In vitro evidence for impaired neuroprotective capacities of adult mesenchymal stem cells derived from a rat model of familial amyotrophic lateral sclerosis (hSOD1G93A)

Experimental Neurology

Volumn 212, Issue 2, 2008, Pages 557-561

  Boucherie, Cédric ^a,b   Caumont, Anne Sophie ^a   Maloteaux, Jean Marie ^a   Hermans, Emmanuel ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b European Graduate School for Neuroscience EURON   (Netherlands)

Author keywords

Amyotrophic lateral sclerosis; Astrocytes; Glial derived neurotrophic factor; Glutamate; Mesenchymal stem cells; Riluzole

Indexed keywords

ASPARTIC ACID; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR; RILUZOLE; VESICULAR GLUTAMATE TRANSPORTER 1;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; AUTOLOGOUS STEM CELL TRANSPLANTATION; BONE MARROW; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; DEGENERATIVE DISEASE; IN VITRO STUDY; MESENCHYMAL STEM CELL; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT STRAIN; UPREGULATION;

AMINO ACID TRANSPORT SYSTEM X-AG; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HUMANS; MESENCHYMAL STEM CELLS; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; RILUZOLE; SUPEROXIDE DISMUTASE;

EID: 47349083335     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.04.030     Document Type: Article

References (31)

1. Azizi S.A., Stokes D., Augelli B.J., DiGirolamo C., and Prockop D.J. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats - similarities to astrocyte grafts. Proc. Nat. Acad. Sci. U. S. A. 95 (1998) 3908-3913
2. Bendotti C., Atzori C., Piva R., Tortarolo M., Strong M.J., DeBiasi S., and Migheli A. Activated p38MAPK is a novel component of the intracellular inclusions found in human amyotrophic lateral sclerosis and mutant SOD1 transgenic mice. J. Neuropathol. Exp. Neurol. 63 (2004) 113-119
3. Boillee S., Yamanaka K., Lobsiger C.S., Copeland N.G., Jenkins N.A., Kassiotis G., Kollias G., and Cleveland D.W. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312 (2006) 1389-1392
4. Caumont A.S., Octave J.N., and Hermans E. Specific regulation of rat glial cell line-derived neurotrophic factor gene expression by riluzole in C6 glioma cells. J. Neurochem. 97 (2006) 128-139
5. Chen J., Li Y., Wang L., Zhang Z., Lu D., Lu M., and Chopp M. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 32 (2001) 1005-1011
6. Chi L., Ke Y., Luo C., Li B., Gozal D., Kalyanaraman B., and Liu R. Motor neuron degeneration promotes neural progenitor cell proliferation, migration, and neurogenesis in the spinal cords of amyotrophic lateral sclerosis mice. Stem Cells 24 (2006) 34-43
7. Cizkova D., Rosocha J., Vanicky I., Jergova S., and Cizek M. Transplants of Human Mesenchymal Stem Cells Improve Functional Recovery After Spinal Cord Injury in the Rat. Cell. Mol. Neurobiol. 26 (2006) 1167-1180
8. Clement A.M., Nguyen M.D., Roberts E.A., Garcia M.L., Boillee S., Rule M., McMahon A.P., Doucette W., Siwek D., Ferrante R.J., Brown Jr. R.H., Julien J.P., Goldstein L.S., and Cleveland D.W. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302 (2003) 113-117
9. Corti S., Locatelli F., Donadoni C., Guglieri M., Papadimitriou D., Strazzer S., Del Bo R., and Comi G.P. Wild-type bone marrow cells ameliorate the phenotype of SOD1-G93A ALS mice and contribute to CNS, heart and skeletal muscle tissues. Brain 127 (2004) 1-15
10. de Hemptinne I., Vermeiren C., Maloteaux J.M., and Hermans E. Induction of glial glutamate transporters in adult mesenchymal stem cells. J. Neurochem. 91 (2004) 155-166
11. de Hemptinne I., Boucherie C., Pochet R., Bantubungi K., Schiffmann S.N., Maloteaux J.M., and Hermans E. Unilateral induction of progenitors in the spinal cord of hSOD1(G93A) transgenic rats correlates with an asymmetrical hind limb paralysis. Neurosci. Lett. 401 (2006) 25-29
12. Dowd E., Monville C., Torres E.M., Wong L.F., Azzouz M., Mazarakis N.D., and Dunnett S.B. Lentivector-mediated delivery of GDNF protects complex motor functions relevant to human Parkinsonism in a rat lesion model. Eur. J. Neurosci. 22 (2005) 2587-2595
13. Erie E.A., Shim H., Smith A.L., Lin X., Keyvanfar K., Xie C., Chen J., and Cai H. Mice deficient in the ALS2 gene exhibit lymphopenia and abnormal hematopietic function. J. Neuroimmunol. 182 (2007) 226-231
14. Hisaoka K., Nishida A., Koda T., Miyata M., Zensho H., Morinobu S., Ohta M., and Yamawaki S. Antidepressant drug treatments induce glial cell line-derived neurotrophic factor (GDNF) synthesis and release in rat C6 glioblastoma cells. J. Neurochem. 79 (2001) 25-34
15. Howland D.S., Liu J., She Y., Goad B., Maragakis N.J., Kim B., Erickson J., Kulik J., DeVito L., Psaltis G., DeGennaro L.J., Cleveland D.W., and Rothstein J.D. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl. Acad. Sci. U. S. A 99 (2002) 1604-1609
16. Jiang Y., Jahagirdar B.N., Reinhardt R.L., Schwartz R.E., Keene C.D., Ortiz-Gonzalez X.R., Reyes M., Lenvik T., Lund T., Blackstad M., Du J., Aldrich S., Lisberg A., Low W.C., Largaespada D.A., and Verfaillie C.M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418 (2002) 41-49
17. Kopen G.C., Prockop D.J., and Phinney D.G. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Nat. Acad. Sci. U. S. A. 96 (1999) 10711-10716
18. Li L., Wu W., Lin L.F., Lei M., Oppenheim R.W., and Houenou L.J. Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 9771-9775
19. Liu Z., and Martin L.J. The adult neural stem and progenitor cell niche is altered in amyotrophic lateral sclerosis mouse brain. J. Comp. Neurol. 497 (2006) 468-488
20. Maric D., Maric I., Chang Y.H., and Barker J.L. Prospective cell sorting of embryonic rat neural stem cells and neuronal and glial progenitors reveals selective effects of basic fibroblast growth factor and epidermal growth factor on self-renewal and differentiation. J. Neurosci. 23 (2003) 240-251
21. McBride J.L., Ramaswamy S., Gasmi M., Bartus R.T., Herzog C.D., Brandon E.P., Zhou L., Pitzer M.R., Berry-Kravis E.M., and Kordower J.H. Viral delivery of glial cell line-derived neurotrophic factor improves behavior and protects striatal neurons in a mouse model of Huntington's disease. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 9345-9350
22. Mizuta I., Ohta M., Ohta K., Nishimura M., Mizuta E., and Kuno S. Riluzole stimulates nerve growth factor, brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor synthesis in cultured mouse astrocytes. Neurosci. Lett. 310 (2001) 117-120
23. Nagai M., Re D.B., Nagata T., Chalazonitis A., Jessell T.M., Wichterle H., and Przedborski S. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat. Neurosci. 10 (2007) 615-622
24. Rothstein J.D., Van Kammen M., Levey A.I., Martin L.J., and Kuncl R.W. Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann. Neurol. 38 (1995) 73-84
25. Rothstein J.D., DykesHoberg M., Pardo C.A., Bristol L.A., Jin L., Kuncl R.W., Kanai Y., Hediger M.A., Wang Y.F., Schielke J.P., and Welty D.F. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16 (1996) 675-686
26. Rothstein J.D., Patel S., Regan M.R., Haenggeli C., Huang Y.H., Bergles D.E., Jin L., Dykes H.M., Vidensky S., Chung D.S., Toan S.V., Bruijn L.I., Su Z.Z., Gupta P., and Fisher P.B. Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 433 (2005) 73-77
27. Tortarolo M., Veglianese P., Calvaresi N., Botturi A., Rossi C., Giorgini A., Migheli A., and Bendotti C. Persistent activation of p38 mitogen-activated protein kinase in a mouse model of familial amyotrophic lateral sclerosis correlates with disease progression. Mol. Cell. Neurosci. 23 (2003) 180-192
28. Trotti D., Aoki M., Pasinelli P., Berger U.V., Danbolt N.C., Brown R.H., and Hediger M.A. Amyotrophic lateral sclerosis-linked glutamate transporter mutant has impaired glutamate clearance capacity. J. Biol. Chem. 276 (2001) 576-582
29. Van Damme P., Dewil M., Robberecht W., and Van Den B.L. Excitotoxicity and amyotrophic lateral sclerosis. Neurodegener. Dis. 2 (2005) 147-159
30. Vanhoutte N., de Hemptinne I., Vermeiren C., Maloteaux J.M., and Hermans E. In vitro differentiated neural stem cells express functional glial glutamate transporters. Neurosci. Lett. 370 (2004) 230-235
31. Wang L.J., Lu Y.Y., Muramatsu S., Ikeguchi K., Fujimoto K., Okada T., Mizukami H., Matsushita T., Hanazono Y., Kume A., Nagatsu T., Ozawa K., and Nakano I. Neuroprotective effects of glial cell line-derived neurotrophic factor mediated by an adeno-associated virus vector in a transgenic animal model of amyotrophic lateral sclerosis. J. Neurosci. 22 (2002) 6920-6928