Nerve growth factor selectively decreases activity-dependent conduction slowing in mechano-insensitive C-nociceptors

Pain

Volumn 152, Issue 9, 2011, Pages 2138-2146

  Obreja, Otilia ^a   Ringkamp, Matthias ^b   Turnquist, Brian ^c   Hirth, Michael ^a   Forsch, Elmar ^a   Rukwied, Roman ^a   Petersen, Marlen ^a   Schmelz, Martin ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c BETHEL UNIVERSITY   (United States)

Author keywords

Activity dependent slowing; Conduction velocity; Growth factors; Hyperalgesia; Mechano insensitive afferents; Pain; Pig

Indexed keywords

NERVE GROWTH FACTOR;

ACTIVITY DEPENDENT SLOWING; ANIMAL EXPERIMENT; ARTICLE; C FIBER; CONTROLLED STUDY; FEMALE; HYPERALGESIA; MALE; MECHANO INSENSITIVE AFFERENT; MECHANO SENSITIVE AFFERENT; NERVE CONDUCTION; NERVE STIMULATION; NOCICEPTIVE RECEPTOR; NONHUMAN; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; SAPHENOUS NERVE; SENSORY NERVE CONDUCTION; SWINE;

ANIMALS; FEMALE; HUMANS; HYPERALGESIA; INJECTIONS, INTRADERMAL; MALE; NERVE FIBERS, UNMYELINATED; NERVE GROWTH FACTOR; NEURAL CONDUCTION; NOCICEPTORS; SUS SCROFA;

EID: 80051781647     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2011.05.021     Document Type: Article

References (67)

1. P. Anand Neurotrophic factors and their receptors in human sensory neuropathies Prog Brain Res 146 2004 477 492 (Pubitemid 37541400)
2. N.Y. Andreev, N. Dimitrieva, M. Koltzenburg, and S.B. McMahon Peripheral administration of nerve growth factor in the adult rat produces a thermal hyperalgesia that requires the presence of sympathetic post-ganglionic neurones Pain 63 1995 109 115
3. R.D. Beise, E. Carstens, and L.U. Kohlloffel Psychophysical study of stinging pain evoked by brief freezing of superficial skin and ensuing short-lasting changes in sensations of cool and cold pain Pain 74 1998 275 286 (Pubitemid 28081614)
4. T. Bishop, F. Marchand, A.R. Young, G.R. Lewin, and S.B. McMahon Ultraviolet-B-induced mechanical hyperalgesia: a role for peripheral sensitisation Pain 150 2010 141 152
5. + channel III and SNS gene expression in spinal sensory neurons Neuroreport 8 1997 2331 2335 (Pubitemid 27319696)
6. M.K. Boettger, S. Till, M.X. Chen, U. Anand, W.R. Otto, C. Plumpton, D.J. Trezise, S.N. Tate, C. Bountra, K. Coward, R. Birch, and P. Anand Calcium-activated potassium channel SK1- and IK1-like immunoreactivity in injured human sensory neurones and its regulation by neurotrophic factors Brain 125 2002 252 263 (Pubitemid 34127428)
7. J.N. Campbell, and R.A. Meyer Sensitization of unmyelinated nociceptive afferents in monkey varies with skin type J Neurophysiol 49 1983 98 110 (Pubitemid 13152928)
8. M. Campero, J. Serra, H. Bostock, and J.L. Ochoa Partial reversal of conduction slowing during repetitive stimulation of single sympathetic efferents in human skin Acta Physiol Scand 182 2004 305 311 (Pubitemid 39468681)
9. J.R. Chan, T.A. Watkins, J.M. Cosgaya, C. Zhang, L. Chen, L.F. Reichardt, E.M. Shooter, and B.A. Barres NGF controls axonal receptivity to myelination by Schwann cells or oligodendrocytes Neuron 43 2004 183 191 (Pubitemid 38942959)
10. P. Chevrier, K. Vijayaragavan, and M. Chahine Differential modulation of Nav1.7 and Nav1.8 peripheral nerve sodium channels by the local anesthetic lidocaine Br J Pharmacol 142 2004 576 584 (Pubitemid 38869872)
11. T.R. Cummins, S.D. Dib-Hajj, and S.G. Waxman Electrophysiological properties of mutant Nav1.7 sodium channels in a painful inherited neuropathy J Neurosci 24 2004 8232 8236 (Pubitemid 39280802)
12. B.M. Davis, G.R. Lewin, L.M. Mendell, M.E. Jones, and K.M. Albers Altered expression of nerve growth factor in the skin of transgenic mice leads to changes in response to mechanical stimuli Neuroscience 56 1993 789 792 (Pubitemid 23308636)
13. R. De Col, K. Messlinger, and R.W. Carr Conduction velocity is regulated by sodium channel inactivation in unmyelinated axons innervating the rat cranial meninges J Physiol 586 2008 1089 1103 (Pubitemid 351267348)
14. S.D. Dib-Hajj, J.A. Black, T.R. Cummins, A.M. Kenney, J.D. Kocsis, and S.G. Waxman Rescue of alpha-SNS sodium channel expression in small dorsal root ganglion neurons after axotomy by nerve growth factor in vivo J Neurophysiol 79 1998 2668 2676 (Pubitemid 28261650)
15. S.D. Dib-Hajj, M. Estacion, B.W. Jarecki, L. Tyrrell, T.Z. Fischer, M. Lawden, T.R. Cummins, and S.G. Waxman Paroxysmal extreme pain disorder M1627K mutation in human Nav1.7 renders DRG neurons hyperexcitable Mol Pain 4 2008 37
16. E. Dicou, S. Perrot, C.J. Menkes, C. Masson, and V. Nerriere Nerve growth factor (NGF) autoantibodies and NGF in the synovial fluid: implications in spondylarthropathies Autoimmunity 24 1996 1 9 (Pubitemid 26379162)
17. J.K. Diss, M. Calissano, D. Gascoyne, M.B. Djamgoz, and D.S. Latchman Identification and characterization of the promoter region of the Nav1.7 voltage-gated sodium channel gene (SCN9A) Mol Cell Neurosci 37 2008 537 547
18. L. Djouhri, D. Dawbarn, A. Robertson, R. Newton, and S.N. Lawson Time course and nerve growth factor dependence of inflammation-induced alterations in electrophysiological membrane properties in nociceptive primary afferent neurons J Neurosci 21 2001 8722 8733 (Pubitemid 33054836)
19. M. Dusch, M. Schley, O. Obreja, E. Forsch, M. Schmelz, and R. Rukwied Comparison of electrically induced flare response patterns in human and pig skin Inflamm Res 58 2009 639 648
20. P.J. Dyck, S. Peroutka, C. Rask, E. Burton, M.K. Baker, K.A. Lehman, D.A. Gillen, J.L. Hokanson, and P.C. O'Brien Intradermal recombinant human nerve growth factor induces pressure allodynia and lowered heat-pain threshold in humans Neurology 48 1997 501 505 (Pubitemid 27087628)
21. M. Estacion, S.D. Dib-Hajj, P.J. Benke, R.H. te Morsche, E.M. Eastman, L.J. Macala, J.P. Drenth, and S.G. Waxman NaV1.7 gain-of-function mutations as a continuum: A1632E displays physiological changes associated with erythromelalgia and paroxysmal extreme pain disorder mutations and produces symptoms of both disorders J Neurosci 28 2008 11079 11088
22. X. Fang, L. Djouhri, S. McMullan, C. Berry, K. Okuse, S.G. Waxman, and S.N. Lawson TrkA is expressed in nociceptive neurons and influences electrophysiological properties via Nav1.8 expression in rapidly conducting nociceptors J Neurosci 25 2005 4868 4878 (Pubitemid 40664133)
23. J. Fjell, T.R. Cummins, S.D. Dib-Hajj, K. Fried, J.A. Black, and S.G. Waxman 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 1999 267 282 (Pubitemid 29193183)
24. J. Fjell, T.R. Cummins, K. Fried, J.A. Black, and S.G. Waxman In vivo NGF deprivation reduces SNS expression and TTX-R sodium currents in IB4-negative DRG neurons J Neurophysiol 81 1999 803 810 (Pubitemid 29264524)
25. M.D. Gee, B. Lynn, and B. Cotsell Activity-dependent slowing of conduction velocity provides a method for identifying different functional classes of C-fibre in the rat saphenous nerve Neuroscience 73 1996 667 675 (Pubitemid 26260930)
26. H.J. Gould III, J.D. England, R.D. Soignier, P. Nolan, L.D. Minor, Z.P. Liu, S.R. Levinson, and D. Paul Ibuprofen blocks changes in Na v 1.7 and 1.8 sodium channels associated with complete Freund's adjuvant-induced inflammation in rat J Pain 5 2004 270 280 (Pubitemid 38859681)
27. H.J. Gould III, T.N. Gould, J.D. England, D. Paul, Z.P. Liu, and S.R. Levinson A possible role for nerve growth factor in the augmentation of sodium channels in models of chronic pain Brain Res 854 2000 19 29 (Pubitemid 30067656)
28. C. Han, A.M. Rush, S.D. Dib-Hajj, S. Li, Z. Xu, Y. Wang, L. Tyrrell, X. Wang, Y. Yang, and S.G. Waxman Sporadic onset of erythermalgia: a gain-of-function mutation in Nav1.7 Ann Neurol 59 2006 553 558 (Pubitemid 43358077)
29. Z. Jia, J. Bei, L. Rodat-Despoix, B. Liu, Q. Jia, P. Delmas, and H. Zhang 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 2008 575 587 (Pubitemid 351749198)
30. M. Koltzenburg The changing sensitivity in the life of the nociceptor Pain 82 1999 S93 S102
31. M. Koltzenburg, D.L. Bennett, D.L. Shelton, and S.B. McMahon Neutralization of endogenous NGF prevents the sensitization of nociceptors supplying inflamed skin Eur J Neurosci 11 1999 1698 1704 (Pubitemid 29192245)
32. W. Koppert, V. Brueckl, C. Weidner, and M. Schmelz Mechanically induced axon reflex and hyperalgesia in human UV-B burn are reduced by systemic lidocaine Eur J Pain 8 2004 237 244 (Pubitemid 38596086)
33. N. Lane, T.J. Schnitzer, C.A. Birbara, M. Mokhtarani, D.L. Shelton, M.D. Smith, and M.T. Brown Tanezumab for the treatment of pain from osteoarthritis of the knee N Engl J Med 363 2010 1521 1531
34. G.R. Lewin, A.M. Ritter, and L.M. Mendell Nerve growth factor-induced hyperalgesia in the neonatal and adult rat J Neurosci 13 1993 2136 2148 (Pubitemid 23113422)
35. G.R. Lewin, A. Rueff, and L.M. Mendell Peripheral and central mechanisms of NGF-induced hyperalgesia Eur J Neurosci 6 1994 1903 1912
36. B. Lynn, K. Faulstroh, and F.K. Pierau The classification and properties of nociceptive afferent units from the skin of the anaesthetized pig Eur J Neurosci 7 1995 431 437
37. B. Lynn, S. Schutterle, and F.K. Pierau The vasodilator component of neurogenic inflammation is caused by a special subclass of heat-sensitive nociceptors in the skin of the pig J Physiol 494 1996 587 593 (Pubitemid 26318794)
38. R.A. Meyer, K.D. Davis, R.H. Cohen, R.D. Treede, and J.N. Campbell Mechanically insensitive afferents (MIAs) in cutaneous nerves of monkey Brain Res 561 1991 252 261
39. M.A. Nassar, L.C. Stirling, G. Forlani, M.D. Baker, E.A. Matthews, A.H. Dickenson, and J.N. Wood Nociceptor-specific gene deletion reveals a major role for Nav1.7 (PN1) in acute and inflammatory pain Proc Natl Acad Sci USA 101 2004 12706 12711 (Pubitemid 39122087)
40. G.D. Nicol, and M.R. Vasko Unraveling the story of NGF-mediated sensitization of nociceptive sensory neurons: ON or OFF the Trks? Mol Interv 7 2007 26 41 (Pubitemid 46364322)
41. K. Obata, H. Yamanaka, Y. Dai, T. Tachibana, T. Fukuoka, A. Tokunaga, H. Yoshikawa, and K. Noguchi Differential activation of extracellular signal-regulated protein kinase in primary afferent neurons regulates brain-derived neurotrophic factor expression after peripheral inflammation and nerve injury J Neurosci 23 2003 4117 4126 (Pubitemid 36958431)
42. O. Obreja, M. Ringkamp, B. Namer, E. Forsch, A. Klusch, R. Rukwied, M. Petersen, and M. Schmelz Patterns of activity-dependent conduction velocity changes differentiate classes of unmyelinated mechano-insensitive afferents including cold nociceptors, in pig and in human Pain 148 2010 59 69
43. S. Ochs Rate of fast axoplasmic transport in mammalian nerve fibres J Physiol 227 1972 627 645
44. K. Okuse, S.R. Chaplan, S.B. McMahon, Z.D. Luo, N.A. Calcutt, B.P. Scott, A.N. Akopian, and J.N. Wood Regulation of expression of the sensory neuron-specific sodium channel SNS in inflammatory and neuropathic pain Mol Cell Neurosci 10 1997 196 207 (Pubitemid 28144510)
45. K. Orstavik, B. Namer, R. Schmidt, M. Schmelz, M. Hilliges, C. Weidner, R.W. Carr, H. Handwerker, E. Jorum, and H.E. Torebjork Abnormal function of C-fibers in patients with diabetic neuropathy J Neurosci 26 2006 11287 11294 (Pubitemid 44772158)
46. B.G. Petty, D.R. Cornblath, B.T. Adornato, V. Chaudhry, C. Flexner, M. Wachsman, D. Sinicropi, L.E. Burton, and S.J. Peroutka The effect of systemically administered recombinant human nerve growth factor in healthy human subjects Ann Neurol 36 1994 244 246 (Pubitemid 24239246)
47. M. Ringkamp, L.M. Johanek, J. Borzan, T.V. Hartke, G. Wu, E.M. Pogatzki-Zahn, J.N. Campbell, B. Shim, R.J. Schepers, and R.A. Meyer Conduction properties distinguish unmyelinated sympathetic efferent fibers and unmyelinated primary afferent fibers in the monkey PLoS ONE 5 2010 e9076
48. R. Rukwied, A. Mayer, O. Kluschina, O. Obreja, M. Schley, and M. Schmelz NGF induces non-inflammatory localized and lasting mechanical and thermal hypersensitivity in human skin Pain 148 2010 407 413
49. R. Rukwied, M. Schley, E. Forsch, O. Obreja, M. Dusch, and M. Schmelz Nerve growth factor-evoked nociceptor sensitization in pig skin in vivo J Neurosci Res 88 2010 2066 2072
50. I. Sabsovich, T. Wei, T.Z. Guo, R. Zhao, X. Shi, X. Li, D.C. Yeomans, M. Klyukinov, W.S. Kingery, and J.D. Clark Effect of anti-NGF antibodies in a rat tibia fracture model of complex regional pain syndrome type I Pain 138 2008 47 60
51. P. Sarchielli, M.L. Mancini, A. Floridi, F. Coppola, C. Rossi, K. Nardi, M. Acciarresi, L.A. Pini, and P. Calabresi Increased levels of neurotrophins are not specific for chronic migraine: evidence from primary fibromyalgia syndrome J Pain 8 2007 737 745 (Pubitemid 47362835)
52. M. Schmelz, C. Forster, R. Schmidt, M. Ringkamp, H.O. Handwerker, and H.E. Torebjörk Delayed responses to electrical stimuli reflect C-fiber responsiveness in human microneurography Exp Brain Res 104 1995 331 336
53. M. Schmelz, K. Michael, C. Weidner, R. Schmidt, H.E. Torebjörk, and H.O. Handwerker Which nerve fibers mediate the axon reflex flare in human skin? Neuroreport 11 2000 645 648 (Pubitemid 30120491)
54. M. Schmelz, R. Schmidt, H.O. Handwerker, and H.E. Torebjörk Encoding of burning pain from capsaicin-treated human skin in two categories of unmyelinated nerve fibres Brain 123 2000 560 571 (Pubitemid 30099540)
55. J. Serra, M. Campero, J. Ochoa, and H. Bostock Activity-dependent slowing of conduction differentiates functional subtypes of C fibres innervating human skin J Physiol 515 1999 799 811 (Pubitemid 29140114)
56. B. Shim, M. Ringkamp, G.L. Lambrinos, T.V. Hartke, J.W. Griffin, and R.A. Meyer Activity-dependent slowing of conduction velocity in uninjured L4 C fibers increases after an L5 spinal nerve injury in the rat Pain 128 2007 40 51 (Pubitemid 46216596)
57. S. Stamboulian, J.S. Choi, H.S. Ahn, Y.W. Chang, L. Tyrrell, J.A. Black, S.G. Waxman, and S.D. Dib-Hajj ERK1/2 mitogen-activated protein kinase phosphorylates sodium channel Na(v)1.7 and alters its gating properties J Neurosci 30 2010 1637 1647
58. A.T. Stein, C.A. Ufret-Vincenty, L. Hua, L.F. Santana, and S.E. Gordon Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane J Gen Physiol 128 2006 509 522 (Pubitemid 44664629)
59. K. Stoeckel, M. Schwab, and H. Thoenen Specificity of retrograde transport of nerve growth factor (NGF) in sensory neurons: a biochemical and morphological study Brain Res 89 1975 1 14
60. C.L. Stucky, M. Koltzenburg, M. Schneider, M.G. Engle, K.M. Albers, and B.M. Davis Overexpression of nerve growth factor in skin selectively affects the survival and functional properties of nociceptors J Neurosci 19 1999 8509 8516 (Pubitemid 30226769)
61. T. Taguchi, H. Ota, T. Matsuda, S. Murase, and K. Mizumura Cutaneous C-fiber nociceptor responses and nociceptive behaviors in aged Sprague-Dawley rats Pain 151 2010 771 782
62. J.G. Thalhammer, S.A. Raymond, F.A. Popitz-Bergez, and G.R. Strichartz Modality-dependent modulation of conduction by impulse activity in functionally characterized single cutaneous afferents in the rat Somatosens Mot Res 11 1994 243 257
63. H.E. Torebjörk, and R.G. Hallin Responses in human A and C fibres to repeated electrical intradermal stimulation J Neurol Neurosurg Psychiatry 37 1974 653 664
64. B. Turnquist, M. Leverentz, and E. Swanson Neural spike classification using parallel selection of all algorithm parameters J Neurosci Methods 137 2004 291 298 (Pubitemid 38942893)
65. C. Weidner, M. Schmelz, R. Schmidt, B. Hansson, H.O. Handwerker, and H.E. Torebjork Functional attributes discriminating mechano-insensitive and mechano-responsive C nociceptors in human skin J Neurosci 19 1999 10184 10190 (Pubitemid 30226690)
66. D.E. Willis, E.A. van Niekerk, Y. Sasaki, M. Mesngon, T.T. Merianda, G.G. Williams, M. Kendall, D.S. Smith, G.J. Bassell, and J.L. Twiss Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs J Cell Biol 178 2007 965 980 (Pubitemid 47443320)
67. M. Zimmermann Ethical guidelines for investigations of experimental pain in conscious animals Pain 16 1983 109 110 (Pubitemid 13058546)