Gene expression changes in dorsal root ganglia following peripheral nerve injury: roles in inflammation,cell death and nociception
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摘要
Subsequent to a peripheral nerve injury, there are changes in gene expression within the dorsal root ganglia in response to the damage. This review selects factors which are well-known to be vital for inflammation, cell death and nociception, and highlights how alterations in their gene expression within the dorsal root ganglia can affect functional recovery. The majority of studies used polymerase chain reaction within animal models to analyse the dynamic changes following peripheral nerve injuries. This review aims to highlight the factors at the gene expression level that impede functional recovery and are hence are potential targets for therapeutic approaches. Where possible the experimental model, specific time-points and cellular location of expression levels are reported.
Subsequent to a peripheral nerve injury, there are changes in gene expression within the dorsal root ganglia in response to the damage. This review selects factors which are well-known to be vital for inflammation, cell death and nociception, and highlights how alterations in their gene expression within the dorsal root ganglia can affect functional recovery. The majority of studies used polymerase chain reaction within animal models to analyse the dynamic changes following peripheral nerve injuries. This review aims to highlight the factors at the gene expression level that impede functional recovery and are hence are potential targets for therapeutic approaches. Where possible the experimental model, specific time-points and cellular location of expression levels are reported.
Subsequent to a peripheral nerve injury, there are changes in gene expression within the dorsal root ganglia in response to the damage. This review selects factors which are well-known to be vital for inflammation, cell death and nociception, and highlights how alterations in their gene expression within the dorsal root ganglia can affect functional recovery. The majority of studies used polymerase chain reaction within animal models to analyse the dynamic changes following peripheral nerve injuries. This review aims to highlight the factors at the gene expression level that impede functional recovery and are hence are potential targets for therapeutic approaches. Where possible the experimental model, specific time-points and cellular location of expression levels are reported.
引文
Abbadie C(2005)Chemokines,chemokine receptors and pain.Trends Immunol 26:529-534.
Abe N,Cavalli V(2008)Nerve injury signaling.Curr Opin Neurobiol 18:276-283.
Abe S,Mizusawa I,Kanno K,Yabashi A,Suto M,Kuraya M,Honda T,Hiraiwa K(2003)Nitric oxide synthase expressions in rat dorsal root ganglion after a hind limb tourniquet.Neuroreport 14:2267-2270.
Attal N,Bouhassira D(1999)Mechanisms of pain in peripheral neuropathy.Acta Neurol Scand Suppl 173:12-24;discussion 48-52.
Birder LA,Perl ER(1999)Expression of alpha2-adrenergic receptors in rat primary afferent neurones after peripheral nerve injury or inflammation.J Physiol 515:533-542.
Bisby MA,Chen S(1990)Delayed wallerian degeneration in sciatic nerves of C57BL/Ola mice is associated with impaired regeneration of sensory axons.Brain Res 530:117-120.
Bradley JR(2008)TNF-mediated inflammatory disease.J Pathol214:149-160.
Campbell WW(2008)Evaluation and management of peripheral nerve injury.Clin Neurophysiol 119:1951-1965.
Chandran V,Coppola G,Nawabi H,Omura T,Versano R,Huebner EA,Zhang A,Costigan M,Yekkirala A,Barrett L,Blesch A,Michaelevski I,Davis-Turak J,Gao F,Langfelder P,Horvath S,He Z,Benowitz L,Fainzilber M,Tuszynski M,et al.(2016)A Systems-level analysis of the peripheral nerve intrinsic axonal growth program.Neuron 89:956-970.
Chen F,Castranova V,Shi X,Demers LM(1999)New insights into the role of nuclear factor-kappaB,a ubiquitous transcription factor in the initiation of diseases.Clin Chem 45:7-17.
Cheng C,Zochodne DW(2002)In vivo proliferation,migration and phenotypic changes of Schwann cells in the presence of myelinated fibers.Neuroscience 115:321-329.
Copray JC,Mantingh I,Brouwer N,Biber K,Kust BM,Liem RS,Huitinga I,Tilders FJ,Van Dam AM,Boddeke HW(2001)Expression of interleukin-1 beta in rat dorsal root ganglia.J Neuroimmunol 118:203-211.
Dahlin LB,Brandt J(2004)Basic science of peripheral nerve repair:Wallerian degeneration/growth cones.Oper Tech Orthop14:138-145.
Drummond PD(2014)Neuronal changes resulting in up-regulation of alpha-1 adrenoceptors after peripheral nerve injury.Neural Regen Res 9:1337-1340.
DubovyP,Jan?álek R,KlusákováI,Sví?enskáI,PejchalováK(2006)Intra-and extraneuronal changes of immunofluorescence staining for TNF-alpha and TNFR1 in the dorsal root ganglia of rat peripheral neuropathic pain models.Cell Mol Neurobiol 26:1203-1215.
Fregnan F,Muratori L,Simoes AR,Giacobini-Robecchi MG,Raimondo S(2012)Role of inflammatory cytokines in peripheral nerve injury.Neural Regen Res 7:2259-2266.
Fu C,Yin Z,Yu D,Yang Z(2013)Substance P and calcitonin gene-related peptide expression in dorsal root ganglia in sciatic nerve injury rats.Neural Regen Res 8:3124-3130.
George EB,Glass JD,Griffin JW(1995)Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels.J Neurosci 15:6445-6452.
Gillardon F,Klimaschewski L,Wickert H,Krajewski S,Reed JC,Zimmermann M(1996)Expression pattern of candidate cell death effector proteins Bax,Bcl-2,Bcl-X,and c-Jun in sensory and motor neurons following sciatic nerve transection in the rat.Brain Res 739:244-250.
Goubier JN,Teboul F(2015)Chapter 38-grading of nerve injuries.In:Nerves and Nerve Injuries(Tubbs RS,Rizk E,Shoja MM,Loukas M,Barbaro N,Spinner RJ,eds),pp 603-610.San Diego:Academic Press.
Groves MJ,Christopherson T,Giometto B,Scaravilli F(1997)Axotomy-induced apoptosis in adult rat primary sensory neurons.JNeurocytol 26:615-624.
Ha SO,Kim JK,Hong HS,Kim DS,Cho HJ(2001)Expression of brain-derived neurotrophic factor in rat dorsal root ganglia,spinal cord and gracile nuclei in experimental models of neuropathic pain.Neuroscience 107:301-309.
Hanani M(2010)Satellite glial cells in sympathetic and parasympathetic ganglia:in search of function.Brain Res Rev 64:304-327.
Hanstein R,Hanani M,Scemes E,Spray DC(2016)Glial pannexin1contributes to tactile hypersensitivity in a mouse model of orofacial pain.Sci Rep 6:38266.
Hart AM,Terenghi G,Wiberg M(2008)Neuronal death after peripheral nerve injury and experimental strategies for neuroprotection.Neurol Res 30:999-1011.
Hilliard MA(2009)Axonal degeneration and regeneration:a mechanistic tug-of-war.J Neurochem 108:23-32.
Huebner EA,Strittmatter SM(2009)Axon regeneration in the peripheral and central nervous systems.Results Probl Cell Differ48:339-351.
Jeon SM,Lee KM,Cho HJ(2009)Expression of monocyte chemoattractant protein-1 in rat dorsal root ganglia and spinal cord in experimental models of neuropathic pain.Brain Res 1251:103-111.
Kandel ER,Schwartz JH,Jessel TM(2000)Principles of Neural Science.4th ed.New York:McGraw-Hill Companies.
Kato N,Nemoto K,Arino H,Fujikawa K(2003)Influence of peripheral inflammation on growth-associated phosphoprotein(GAP-43)expression in dorsal root ganglia and on nerve recovery after crush injury.Neurosci Res 45:297-303.
Kim SH,Chung JM(1992)An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat.Pain 50:355-363.
Kraft GH(1990)Fibrillation potential amplitude and muscle atrophy following peripheral nerve injury.Muscle Nerve 13:814-821.
Kwon MJ,Kim J,Shin H,Jeong SR,Kang YM,Choi JY,Hwang DH,Kim BG(2013)Contribution of macrophages to enhanced regenerative capacity of dorsal root ganglia sensory neurons by conditioning injury.J Neurosci 33:15095-15108.
Latremoliere A,Woolf CJ(2009)Central sensitization:a generator of pain hypersensitivity by central neural plasticity.J Pain 10:895-926.
Lawrence T(2009)The nuclear factor NF-kappaB pathway in inflammation.Cold Spring Harb Perspect Biol 1:a001651.
Li S,Xue C,Yuan Y,Zhang R,Wang Y,Wang Y,Yu B,Liu J,Ding F,Yang Y,Gu X(2015a)The transcriptional landscape of dorsal root ganglia after sciatic nerve transection.Sci Rep 5:16888.
Li YS,Xi Y,Li XJ,Leng CL,Jia MM,Zhang WK,Tang HB(2015b)Up-regulation of the biosynthesis and release of substance Pthrough Wnt/beta-catenin signaling pathway in rat dorsal root ganglion cells.PLoS One 10:e0129701.
Lu X,Richardson PM(1991)Inflammation near the nerve cell body enhances axonal regeneration.J Neurosci 11:972-978.
Lyon MF,Ogunkolade BW,Brown MC,Atherton DJ,Perry VH(1993)A gene affecting Wallerian nerve degeneration maps distally on mouse chromosome 4.Proc Natl Acad Sci U S A 90:9717-9720.
Mc Kay Hart A,Brannstrom T,Wiberg M,Terenghi G(2002)Primary sensory neurons and satellite cells after peripheral axotomy in the adult rat:timecourse of cell death and elimination.Exp Brain Res 142:308-318.
Menetski J,Mistry S,Lu M,Mudgett JS,Ransohoff RM,Demartino JA,Macintyre DE,Abbadie C(2007)Mice overexpressing chemokine ligand 2(CCL2)in astrocytes display enhanced nociceptive responses.Neuroscience 149:706-714.
Micheau O,Tschopp J(2003)Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes.Cell 114:181-190.
Momeni HR,Soleimani Mehranjani M,Shariatzadeh MA,Haddadi M(2013)Caspase-mediated apoptosis in sensory neurons of cultured dorsal root Ganglia in adult mouse.Cell J 15:212-217.
Murphy PG,Grondin J,Altares M,Richardson PM(1995)Induction of interleukin-6 in axotomized sensory neurons.J Neurosci15:5130-5138.
Mydlarz WK,Boahene KO(2013)Sunderland classification of nerve injury.In:Encyclopedia of Otolaryngology,Head and Neck Surgery(Kountakis SE,ed),pp 2615-2616.Berlin,Heidelberg:Springer Berlin Heidelberg.
Nascimento RS,Santiago MF,Marques SA,Allodi S,Martinez AM(2008)Diversity among satellite glial cells in dorsal root ganglia of the rat.Braz J Med Biol Res 41:1011-1017.
Obata K,Noguchi K(2006)BDNF in sensory neurons and chronic pain.Neurosci Res 55:1-10.
Ohara PT,Vit JP,Bhargava A,Romero M,Sundberg C,Charles AC,Jasmin L(2009)Gliopathic pain:when satellite glial cells go bad.Neuroscientist 15:450-463.
Ohtori S,Takahashi K,Moriya H,Myers RR(2004)TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury:studies in murine DRG and spinal cord.Spine(Phila Pa 1976)29:1082-1088.
Osborne NR,Anastakis DJ,Davis KD(2018)Peripheral nerve injuries,pain,and neuroplasticity.J Hand Ther 31:184-194.
Pertovaara A(2006)Noradrenergic pain modulation.Prog Neurobiol 80:53-83.
Petersen M,Zhang J,Zhang JM,LaMotte RH(1996)Abnormal spontaneous activity and responses to norepinephrine in dissociated dorsal root ganglion cells after chronic nerve constriction.Pain 67:391-397.
Poplawski G,Ishikawa T,Brifault C,Lee-Kubli C,Regestam R,Henry KW,Shiga Y,Kwon H,Ohtori S,Gonias SL,Campana WM(2018)Schwann cells regulate sensory neuron gene expression before and after peripheral nerve injury.Glia doi:10.1002/glia.23325.
Rock KL(2009)Pathobiology of inflammation to cell death.Biol Blood Marrow Transplant 15:137-138.
Rotshenker S(2011)Wallerian degeneration:the innate-immune response to traumatic nerve injury.J Neuroinflammation 8:109.
Sacerdote P,Franchi S,Trovato AE,Valsecchi AE,Panerai AE,Colleoni M(2008)Transient early expression of TNF-alpha in sciatic nerve and dorsal root ganglia in a mouse model of painful peripheral neuropathy.Neurosci Lett 436:210-213.
Sch?fers M,Svensson CI,Sommer C,Sorkin LS(2003)Tumor necrosis factor-alpha induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons.JNeurosci 23:2517-2521.
Sch?fers M,Geis C,Brors D,Yaksh TL,Sommer C(2002)Anterograde transport of tumor necrosis factor-alpha in the intact and injured rat sciatic nerve.J Neurosci 22:536-545.
Scheib J,H?ke A(2013)Advances in peripheral nerve regeneration.Nat Rev Neurol 9:668-676.
Seddon HJ(1942)A classification of nerve injuries.Br Med J 2:237-239.
Seltzer Z,Dubner R,Shir Y(1990)A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury.Pain 43:205-218.
Shi TJ,Cui JG,Meyerson BA,Linderoth B,Hokfelt T(1999)Regulation of galanin and neuropeptide Y in dorsal root ganglia and dorsal horn in rat mononeuropathic models:possible relation to tactile hypersensitivity.Neuroscience 93:741-757.
Shi TJ,Tandrup T,Bergman E,Xu ZQ,Ulfhake B,Hokfelt T(2001)Effect of peripheral nerve injury on dorsal root ganglion neurons in the C57 BL/6J mouse:marked changes both in cell numbers and neuropeptide expression.Neuroscience 105:249-263.
Stone LS,Vulchanova L,Riedl MS,Wang J,Williams FG,Wilcox GL,Elde R(1999)Effects of peripheral nerve injury on alpha-2Aand alpha-2C adrenergic receptor immunoreactivity in the rat spinal cord.Neuroscience 93:1399-1407.
Sun JH,Yang B,Donnelly DF,Ma C,LaMotte RH(2006)MCP-1enhances excitability of nociceptive neurons in chronically compressed dorsal root ganglia.J Neurophysiol 96:2189-2199.
Tanaka T,Minami M,Nakagawa T,Satoh M(2004)Enhanced production of monocyte chemoattractant protein-1 in the dorsal root ganglia in a rat model of neuropathic pain:possible involvement in the development of neuropathic pain.Neurosci Res 48:463-469.
Terenghi G(1999)Peripheral nerve regeneration and neurotrophic factors.J Anat 194:1-14.
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Abe N,Cavalli V(2008)Nerve injury signaling.Curr Opin Neurobiol 18:276-283.
Abe S,Mizusawa I,Kanno K,Yabashi A,Suto M,Kuraya M,Honda T,Hiraiwa K(2003)Nitric oxide synthase expressions in rat dorsal root ganglion after a hind limb tourniquet.Neuroreport 14:2267-2270.
Attal N,Bouhassira D(1999)Mechanisms of pain in peripheral neuropathy.Acta Neurol Scand Suppl 173:12-24;discussion 48-52.
Birder LA,Perl ER(1999)Expression of alpha2-adrenergic receptors in rat primary afferent neurones after peripheral nerve injury or inflammation.J Physiol 515:533-542.
Bisby MA,Chen S(1990)Delayed wallerian degeneration in sciatic nerves of C57BL/Ola mice is associated with impaired regeneration of sensory axons.Brain Res 530:117-120.
Bradley JR(2008)TNF-mediated inflammatory disease.J Pathol214:149-160.
Campbell WW(2008)Evaluation and management of peripheral nerve injury.Clin Neurophysiol 119:1951-1965.
Chandran V,Coppola G,Nawabi H,Omura T,Versano R,Huebner EA,Zhang A,Costigan M,Yekkirala A,Barrett L,Blesch A,Michaelevski I,Davis-Turak J,Gao F,Langfelder P,Horvath S,He Z,Benowitz L,Fainzilber M,Tuszynski M,et al.(2016)A Systems-level analysis of the peripheral nerve intrinsic axonal growth program.Neuron 89:956-970.
Chen F,Castranova V,Shi X,Demers LM(1999)New insights into the role of nuclear factor-kappaB,a ubiquitous transcription factor in the initiation of diseases.Clin Chem 45:7-17.
Cheng C,Zochodne DW(2002)In vivo proliferation,migration and phenotypic changes of Schwann cells in the presence of myelinated fibers.Neuroscience 115:321-329.
Copray JC,Mantingh I,Brouwer N,Biber K,Kust BM,Liem RS,Huitinga I,Tilders FJ,Van Dam AM,Boddeke HW(2001)Expression of interleukin-1 beta in rat dorsal root ganglia.J Neuroimmunol 118:203-211.
Dahlin LB,Brandt J(2004)Basic science of peripheral nerve repair:Wallerian degeneration/growth cones.Oper Tech Orthop14:138-145.
Drummond PD(2014)Neuronal changes resulting in up-regulation of alpha-1 adrenoceptors after peripheral nerve injury.Neural Regen Res 9:1337-1340.
DubovyP,Jan?álek R,KlusákováI,Sví?enskáI,PejchalováK(2006)Intra-and extraneuronal changes of immunofluorescence staining for TNF-alpha and TNFR1 in the dorsal root ganglia of rat peripheral neuropathic pain models.Cell Mol Neurobiol 26:1203-1215.
Fregnan F,Muratori L,Simoes AR,Giacobini-Robecchi MG,Raimondo S(2012)Role of inflammatory cytokines in peripheral nerve injury.Neural Regen Res 7:2259-2266.
Fu C,Yin Z,Yu D,Yang Z(2013)Substance P and calcitonin gene-related peptide expression in dorsal root ganglia in sciatic nerve injury rats.Neural Regen Res 8:3124-3130.
George EB,Glass JD,Griffin JW(1995)Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels.J Neurosci 15:6445-6452.
Gillardon F,Klimaschewski L,Wickert H,Krajewski S,Reed JC,Zimmermann M(1996)Expression pattern of candidate cell death effector proteins Bax,Bcl-2,Bcl-X,and c-Jun in sensory and motor neurons following sciatic nerve transection in the rat.Brain Res 739:244-250.
Goubier JN,Teboul F(2015)Chapter 38-grading of nerve injuries.In:Nerves and Nerve Injuries(Tubbs RS,Rizk E,Shoja MM,Loukas M,Barbaro N,Spinner RJ,eds),pp 603-610.San Diego:Academic Press.
Groves MJ,Christopherson T,Giometto B,Scaravilli F(1997)Axotomy-induced apoptosis in adult rat primary sensory neurons.JNeurocytol 26:615-624.
Ha SO,Kim JK,Hong HS,Kim DS,Cho HJ(2001)Expression of brain-derived neurotrophic factor in rat dorsal root ganglia,spinal cord and gracile nuclei in experimental models of neuropathic pain.Neuroscience 107:301-309.
Hanani M(2010)Satellite glial cells in sympathetic and parasympathetic ganglia:in search of function.Brain Res Rev 64:304-327.
Hanstein R,Hanani M,Scemes E,Spray DC(2016)Glial pannexin1contributes to tactile hypersensitivity in a mouse model of orofacial pain.Sci Rep 6:38266.
Hart AM,Terenghi G,Wiberg M(2008)Neuronal death after peripheral nerve injury and experimental strategies for neuroprotection.Neurol Res 30:999-1011.
Hilliard MA(2009)Axonal degeneration and regeneration:a mechanistic tug-of-war.J Neurochem 108:23-32.
Huebner EA,Strittmatter SM(2009)Axon regeneration in the peripheral and central nervous systems.Results Probl Cell Differ48:339-351.
Jeon SM,Lee KM,Cho HJ(2009)Expression of monocyte chemoattractant protein-1 in rat dorsal root ganglia and spinal cord in experimental models of neuropathic pain.Brain Res 1251:103-111.
Kandel ER,Schwartz JH,Jessel TM(2000)Principles of Neural Science.4th ed.New York:McGraw-Hill Companies.
Kato N,Nemoto K,Arino H,Fujikawa K(2003)Influence of peripheral inflammation on growth-associated phosphoprotein(GAP-43)expression in dorsal root ganglia and on nerve recovery after crush injury.Neurosci Res 45:297-303.
Kim SH,Chung JM(1992)An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat.Pain 50:355-363.
Kraft GH(1990)Fibrillation potential amplitude and muscle atrophy following peripheral nerve injury.Muscle Nerve 13:814-821.
Kwon MJ,Kim J,Shin H,Jeong SR,Kang YM,Choi JY,Hwang DH,Kim BG(2013)Contribution of macrophages to enhanced regenerative capacity of dorsal root ganglia sensory neurons by conditioning injury.J Neurosci 33:15095-15108.
Latremoliere A,Woolf CJ(2009)Central sensitization:a generator of pain hypersensitivity by central neural plasticity.J Pain 10:895-926.
Lawrence T(2009)The nuclear factor NF-kappaB pathway in inflammation.Cold Spring Harb Perspect Biol 1:a001651.
Li S,Xue C,Yuan Y,Zhang R,Wang Y,Wang Y,Yu B,Liu J,Ding F,Yang Y,Gu X(2015a)The transcriptional landscape of dorsal root ganglia after sciatic nerve transection.Sci Rep 5:16888.
Li YS,Xi Y,Li XJ,Leng CL,Jia MM,Zhang WK,Tang HB(2015b)Up-regulation of the biosynthesis and release of substance Pthrough Wnt/beta-catenin signaling pathway in rat dorsal root ganglion cells.PLoS One 10:e0129701.
Lu X,Richardson PM(1991)Inflammation near the nerve cell body enhances axonal regeneration.J Neurosci 11:972-978.
Lyon MF,Ogunkolade BW,Brown MC,Atherton DJ,Perry VH(1993)A gene affecting Wallerian nerve degeneration maps distally on mouse chromosome 4.Proc Natl Acad Sci U S A 90:9717-9720.
Mc Kay Hart A,Brannstrom T,Wiberg M,Terenghi G(2002)Primary sensory neurons and satellite cells after peripheral axotomy in the adult rat:timecourse of cell death and elimination.Exp Brain Res 142:308-318.
Menetski J,Mistry S,Lu M,Mudgett JS,Ransohoff RM,Demartino JA,Macintyre DE,Abbadie C(2007)Mice overexpressing chemokine ligand 2(CCL2)in astrocytes display enhanced nociceptive responses.Neuroscience 149:706-714.
Micheau O,Tschopp J(2003)Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes.Cell 114:181-190.
Momeni HR,Soleimani Mehranjani M,Shariatzadeh MA,Haddadi M(2013)Caspase-mediated apoptosis in sensory neurons of cultured dorsal root Ganglia in adult mouse.Cell J 15:212-217.
Murphy PG,Grondin J,Altares M,Richardson PM(1995)Induction of interleukin-6 in axotomized sensory neurons.J Neurosci15:5130-5138.
Mydlarz WK,Boahene KO(2013)Sunderland classification of nerve injury.In:Encyclopedia of Otolaryngology,Head and Neck Surgery(Kountakis SE,ed),pp 2615-2616.Berlin,Heidelberg:Springer Berlin Heidelberg.
Nascimento RS,Santiago MF,Marques SA,Allodi S,Martinez AM(2008)Diversity among satellite glial cells in dorsal root ganglia of the rat.Braz J Med Biol Res 41:1011-1017.
Obata K,Noguchi K(2006)BDNF in sensory neurons and chronic pain.Neurosci Res 55:1-10.
Ohara PT,Vit JP,Bhargava A,Romero M,Sundberg C,Charles AC,Jasmin L(2009)Gliopathic pain:when satellite glial cells go bad.Neuroscientist 15:450-463.
Ohtori S,Takahashi K,Moriya H,Myers RR(2004)TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury:studies in murine DRG and spinal cord.Spine(Phila Pa 1976)29:1082-1088.
Osborne NR,Anastakis DJ,Davis KD(2018)Peripheral nerve injuries,pain,and neuroplasticity.J Hand Ther 31:184-194.
Pertovaara A(2006)Noradrenergic pain modulation.Prog Neurobiol 80:53-83.
Petersen M,Zhang J,Zhang JM,LaMotte RH(1996)Abnormal spontaneous activity and responses to norepinephrine in dissociated dorsal root ganglion cells after chronic nerve constriction.Pain 67:391-397.
Poplawski G,Ishikawa T,Brifault C,Lee-Kubli C,Regestam R,Henry KW,Shiga Y,Kwon H,Ohtori S,Gonias SL,Campana WM(2018)Schwann cells regulate sensory neuron gene expression before and after peripheral nerve injury.Glia doi:10.1002/glia.23325.
Rock KL(2009)Pathobiology of inflammation to cell death.Biol Blood Marrow Transplant 15:137-138.
Rotshenker S(2011)Wallerian degeneration:the innate-immune response to traumatic nerve injury.J Neuroinflammation 8:109.
Sacerdote P,Franchi S,Trovato AE,Valsecchi AE,Panerai AE,Colleoni M(2008)Transient early expression of TNF-alpha in sciatic nerve and dorsal root ganglia in a mouse model of painful peripheral neuropathy.Neurosci Lett 436:210-213.
Sch?fers M,Svensson CI,Sommer C,Sorkin LS(2003)Tumor necrosis factor-alpha induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons.JNeurosci 23:2517-2521.
Sch?fers M,Geis C,Brors D,Yaksh TL,Sommer C(2002)Anterograde transport of tumor necrosis factor-alpha in the intact and injured rat sciatic nerve.J Neurosci 22:536-545.
Scheib J,H?ke A(2013)Advances in peripheral nerve regeneration.Nat Rev Neurol 9:668-676.
Seddon HJ(1942)A classification of nerve injuries.Br Med J 2:237-239.
Seltzer Z,Dubner R,Shir Y(1990)A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury.Pain 43:205-218.
Shi TJ,Cui JG,Meyerson BA,Linderoth B,Hokfelt T(1999)Regulation of galanin and neuropeptide Y in dorsal root ganglia and dorsal horn in rat mononeuropathic models:possible relation to tactile hypersensitivity.Neuroscience 93:741-757.
Shi TJ,Tandrup T,Bergman E,Xu ZQ,Ulfhake B,Hokfelt T(2001)Effect of peripheral nerve injury on dorsal root ganglion neurons in the C57 BL/6J mouse:marked changes both in cell numbers and neuropeptide expression.Neuroscience 105:249-263.
Stone LS,Vulchanova L,Riedl MS,Wang J,Williams FG,Wilcox GL,Elde R(1999)Effects of peripheral nerve injury on alpha-2Aand alpha-2C adrenergic receptor immunoreactivity in the rat spinal cord.Neuroscience 93:1399-1407.
Sun JH,Yang B,Donnelly DF,Ma C,LaMotte RH(2006)MCP-1enhances excitability of nociceptive neurons in chronically compressed dorsal root ganglia.J Neurophysiol 96:2189-2199.
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