Promotion of Spinal Cord Regeneration by Neural Stem Cell-Secreted Trimerized Cell Adhesion Molecule L1

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  He, Xiaowen ^a   Knepper, Michael ^b   Ding, Cheng ^a   Li, Jun ^a   Castro, Suita ^a   Siddiqui, Maham ^a   Schachner, Melitta ^a,c  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN SULFATE; MYELIN; NERVE CELL ADHESION MOLECULE L1; NG2 PROTEOGLYCAN; PROTEOGLYCAN; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR CHANGE; CELL ENGINEERING; CONTROLLED STUDY; EMBRYO; FEMALE; GROWTH INHIBITION; LOCOMOTION; MOLECULAR INTERACTION; MOUSE; NERVE FIBER GROWTH; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PYRAMIDAL TRACT; REMYELINIZATION; SPINAL CORD COMPRESSION; SPINAL CORD REGENERATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CHONDROITIN SULFATE PROTEOGLYCANS; EMBRYONIC STEM CELLS; FEMALE; IMMUNOHISTOCHEMISTRY; MICE; MOTOR ACTIVITY; NERVE REGENERATION; NEURAL CELL ADHESION MOLECULE L1; NEURAL STEM CELLS; SPINAL CORD INJURIES; SPINAL CORD REGENERATION;

MUS;

EID: 84866659467     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046223     Document Type: Article

References (41)

1. 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.
2. Roonprapunt C, Huang W, Grill R, Friedlander D, Grumet M, et al. (2003) Soluble cell adhesion molecule L1-Fc promotes locomotor recovery in rats after spinal cord injury. J Neurotrauma 20: 871-882.
3. Xu G, Nie DY, Wang WZ, Zhang PH, Shen J, et al. (2004) Optic nerve regeneration in polyglycolic acid-chitosan conduits coated with recombinant L1-Fc. Neuroreport 15: 2167-2172.
4. 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.
5. 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.
6. Castellani V, De Angelis E, Kenwrick S, Rougon G, (2002) Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO J 21: 6348-6357.
7. Chen S, Mantei N, Dong L, Schachner M, (1999) Prevention of neuronal cell death by neural adhesion molecules L1 and CHL1. J Neurobiol 38: 428-439.
8. Kamiguchi H, Yoshihara F, (2001) The role of endocytic l1 trafficking in polarized adhesion and migration of nerve growth cones. J Neurosci 21: 9194-9203.
9. Kleene R, Yang H, Kutsche M, Schachner M, (2001) The neural recognition molecule L1 is a sialic acid-binding lectin for CD24, which induces promotion and inhibition of neurite outgrowth. J Biol Chem 276: 21656-21663.
10. Lemmon V, Farr KL, Lagenaur C, (1989) L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron 2: 1597-1603.
11. Fransen E, D'Hooge R, Van Camp G, Verhoye M, Sijbers J, et al. (1998) L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Hum Mol Genet 7: 999-1009.
12. Luthl A, Laurent JP, Figurov A, Muller D, Schachner M, (1994) Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 372: 777-779.
13. Barbin G, Aigrot MS, Charles P, Foucher A, Grumet M, et al. (2004) Axonal cell-adhesion molecule L1 in CNS myelination. Neuron Glia Biol 1: 65-72.
14. Haney CA, Sahenk Z, Li C, Lemmon VP, Roder J, et al. (1999) Heterophilic binding of L1 on unmyelinated sensory axons mediates Schwann cell adhesion and is required for axonal survival. J Cell Biol 146: 1173-1184.
15. Seilheimer B, Persohn E, Schachner M, (1989) Neural cell adhesion molecule expression is regulated by Schwann cell-neuron interactions in culture. J Cell Biol 108: 1909-1915.
16. Wood P, Moya F, Eldridge C, Owens G, Ranscht B, et al. (1990) Studies of the initiation of myelination by Schwann cells. Ann N Y Acad Sci 605: 1-14.
17. Loers G, Chen S, Grumet M, Schachner M, (2005) Signal transduction pathways implicated in neural recognition molecule L1 triggered neuroprotection and neuritogenesis. J Neurochem 92: 1463-1476.
18. Loers G, Makhina T, Bork U, Dorner A, Schachner M, et al. (2012) The interaction between cell adhesion molecule L1, matrix metalloproteinase 14, and adenine nucleotide translocator at the plasma membrane regulates L1-mediated neurite outgrowth of murine cerebellar neurons. J Neurosci 32: 3917-3930.
19. Loers G, Schachner M, (2007) Recognition molecules and neural repair. J Neurochem 101: 865-882.
20. Maness PF, Schachner M, (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10: 19-26.
21. Nagaraj K, Hortsch M, (2006) Phosphorylation of L1-type cell-adhesion molecules-ankyrins away!. Trends Biochem Sci 31: 544-546.
22. Thelen K, Kedar V, Panicker AK, Schmid RS, Midkiff BR, et al. (2002) The neural cell adhesion molecule L1 potentiates integrin-dependent cell migration to extracellular matrix proteins. J Neurosci 22: 4918-4931.
23. 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.
24. Zhang Y, Yeh J, Richardson PM, Bo X, (2008) Cell adhesion molecules of the immunoglobulin superfamily in axonal regeneration and neural repair. Restor Neurol Neurosci 26: 81-96.
25. 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.
26. 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.
27. 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.
28. Guseva D, Angelov DN, Irintchev A, Schachner M, (2009) Ablation of adhesion molecule L1 in mice favours Schwann cell proliferation and functional recovery after peripheral nerve injury. Brain 132: 2180-2195.
29. Hall H, Bozic D, Fauser C, Engel J, (2000) Trimerization of cell adhesion molecule L1 mimics clustered L1 expression on the cell surface: influence on L1-ligand interactions and on promotion of neurite outgrowth. J Neurochem 75: 336-346.
30. Chen J, Leong SY, Schachner M, (2005) Differential expression of cell fate determinants in neurons and glial cells of adult mouse spinal cord after compression injury. Eur J Neurosci 22: 1895-1906.
31. 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.
32. Chen J, Joon Lee H, Jakovcevski I, Shah R, Bhagat N, et al. (2010) The extracellular matrix glycoprotein tenascin-C is beneficial for spinal cord regeneration. Mol Ther 18: 1769-1777.
33. 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.
34. Engesser-Cesar C, Anderson AJ, Basso DM, Edgerton VR, Cotman CW, (2005) Voluntary wheel running improves recovery from a moderate spinal cord injury. J Neurotrauma 22: 157-171.
35. 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.
36. Barritt AW, Davies M, Marchand F, Hartley R, Grist J, et al. (2006) Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J Neurosci 26: 10856-10867.
37. Mori M, Kose A, Tsujino T, Tanaka C, (1990) Immunocytochemical localization of protein kinase C subspecies in the rat spinal cord: light and electron microscopic study. J Comp Neurol 299: 167-177.
38. Nishimura T, Fukata Y, Kato K, Yamaguchi T, Matsuura Y, et al. (2003) CRMP-2 regulates polarized Numb-mediated endocytosis for axon growth. Nat Cell Biol 5: 819-826.
39. Castellani V, Chedotal A, Schachner M, Faivre-Sarrailh C, Rougon G, (2000) Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron 27: 237-249.
40. 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.
41. Castellani V, (2002) The function of neuropilin/L1 complex. Adv Exp Med Biol 515: 91-102.