Co-transplantation of olfactory ensheathing glia and mesenchymal stromal cells does not have synergistic effects after spinal cord injury in the rat

References

• Verdu E, Garcia-Alias G, Fores J, Gudino-Cabrera G, Muneton VC, Nieto-Sampedro M, . Effects of ensheathing cells transplanted into photochemically damaged spinal cord. Neuroreport. 2001;12:2303–9.
   Google Scholar
• Ramer LM, Au E, Richter MW, Liu J, Tetzlaff W, Roskams AJ. Peripheral olfactory ensheathing cells reduce scar and cavity formation and promote regeneration after spinal cord injury. J Comp Neurol. 2004;473:1–15.
   PubMed Web of Science ®Google Scholar
• Takami T, Oudega M, Bates ML, Woo PM, Kleitman N, Bunge MB. Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci. 2002;22:6670–81.
   PubMed Web of Science ®Google Scholar
• Lakatos A, Barnett, SC, Franklin JM. Olfactory ensheathing cells induce less host astrocyte response and chondroitin sulphate proteoglycan expression than Schwann cells following transplantation into adult CNS white matter. Exp Neurol. 2003;184:237–46.
   PubMed Web of Science ®Google Scholar
• Ramon-Cueto A, Avila J. Olfactory ensheathing glia: properties and function. Brain Res Bull. 1998;46:175–87.
   PubMed Web of Science ®Google Scholar
• Woodhall E, West AK, Chuah MI. Cultured olfactory ensheathing cells express nerve growth factor, brain-derived neurotrophic factor, glia cell line-derived neurotrophic factor and their receptors. Mol Brain Res. 2001;88:203–13.
   PubMedGoogle Scholar
• Au E, Roskams AJ. Olfactory ensheathing cells of the lamina propria in vivo and in vitro. Glia. 2003;41:224–36.
   PubMedGoogle Scholar
• Rojas-Mayorquin AE, Torres-Ruiz NM, Orituno-Sahagun D, Gudino-Cabrera G. Microarray analysis of striatal embryonic stem cells induced to differentiate by ensheathing cell conditioned media. Dev Dyn. 2008;237:979–94.
   Google Scholar
• Ramon-Cueto A, Nieto-Sampedro M. Regeneration into the spinal cord of transected dorsal root axons is promoted by ensheathing glia transplants. Exp Neurol. 1994;127:232–44.
   PubMed Web of Science ®Google Scholar
• Au E, Richter MW, Tetzlaff W, Aebersold R, Sage EH, Roskams AJ. SPARC from olfactory ensheathing cells stimulates Schwann cells to promote neurite outgrowth and enhances spinal cord repair. J Neurosci. 2007;27:7208–21.
   PubMed Web of Science ®Google Scholar
• Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol. 2007;213:341–7.
   PubMed Web of Science ®Google Scholar
• Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem. 2006;93:1076–84.
   Google Scholar
• Opydo-Canek M. Bone marrow stromal cells in traumatic brain injury therapy: true perspective or false hope? Acta Neurobiol Exp. 2007;67:187–95.
   Google Scholar
• Chen L, Tredget EE, Wu PYG, Wu Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PloS One. 2008;3:e1886.
   PubMed Web of Science ®Google Scholar
• Dasari VR, Spomar DG, Cady C, Gujrati M, Rao JS, Dinh DH. Mesenchymal stem cells from rat bone marrow downregulate caspase-3-mediated apoptotic pathway after spinal cord injury in rats. Neurochem Res. 2007;32:2080–93.
   PubMed Web of Science ®Google Scholar
• Ucelli A, Moretta L, Pistoia V. Immunoregulatory function of mesenchymal stem cells. Eur J Immunol. 2006;36:2566–73.
   Google Scholar
• Pedemonte E, Benvenuto F, Casazza S, Mancardi G, Oksenberg JR, Uccelli A, . The molecular signature of therapeutic mesenchymal stem cells exposes the architecture of the hematopoietic stem cell niche synapse. BMC Genomics. 2007;8:65.
   PubMedGoogle Scholar
• Sykova E, Jendelova P. In vivo tracking of stem cells in brain and spinal cord injury. Prog Brain Res. 2007;161:367–83.
   PubMed Web of Science ®Google Scholar
• Urdzikova L, Jendelova P, Glogarova K, Burian M, Hajek M, Sykova E. Transplantation of bone marrow stem cells as well as mobilization by granulocyte-colony stimulating factor promotes recovery after spinal cord injury in rats. J Neurotrauma. 2006;23:1379–91.
   PubMed Web of Science ®Google Scholar
• Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, Manira AE, Prockop DJ, . Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci USA. 2002;99:2199–204.
   PubMed Web of Science ®Google Scholar
• Vanicky I, Urdzikova L, Saganova K, Cizkova D, Galik J. A simple and reproducible model of spinal cord injury induced by epidural balloon inflation in the rat. J Neurotrauma. 2001;18:1399–407.
   PubMed Web of Science ®Google Scholar
• Sedy J, Urdzikova L, Likavcanova K, Hejcl A, Jendelova P, Sykova Y. A new model of severe neurogenic pulmonary edema in spinal cord injured rat. Neurosci Lett. 2007;423:167–71.
   PubMed Web of Science ®Google Scholar
• Bianco JI, Perry C, Harkin DG, Mackay-Sim A, Feron F. Neurotrophin 3 promotes purification and proliferation of olfactory ensheathing cells from human nose. Glia. 2004;45:111–23.
   PubMed Web of Science ®Google Scholar
• Woodhall E, West AK, Vickers AK, Chuah MI. Olfactory ensheathing cell phenotype following implantation in the lesioned spinal cord. Cell Mol Life Sci. 2003;60:2241–53.
   Google Scholar
• Azizi SA, Stokes D, Augelli BJ, Digirolamo C, Prockop DJ. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats: similarities to astrocyte grafts. Proc Natl Acad Sci USA. 1998;95:3908–18.
   PubMed Web of Science ®Google Scholar
• Imaizumi T, Lankford KL, Kocsis JD. Transplantation of olfactory ensheathing cells or Schwann cells restores rapid and secure conduction across the transected spinal cord. Brain Res. 2000;854:70–8.
   Google Scholar
• Li X, Dancausse H, Grijalva I, Oliveira M, Levi DO. Labeling Schwann cells with CFSE: an in vitro and in vivo study. J Neurosci Methods. 2003;125:83–91.
   PubMed Web of Science ®Google Scholar
• Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. Green mice as a source of ubiquitous green cells. FASEB Lett. 1977;407:313–9.
   Google Scholar
• Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma. 1995;12:1–12.
   PubMed Web of Science ®Google Scholar
• Sykova E, Homola A, Mazanec R, Lachman H, Konradova SL, Kobylka P, . Autologous bone marrow transplantation in patients with subacute and chronic spinal cord injury. Cell Transplant. 2006;15:675–87.
   PubMed Web of Science ®Google Scholar
• Parr AM, Kulbatski I, Tator CH. Transplantation of adult rat spinal cord stem/progenitor cells for spinal cord injury. J Neurotrauma. 2007;24:835–45.
   PubMed Web of Science ®Google Scholar
• Park E, Velumian AA, Fehlings MG. The role of excitatoxicity in secondary mechanisms of spinal cord injury: a review with an emphasis on the implications for white matter degeneration. J Neurotrauma. 2004;21:754–74.
   PubMed Web of Science ®Google Scholar
• Rowland JW, Hawryluk GWJ, Kwon B, Fehlings MG. Current status of acute spinal cord injury pathophysiology and emerging therapies: promise on the horizon. Neurosurg Focus. 2008;25[5]:e2.
   Google Scholar
• Rolls A, Shechter R, Londong A, Segev Y, Jacob-Hirsch J, Amariglio N, . Two faces of chondroitin sulfate proteoglycan in spinal cord repair: a role in microglia/macrophage activation. PLoS Med. 2008;5:e171.
   PubMed Web of Science ®Google Scholar
• Morino T, Ogata T, Horiuchi H, Takeba J, Okumura H, Miyazaki T, . Delayed neuronal dagame related to microglia proliferation after mild spinal cord compression injury. Neurosci Res. 2003;46:309–18.
   Google Scholar
• Richter MW, Fletcher PA, Liu J, Tetzlaff W, Roskams AJ. Lamina propria and olfactory bulb ensheathing cells exhibit differential integration and migration and promote differential axon sprouting in the lesioned spinal cord. J Neurosci. 2005;25:10700–11.
   Google Scholar
• Uccelli A, Pistia V, Moretta L. Mesenchymal stem cells: a new strategy for immunosuppression? Trends Immunol. 2007;28:219–26.
   PubMed Web of Science ®Google Scholar
• Sordi V, Malosio ML, Marchesi, F, Mercalli A, Melzi R, Giordano T, . Bone marrow mesenchymal cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 2005;106:419–27.
   PubMed Web of Science ®Google Scholar
• Lu P, Yang H, Culbertson M, Graham L, Roskams AJ, Tuszynski MH. Olfactory ensheathing cells do not exhibit unique migratory or axonal growth-promoting properties after spinal cord injury. J Neurosci. 2006;26:11120–30.
   PubMed Web of Science ®Google Scholar
• Su Z, Cao L, Zhu Y, Liu X, Huang Z, Huang A, . Nogo enhances the adhesion of olfactory ensheathing cells and inhibits their migration. J Cell Sci. 2007;120:1877–87.
   PubMedGoogle Scholar
• Dubreuil CI, Winton MJ, McKerracher L. Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system. J Cell Biol. 2003;162:233–43.
   PubMed Web of Science ®Google Scholar
• Madura T, Yamashita T, Kubo T. Activation of Rho in the injured axons following spinal cord injury. EMBO Rep. 2004;5:412–7.
   PubMed Web of Science ®Google Scholar
• Meriane M, Duhamel S, Lejeune L, Galipeau J, Annabi B, . Cooperation of matrix metalloproteinases with the RhoA/Rho kinase and mitogen-activated protein kinase kinase-1/extracellular signal-regulated kinase signaling pathways is required for the sphingosine-1-phosphate-induced mobilization of marrow-derived stromal cells. Stem Cells. 2006;24:2557–65.
   PubMedGoogle Scholar
• Jaganathan BG, Ruester B, Dressel L, Stein S, Grez M, Seifried E, . Rho inhibition induces migration of mesenchymal stromal cells. Stem Cells. 2007;25:1966–74.
   PubMed Web of Science ®Google Scholar
• McKerracher L, Higuchi H. Targeting Rho to stimulate repair after spinal cord injury. J Neurotrauma. 2006;23:309–17.
   PubMed Web of Science ®Google Scholar
• Fouad K, Pedersen V, Schwab ME. Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr Biol. 2001;11:1766–70.
   PubMed Web of Science ®Google Scholar
• Deumens R, Koopmans GC, Joosten EAJ. Regeneration of descending axon tracts spinal cord injury. Prog Neurobiol. 2005;77:57–89.
   Google Scholar
• Steward O, Zheng B, Tessier-Lavigne M, Hofstdter M, Sharp K, Yee KM. Regeneration beyond the glial scar. J Neurosci. 2008;28:6836–47.
   Google Scholar
• Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME. The injured spinal cord spontaneously forms a new intraspinal circuits in adult rats. Nat Neurosci. 2004;7:269–77.
   PubMed Web of Science ®Google Scholar
• Courtine G, Song B, Roy RR, Zhong H, Hermann JE, Ao Y, . Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat Med. 2008;14:69–74.
   PubMed Web of Science ®Google Scholar
• Oria M, Chatauret N, Raguer N, Cordoba J. A new method for measuring motor evoked potentials in the awake rat: effects of anesthetics. J Neurotrauma. 2008;25:266–75.
   Google Scholar
• Ondrejcak T, Vanicky I, Galik J, Saganova K. Chronically implanted electrodes for repeated stimulation and recording of spinal cord potentials. J Neurosci Methods. 2005;141:125–34.
   PubMed Web of Science ®Google Scholar
• Smith HC, Savic G, Frankel HL, Ellawa PH, Maskill DW, Jamous MA, . Corticospinal function studied over time following incomplete spinal cord injury. Spinal Cord. 2000;38:292–300.
   PubMed Web of Science ®Google Scholar
• Fehlings MG, Tator CH. The relationships among the severity of spinal cord injury, residual neurological function, axon counts, and counts of retrogradely labeled neurons after experimental spinal cord injury. Exp Neurol. 1995;132:220–8.
   PubMed Web of Science ®Google Scholar
• Totoiu MO, Keirstead HS. Spinal cord injury is accompanied by chronic progressive demyelination. J Comp Neurol. 2005;486:373–83.
   PubMed Web of Science ®Google Scholar
• Siegenthaler MM, Tu MK, Keirstead HS. The extent of myelin pathology differs following contusion and transection spinal cord injury. J Neurotrauma. 2007;24:1631–46.
   Google Scholar
• Franklin RJM. Remyelination by transplanted olfactory ensheathing cells. Anat Rec B New Anat. 2003;271:71–6.
   PubMedGoogle Scholar
• Boyd JG, Doucette R, Kawaja MD. Defining the role of the olfactory ensheathing cells in facilitating axon remyelination following damage to the spinal cord. FASEB J. 2005;19:694–703.
   PubMed Web of Science ®Google Scholar
• Raineteau O, Schwab ME. Plasticity of motor systems after incomplete spinal cord injury. Nat Rev Neurosci. 2001;2:263–73.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Ringden O. Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med. 2007;262:509–25.
   PubMed Web of Science ®Google Scholar
• Firouzi M, Mashayedi P, Saberi H, Mobasheri H, Abolhassani F, Jahanzad I, . Transplantation of Schwann cells to subarachnoid space induces repair in contused rat spinal cord. Neurosci Lett. 2006;402:66–70.
   PubMed Web of Science ®Google Scholar
• Lin CR, Wu PC, Shih HC, Cheng JT, Lu CY, Chou AK, . Intrathecal spinal progenitor cell transplantation for the treatment of neurotrophic pain. Cell Transplant. 2002;11:17–24.
   PubMed Web of Science ®Google Scholar
• Ohta M, Suzuki Y, Noda T, Ejiri Y, Dezawa M, Kataoka K, . Bone marrow stromal infused into the cerebrospinal fluid promote functional recovery of the injured rat spinal cord with reduced cavity formation. Exp Neurol. 2004;187:266–78.
   PubMed Web of Science ®Google Scholar
• Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, . Multilineage potential of adult human mesenchymal stem cells. Science. 1998;284:143–7.
   Google Scholar
• Lu P, Blesch A, Tuszynski MH. Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artifact? J Neurosci Res. 2004;77:174–91.
   Google Scholar
• Krabbe C, Zimmer J, Meyer M. Neural trasndifferentiation of mesenchymal stem cells: a critical review. APMIS. 2005;113:831–44.
   PubMedGoogle Scholar
• Ross JJ, Verfaillie CM. Evaluation of neural plasticity in adult stem cells. Philos Trans R Sco Lond B Biol Sci. 2008;363:199–205.
   Google Scholar