Role of nerve growth factor in pain

Handbook of Experimental Pharmacology

Volumn 227, Issue , 2015, Pages 57-77

  Mizumura, Kazue ^a   Murase, Shiori ^a  

^a CHUBU UNIVERSITY   (Japan)

Author keywords

Cancer pain; Delayed onset muscle soreness; Heat hyperalgesia; Mechanical hyperalgesia; Neuropathic pain; Noninflammatory pain

Indexed keywords

BRADYKININ; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NERVE GROWTH FACTOR; PROTEIN TYROSINE KINASE A; TANEZUMAB; VANILLOID RECEPTOR 1;

ADULT; ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER PAIN; CONTROLLED STUDY; GASTROCNEMIUS MUSCLE; HUMAN; HYPERALGESIA; INJECTION SITE; MASSETER MUSCLE; MECHANICAL STIMULATION; MOUSE; MUSCULOSKELETAL PAIN; MYALGIA; NERVE INJURY; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PAIN RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SPINAL CORD; SYMPATHECTOMY; SYMPATHETIC NERVE; TEMPORAL SUMMATION; TIBIALIS ANTERIOR MUSCLE; UPREGULATION; ANIMAL; METABOLISM; OSTEOARTHRITIS; PAIN; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; HUMANS; NERVE GROWTH FACTOR; OSTEOARTHRITIS; PAIN; PHOSPHORYLATION; RECEPTOR, TRKA;

EID: 84927604240     PISSN: 01712004     EISSN: 18650325     Source Type: Book Series    
DOI: 10.1007/978-3-662-46450-2_4     Document Type: Article

References (110)

1. Aloe L, Tuveri MA, Carcassi U, Levi-Montalcini R (1992) Nerve growth factor in the synovial fluid of patients with chronic arthritis. Arthritis Rheum 35:351-355
2. Amann R, Schuligoi R, Herzog G, Donnerer J (1996) Intraplantar injection of nerve growth factor into the rat hind paw: local edema and effects on thermal nociceptive threshold. Pain64:323-329
3. Andersen H, Arendt-Nielsen L, Danneskiold-Samsoe B, Graven-Nielsen T (2006) Pressure pain sensitivity and hardness along human normal and sensitized muscle. Somatosens Mot Res23:97-109
4. Andersen H, Arendt-Nielsen L, Svensson P, Danneskiold-Samsoe B, Graven-Nielsen T (2008) Spatial and temporal aspects of muscle hyperalgesia induced by nerve growth factor in humans. Exp Brain Res 191:371-382
5. Andreev NY, Dimitrieva N, Koltzenburg M, Mcmahon SB (1995) Peripheral administration of nerve growth factor in the adult rat produces a thermal hyperalgesia that requires the presence of sympathetic post-ganglionic neurones. Pain 63:109-115
6. Armstrong RB (1984) Mechanisms of exercise-induced delayed onset muscular soreness: a brief review. Med Sci Sports Exerc 16:529-538
7. Bennett DLH, Koltzenburg M, Priestley JV, Shelton DL, Mcmahon SB (1998) Endogenous nerve growth factor regulates the sensitivity of nociceptors in the adult rat. Eur J Neurosci10:1282-1291
8. Bergmann I, Reiter R, Toyka KV, Koltzenburg M (1998) Nerve growth factor evokes hyperalgesia in mice lacking the low-affinity neurotrophin receptor p75. Neurosci Lett 255:87-90.
9. Berry A, Bindocci E, Alleva E (2012) NGF, brain and behavioral plasticity. Neural Plast2012:784040
10. Bhave G, Hu HJ, Glauner KS, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW (2003) Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci USA 100:12480-12485.
11. Bhide AA, Cartwright R, Khullar V, Digesu GA (2013) Biomarkers in overactive bladder. Int Urogynecol J 24:1065-1072
12. Bielefeldt K, Ozaki N, Gebhart GF (2003) Role of nerve growth factor in modulation of gastric afferent neurons in the rat. Am J Physiol Gastrointest Liver Physiol 284:G499-G507.
13. Bloom AP, Jimenez-Andrade JM, Taylor RN, Castaneda-Corral G, Kaczmarska MJ, Freeman KT, Coughlin KA, Ghilardi JR, Kuskowski MA, Mantyh PW (2011) Breast cancer-induced bone remodeling, skeletal pain, and sprouting of sensory nerve fibers. J Pain 12:698-711.
14. Boix F, Rosenborg L, Hilgenfeldt U, Knardahl S (2002) Contraction-related factors affect the concentration of a kallidin-like peptide in rat muscle tissue. J Physiol 544:127-136.
15. Bonnington JK, McNaughton PA (2003) Signalling pathways involved in the sensitisation of mouse nociceptive neurones by nerve growth factor. J Physiol 551:433-446.
16. 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 389:816-824.
17. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Kolzenburg M,Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-313
18. Chen TC, Nosaka K, Sacco P (2007) Intensity of eccentric exercise, shift of optimum angle, and the magnitude of repeated-bout effect. J Appl Physiol 102:992-999.
19. Cheung K, Hume P, Maxwell L (2003) Delayed onset muscle soreness: treatment strategies and performance factors. Sports Med 33:145-164
20. Chuang H-H, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV, Julius D (2001) Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411:957-962
21. Crameri RM, Aagaard P, Qvortrup K, Langberg H, Olesen J, Kjaer M (2007) Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J Physiol583:365-380
22. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pittsmeek S, Armanini MP, Ling LH, Mcmahon SB, Shelton DL, Levinson AD, Phillips HS (1994) Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76:1001-1011
23. 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 405:183-187
24. De Col R, Messlinger K, Carr RW (2008) Conduction velocity is regulated by sodium channel inactivation in unmyelinated axons innervating the rat cranial meninges. J Physiol586:1089-1103
25. Deising S, Weinkauf B, Blunk J, Obreja O, Schmelz M, Rukwied R (2012) NGF-evoked sensitization of muscle fascia nociceptors in humans. Pain 153:1673-1679.
26. Di Castro A, Drew LJ, Wood JN, Cesare P (2006) Modulation of sensory neuron mechanotransduction by PKC- and nerve growth factor-dependent pathways. Proc Natl Acad Sci U S A 103:4699-4704.
27. di Mola FF, Friess H, Zhu ZW, Koliopanos A, Bley T, Di Sebastiano P, Innocenti P, Zimmermann A, Buchler MW (2000) Nerve growth factor and Trk high affinity receptor (TrkA) gene expression in inflammatory bowel disease. Gut 46:670-679.
28. Djouhri L, Dawbarn D, Robertson A, Newton R, Lawson SN (2001) Time course and nerve growth factor dependence of inflammation-induced alterations in electrophysiological membrane properties in nociceptive primary afferent neurons. J Neurosci 21:8722-8733.
29. Donnerer J, Schuligoi R, Stein C (1992) Increased content and transport of substance P and calcitonin gene-related peptide in sensory nerves innervating inflamed tissue: evidence for a regulatory function of nerve growth factor in vivo. Neuroscience 49:693-698.
30. Donnerer J, Schuligoi R, Stein C, Amann R (1993) Upregulation, release and axonal transport of substance-P and calcitonin gene-related peptide in adjuvant inflammation and regulatory function of nerve growth factor. Regul Pept 46:150-154.
31. Donnerer J, Liebmann I, Schicho R (2005) Differential regulation of 3-beta-hydroxysteroid dehydrogenase and vanilloid receptor TRPV1 mRNA in sensory neurons by capsaicin and NGF. Pharmacology 73:97-101
32. Dyck PJ, Peroutka S, Rask C, Burton E, Baker MK, Lehman KA, Gillen DA, Hokanson JL, O’Brien PC (1997) Intradermal recombinant human nerve growth factor induces pressure allodynia and lowered heat-pain threshold in humans. Neurology 48:501-505.
33. Eibl JK, Strasser BC, Ross GM (2012) Structural, biological, and pharmacological strategies for the inhibition of nerve growth factor. Neurochem Int 61:1266-1275.
34. Einarsdottir E, Carlsson A, Minde J, Toolanen G, Svensson O, Solders G, Holmgren G, Holmberg D, Holmberg M (2004) A mutation in the nerve growth factor beta gene (NGFB) causes loss of pain perception. Hum Mol Genet 13:799-805.
35. Fjell J, Cummins TR, Dib-Hajj SD, Fried K, Black JA, Waxman SG (1999) Differential role of GDNF and NGF in the maintenance of two TTX-resistant sodium channels in adult DRG neurons. Mol Brain Res 67:267-282
36. Freemont AJ, Watkins A, Le MC, Baird P, Jeziorska M, Knight MT, Ross ER, O’Brien JP, Hoyland JA (2002) Nerve growth factor expression and innervation of the painful intervertebral disc. J Pathol 197:286-292
37. Fujii Y, Ozaki N, Taguchi T, Mizumura K, Sugiura Y (2008) TRP channels and ASICs mediate mechanical hyperalgesia in models of inflammatory muscle pain and delayed onset muscle soreness. Pain 140:292-304
38. Fukuoka T, Kondo E, Dai Y, Hashimoto N, Noguchi K (2001) Brain-derived neurotrophic factor increases in the uninjured dorsal root ganglion neurons in selective spinal nerve ligation model. J Neurosci 21:4891-4900
39. Ghilardi JR, Freeman KT, Jimenez-Andrade JM, Mantyh WG, Bloom AP, Bouhana KS, Trollinger D, Winkler J, Lee P, Andrews SW, Kuskowski MA, Mantyh PW (2011) Sustained blockade of neurotrophin receptors TrkA, TrkB and TrkC reduces non-malignant skeletal pain but not the maintenance of sensory and sympathetic nerve fibers. Bone 48:389-398.
40. Giovengo SL, Russell IJ, Larson AA (1999) Increased concentrations of nerve growth factor in cerebrospinal fluid of patients with fibromyalgia. J Rheumatol 26:1564-1569.
41. Guo TZ, Offley SC, Boyd EA, Jacobs CR, Kingery WS (2004) Substance P signaling contributes to the vascular and nociceptive abnormalities observed in a tibial fracture rat model of complex regional pain syndrome type I. Pain 108:95-107
42. Halliday DA, Zettler C, Rush RA, Scicchitano R, McNeil JD (1998) Elevated nerve growth factor levels in the synovial fluid of patients with inflammatory joint disease. Neurochem Res23:919-922
43. Halvorson KG, Kubota K, Sevcik MA, Lindsay TH, Sotillo JE, Ghilardi JR, Rosol TJ, Boustany L, Shelton DL, Mantyh PW (2005) A blocking antibody to nerve growth factor attenuates skeletal pain induced by prostate tumor cells growing in bone. Cancer Res 65:9426-9435.
44. Hayashi K, Shiozawa S, Ozaki N, Mizumura K, Graven-Nielsen T (2013) Repeated intramuscular injections of nerve growth factor induced progressive muscle hyperalgesia, facilitated temporal summation and expanded pain areas. Pain 154:2344-2352
45. Hirth M, Rukwied R, Gromann A, Tumquist B, Weinkauf B, Francke K, Albrecht P, Rice F, Hagglof B, Ringkamp M, Engelhardt M, Schultz C, Schmelz M, Obreja O (2013) Nerve growth factor induces sensitization of nociceptors without evidence for increased intraepidermal nerve fiber density. Pain 154:2500-2511.
46. Hoheisel U, Unger T, Mense S (2005) Excitatory and modulatory effects of inflammatory cytokines and neurotrophins on mechanosensitive group IV muscle afferents in the rat. Pain114:168-176
47. Hoheisel U, Taguchi T, Treede RD, Mense S (2011) Nociceptive input from the rat thoracolumbar fascia to lumbar dorsal horn neurones. Eur J Pain 15:810-815.
48. Hoheisel U, Taguchi T, Mense S (2012) Nociception: the thoracolumbar fascia as a sensory organ. In: Schleip R, Findley TW, Chaitow L, Huijing PA (eds) Fascia: the tensional network of the human body: the science and clinical applications in manual and movement therapy. Churchill Livingstone/Elsevier, Edinburgh, pp 95-101
49. Iannone F, De BC, Dell’Accio F, Covelli M, Patella V, Lo BG, Lapadula G (2002) Increased expression of nerve growth factor (NGF) and high affinity NGF receptor (p140 TrkA) in human osteoarthritic chondrocytes. Rheumatology 41:1413-1418.
50. Indo Y, Tsuruta M, Hayashida Y, Karim MA, Ohta K, Kawano T, Mitsubuchi H, Tonoki H,Awaya Y, Matsuda I (1996) Mutations in the TRKA/NGF receptor gene in patients with congenital insensitivity to pain with anhidrosis. Nat Genet 13:485-488.
51. Itoh K, Okada K, Kawakita K (2004) A proposed experimental model of myofascial trigger points in human muscle after slow eccentric exercise. Acupunct Med 22:2-12.
52. Iwakura N, Ohtori S, Orita S, Yamashita M, Takahashi K, Kuniyoshi K (2010) Role of low-affinity nerve growth factor receptor inhibitory antibody in reducing pain behavior and calcitonin gene-related Peptide expression in a rat model of wrist joint inflammatory pain. J Hand Surg Am35:267-273
53. Ji R, Samad T, Jin S, Schmoll R, Woolf C (2002) p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36:57-68
54. Jiang YH, Peng CH, Liu HT, Kuo HC (2013) Increased pro-inflammatory cytokines, C-reactive protein and nerve growth factor expressions in serum of patients with interstitial cystitis/ bladder pain syndrome. PLoS One 8:e76779
55. Kawakita K, Itoh K, Okada K (2008) Experimental model of trigger points using eccentric exercise. J Musculoskelet Pain 16:29-35
56. Khodorova A, Nicol GD, Strichartz G (2013) The p75(NTR) signaling cascade mediates mechanical hyperalgesia induced by nerve growth factor injected into the rat hind paw. Neuroscience 254:312-323
57. Kim JC, Park EY, Seo SI, Park YH, Hwang TK (2006) Nerve growth factor and prostaglandins in the urine of female patients with overactive bladder. J Urol 175:1773-1776.
58. Kivitz AJ, Gimbel JS, Bramson C, Nemeth MA, Keller DS, Brown MT, West CR, Verburg KM(2013) Efficacy and safety of tanezumab versus naproxen in the treatment of chronic low back pain. Pain 154:1009-1021
59. Koltzenburg M, Bennett DL, Shelton DL, Mcmahon SB (1999) Neutralization of endogenous NGF prevents the sensitization of nociceptors supplying inflamed skin. Eur J Neurosci11:1698-1704
60. Lamb K, Gebhart GF, Bielefeldt K (2004) Increased nerve growth factor expression triggers bladder overactivity. J Pain 5:150-156
61. Leslie TA, Emson PC, Dowd PM, Woolf CJ (1995) Nerve growth factor contributes to the up-regulation of growth- associated protein 43 and preprotachykinin A messenger RNAs in primary sensory neurons following peripheral inflammation. Neuroscience 67:753-76.
62. Lewin GR, Nykjaer A (2014) Pro-neurotrophins, sortilin, and nociception. Eur J Neurosci39:363-374
63. Lewin GR, Winter J, Mcmahon SB (1992) Regulation of afferent connectivity in the adult spinal cord by nerve growth factor. Eur J Neurosci 4:700-707
64. Lewin GR, Ritter AM, Mendell LM (1993) Nerve growth factor-induced hyperalgesia in the neonatal and adult rat. J Neurosci 13:2136-2148
65. Lewin GR, Rueff A, Mendell LM (1994) Peripheral and central mechanisms of NGF-induced hyperalgesia. Eur J Neurosci 6:1903-1912
66. Liu HT, Chancellor MB, Kuo HC (2009) Decrease of urinary nerve growth factor levels after antimuscarinic therapy in patients with overactive bladder. BJU Int 103:1668-1672
67. Liu HT, Jiang YH, Kuo HC (2013) Increased serum adipokines implicate chronic inflammation in the pathogenesis of overactive bladder syndrome refractory to antimuscarinic therapy. PLoS One 8:e76706
68. Malik-Hall M, Dina OA, Levine JD (2005) Primary afferent nociceptor mechanisms mediating NGF-induced mechanical hyperalgesia. Eur J Neurosci 21:3387-3394
69. Mamet J, Baron A, Lazdunski M, Voilley N (2002) Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels. J Neurosci22:10662-10670
70. Mann MK, Dong XD, Svensson P, Cairns BE (2006) Influence of intramuscular nerve growth factor injection on the response properties of rat masseter muscle afferent fibers. J Orofac Pain20:325-336
71. Matsuura Y, Iwakura N, Ohtori S, Suzuki T, Kuniyoshi K, Murakami K, Hiwatari R, Hashimoto K, Okamoto S, Shibayama M, Kobayashi T, Ogawa Y, Sukegawa K, Takahashi K (2013) The effect of Anti-NGF receptor (p75 Neurotrophin Receptor) antibodies on nociceptive behavior and activation of spinal microglia in the rat brachial plexus avulsion model. Spine (Phila Pa1976) 38:E332-E338
72. Mcmahon SB, Bennett DL, Priestley JV, Shelton DL (1995) The biological effects of endogenous nerve growth factor on adult sensory neurons revealed by a trkA-IgG fusion molecule. Nat Med1:774-780
73. McNamee KE, Burleigh A, Gompels LL, Feldmann M, Allen SJ, Williams RO, Dawbarn D, Vincent TL, Inglis JJ (2010) Treatment of murine osteoarthritis with TrkAd5 reveals a pivotal role for nerve growth factor in non-inflammatory joint pain. Pain 149:386-392
74. Murase S, Terazawa E, Queme F, Ota H, Matsuda T, Hirate K, Kozaki Y, Katanosaka K, Taguchi T, Mizumura K (2010) Bradykinin and nerve growth factor play pivotal roles in muscular mechanical hyperalgesia after exercise (delayed onset muscle soreness). J Neurosci30:3752-3761
75. Murase S, Yamanaka Y, Kanda H, Mizumura K (2012) COX-2, nerve growth factor (NGF) and glial cell-derived neurotrophic factor (GDNF), which play pivotal roles in delayed onset muscle soreness (DOMS), are produced by exercised skeletal muscle. J Physiol Sci 62 (Suppl):S179
76. Murase S, Terazawa E, Hirate K, Yamanaka H, Kanda H, Noguchi K, Ota H, Queme F, Taguchi T, Mizumura K (2013) Upregulated glial cell line-derived neurotrophic factor through cyclooxygenase-2 activation in the muscle is required for mechanical hyperalgesia after exercise in rats. J Physiol 591:3035-3048
77. Nicol GD, Vasko MR (2007) Unraveling the story of NGF-mediated sensitization of nociceptive sensory neurons: ON or OFF the Trks? Mol Interv 7:26-41
78. Nishigami T, Osako Y, Ikeuchi M, Yuri K, Ushida T (2013) Development of heat hyperalgesia and changes of TRPV1 and NGF expression in rat dorsal root ganglion following joint immobilization. Physiol Res 62:215-219
79. Oddiah D, Anand P, Mcmahon SB, Rattray M (1998) Rapid increase of NGF, BDNF and NT-3 mRNAs in inflamed bladder. Neuroreport 9:1455-1458
80. Ohmichi Y, Sato J, Ohmichi M, Sakurai H, Yoshimoto T, Morimoto A, Hashimoto T, Eguchi K, Nishihara M, Arai YC, Ohishi H, Asamoto K, Ushida T, Nakano T, Kumazawa T (2012)Two-week cast immobilization induced chronic widespread hyperalgesia in rats. Eur J Pain16:338-348
81. Ota H, Katanosaka K, Murase S, Kashio M, Tominaga M, Mizumura K (2013) TRPV1 and TRPV4 play pivotal roles in delayed onset muscle soreness. PLoS One 8:e65751
82. Pantano F, Zoccoli A, Iuliani M, Lanzetta G, Vincenzi B, Tonini G, Santini D (2011) New targets, new drugs for metastatic bone pain: a new philosophy. Expert Opin Emerg Drugs 16:403-405.
83. Petty BG, Cornblath DR, Adornato BT, Chaudhry V, Flexner C, Wachsman M, Sinicropi D,Burton LE, Peroutka SJ (1994) The effect of systemically administered recombinant human nerve growth factor in healthy human subjects. Ann Neurol 36:244-246.
84. Queme F, Taguchi T, Mizumura K, Graven-Nielsen T (2013) Muscular heat and mechanical pain sensitivity after lengthening contractions in humans and animals. J Pain 14:1425-1436.
85. Ritter AM, Lewin GR, Kremer NE, Mendell LM (1991) Requirement for nerve growth factor in the development of myelinated nociceptors in vivo. Nature 350:500-502.
86. Rukwied R, Mayer A, Kluschina O, Obreja O, Schley M, Schmelz M (2010) NGF induces non-inflammatory localized and lasting mechanical and thermal hypersensitivity in human skin. Pain 148:407-413
87. Sanga P, Katz N, Polverejan E, Wang S, Kelly KM, Haeussler J, Thipphawong J (2013) Efficacy, safety, and tolerability of fulranumab, an anti-nerve growth factor antibody, in the treatment of patients with moderate to severe osteoarthritis pain. Pain 154:1910-1919.
88. Sarchielli P, Mancini ML, Floridi A, Coppola F, Rossi C, Nardi K, Acciarresi M, Pini LA, Calabresi P (2007) Increased levels of neurotrophins are not specific for chronic migraine: evidence from primary fibromyalgia syndrome. J Pain 8:737-745.
89. Schmieg N, Menendez G, Schiavo G, Terenzio M (2014) Signalling endosomes in axonal transport: travel updates on the molecular highway. Semin Cell Dev Biol 27:32-43. doi:10.1016/j.semcdb.2013.10.004
90. Sekino Y, Nakano J, Hamaue Y, Chuganji S, Sakamoto J, Yoshimura T, Origuchi T, Okita M (2014) Sensory hyperinnervation and increase in NGF, TRPV1 and P2X3 expression in the epidermis following cast immobilization in rats. Eur J Pain 18:639-648.
91. Shu X, Mendell LM (1999) Nerve growth factor acutely sensitizes the response of adult rat sensory neurons to capsaicin. Neurosci Lett 274:159-162.
92. Shu X, Mendell LM (2001) Acute sensitization by NGF of the response of small-diameter sensory neurons to capsaicin. J Neurophysiol 86:2931-2938.
93. Smith LL (1991) Acute inflammation—the underlying mechanism in delayed onset muscle soreness. Med Sci Sports Exerc 23:542-551
94. Stein AT, Ufret-Vincenty CA, Hua L, Santana LF, Gordon SE (2006) Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J Gen Physiol 128:509-522
95. Svensson P, Cairns BE, Wang K, Arendt-Nielsen L (2003) Injection of nerve growth factor into human masseter muscle evokes long-lasting mechanical allodynia and hyperalgesia. Pain104:241-247
96. Taguchi T, Matsuda T, Tamura R, Sato J, Mizumura K (2005a) Muscular mechanical hyperalgesia revealed by behavioural pain test and c-Fos expression in the spinal dorsal horn after eccentric contraction in rats. J Physiol 564:259-268
97. Taguchi T, Sato J, Mizumura K (2005b) Augmented mechanical response of muscle thin-fiber sensory receptors recorded from rat muscle-nerve preparations in vitro after eccentric contraction. J Neurophysiol 94:2822-2831
98. Taguchi T, Hoheisel U, Mense S (2008a) Dorsal horn neurons having input from low back structures in rats. Pain 138:119-129
99. Taguchi T, Hoheisel U, Mense S (2008b) Neuroanatomy and electrophysiology of low back pain: experiments on rats. Aktuelle Urol 34:472-477
100. Taguchi T, Yasui M, Kubo A, Abe M, Kiyama H, Yamanaka A, Mizumura K (2013) Nociception originating from the crural fascia in rats. Pain 154:1103-1114.
101. Urai H, Murase S, Mizumura K (2012) Decreased nerve growth factor upregulation is a mechanism for reduced mechanical hyperalgesia after the second bout of exercise in rats. Scand J Med Sci Sports 23:e96-e101
102. Wild KD, Bian D, Zhu D, Davis J, Bannon AW, Zhang TJ, Louis JC (2007) Antibodies to nerve growth factor reverse established tactile allodynia in rodent models of neuropathic pain without tolerance. J Pharmacol Exp Ther 322:282-287
103. Woolf CJ, Safieh-Garabedian B, Ma QP, Crilly P, Winter J (1994) Nerve growth factor contributes to the generation of inflammatory sensory hypersensitivity. Neuroscience 62:327-331.
104. Woolf CJ, Ma QP, Allchorne A, Poole S (1996) Peripheral cell types contributing to the hyperalgesic action of nerve growth factor in inflammation. J Neurosci 16:2716-2723.
105. Xue Q, Jong B, Chen T, Schumacher MA (2007) Transcription of rat TRPV1 utilizes a dual promoter system that is positively regulated by nerve growth factor. J Neurochem 101:212-222.
106. Ye Y, Dang D, Zhang J, Viet CT, Lam DK, Dolan JC, Gibbs JL, Schmidt BL (2011) Nerve growth factor links oral cancer progression, pain, and cachexia. Mol Cancer Ther 10:1667-1676.
107. Zhang X, Huang J, McNaughton PA (2005) NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J 24:4211-4223.
108. Zhang YH, Kays J, Hodgdon KE, Sacktor TC, Nicol GD (2012) Nerve growth factor enhances the excitability of rat sensory neurons through activation of the atypical protein kinase C isoform, PKMzeta. J Neurophysiol 107:315-335
109. Zhu W, Oxford GS (2007) Phosphoinositide-3-kinase and mitogen activated protein kinase signaling pathways mediate acute NGF sensitization of TRPV1. Mol Cell Neurosci34:689-700
110. Zhu W, Galoyan SM, Petruska JC, Oxford GS, Mendell LM (2004) A developmental switch in acute sensitization of small dorsal root ganglion (DRG) neurons to capsaicin or noxious heating by NGF. J Neurophysiol 92:3148-3152