Lentiviral vector delivery of short hairpin RNA to NG2 and neurotrophin-3 promotes locomotor recovery in injured rat spinal cord

References

• Dietz V, Curt A. Neurological aspects of spinal cord repair: promises and challenges. Lancet Neurol. 2006;5:688–94.
   PubMed Web of Science ®Google Scholar
• Houle JD, Tessler A. Repair of chronic spinal cord injury. Exp Neurol. 2003;182:247–60.
   PubMed Web of Science ®Google Scholar
• Hulsebosch CE. Recent advances in pathophysiology and treatment of spinal cord injury. Adv Physiol Edu. 2002;26: 238–55.
   PubMed Web of Science ®Google Scholar
• Zai LJ, Yoo S, Wrathall JR. Increased growth factor expression and cell proliferation after contusive spinal cord injury. Brain Res. 2005;1052:147–55.
   PubMed Web of Science ®Google Scholar
• Rudge JS, Silver J. Inhibition of neurite outgrowth on astroglial scars in vitro. J Neurosci. 1990;10:3594–603.
   PubMed Web of Science ®Google Scholar
• Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci. 2004;24:2143–55.
   PubMed Web of Science ®Google Scholar
• McKeon RJ, Schreiber RC, Rudge JS, Silver J. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci. 1991;11:3398–411.
   PubMed Web of Science ®Google Scholar
• Bradbury EJ, McMahon SB, Ramer MS. Keeping in touch: sensory neurone regeneration in the CNS. Trends Pharmacol Sci. 2000;21:389–94.
   PubMed Web of Science ®Google Scholar
• Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, . Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 2002;416: 636–40.
   PubMed Web of Science ®Google Scholar
• Bu J, Akhtar N, Nishiyama A. Transient expression of the NG2 proteoglycan by a subpopulation of activated macrophages in an excitotoxic hippocampal lesion. Glia. 2001;34:296–310.
   PubMed Web of Science ®Google Scholar
• Ughrin YM, Chen ZJ, Levine JM. Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J Neurosci. 2003;23:175–86.
   PubMedGoogle Scholar
• Tan AM, Colletti M, Rorai AT, Skene JH, Levine JM. Antibodies against the NG2 proteoglycan promote the regeneration of sensory axons within the dorsal columns of the spinal cord. J Neurosci. 2006;26:4729–39.
   PubMed Web of Science ®Google Scholar
• Jones LL, Margolis RU, Tuszynski MH. The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan and versican are differentially regulated following spinal cord injury. Exp Neurol. 2003;182:399–411.
   PubMed Web of Science ®Google Scholar
• Jones LL, Sajed D, Tuszynski MH. Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J Neurosci. 2003;23:9276–88.
   PubMed Web of Science ®Google Scholar
• Hossain-Ibrahim MK, Rezajooi K, Stallcup WB, Lieberman AR, Anderson PN. Analysis of axonal regeneration in the central and peripheral nervous systems of the NG2-deficient mouse. BMC Neurosci. 2007;8:1–22.
   PubMedGoogle Scholar
• McTigue DM, Tripathi R, Wei P. NG2 colocalizes with axons and is expressed by a mixed cell population in spinal cord lesions. J Neuropath Exp Neurol. 2006;65:406–20.
   PubMedGoogle Scholar
• Harper SQ, Staber PD, He X, Eliason SL, Martins IH, Mao Q, . RNA interference improves motor and neuropathological abnormalities in a Huntington's disease mouse model. Proc Natl Acad Sci USA. 2005;102:5820–5.
   PubMed Web of Science ®Google Scholar
• Singer O, Marr RA, Rockenstein E. Targeting BACE1 with siRNAs ameliorates Alzheimer disease neuropathology in a transgenic model. Nature Neurosci. 2005;8:1343–9.
   PubMed Web of Science ®Google Scholar
• Donnelly EM, Strappe PM, McGinley LM, Madigan NN, Geurts E, Rooney GE, . Lentiviral vector-mediated knockdown of the neuroglycan 2 proteoglycan or expression of neurotrophin-3 promotes neurite outgrowth in a cell culture model of the glial scar. J Gene Med. 2010;12: 863–72.
   PubMedGoogle Scholar
• Tessarollo L, Tsoulfas P, Martin-Zanca D, Gilbert DJ, Jenkins NA, Copeland NG, Parada LF. trkC, a receptor for neurotrophin-3, is widely expressed in the developing nervous system and in non-neuronal tissues. Development. 1993;118:463–75.
   PubMedGoogle Scholar
• Williams R, Backstrom A, Kullander K, Hallbook F, Ebendal T. Developmentally regulated expression of mRNA for neurotrophin high-affinity (trk) receptors within chick trigeminal sensory neurons. Eur J Neurosci. 1995;7:116–28.
   PubMedGoogle Scholar
• Hari A, Djohar B, Skutella T, Montazeri S. Neurotrophins and extracellular matrix molecules modulate sensory axon outgrowth. Int J Develop Neurosci. 2004;22:113–7.
   PubMed Web of Science ®Google Scholar
• Alto LT, Havton LA, Conner JM, Hollis IER, Blesch A, Tuszynski MH. Chemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury. Nature Neurosci. 2009;12:1106–13.
   PubMed Web of Science ®Google Scholar
• Grill R, Murai K, Blesch A, Gage FH, Tuszynski MH. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J Neurosci. 1997;17:5560–72.
   PubMed Web of Science ®Google Scholar
• Hory-Lee F, Russell M, Lindsay RM, Frank E. Neurotrophin 3 supports the survival of developing muscle sensory neurons in culture. Proc Natl Acad Sci USA. 1993;90:2613–7.
   PubMed Web of Science ®Google Scholar
• Massey JM, Amps J, Viapiano MS, Matthews RT, Wagoner MR, Whitaker CM, . Increased chondroitin sulfate proteoglycan expression in denervated brainstem targets following spinal cord injury creates a barrier to axonal regeneration overcome by chondroitinase ABC and neurotrophin-3. Exp Neurol. 2008;209:426–45.
   PubMed Web of Science ®Google Scholar
• Ramer MS, Bishop T, Dockery P, Mobarak MS, O’Leary D, Fraher JP, . Neurotrophin-3-mediated regeneration and recovery of proprioception following dorsal rhizotomy. Mol Cell Neurosci. 2002;19:239–49.
   PubMed Web of Science ®Google Scholar
• Zhou L, Baumgartner BJ, Hill-Felberg SJ, McGowen LR, Shine HD. Neurotrophin-3 expressed in situ induces axonal plasticity in the adult injured spinal cord. J Neurosci. 2003;23:1424–31.
   PubMed Web of Science ®Google Scholar
• Blits B, Dijkhuizen PA, Boer GJ, Verhaagen J. Intercostal nerve implants transduced with an adenoviral vector encoding neurotrophin-3 promote regrowth of injured rat corticospinal tract fibers and improve hindlimb function. Exp Neurol. 2000;164:25–37.
   PubMedGoogle Scholar
• Bradbury EJ, Khemani S, King VR, Priestley JV, McMahon SB. NT-3 promotes growth of lesioned adult rat sensory axons ascending in the dorsal columns of the spinal cord. Eur J Neurosci. 1999;11:3873–83.
   PubMedGoogle Scholar
• Galtrey CM, Asher RA, Nothias F, Fawcett JW. Promoting plasticity in the spinal cord with chondroitinase improves functional recovery after peripheral nerve repair. Brain. 2007;130:926–39.
   PubMedGoogle Scholar
• Ikegami T, Nakamura M, Yamane J, Katoh H, Okada S, Iwanami A, . Chondroitinase ABC combined with neural stem/progenitor cell transplantation enhances graft cell migration and outgrowth of growth-associated protein-43-positive fibers after rat spinal cord injury. Eur J Neurosci. 2005;22:3036–46.
   PubMed Web of Science ®Google Scholar
• Schnell L, Schneider R, Kolbeck R, Barde Y-A, Schwab ME. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature. 1994;367:170–3.
   PubMed Web of Science ®Google Scholar
• de Castro R Jr, Tajrishi R, Claros J, Stallcup WB. Differential responses of spinal axons to transection: influence of the NG2 proteoglycan. Exp Neurol. 2005;192: 299–309.
   PubMed Web of Science ®Google Scholar
• Jones LL, Sajed D, Tuszynski MH. Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J Neurosci. 2003;23:9276–88.
   PubMed Web of Science ®Google Scholar
• Silver J, Miller JH. Regeneration beyond the glial scar. Nature Rev Neurosci. 2004;5:146–56.
   PubMed Web of Science ®Google Scholar
• Rolls A, Shechter R, Schwartz M. The bright side of the glial scar in CNS repair. Nature Rev Neurosci. 2009;10: 235–41.
   PubMed Web of Science ®Google Scholar
• Giulian D, Woodward J, Young D, Krebs J, Lachman L. Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization. J Neurosci. 1988;8: 2485–90.
   PubMed Web of Science ®Google Scholar
• Nishino A, Suzuki M, Ohtani H, Motohashi O, Umezawa K, Nagura H, Yoshimoto T. Thrombin may contribute to the pathophysiology of central nervous system injury. J Neurotrauma. 1993;10:167–79.
   PubMedGoogle Scholar
• Winter CG, Saotome Y, Levison SW, Hirsh D. A role for ciliary neurotrophic factor as an inducer of reactive gliosis, the glial response to central nervous system injury. Proc Natl Acad Sci USA. 1995;92:5865–9.
   PubMedGoogle Scholar
• Elkabes S, DiCicco-Bloom E, Black I. Brain microglia/ macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci. 1996;16:2508–21.
   PubMed Web of Science ®Google Scholar
• Rabchevsky AG, Streit WJ. Role of microglia in postinjury repair and regeneration of the CNS. Mental Retard Develop Disabilities Res Rev. 1998;4:187–92.
   Google Scholar
• Fitch MT, Doller C, Combs CK, Landreth GE, Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J Neurosci. 1999;19:8182–98.
   PubMed Web of Science ®Google Scholar
• Fitch MT, Silver J. Activated macrophages and the blood–brain barrier: inflammation after CNS injury leads to increases in putative inhibitory molecules. Exp Neurol. 1997;148:587–603.
   PubMed Web of Science ®Google Scholar