Embryonic stem cell-derived L1 overexpressing neural aggregates enhance recovery after spinal cord injury in mice

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Cui, Yi Fang ^a,b   Xu, Jin Chong ^a   Hargus, Gunnar ^a   Jakovcevski, Igor ^a   Schachner, Melitta ^a,c   Bernreuther, Christian ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b GERMAN PRIMATE CENTER   (Germany)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE CELL ADHESION MOLECULE L1; PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CATECHOLAMINE NERVE CELL; CELL ACTIVITY; CELL AGGREGATION; CELL COUNT; CELL FUNCTION; CELL MIGRATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CONVALESCENCE; EARLY INTERVENTION; EMBRYO; EMBRYONIC STEM CELL; FEMALE; GENE OVEREXPRESSION; GENETIC ENGINEERING; IMMUNE RESPONSE; INTERNEURON; LOCOMOTION; MICROENVIRONMENT; MICROGLIA; MOTONEURON; MOUSE; NERVE CELL DIFFERENTIATION; NERVE COMPRESSION; NERVE FIBER GROWTH; NERVE GROWTH; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; SCAR FORMATION; SPINAL CORD INJURY; SPINAL CORD LESION; SPINAL CORD REGENERATION; THERAPY EFFECT; WILD TYPE; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; GLIA; METABOLISM; STEM CELL TRANSPLANTATION;

MAMMALIA; MURINAE; MUS;

ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; INTERNEURONS; MICE; NEURAL CELL ADHESION MOLECULE L1; NEUROGLIA; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION;

EID: 79952802524     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017126     Document Type: Article

References (58)

1. Di Giovanni S, (2006) Regeneration following spinal cord injury, from experimental models to humans: where are we? Expert Opin Ther Targets 10: 363-376.
2. Thuret S, Moon LD, Gage FH, (2006) Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 7: 628-643.
3. Nandoe Tewarie RS, Hurtado A, Bartels RH, Grotenhuis A, Oudega M, (2009) Stem cell-based therapies for spinal cord injury. J Spinal Cord Med 32: 105-114.
4. Jain KK, (2009) Cell therapy for CNS trauma. Mol Biotechnol 42: 367-376.
5. Chen J, Bernreuther C, Dihne M, Schachner M, (2005) Cell adhesion molecule l1-transfected embryonic stem cells with enhanced survival support regrowth of corticospinal tract axons in mice after spinal cord injury. J Neurotrauma 22: 896-906.
6. Harper JM, Krishnan C, Darman JS, Deshpande DM, Peck S, et al. (2004) Axonal growth of embryonic stem cell-derived motoneurons in vitro and in motoneuron-injured adult rats. Proc Natl Acad Sci U S A 101: 7123-7128.
7. Howard MJ, Liu S, Schottler F, Joy Snider B, Jacquin MF, (2005) Transplantation of apoptosis-resistant embryonic stem cells into the injured rat spinal cord. Somatosens Mot Res 22: 37-44.
8. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, et al. (2005) Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25: 4694-4705.
9. Appel F, Holm J, Conscience JF, Schachner M, (1993) Several extracellular domains of the neural cell adhesion molecule L1 are involved in neurite outgrowth and cell body adhesion. J Neurosci 13: 4764-4775.
10. Lindner J, Rathjen FG, Schachner M, (1983) L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 305: 427-430.
11. Moos M, Tacke R, Scherer H, Teplow D, Fruh K, et al. (1988) Neural adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin. Nature 334: 701-703.
12. Rathjen FG, Schachner M, (1984) Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. Embo J 3: 1-10.
13. Bernreuther C, Dihne M, Johann V, Schiefer J, Cui Y, et al. (2006) Neural cell adhesion molecule L1-transfected embryonic stem cells promote functional recovery after excitotoxic lesion of the mouse striatum. J Neurosci 26: 11532-11539.
14. Dihne M, Bernreuther C, Sibbe M, Paulus W, Schachner M, (2003) A new role for the cell adhesion molecule L1 in neural precursor cell proliferation, differentiation, and transmitter-specific subtype generation. J Neurosci 23: 6638-6650.
15. Dong L, Chen S, Schachner M, (2003) Single chain Fv antibodies against neural cell adhesion molecule L1 trigger L1 functions in cultured neurons. Mol Cell Neurosci 22: 234-247.
16. Cui YF, Hargus G, Xu JC, Schmid JS, Shen YQ, et al. (2010) Embryonic stem cell-derived L1 overexpressing neural aggregates enhance recovery in Parkinsonian mice. Brain 133: 189-204.
17. Chen J, Wu J, Apostolova I, Skup M, Irintchev A, et al. (2007) Adeno-associated virus-mediated L1 expression promotes functional recovery after spinal cord injury. Brain 130: 954-969.
18. Lavdas AA, Chen J, Papastefanaki F, Chen S, Schachner M, et al. (2009) Schwann cells engineered to express the cell adhesion molecule L1 accelerate myelination and motor recovery after spinal cord injury. Exp Neurol.
19. Dihne M, Bernreuther C, Hagel C, Wesche KO, Schachner M, (2006) Embryonic stem cell-derived neuronally committed precursor cells with reduced teratoma formation after transplantation into the lesioned adult mouse brain. Stem Cells 24: 1458-1466.
20. Lee SH, Lumelsky N, Studer L, Auerbach JM, McKay RD, (2000) Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat Biotechnol 18: 675-679.
21. Apostolova I, Irintchev A, Schachner M, (2006) Tenascin-R restricts posttraumatic remodeling of motoneuron innervation and functional recovery after spinal cord injury in adult mice. J Neurosci 26: 7849-7859.
22. Lee HJ, Jakovcevski I, Radonjic N, Hoelters L, Schachner M, et al. (2009) Better functional outcome of compression spinal cord injury in mice is associated with enhanced H-reflex responses. Exp Neurol 216: 365-374.
23. Davidoff MS, Irintchev AP, (1986) Acetylcholinesterase activity and type C synapses in the hypoglossal, facial and spinal-cord motor nuclei of rats. An electron-microscope study. Histochemistry 84: 515-524.
24. Hellstrom J, Oliveira AL, Meister B, Cullheim S, (2003) Large cholinergic nerve terminals on subsets of motoneurons and their relation to muscarinic receptor type 2. J Comp Neurol 460: 476-486.
25. Kiehn O, Rostrup E, Moller M, (1992) Monoaminergic systems in the brainstem and spinal cord of the turtle Pseudemys scripta elegans as revealed by antibodies against serotonin and tyrosine hydroxylase. J Comp Neurol 325: 527-547.
26. Shapiro S, (1997) Neurotransmission by neurons that use serotonin, noradrenaline, glutamate, glycine, and gamma-aminobutyric acid in the normal and injured spinal cord. Neurosurgery 40: 168-176 discussion 177.
27. Fouad K, Pearson K, (2004) Restoring walking after spinal cord injury. Prog Neurobiol 73: 107-126.
28. Jakovcevski I, Wu J, Karl N, Leshchyns'ka I, Sytnyk V, et al. (2007) Glial scar expression of CHL1, the close homolog of the adhesion molecule L1, limits recovery after spinal cord injury. J Neurosci 27: 7222-7233.
29. Sadoul K, Sadoul R, Faissner A, Schachner M, (1988) Biochemical characterization of different molecular forms of the neural cell adhesion molecule L1. J Neurochem 50: 510-521.
30. Silletti S, Mei F, Sheppard D, Montgomery AM, (2000) Plasmin-sensitive dibasic sequences in the third fibronectin-like domain of L1-cell adhesion molecule (CAM) facilitate homomultimerization and concomitant integrin recruitment. J Cell Biol 149: 1485-1502.
31. Kalus I, Schnegelsberg B, Seidah NG, Kleene R, Schachner M, (2003) The proprotein convertase PC5A and a metalloprotease are involved in the proteolytic processing of the neural adhesion molecule L1. J Biol Chem 278: 10381-10388.
32. Nesic O, Lee J, Johnson KM, Ye Z, Xu GY, et al. (2005) Transcriptional profiling of spinal cord injury-induced central neuropathic pain. J Neurochem 95: 998-1014.
33. De Biase A, Knoblach SM, Di Giovanni S, Fan C, Molon A, et al. (2005) Gene expression profiling of experimental traumatic spinal cord injury as a function of distance from impact site and injury severity. Physiol Genomics 22: 368-381.
34. Belegu V, Oudega M, Gary DS, McDonald JW, (2007) Restoring function after spinal cord injury: promoting spontaneous regeneration with stem cells and activity-based therapies. Neurosurg Clin N Am 18: 143-168, xi.
35. Kerr DA, Llado J, Shamblott MJ, Maragakis NJ, Irani DN, et al. (2003) Human embryonic germ cell derivatives facilitate motor recovery of rats with diffuse motor neuron injury. J Neurosci 23: 5131-5140.
36. Kimura H, Yoshikawa M, Matsuda R, Toriumi H, Nishimura F, et al. (2005) Transplantation of embryonic stem cell-derived neural stem cells for spinal cord injury in adult mice. Neurol Res 27: 812-819.
37. Ogawa Y, Sawamoto K, Miyata T, Miyao S, Watanabe M, et al. (2002) Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. J Neurosci Res 69: 925-933.
38. Okano H, (2002) Stem cell biology of the central nervous system. J Neurosci Res 69: 698-707.
39. Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, El Manira A, et al. (2002) Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci U S A 99: 2199-2204.
40. Busch SA, Silver J, (2007) The role of extracellular matrix in CNS regeneration. Curr Opin Neurobiol 17: 120-127.
41. Menet V, Prieto M, Privat A, Gimenez y Ribotta M, (2003) Axonal plasticity and functional recovery after spinal cord injury in mice deficient in both glial fibrillary acidic protein and vimentin genes. Proc Natl Acad Sci U S A 100: 8999-9004.
42. Bessis A, Bechade C, Bernard D, Roumier A, (2007) Microglial control of neuronal death and synaptic properties. Glia 55: 233-238.
43. Loers G, Schachner M, (2007) Recognition molecules and neural repair. J Neurochem 101: 865-882.
44. Barnes CD, Schadt JC, (1979) Release of function in the spinal cord. Prog Neurobiol 12: 1-13.
45. Hulley P, Schachner M, Lubbert H, (1998) L1 neural cell adhesion molecule is a survival factor for fetal dopaminergic neurons. J Neurosci Res 53: 129-134.
46. Pearse DD, Bunge MB, (2006) Designing cell- and gene-based regeneration strategies to repair the injured spinal cord. J Neurotrauma 23: 438-452.
47. Miles GB, Hartley R, Todd AJ, Brownstone RM, (2007) Spinal cholinergic interneurons regulate the excitability of motoneurons during locomotion. Proc Natl Acad Sci U S A 104: 2448-2453.
48. Nishimune H, Bernreuther C, Carroll P, Chen S, Schachner M, et al. (2005) Neural adhesion molecules L1 and CHL1 are survival factors for motoneurons. J Neurosci Res 80: 593-599.
49. Schuch U, Lohse MJ, Schachner M, (1989) Neural cell adhesion molecules influence second messenger systems. Neuron 3: 13-20.
50. Dekkers J, Greensmith L, Navarrete R, (2002) Changes in the expression of parvalbumin immunoreactivity in the lumbar spinal cord of the rat following neonatal nerve injury. Dev Neurosci 24: 283-293.
51. Celio M, (1984) Parvalbumin as a marker of fast firing neurons. Neurosci Lett 18 (Suppl).
52. Celio MR, (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35: 375-475.
53. Irintchev A, Simova O, Eberhardt KA, Morellini F, Schachner M, (2005) Impacts of lesion severity and tyrosine kinase receptor B deficiency on functional outcome of femoral nerve injury assessed by a novel single-frame motion analysis in mice. Eur J Neurosci 22: 802-808.
54. Gozariu M, Roth V, Keime F, Le Bars D, Willer JC, (1998) An electrophysiological investigation into the monosynaptic H-reflex in the rat. Brain Res 782: 343-347.
55. Li D, Zhou J, Wang L, Shin ME, Su P, et al. (2010) Integrated biochemical and mechanical signals regulate multifaceted human embryonic stem cell functions. J Cell Biol.
56. Curtis R, Green D, Lindsay RM, Wilkin GP, (1993) Up-regulation of GAP-43 and growth of axons in rat spinal cord after compression injury. J Neurocytol 22: 51-64.
57. Basso DM, Beattie MS, Bresnahan JC, (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12: 1-21.
58. Joshi M, Fehlings MG, (2002) Development and characterization of a novel, graded model of clip compressive spinal cord injury in the mouse: Part 1. Clip design, behavioral outcomes, and histopathology. J Neurotrauma 19: 175-190.