NGF enhances electrically induced pain, but not axon reflex sweating

Pain

Volumn 152, Issue 8, 2011, Pages 1856-1863

  Obreja, Otilia ^a   Kluschina, Olga ^a   Mayer, Alexandra ^a   Hirth, Michael ^a   Schley, Marcus ^a   Schmelz, Martin ^a   Rukwied, Roman ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Activity dependent slowing; Axonal excitability; Nociceptors; QSART; Sudomotor; Sweat

Indexed keywords

NERVE GROWTH FACTOR; RECOMBINANT NERVE GROWTH FACTOR; SODIUM CHANNEL;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EFFERENT NERVE; ELECTROSTIMULATION; FEMALE; HUMAN; HUMAN EXPERIMENT; HYPERALGESIA; MALE; NERVE EXCITABILITY; NERVE FIBER; NOCICEPTION; NOCICEPTIVE RECEPTOR; NONHUMAN; NORMAL HUMAN; PAIN ASSESSMENT; PAIN THRESHOLD; PRIORITY JOURNAL; RECEPTOR AFFINITY; RECEPTOR SENSITIVITY; REFLEX; SENSORY NERVE; SWEATING; SYMPATHETIC INNERVATION;

ADRENERGIC FIBERS; ADULT; ANALYSIS OF VARIANCE; ANIMALS; BIOPHYSICS; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; FEMALE; FOREARM; HUMANS; MALE; MIDDLE AGED; NERVE GROWTH FACTOR; PAIN; PAIN THRESHOLD; REFLEX; SWEATING; SWINE;

EID: 79960448012     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2011.04.002     Document Type: Article

References (54)

1. A.N. Akopian, L. Sivilotti, and J.N. Wood A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons Nature 379 1996 257 262
2. B. Bjerre, A. Bjorklund, W. Mobley, and E. Rosengren Short- and long-term effects of nerve growth factor on the sympathetic nervous system in the adult mouse Brain Res 94 1975 263 277
3. + channel III and SNS gene expression in spinal sensory neurons Neuroreport 8 1997 2331 2335 (Pubitemid 27319696)
4. C. Brodski, A. Schaubmar, and G. Dechant Opposing functions of GDNF and NGF in the development of cholinergic and noradrenergic sympathetic neurons Mol Cell Neurosci 19 2002 528 538 (Pubitemid 34499532)
5. 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)
6. 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)
7. B.M. Davis, B.T. Fundin, K.M. Albers, T.P. Goodness, K.M. Cronk, and F.L. Rice Overexpression of nerve growth factor in skin causes preferential increases among innervation to specific sensory targets J Comp Neurol 387 1997 489 506 (Pubitemid 27467434)
8. B.M. Davis, T.P. Goodness, A. Soria, and K.M. Albers Over-expression of NGF in skin causes formation of novel sympathetic projections to trkA-positive sensory neurons Neuroreport 9 1998 1103 1107 (Pubitemid 28266631)
9. 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)
10. A. Diogenes, A.N. Akopian, and K.M. Hargreaves NGF Up-regulates TRPA1: implications for orofacial pain J Dent Res 86 2007 550 555
11. H.A. Drummond, M.M. Furtado, S. Myers, S. Grifoni, K.A. Parker, A. Hoover, and D.E. Stec ENaC proteins are required for NGF-induced neurite growth Am J Physiol Cell Physiol 290 2006 C404 C410
12. M. Dusch, M. Schley, R. Rukwied, and M. Schmelz Rapid flare development evoked by current frequency-dependent stimulation analyzed by full-field laser perfusion imaging Neuroreport 18 2007 1101 1105 (Pubitemid 46988060)
13. 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)
14. 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)
15. C.P. Ford, K.V. Wong, V.B. Lu, C.E. Posse de, and P.A. Smith Differential neurotrophic regulation of sodium and calcium channels in an adult sympathetic neuron J Neurophysiol 99 2008 1319 1332 (Pubitemid 351413713)
16. T. Fukuoka, K. Kobayashi, H. Yamanaka, K. Obata, Y. Dai, and K. Noguchi Comparative study of the distribution of the alpha-subunits of voltage-gated sodium channels in normal and axotomized rat dorsal root ganglion neurons J Comp Neurol 510 2008 188 206
17. N.O. Glebova, and D.D. Ginty Heterogeneous requirement of NGF for sympathetic target innervation in vivo J Neurosci 24 2004 743 751 (Pubitemid 38166500)
18. 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)
19. G. Guidry, S.C. Landis, B.M. Davis, and K.M. Albers Overexpression of nerve growth factor in epidermis disrupts the distribution and properties of sympathetic innervation in footpads J Comp Neurol 393 1998 231 243 (Pubitemid 28141647)
20. R.I. Herzog, T.R. Cummins, F. Ghassemi, S.D. Dib-Hajj, and S.G. Waxman Distinct repriming and closed-state inactivation kinetics of Nav1.6 and Nav1.7 sodium channels in mouse spinal sensory neurons J Physiol 551 2003 741 750 (Pubitemid 37221069)
21. R.R. Ji, T.A. Samad, S.X. Jin, R. Schmoll, and C.J. Woolf p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia Neuron 36 2002 57 68
22. K. Kobayashi, T. Fukuoka, K. Obata, H. Yamanaka, Y. Dai, A. Tokunaga, and K. Noguchi Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors J Comp Neurol 493 2005 596 606 (Pubitemid 41780630)
23. + channels J Pharmacol Exp Ther 320 2007 354 364 (Pubitemid 46025750)
24. 2+ channels in adult frog sympathetic ganglion B cells by nerve growth factor in vitro and in vivo J Neurophysiol 78 1997 3359 3370 (Pubitemid 28098839)
25. S. Lei, W.F. Dryden, and P.A. Smith Nerve growth factor regulates sodium but not potassium channel currents in sympathetic B neurons of adult bullfrogs J Neurophysiol 86 2001 641 650 (Pubitemid 32738556)
26. P.A. Low, P.E. Caskey, R.R. Tuck, R.D. Fealey, and P.J. Dyck Quantitative sudomotor axon reflex test in normal and neuropathic subjects Ann Neurol 14 1983 573 580 (Pubitemid 14239727)
27. J.A. Luther, and S.J. Birren Nerve growth factor decreases potassium currents and alters repetitive firing in rat sympathetic neurons J Neurophysiol 96 2006 946 958 (Pubitemid 44155230)
28. J.A. Luther, and S.J. Birren p75 and TrkA signaling regulates sympathetic neuronal firing patterns via differential modulation of voltage-gated currents J Neurosci 29 2009 5411 5424
29. 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
30. J. Mamet, M. Lazdunski, and N. Voilley How nerve growth factor drives physiological and inflammatory expressions of acid-sensing ion channel 3 in sensory neurons J Biol Chem 278 2003 48907 48913
31. S.B. McMahon, M.P. Armanini, L.H. Ling, and H.S. Phillips Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets Neuron 12 1994 1161 1171 (Pubitemid 24178207)
32. G.J. Michael, S. Averill, A. Nitkunan, M. Rattray, D.L. Bennett, Q. Yan, and J.V. Priestley Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord J Neurosci 17 1997 8476 8490 (Pubitemid 27461069)
33. F.D. Miller, A. Speelman, T.C. Mathew, J. Fabian, E. Chang, C. Pozniak, and J.G. Toma Nerve growth factor derived from terminals selectively increases the ratio of p75 to trkA NGF receptors on mature sympathetic neurons Dev Biol 161 1994 206 217 (Pubitemid 24049168)
34. B. Namer, A. Bickel, H. Kramer, F. Birklein, and M. Schmelz Chemically and electrically induced sweating and flare reaction Auton Neurosci 114 2004 72 82 (Pubitemid 39149834)
35. O. Obreja, M. Ringkamp, B. Namer, E. Forsch, A. Klusch, R. Rukwied, M. Petersen, and M. Schmelz Patterns of axonal excitability changes differentiate classes of unmyelinated mechano-insensitive afferents including cold nociceptors, in pig and in human Pain 148 2010 59 69
36. 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)
37. S. Pezet, and S.B. McMahon Neurotrophins: mediators and modulators of pain Annu Rev Neurosci 29 2006 507 538 (Pubitemid 44476854)
38. F.L. Rice, K.M. Albers, B.M. Davis, I. Silos-Santiago, G.A. Wilkinson, A.M. LeMaster, P. Ernfors, R.J. Smeyne, H. Aldskogius, H.S. Phillips, M. Barbacid, T.M. DeChiara, G.D. Yancopoulos, C.E. Dunne, and B.T. Fundin Differential dependency of unmyelinated and A delta epidermal and upper dermal innervation on neurotrophins, trk receptors, and p75LNGFR Dev Biol 198 1998 57 81 (Pubitemid 28272702)
39. 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
40. A.M. Rush, S.D. Dib-Hajj, S. Liu, T.R. Cummins, J.A. Black, and S.G. Waxman A single sodium channel mutation produces hyper- or hypoexcitability in different types of neurons Proc Natl Acad Sci USA 103 2006 8245 8250 (Pubitemid 43801083)
41. 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)
42. P. Sommer, O. Kluschina, M. Schley, B. Namer, M. Schmelz, and R. Rukwied Electrically induced quantitative sudomotor axon reflex test in human volunteers Auton Neurosci 159 2011 111 116
43. 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 Nav1.7 and alters its gating properties J Neurosci 30 2010 1637 1647
44. 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
45. J.J. Toledo-Aral, B.L. Moss, Z.J. He, A.G. Koszowski, T. Whisenand, S.R. Levinson, J.J. Wolf, I. Silos-Santiago, S. Halegoua, and G. Mandel Identification of PN1, a predominant voltage-dependent sodium channel expressed principally in peripheral neurons Proc Natl Acad Sci USA 94 1997 1527 1532 (Pubitemid 27087885)
46. H.E. Torebjork, and R.G. Hallin Responses in human A and C fibres to repeated electrical intradermal stimulation J Neurol Neurosurg Psychiatry 37 1974 653 664
47. 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)
48. J.A. Vega, E. Vazquez, F.J. Naves, M.E. Del Valle, B. Calzada, and J.J. Represa Immunohistochemical localization of the high-affinity NGF receptor (gp140-trkA) in the adult human dorsal root and sympathetic ganglia and in the nerves and sensory corpuscles supplying digital skin Anat Rec 240 1994 579 588 (Pubitemid 24350492)
49. C. Weidner, M. Schmelz, R. Schmidt, B. Hammarberg, K. Orstavik, M. Hilliges, H.E. Torebjörk, and H.O. Handwerker Neural signal processing: the underestimated contribution of peripheral human C-fibers J Neurosci 22 2002 6704 6712 (Pubitemid 35386426)
50. 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)
51. J. Winston, H. Toma, M. Shenoy, and P.J. Pasricha Nerve growth factor regulates VR-1 mRNA levels in cultures of adult dorsal root ganglion neurons Pain 89 2001 181 186 (Pubitemid 32146397)
52. Y.H. Zhang, and G.D. Nicol NGF-mediated sensitization of the excitability of rat sensory neurons is prevented by a blocking antibody to the p75 neurotrophin receptor Neurosci Lett 366 2004 187 192 (Pubitemid 38970153)
53. W. Zhu, and G.S. Oxford Phosphoinositide-3-kinase and mitogen activated protein kinase signaling pathways mediate acute NGF sensitization of TRPV1 Mol Cell Neurosci 34 2007 689 700 (Pubitemid 46486710)
54. Z.R. Zhu, X.W. Tang, W.T. Wang, W. Ren, J.L. Xing, J.R. Zhang, J.H. Duan, Y.Y. Wang, X. Jiao, and S.J. Hu Conduction failures in rabbit saphenous nerve unmyelinated fibers Neurosignals 17 2009 181 195