Regenerative peripheral neuropathic pain: novel pathological pain, new therapeutic dimension

References

Agthong, S., Koonam, J., Kaewsema, A., and Chentanez, V. (2009). Inhibition of MAPK ERK impairs axonal regeneration without an effect on neuronal loss after nerve injury. Neurol. Res. 31, 1068–1074.10.1179/174313209X380883Search in Google Scholar

Allodi, I., Udina, E., and Navarro, X. (2012). Specificity of peripheral nerve regeneration: interactions at the axon level. Prog. Neurobiol. 98, 16–37.10.1016/j.pneurobio.2012.05.005Search in Google Scholar

Baron, R., Tolle, T.R., Gockel, U., Brosz, M., and Freynhagen, R. (2009). A cross-sectional cohort survey in 2100 patients with painful diabetic neuropathy and postherpetic neuralgia: differences in demographic data and sensory symptoms. Pain 146, 34–40.10.1016/j.pain.2009.06.001Search in Google Scholar

Barrot, M. (2012). Tests and models of nociception and pain in rodents. Neuroscience 211, 39–50.10.1016/j.neuroscience.2011.12.041Search in Google Scholar

Basbaum, A.I., Bautista, D.M., Scherrer, G., and Julius, D. (2009). Cellular and molecular mechanisms of pain. Cell 139, 267–284.10.1016/j.cell.2009.09.028Search in Google Scholar

Bester, H., Beggs, S., and Woolf, C.J. (2000). Changes in tactile stimuli-induced behavior and c-Fos expression in the superficial dorsal horn and in parabrachial nuclei after sciatic nerve crush. J. Comp. Neurol. 428, 45–61.10.1002/1096-9861(20001204)428:1<45::AID-CNE5>3.0.CO;2-ASearch in Google Scholar

Chen, J.T., Guo, D., Campanelli, D., Frattini, F., Mayer, F., Zhou, L., Kuner, R., Heppenstall, P.A., Knipper, M., and Hu, J. (2014a). Presynaptic GABAergic inhibition regulated by BDNF contributes to neuropathic pain induction. Nat. Commun. 5, 5331.10.1038/ncomms6331Search in Google Scholar

Chen, W., Walwyn, W., Ennes, H.S., Kim, H., McRoberts, J.A., and Marvizón, J.C. (2014b). BDNF released during neuropathic pain potentiates NMDA receptors in primary afferent terminals. Eur. J. Neurosci. 39, 1439–1454.10.1111/ejn.12516Search in Google Scholar

Cheng, C. and Zochodne, D.W. (2002). In vivo proliferation, migration and phenotypic changes of Schwann cells in the presence of myelinated fibers. Neuroscience 115, 321–329.10.1016/S0306-4522(02)00291-9Search in Google Scholar

Cho, H.J., Kim, J.K., Park, H.C., Kim, J.K., Kim, D.S., Ha, S.O., and Hong, H.S. (1998). Changes in brain-derived neurotrophic factor immunoreactivity in rat dorsal root ganglia, spinal cord, and gracile nuclei following cut or crush injuries. Exp. Neurol. 154, 224–230.10.1006/exnr.1998.6936Search in Google Scholar

Chung, J.M., Choi, Y., Yoon, Y.W., and Na, H.S. (1995). Effects of age on behavioral signs of neuropathic pain in an experimental rat model. Neurosci. Lett. 183, 54–57.10.1016/0304-3940(94)11113-WSearch in Google Scholar

Chung, J.M. and Chung, K. (2002). Importance of hyperexcitability of DRG neurons in neuropathic pain. Pain Pract. 2, 87–97.10.1046/j.1533-2500.2002.02011.xSearch in Google Scholar

Cobianchi, S., de Cruz, J., and Navarro, X. (2014). Assessment of sensory thresholds and nociceptive fiber growth after sciatic nerve injury reveals the differential contribution of collateral reinnervation and nerve regeneration to neuropathic pain. Exp. Neurol. 255, 1–11.10.1016/j.expneurol.2014.02.008Search in Google Scholar

Costigan, M., Scholz, J., and Woolf, C.J. (2009). Neuropathic pain: a maladaptive response of the nervous system to damage. Annu. Rev. Neurosci. 32, 1–32.10.1146/annurev.neuro.051508.135531Search in Google Scholar

Coull, J.A., Boudreau, D., Bachand, K., Prescott, S.A., Nault, F., Sík, A., De Koninck, P., and De Koninck, Y. (2003). Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424, 938–942.10.1038/nature01868Search in Google Scholar

Coull, J.A., Beggs, S., Boudreau, D., Boivin, D., Tsuda, M., Inoue, K., Gravel, C., Salter, M.W., and De Koninck, Y. (2005). BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438, 1017–1021.10.1038/nature04223Search in Google Scholar

Davis, K.D. (1998). Cold-induced pain and prickle in the glabrous and hairy skin. Pain 75, 47–57.10.1016/S0304-3959(97)00203-0Search in Google Scholar

Decosterd, I., Allchorne, A., and Woolf, C.J. (2002). Progressive tactile hypersensitivity after a peripheral nerve crush: non-noxious mechanical stimulus-induced neuropathic pain. Pain 100, 155–162.10.1016/S0304-3959(02)00275-0Search in Google Scholar

deMedinacell, L., Hurpeau, J., Merle, M., and Begorre, H. (1989). Cold and post-traumatic pain: modeling of the peripheral nerve message. BioSystems 496, 228–240.Search in Google Scholar

de Ruiter, G.C., Spinner, R.J., Verhaagen, J., and Malessy, M.J. (2014). Misdirection and guidance of regenerating axons after experimental nerve injury and repair. J. Neurosurg. 120, 493–501.10.3171/2013.8.JNS122300Search in Google Scholar PubMed

Dubový, P., Klusáková, I., and Hradilová Svíženská, I. (2014). Inflammatory profiling of Schwann cells in contact with growing axons distal to nerve injury. Biomed. Res. Int. 2014, 691041.10.1155/2014/691041Search in Google Scholar PubMed PubMed Central

Dyck, P.J., Lambert, E.H., Wood, M.B., and Linscheid, R.L. (1998). Assessment of nerve regeneration and adaptation after median nerve reconnection and digital neurovascular flap transfer. Neurology 38, 1586–1591.10.1212/WNL.38.10.1586Search in Google Scholar

Gold, M.S., Weinreich, D., Kim, C.S., Wang, R., Treanor, J., Porreca, F., and Lai, J. (2003). Redistribution of Na (V) 1.8 in uninjured axons enables neuropathic pain. J. Neurosci. 23, 158–166.10.1523/JNEUROSCI.23-01-00158.2003Search in Google Scholar

Grossmann, L., Gorodetskaya, N., Baron, R., and Jänig, W. (2009). Enhancement of ectopic discharge in regenerating A- and C-fibers by inflammatory mediators. J. Neurophysiol. 101, 2762–2774.10.1152/jn.91091.2008Search in Google Scholar

Hsieh, Y.L., Lin, W.M., Lue, J.H., Chang, M.F., and Hsieh, S.T. (2009). Effects of 4-methylcatechol on skin reinnervation: promotion of cutaneous nerve regeneration after crush injury. J. Neuropathol. Exp. Neurol. 68, 1269–1281.10.1097/NEN.0b013e3181c17b46Search in Google Scholar

Jang, J.H., Kim, K.H., Nam, T.S., Lee, W.T., Park, K.A., Kim, D.W., and Leem, J.W. (2007). The role of uninjured C-afferents and injured afferents in the generation of mechanical hypersensitivity after partial peripheral nerve injury in the rat. Exp. Neurol. 204, 288–298.10.1016/j.expneurol.2006.11.004Search in Google Scholar

Jänig, W., Grossmann, L., and Gorodetskaya, N. (2009). Mechano- and thermosensitivity of regenerating cutaneous afferent nerve fibers. Exp. Brain Res. 196, 101–114.10.1007/s00221-008-1673-5Search in Google Scholar

Kenney, A.M. and Kocsis, J.D. (1998). Peripheral axotomy induces long-term c-Jun amino-terminal kinase-1 activation and activator protein-1 binding activity by c-Jun and junD in adult rat dorsal root ganglia in vivo. J. Neurosci. 18, 1318–1328.10.1523/JNEUROSCI.18-04-01318.1998Search in Google Scholar

Li, Y., Dorsi, M.J., Meyer, R.A., and Belzberg, A.J. (2000). Mechanical hyperalgesia after an L5 spinal nerve lesion in the rat is not dependent on input from injured nerve fibers. Pain 85, 493–502.10.1016/S0304-3959(00)00250-5Search in Google Scholar

Mahn, F., Hullemann, P., Gockel, U., Brosz, M., Freynhagen, R., Tolle, T.R., and Baron, R. (2011). Sensory symptom profiles and co-morbidities in painful radiculopathy. PLoS One 6, e18018.10.1371/journal.pone.0018018Search in Google Scholar PubMed PubMed Central

Nakagawa, K., Takeda, M., Tsuboi, Y., Kondo, M., Kitagawa, J., Matsumoto, S., Kobayashi, A., Sessle, B.J., Shinoda, M., and Iwata, K. (2010). Alteration of primary afferent activity following inferior alveolar nerve transection in rats. Mol. Pain 6, 9.10.1186/1744-8069-6-9Search in Google Scholar PubMed PubMed Central

Nascimento, F.P., Magnussen, C., Yousefpour, N., and RibeirodaSilva, A. (2015). Sympathetic fibre sprouting in the skin contributes to pain-related behaviour in spared nerve injury and cuff models of neuropathic pain. Mol. Pain. 11, 59.10.1186/s12990-015-0062-xSearch in Google Scholar

Navarro, X., Vivó, M., and Valero-Cabré, A. (2007). Neural plasticity after peripheral nerve injury and regeneration. Prog. Neurobiol. 82, 163–201.10.1016/j.pneurobio.2007.06.005Search in Google Scholar

Nikolajsen, L., Black, J.A., Kroner, K., Jensen, T.S., and Waxman, S.G. (2010). Neuroma removal for neuropathic pain: efficacy and predictive value of lidocaine infusion. Clin. J. Pain 26, 788–793.10.1097/AJP.0b013e3181ed0823Search in Google Scholar

Obata, K., Yamanaka, H., Fukuoka, T., Yi, D., Tokunaga, A., Hashimoto, N., Yoshikawa, H., and Noguchi, K. (2003). Contribution of injured and uninjured dorsal root ganglion neurons to pain behavior and the changes in gene expression following chronic constriction injury of the sciatic nerve in rats. Pain 101, 65–77.10.1016/S0304-3959(02)00296-8Search in Google Scholar

Obata, K., Yamanaka, H., Kobayashi, K., Dai, Y., Mizushima, T., Katsura, H., Fukuoka, T., Tokunaga, A., and Noguchi, K. (2004). Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation. J. Neurosci. 24, 10211–10222.10.1523/JNEUROSCI.3388-04.2004Search in Google Scholar

Ochs, G., Schenk, M., and Struppler, A. (1989). Painful dysaesthesia following peripheral nerve injury: clinical and electrophysiological study. Brain Res. 496, 228–240.10.1016/0006-8993(89)91070-6Search in Google Scholar

Peleshok, J.C. and Ribeiro-da-Silva, A. (2012). Neurotrophic factor changes in the rat thick skin following chronic constriction injury of the sciatic nerve. Mol. Pain 8, 1.10.1186/1744-8069-8-1Search in Google Scholar PubMed PubMed Central

Qu, L.T. and Ma, C. (2011). Animal models of pain after peripheral nerve injury. Animal Models of Pain. C. Ma and J.M. Zhang, eds. (Totowa, NJ: Humana Press Inc.), pp. 69–80.10.1007/978-1-60761-880-5_4Search in Google Scholar

Reinhold, A.K., Batti, L., Bilbao, D., Rittner, H.L., and Heppenstall, P.A. (2015). Differential transcriptional profiling of damaged and intact adjacent dorsal root ganglia neurons in neuropathic pain. PLoS One 10, e0123342.10.1371/journal.pone.0123342Search in Google Scholar PubMed PubMed Central

Ren, H.Y., Ding, Y.Q., Xiao, X., Xie, W.Z., Feng, Y.P., Li, X.Y., and Qi, J.G. (2016). Behavioral characterization of neuropathic pain on the glabrous skin areas reinnervated solely by axotomy-regenerative axons after adult rat sciatic nerve crush. Neuroreport, 27, 404–414.10.1097/WNR.0000000000000554Search in Google Scholar PubMed

Sah, D.W., Ossipo, M.H., and Porreca, F. (2003). Neurotrophic factors as novel therapeutics for neuropathic pain. Nat. Rev. Drug Discov. 2, 460–472.10.1038/nrd1107Search in Google Scholar PubMed

Saito, T., Schbamori, Y., Manabe, Y., Yamagishi, T., Yamamoto, T., Ohtsubo, T., and Saito, H. (2000). Morphological and functional study of regenerated corda tympani nerves in humans. Ann. Otol. Rhinol. Larygol. 109, 703–709.10.1177/000348940010900801Search in Google Scholar PubMed

Saito, K., Hitomi, S., Suzuki, I., Masuda, Y., Kitagawa, J., Tsuboi, Y., Kondo, M., Sessle, B.J., and Iwata, K. (2008). Modulation of trigeminal spinal subnucleus caudalis neuronal activity following regeneration of transected inferior alveolar nerve in rats. J. Neurophysiol. 99, 2251–2263.10.1152/jn.00794.2007Search in Google Scholar PubMed

Sapunar, D., Kostic, S., Banozic, A., and Puljak, L. (2012). Dorsal root ganglion – a potential new therapeutic target for neuropathic pain. J. Pain Res. 5, 31–38.10.2147/JPR.S26603Search in Google Scholar PubMed PubMed Central

Sawai, S., Kanai, K., Nakata, M., Hiraga, A., Misawa, S., Isose, S., Hattori, T., and Kuwabara, S. (2008). Changes in excitability properties associated with axonal regeneration in human neuropathy and mouse Wallerian degeneration. Clin. Neurophysiol. 119, 1097–1105.10.1016/j.clinph.2008.01.022Search in Google Scholar PubMed

Scheib, J. and Höke, A. (2013). Advances in peripheral nerve regeneration. Nat. Rev. Neurol. 9, 668–676.10.1038/nrneurol.2013.227Search in Google Scholar PubMed

Schley, M.T., Wilms, P., Toepfner, S., Schaller, H.P., Schmelz, M., Konrad, C.J., and Birbaumer, N. (2008). Painful and nonpainful phantom and stump sensations in acute traumatic amputees. J. Trauma 65, 858–864.10.1097/TA.0b013e31812eed9eSearch in Google Scholar PubMed

Scholz, J. and Woolf, C.J. (2007). The neuropathic pain triad: neurons, immune cells and glia. Nat. Neurosci. 10, 1361–1368.10.1038/nn1992Search in Google Scholar PubMed

Scholz, J., Mannion, R.J., Hord, D.E., Griffin, R.S., Rawal, B., Zheng, H., Scoffings, D., Phillips, A., Guo, J., Laing, R.J., et al. (2009). A novel tool for the assessment of pain: validation in low back pain. PLoS Med. 6, e1000047.10.1371/journal.pmed.1000047Search in Google Scholar PubMed PubMed Central

Takeda, M., Tsuboi, Y., Kitagawa, J., Nakagawa, K., Iwata, K., and Matsumoto, S. (2011). Potassium channels as a potential therapeutic target for trigeminal neuropathic and inflammatory pain. Mol. Pain 7, 5.10.1186/1744-8069-7-5Search in Google Scholar PubMed PubMed Central

Taylor, A.M. and Ribeiro-da-Silva, A. (2011). GDNF levels in the lower lip skin in a rat model of trigeminal neuropathic pain: implications for nonpeptidergic fiber reinnervation and parasympathetic sprouting. Pain 152, 1502–1510.10.1016/j.pain.2011.02.035Search in Google Scholar PubMed

Toth, C., Lander, J., and Wiebe, S. (2009). The prevalence and impact of chronic pain with neuropathic pain symptoms in the general population. Pain Med. 10, 918–929.10.1111/j.1526-4637.2009.00655.xSearch in Google Scholar PubMed

von Hehn, C.A., Baron, R., and Woolf, C.J. (2012). Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron 73, 638–652.10.1016/j.neuron.2012.02.008Search in Google Scholar PubMed PubMed Central

Wong, K.H., Kanagasabapathy, G., Bakar, R., Phan, C.-W., and Sabaratnam, V. (2015). Restoration of sensory dysfunction following peripheral nerve injury by the polysaccharide from culinary and medicinal mushroom, Hericium erinaceus (Bull.: Fr.) Pers. through its neuroregenerative action. Food Sci. Technol. (Campinas) 5, 712–721.10.1590/1678-457X.6838Search in Google Scholar

Woolf, C.J. and Ma, Q. (2007). Nociceptors-noxious stimulus detectors. Neuron 55, 353–364.10.1016/j.neuron.2007.07.016Search in Google Scholar PubMed

Woolf, C.J., Shortland, P., Reynolds, M., Ridings, J., Doubell, T., and Coggeshall, R.E. (1995). Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J. Comp. Neurol. 360, 121–134.10.1002/cne.903600109Search in Google Scholar PubMed

Wu, L., Wu, J., Chang, H.H., and Havton, L.A. (2012). Selective plasticity of primary afferent innervation to the dorsal horn and autonomic nuclei following lumbosacral ventral root avulsion and reimplantation in long term studies. Exp. Neurol. 233, 758–766.10.1016/j.expneurol.2011.11.034Search in Google Scholar PubMed

Xu, J.T., Xin, W.J., Wei, X.H., Wu, C.Y., Ge, Y.X., Liu, Y.L., Zang, Y., Zhang, T., Li, Y.Y., and Liu, X.G. (2007). p38 Activation in uninjured primary afferent neurons and in spinal microglia contributes to the development of neuropathic pain induced by selective motor fiber injury. Exp. Neurol. 204, 355–365.10.1016/j.expneurol.2006.11.016Search in Google Scholar PubMed

Yoon, Y.W., Lee, D.H., Lee, B.H., Chung, K., and Chung, J.M. (1999). Different strains and substrains of rats show different levels of neuropathic pain behaviors. Exp. Brain Res. 129, 167–171.10.1007/s002210050886Search in Google Scholar PubMed

Zheng, J.H., Walters, E.T., and Song, X.J. (2007). Dissociation of dorsal root ganglion neurons induces hyperexcitability that is maintained by increased responsiveness to cAMP and cGMP. J. Neurophysiol. 97, 15–25.10.1152/jn.00559.2006Search in Google Scholar PubMed

Zhou, L.J., Yang, T., Wei, X., Liu, Y., Xin, W.J., Chen, Y., Pang, R.P., Zang, Y., Li, Y.Y., and Liu, X.G. (2011). Brain-derived neurotrophic factor contributes to spinal long-term potentiation and mechanical hypersensitivity by activation of spinal microglia in rat. Brain Behav. Immun. 25, 322–334.10.1016/j.bbi.2010.09.025Search in Google Scholar PubMed