGRP8-37) on skin vasodilatation and oedema induced by stimulation of the rat saphenous nerve. Br J Pharmacol 110(2):772–776CrossRefPubMedPubMedCentral Escott KJ, Brain SD (1993) Effect of a calcitonin gene-related peptide antagonist (CGRP8-37) on skin vasodilatation and oedema induced by stimulation of the rat saphenous nerve. Br J Pharmacol 110(2):772–776CrossRefPubMedPubMedCentral
51.
go back to reference Murota H, Katayama I (2016) Evolving understanding on the aetiology of thermally provoked itch. Eur J Pain 20(1):47–50CrossRefPubMed Murota H, Katayama I (2016) Evolving understanding on the aetiology of thermally provoked itch. Eur J Pain 20(1):47–50CrossRefPubMed
52.
53.
go back to reference Smillie SJ, Brain SD (2011) Calcitonin gene-related peptide (CGRP) and its role in hypertension. Neuropeptides 45(2):93–104CrossRefPubMed Smillie SJ, Brain SD (2011) Calcitonin gene-related peptide (CGRP) and its role in hypertension. Neuropeptides 45(2):93–104CrossRefPubMed
54.
go back to reference Kirkby NS, Hadoke PW, Bagnall AJ, Webb DJ (2008) The endothelin system as a therapeutic target in cardiovascular disease: great expectations or bleak house? Br J Pharmacol 153(6):1105–1119CrossRefPubMed Kirkby NS, Hadoke PW, Bagnall AJ, Webb DJ (2008) The endothelin system as a therapeutic target in cardiovascular disease: great expectations or bleak house? Br J Pharmacol 153(6):1105–1119CrossRefPubMed
55.
go back to reference Opitz CF, Ewert R (2006) Dual ET(A)/ET(B) vs. selective ET(A) endothelin receptor antagonism in patients with pulmonary hypertension. Eur J Clin Invest 36(Suppl 3):1–9CrossRefPubMed Opitz CF, Ewert R (2006) Dual ET(A)/ET(B) vs. selective ET(A) endothelin receptor antagonism in patients with pulmonary hypertension. Eur J Clin Invest 36(Suppl 3):1–9CrossRefPubMed
56.
go back to reference Gamse R, Lackner D, Gamse G, Leeman SE (1981) Effect of capsaicin pretreatment on capsaicin-evoked release of immunoreactive somatostatin and substance P from primary sensory neurons. Naunyn-Schmiedeberg’s Arch Pharmacol 316(1):38–41CrossRef Gamse R, Lackner D, Gamse G, Leeman SE (1981) Effect of capsaicin pretreatment on capsaicin-evoked release of immunoreactive somatostatin and substance P from primary sensory neurons. Naunyn-Schmiedeberg’s Arch Pharmacol 316(1):38–41CrossRef
57.
go back to reference Szolcsanyi J, Pinter E, Helyes Z, Petho G (2011) Inhibition of the function of TRPV1-expressing nociceptive sensory neurons by somatostatin 4 receptor agonism: mechanism and therapeutical implications. Curr Top Med Chem 11(17):2253–2263CrossRefPubMed Szolcsanyi J, Pinter E, Helyes Z, Petho G (2011) Inhibition of the function of TRPV1-expressing nociceptive sensory neurons by somatostatin 4 receptor agonism: mechanism and therapeutical implications. Curr Top Med Chem 11(17):2253–2263CrossRefPubMed
59.
go back to reference Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389(6653):816–824CrossRefPubMed Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389(6653):816–824CrossRefPubMed
60.
go back to reference Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288(5464):306–313CrossRefPubMed Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288(5464):306–313CrossRefPubMed
61.
go back to reference Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405(6783):183–187CrossRefPubMed Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405(6783):183–187CrossRefPubMed
62.
go back to reference Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112(6):819–829CrossRefPubMed Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112(6):819–829CrossRefPubMed
63.
go back to reference Andersson DA, Gentry C, Moss S, Bevan S (2008) Transient receptor potential A1 is a sensory receptor for multiple products of oxidative stress. J Neurosci 28(10):2485–2494CrossRefPubMedPubMedCentral Andersson DA, Gentry C, Moss S, Bevan S (2008) Transient receptor potential A1 is a sensory receptor for multiple products of oxidative stress. J Neurosci 28(10):2485–2494CrossRefPubMedPubMedCentral
64.
go back to reference Eberhardt M, Dux M, Namer B, Miljkovic J, Cordasic N, Will C, Kichko TI, de la Roche J, Fischer M, Suarez SA, Bikiel D, Dorsch K, Leffler A, Babes A, Lampert A, Lennerz JK, Jacobi J, Marti MA, Doctorovich F, Hogestatt ED, Zygmunt PM, Ivanovic-Burmazovic I, Messlinger K, Reeh P, Filipovic MR (2014) H2S and NO cooperatively regulate vascular tone by activating a neuroendocrine HNO-TRPA1-CGRP signalling pathway. Nat Commun 5:4381CrossRefPubMed Eberhardt M, Dux M, Namer B, Miljkovic J, Cordasic N, Will C, Kichko TI, de la Roche J, Fischer M, Suarez SA, Bikiel D, Dorsch K, Leffler A, Babes A, Lampert A, Lennerz JK, Jacobi J, Marti MA, Doctorovich F, Hogestatt ED, Zygmunt PM, Ivanovic-Burmazovic I, Messlinger K, Reeh P, Filipovic MR (2014) H2S and NO cooperatively regulate vascular tone by activating a neuroendocrine HNO-TRPA1-CGRP signalling pathway. Nat Commun 5:4381CrossRefPubMed
65.
go back to reference Aubdool AA, Graepel R, Kodji X, Alawi KM, Bodkin JV, Srivastava S, Gentry C, Heads R, Grant AD, Fernandes ES, Bevan S, Brain SD (2014) TRPA1 is essential for the vascular response to environmental cold exposure. Nat Commun 5:5732CrossRefPubMed Aubdool AA, Graepel R, Kodji X, Alawi KM, Bodkin JV, Srivastava S, Gentry C, Heads R, Grant AD, Fernandes ES, Bevan S, Brain SD (2014) TRPA1 is essential for the vascular response to environmental cold exposure. Nat Commun 5:5732CrossRefPubMed
66.
go back to reference Keeble J, Russell F, Curtis B, Starr A, Pinter E, Brain SD (2005) Involvement of transient receptor potential vanilloid 1 in the vascular and hyperalgesic components of joint inflammation. Arthritis Rheum 52(10):3248–3256CrossRefPubMed Keeble J, Russell F, Curtis B, Starr A, Pinter E, Brain SD (2005) Involvement of transient receptor potential vanilloid 1 in the vascular and hyperalgesic components of joint inflammation. Arthritis Rheum 52(10):3248–3256CrossRefPubMed
67.
go back to reference Fernandes ES, Russell FA, Spina D, McDougall JJ, Graepel R, Gentry C, Staniland AA, Mountford DM, Keeble JE, Malcangio M, Bevan S, Brain SD (2011) A distinct role for transient receptor potential ankyrin 1, in addition to transient receptor potential vanilloid 1, in tumor necrosis factor alpha-induced inflammatory hyperalgesia and Freund’s complete adjuvant-induced monarthritis. Arthritis Rheum 63(3):819–829CrossRefPubMed Fernandes ES, Russell FA, Spina D, McDougall JJ, Graepel R, Gentry C, Staniland AA, Mountford DM, Keeble JE, Malcangio M, Bevan S, Brain SD (2011) A distinct role for transient receptor potential ankyrin 1, in addition to transient receptor potential vanilloid 1, in tumor necrosis factor alpha-induced inflammatory hyperalgesia and Freund’s complete adjuvant-induced monarthritis. Arthritis Rheum 63(3):819–829CrossRefPubMed
68.
go back to reference Gavva NR, Bannon AW, Surapaneni S, Hovland DN Jr, Lehto SG, Gore A, Juan T, Deng H, Han B, Klionsky L, Kuang R, Le A, Tamir R, Wang J, Youngblood B, Zhu D, Norman MH, Magal E, Treanor JJ, Louis JC (2007) The vanilloid receptor TRPV1 is tonically activated in vivo and involved in body temperature regulation. J Neurosci 27(13):3366–3374CrossRefPubMedPubMedCentral Gavva NR, Bannon AW, Surapaneni S, Hovland DN Jr, Lehto SG, Gore A, Juan T, Deng H, Han B, Klionsky L, Kuang R, Le A, Tamir R, Wang J, Youngblood B, Zhu D, Norman MH, Magal E, Treanor JJ, Louis JC (2007) The vanilloid receptor TRPV1 is tonically activated in vivo and involved in body temperature regulation. J Neurosci 27(13):3366–3374CrossRefPubMedPubMedCentral
70.
go back to reference Preti D, Saponaro G, Szallasi A (2015) Transient receptor potential ankyrin 1 (TRPA1) antagonists. Pharm Pat Anal 4(2):75–94CrossRefPubMed Preti D, Saponaro G, Szallasi A (2015) Transient receptor potential ankyrin 1 (TRPA1) antagonists. Pharm Pat Anal 4(2):75–94CrossRefPubMed
71.
go back to reference Yiangou Y, Facer P, Dyer NH, Chan CL, Knowles C, Williams NS, Anand P (2001) Vanilloid receptor 1 immunoreactivity in inflamed human bowel. Lancet 357(9265):1338–1339CrossRefPubMed Yiangou Y, Facer P, Dyer NH, Chan CL, Knowles C, Williams NS, Anand P (2001) Vanilloid receptor 1 immunoreactivity in inflamed human bowel. Lancet 357(9265):1338–1339CrossRefPubMed
72.
go back to reference Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, Story GM, Colley S, Hogenesch JB, McIntyre P, Bevan S, Patapoutian A (2002) A heat-sensitive TRP channel expressed in keratinocytes. Science 296(5575):2046–2049CrossRefPubMed Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, Story GM, Colley S, Hogenesch JB, McIntyre P, Bevan S, Patapoutian A (2002) A heat-sensitive TRP channel expressed in keratinocytes. Science 296(5575):2046–2049CrossRefPubMed
73.
go back to reference Zimmermann K, Leffler A, Fischer MM, Messlinger K, Nau C, Reeh PW (2005) The TRPV1/2/3 activator 2-aminoethoxydiphenyl borate sensitizes native nociceptive neurons to heat in wildtype but not TRPV1 deficient mice. Neuroscience 135(4):1277–1284CrossRefPubMed Zimmermann K, Leffler A, Fischer MM, Messlinger K, Nau C, Reeh PW (2005) The TRPV1/2/3 activator 2-aminoethoxydiphenyl borate sensitizes native nociceptive neurons to heat in wildtype but not TRPV1 deficient mice. Neuroscience 135(4):1277–1284CrossRefPubMed
74.
go back to reference Kimball ES, Prouty SP, Pavlick KP, Wallace NH, Schneider CR, Hornby PJ (2007) Stimulation of neuronal receptors, neuropeptides and cytokines during experimental oil of mustard colitis. Neurogastroenterol Motil 19(5):390–400CrossRefPubMed Kimball ES, Prouty SP, Pavlick KP, Wallace NH, Schneider CR, Hornby PJ (2007) Stimulation of neuronal receptors, neuropeptides and cytokines during experimental oil of mustard colitis. Neurogastroenterol Motil 19(5):390–400CrossRefPubMed
75.
go back to reference Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103(3):525–535CrossRefPubMedPubMedCentral Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103(3):525–535CrossRefPubMedPubMedCentral
76.
go back to reference Vergnolle N, Cenac N, Altier C, Cellars L, Chapman K, Zamponi GW, Materazzi S, Nassini R, Liedtke W, Cattaruzza F, Grady EF, Geppetti P, Bunnett NW (2010) A role for transient receptor potential vanilloid 4 in tonicity-induced neurogenic inflammation. Br J Pharmacol 159(5):1161–1173CrossRefPubMedPubMedCentral Vergnolle N, Cenac N, Altier C, Cellars L, Chapman K, Zamponi GW, Materazzi S, Nassini R, Liedtke W, Cattaruzza F, Grady EF, Geppetti P, Bunnett NW (2010) A role for transient receptor potential vanilloid 4 in tonicity-induced neurogenic inflammation. Br J Pharmacol 159(5):1161–1173CrossRefPubMedPubMedCentral
77.
go back to reference McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416(6876):52–58CrossRefPubMed McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416(6876):52–58CrossRefPubMed
78.
go back to reference Olsen RV, Andersen HH, Moller HG, Eskelund PW, Arendt-Nielsen L (2014) Somatosensory and vasomotor manifestations of individual and combined stimulation of TRPM8 and TRPA1 using topical L-menthol and trans-cinnamaldehyde in healthy volunteers. Eur J Pain 18(9):1333–1342CrossRefPubMed Olsen RV, Andersen HH, Moller HG, Eskelund PW, Arendt-Nielsen L (2014) Somatosensory and vasomotor manifestations of individual and combined stimulation of TRPM8 and TRPA1 using topical L-menthol and trans-cinnamaldehyde in healthy volunteers. Eur J Pain 18(9):1333–1342CrossRefPubMed
79.
go back to reference Vriens J, Owsianik G, Hofmann T, Philipp SE, Stab J, Chen X, Benoit M, Xue F, Janssens A, Kerselaers S, Oberwinkler J, Vennekens R, Gudermann T, Nilius B, Voets T (2011) TRPM3 is a nociceptor channel involved in the detection of noxious heat. Neuron 70(3):482–494CrossRefPubMed Vriens J, Owsianik G, Hofmann T, Philipp SE, Stab J, Chen X, Benoit M, Xue F, Janssens A, Kerselaers S, Oberwinkler J, Vennekens R, Gudermann T, Nilius B, Voets T (2011) TRPM3 is a nociceptor channel involved in the detection of noxious heat. Neuron 70(3):482–494CrossRefPubMed
80.
go back to reference Held K, Kichko T, De Clercq K, Klaassen H, Van Bree R, Vanherck JC, Marchand A, Reeh PW, Chaltin P, Voets T, Vriens J (2015) Activation of TRPM3 by a potent synthetic ligand reveals a role in peptide release. Proc Natl Acad Sci U S A 112(11):E1363–E1372CrossRefPubMedPubMedCentral Held K, Kichko T, De Clercq K, Klaassen H, Van Bree R, Vanherck JC, Marchand A, Reeh PW, Chaltin P, Voets T, Vriens J (2015) Activation of TRPM3 by a potent synthetic ligand reveals a role in peptide release. Proc Natl Acad Sci U S A 112(11):E1363–E1372CrossRefPubMedPubMedCentral
81.
go back to reference von Euler US, Gaddum JH (1931) An unidentified depressor substance in certain tissue extracts. J Physiol 72(1):74–87CrossRef von Euler US, Gaddum JH (1931) An unidentified depressor substance in certain tissue extracts. J Physiol 72(1):74–87CrossRef
82.
go back to reference Rosenfeld MG, Mermod JJ, Amara SG, Swanson LW, Sawchenko PE, Rivier J, Vale WW, Evans RM (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature 304(5922):129–135CrossRefPubMed Rosenfeld MG, Mermod JJ, Amara SG, Swanson LW, Sawchenko PE, Rivier J, Vale WW, Evans RM (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature 304(5922):129–135CrossRefPubMed
83.
go back to reference Masu Y, Nakayama K, Tamaki H, Harada Y, Kuno M, Nakanishi S (1987) cDNA cloning of bovine substance-K receptor through oocyte expression system. Nature 329(6142):836–838CrossRefPubMed Masu Y, Nakayama K, Tamaki H, Harada Y, Kuno M, Nakanishi S (1987) cDNA cloning of bovine substance-K receptor through oocyte expression system. Nature 329(6142):836–838CrossRefPubMed
84.
go back to reference Olesen J, Diener HC, Husstedt IW, Goadsby PJ, Hall D, Meier U, Pollentier S, Lesko LM, Group BBCPoCS (2004) Calcitonin gene-related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine. N Engl J Med 350(11):1104–1110CrossRefPubMed Olesen J, Diener HC, Husstedt IW, Goadsby PJ, Hall D, Meier U, Pollentier S, Lesko LM, Group BBCPoCS (2004) Calcitonin gene-related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine. N Engl J Med 350(11):1104–1110CrossRefPubMed
85.
go back to reference Dodick DW, Goadsby PJ, Silberstein SD, Lipton RB, Olesen J, Ashina M, Wilks K, Kudrow D, Kroll R, Kohrman B, Bargar R, Hirman J, Smith J, investigators ALDs (2014) Safety and efficacy of ALD403, an antibody to calcitonin gene-related peptide, for the prevention of frequent episodic migraine: a randomised, double-blind, placebo-controlled, exploratory phase 2 trial. Lancet Neurol 13(11):1100–1107CrossRefPubMed Dodick DW, Goadsby PJ, Silberstein SD, Lipton RB, Olesen J, Ashina M, Wilks K, Kudrow D, Kroll R, Kohrman B, Bargar R, Hirman J, Smith J, investigators ALDs (2014) Safety and efficacy of ALD403, an antibody to calcitonin gene-related peptide, for the prevention of frequent episodic migraine: a randomised, double-blind, placebo-controlled, exploratory phase 2 trial. Lancet Neurol 13(11):1100–1107CrossRefPubMed
86.
go back to reference Dodick DW, Goadsby PJ, Spierings EL, Scherer JC, Sweeney SP, Grayzel DS (2014) Safety and efficacy of LY2951742, a monoclonal antibody to calcitonin gene-related peptide, for the prevention of migraine: a phase 2, randomised, double-blind, placebo-controlled study. Lancet Neurol 13(9):885–892CrossRefPubMed Dodick DW, Goadsby PJ, Spierings EL, Scherer JC, Sweeney SP, Grayzel DS (2014) Safety and efficacy of LY2951742, a monoclonal antibody to calcitonin gene-related peptide, for the prevention of migraine: a phase 2, randomised, double-blind, placebo-controlled study. Lancet Neurol 13(9):885–892CrossRefPubMed
87.
go back to reference Bigal ME, Dodick DW, Rapoport AM, Silberstein SD, Ma Y, Yang R, Loupe PS, Burstein R, Newman LC, Lipton RB (2015) Safety, tolerability, and efficacy of TEV-48125 for preventive treatment of high-frequency episodic migraine: a multicentre, randomised, double-blind, placebo-controlled, phase 2b study. Lancet Neurol 14(11):1081–1090CrossRefPubMed Bigal ME, Dodick DW, Rapoport AM, Silberstein SD, Ma Y, Yang R, Loupe PS, Burstein R, Newman LC, Lipton RB (2015) Safety, tolerability, and efficacy of TEV-48125 for preventive treatment of high-frequency episodic migraine: a multicentre, randomised, double-blind, placebo-controlled, phase 2b study. Lancet Neurol 14(11):1081–1090CrossRefPubMed
88.
go back to reference Sun H, Dodick DW, Silberstein S, Goadsby PJ, Reuter U, Ashina M, Saper J, Cady R, Chon Y, Dietrich J, Lenz R (2016) Safety and efficacy of AMG 334 for prevention of episodic migraine: a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Neurol 15(4):382–390CrossRefPubMed Sun H, Dodick DW, Silberstein S, Goadsby PJ, Reuter U, Ashina M, Saper J, Cady R, Chon Y, Dietrich J, Lenz R (2016) Safety and efficacy of AMG 334 for prevention of episodic migraine: a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Neurol 15(4):382–390CrossRefPubMed
Metadata
Title
A historical perspective on the role of sensory nerves in neurogenic inflammation
Authors
João Sousa-Valente
Susan D. Brain
Publication date
01-05-2018
Publisher
Springer Berlin Heidelberg
Published in
Seminars in Immunopathology / Issue 3/2018
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-018-0673-1

Other articles of this Issue 3/2018

Seminars in Immunopathology 3/2018 Go to the issue