Chimerization of astroglial population in the lumbar spinal cord after mesenchymal stem cell transplantation prolongs survival in a rat model of amyotrophic lateral sclerosis

Journal of Neuroscience Research

Volumn 87, Issue 9, 2009, Pages 2034-2046

  Boucherie, Cédric ^a,b   Schäfer, Sabrina ^a,b   Lavand'homme, Patricia ^a   Maloteaux, Jean Marie ^a   Hermans, Emmanuel ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b European Graduate School of Neuroscience   (Netherlands)

Author keywords

ALS; Astrocytes; Glial differentiation; Mesenchymal stem cells

Indexed keywords

CYCLOOXYGENASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL INFILTRATION; CELL PROLIFERATION; CELL REGENERATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DISEASE COURSE; GRAFT SURVIVAL; HISTOCOMPATIBILITY; LUMBAR SPINAL CORD; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROGLIA; NERVE CELL DIFFERENTIATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SURVIVAL RATE; TRANSGENIC RAT; TREATMENT RESPONSE;

EID: 65849291460     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22038     Document Type: Article

References (63)

1. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM. 2007. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10:1538-1543.
2. Almer G, Guegan C, Teismann P, Naini A, Rosoklija G, Hays AP, Chen C, Przedborski S. 2001. Increased expression of the pro-inflammatory enzyme cyclooxygenase-2 in amyotrophic lateral sclerosis. Ann Neurol 49:176-185.
3. Arnhold S, Klein H, Klinz FJ, Absenger Y, Schmidt A, Schinkothe T, Brixius K, Kozlowski J, Desai B, Bloch W, Addicks K. 2006. Human bone marrow stroma cells display certain neural characteristics and integrate in the subventricular compartment after injection into the liquor system. Eur J Cell Biol 85:551-565.
4. Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ. 1998. 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 95:3908-3913.
5. Bantubungi K, Blum D, Cuvelier L, Wislet-Gendebien S, Rogister B, Brouillet E, Schiffmann SN. 2008. Stem cell factor and mesenchymal and neural stem cell transplantation in a rat model of Huntington's disease. Mol Cell Neurosci 37:454-470.
6. Beers DR, Henkel JS, Xiao Q, Zhao W, Wang J, Yen AA, Siklos L, McKercher SR, Appel SH. 2006. Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A 103:16021-16026.
7. Boillee S, Vande VC, Cleveland DW. 2006a. ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52:39-59.
8. Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW. 2006b. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312:1389-1392.
9. G93A). Exp Neurol 212:557-561.
10. Boucherie C, Hermans E. 2009. Adult stem cell therapy for neurological disorders: benefit beyond neuronal replacement? J Neurosci Res Epub ahead of print [doi.10.1002/jnr.21970].
11. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, Rule M, McMahon AP, Doucette W, Siwek D, Ferrante RJ, Brown RH, Jr., Julien JP, Goldstein LS, Cleveland DW. 2003. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302:113-117.
12. Cleveland DW. 1999. From Charcot to SOD1: mechanisms of selective motor neuron death in ALS. Neuron 24:515-520.
13. Corti S, Locatelli F, Donadoni C, Guglieri M, Papadimitriou D, Strazzer S, Del Bo R, Comi GP. 2004. Wild-type bone marrow cells ameliorate the phenotype of SOD1-G93A ALS mice and contribute to CNS, heart and skeletal muscle tissues. Brain 127:1-15.
14. Corti S, Locatelli F, Papadimitriou D, Del Bo R, Nizzardo M, Nardini M, Donadoni C, Salani S, Fortunato F, Strazzer S, Bresolin N, Comi GP. 2007. Neural stem cells LewisX+ CXCR4+ modify disease progression in an amyotrophic lateral sclerosis model. Brain 130:1289-1305.
15. Corti S, Locatelli F, Papadimitriou D, Donadoni C, Del Bo R, Crimi M, Bordoni A, Fortunato F, Strazzer S, Menozzi G, Salani S, Bresolin N, Comi GP. 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.
16. Corti S, Nizzardo M, Nardini M, Donadoni C, Salani S, Ronchi D, Saladino F, Bordoni A, Fortunato F, Del Bo R, Papadimitriou D, Locatelli F, Menozzi G, Strazzer S, Bresolin N, Comi GP. 2008. Neural stem cell transplantation can ameliorate the phenotype of a mouse model of spinal muscular atrophy. J Clin Invest 118:3316-3330.
17. de Hemptinne I, Boucherie C, Pochet R, Bantubungi K, Schiffmann SN, Maloteaux JM, Hermans E. 2006. Unilateral induction of progenitors in the spinal cord of hSOD1(G93A) transgenic rats correlates with an asymmetrical hind limb paralysis. Neurosci Lett 401:25-29.
18. Di Giorgio FP, Carrasco MA, Siao MC, Maniatis T, 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.
19. Drachman DB, Frank K, Dykes-Hoberg M, Teismann P, Almer G, Przedborski S, Rothstein JD. 2002. Cyclooxygenase 2 inhibition protects motor neurons and prolongs survival in a transgenic mouse model of ALS. Ann Neurol 52:771-778.
20. Dunlop J, Beal MH, She Y, Howland DS. 2003. Impaired spinal cord glutamate transport capacity and reduced sensitivity to riluzole in a transgenic superoxide dismutase mutant rat model of amyotrophic lateral sclerosis. J Neurosci 23:1688-1696.
21. Hall ED, Oostveen JA, Gurney ME. 1998. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23:249-256.
22. Harraz MM, Marden JJ, Zhou W, Zhang Y, Williams A, Sharov VS, Nelson K, Luo M, Paulson H, Schoneich C, Engelhardt JF. 2008. SOD1 mutations disrupt redox-sensitive Rac regulation of NADPH oxidase in a familial ALS model. J Clin Invest 118:659-670.
23. Hedlund E, Hefferan MP, Marsala M, Isacson O. 2007. Cell therapy and stem cells in animal models of motor neuron disorders. Eur J Neurosci 26:1721-1737.
24. Henkel JS, Engelhardt JI, Siklos L, Simpson EP, Kim SH, Pan T, Goodman JC, Siddique T, Beers DR, Appel SH. 2004. Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann Neurol 55:221-235.
25. Howland DS, Liu J, She Y, Goad B, Maragakis NJ, Kim B, Erickson J, Kulik J, DeVito L, Psaltis G, DeGennaro LJ, Cleveland DW, Rothstein JD. 2002. 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 99:1604-1609.
26. Kawamata T, Akiyama H, Yamada T, McGeer PL. 1992. Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Am J Pathol 140:691-707.
27. Kerr DA, Llado J, Shamblott MJ, Maragakis NJ, Irani DN, Crawford TO, Krishnan C, Dike S, Gearhart JD, Rothstein JD. 2003. Human embryonic germ cell derivatives facilitate motor recovery of rats with diffuse motor neuron injury. J Neurosci 23:5131-5140.
28. Kopen GC, Prockop DJ, Phinney DG. 1999. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Nat Acad Sci USA 96:10711-10716.
29. Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW. 2008. Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat Med 14:504-506.
30. Kostianovsky AM, Maier LM, Anderson RC, Bruce JN, Anderson DE. 2008. Astrocytic regulation of human monocytic/microglial activation. J Immunol 181:5425-5432.
31. Kriz J, Nguyen MD, Julien JP. 2002. Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 10:268-278.
32. Lepore AC, Bakshi A, Swanger SA, Rao MS, Fischer I. 2005. Neural precursor cells can be delivered into the injured cervical spinal cord by intrathecal injection at the lumbar cord. Brain Res 1045:206-216.
33. Lepore AC, Dejea C, Carmen J, Rauck B, Kerr DA, Sofroniew MV, Maragakis NJ. 2008a. Selective ablation of proliferating astrocytes does not affect disease outcome in either acute or chronic models of motor neuron degeneration. Exp Neurol 211:423-432.
34. Lepore AC, Rauck B, Dejea C, Pardo AC, Rao MS, Rothstein JD, Maragakis NJ. 2008b. Focal transplantation-based astrocyte replacement is neuroprotective in a model of motor neuron disease. Nat Neurosci 11:1294-1301.
35. Li JY, Englund E, Holton JL, Soulet D, Hagell P, Lees AJ, Lashley T, Quinn NP, Rehncrona S, Bjorklund A, Widner H, Revesz T, Lindvall O, Brundin P. 2008. Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14:501-503.
36. Lino MM, Schneider C, Caroni P. 2002. Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J Neurosci 22:4825-4832.
37. Magnus T, Carmen J, Deleon J, Xue H, Pardo AC, Lepore AC, Mattson MP, Rao MS, Maragakis NJ. 2008. Adult glial precursor proliferation in mutant SOD1G93A mice. Glia 56:200-208.
38. Matsumoto A, Okada Y, Nakamichi M, Nakamura M, Toyama Y, Sobue G, Nagai M, Aoki M, Itoyama Y, Okano H. 2006. Disease progression of human SOD1 (G93A) transgenic ALS model rats. J Neurosci Res 83:119-133.
39. Morita E, Watanabe Y, Ishimoto M, Nakano T, Kitayama M, Yasui K, Fukada Y, Doi K, Karunaratne A, Murrell WG, Sutharsan R, Mackay- Sim A, Hata Y, Nakashima K. 2008. A novel cell transplantation protocol and its application to an ALS mouse model. Exp Neurol 213:431-438.
40. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S. 2007. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10: 615-622.
41. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, Dina G, Galli R, Del Carro U, Amadio S, Bergami A, Furlan R, Comi G, Vescovi AL, Martino G. 2003. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422:688-694.
42. Pompl PN, Ho L, Bianchi M, McManus T, Qin W, Pasinetti GM. 2003. A therapeutic role for cyclooxygenase-2 inhibitors in a transgenic mouse model of amyotrophic lateral sclerosis. FASEB J 17:725-727.
43. Pramatarova A, Laganiere J, Roussel J, Brisebois K, Rouleau GA. 2001. Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J Neurosci 21:3369-3374.
44. Rao SD, Weiss JH. 2004. Excitotoxic and oxidative cross-talk between motor neurons and glia in ALS pathogenesis. Trends Neurosci 27:17-23.
45. Rao SD, Yin HZ, Weiss JH. 2003. Disruption of glial glutamate transport by reactive oxygen species produced in motor neurons. J Neurosci 23:2627-2633.
46. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX. 1993. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59-62.
47. Rothstein JD, Patel S, Regan MR, Haenggeli C, Huang YH, Bergles DE, Jin L, Dykes-Hoberg M, Vidensky S, Chung DS, Toan SV, Bruijn LI, Su ZZ, Gupta P, Fisher PB. 2005. Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 433:73-77.
48. Satake K, Lou J, Lenke LG. 2004. Migration of mesenchymal stem cells through cerebrospinal fluid into injured spinal cord tissue. Spine 29: 1971-1979.
49. Son M, Fathallah-Shaykh HM, Elliott JL. 2001. Survival in a transgenic model of FALS is independent of iNOS expression. Ann Neurol 50: 273.
50. Turner BJ, Talbot K. 2008. Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog Neurobiol 85:94-134.
51. Turner MR, Cagnin A, Turkheimer FE, Miller CC, Shaw CE, Brooks DJ, Leigh PN, Banati RB. 2004. Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)- PK11195 positron emission tomography study. Neurobiol Dis 15:601-609.
52. Urushitani M, Sik A, Sakurai T, Nukina N, Takahashi R, Julien JP. 2006. Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat Neurosci 9: 108-118.
53. Vercelli A, Mereuta OM, Garbossa D, Muraca G, Mareschi K, Rustichelli D, Ferrero I, Mazzini L, Madon E, Fagioli F. 2008. Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinflammation in mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 31:395-405.
54. Weydt P, Yuen EC, Ransom BR, Moller T. 2004. Increased cytotoxic potential of microglia from ALS-transgenic mice. Glia 48:179-182.
55. Wu DC, Re DB, Nagai M, Ischiropoulos H, Przedborski S. 2006. The inflammatory NADPH oxidase enzyme modulates motor neuron degeneration in amyotrophic lateral sclerosis mice. Proc Natl Acad Sci U S A 103:12132-12137.
56. Wu S, Suzuki Y, Noda T, Bai H, Kitada M, Kataoka K, Nishimura Y, Ide C. 2002. Immunohistochemical and electron microscopic study of invasion and differentiation in spinal cord lesion of neural stem cells grafted through cerebrospinal fluid in rat. J Neurosci Res 69:940-945.
57. Xiao Q, Zhao W, Beers DR, Yen AA, Xie W, Henkel JS, Appel SH. 2007. Mutant SOD1(G93A) microglia are more neurotoxic relative to wild-type microglia. J Neurochem 102:2008-2019.
58. Xu L, Yan J, Chen D, Welsh AM, Hazel T, Johe K, Hatfield G, Koliatsos VE. 2006. Human neural stem cell grafts ameliorate motor neuron disease in SOD-1 transgenic rats. Transplantation 82:865-875.
59. Yaksh TL, Rudy TA. 1976. Chronic catheterization of the spinal subarachnoid space. Physiol Behav 17:1031-1036.
60. Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, Gutmann DH, Takahashi R, Misawa H, Cleveland DW. 2008. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 11:251-253.
61. Yasojima K, Tourtellotte WW, McGeer EG, McGeer PL. 2001. Marked increase in cyclooxygenase-2 in ALS spinal cord: implications for therapy. Neurology 57:952-956.
62. Yiangou Y, Facer P, Durrenberger P, Chessell IP, Naylor A, Bountra C, Banati RR, Anand P. 2006. COX-2, CB2 and P2X7-immunoreactivities are increased in activated microglial cells/macrophages of multiple sclerosis and amyotrophic lateral sclerosis spinal cord. BMC Neurol 6:12.
63. Yin HZ, Tang DT, Weiss JH. 2007. Intrathecal infusion of a Ca(21)- permeable AMPA channel blocker slows loss of both motor neurons and of the astrocyte glutamate transporter, GLT-1 in a mutant SOD1 rat model of ALS. Exp Neurol 207:177-185.