502
Views
50
CrossRef citations to date
0
Altmetric
Theme: Pain - Review

Nerve growth factor, pain, itch and inflammation: lessons from congenital insensitivity to pain with anhidrosis

Pages 1707-1724 | Published online: 09 Jan 2014

References

  • Breivik H, Collett B, Ventafridda V, Cohen R, Gallacher D. Survey of chronic pain in Europe: prevalence, impact on daily life, and treatment. Eur. J. Pain10(4), 287–333 (2006).
  • Lacroix-Fralish ML, Mogil JS. Progress in genetic studies of pain and analgesia. Annu. Rev. Pharmacol. Toxicol.49, 97–121 (2009).
  • Mogil JS. Animal models of pain: progress and challenges. Nat. Rev. Neurosci.10(4), 283–294 (2009).
  • Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci.3(8), 655–666 (2002).
  • Craig AD. A rat is not a monkey is not a human: comment on Mogil (Nature Rev. Neurosci.10, 283–294 [2009]). Nat. Rev. Neurosci.10(6), 466 (2009).
  • Craig AD. How do you feel – now? The anterior insula and human awareness. Nat. Rev. Neurosci.10(1), 59–70 (2009).
  • Ikoma A, Steinhoff M, Stander S, Yosipovitch G, Schmelz M. The neurobiology of itch. Nat. Rev. Neurosci.7(7), 535–547 (2006).
  • Steinhoff M, Bienenstock J, Schmelz M, Maurer M, Wei E, Biro T. Neurophysiological, neuroimmunological, and neuroendocrine basis of pruritus. J. Invest. Dermatol.126(8), 1705–1718 (2006).
  • Miller G. Biomedicine. Grasping for clues to the biology of itch. Science318(5848), 188–189 (2007).
  • Roosterman D, Goerge T, Schneider SW, Bunnett NW, Steinhoff M. Neuronal control of skin function: the skin as a neuroimmunoendocrine organ. Physiol. Rev.86(4), 1309–1379 (2006).
  • Schmelz M, Handwerker HO. Itch. In: Wall and Melzack’s Textbook of Pain.McMahon SB, Kolzenburg M (Eds.), Elsevier, Philadelphia, PA, USA, 219–227 (2006).
  • Stander S, Schmelz M. Chronic itch and pain – similarities and differences. Eur. J. Pain10(5), 473–478 (2006).
  • Stander S, Weisshaar E, Luger TA. Neurophysiological and neurochemical basis of modern pruritus treatment. Exp. Dermatol.17(3), 161–169 (2008).
  • Paus R, Schmelz M, Biro T, Steinhoff M. Frontiers in pruritus research: scratching the brain for more effective itch therapy. J. Clin. Invest.116(5), 1174–1186 (2006).
  • Biro T, Ko MC, Bromm B et al. How best to fight that nasty itch – from new insights into the neuroimmunological, neuroendocrine, and neurophysiological bases of pruritus to novel therapeutic approaches. Exp. Dermatol.14(3), 225–240 (2005).
  • Aloe L. Rita Levi-Montalcini: the discovery of nerve growth factor and modern neurobiology. Trends Cell. Biol.14(7), 395–399 (2004).
  • Levi-Montalcini R. The nerve growth factor 35 years later. Science237(4819), 1154–1162 (1987).
  • Pezet S, McMahon SB. Neurotrophins: mediators and modulators of pain. Annu. Rev. Neurosci.29, 507–538 (2006).
  • Reichardt LF. Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond. B. Biol. Sci.361(1473), 1545–1564 (2006).
  • Roux PP, Barker PA. Neurotrophin signaling through the p75 neurotrophin receptor. Prog. Neurobiol.67(3), 203–233 (2002).
  • Barker PA. High affinity not in the vicinity? Neuron53(1), 1–4 (2007).
  • Chao MV, Rajagopal R, Lee FS. Neurotrophin signalling in health and disease. Clin. Sci. (Lond.)110(2), 167–173 (2006).
  • Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci.24, 677–736 (2001).
  • Huang EJ, Reichardt LF. Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem.72, 609–642 (2003).
  • Miller FD, Kaplan DR. On Trk for retrograde signaling. Neuron32(5), 767–770 (2001).
  • Wehrman T, He X, Raab B, Dukipatti A, Blau H, Garcia KC. Structural and mechanistic insights into nerve growth factor interactions with the TrkA and p75 receptors. Neuron53(1), 25–38 (2007).
  • Foulkes T, Wood JN. Pain genes. PLoS Genet.4(7), e1000086 (2008).
  • Oertel B, Lotsch J. Genetic mutations that prevent pain: implications for future pain medication. Pharmacogenomics9(2), 179–194 (2008).
  • Auer-Grumbach M, Mauko B, Auer-Grumbach P, Pieber TR. Molecular genetics of hereditary sensory neuropathies. Neuromolecular Med.8(1–2), 147–158 (2006).
  • Axelrod FB, Chelimsky GG, Weese-Mayer DE. Pediatric autonomic disorders. Pediatrics118(1), 309–321 (2006).
  • Freeman R. Autonomic peripheral neuropathy. Lancet365(9466), 1259–1270 (2005).
  • Indo Y. Molecular basis of congenital insensitivity to pain with anhidrosis (CIPA): mutations and polymorphisms in TRKA (NTRK1) gene encoding the receptor tyrosine kinase for nerve growth factor. Hum. Mutat.18(6), 462–471 (2001).
  • Indo Y. Genetics of congenital insensitivity to pain with anhidrosis (CIPA) or hereditary sensory and autonomic neuropathy type IV. Clinical, biological and molecular aspects of mutations in TRKA (NTRK1) gene encoding the receptor tyrosine kinase for nerve growth factor. Clin. Auton. Res.12(Suppl. 1), I20–I32 (2002).
  • Indo Y. Congenital insensitivity to pain. In: The Genetics of Pain. Mogil JS (Ed.), IASP Press, Seattle, WA, USA, 171–191 (2004).
  • Indo Y. Nerve growth factor, interoception, and sympathetic neuron: lesson from congenital insensitivity to pain with anhidrosis. Auton. Neurosci.147(1–2), 3–8 (2009).
  • Rotthier A, Baets J, De Vriendt E et al. Genes for hereditary sensory and autonomic neuropathies: a genotype-phenotype correlation. Brain132(Pt 10), 2699–2711 (2009).
  • Indo Y, Mardy S, Miura Y et al. Congenital insensitivity to pain with anhidrosis (CIPA): novel mutations of the TRKA(NTRK1) gene, a putative uniparental disomy, and a linkage of the mutant TRKA and PKLR genes in a family with CIPA and pyruvate kinase deficiency. Hum. Mutat.18(4), 308–318 (2001).
  • Indo Y, Tsuruta M, Hayashida Y et al. Mutations in the TRKA/NGF receptor gene in patients with congenital insensitivity to pain with anhidrosis. Nat. Genet.13(4), 485–488 (1996).
  • Mardy S, Miura Y, Endo F, Matsuda I, Indo Y. Congenital insensitivity to pain with anhidrosis (CIPA): effect of TRKA (NTRK1) missense mutations on autophosphorylation of the receptor tyrosine kinase for nerve growth factor. Hum. Mol. Genet.10(3), 179–188 (2001).
  • Mardy S, Miura Y, Endo F et al. Congenital insensitivity to pain with anhidrosis: novel mutations in the TRKA (NTRK1) gene encoding a high-affinity receptor for nerve growth factor. Am. J. Hum. Genet.64(6), 1570–1579 (1999).
  • Miura Y, Mardy S, Awaya Y et al. Mutation and polymorphism analysis of the TRKA(NTRK1) gene encoding a high-affinity receptor for nerve growth factor in congenital insensitivity to pain with anhidrosis (CIPA) families. Hum. Genet.106(1), 116–124 (2000).
  • Kumazawa T. The polymodal receptor: bio-warning and defense system. In: Prog. Brain Res. (113). The Polymodal Receptor – a Gateway to Pathological Pain. Kumazawa T, Kruger L, Mizumura K (Eds.). Elsevier, Amsterdam, the Netherlands, 3–18 (1996).
  • Schmelz M, Schmidt R, Bickel A, Handwerker HO, Torebjork HE. Specific C-receptors for itch in human skin. J. Neurosci.17(20), 8003–8008 (1997).
  • Ikoma A, Handwerker H, Miyachi Y, Schmelz M. Electrically evoked itch in humans. Pain113(1–2), 148–154 (2005).
  • Johanek LM, Meyer RA, Hartke T et al. Psychophysical and physiological evidence for parallel afferent pathways mediating the sensation of itch. J. Neurosci.27(28), 7490–7497 (2007).
  • Mense S. Algesic agents exciting muscle nociceptors. Exp. Brain Res.196(1), 89–100 (2009).
  • Meyer RA, Ringkamp M, Campbell JN, Raja SN. Peripheral mechanisms of cutaneous nociception. In: Wall and Melzack’s Textbook of Pain. McMahon SB, Kolzenburg M (Eds). Elsevier, PA, USA, 3–34 (2006).
  • Izumi H. Nervous control of blood flow in the orofacial region. Pharmacol. Ther.81(2), 141–161 (1999).
  • Brogden KA, Guthmiller JM, Salzet M, Zasloff M. The nervous system and innate immunity: the neuropeptide connection. Nat. Immunol.6(6), 558–564 (2005).
  • Craig AD. Interoception and Emotion. In: Handbook of Emotions. Lewis M, Haviland-Jones JM, Barrett LF (Eds). The Guilford Press, New York, NY, USA, 272–288 (2008).
  • Damasio AR. Descartes’ Error: Emotion, Reason, and the Human Brain.Putnam, New York, NY, USA (1994).
  • Damasio AR. Looking for Spinoza.Harcourt, Orlando, FL, USA (2003).
  • Wiens S. Interoception in emotional experience. Curr. Opin. Neurol.18(4), 442–447 (2005).
  • Julius D, Basbaum AI. Molecular mechanisms of nociception. Nature413(6852), 203–210 (2001).
  • Holzer P. Neurogenic vasodilatation and plasma leakage in the skin. Gen. Pharmacol.30(1), 5–11 (1998).
  • Sauerstein K, Klede M, Hilliges M, Schmelz M. Electrically evoked neuropeptide release and neurogenic inflammation differ between rat and human skin. J. Physiol.529(Pt 3), 803–810 (2000).
  • Schmelz M, Zeck S, Raithel M, Rukwied R. Mast cell tryptase in dermal neurogenic inflammation. Clin. Exp. Allergy29(5), 695–702 (1999).
  • Weidner C, Klede M, Rukwied R et al. Acute effects of substance P and calcitonin gene-related peptide in human skin – a microdialysis study. J. Invest. Dermatol.115(6), 1015–1020 (2000).
  • Smeyne RJ, Klein R, Schnapp A et al. Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature368(6468), 246–249 (1994).
  • Fagan AM, Garber M, Barbacid M, Silos-Santiago I, Holtzman DM. A role for TrkA during maturation of striatal and basal forebrain cholinergic neurons in vivo.J. Neurosci.17(20), 7644–7654 (1997).
  • Elenkov IJ, Wilder RL, Chrousos GP, Vizi ES. The sympathetic nerve – an integrative interface between two supersystems: the brain and the immune system. Pharmacol. Rev.52(4), 595–638 (2000).
  • Paus R, Theoharides TC, Arck PC. Neuroimmunoendocrine circuitry of the ‘brain–skin connection’. Trends Immunol.27(1), 32–39 (2006).
  • Chrousos GP. The hypothalamic–pituitary–adrenal axis and immune-mediated inflammation. N. Engl. J. Med.332(20), 1351–1362 (1995).
  • Chrousos GP. Stressors, stress, and neuroendocrine integration of the adaptive response. The 1997 Hans Selye Memorial Lecture. Ann. NY Acad. Sci.851, 311–335 (1998).
  • Chrousos GP. Stress, chronic inflammation, and emotional and physical well-being: concurrent effects and chronic sequelae. J. Allergy Clin. Immunol.106(5 Suppl), S275–S291 (2000).
  • Elenkov IJ. Neurohormonal–cytokine interactions: implications for inflammation, common human diseases and well-being. Neurochem. Int.52(1–2), 40–51 (2008).
  • Sternberg EM. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat. Rev. Immunol.6(4), 318–328 (2006).
  • Tracey KJ. The inflammatory reflex. Nature420(6917), 853–859 (2002).
  • Zoumakis E, Kalantaridou SN, Chrousos GP. The “brain–skin connection”: nerve growth factor-dependent pathways for stress-induced skin disorders. J. Mol. Med.85(12), 1347–1349 (2007).
  • Mizumura K, Sugiura T, Katanosaka K, Banik RK, Kozaki Y. Excitation and sensitization of nociceptors by bradykinin: what do we know? Exp. Brain Res.196(1), 53–65 (2009).
  • Dallos A, Kiss M, Polyanka H, Dobozy A, Kemeny L, Husz S. Effects of the neuropeptides substance P, calcitonin gene-related peptide, vasoactive intestinal polypeptide and galanin on the production of nerve growth factor and inflammatory cytokines in cultured human keratinocytes. Neuropeptides40(4), 251–263 (2006).
  • Galli SJ, Tsai M, Piliponsky AM. The development of allergic inflammation. Nature454(7203), 445–454 (2008).
  • Nockher WA, Renz H. Neurotrophins in allergic diseases: from neuronal growth factors to intercellular signaling molecules. J. Allergy Clin. Immunol.117(3), 583–589 (2006).
  • Costigan M, Scholz J, Woolf CJ. Neuropathic pain: a maladaptive response of the nervous system to damage. Annu. Rev. Neurosci.32, 1–32 (2009).
  • Bielefeldt K, Lamb K, Gebhart GF. Convergence of sensory pathways in the development of somatic and visceral hypersensitivity. Am. J. Physiol. Gastrointest. Liver Physiol.291(4), G658–G665 (2006).
  • Winston JH, Xu GY, Sarna SK. Adrenergic stimulation mediates visceral hypersensitivity to colorectal distension following heterotypic chronic stress. Gastroenterology138(1), 294–304 e3 (2010).
  • Marchand F, Perretti M, McMahon SB. Role of the immune system in chronic pain. Nat. Rev. Neurosci.6(7), 521–532 (2005).
  • Devor M. Ectopic discharge in Abeta afferents as a source of neuropathic pain. Exp. Brain Res.196(1), 115–128 (2009).
  • Scadding JW, Koltzenburg M. Painful peripheral neuropathies. In: Wall and Melzack’s Textbook of Pain. McMahon SB, Kolzenburg M (Eds). Elsevier, PA, USA, 973–999 (2006).
  • Ogata M, Misago N, Suzuki Y et al. A case of herpes zoster in a child with congenital insensitivity to pain with anhidrosis. Br. J. Dermatol.156(5), 1084–1086 (2007).
  • Seal RP, Wang X, Guan Y et al. Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature462(7273), 651–655 (2009).
  • Schmelz M. How pain becomes itch. Pain144(1–2), 14–15 (2009).
  • Andrew D, Craig AD. Spinothalamic lamina I neurons selectively sensitive to histamine: a central neural pathway for itch. Nat. Neurosci.4(1), 72–77 (2001).
  • Schmelz M. A neural pathway for itch. Nat. Neurosci.4(1), 9–10 (2001).
  • Davidson S, Zhang X, Yoon CH, Khasabov SG, Simone DA, Giesler GJ Jr. The itch-producing agents histamine and cowhage activate separate populations of primate spinothalamic tract neurons. J. Neurosci.27(37), 10007–10014 (2007).
  • Simone DA, Zhang X, Li J et al. Comparison of responses of primate spinothalamic tract neurons to pruritic and algogenic stimuli. J. Neurophysiol.91(1), 213–222 (2004).
  • Imamachi N, Park GH, Lee H et al. TRPV1-expressing primary afferents generate behavioral responses to pruritogens via multiple mechanisms. Proc. Natl Acad. Sci. USA106(27), 11330–11335 (2009).
  • Sikand P, Shimada SG, Green BG, LaMotte RH. Similar itch and nociceptive sensations evoked by punctate cutaneous application of capsaicin, histamine and cowhage. Pain144(1–2), 66–75 (2009).
  • Sun YG, Chen ZF. A gastrin-releasing peptide receptor mediates the itch sensation in the spinal cord. Nature448(7154), 700–703 (2007).
  • Sun YG, Zhao ZQ, Meng XL, Yin J, Liu XY, Chen ZF. Cellular basis of itch sensation. Science325(5947), 1531–1534 (2009).
  • Kerr BJ, Bradbury EJ, Bennett DL et al. Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord. J. Neurosci.19(12), 5138–5148 (1999).
  • Lewin GR, Rueff A, Mendell LM. Peripheral and central mechanisms of NGF-induced hyperalgesia. Eur J. Neurosci.6(12), 1903–1912 (1994).
  • Thompson SW, Bennett DL, Kerr BJ, Bradbury EJ, McMahon SB. Brain-derived neurotrophic factor is an endogenous modulator of nociceptive responses in the spinal cord. Proc. Natl Acad. Sci. USA96(14), 7714–7718 (1999).
  • Joachim RA, Kuhlmei A, Dinh QT et al. Neuronal plasticity of the ‘brain-skin connection’: stress-triggered up-regulation of neuropeptides in dorsal root ganglia and skin via nerve growth factor-dependent pathways. J. Mol. Med.85(12), 1369–1378 (2007).
  • Hendrix S, Peters EM. Neuronal plasticity and neuroregeneration in the skin – the role of inflammation. J. Neuroimmunol.184(1–2), 113–126 (2007).
  • Allen SJ, Dawbarn D. Clinical relevance of the neurotrophins and their receptors. Clin. Sci. (Lond.)110(2), 175–191 (2006).
  • Guerios SD, Wang ZY, Boldon K, Bushman W, Bjorling DE. Blockade of NGF and trk receptors inhibits increased peripheral mechanical sensitivity accompanying cystitis in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol.295(1), R111–R122 (2008).
  • Hefti FF, Rosenthal A, Walicke PA et al. Novel class of pain drugs based on antagonism of NGF. Trends Pharmacol. Sci.27(2), 85–91 (2006).
  • McMahon SB, Bennett DLH, Bevan S. Inflammatory mediators and modulators of pain. In: Wall and Melzack’s Textbook of Pain. McMahon SB, Kolzenburg M (Eds). Elsevier, PA, USA, 49–72 (2006).
  • Obata K, Noguchi K. BDNF in sensory neurons and chronic pain. Neurosci. Res.55(1), 1–10 (2006).
  • Tominaga M, Tominaga T. Structure and function of TRPV1. Pflugers Arch.451(1), 143–150 (2005).
  • Diss JK, Calissano M, Gascoyne D, Djamgoz MB, Latchman DS. Identification and characterization of the promoter region of the Nav1.7 voltage-gated sodium channel gene (SCN9A).Mol. Cell Neurosci.37(3), 537–547 (2008).
  • Fjell J, Cummins TR, Dib-Hajj SD, Fried K, Black JA, Waxman SG. Differential role of GDNF and NGF in the maintenance of two TTX-resistant sodium channels in adult DRG neurons. Brain Res. Mol. Brain Res.67(2), 267–282 (1999).
  • Fjell J, Cummins TR, Fried K, Black JA, Waxman SG. In vivo NGF deprivation reduces SNS expression and TTX-R sodium currents in IB4-negative DRG neurons. J. Neurophysiol.81(2), 803–810 (1999).
  • Gould HJ 3rd, Gould TN, England JD, Paul D, Liu ZP, Levinson SR. A possible role for nerve growth factor in the augmentation of sodium channels in models of chronic pain. Brain Res.854(1–2), 19–29 (2000).
  • Jia Z, Bei J, Rodat-Despoix L et al. NGF inhibits M/KCNQ currents and selectively alters neuronal excitability in subsets of sympathetic neurons depending on their M/KCNQ current background. J. Gen. Physiol.131(6), 575–587 (2008).
  • Willis DE, van Niekerk EA, Sasaki Y et al. Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J. Cell Biol.178(6), 965–980 (2007).
  • Janig W, Levine JD. Autonomic-endocrine-immune interactions in acute and chronic pain. In: Wall and Melzack’s Textbook of Pain. McMahon SB, Kolzenburg M (Eds). Elsevier, PA, USA, 205–218 (2006).
  • Luther JA, Birren SJ. p75 and TrkA signaling regulates sympathetic neuronal firing patterns via differential modulation of voltage-gated currents. J. Neurosci.29(17), 5411–5424 (2009).
  • Bjerre B, Bjorklund A, Mobley W, Rosengren E. Short- and long-term effects of nerve growth factor on the sympathetic nervous system in the adult mouse. Brain Res.94(2), 263–277 (1975).
  • Glebova NO, Ginty DD. Heterogeneous requirement of NGF for sympathetic target innervation in vivo.J. Neurosci.24(3), 743–751 (2004).
  • Ford CP, Wong KV, Lu VB, Posse de Chaves E, Smith PA. Differential neurotrophic regulation of sodium and calcium channels in an adult sympathetic neuron. J. Neurophysiol.99(3), 1319–1332 (2008).
  • Lei S, Dryden WF, Smith PA. Nerve growth factor regulates sodium but not potassium channel currents in sympathetic B neurons of adult bullfrogs. J. Neurophysiol.86(2), 641–650 (2001).
  • Lei S, Dryden WF, Smith PA. Regulation of N- and L-type Ca2+ channels in adult frog sympathetic ganglion B cells by nerve growth factor in vitro and in vivo.J. Neurophysiol.78(6), 3359–3370 (1997).
  • Luther JA, Birren SJ. Nerve growth factor decreases potassium currents and alters repetitive firing in rat sympathetic neurons. J. Neurophysiol.96(2), 946–958 (2006).
  • Nockher WA, Renz H. Neurotrophins and asthma: novel insight into neuroimmune interaction. J. Allergy Clin. Immunol.117(1), 67–71 (2006).
  • Takei Y, Laskey R. Interpreting crosstalk between TNF-α and NGF: potential implications for disease. Trends Mol. Med.14(9), 381–388 (2008).
  • Freund-Michel V, Frossard N. The nerve growth factor and its receptors in airway inflammatory diseases. Pharmacol. Ther.117(1), 52–76 (2008).
  • Nassenstein C, Schulte-Herbruggen O, Renz H, Braun A. Nerve growth factor: the central hub in the development of allergic asthma? Eur. J. Pharmacol.533(1–3), 195–206 (2006).
  • Seidel MF, Herguijuela M, Forkert R, Otten U. Nerve growth factor in rheumatic diseases. Semin. Arthritis Rheum. DOI: S0049–0172(09)00035–3 [pii]10.1016/j.semarthrit.2009.03.002 (2009) (Epub ahead of print).
  • Boguniewicz M, Schmid-Grendelmeier P, Leung DY. Atopic dermatitis. J. Allergy Clin. Immunol.118(1), 40–43 (2006).
  • Botchkarev VA, Yaar M, Peters EM et al. Neurotrophins in skin biology and pathology. J. Invest. Dermatol.126(8), 1719–1727 (2006).
  • Takaoka K, Shirai Y, Saito N. Inflammatory cytokine tumor necrosis factor-α enhances nerve growth factor production in human keratinocytes, HaCaT cells. J. Pharmacol. Sci.111(4), 381–391 (2009).
  • Dou YC, Hagstromer L, Emtestam L, Johansson O. Increased nerve growth factor and its receptors in atopic dermatitis: an immunohistochemical study. Arch. Dermatol. Res.298(1), 31–37 (2006).
  • Shaker OG, El-Komy M, Tawfic SO, Zeidan N, Tomairek RH. Possible role of nerve growth factor and interleukin-18 in pathogenesis of eczematous lesions of atopic dermatitis. J. Dermatol. Sci.53(2), 153–154 (2009).
  • Tominaga M, Tengara S, Kamo A, Ogawa H, Takamori K. Psoralen-ultraviolet A therapy alters epidermal Sema3A and NGF levels and modulates epidermal innervation in atopic dermatitis. J. Dermatol. Sci.55(1), 40–46 (2009).
  • Yamaguchi J, Aihara M, Kobayashi Y, Kambara T, Ikezawa Z. Quantitative analysis of nerve growth factor (NGF) in the atopic dermatitis and psoriasis horny layer and effect of treatment on NGF in atopic dermatitis. J. Dermatol. Sci.53(1), 48–54 (2009).
  • Horiuchi Y, Bae S, Katayama I. Nerve growth factor (NGF) and epidermal nerve fibers in atopic dermatitis model NC/Nga mice. J. Dermatol. Sci.39(1), 56–58 (2005).
  • Tanaka A, Matsuda H. Expression of nerve growth factor in itchy skins of atopic NC/NgaTnd mice. J. Vet. Med. Sci.67(9), 915–919 (2005).
  • Tokime K, Katoh-Semba R, Yamanaka K, Mizoguchi A, Mizutani H. Enhanced production and secretion of glial cell line-derived neurotrophic factor and nerve growth factor from the skin in atopic dermatitis mouse model. Arch. Dermatol. Res.300(7), 343–352 (2008).
  • Tominaga M, Ozawa S, Ogawa H, Takamori K. A hypothetical mechanism of intraepidermal neurite formation in NC/Nga mice with atopic dermatitis. J. Dermatol. Sci.46(3), 199–210 (2007).
  • Tominaga M, Ozawa S, Tengara S, Ogawa H, Takamori K. Intraepidermal nerve fibers increase in dry skin of acetone-treated mice. J. Dermatol. Sci.48(2), 103–111 (2007).
  • Yamaoka J, Di ZH, Sun W, Kawana S. Erratum to “changes in cutaneous sensory nerve fibers induced by skin-scratching in mice”. J. Dermatol. Sci.47(2), 172–182 (2007).
  • Yoshioka T, Hikita I, Asakawa M et al. Spontaneous scratching behaviour in DS-Nh mice as a possible model for pruritus in atopic dermatitis. Immunology118(3), 293–301 (2006).
  • Sugiura H, Omoto M, Hirota Y, Danno K, Uehara M. Density and fine structure of peripheral nerves in various skin lesions of atopic dermatitis. Arch. Dermatol. Res.289(3), 125–131 (1997).
  • Urashima R, Mihara M. Cutaneous nerves in atopic dermatitis. A histological, immunohistochemical and electron microscopic study. Virchows Arch.432(4), 363–370 (1998).
  • Bresciani M, Laliberte F, Laliberte MF, Gramiccioni C, Bonini S. Nerve growth factor localization in the nasal mucosa of patients with persistent allergic rhinitis. Allergy64(1), 112–117 (2009).
  • Coffey CS, Mulligan RM, Schlosser RJ. Mucosal expression of nerve growth factor and brain-derived neurotrophic factor in chronic rhinosinusitis. Am. J. Rhinol. Allergy23(6), 571–574 (2009).
  • O’Hanlon S, Facer P, Simpson KD, Sandhu G, Saleh HA, Anand P. Neuronal markers in allergic rhinitis: expression and correlation with sensory testing. Laryngoscope117(9), 1519–1527 (2007).
  • Raap U, Braunstahl GJ. The role of neurotrophins in the pathophysiology of allergic rhinitis. Curr. Opin. Allergy Clin. Immunol.10(1), 8–13 (2010).
  • Raap U, Fokkens W, Bruder M, Hoogsteden H, Kapp A, Braunstahl GJ. Modulation of neurotrophin and neurotrophin receptor expression in nasal mucosa after nasal allergen provocation in allergic rhinitis. Allergy63(4), 468–475 (2008).
  • Sanico AM, Stanisz AM, Gleeson TD et al. Nerve growth factor expression and release in allergic inflammatory disease of the upper airways. Am. J. Respir. Crit. Care Med.161(5), 1631–1635 (2000).
  • Wu X, Myers AC, Goldstone AC, Togias A, Sanico AM. Localization of nerve growth factor and its receptors in the human nasal mucosa. J. Allergy Clin. Immunol.118(2), 428–433 (2006).
  • de Vries A, Engels F, Henricks PA et al. Airway hyper-responsiveness in allergic asthma in guinea-pigs is mediated by nerve growth factor via the induction of substance P: a potential role for trkA. Clin. Exp. Allergy36(9), 1192–1200 (2006).
  • El-Hashim AZ, Jaffal SM. Nerve growth factor enhances cough and airway obstruction via TrkA receptor- and TRPV1-dependent mechanisms. Thorax64(9), 791–797 (2009).
  • Nassenstein C, Dawbarn D, Pollock K et al. Pulmonary distribution, regulation, and functional role of Trk receptors in a murine model of asthma. J. Allergy Clin. Immunol.118(3), 597–605 (2006).
  • Quarcoo D, Schulte-Herbruggen O, Lommatzsch M et al. Nerve growth factor induces increased airway inflammation via a neuropeptide-dependent mechanism in a transgenic animal model of allergic airway inflammation. Clin. Exp. Allergy34(7), 1146–1151 (2004).
  • Bachar O, Adner M, Uddman R, Cardell LO. Nerve growth factor enhances cholinergic innervation and contractile response to electric field stimulation in a murine in vitro model of chronic asthma. Clin. Exp. Allergy34(7), 1137–1145 (2004).
  • Hazari MS, Pan JH, Myers AC. Nerve growth factor acutely potentiates synaptic transmission in vitro and induces dendritic growth in vivo on adult neurons in airway parasympathetic ganglia. Am. J. Physiol. Lung Cell. Mol. Physiol.292(4), L992–L1001 (2007).
  • Abram M, Wegmann M, Fokuhl V et al. Nerve growth factor and neurotrophin-3 mediate survival of pulmonary plasma cells during the allergic airway inflammation. J. Immunol.182(8), 4705–4712 (2009).
  • Hahn C, Islamian AP, Renz H, Nockher WA. Airway epithelial cells produce neurotrophins and promote the survival of eosinophils during allergic airway inflammation. J. Allergy Clin. Immunol.117(4), 787–794 (2006).
  • Verbout NG, Jacoby DB, Gleich GJ, Fryer AD. Atropine-enhanced, antigen challenge-induced airway hyperreactivity in guinea pigs is mediated by eosinophils and nerve growth factor. Am. J. Physiol. Lung Cell. Mol. Physiol.297(2), L228–L237 (2009).
  • Freund-Michel V, Frossard N. Overexpression of functional TrkA receptors after internalisation in human airway smooth muscle cells. Biochim. Biophys. Acta1783(10), 1964–1971 (2008).
  • Frossard N, Naline E, Olgart Hoglund C, Georges O, Advenier C. Nerve growth factor is released by IL-1b and induces hyperresponsiveness of the human isolated bronchus. Eur. Respir. J.26(1), 15–20 (2005).
  • Othumpangat S, Gibson LF, Samsell L, Piedimonte G. NGF is an essential survival factor for bronchial epithelial cells during respiratory syncytial virus infection. PLoS One4(7), e6444 (2009).
  • Tortorolo L, Langer A, Polidori G et al. Neurotrophin overexpression in lower airways of infants with respiratory syncytial virus infection. Am. J. Respir. Crit. Care Med.172(2), 233–237 (2005).
  • Piedimonte G. Contribution of neuroimmune mechanisms to airway inflammation and remodeling during and after respiratory syncytial virus infection. Pediatr. Infect. Dis. J.22(2 Suppl.), S66–S74; discussion S74–S65 (2003).
  • Schaible HG, Richter F, Ebersberger A et al. Joint pain. Exp. Brain Res.196(1), 153–162 (2009).
  • Scott DL. Osteoarthritis and rheumatoid arthritis. In: Wall and Melzack’s Textbook of Pain. McMahon SB, Kolzenburg M (Eds). Elsevier, PA, USA, 653–667 (2006).
  • Niissalo S, Hukkanen M, Imai S, Tornwall J, Konttinen YT. Neuropeptides in experimental and degenerative arthritis. Ann. NY Acad. Sci.966, 384–399 (2002).
  • Schaible HG, Ebersberger A, Von Banchet GS. Mechanisms of pain in arthritis. Ann. NY Acad. Sci.966, 343–354 (2002).
  • Abe Y, Akeda K, An HS et al. Proinflammatory cytokines stimulate the expression of nerve growth factor by human intervertebral disc cells. Spine (Phila. Pa 1976)32(6), 635–642 (2007).
  • Barthel C, Yeremenko N, Jacobs R et al. Nerve growth factor and receptor expression in rheumatoid arthritis and spondyloarthritis. Arthritis Res. Ther.11(3), R82 (2009).
  • Purmessur D, Freemont AJ, Hoyland JA. Expression and regulation of neurotrophins in the nondegenerate and degenerate human intervertebral disc. Arthritis Res. Ther.10(4), R99 (2008).
  • Raychaudhuri SK, Raychaudhuri SP. NGF and its receptor system: a new dimension in the pathogenesis of psoriasis and psoriatic arthritis. Ann. NY Acad. Sci.1173, 470–477 (2009).
  • Raychaudhuri SP, Raychaudhuri SK. The regulatory role of nerve growth factor and its receptor system in fibroblast-like synovial cells. Scand. J. Rheumatol.38(3), 207–215 (2009).
  • Shelton DL, Zeller J, Ho WH, Pons J, Rosenthal A. Nerve growth factor mediates hyperalgesia and cachexia in auto-immune arthritis. Pain116(1–2), 8–16 (2005).
  • Surace MF, Prestamburgo D, Campagnolo M, Fagetti A, Murena L. Presence of NGF and its receptor TrkA in degenerative lumbar facet joint specimens. Eur. Spine J.18(Suppl. 1), 122–125 (2009).
  • Rukwied R, Mayer A, Kluschina O, Obreja O, Schley M, Schmelz M. NGF induces non-inflammatory localized and lasting mechanical and thermal hypersensitivity in human skin. Pain148(3), 407–413 (2010).
  • Wang T, Yu D, Lamb ML. Trk kinase inhibitors as new treatments for cancer and pain. Expert Opin. Ther. Pat.19(3), 305–319 (2009).
  • Watson JJ, Allen SJ, Dawbarn D. Targeting nerve growth factor in pain: what is the therapeutic potential? BioDrugs22(6), 349–359 (2008).
  • Cattaneo A. Tanezumab, a recombinant humanized mAb against nerve growth factor for the treatment of acute and chronic pain. Curr. Opin. Mol. Ther.12(1), 94–106 (2010).
  • Eibl JK, Chapelsky SA, Ross GM. Multipotent neurotrophin antagonist targets brain-derived neurotrophic factor and nerve growth factor. J. Pharmacol. Exp. Ther.332(2), 446–454 (2010).
  • McNamee KE, Burleigh A, Gompels LL et al. Treatmentof murine osteoarthritis with TrkAd5 reveals a pivotal role for nerve growth factor in non-inflammatory joint pain. Pain149(2), 386–392 (2010).
  • Dawbarn D, Fahey M, Watson J et al. NGF receptor TrkAd5: therapeutic agent and drug design target. Biochem. Soc. Trans.34(Pt 4), 587–590 (2006).
  • Halvorson KG, Kubota K, Sevcik MA et al. A blocking antibody to nerve growth factor attenuates skeletal pain induced by prostate tumor cells growing in bone. Cancer Res.65(20), 9426–9435 (2005).
  • Jimenez-Andrade JM, Martin CD, Koewler NJ et al. Nerve growth factor sequestering therapy attenuates non-malignant skeletal pain following fracture. Pain133(1–3), 183–196 (2007).
  • McMahon SB. NGF as a mediator of inflammatory pain. Philos. Trans. R. Soc. Lond. B. Biol. Sci.351(1338), 431–440 (1996).
  • Obata K, Katsura H, Mizushima T et al. TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J. Clin. Invest.115(9), 2393–2401 (2005).
  • Sabsovich I, Wei T, Guo TZ et al. Effect of anti-NGF antibodies in a rat tibia fracture model of complex regional pain syndrome type I. Pain138(1), 47–60 (2008).
  • Sevcik MA, Ghilardi JR, Peters CM et al. Anti-NGF therapy profoundly reduces bone cancer pain and the accompanying increase in markers of peripheral and central sensitization. Pain115(1–2), 128–141 (2005).
  • Ugolini G, Marinelli S, Covaceuszach S, Cattaneo A, Pavone F. The function neutralizing anti-TrkA antibody MNAC13 reduces inflammatory and neuropathic pain. Proc. Natl Acad. Sci. USA104(8), 2985–2990 (2007).
  • Wild KD, Bian D, Zhu D et al. Antibodies to nerve growth factor reverse established tactile allodynia in rodent models of neuropathic pain without tolerance. J. Pharmacol. Exp. Ther.322(1), 282–287 (2007).
  • Johansson O, Liang Y, Emtestam L. Increased nerve growth factor- and tyrosine kinase A-like immunoreactivities in prurigo nodularis skin – an exploration of the cause of neurohyperplasia. Arch. Dermatol. Res.293(12), 614–619 (2002).
  • Toyoda M, Nakamura M, Makino T, Hino T, Kagoura M, Morohashi M. Nerve growth factor and substance P are useful plasma markers of disease activity in atopic dermatitis. Br. J. Dermatol.147(1), 71–79 (2002).
  • Stander S, Siepmann D, Herrgott I, Sunderkotter C, Luger TA. Targeting the neurokinin receptor 1 with aprepitant: a novel antipruritic strategy. PLoS One5(6), e10968 (2010).
  • Takano N, Sakurai T, Kurachi M. Effects of anti-nerve growth factor antibody on symptoms in the NC/Nga mouse, an atopic dermatitis model. J. Pharmacol. Sci.99(3), 277–286 (2005).
  • Takano N, Sakurai T, Ohashi Y, Kurachi M. Effects of high-affinity nerve growth factor receptor inhibitors on symptoms in the NC/Nga mouse atopic dermatitis model. Br. J. Dermatol.156(2), 241–246 (2007).
  • Williams B, Granholm AC, Sambamurti K. Age-dependent loss of NGF signaling in the rat basal forebrain is due to disrupted MAPK activation. Neurosci. Lett.413(2), 110–114 (2007).
  • Wu CW, Yeh HH. Nerve growth factor rapidly increases muscarinic tone in mouse medial septum/diagonal band of Broca. J. Neurosci.25(17), 4232–4242 (2005).
  • Mufson EJ, Counts SE, Perez SE, Ginsberg SD. Cholinergic system during the progression of Alzheimer’s disease: therapeutic implications. Expert Rev. Neurother.8(11), 1703–1718 (2008).
  • Ginsberg SD, Che S, Wuu J, Counts SE, Mufson EJ. Down regulation of Trk but not p75NTR gene expression in single cholinergic basal forebrain neurons mark the progression of Alzheimer’s disease. J. Neurochem.97(2), 475–487 (2006).
  • Tuszynski MH, Thal L, Pay M et al. A Phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nat. Med.11(5), 551–555 (2005).
  • Adcock JJ. TRPV1 receptors in sensitisation of cough and pain reflexes. Pulm. Pharmacol. Ther.22(2), 65–70 (2009).
  • Gavva NR, Treanor JJ, Garami A et al. Pharmacological blockade of the vanilloid receptor TRPV1 elicits marked hyperthermia in humans. Pain136(1–2), 202–210 (2008).
  • Zhang X, Huang J, McNaughton PA. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. Embo. J.24(24), 4211–4223 (2005).
  • Caterina MJ. Transient receptor potential ion channels as participants in thermosensation and thermoregulation. Am. J. Physiol. Regul. Integr. Comp. Physiol.292(1), R64–R76 (2007).
  • Talavera K, Nilius B, Voets T. Neuronal TRP channels: thermometers, pathfinders and life-savers. Trends Neurosci.31(6), 287–295 (2008).
  • Snider WD, McMahon SB. Tackling pain at the source: new ideas about nociceptors. Neuron20(4), 629–632 (1998).
  • Fang X, Djouhri L, McMullan S et al. Intense isolectin-B4 binding in rat dorsal root ganglion neurons distinguishes C-fiber nociceptors with broad action potentials and high Nav1.9 expression. J. Neurosci.26(27), 7281–7292 (2006).
  • Golden JP, Hoshi M, Nassar MA et al. RET signaling is required for survival and normal function of nonpeptidergic nociceptors. J. Neurosci.30(11), 3983–3994 (2010).
  • Luo W, Wickramasinghe SR, Savitt JM, Griffin JW, Dawson TM, Ginty DD. A hierarchical NGF signaling cascade controls Ret-dependent and Ret-independent events during development of nonpeptidergic DRG neurons. Neuron54(5), 739–754 (2007).
  • Nicol GD, Vasko MR. Unraveling the story of NGF-mediated sensitization of nociceptive sensory neurons: ON or OFF the Trks? Mol. Interv.7(1), 26–41 (2007).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.