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Spontaneously Immortalized Adult Rodent Schwann Cells as Valuable Tools for the Study of Peripheral Nerve Degeneration and Regeneration

  • Kazunori SangoEmail author
  • Masami Tsukamoto
  • Kazunori Utsunomiya
  • Kazuhiko Watabe
Chapter

Abstract

We have established spontaneously immortalized Schwann cell lines from normal adult mice and rats, as well as murine disease models. One of the normal mouse cell lines, IMS32, possesses some biological properties of mature Schwann cells and high proliferative activities. The IMS32 cells have been utilized to investigate the action mechanisms of various molecules involved in peripheral nerve regeneration [e.g., ciliary neurotrophic factor (CNTF), sonic hedgehog, and galectin-1], and the pathogenesis of diabetic neuropathy, particularly the polyol pathway hyperactivity. The cell lines derived from murine disease models (e.g., lysosomal storage diseases, Charcot-Marie-Tooth disease, and neurofibromatosis) retain genomic and biochemical abnormalities, sufficiently representing the pathological features of the mutant mice. A normal rat cell line, IFRS1, retains the characteristic features of mature Schwann cells and the fundamental ability to myelinate axons in coculture with adult rat DRG neurons and PC12 cells. These Schwann cell lines can be valuable tools for exploring neuron–Schwann cell interactions, the pathobiology of axonal degeneration and regeneration in the peripheral nervous system, and novel therapeutic approaches against neurological disorders in patients with relevant diseases.

Keywords

Adult rodents Axonal regeneration Immortalized Schwann cells Murine disease models Myelination Peripheral neuropathies 

Notes

Acknowledgments

The work of our laboratory reported in this review was supported by a Grant-in-aid for Scientific Research from the Ministry of Education, Science, Sports and Culture of Japan (grant number: 22500324), the Umehara Fund of the Yokohama Foundation for the Advancement of Medical Science, Japan, and grants from the Sanwa Kagaku Kenkyusho, Suzuken Memorial Foundation, and the Japan Diabetes Foundation. We thank Drs. Koichi Kato, Yasushi Kanazawa, Shizuka Takaku, Hiroko Yanagisawa, and Miwa Sango-Hirade for helpful suggestions; Emiko Kawakami, Kentaro Endo, and the late Kyoko Ajiki for technical assistance with our studies; Enago (www.enago.jp) for the English language review; and John Wiley and Sons for permission to reproduce the illustrations.

References

  1. Abe K, Namikawa K, Honma M, Iwata T, Matsuoka I, Watabe K, Kiyama H (2001) Inhibition of Ras extracellular-signal-regulated kinase (ERK) mediated signaling promotes ciliary neurotrophic factor (CNTF) expression in Schwann cells. J Neurochem 77(2):700–703PubMedCrossRefGoogle Scholar
  2. Adler R, Landa KB, Manthorpe M, Varon S (1979) Cholinergic neuronotrophic factors: intraocular distribution of soluble trophic activity for ciliary neurons. Science 204(4400):1434–1436PubMedCrossRefGoogle Scholar
  3. Airaksinen MS, Saarma M (2002) The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci 3(5):383–394PubMedCrossRefGoogle Scholar
  4. Aragno M, Mastrocola R, Medana C, Restivo F, Catalano MG, Pons N, Danni O, Boccuzzi G (2005) Up-regulation of advanced glycated products receptors in the brain of diabetic rats is prevented by antioxidant treatment. Endocrinology 146(12):5561–5567PubMedCrossRefGoogle Scholar
  5. Arroyo EJ, Scherer SS (2007) The molecular organization of myelinating Schwann cells. In: Armati P (ed) The biology of Schwann cells. Cambridge University Press, New York, pp 37–54CrossRefGoogle Scholar
  6. Banerjee TK (2004) Fabry disease with special reference to neurological manifestations. Eur Rev Med Pharmacol Sci 8:275–281PubMedGoogle Scholar
  7. Bolin LM, Iismaa TP, Shooter EM (1992) Isolation of activated adult Schwann cells and a spontaneously immortal Schwann cell clone. J Neurosci Res 33(2):231–238PubMedCrossRefGoogle Scholar
  8. Brannan CI, Perkins AS, Vogel KS, Ratner N, Nordlund ML, Reid SW, Buchberg AM, Jenkins NA, Parada LF, Copeland NG (1994) Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes Dev 8(9):1019–1029PubMedCrossRefGoogle Scholar
  9. Brockes JP, Fryxell KJ, Lemke GE (1981) Studies on cultured Schwann cells: the induction of myelin synthesis, and the control of their proliferation by a new growth factor. J Exp Biol 95:215–230PubMedGoogle Scholar
  10. Bunge RP (1993) Expanding roles for the Schwann cell: ensheathment, myelination, trophism and regeneration. Curr Opin Neurobiol 3(5):805–809PubMedCrossRefGoogle Scholar
  11. Calcutt NA, Allendoerfer KL, Mizisin AP, Middlemas A, Freshwater JD, Burgers M, Ranciato R, Delcroix JD, Taylor FR, Shapiro R, Strauch K, Dudek H, Engber TM, Galdes A, Rubin LL, Tomlinson DR (2003) Therapeutic efficacy of sonic hedgehog protein in experimental diabetic neuropathy. J Clin Invest 111(4):507–514PubMedCentralPubMedCrossRefGoogle Scholar
  12. Camby I, Le Mercier M, Lefranc F, Kiss R (2006) Galectin-1: a small protein with major functions. Glycobiology 16(11):137R–157RPubMedCrossRefGoogle Scholar
  13. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C, Gu J, Rosenfeld MA, Pavan WJ, Krizman DB, Nagle J, Polymeropoulos MH, Sturley SL, Ioannou YA, Higgins ME, Comly M, Cooney A, Brown A, Kaneski CR, Blanchette-Mackie EJ, Dwyer NK, Neufeld EB, Chang TY, Liscum L, Strauss JF 3rd, Ohno K, Zeigler M, Carmi R, Sokol J, Markie D, O’Neill RR, van Diggelen OP, Elleder M, Patterson MC, Brady RO, Vanier MT, Pentchev PG, Tagle DA (1997) Niemann–Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 277(5323):228–231PubMedCrossRefGoogle Scholar
  14. Chi H, Horie H, Hikawa N, Takenaka T (1993) Isolation and age-related characterization of mouse Schwann cells from dorsal root ganglion explants in type I collagen gels. J Neurosci Res 35(2):183–187PubMedCrossRefGoogle Scholar
  15. Cichowski K, Jacks T (2001) NF1 tumor suppressor gene function: narrowing the GAP. Cell 104(4):593–604PubMedCrossRefGoogle Scholar
  16. Cooper DN, Barondes SH (1990) Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J Cell Biol 110(5):1681–1691PubMedCrossRefGoogle Scholar
  17. De Vries GH, Boullerne AI (2010) Glial cell lines: an overview. Neurochem Res 35(12):1978–2000PubMedCrossRefGoogle Scholar
  18. Dyck PJ, Giannini C (1996) Pathologic alterations in the diabetic neuropathies of humans: a review. J Neuropathol Exp Neurol 55(12):1181–1193PubMedCrossRefGoogle Scholar
  19. Eccleston PA, Mirsky R, Jessen KR (1991) Spontaneous immortalisation of Schwann cells in culture: short-term cultured Schwann cells secrete growth inhibitory activity. Development (Camb) 112(1):33–42Google Scholar
  20. Eckersley L (2002) Role of the Schwann cell in diabetic neuropathy. Int Rev Neurobiol 50:293–321PubMedCrossRefGoogle Scholar
  21. Fleming CE, Mar FM, Franquinho F, Sousa MM (2009) Transthyretin: an enhancer of nerve regeneration. Int Rev Neurobiol 87:337–346PubMedCrossRefGoogle Scholar
  22. Friedman B, Scherer SS, Rudge JS, Helgren M, Morrisey D, McClain J, Wang D, Wiegand SJ, Furth ME, Lindsay RM, Ip NY (1992) Regulation of ciliary neurotrophic factor expression in myelin-related Schwann cells in vivo. Neuron 9(2):295–305PubMedCrossRefGoogle Scholar
  23. Fukunaga M, Miyata S, Liu BF, Miyazaki H, Hirota Y, Higo S, Hamada Y, Ueyama S, Kasuga M (2004) Methylglyoxal induces apoptosis through activation of p38 MAPK in rat Schwann cells. Biochem Biophys Res Commun 320(3):689–695PubMedCrossRefGoogle Scholar
  24. Giese KP, Martini R, Lemke G, Soriano P, Schachner M (1992) Mouse P0 gene disruption leads to hypomyelination, abnormal expression of recognition molecules, and degeneration of myelin and axons. Cell 71(4):565–576PubMedCrossRefGoogle Scholar
  25. Gingras M, Beaulieu MM, Gagnon V, Durham HD, Berthod F (2008) In vitro study of axonal migration and myelination of motor neurons in a three-dimensional tissue-engineered model. Glia 56:354–364PubMedCrossRefGoogle Scholar
  26. Gustavsson P, Linsmeier CE, Leffler H, Kanje M (2007) Galectin-3 inhibits Schwann cell proliferation in cultured sciatic nerve. Neuroreport 18(7):669–673PubMedCrossRefGoogle Scholar
  27. Haastert K, Mauritz C, Chaturvedi S, Grothe C (2007) Human and rat adult Schwann cell cultures: fast and efficient enrichment and highly effective non-viral transfection protocol. Nat Protoc 2(1):99–104PubMedCrossRefGoogle Scholar
  28. Hashimoto M, Ishii K, Nakamura Y, Watabe K, Kohsaka S, Akazawa C (2008) Neuroprotective effect of sonic hedgehog up-regulated in Schwann cells following sciatic nerve injury. J Neurochem 107(4):918–927PubMedGoogle Scholar
  29. Horie H, Inagaki Y, Sohma Y, Nozawa R, Okawa K, Hasegawa M, Muramatsu N, Kawano H, Horie M, Koyama H, Sakai I, Takeshita K, Kowada Y, Takano M, Kadoya T (1999) Galectin-1 regulates initial axonal growth in peripheral nerves after axotomy. J Neurosci 19(22):9964–9974PubMedGoogle Scholar
  30. Horie H, Kadoya T, Hikawa N, Sango K, Inoue H, Takeshita K, Asawa R, Hiroi T, Sato M, Yoshioka T, Ishikawa Y (2004) Oxidized galectin-1 stimulates macrophages to promote axonal regeneration in peripheral nerves after axotomy. J Neurosci 24(8):1873–1880PubMedCrossRefGoogle Scholar
  31. Ito Y, Wiese S, Funk N, Chittka A, Rossoll W, Bömmel H, Watabe K, Wegner M, Sendtner M (2006) Sox10 regulates ciliary neurotrophic factor gene expression in Schwann cells. Proc Natl Acad Sci USA 103(20):7871–7876PubMedCrossRefGoogle Scholar
  32. Kawashima I, Watabe K, Tajima Y, Fukushige T, Kanzaki T, Kanekura T, Sugawara K, Ohyanagi N, Suzuki T, Togawa T, Sakuraba H (2007) Establishment of immortalized Schwann cells from Fabry mice and their low uptake of recombinant alpha-galactosidase. J Hum Genet 52(12):1018–1025PubMedCrossRefGoogle Scholar
  33. Kieseier BC, Hu W, Hartung H-P (2007) Schwann cells as immunomodulatory cells. In: Armati P (ed) The biology of Schwann cells. Cambridge University Press, New York, pp 118–125CrossRefGoogle Scholar
  34. Kleitman N, Wood PM, Bunge RP (1998) Tissue culture methods for the study of myelination. In: Banker G, Goslin K (eds) Culturing nerve cells, 2nd edn. MIT Press, Cambridge, pp 545–594Google Scholar
  35. Kobayashi T, Yamanaka T, Jacobs JM, Teixeira F, Suzuki K (1980) The Twitcher mouse: an enzymatically authentic model of human globoid cell leukodystrophy (Krabbe disease). Brain Res 202(2):479–483PubMedCrossRefGoogle Scholar
  36. Lehmann HC, Höke A (2010) Schwann cells as a therapeutic target for peripheral neuropathies. CNS Neurol Disord Drug Targets 9(6):801–806PubMedCrossRefGoogle Scholar
  37. Lehmann HC, Köhne A, Bernal F, Jangouk P, Meyer Zu Hörste G, Dehmel T, Hartung HP, Previtali SC, Kieseier BC (2009) Matrix metalloproteinase-2 is involved in myelination of dorsal root ganglia neurons. Glia 57:479–489PubMedCrossRefGoogle Scholar
  38. Li R (1998) Culture methods for selective growth of normal rat and human Schwann cells. Methods Cell Biol 57:167–186PubMedCrossRefGoogle Scholar
  39. Loftus SK, Morris JA, Carstea ED, Gu JZ, Cummings C, Brown A, Ellison J, Ohno K, Rosenfeld MA, Tagle DA, Pentchev PG, Pavan WJ (1997) Murine model of Niemann–Pick C disease: mutation in a cholesterol homeostasis gene. Science 277(5323):232–235PubMedCrossRefGoogle Scholar
  40. Magnaghi V, Procacci P, Tata AM (2009) Novel pharmacological approaches to Schwann cells as neuroprotective agents for peripheral nerve regeneration. Int Rev Neurobiol 87:295–315PubMedCrossRefGoogle Scholar
  41. Mathon NF, Malcolm DS, Harrisingh MC, Cheng L, Lloyd AC (2001) Lack of replicative senescence in normal rodent glia. Science 291(5505):872–875PubMedCrossRefGoogle Scholar
  42. Mirsky R, Jessen KR (2007) Early events in Schwann cell development. In: Armati P (ed) The biology of Schwann cells. Cambridge University Press, New York, pp 13–36CrossRefGoogle Scholar
  43. Miyawaki S, Mitsuoka S, Sakiyama T, Kitagawa T (1982) Sphingomyelinosis, a new mutation in the mouse: a model of Niemann–Pick disease in humans. J Hered 73(4):257–263PubMedGoogle Scholar
  44. Mizisin AP, Li L, Perello M, Freshwater JD, Kalichman MW, Roux L, Calcutt NA (1996) Polyol pathway and osmoregulation in JS1 Schwann cells grown in hyperglycemic and hyperosmotic conditions. Am J Physiol 270(1 pt 2):F90–F97PubMedGoogle Scholar
  45. Muir D, Varon S, Manthorpe M (1990) Schwann cell proliferation in vitro is under negative autocrine control. J Cell Biol 111(6 pt 1):2663–2671PubMedCrossRefGoogle Scholar
  46. Murakami T, Ohsawa Y, Zhenghua L, Yamamura K, Sunada Y (2010) The transthyretin gene is expressed in Schwann cells of peripheral nerves. Brain Res 1348:222–225PubMedCrossRefGoogle Scholar
  47. Naureckiene S, Sleat DE, Lackland H, Fensom A, Vanier MT, Wattiaux R, Jadot M, Lobel P (2000) Identification of HE1 as the second gene of Niemann–Pick C disease. Science 290(5500):2298–2301PubMedCrossRefGoogle Scholar
  48. Nishikawa T, Araki E (2007) Impact of mitochondrial ROS production in the pathogenesis of diabetes mellitus and its complications. Antioxid Redox Signal 9(3):343–353PubMedCrossRefGoogle Scholar
  49. Ogata T, Iijima S, Hoshikawa S, Miura T, Yamamoto S, Oda H, Nakamura K, Tanaka S (2004) Opposing extracellular signal-regulated kinase and Akt pathways control Schwann cell myelination. J Neurosci 24(30):6724–6732PubMedCrossRefGoogle Scholar
  50. Ohsawa M, Kotani M, Tajima Y, Tsuji D, Ishibashi Y, Kuroki A, Itoh K, Watabe K, Sango K, Yamanaka S, Sakuraba H (2005) Establishment of immortalized Schwann cells from Sandhoff mice and corrective effect of recombinant human beta-hexosaminidase A on the accumulated GM2 ganglioside. J Hum Genet 50(9):460–467PubMedCrossRefGoogle Scholar
  51. Ohshima T, Murray GJ, Swaim WD, Longenecker G, Quirk JM, Cardarelli CO, Sugimoto Y, Pastan I, Gottesman MM, Brady RO, Kulkarni AB (1997) Alpha-galactosidase A deficient mice: a model of Fabry disease. Proc Natl Acad Sci USA 94(6):2540–2544PubMedCrossRefGoogle Scholar
  52. Ota K, Nakamura J, Li W, Kozakae M, Watarai A, Nakamura N, Yasuda Y, Nakashima E, Naruse K, Watabe K, Kato K, Oiso Y, Hamada Y (2007) Metformin prevents methylglyoxal-induced apoptosis of mouse Schwann cells. Biochem Biophys Res Commun 357(1):270–275PubMedCrossRefGoogle Scholar
  53. Padilla A, Descorbeth M, Almeyda AL, Payne K, De Leon M (2011) Hyperglycemia magnifies Schwann cell dysfunction and cell death triggered by PA-induced lipotoxicity. Brain Res 1370:64–79PubMedCentralPubMedCrossRefGoogle Scholar
  54. Paratcha G, Ledda F, Ibáñez CF (2003) The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113(7):867–879PubMedCrossRefGoogle Scholar
  55. Peden KW, Charles C, Sanders L, Tennekoon GI (1989) Isolation of rat Schwann cell lines: use of SV40 T antigen gene regulated by synthetic metallothionein promoters. Exp Cell Res 185(1):60–72PubMedCrossRefGoogle Scholar
  56. Pentchev PG, Gal AE, Booth AD, Omodeo-Sale F, Fouks J, Neumeyer BA, Quirk JM, Dawson G, Brady RO (1980) A lysosomal storage disorder in mice characterized by a dual deficiency of sphingomyelinase and glucocerebrosidase. Biochim Biophys Acta 619(3):669–679PubMedCrossRefGoogle Scholar
  57. Plachta N, Annaheim C, Bissière S, Lin S, Rüegg M, Hoving S, Müller D, Poirier F, Bibel M, Barde YA (2007) Identification of a lectin causing the degeneration of neuronal processes using engineered embryonic stem cells. Nat Neurosci 10(6):712–719PubMedCrossRefGoogle Scholar
  58. Porter S, Glaser L, Bunge RP (1987) Release of autocrine growth factor by primary and immortalized Schwann cells. Proc Natl Acad Sci USA 84(21):7768–7772PubMedCrossRefGoogle Scholar
  59. Pricci F, Leto G, Amadio L, Iacobini C, Romeo G, Cordone S, Gradini R, Barsotti P, Liu FT, Di Mario U, Pugliese G (2000) Role of galectin-3 as a receptor for advanced glycosylation end products. Kidney Int Suppl 77:S31–S39PubMedCrossRefGoogle Scholar
  60. Sandhoff K (2001) The GM2 gangliosidoses and the elucidation of the β-hexosaminidase system. In: Desnick RJ, Kaback MM (eds) Tay–Sachs disease, vol 44, Advances in genetics. Academic, San Diego, pp 67–91Google Scholar
  61. Sango K, Verdes JM, Hikawa N, Horie H, Tanaka S, Inoue S, Sotelo JR, Takenaka T (1994) Nerve growth factor (NGF) restores depletions of calcitonin gene-related peptide and substance P in sensory neurons from diabetic mice in vitro. J Neurol Sci 126(1):1–5PubMedCrossRefGoogle Scholar
  62. Sango K, Yamanaka S, Hoffmann A, Okuda Y, Grinberg A, Westphal H, McDonald MP, Crawley JN, Sandhoff K, Suzuki K, Proia RL (1995) Mouse models of Tay–Sachs and Sandhoff diseases differ in neurologic phenotype and ganglioside metabolism. Nat Genet 11(2):170–176PubMedCrossRefGoogle Scholar
  63. Sango K, Tokashiki A, Ajiki K, Horie M, Kawano H, Watabe K, Horie H, Kadoya T (2004) Synthesis, localization and externalization of galectin-1 in mature dorsal root ganglion neurons and Schwann cells. Eur J Neurosci 19(1):55–64PubMedCrossRefGoogle Scholar
  64. Sango K, Saito H, Takano M, Tokashiki A, Inoue S, Horie H (2006a) Cultured adult animal neurons and Schwann cells give us new insights into diabetic neuropathy. Curr Diabetes Rev 2(2):169–183PubMedCrossRefGoogle Scholar
  65. Sango K, Suzuki T, Yanagisawa H, Takaku S, Hirooka H, Tamura M, Watabe K (2006b) High glucose-induced activation of the polyol pathway and changes of gene expression profiles in immortalized adult mouse Schwann cells IMS32. J Neurochem 98(2):446–458PubMedCrossRefGoogle Scholar
  66. Sango K, Yanagisawa H, Komuta Y, Si Y, Kawano H (2008a) Neuroprotective properties of ciliary neurotrophic factor for cultured adult rat dorsal root ganglion neurons. Histochem Cell Biol 130(4):669–679PubMedCrossRefGoogle Scholar
  67. Sango K, Yanagisawa H, Kato K, Kato N, Hirooka H, Watabe K (2008b) Differential effects of high glucose and methylglyoxal on viability and polyol metabolism in immortalized adult mouse Schwann cells. Open Diabetes J 1:1–11CrossRefGoogle Scholar
  68. Sango K, Yanagisawa H, Kawakami E, Takaku S, Ajiki K, Watabe K (2011a) Spontaneously immortalized Schwann cells from adult Fischer rat as a valuable tool for exploring neuron-Schwann cell interactions. J Neurosci Res 89(6):898–908PubMedCrossRefGoogle Scholar
  69. Sango K, Yanagisawa H, Takaku S, Kawakami E, Watabe K (2011b) Immortalized adult rodent Schwann cells as in vitro models to study diabetic neuropathy. Exp Diabetes Res 2011:374943PubMedCentralPubMedCrossRefGoogle Scholar
  70. Sango K, Yanagisawa H, Watabe K, Horie H, Kadoya T (2012a) Galectin-1 as a multifunctional molecule in the peripheral nervous system after injury. In: Rayegani SM (ed) Basic principles of peripheral nerve disorders. InTech Doo, Rijeka, pp 31–46 http://www.intechopen.com/books/basic-principles-of-peripheral-nerve-disorders/galectin-1-as-a-multifunctional-molecule-in-the-peripheral-nervous-system-after-injury Google Scholar
  71. Sango K, Kawakami E, Yanagisawa H, Takaku S, Tsukamoto M, Utsunomiya K, Watabe K (2012b) Myelination in coculture of established neuronal and Schwann cell lines. Histochem Cell Biol 137(6):829–839PubMedCrossRefGoogle Scholar
  72. Sasaki T, Hirabayashi J, Manya H, Kasai K, Endo T (2004) Galectin-1 induces astrocyte differentiation, which leads to production of brain-derived neurotrophic factor. Glycobiology 14(4):357–363PubMedCrossRefGoogle Scholar
  73. Sendtner M, Stockli KA, Thoenen H (1992) Synthesis and localization of ciliary neurotrophic factor in the sciatic nerve of the adult rat after lesion and during regeneration. J Cell Biol 118(1):139–148PubMedCrossRefGoogle Scholar
  74. Shen JS, Watabe K, Meng XL, Ida H, Ohashi T, Eto Y (2002) Establishment and characterization of spontaneously immortalized Schwann cells from murine model of globoid cell leukodystrophy (twitcher). J Neurosci Res 68(5):588–594PubMedCrossRefGoogle Scholar
  75. Song Z, Fu DT, Chan YS, Leung S, Chung SS, Chung SK (2003) Transgenic mice overexpressing aldose reductase in Schwann cells show more severe nerve conduction velocity deficit and oxidative stress under hyperglycemic stress. Mol Cell Neurosci 23(4):638–647PubMedCrossRefGoogle Scholar
  76. Sousa MM, Saraiva MJ (2003) Neurodegeneration in familial amyloid polyneuropathy: from pathology to molecular signaling. Prog Neurobiol 71(5):385–400PubMedCrossRefGoogle Scholar
  77. Sugimoto K, Yasujima M, Yagihashi S (2008) Role of advanced glycation end products in diabetic neuropathy. Curr Pharm Des 14(10):953–961PubMedCrossRefGoogle Scholar
  78. Suzuki K, Vanier MT, Suzuki K (1999) Lysosomal disorders. In: Popko B (ed) Mouse models in the study of genetic neurological disorders, vol 9, Advances in neurochemistry. Kluwer, New York, pp 245–283CrossRefGoogle Scholar
  79. Suzuki J, Akahane K, Nakamura J, Naruse K, Kamiya H, Himeno T, Nakamura N, Shibata T, Kondo M, Nagasaki H, Fujiya A, Oiso Y, Hamada Y (2011) Palmitate induces apoptosis in Schwann cells via both ceramide-dependent and independent pathways. Neuroscience 176:188–198PubMedCrossRefGoogle Scholar
  80. Takaku S, Yanagisawa H, Watabe K, Horie H, Kadoya T, Sakumi K, Nakabeppu Y, Poirier F, Sango K (2013) GDNF promotes neurite outgrowth and upregulates galectin-1 through the RET/PI3K signaling in cultured adult rat dorsal root ganglion neurons. Neurochem Int 62(3):330–339PubMedCrossRefGoogle Scholar
  81. Toda K, Small JA, Goda S, Quarles RH (1994) Biochemical and cellular properties of three immortalized Schwann cell lines expressing different levels of the myelin-associated glycoprotein. J Neurochem 63(5):1646–1657PubMedCrossRefGoogle Scholar
  82. Tosaki T, Kamiya H, Yasuda Y, Naruse K, Kato K, Kozakae M, Nakamura N, Shibata T, Hamada Y, Nakashima E, Oiso Y, Nakamura J (2008) Reduced NGF secretion by Schwann cells under the high glucose condition decreases neurite outgrowth of DRG neurons. Exp Neurol 213(2):381–387PubMedCrossRefGoogle Scholar
  83. Traiffort E, Angot E, Ruat M (2010) Sonic Hedgehog signaling in the mammalian brain. J Neurochem 113(3):576–590PubMedCrossRefGoogle Scholar
  84. Verdú E, Ceballos D, Vilches JJ, Navarro X (2000) Influence of aging on peripheral nerve function and regeneration. J Peripher Nerv Syst 5(4):191–208PubMedCrossRefGoogle Scholar
  85. Watabe K, Yamada M, Kawamura T, Kim SU (1990) Transfection and stable transformation of adult mouse Schwann cells with SV-40 large T antigen gene. J Neuropathol Exp Neurol 49(5):455–467PubMedCrossRefGoogle Scholar
  86. Watabe K, Fukuda T, Tanaka J, Toyohara K, Sakai O (1994) Mitogenic effects of platelet-derived growth factor, fibroblast growth factor, transforming growth factor-beta, and heparin-binding serum factor for adult mouse Schwann cells. J Neurosci Res 39(5):525–534PubMedCrossRefGoogle Scholar
  87. Watabe K, Fukuda T, Tanaka J, Honda H, Toyohara K, Sakai O (1995) Spontaneously immortalized adult mouse Schwann cells secrete autocrine and paracrine growth-promoting activities. J Neurosci Res 41(2):279–290PubMedCrossRefGoogle Scholar
  88. Watabe K, Ida H, Uehara K, Oyanagi K, Sakamoto T, Tanaka J, Garver WS, Miyawaki S, Ohno K, Eto Y (2001) Establishment and characterization of immortalized Schwann cells from murine model of Niemann–Pick disease type C (spm/spm). J Peripher Nerv Syst 6(2):85–94PubMedCrossRefGoogle Scholar
  89. Watabe K, Sakamoto T, Kawazoe Y, Michikawa M, Miyamoto K, Yamamura T, Saya H, Araki N (2003) Tissue culture methods to study neurological disorders: establishment of immortalized Schwann cells from murine disease models. Neuropathology 23(1):68–78PubMedCrossRefGoogle Scholar
  90. Yamauchi J, Miyamoto Y, Chan JR, Tanoue A (2008) ErbB2 directly activates the exchange factor Dock7 to promote Schwann cell migration. J Cell Biol 181(2):351–365PubMedCrossRefGoogle Scholar
  91. Zhang L, Ma Z, Smith GM, Wen X, Pressman Y, Wood PM, Xu XM (2009) GDNF-enhanced axonal regeneration and myelination following spinal cord injury is mediated by primary effects on neurons. Glia 57:1178–1191PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2014

Authors and Affiliations

  • Kazunori Sango
    • 1
    Email author
  • Masami Tsukamoto
    • 2
    • 3
  • Kazunori Utsunomiya
    • 3
  • Kazuhiko Watabe
    • 1
  1. 1.ALS/Neuropathy Project, Department of Sensory and Motor SystemsTokyo Metropolitan Institute of Medical ScienceSetagaya-kuJapan
  2. 2.Laboratory of Peripheral Nerve Pathophysiology (ALS/Neuropathy Project), Department of Sensory and Motor SystemsTokyo Metropolitan Institute of Medical ScienceSetagaya-kuJapan
  3. 3.Division of Diabetes, Metabolism and Endocrinology, Department of Internal MedicineJikei University School of MedicineMinato-kuJapan

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