Astrocytes and Microglia-Mediated Immune Response in Maladaptive Plasticity is Differently Modulated by NGF in the Ventral Horn of the Spinal Cord Following Peripheral Nerve Injury

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• 作者：Ciro De Luca ; Leonilde Savarese…
• 关键词：Glial cells ; Maladaptive plasticity ; NGF ; Spinal cord
• 刊名：Cellular and Molecular Neurobiology
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：36
• 期：1
• 页码：37-46
• 全文大小：3,933 KB
• 参考文献：Blits B, Oudega M, Boer GJ, Bartlett Bunge M, Verhaagen J (2003) Adeno-associated viral vector-mediated neurotrophin gene transfer in the injured adult rat spinal cord improves hind-limb function. Neuroscience 118(1):271–281PubMed CrossRef
  Bruno MA, Cuello AC (2006) Activity-dependent release of precursor nerve growth factor, conversion to mature nerve growth factor, and its degradation by a protease cascade. Proc Natl Acad Sci USA 103(17):6735–6740PubMed PubMedCentral CrossRef
  Carulli D, Foscarin S, Faralli A, Pajaj E, Rossi F (2013) Modulation of semaphorin3A in perineuronal nets during structural plasticity in the adult cerebellum. Mol Cell Neurosci 57:10–22PubMed CrossRef
  Cavaliere C, Cirillo G, Rosaria Bianco M, Rossi F, De Novellis V, Maione S, Papa M (2007) Gliosis alters expression and uptake of spinal glial amino acid transporters in a mouse neuropathic pain model. Neuron Glia Biol 3(2):141–153PubMed CrossRef
  Cirillo G, Cavaliere C, Bianco MR, De Simone A, Colangelo AM, Sellitti S, Alberghina L, Papa M (2010) Intrathecal NGF administration reduces reactive astrocytosis and changes neurotrophin receptors expression pattern in a rat model of neuropathic pain. Cell Mol Neurobiol 30(1):51–62PubMed CrossRef
  Cirillo G, Bianco MR, Colangelo AM, Cavaliere C, de Daniele L, Zaccaro L, Alberghina L, Papa M (2011) Reactive astrocytosis-induced perturbation of synaptic homeostasis is restored by nerve growth factor. Neurobiol Dis 41(3):630–639PubMed CrossRef
  Cirillo G, Colangelo AM, Bianco MR, Cavaliere C, Zaccaro L, Sarmientos P, Alberghina L, Papa M (2012) BB14, a Nerve Growth Factor (NGF)-like peptide shown to be effective in reducing reactive astrogliosis and restoring synaptic homeostasis in a rat model of peripheral nerve injury. Biotechnol Adv 30(1):223–232PubMed CrossRef
  Cirillo G, Colangelo AM, Berbenni M, Ippolito VM, De Luca C, Verdesca F, Savarese L, Alberghina L, Maggio N, Papa M (2014) Purinergic modulation of spinal neuroglial maladaptive plasticity following peripheral nerve injury. Mol Neurobiol. doi:10.​1007/​s12035-014-8943-y
  Cobianchi S, Casals-Diaz L, Jaramillo J, Navarro X (2013) Differential effects of activity dependent treatments on axonal regeneration and neuropathic pain after peripheral nerve injury. Exp Neurol 240:157–167PubMed CrossRef
  Coderre TJ, Melzack R (1992) The contribution of excitatory amino acids to central sensitization and persistent nociception after formalin-induced tissue injury. J Neurosci 12(9):3665–3670PubMed
  Colangelo AM, Bianco MR, Vitagliano L, Cavaliere C, Cirillo G, De Gioia L, Diana D, Colombo D, Redaelli C, Zaccaro L, Morelli G, Papa M, Sarmientos P, Alberghina L, Martegani E (2008) A new nerve growth factor-mimetic peptide active on neuropathic pain in rats. J Neurosci 28(11):2698–2709PubMed CrossRef
  Colangelo AM, Cirillo G, Lavitrano ML, Alberghina L, Papa M (2012) Targeting reactive astrogliosis by novel biotechnological strategies. Biotechnol Adv 30(1):261–271PubMed CrossRef
  Corvetti L, Rossi F (2005) Degradation of chondroitin sulfate proteoglycans induces sprouting of intact purkinje axons in the cerebellum of the adult rat. J Neurosci 25(31):7150–7158PubMed CrossRef
  Cullheim S, Thams S (2007) The microglial networks of the brain and their role in neuronal network plasticity after lesion. Brain Res Rev 55(1):89–96PubMed CrossRef
  Davis-López de Carrizosa MA, Morado-Díaz CJ, Tena JJ, Benítez-Temiño B, Pecero ML, Morcuende SR, de la Cruz RR, Pastor AM (2009) Complementary actions of BDNF and neurotrophin-3 on the firing patterns and synaptic composition of motoneurons. J Neurosci 29(2):575–587PubMed CrossRef
  Decosterd I, Woolf CJ (2000) Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87(2):149–158PubMed CrossRef
  Foscarin S, Ponchione D, Pajaj E, Leto K, Gawlak M, Wilczynski GM, Rossi F, Carulli D (2011) Experience-dependent plasticity and modulation of growth regulatory molecules at central synapses. PLoS One 6(1):e16666PubMed PubMedCentral CrossRef
  Gordon T, You S, Cassar SL, Tetzlaff W (2015) Reduced expression of regeneration associated genes in chronically axotomized facial motoneurons. Exp Neurol 264:26–32PubMed CrossRef
  Haftel VK, Bichler EK, Wang QB, Prather JF, Pinter MJ, Cope TC (2005) Central suppression of regenerated proprioceptive afferents. J Neurosci 25(19):4733–4742PubMed CrossRef
  Hua X, Malarkey EB, Sunjara V, Rosenwald SE, Li WH, Parpura V (2004) Ca(2+)-dependent glutamate release involves two classes of endoplasmic reticulum Ca(2+) stores in astrocytes. J Neurosci Res 76:86–97PubMed CrossRef
  Kwok JC, Dick G, Wang D, Fawcett JW (2011) Extracellular matrix and perineuronal nets in CNS repair. Dev Neurobiol 71(11):1073–1089PubMed CrossRef
  Liu H, Xu H, Yu T, Yao J, Zhao C, Yin ZQ (2013) Expression of perineuronal nets, parvalbumin and protein tyrosine phosphatase σ in the rat visual cortex during development and after BFD. Curr Eye Res 38(10):1083–1094PubMed CrossRef
  Lüscher C, Malenka RC (2012) NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol 4(6):a005710. doi:10.​1101/​cshperspect.​a005710
  Massey JM, Hubscher CH, Wagoner MR, Decker JA, Amps J, Silver J, Onifer SM (2006) Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J Neurosci 26(16):4406–4414PubMed CrossRef
  McRae PA, Rocco MM, Kelly G, Brumberg JC, Matthews RT (2007) Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J Neurosci 27(20):5405–5413PubMed CrossRef
  Meisner JG, Marsh AD, Marsh DR (2010) Loss of GABAergic interneurons in laminae I–III of the spinal cord dorsal horn contributes to reduced GABAergic tone and neuropathic pain after spinal cord injury. J Neurotrauma 27(4):729–737PubMed CrossRef
  Milligan ED, Watkins LR (2009) Pathological and protective roles of glia in chronic pain. Nat Rev Neurosci 10(1):23–36PubMed PubMedCentral CrossRef
  Molteni R, Zheng JQ, Ying Z, Gómez-Pinilla F, Twiss JL (2004) Voluntary exercise increases axonal regeneration from sensory neurons. Proc Natl Acad Sci USA 101(22):8473–8478PubMed PubMedCentral CrossRef
  Morris GP, Clark IA, Zinn R, Vissel B (2013) Microglia: a new frontier for synaptic plasticity, learning and memory, and neurodegenerative disease research. Neurobiol Learn Mem 105:40–53PubMed CrossRef
  Murdock BJ, Bender DE, Segal BM, Feldman EL (2015) The dual roles of immunity in ALS: injury overrides protection. Neurobiol Dis 77:1–12PubMed CrossRef
  Novikov LN, Novikova LN, Holmberg P, Kellerth J (2000) Exogenous brain-derived neurotrophic factor regulates the synaptic composition of axonally lesioned and normal adult rat motoneurons. Neuroscience 100(1):171–181PubMed CrossRef
  Papa M, De Luca C, Petta F, Alberghina L, Cirillo G (2014) Astrocyte-neuron interplay in maladaptive plasticity. Neurosci Biobehav Rev 42:35–54PubMed CrossRef
  Raineteau O, Schwab ME (2001) Plasticity of motor systems after incomplete spinal cord injury. Nat Rev Neurosci 2(4):263–273PubMed CrossRef
  Schwab ME, Strittmatter SM (2014) Nogo limits neural plasticity and recovery from injury. Curr Opin Neurobiol 27:53–60PubMed CrossRef
  Su H, Zhang W, Guo J, Guo A, Yuan Q, Wu W (2009) Neural progenitor cells enhance the survival and axonal regeneration of injured motoneurons after transplantation into the avulsed ventral horn of adult rats. J Neurotrauma 26(1):67–80PubMed CrossRef
  Svensson M, Eriksson P, Persson JK, Molander C, Arvidsson J, Aldskogius H (1993) The response of central glia to peripheral nerve injury. Brain Res Bull 30(3–4):499–506PubMed CrossRef
  Takahashi-Iwanaga H, Murakami T, Abe K (1998) Three-dimensional microanatomy of perineuronal proteoglycan nets enveloping motor neurons in the rat spinal cord. J Neurocytol 27(11):817–827PubMed CrossRef
  Verkhratsky A, Kirchhoff F (2007) Glutamate-mediated neuronal-glial transmission. J Anat 210(6):651–660PubMed PubMedCentral CrossRef
  Wang D, Ichiyama RM, Zhao R, Andrews MR, Fawcett JW (2011) Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J Neurosci 31(25):9332–9344PubMed CrossRef
  
• 作者单位：Ciro De Luca (1)
  Leonilde Savarese (1) (3)
  Anna Maria Colangelo (2) (3)
  Maria Rosaria Bianco (1)
  Giovanni Cirillo (1)
  Lilia Alberghina (2) (3)
  Michele Papa (1) (3)
  
  1. Laboratory of Neuronal Networks, Department of Mental and Physical Health and Preventive Medicine, Second University of Naples, Via L. Armanni, 5, 80138, Naples, Italy
  3. SYSBIO, Centre of Systems Biology, University of Milano-Bicocca, Milan, Italy
  2. Laboratory of Neuroscience “R. Levi-Montalcini”, Department of Biotechnology and Biosciences, University of Milano-Bicocca, Milan, Italy
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Neurosciences
  Animal Anatomy, Morphology and Histology
  
• 出版者：Springer Netherlands
• ISSN：1573-6830

文摘

Reactive astrocytes and activated microglia are the key players in several pathophysiologic modifications of the central nervous system. We used the spared nerve injury (SNI) of the sciatic nerve to induce glial maladaptive response in the ventral horn of lumbar spinal cord and examine its role in the remodeling of the tripartite synapse plasticity. Imaging the ventral horn revealed that SNI was associated with both an early microglial and astrocytic activation, assessed, respectively, by analysis of Iba1 and GFAP expression. Microglia, in particular, localized peculiarly surrounding the motor neurons somata. Perineuronal astrocytes, which play a key role in maintaining the homeostasis of neuronal circuitry, underwent a substantial phenotypic change following peripheral axotomy, producing reactive gliosis. The gliosis was associated with the reduction of glial aminoacid transporters (GLT1 and GlyT1) and increase of neuronal glutamate transporter EAAC1. Although the expression of GABAergic neuronal marker GAD65/67 showed no change, glutamate increase, as demonstrated by HPLC analysis, shifted the excitatory/inhibitory balance as showed by the net increase of the glutamate/GABA ratio. Moreover, endogenous NGF levels were altered in SNI animals and not restored by the intrathecal NGF administration. This treatment reverted phenotypic changes associated with reactive astrocytosis, but failed to modify microglia activation. These findings on one hand confirm the correlation between gliopathy and maladaptive plasticity of the spinal synaptic circuitry, on the other hand add new data concerning the complex peculiar behavior of different glial cells in neuronal degenerative processes, defining a special role of microglia in sustaining the inflammatory response. Keywords Glial cells Maladaptive plasticity NGF Spinal cord