Abstract
Nerve growth factor (NGF), a member of the neurotrophin family, is essential for the development and maintenance of sensory neurons and for the formation of central pain circuitry. The current study was designed to evaluate the expression of NGF in the brain of rats with spared nerve injury (SNI), using immunohistochemical technique. The results showed that the level of NGF in the Red nucleus (RN) of SNI rats was apparently higher than that of sham-operated rats. To further study the effect of NGF in the development of neuropathic pain, different doses of anti-NGF antibody (20, 2.0 and 0.2 μg/ml) were microinjected into the RN contralateral to the nerve injury side of SNI rats. The data suggested that the higher doses of anti-NGF antibody (20 and 2.0 μg/ml) significantly attenuated the mechanical allodynia of neuropathic rats, while the 0.2 μg/ml antibody showed no analgesic effect. These results suggest that the NGF of RN is involved in the development of neuropathic allodynia in SNI rats.
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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(6):1001–1011. doi:10.1016/0092-8674(94)90378-6
Levi-Montalcini R (1987) The nerve growth factor 35 years later. Science 237:1154–1162. doi:10.1126/science.3306916
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(3):693–698. doi:10.1016/0306-4522(92)90237-V
Aloe L, Tuveri MA, Levi-Montalcini R (1992) Studies on carrageenan-induced arthritis in adult rats: presence of nerve growth factor and role of sympathetic innervation. Rheumatol Int 12(5):213–216. doi:10.1007/BF00302155
Okragly AJ, Niles AL, Saban R, Schmidt D, Hoffman RL, Warner TF, Moon TD, Uehling DT, Haak-Frendscho M (1999) Elevated tryptase, nerve growth factor, neurotrophin-3 and glial cell line-derived neurotrophic factor levels in the urine of interstitial cystitis and bladder cancer patients. J Urol 161(2):438–441. doi:10.1016/S0022-5347(01)61915-3
Heumann R, Korshin S, Bandtlow C, Thoenen H (1987) Changes of nerve growth factor synthesis in non-neuronal cells in response to sciatic nerve transaction. J Cell Biol 104(1):1623–1631. doi:10.1083/jcb.104.6.1623
Wells MR, Vaidya U, Schwartz JP (1994) Bilateral phasic increases in dorsal root ganglia nerve growth factor synthesis after unilateral sciatic nerve crush. Exp Brain Res 101(1):53–58. doi:10.1007/BF00243216
Zhou XF, Deng YS, Chie E et al (1999) Satellite-cell-derived nerve growth factor and neurotrophin-3 are involved in noradrenergic sprouting in the dorsal root ganglia following peripheral nerve injury in the rat. Eur J Neurosci 11:1711–1722. doi:10.1046/j.1460-9568.1999.00589.x
Lewin GR, Rueff A, Mendell LM (1994) Peripheral and central mechanisms of NGF-induced hyperalgesia. Eur J Neurosci 6(12):1903–1912. doi:10.1111/j.1460-9568.1994.tb00581.x
Ramer MS, French GD, Fahnestock M, Bisby MA (1995) Strain differences in neuropathic pain behavior in mice following chronic constriction injury: correlation with NGF production in injured nerve. Soc Neurosci Abstr 21:897
Woolf CJ, Safieh-Garabedian B, Ma QP et al (1994) Nerve growth factor contributes to the generation of inflammatory sensory hypersensitivity. Neuroscience 62(2):327–331. doi:10.1016/0306-4522(94)90366-2
McMahon SB, Bennett DL, Priestly JV et al (1995) The biological effects of endogenous nerve growth factor on adult sensory neurons revealed by a trkA-IgG fusion molecule. Nat Med 1(8):774–780. doi:10.1038/nm0895-774
Ramer MS, Bisby MA (1999) Adrenergic innervation of rat sensory ganglia following proximal or distal painful sciatic neuropathy: distinct mechanisms revealed by anti-NGF treatment. Eur J Neurosci 11:837–846. doi:10.1046/j.1460-9568.1999.00491.x
Ro LS, Chen ST, Tang LM, Jacobs JM (1999) Effect of NGF and anti-NGF on neuropathic pain in rats following chronic constriction injury of the sciatic nerve. Pain 79:265–274. doi:10.1016/S0304-3959(98)00164-X
Li X, Wang J, Wang Z, Dong C, Dong X, Jing Y, Yuan Y, Fan G (2008) Tumor necrosis factor-alpha of Red nucleus involved in the development of neuropathic allodynia. Brain Res Bull 77(5):233–236. doi:10.1016/j.brainresbull.2008.08.025
Wang Z, Wang J, Li X, Yuan Y, Fan G (2008) Interleukin-1 beta of Red nucleus involved in the development of allodynia in spared nerve injury rats. Exp Brain Res 188(3):379–384. doi:10.1007/s00221-008-1365-1
Zimmermann M (1983) Ethical guideline for investigations of experimental pain in conscious animals. Pain 16(2):109–110. doi:10.1016/0304-3959(83)90201-4
Decosterd I, Woolf CJ (2000) Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87(2):149–158. doi:10.1016/S0304-3959(00)00276-1
Paxinos G, Watson C (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, Sydney
Chaplan SR, Bach FW, Pogrel JW, Chung JW, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. Neurosci Methods 53:55–63. doi:10.1016/0165-0270(94)90144-9
Dixon WJ (1980) Efficient analysis of experimental observation. Ann Rev Pharmacol Toxicol 20:441–462. doi:10.1146/annurev.pa.20.040180.002301
Maier SF, Wiertelak EP, Martin D, Watkins LR (1993) Interleukin-1 mediates the behavioral hyperalgesia produced by lithium chloride and endotoxin. Brain Res 623:321–324. doi:10.1016/0006-8993(93)91446-Y
Basso DM, Beattie MS, Bresnahan JC (2002) Descending systems contributing to locomotor recovery after mild or moderate spinal cord injury in rats: experimental evidence and a review of literature. Restor Neurol Neurosci 20:189–218
Huang M, Liu M, Li X (1992) The analgesic effect of red nucleus and preliminary research on its mechanism. Zhen Ci Yan Jiu 17:166–170
Liu M, Liu X, Liu B (1991) The analgesia effect of red nucleus and strengthening effect thereof to the acupuncture analgesia. Zhen Ci Yan Jiu 1:48–53
Ramer MS, Kawaja MD, Henderson JT, Roder JC, Bisby MA (1998) Glial overexpression of NGF enhances neuropathic pain and adrenergic sprouting into DRG following chronic sciatic constriction in mice. Neurosci Lett 251:53–56. doi:10.1016/S0304-3940(98)00493-5
Oh EJ, Yoon YW, Lee SE, Hong SK (2000) Changes in nerve growth factor levels in dorsal root ganglia and spinal nerves in a rat neuropathic pain model. Exp Brain Res 130:93–99. doi:10.1007/s002219900233
Herzberg U, Eliav E, Dorsey JM, Gracely RH, Kopin IJ (1997) NGF involvement in pain induced by chronic constriction injury of the rat sciatic nerve. Neuroreport 8:1613–1618. doi:10.1097/00001756-199705060-00012
Wild KD, Bian D, Zhu D et al (2007) 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. doi:10.1124/jpet.106.116236
Apfel SC, Arezzo JC, Brownlee M, Federoff H, Kessler JA (1994) Nerve growth factor administration protects against experimental diabetic sensory neuropathy. Brain Res 634(1):7–12. doi:10.1016/0006-8993(94)90252-6
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The Authors wish to thank Dr. Jingshi Tang and Dr. Shudong Qiu for their expert help in reviewing the manuscript.
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Jing, YY., Wang, JY., Li, XL. et al. Nerve Growth Factor of Red Nucleus Involvement in Pain Induced by Spared Nerve Injury of the Rat Sciatic Nerve. Neurochem Res 34, 1612–1618 (2009). https://doi.org/10.1007/s11064-009-9950-7
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DOI: https://doi.org/10.1007/s11064-009-9950-7