Transplantation of CX3CL1-expressing Mesenchymal Stem Cells Provides Neuroprotective and Immunomodulatory Effects in a Rat Model of Retinal Degeneration

References

• Xu W, Xu GX. Mesenchymal stem cells for retinal diseases. Int J Ophthalmol. 2011;4:413–421
   PubMed Web of Science ®Google Scholar
• Quevedo HC, Hatzistergos KE, Oskouei BN, et al. Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity. Proc Natl Acad Sci U S A. 2009;106:14022–14027
   PubMed Web of Science ®Google Scholar
• Johnson TV, Bull ND, Hunt DP, et al. Neuroprotective effects of intravitreal mesenchymal stem cell transplantation in experimental glaucoma. Invest Ophthalmol Vis Sci. 2010;51:2051–2059
   PubMed Web of Science ®Google Scholar
• Kassis I, Grigoriadis N, Gowda-Kurkalli B, et al. Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Arch Neurol. 2008;65:753–761
   PubMed Web of Science ®Google Scholar
• Inoue Y, Iriyama A, Ueno S, et al. Subretinal transplantation of bone marrow mesenchymal stem cells delays retinal degeneration in the RCS rat model of retinal degeneration. Exp Eye Res. 2007;85:234–241
   PubMed Web of Science ®Google Scholar
• Li N, Li XR, Yuan JQ. Effects of bone-marrow mesenchymal stem cells transplanted into vitreous cavity of rat injured by ischemia/reperfusion. Graefes Arch Clin Exp Ophthalmol. 2009;247:503–514
   PubMed Web of Science ®Google Scholar
• Wang S, Lu B, Girman S, et al. Non-invasive stem cell therapy in a rat model for retinal degeneration and vascular pathology. PLOS ONE. 2010;5:e9200
   PubMed Web of Science ®Google Scholar
• Tasso R, Augello A, Boccardo S, et al. Recruitment of a host’s osteoprogenitor cells using exogenous mesenchymal stem cells seeded on porous ceramic. Tissue Eng Part A. 2009;15:2203–2212
   PubMed Web of Science ®Google Scholar
• Al JMA, Abumaree MH. The immunomodulatory and neuroprotective effects of mesenchymal stem cells (MSCs) in experimental autoimmune encephalomyelitis (EAE): a model of multiple sclerosis (MS). Int J Mol Sci. 2012;13:9298–9331
   PubMed Web of Science ®Google Scholar
• Tasso R, Ilengo C, Quarto R, et al. Mesenchymal stem cells induce functionally active T-regulatory lymphocytes in a paracrine fashion and ameliorate experimental autoimmune uveitis. Invest Ophthalmol Vis Sci. 2012;53:786–793
   PubMed Web of Science ®Google Scholar
• Zhang Y, Wang W. Effects of bone marrow mesenchymal stem cell transplantation on light-damaged retina. Invest Ophthalmol Vis Sci. 2010;51:3742–3748
   PubMed Web of Science ®Google Scholar
• Zhang M, Xu G, Liu W, et al. Role of fractalkine/CX3CR1 interaction in light-induced photoreceptor degeneration through regulating retinal microglial activation and migration. PLOS ONE. 2012;7:e35446
   Web of Science ®Google Scholar
• Karlstetter M, Ebert S, Langmann T. Microglia in the healthy and degenerating retina: insights from novel mouse models. Immunobiology. 2010;215:685–691
   PubMed Web of Science ®Google Scholar
• Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci. 2007;10:1387–1394
   PubMed Web of Science ®Google Scholar
• Silverman MD, Zamora DO, Pan Y, et al. Constitutive and inflammatory mediator-regulated fractalkine expression in human ocular tissues and cultured cells. Invest Ophthalmol Vis Sci. 2003;44:1608–1615
   PubMed Web of Science ®Google Scholar
• Juel HB, Faber C, Udsen MS, et al. Chemokine expression in retinal pigment epithelial ARPE-19 cells in response to coculture with activated T cells. Invest Ophthalmol Vis Sci. 2012;53:8472–8480
   PubMed Web of Science ®Google Scholar
• Harrison JK, Jiang Y, Chen S, et al. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci U S A. 1998;95:10896–10901
   PubMed Web of Science ®Google Scholar
• Honczarenko M, Le Y, Swierkowski M, et al. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells. 2006;24:1030–1041
   PubMed Web of Science ®Google Scholar
• Cardona AE, Pioro EP, Sasse ME, et al. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci. 2006;9:917–924
   PubMed Web of Science ®Google Scholar
• Chandrasekar B, Mummidi S, Perla RP, et al. Fractalkine (CX3CL1) stimulated by nuclear factor kappaB (NF-kappaB)-dependent inflammatory signals induces aortic smooth muscle cell proliferation through an autocrine pathway. Biochem J. 2003;373:547–558
   PubMed Web of Science ®Google Scholar
• Clark AK, Staniland AA, Malcangio M. Fractalkine/CX3CR1 signalling in chronic pain and inflammation. Curr Pharm Biotechnol. 2011;12:1707–1714
   PubMed Web of Science ®Google Scholar
• Combadiere C, Feumi C, Raoul W, et al. CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J Clin Invest. 2007;117:2920–2928
   PubMed Web of Science ®Google Scholar
• Chen J, Connor KM, Smith LE. Overstaying their welcome: defective CX3CR1 microglia eyed in macular degeneration. J Clin Invest. 2007;117:2758–2762
   PubMed Web of Science ®Google Scholar
• Lin JQ, Lin CZ, Lin XZ, et al. Construction of a bicistronic recombinant adenoviral vector for human interleukin-10 and enhanced green fluorescent protein expression in bone marrow mesenchymal stem cells. Chin Med J (Engl). 2012;125:102–108
   PubMed Web of Science ®Google Scholar
• Gong L, Wu Q, Song B, et al. Differentiation of rat mesenchymal stem cells transplanted into the subretinal space of sodium iodate-injected rats. Clin Exp Ophthalmol. 2008;36:666–671
   PubMed Web of Science ®Google Scholar
• Harper MM, Grozdanic SD, Blits B, et al. Transplantation of BDNF-secreting mesenchymal stem cells provides neuroprotection in chronically hypertensive rat eyes. Invest Ophthalmol Vis Sci. 2011;52:4506–4515
   PubMed Web of Science ®Google Scholar
• Harada T, Harada C, Kohsaka S, et al. Microglia-Muller glia cell interactions control neurotrophic factor production during light-induced retinal degeneration. J Neurosci. 2002;22:9228–9236
   PubMed Web of Science ®Google Scholar
• Graeber MB, Streit WJ, Kiefer R, et al. New expression of myelomonocytic antigens by microglia and perivascular cells following lethal motor neuron injury. J Neuroimmunol. 1990;27:121–132
   Google Scholar
• Deans RJ, Moseley AB. Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol. 2000;28:875–884
   PubMed Web of Science ®Google Scholar
• Wenzel A, Grimm C, Samardzija M, Reme CE. Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog Retin Eye Res. 2005;24:275–306
   PubMed Web of Science ®Google Scholar
• Lund RD, Wang S, Lu B, et al. Cells isolated from umbilical cord tissue rescue photoreceptors and visual functions in a rodent model of retinal disease. Stem Cells. 2007;25:602–611
   PubMed Web of Science ®Google Scholar
• Yu S, Tanabe T, Dezawa M, et al. Effects of bone marrow stromal cell injection in an experimental glaucoma model. Biochem Biophys Res Commun. 2006;344:1071–1079
   PubMed Web of Science ®Google Scholar
• Pisati F, Bossolasco P, Meregalli M, et al. Induction of neurotrophin expression via human adult mesenchymal stem cells: implication for cell therapy in neurodegenerative diseases. Cell Transplant. 2007;16:41–55
   PubMed Web of Science ®Google Scholar
• Arnhold S, Heiduschka P, Klein H, et al. Adenovirally transduced bone marrow stromal cells differentiate into pigment epithelial cells and induce rescue effects in RCS rats. Invest Ophthalmol Vis Sci. 2006;47:4121–4129
   PubMed Web of Science ®Google Scholar
• Levkovitch-Verbin H, Sadan O, Vander S, et al. Intravitreal injections of neurotrophic factors secreting mesenchymal stem cells are neuroprotective in rat eyes following optic nerve transection. Invest Ophthalmol Vis Sci. 2010;51:6394–6400
   PubMed Web of Science ®Google Scholar
• Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol. 2008;8:726–736
   PubMed Web of Science ®Google Scholar
• Giunti D, Parodi B, Usai C, et al. Mesenchymal stem cells shape microglia effector functions through the release of CX3CL1. Stem Cells. 2012;30:2044–2053
   PubMed Web of Science ®Google Scholar
• Kim YJ, Park HJ, Lee G, et al. Neuroprotective effects of human mesenchymal stem cells on dopaminergic neurons through anti-inflammatory action. Glia. 2009;57:13–23
   PubMed Web of Science ®Google Scholar
• Zhou C, Zhang C, Chi S, et al. Effects of human marrow stromal cells on activation of microglial cells and production of inflammatory factors induced by lipopolysaccharide. Brain Res. 2009;1269:23–30
   PubMed Web of Science ®Google Scholar
• Bazan JF, Bacon KB, Hardiman G, et al. A new class of membrane-bound chemokine with a CX3C motif. Nature. 1997;385:640–644
   PubMed Web of Science ®Google Scholar
• Re DB, Przedborski S. Fractalkine: moving from chemotaxis to neuroprotection. Nat Neurosci. 2006;9:859–861
   PubMed Web of Science ®Google Scholar
• Raoul W, Keller N, Rodero M, et al. Role of the chemokine receptor CX3CR1 in the mobilization of phagocytic retinal microglial cells. J Neuroimmunol. 2008;198:56–61
   PubMed Web of Science ®Google Scholar
• Sasahara M, Otani A, Oishi A, et al. Activation of bone marrow-derived microglia promotes photoreceptor survival in inherited retinal degeneration. Am J Pathol. 2008;172:1693–1703
   PubMed Web of Science ®Google Scholar
• Hosoda L, Adachi-Usami E, Mizota A, et al. Early effects of sodium iodate injection on ERG in mice. Acta Ophthalmol (Copenh). 1993;71:616–622
   PubMed Web of Science ®Google Scholar
• Harper MM, Adamson L, Blits B, et al. Brain-derived neurotrophic factor released from engineered mesenchymal stem cells attenuates glutamate- and hydrogen peroxide-mediated death of staurosporine-differentiated RGC-5 cells. Exp Eye Res. 2009;89:538–548
   PubMed Web of Science ®Google Scholar
• Park HY, Kim JH, Sun KH, Park CK. Stem cell-based delivery of brain-derived neurotrophic factor gene in the rat retina. Brain Res. 2012;1469:10–23
   PubMed Web of Science ®Google Scholar
• Xin H, Sun R, Kanehira M, et al. Intratracheal delivery of CX3CL1-expressing mesenchymal stem cells to multiple lung tumors. Mol Med. 2009;15:321–327
   PubMed Web of Science ®Google Scholar
• Xin H, Kanehira M, Mizuguchi H, et al. Targeted delivery of CX3CL1 to multiple lung tumors by mesenchymal stem cells. Stem Cells. 2007;25:1618–1626
   PubMed Web of Science ®Google Scholar