Systemic transplantation of c-kit+ cells exerts a therapeutic effect in a model of amyotrophic lateral sclerosis

Human Molecular Genetics

Volumn 19, Issue 19, 2010, Pages 3782-3796

  Corti, Stefania ^a   Nizzardo, Monica ^a   Nardini, Martina ^a   Donadoni, Chiara ^a   Salani, Sabrina ^a   Simone, Chiara ^a   Falcone, Marianna ^a   Riboldi, Giulietta ^a   Govoni, Alessandra ^a   Bresolin, Nereo ^a,b   Comi, Giacomo P ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b SCIENTIFIC INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; STEM CELL FACTOR; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; LIFESPAN; MALE; MOTONEURON; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; STEM CELL TRANSPLANTATION; TRANSGENIC MOUSE;

AMINO ACID TRANSPORT SYSTEM X-AG; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BIOLOGICAL ASSAY; BLOOD VESSELS; BONE MARROW CELLS; CELL DEATH; CELL SEPARATION; CELL SURVIVAL; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; EXTRACELLULAR SPACE; GLUTAMATES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MOTOR NEURONS; MUTANT PROTEINS; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-KIT; STEM CELL TRANSPLANTATION; SUPEROXIDE DISMUTASE; SURVIVAL ANALYSIS;

MUS;

EID: 77956524950     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq293     Document Type: Article

References (58)

1. Bruijn, L.I., Miller, T.M. and Cleveland, D.W. (2004) Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci., 27, 723-749.
2. Rosen, D.R., Siddique, T., Patterson, D., Figlewicz, D.A., Sapp, P., Hentati, A., Donaldson, D., Goto, J., O'Regan, J.P., Deng, H.X. et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature, 362, 59-62.
3. Pasinelli, P. and Brown, R.H. (2006) Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat. Rev. Neurosci., 7, 710-723.
4. Greenway, M.J., Andersen, P.M., Russ, C., Ennis, S., Cashman, S., Donaghy, C., Patterson, V., Swingler, R., Kieran, D., Prehn, J. et al. (2006) ANG mutations segregate with familial and 'sporadic' amyotrophic lateral sclerosis. Nat. Genet., 38, 411-413.
5. Kabashi, E., Valdmanis, P.N., Dion, P., Spiegelman, D., McConkey, B.J., Vande Velde, C., Bouchard, J.P., Lacomblez, L., Pochigaeva, K., Salachas, F. et al. (2008) TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet., 40, 572-574.
6. Kwiatkowski, T.J. Jr, Bosco, D.A., Leclerc, A.L., Tamrazian, E., Vanderburg, C.R., Russ, C., Davis, A., Gilchrist, J., Kasarskis, E.J., Munsat, T. et al. (2009) Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science, 323, 1205-1208.
7. Maruyama, H., Morino, H., Ito, H., Izumi, Y., Kato, H., Watanabe, Y., Kinoshita, Y., Kamada, M., Nodera, H., Suzuki, H. et al. (2010) Mutations of optineurin in amyotrophic lateral sclerosis. Nature, 465, 223-226.
8. Gurney, M.E., Pu, H., Chiu, A.Y., Dal Canto, M.C., Polchow, C.Y., Alexander, D.D., Caliendo, J., Hentati, A., Kwon, Y.W., Deng, H.X. et al. (1994) Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science, 264, 1772-1775.
9. Nagai, M., Aoki, M., Miyoshi, I., Kato, M., Pasinelli, P., Kasai, N., Brown, R.H. Jr and Itoyama, Y. (2001) Rats expressing human cytosolic copper-zinc superoxide dismutase transgenes with amyotrophic lateral sclerosis: associated mutations develop motor neuron disease. J. Neurosci., 21, 9246-9254.
10. Yamanaka, K., Boillee, S., Roberts, E.A., Garcia, M.L., McAlonis-Downes, M., Mikse, O.R., Cleveland, D.W. and Goldstein, L.S. (2008) Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice. Proc. Natl Acad. Sci. USA, 105, 7594-7599.
11. McGeer, P.L. and McGeer, E.G. (2002) Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve, 26, 459-470.
12. Rothstein, J.D., Dykes-Hoberg, M., Pardo, C.A., Bristol, L.A., Jin, L., Kuncl, R.W., Kanai, Y., Hediger, M.A., Wang, Y., Schielke, J.P. et al. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron, 16, 675-686.
13. Clement, A.M., Nguyen, M.D., Roberts, E.A., Garcia, M.L., Boillée, S., Rule, M., McMahon, A.P., Doucette, W., Siwek, D., Ferrante, R.J. et al. (2003) Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science, 302, 113-117.
14. Boillée, S., Yamanaka, K., Lobsiger, C.S., Copeland, N.G., Jenkins, N.A., Kassiotis, G., Kollias, G. and Cleveland, D.W. (2006) Onset and progression in inherited ALS determined by motor neurons and microglia. Science, 312, 1389-1392.
15. Yamanaka, K., Chun, S.J., Boillee, S., Fujimori-Tonou, N., Yamashita, H., Gutmann, D.H., Takahashi, R., Misawa, H. and Cleveland, D.W. (2008) Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat. Neurosci., 11, 251-253.
16. Corti, S., Locatelli, F., Donadoni, C., Guglieri, M., Papadimitriou, D., Strazzer, S., Del Bo, R. and Comi, G.P. (2004) Wild-type bone marrow cells ameliorate the phenotype of SOD1-G93A ALS mice and contribute to CNS, heart and skeletal muscle tissues. Brain, 127, 2518-2532.
17. Beers, D.R., Henkel, J.S., Xiao, Q., Zhao, W., Wang, J., Yen, A.A., Siklos, L., McKercher, S.R. and Appel, S.H. (2006) Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA, 103, 16021-16026.
18. Solomon, J.N., Lewis, C.A., Ajami, B., Corbel, S.Y., Rossi, F.M. and Krieger, C. (2006) Origin and distribution of bone marrow-derived cells in the central nervous system in a mouse model of amyotrophic lateral sclerosis. Glia, 53, 744-753.
19. Di Giorgio, F.P., Carrasco, M.A., Siao, M.C., Maniatis, T. and Eggan, K. (2007) Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat. Neurosci., 10, 608-614.
20. Di Giorgio, F.P., Boulting, G.L., Bobrowicz, S. and Eggan, K.C. (2008) Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation. Cell Stem Cell, 3, 637-648.
21. Nagai, M., Re, D.B., Nagata, T., Chalazonitis, A., Jessell, T.M., Wichterle, H. and Przedborski, S. (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat. Neurosci., 10, 615-622.
22. Marchetto, M.C., Muotri, A.R., Mu, Y., Smith, A.M., Cezar, G.G. and Gage, F.H. (2008) Non-cell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell Stem Cell, 3, 649-657.
23. Saxena, S., Cabuy, E. and Caroni, P. (2009) A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat. Neurosci., 12, 627-636.
24. Jaarsma, D., Teuling, E., Haasdijk, E.D., De Zeeuw, C.I. and Hoogenraad, C.C. (2008) Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. J. Neurosci., 28, 2075-2088.
25. Ikuta, K. and Weissman, I.L. (1992) Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc. Natl Acad. Sci., 89, 1502-1506.
26. Kabrun, N., Bühring, H.J., Choi, K., Ullrich, A., Risau, W. and Keller, G. (1997) Flk-1 expression defines a population of early embryonic hematopoietic precursors. Development, 124, 2039-2048.
27. Nishikawa, S.I., Nishikawa, S., Hirashima, M., Matsuyoshi, N. and Kodama, H. (1998) Progressive lineage analysis by cell sorting and culture identifies FLK1 + VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development, 125, 1747-1757.
28. Rafii, S. and Lyden, D. (2003) Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat. Med., 9, 702-712.
29. Lacaud, G., Keller, G. and Kouskoff, V. (2004) Tracking mesoderm formation and specification to the hemangioblast in vitro. Trends Cardiovasc. Med., 14, 314-317.
30. Anversa, P., Kajstura, J. and Leri, A. (2007) If I can stop one heart from breaking. Circulation, 115, 829-832.
31. Lepore, A.C., Rauck, B., Dejea, C., Pardo, A.C., Rao, M.S., Rothstein, J.D. and Maragakis, N.J. (2008) Focal transplantation-based astrocyte replacement is neuroprotective in a model of motor neuron disease. Nat. Neurosci., 11, 1294-1301.
32. Maragakis, N.J. and Rothstein, J.D. (2004) Glutamate transporters: animal models to neurologic disease. Neurobiol. Dis., 15, 461-473.
33. Fazel, S., Cimini, M., Chen, L., Li, S., Angoulvant, D., Fedak, P., Verma, S., Weisel, R.D., Keating, A. and Li, R.K. (2006) Cardioprotective c-kit+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J. Clin. Invest., 116, 1865-1877.
34. Federici, T. and Boulis, N.M. (2006) Gene-based treatment of motor neuron diseases. Muscle Nerve, 33, 302-323.
35. Androutsellis-Theotokis, A., Rueger, M.A., Park, D.M., Mkhikian, H., Korb, E., Poser, S.W., Walbridge, S., Munasinghe, J., Koretsky, A.P., Lonser, R.R. et al. (2009) Targeting neural precursors in the adult brain rescues injured dopamine neurons. Proc. Natl Acad. Sci. USA, 106, 13570-13575.
36. Kim, H., Lee, J.M., Park, J.S., Jo, S.A., Kim, Y.O., Kim, C.W. and Jo, I. (2008) Dexamethasone coordinately regulates angiopoietin-1 and VEGF: a mechanism of glucocorticoid-induced stabilization of blood-brain barrier. Biochem. Biophys. Res. Commun., 372, 243-248.
37. Zhong, Z., Deane, R., Ali, Z., Parisi, M., Shapovalov, Y., O'Banion, M.K., Stojanovic, K., Sagare, A., Boillee, S., Cleveland, D.W. et al. (2008) ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat. Neurosci., 11, 420-422.
38. Rothstein, J.D., Jin, L., Dykes-Hoberg, M. and Kuncl, R.W. (1993) Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc. Natl Acad. Sci. USA, 90, 6591-6595.
39. Henkel, J.S., Beers, D.R., Zhao, W. and Appel, S.H. (2009) Microglia in ALS: the good, the bad, and the resting. J. Neuroimmune Pharmacol., 4, 389-398.
40. Weber, U.J., Bock, T., Buschard, K. and Pakkenberg, B. (1997) Total number and size distribution of motor neurons in the spinal cord of normal and EMC-virus infected mice-a stereological study. J. Anat., 191, 347-353.
41. Oyanagi, K., Ikuta, F. and Horikawa, Y. (1989) Evidence for sequential degeneration of the neurons in the intermediate zone of the spinal cord in amyotrophic lateral sclerosis: a topographic and quantitative investigation. Acta Neuropathol., 77, 343-349.
42. Berger, U.V. and Hediger, M.A. (2006) Distribution of the glutamate transporters GLT1 (SLC1A2) and GLAST (SLC1A3) in peripheral organs. Anat. Embryol., 211, 595-606.
43. Ohnishi, S., Ito, H., Suzuki, Y., Adachi, Y., Wate, R., Zhang, J., Nakano, S., Kusaka, H. and Ikehara, S. (2009) Intra-bone marrow-bone marrow transplantation slows disease progression and prolongs survival in G93A mutant SOD1 transgenic mice, an animal model mouse for amyotrophic lateral sclerosis. Brain Res., 1296, 216-224.
44. Papadeas, S.T., Kraig, S.E., O'Banion, C., Lepore, A.C. and Maragakis, N.J. (2009) Mutant SOD1-specific influences on glial biology in ALS Neuroscience Meeting Chicago. Soc. Neurosci., 631.21/L25.
45. Noda, S., Ichikawa, H. and Miyoshi, H. (2009) Hematopoietic stem cell aging is associated with functional decline and delayed cell cycle progression. Biochem. Biophys. Res. Commun., 383, 210-215.
46. Lunn, J.S., Hefferan, M.P., Marsala, M. and Feldman, E.L. (2009) Stem cells: comprehensive treatments for amyotrophic lateral sclerosis in conjunction with growth factor delivery. Growth Factors, 27, 133-140.
47. Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T. and Nishimune, Y. (1997) 'Green mice' as a source of ubiquitous green cells. FEBS Lett., 407, 313-319.
48. Corti, S., Locatelli, F., Papadimitriou, D., Donadoni, C., Del Bo, R., Crimi, M., Bordoni, A., Fortunato, F., Strazzer, S., Menozzi, G. et al. (2006) Transplanted ALDHhiSSClo neural stem cells generate motor neurons and delay disease progression of nmd mice, an animal model of SMARD1. Hum. Mol. Genet., 15, 167-187.
49. Huard, C., Moisset, P.A., Dicaire, A., Merly, F., Tardif, F., Asselin, I. and Tremblay, J.P. (1998) Transplantation of dermal fibroblasts expressing MyoD1 in mouse muscles. Biochem. Biophys. Res. Commun., 248, 648-654.
50. Gundersen, H.J. (1988) The nucleator. J. Microsc., 151, 3-21.
51. Messina, A., Sangster, C.L., Morrison, W.A. and Galea, M.P. (2000) Requirements for obtaining unbiased estimates of neuronal numbers in frozen sections. J. Neurosci. Methods, 97, 133-137.
52. Li, M., Ona, V.O., Guégan, C., Chen, M., Jackson-Lewis, V., Andrews, L.J., Olszewski, A.J., Stieg, P.E., Lee, J.P., Przedborski, S. and Friedlander, R.M. (2000) Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science, 288, 335-339.
53. Jablonka, S., Schrank, B., Kralewski, M., Rossoll, W. and Sendtner, M. (2000) Reduced survival motor neuron (Smn) gene does in mice leads to motor neuron degeneration: an animal model for spinal muscular atrophy type III. Hum. Mol. Genet., 9, 341-346.
54. Rothstein, J.D., Martin, L., Levey, A.I., Dykes-Hoberg, M., Jin, L., Wu, D., Nash, N. and Kuncl, R.W. (1994) Localization of neuronal and glial glutamate transporters. Neuron, 13, 713-725.
55. Lukasz, A., Hellpap, J., Horn, R., Kielstein, J.T., David, S., Haller, H. and Kümpers, P. (2008) Circulating angiopoietin-1 and angiopoietin-2 in critically ill patients: development and clinical application of two new immunoassays. Crit. Care, 12, R94.
56. Corti, S., Nizzardo, M., Nardini, M., Donadoni, C., Salani, S., Ronchi, D., Saladino, F., Bordoni, A., Fortunato, F., Del Bo, R. et al. (2008) Neural stem cell transplantation can ameliorate the phenotype of a mouse model of spinal muscular atrophy. J. Clin. Invest., 118, 3316-3330.
57. Silva, G.A., Feeney, C., Mills, L.R. and Theriault, E. (1998) A novel and rapid method or culturing pure rat spinal cord astrocytes on untreated glass. J. Neurosci. Methods, 80, 75-79.
58. Chen, C.J., Liao, S.L. and Kuo, J.S. (2000) Gliotoxic action of glutamate on cultured astrocytes. J. Neurochem., 75, 1557-1565.