Transplantation of Cerebral Dopamine Neurotrophic Factor Transducted BMSCs in Contusion Spinal Cord Injury of Rats: Promotion of Nerve Regeneration by Alleviating Neuroinflammation
详细信息    查看全文
  • 作者:Hua Zhao ; Lei Cheng ; Xinwen Du ; Yong Hou ; Yi Liu ; Zhaoqiang Cui…
  • 关键词:Spinal cord injury ; Cell therapy ; Bone marrow ; derived mesenchymal stem cells ; Cerebral dopamine neurotrophic factor ; Nerve regeneration ; Neuroinflammation
  • 刊名:Molecular Neurobiology
  • 出版年:2016
  • 出版时间:January 2016
  • 年:2016
  • 卷:53
  • 期:1
  • 页码:187-199
  • 全文大小:2,476 KB
  • 参考文献:1.Nashmi R, Fehlings MG (2001) Mechanisms of axonal dysfunction after spinal cord injury: with an emphasis on the role of voltage-gated potassium channels. Brain Res Brain Res Rev 38(1–2):165–191CrossRef PubMed
    2.Parr AM, Kulbatski I, Zahir T, Wang X, Yue C, Keating A, Tator CH (2008) Transplanted adult spinal cord-derived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience 155(3):760–770. doi:10.​1016/​j.​neuroscience.​2008.​05.​042 CrossRef PubMed
    3.Wright KT, El Masri W, Osman A, Chowdhury J, Johnson WE (2011) Concise review: bone marrow for the treatment of spinal cord injury: mechanisms and clinical applications. Stem Cells 29(2):169–178. doi:10.​1002/​stem.​570 CrossRef PubMed PubMedCentral
    4.Thuret S, Moon LD, Gage FH (2006) Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 7(8):628–643. doi:10.​1038/​nrn1955 CrossRef PubMed
    5.Silva NA, Sousa N, Reis RL, Salgado AJ (2014) From basics to clinical: a comprehensive review on spinal cord injury. Prog Neurobiol 114:25–57. doi:10.​1016/​j.​pneurobio.​2013.​11.​002 CrossRef PubMed
    6.Bradbury EJ, McMahon SB (2006) Spinal cord repair strategies: why do they work? Nat Rev Neurosci 7(8):644–653. doi:10.​1038/​nrn1964 CrossRef PubMed
    7.Bydon M, Lin J, Macki M, Gokaslan ZL, Bydon A (2013) The current role of steroids in acute spinal cord injury. World Neurosurg. doi:10.​1016/​j.​wneu.​2013.​02.​062
    8.Markandaya M, Stein DM, Menaker J (2012) Acute treatment options for spinal cord injury. Curr Treat Options Neurol. doi:10.​1007/​s11940-011-0162-5 PubMed
    9.Miller SM (2008) Methylprednisolone in acute spinal cord injury: a tarnished standard. J Neurosurg Anesthesiol 20(2):140–142. doi:10.​1097/​01.​ana.​0000314442.​40952.​0d CrossRef PubMed
    10.Okano H, Nakamura M, Yoshida K, Okada Y, Tsuji O, Nori S, Ikeda E, Yamanaka S, Miura K (2013) Steps toward safe cell therapy using induced pluripotent stem cells. Circ Res 112(3):523–533. doi:10.​1161/​CIRCRESAHA.​111.​256149 CrossRef PubMed
    11.Ruff CA, Fehlings MG (2010) Neural stem cells in regenerative medicine: bridging the gap. Panminerva Med 52(2):125–147PubMed
    12.Forraz N, Wright KE, Jurga M, McGuckin CP (2013) Experimental therapies for repair of the central nervous system: stem cells and tissue engineering. J Tissue Eng Regen Med 7(7):523–536. doi:10.​1002/​term.​552 CrossRef PubMed
    13.Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, El Manira A, Prockop DJ, Olson L (2002) Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci U S A 99(4):2199–2204. doi:10.​1073/​pnas.​042678299 CrossRef PubMed PubMedCentral
    14.Himes BT, Neuhuber B, Coleman C, Kushner R, Swanger SA, Kopen GC, Wagner J, Shumsky JS, Fischer I (2006) Recovery of function following grafting of human bone marrow-derived stromal cells into the injured spinal cord. Neurorehabil Neural Repair 20(2):278–296. doi:10.​1177/​1545968306286976​ CrossRef PubMed
    15.Mahmood A, Lu D, Wang L, Chopp M (2002) Intracerebral transplantation of marrow stromal cells cultured with neurotrophic factors promotes functional recovery in adult rats subjected to traumatic brain injury. J Neurotrauma 19(12):1609–1617. doi:10.​1089/​0897715027623002​65 CrossRef PubMed
    16.Ritfeld GJ, Nandoe Tewarie RD, Vajn K, Rahiem ST, Hurtado A, Wendell DF, Roos RA, Oudega M (2012) Bone marrow stromal cell-mediated tissue sparing enhances functional repair after spinal cord contusion in adult rats. Cell Transplant 21(7):1561–1575. doi:10.​3727/​096368912X640484​ CrossRef PubMed
    17.Cho SR, Kim YR, Kang HS, Yim SH, Park CI, Min YH, Lee BH, Shin JC, Lim JB (2009) Functional recovery after the transplantation of neurally differentiated mesenchymal stem cells derived from bone barrow in a rat model of spinal cord injury. Cell Transplant 18(12):1359–1368. doi:10.​3727/​096368909X475329​ CrossRef PubMed
    18.Cho JS, Park HW, Park SK, Roh S, Kang SK, Paik KS, Chang MS (2009) Transplantation of mesenchymal stem cells enhances axonal outgrowth and cell survival in an organotypic spinal cord slice culture. Neurosci Lett 454(1):43–48. doi:10.​1016/​j.​neulet.​2009.​02.​024 CrossRef PubMed
    19.Nauta AJ, Fibbe WE (2007) Immunomodulatory properties of mesenchymal stromal cells. Blood 110(10):3499–3506. doi:10.​1182/​blood-2007-02-069716 CrossRef PubMed
    20.Mei JM, Niu CS (2014) Effects of CDNF on 6-OHDA-induced apoptosis in PC12 cells via modulation of Bcl-2/Bax and caspase-3 activation. Neurol Sci. doi:10.​1007/​s10072-014-1700-1
    21.Yoon SH, Shim YS, Park YH, Chung JK, Nam JH, Kim MO, Park HC, Park SR, Min BH, Kim EY, Choi BH, Park H, Ha Y (2007) Complete spinal cord injury treatment using autologous bone marrow cell transplantation and bone marrow stimulation with granulocyte macrophage-colony stimulating factor: phase I/II clinical trial. Stem Cells 25(8):2066–2073. doi:10.​1634/​stemcells.​ 2006-0807 CrossRef PubMed
    22.Bernardo ME, Pagliara D, Locatelli F (2012) Mesenchymal stromal cell therapy: a revolution in regenerative medicine? Bone Marrow Transplant 47(2):164–171. doi:10.​1038/​bmt.​2011.​81 CrossRef PubMed
    23.Mahmood A, Lu D, Chopp M (2004) Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J Neurotrauma 21(1):33–39. doi:10.​1089/​0897715047726959​22 CrossRef PubMed
    24.Caplan AI (2009) Why are MSCs therapeutic? New data: new insight. J Pathol 217(2):318–324. doi:10.​1002/​path.​2469 CrossRef PubMed
    25.Hawryluk GW, Mothe A, Wang J, Wang S, Tator C, Fehlings MG (2012) An in vivo characterization of trophic factor production following neural precursor cell or bone marrow stromal cell transplantation for spinal cord injury. Stem Cells Dev 21(12):2222–2238. doi:10.​1089/​scd.​2011.​0596 CrossRef PubMed PubMedCentral
    26.Caplan AI (2007) Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 213(2):341–347. doi:10.​1002/​jcp.​21200 CrossRef PubMed
    27.Messmer K, Reynolds GP (2005) An in vitro model of inflammatory neurodegeneration and its neuroprotection. Neurosci Lett 388(1):39–44. doi:10.​1016/​j.​neulet.​2005.​06.​047 CrossRef PubMed
    28.Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19(8):312–318CrossRef PubMed
    29.Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS (2000) Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J Neurosci 20(16):6309–6316PubMed
    30.Hall ED, Springer JE (2004) Neuroprotection and acute spinal cord injury: a reappraisal. NeuroRx 1(1):80–100. doi:10.​1602/​neurorx.​1.​1.​80 CrossRef PubMed PubMedCentral
    31.Zhang N, Yin Y, Xu SJ, Wu YP, Chen WS (2012) Inflammation & apoptosis in spinal cord injury. Indian J Med Res 135:287–296PubMed PubMedCentral
    32.Donnelly DJ, Popovich PG (2008) Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp Neurol 209(2):378–388. doi:10.​1016/​j.​expneurol.​2007.​06.​009 CrossRef PubMed PubMedCentral
    33.Karimi-Abdolrezaee S, Billakanti R (2012) Reactive astrogliosis after spinal cord injury—beneficial and detrimental effects. Mol Neurobiol 46(2):251–264. doi:10.​1007/​s12035-012-8287-4 CrossRef PubMed
    34.Lindholm P, Voutilainen MH, Lauren J, Peranen J, Leppanen VM, Andressoo JO, Lindahl M, Janhunen S, Kalkkinen N, Timmusk T, Tuominen RK, Saarma M (2007) Novel neurotrophic factor CDNF protects and rescues midbrain dopamine neurons in vivo. Nature 448(7149):73–77. doi:10.​1038/​nature05957 CrossRef PubMed
    35.Bruhn H (2005) A short guided tour through functional and structural features of saposin-like proteins. Biochem J 389(Pt 2):249–257. doi:10.​1042/​BJ20050051 CrossRef PubMed PubMedCentral
    36.Lindstrom R, Lindholm P, Kallijarvi J, Yu LY, Piepponen TP, Arumae U, Saarma M, Heino TI (2013) Characterization of the structural and functional determinants of MANF/CDNF in drosophila in vivo model. PLoS One 8(9):e73928. doi:10.​1371/​journal.​pone.​0073928 CrossRef PubMed PubMedCentral
    37.Airavaara M, Shen H, Kuo CC, Peranen J, Saarma M, Hoffer B, Wang Y (2009) Mesencephalic astrocyte-derived neurotrophic factor reduces ischemic brain injury and promotes behavioral recovery in rats. J Comp Neurol 515(1):116–124. doi:10.​1002/​cne.​22039 CrossRef PubMed PubMedCentral
    38.Voutilainen MH, Back S, Porsti E, Toppinen L, Lindgren L, Lindholm P, Peranen J, Saarma M, Tuominen RK (2009) Mesencephalic astrocyte-derived neurotrophic factor is neurorestorative in rat model of Parkinson’s disease. J Neurosci 29(30):9651–9659. doi:10.​1523/​JNEUROSCI.​ 0833-09.​2009 CrossRef PubMed
    39.Zhao H, Cheng L, Liu Y, Zhang W, Maharjan S, Cui Z, Wang X, Tang D, Nie L (2014) Mechanisms of anti-inflammatory property of conserved dopamine neurotrophic factor: inhibition of JNK signaling in lipopolysaccharide-induced microglia. J Mol Neurosci 52(2):186–192. doi:10.​1007/​s12031-013-0120-7 CrossRef PubMed
    40.Cheng L, Zhao H, Zhang W, Liu B, Liu Y, Guo Y, Nie L (2013) Overexpression of conserved dopamine neurotrophic factor (CDNF) in astrocytes alleviates endoplasmic reticulum stress-induced cell damage and inflammatory cytokine secretion. Biochem Biophys Res Commun 435(1):34–39. doi:10.​1016/​j.​bbrc.​2013.​04.​029 CrossRef PubMed
    41.Cheng L, Liu Y, Zhao H, Zhang W, Guo YJ, Nie L (2013) Lentiviral-mediated transfer of CDNF promotes nerve regeneration and functional recovery after sciatic nerve injury in adult rats. Biochem Biophys Res Commun 440(2):330–335. doi:10.​1016/​j.​bbrc.​2013.​09.​084 CrossRef PubMed
    42.Sun ZP, Gong L, Huang SH, Geng Z, Cheng L, Chen ZY (2011) Intracellular trafficking and secretion of cerebral dopamine neurotrophic factor in neurosecretory cells. J Neurochem 117(1):121–132. doi:10.​1111/​j.​1471-4159.​2011.​07179.​x CrossRef PubMed
    43.Wu W, Zhao H, Xie B, Liu H, Chen Y, Jiao G, Wang H (2011) Implanted spike wave electric stimulation promotes survival of the bone marrow mesenchymal stem cells and functional recovery in the spinal cord injured rats. Neurosci Lett 491(1):73–78. doi:10.​1016/​j.​neulet.​2011.​01.​009 CrossRef PubMed
    44.Wu W, Lee SY, Wu X, Tyler JY, Wang H, Ouyang Z, Park K, Xu XM, Cheng JX (2014) Neuroprotective ferulic acid (FA)-glycol chitosan (GC) nanoparticles for functional restoration of traumatically injured spinal cord. Biomaterials 35(7):2355–2364. doi:10.​1016/​j.​biomaterials.​2013.​11.​074 CrossRef PubMed PubMedCentral
    45.Pearse DD, Sanchez AR, Pereira FC, Andrade CM, Puzis R, Pressman Y, Golden K, Kitay BM, Blits B, Wood PM, Bunge MB (2007) Transplantation of Schwann cells and/or olfactory ensheathing glia into the contused spinal cord: survival, migration, axon association, and functional recovery. Glia 55(9):976–1000. doi:10.​1002/​glia.​20490 CrossRef PubMed
    46.Ritfeld GJ, Rauck BM, Novosat TL, Park D, Patel P, Roos RA, Wang Y, Oudega M (2014) The effect of a polyurethane-based reverse thermal gel on bone marrow stromal cell transplant survival and spinal cord repair. Biomaterials 35(6):1924–1931. doi:10.​1016/​j.​biomaterials.​2013.​11.​062 CrossRef PubMed PubMedCentral
    47.Bolton DA, Tse AD, Ballermann M, Misiaszek JE, Fouad K (2006) Task specific adaptations in rat locomotion: runway versus horizontal ladder. Behav Brain Res 168(2):272–279. doi:10.​1016/​j.​bbr.​2005.​11.​017 CrossRef PubMed
    48.Li W, Cai WQ, Li CR (2006) Repair of spinal cord injury by neural stem cells modified with BDNF gene in rats. Neurosci Bull 22(1):34–40PubMed
    49.van den Berg ME, Castellote JM, de Pedro-Cuesta J, Mahillo-Fernandez I (2010) Survival after spinal cord injury: a systematic review. J Neurotrauma 27(8):1517–1528. doi:10.​1089/​neu.​2009.​1138 CrossRef PubMed
    50.Fitch MT, Silver J (2008) CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure. Exp Neurol 209(2):294–301. doi:10.​1016/​j.​expneurol.​2007.​05.​014 CrossRef PubMed PubMedCentral
    51.Takami T, Oudega M, Bethea JR, Wood PM, Kleitman N, Bunge MB (2002) Methylprednisolone and interleukin-10 reduce gray matter damage in the contused Fischer rat thoracic spinal cord but do not improve functional outcome. J Neurotrauma 19(5):653–666. doi:10.​1089/​0897715027537541​18 CrossRef PubMed
    52.Hausmann ON (2003) Post-traumatic inflammation following spinal cord injury. Spinal Cord 41(7):369–378. doi:10.​1038/​sj.​sc.​3101483 CrossRef PubMed
    53.Ramer LM, Ramer MS, Steeves JD (2005) Setting the stage for functional repair of spinal cord injuries: a cast of thousands. Spinal Cord 43(3):134–161. doi:10.​1038/​sj.​sc.​3101715 CrossRef PubMed
    54.Johnston H, Boutin H, Allan SM (2011) Assessing the contribution of inflammation in models of Alzheimer’s disease. Biochem Soc Trans 39(4):886–890. doi:10.​1042/​BST0390886 CrossRef PubMed
    55.Zindler E, Zipp F (2010) Neuronal injury in chronic CNS inflammation. Best Pract Res Clin Anaesthesiol 24(4):551–562. doi:10.​1016/​j.​bpa.​2010.​11.​001 CrossRef PubMed
    56.Takakuwa T, Endo S, Nakae H, Kikichi M, Inada K, Yoshida M (1994) PAF acetylhydrolase and arachidonic acid metabolite levels in patients with sepsis. Res Commun Chem Pathol Pharmacol 84(3):283–290PubMed
    57.Kwiatkoski M, Soriano RN, Araujo RM, Azevedo LU, Batalhao ME, Francescato HD, Coimbra TM, Carnio EC, Branco LG (2013) Hydrogen sulfide inhibits preoptic prostaglandin E2 production during endotoxemia. Exp Neurol 240:88–95. doi:10.​1016/​j.​expneurol.​2012.​11.​008 CrossRef PubMed
    58.Zhao H, Liu Y, Cheng L, Liu B, Zhang W, Guo YJ, Nie L (2013) Mesencephalic astrocyte-derived neurotrophic factor inhibits oxygen-glucose deprivation-induced cell damage and inflammation by suppressing endoplasmic reticulum stress in rat primary astrocytes. J Mol Neurosci 51(3):671–678. doi:10.​1007/​s12031-013-0042-4 CrossRef PubMed
    59.Hellman M, Arumae U, Yu LY, Lindholm P, Peranen J, Saarma M, Permi P (2011) Mesencephalic astrocyte-derived neurotrophic factor (MANF) has a unique mechanism to rescue apoptotic neurons. J Biol Chem 286(4):2675–2680. doi:10.​1074/​jbc.​M110.​146738 CrossRef PubMed PubMedCentral
    60.Schiwy N, Brazda N, Muller HW (2009) Enhanced regenerative axon growth of multiple fibre populations in traumatic spinal cord injury following scar-suppressing treatment. Eur J Neurosci 30(8):1544–1553. doi:10.​1111/​j.​1460-9568.​2009.​06929.​x CrossRef PubMed
    61.Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, Bunge MB (2002) Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 22(15):6670–6681PubMed
    62.Guest JD, Herrera L, Margitich I, Oliveria M, Marcillo A, Casas CE (2008) Xenografts of expanded primate olfactory ensheathing glia support transient behavioral recovery that is independent of serotonergic or corticospinal axonal regeneration in nude rats following spinal cord transection. Exp Neurol 212(2):261–274. doi:10.​1016/​j.​expneurol.​2008.​03.​010 CrossRef PubMed
    63.Kubasak MD, Jindrich DL, Zhong H, Takeoka A, McFarland KC, Munoz-Quiles C, Roy RR, Edgerton VR, Ramon-Cueto A, Phelps PE (2008) OEG implantation and step training enhance hindlimb-stepping ability in adult spinal transected rats. Brain 131(Pt 1):264–276. doi:10.​1093/​brain/​awm267 PubMed PubMedCentral
    64.Lu J, Feron F, Ho SM, Mackay-Sim A, Waite PM (2001) Transplantation of nasal olfactory tissue promotes partial recovery in paraplegic adult rats. Brain Res 889(1–2):344–357CrossRef PubMed
    65.Deumens R, Koopmans GC, Honig WM, Maquet V, Jerome R, Steinbusch HW, Joosten EA (2006) Limitations in transplantation of astroglia-biomatrix bridges to stimulate corticospinal axon regrowth across large spinal lesion gaps. Neurosci Lett 400(3):208–212. doi:10.​1016/​j.​neulet.​2006.​02.​050 CrossRef PubMed
    66.Martin D, Robe P, Franzen R, Delree P, Schoenen J, Stevenaert A, Moonen G (1996) Effects of Schwann cell transplantation in a contusion model of rat spinal cord injury. J Neurosci Res 45(5):588–597. doi:10.​1002/​(SICI)1097-4547(19960901)45:​5<588:​:​AID-JNR8>3.​0.​CO;2-8 CrossRef PubMed
  • 作者单位:Hua Zhao (1) (2)
    Lei Cheng (1)
    Xinwen Du (3)
    Yong Hou (1)
    Yi Liu (1) (2)
    Zhaoqiang Cui (2)
    Lin Nie (1)

    1. Department of Spine Surgery, Qilu Hospital of Shandong University, 250012, Jinan, China
    2. Shandong University Qilu Hospital Research Center for Cell Therapy, Key Laboratory of Cardiovascular Remodeling and Function Research, Qilu Hospital of Shandong University, Jinan, China
    3. Department of Pediatric Surgery, Laizhou People’s Hospital, Laizhou, China
  • 刊物主题:Neurosciences; Neurobiology; Cell Biology; Neurology;
  • 出版者:Springer US
  • ISSN:1559-1182
文摘
Traumatic spinal cord injury (SCI) causes neuron death and axonal damage resulting in functional motor and sensory loss, showing limited regeneration because of adverse microenvironment such as neuroinflammation and glial scarring. Currently, there is no effective therapy to treat SCI in clinical practice. Bone marrow-derived mesenchymal stem cells (BMSCs) are candidates for cell therapies but its effect is limited by neuroinflammation and adverse microenvironment in the injured spinal cord. In this study, we developed transgenic BMSCs overexpressing cerebral dopamine neurotrophic factor (CDNF), a secretory neurotrophic factor that showed potent effects on neuron protection, anti-inflammation, and sciatic nerve regeneration in previous studies. Our results showed that the transplantation of CDNF-BMSCs suppressed neuroinflammation and decreased the production of proinflammatory cytokines after SCI, resulting in the promotion of locomotor function and nerve regeneration of the injured spinal cord. This study presents a novel promising strategy for the treatment of spinal cord injury.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700