Cells transplanted onto the surface of the glial scar reveal hidden potential for functional neural regeneration

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 26, 2015, Pages E3431-E3440

  Sekiya, Tetsuji ^a   Holley, Matthew C ^b   Hashido, Kento ^a   Ono, Kazuya ^a,d   Shimomura, Koichiro ^c   Horie, Rie T ^a,e   Hamaguchi, Kiyomi ^a   Yoshida, Atsuhiro ^a   Sakamoto, Tatsunori ^a   Ito, Juichi ^a  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c KYOTO UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^e KYOTO UNIVERSITY   (Japan)

Author keywords

Astrocyte; Auditory system; Cell transplantation; Glial scar; Neurodegenerative diseases

Indexed keywords

CHONDROITIN ABC LYASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; AUDITORY SYSTEM; CELL MIGRATION; CELL SURFACE; CELL TRANSPLANTATION; COCHLEAR NERVE; CONTROLLED STUDY; DEGENERATIVE DISEASE; GLIA CELL; HEARING; HOST; MALE; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SCAR; ANIMAL; CELL PROLIFERATION; DISEASE MODEL; GLIA; HUMAN; NEURODEGENERATIVE DISEASES; PATHOLOGY; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; CELL PROLIFERATION; CHONDROITIN ABC LYASE; COCHLEAR NERVE; DISEASE MODELS, ANIMAL; HUMANS; MALE; NERVE REGENERATION; NEURODEGENERATIVE DISEASES; NEUROGLIA; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84937936302     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1501835112     Document Type: Article

References (59)

1. Björklund A, Stenevi U, Schmidt RH, Dunnett SB, Gage FH (1983) Intracerebral grafting of neuronal cell suspensions. II. Survival and growth of nigral cell suspensions implanted in different brain sites. Acta Physiol Scand Suppl 522:9-18.
2. Kang X, et al. (2014) Dopamine release from transplanted neural stem cells in Parkinsonian rat striatum in vivo. Proc Natl Acad Sci USA 111(44):15804-15809.
3. Cregg JM, et al. (2014) Functional regeneration beyond the glial scar. Exp Neurol 253:197-207.
4. Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5(2):146-156.
5. Buffo A, et al. (2008) Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proc Natl Acad Sci USA 105(9):3581-3586.
6. Pekny M, Lane EB (2007) Intermediate filaments and stress. Exp Cell Res 313(10):2244-2254.
7. Sekiya T, et al. (2011) Mechanical stress-induced reactive gliosis in the auditory nerve and cochlear nucleus. J Neurosurg 114(2):414-425.
8. Sekiya T, et al. (2012) Trauma-specific insults to the cochlear nucleus in the rat. J Neurosci Res 90(10):1924-1931.
9. Forge A, Wright T (2002) The molecular architecture of the inner ear. Br Med Bull 63:5-24.
10. Matsumoto M, Sekiya T, Kojima K, Ito J (2008) An animal experimental model of auditory neuropathy induced in rats by auditory nerve compression. Exp Neurol 210(1):248-256.
11. Sekiya T, et al. (2007) Transplantation of conditionally immortal auditory neuroblasts to the auditory nerve. Eur J Neurosci 25(8):2307-2318.
12. Nicholl AJ, et al. (2005) Differentiation of an auditory neuronal cell line suitable for cell transplantation. Eur J Neurosci 22(2):343-353.
13. Bradbury EJ, et al. (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416(6881):636-640.
14. Tarlov I (1937) Structure of the nerve root. II. Differentiation of sensory from motor roots; observations on identification of function in roots of mixed cranial nerves. Arch Neurol Psychiatry 37:1338-1355.
15. Fraher JP, Delanty FJ (1987) The development of the central-peripheral transitional zone of the rat cochlear nerve. A light microscopic study. J Anat 155:109-118.
16. Asher RA, et al. (2000) Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20(7):2427-2438.
17. Moller AR (2011) Generation of Electrical Activity in the Nervous System and Muscles. Neurophysiological Monitoring (Springer, New York), pp 23-41.
18. Shaw NA (1988) The auditory evoked potential in the rat - A review. Prog Neurobiol 31(1):19-45.
19. Rakic P (1990) Principles of neural cell migration. Experientia 46(9):882-891.
20. Marín O, Rubenstein JL (2003) Cell migration in the forebrain. Annu Rev Neurosci 26:441-483.
21. Wanner IB, et al. (2013) Glial scar borders are formed by newly proliferated, elongated astrocytes that interact to corral inflammatory and fibrotic cells via STAT3-dependent mechanisms after spinal cord injury. J Neurosci 33(31):12870-12886.
22. Lois C, García-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271(5251):978-981.
23. Ghashghaei HT, Lai C, Anton ES (2007) Neuronal migration in the adult brain: Are we there yet? Nat Rev Neurosci 8(2):141-151.
24. Schwanzel-Fukuda M, Pfaff DW (1989) Origin of luteinizing hormone-releasing hormone neurons. Nature 338(6211):161-164.
25. Chen W, et al. (2012) Restoration of auditory evoked responses by human ES-cell-derived otic progenitors. Nature 490(7419):278-282.
26. Ruel J, et al. (2007) Physiology, pharmacology and plasticity at the inner hair cell synaptic complex. Hear Res 227(1-2):19-27.
27. Yuan Y, et al. (2014) Ouabain-induced cochlear nerve degeneration: Synaptic loss and plasticity in a mouse model of auditory neuropathy. J Assoc Res Otolaryngol 15(1):31-43.
28. Rubel EW, Fritzsch B (2002) Auditory system development: Primary auditory neurons and their targets. Annu Rev Neurosci 25:51-101.
29. Shen Y, et al. (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326(5952):592-596.
30. Dickendesher TL, et al. (2012) NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat Neurosci 15(5):703-712.
31. Brown JM, Vivio N, Sheean GL (2012) The clinical practice of reconstructive neurosurgery. Clin Neurol Neurosurg 114(5):506-514.
32. Lu P, Jones LL, Tuszynski MH (2007) Axon regeneration through scars and into sites of chronic spinal cord injury. Exp Neurol 203(1):8-21.
33. Tropea D, Caleo M, Maffei L (2003) Synergistic effects of brain-derived neurotrophic factor and chondroitinase ABC on retinal fiber sprouting after denervation of the superior colliculus in adult rats. J Neurosci 23(18):7034-7044.
34. Skaper SD (2005) Neuronal growth-promoting and inhibitory cues in neuroprotection and neuroregeneration. Ann N Y Acad Sci 1053:376-385.
35. Tom VJ, Doller CM, Malouf AT, Silver J (2004) Astrocyte-associated fibronectin is critical for axonal regeneration in adult white matter. J Neurosci 24(42):9282-9290.
36. Chien PN, Ryu SE (2013) Protein tyrosine phosphatase σ in proteoglycan-mediated neural regeneration regulation. Mol Neurobiol 47(1):220-227.
37. Bartus K, et al. (2014) Large-scale chondroitin sulfate proteoglycan digestion with chondroitinase gene therapy leads to reduced pathology and modulates macrophage phenotype following spinal cord contusion injury. J Neurosci 34(14):4822-4836.
38. Didangelos A, Iberl M, Vinsland E, Bartus K, Bradbury EJ (2014) Regulation of IL-10 by chondroitinase ABC promotes a distinct immune response following spinal cord injury. J Neurosci 34(49):16424-16432.
39. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A (2002) Macrophage polarization: Tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23(11):549-555.
40. Kigerl KA, et al. (2009) Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 29(43):13435-13444.
41. Knoblach SM, Faden AI (1998) Interleukin-10 improves outcome and alters proinflammatory cytokine expression after experimental traumatic brain injury. Exp Neurol 153(1):143-151.
42. Zhou Z, Peng X, Insolera R, Fink DJ, Mata M (2009) IL-10 promotes neuronal survival following spinal cord injury. Exp Neurol 220(1):183-190.
43. Goldshmit Y, et al. (2012) Fgf-dependent glial cell bridges facilitate spinal cord regeneration in zebrafish. J Neurosci 32(22):7477-7492.
44. Filous AR, et al. (2010) Immature astrocytes promote CNS axonal regeneration when combined with chondroitinase ABC. Dev Neurobiol 70(12):826-841.
45. Fraher JP (1999) The transitional zone and CNS regeneration. J Anat 194(Pt 2):161-182.
46. Filbin MT (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 4(9):703-713.
47. Kauhausen J, Thompson LH, Parish CL (2013) Cell intrinsic and extrinsic factors contribute to enhance neural circuit reconstruction following transplantation in Parkinsonian mice. J Physiol 591(Pt 1):77-91.
48. MacLaren RE, et al. (2006) Retinal repair by transplantation of photoreceptor precursors. Nature 444(7116):203-207.
49. Khan AM, et al. (2005) Is word recognition correlated with the number of surviving spiral ganglion cells and electrode insertion depth in human subjects with cochlear implants? Laryngoscope 115(4):672-677.
50. Blight AR (1983) Cellular morphology of chronic spinal cord injury in the cat: Analysis of myelinated axons by line-sampling. Neuroscience 10(2):521-543.
51. Moloney EB, de Winter F, Verhaagen J (2014) ALS as a distal axonopathy: Molecular mechanisms affecting neuromuscular junction stability in the presymptomatic stages of the disease. Front Neurosci 8:252.
52. Howard RS (2005) Poliomyelitis and the postpolio syndrome. BMJ 330(7503):1314-1318.
53. Vucic S, Kiernan MC, Cornblath DR (2009) Guillain-Barré syndrome: An update. J Clin Neurosci 16(6):733-741.
54. Moreels M, Vandenabeele F, Dumont D, Robben J, Lambrichts I (2008) Alpha-smooth muscle actin (alpha-SMA) and nestin expression in reactive astrocytes in multiple sclerosis lesions: Potential regulatory role of transforming growth factor-beta 1 (TGF-beta1). Neuropathol Appl Neurobiol 34(5):532-546.
55. Yuan PX, et al. (2001) The mood stabilizer valproic acid activates mitogen-activated protein kinases and promotes neurite growth. J Biol Chem 276(34):31674-31683.
56. Hackney CM, Osen KK, Kolston J (1990) Anatomy of the cochlear nuclear complex of guinea pig. Anat Embryol (Berl) 182(2):123-149.
57. Elfving B, Plougmann PH, Wegener G (2010) Detection of brain-derived neurotrophic factor (BDNF) in rat blood and brain preparations using ELISA: Pitfalls and solutions. J Neurosci Methods 187(1):73-77.
58. Viberg A, Canlon B (2004) The guide to plotting a cochleogram. Hear Res 197(1-2):1-10.
59. Shiga A, et al. (2005) Aging effects on vestibulo-ocular responses in C57BL/6 mice: Comparison with alteration in auditory function. Audiol Neurootol 10(2):97-104.