Impaired hypoglossal nerve regeneration in mutant mice lacking complex gangliosides: Down-regulation of neurotrophic factors and receptors as possible mechanisms

Glycobiology

Volumn 18, Issue 7, 2008, Pages 509-516

  Kittaka, Daiji ^a   Itoh, Michi Ichirou ^b   Ohmi, Yuhsuke ^a   Kondo, Yuji ^a   Fukumoto, Satoshi ^a   Urano, Takeshi ^a   Tajima, Orie ^a,c   Furukawa, Keiko ^a,c   Furukawa, Koichi ^a  

^a NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b Department of Oral and Maxillofacial Surgery ^*  (Japan)

^c CHUBU UNIVERSITY   (Japan)

Author keywords

Gangliosides; Hypoglossal nerve; Knockout; Neurotrophic factor; Regeneration

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CILIARY NEUROTROPHIC FACTOR RECEPTOR; GANGLIOSIDE; GANGLIOSIDE GD2; GANGLIOSIDE GM2; NEUROTROPHIC FACTOR; NEUROTROPHIC FACTOR RECEPTOR; NEUROTROPHIN RECEPTOR P75; PEROXIDASE; RECEPTOR PROTEIN; SYNTHETASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; GROWTH REGULATION; HYPOGLOSSAL NERVE DISEASE; LASER CAPTURE MICRODISSECTION; MOUSE; NERVE CELL; NERVE FIBER TRANSECTION; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; REGENERATIVE ABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CILIARY NEUROTROPHIC FACTOR; DOWN-REGULATION; GANGLIOSIDES; HYPOGLOSSAL NERVE; MICE; MICE, KNOCKOUT; N-ACETYLGALACTOSAMINYLTRANSFERASES; NERVE GROWTH FACTORS; NERVE REGENERATION; RECEPTOR, TRKB; RECEPTORS, NERVE GROWTH FACTOR;

MUS;

EID: 45749084909     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwn032     Document Type: Article

References (43)

1. Barati S, Hurtado PR, Zhang SH, Tinsley R, Ferguson IA, Rush RA. 2006. GDNF gene delivery via the p75(NTR) receptor rescues injured motor neurons. Exp Neurol. 202:179-188.
2. Barras FM, Pasche P, Bouche N, Aebischer P, Zum AD. 2002. Glial cell line-derived neurotrophic factor released by synthetic guidance channels promotes facial nerve regeneration in the rat. J Neurosci Res. 70:746-755.
3. Blesch A and Tuszynski MH. 2001. GDNF gene delivery to injured adult CNS motor neurons promotes axonal growth, expression of the trophic neuropeptide CGRP, and cellular protection. J Comp Neurol. 436:399-410.
4. Chiavegatto S, Sun J, Nelson RJ, Schnaar RL. 2000. A functional role for complex gangliosides: Motor deficits in GM2/GD2 synthase knockout mice. Exp Neurol. 166:227-234.
5. Chiu AY, Chen EW, Loera S. 1994. Distinct neurotrophic responses of axotomized motor neurons to BDNF and CNTF in adult rats. Neuroreport 5:693-696.
6. English AW, Meador W, Carrasco DI. 2005. Neurotrophin-4/5 is required for the early growth of regenerating axons in peripheral nerves. Eur J Neurosci. 21:2624-2634.
7. Fukumoto S, Mutoh T, Hasegawa T, Miyazaki H, Okada M, Goto G, Furukawa K, Urano T, Furukawa K. 2000. GD3 synthase gene expression in PC12 cells results in the continuous activation of TrkA and ERK1/2 and enhanced proliferation. J Biol Chem. 275:5832-5838.
8. Fukumoto S, Yamamoto A, Hasegawa T, Abe K, Takamiya K, Okada M, Min ZJ, Furukawa K, Miyazaki H, Tsuji Y, et al. 1997. Genetic remodeling of gangliosides resulted in the enhanced reactions to the foreign substances in skin. Glycobiology. 7:1111-1120.
9. Funakoshi H, Risling M, Carlstedt T, Lendahl U, Timmusk T, Metsis M, Yamamoto Y, Ibanez CF. 1998. Targeted expression of a multifunctional chimeric neurotrophin in the lesioned sciatic nerve accelerates regeneration of sensory and motor axons. Proc Natl Acad Sci USA. 95:5269-5274.
10. Furukawa K, Takamiya K, Okada M, Inoue M, Fukumoto S, Furukawa K. 2001. Novel functions of complex carbohydrates elucidated by the mutant mice of glycosyltransferase genes. Biochim Biophys Acta. 1525:1-12.
11. Haraguchi M, Yamashiro S, Yamamoto A, Furukawa K, Takamiya K, Lloyd KO, Shiku H, Furukawa K. 1994. Proc Natl Acad Sci USA. 91:10455-10459.
12. Honma M, Namikawa K, Mansur K, Iwata T, Mori N, Iizuka H, Kiyama H. 2002. Developmental alteration of nerve injury induced glial cell line-derived neurotrophic factor (GDNF) receptor expression is crucial for the determination of injured motoneuron fate. J Neurochem. 82:961-975.
13. Inoue M, Fujii Y, Furukawa K, Okada M, Okumura K, Hayakawa T, Furukawa K, Sugiura Y. 2002. Refractory skin injury in the complex knock-out mice expressing only GM3 ganglioside. J Biol Chem. 277:29881-29888.
14. Itoh M, Fukumoto S, Kiso M, Kuga Y, Mizuno A, Furukawa K. 2001. Specificity of carbohydrate structures of gangliosides in the activity to regenerate the rat axotomized hypoglossal nerve. Glycobiology. 11:125-130.
15. Itoh M, Fukumoto S, Kuga Y, Mizuno A, Furukawa K. 1999. Prevention of the death of the rat axotomized hypoglossal nerve and promotion of its regeneration by bovine brain gangliosides. Glycobiology. 9:1247-1252.
16. Karpiak SE. 1984. Exogenous gangliosides enhance recovery from cns injury. Adv Exp Med Biol. 174:489-497.
17. Karpiak SE and Mahadik SPJ. 1984. Reduction of cerebral edema with GM1 ganglioside. Neurosci Res. 12:485-492.
18. -DCg method. Methods. 25:402-408.
19. Ledeen R, Yu RK. 1982. Ganglioside: Structure, isolation, analysis. Methods Enzymol. 83:139-190.
20. Lehmann HC, Lopez PH, Zhang G, Ngyuen T, Zhang J, Kieseier BC, Mori S, Sheikh KA. 2007. Passive immunization with anti-ganglioside antibodies directly inhibits axon regeneration in an animal model. J Neurosci 27:27-34.
21. Marth JD. 1994. Will the transgenic mouse serve as a Rosetta stone to glyco-conjugate function? Glycoconj J. 11:3-8.
22. Meyer M, Matsuoka I, Wetmore C, Olson L, Thoenen H. 1992. Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: Different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J Cell Biol. 119:45-54.
23. Mutoh T, Tokuda A, Miyadai T, Hamaguchi, M, Fujiki N. 1995. Ganglioside GM1 binds to the Trk protein and regulates receptor function. Proc Natl Acad Sci USA. 92:5087-5091.
24. Nagata Y, Yamashiro S, Yodoi J, Lloyd KO, Shiku H, Furukawa K. 1992. Expression cloning of β1,4-N-acetylgalalctosaminyltransferase cDNAs that determine the expression of GM2 and GD2 gangliosides. J Biol Chem. 267:12082-12089.
25. Nishio M, Fukumoto S, Furukawa K, Ichimura A, Miyazaki H, Kusunoki S, Urano T, Furukawa K. 2004. Over-expressed GM1 suppresses NGF signals by modulating the intra-cellular localization of NGF receptors and membrane fluidity in PC12 cells. J Biol Chem. 279:33368-33378.
26. Okada M, Itoh M, Haraguchi M, Okajima T, Inoue M, Ohishi H, Matsuda Y, Iwamoto T, Kawano T, Fukumoto S, et al. 2002. b-series ganglioside deficiency exhibits no definite changes in the neurogenesis and the sensitivity to Fas-mediated apotosis, but impairs regeneration of the lesioned hypoglossal nerve. J Biol Chem. 277:1633-1636.
27. Pitto M, Mutoh T, Kuriyama M, Ferraretto A, Palestini P, Masserini M. 1998. Influence of endogenous GM1 ganglioside on Trkb activity, in cultured neurons. FEBS Lett. 439:93-96.
28. Russell FD, Koishi K, Jiang Y, McLennan IS. 2000. Anterograde axonal transport of glial cell line-derived neurotrophic factor and its receptors in rat hypoglossal nerve. Neuroscience. 97:575-580.
29. Schengrund CL. 1990. The role(s) of gangliosides in neural differentiation and repair: A perspective. Brain Res Bull. 4:131-141.
30. Schneider JS, Pope A, Simpson K, Taggart J, Smith MJ, DiStefano L. 1992. Recovery from experimental parkinsonism in primates with GM1 ganglioside treatment. Science. 256:843-846.
31. Sheikh KA, Sun J, Liu Y, Kawai H, Crawford TO, Proia RL, Griffin JW, Schnaar RL. 1999. Mice lacking complex gangliosides develop Wallerian degeneration and myelination defects. Proc Natl Acad Sci USA. 96:7532-7537.
32. Smith GM, Rabinovsky ED, McManaman JL, Shine HD. 1993. Temporal and spatial expression of ciliary neurotrophic factor after peripheral nerve injury. Exp Neurol. 121:239-247.
33. Sugiura Y, Furukawa K, Tajima O, Mii T, Honda T, Furukawa K. 2005. Sensory nerve-dominant nerve degeneration and remodeling in the mutant mice lacking complex gangliosides. Neuroscience. 135:1167-1178.
34. Suzuki K. 1965. The pattern of mammalian brain gangliosides: II. Evaluation of the extraction procedures, postmortem changes and the effect of formalin preservation. J Neurochem. 12:629-638.
35. Susuki K, Baba H, Tohyama K, Kanai K, Kuwabara S, Hirata K, Furukawa K, Furukawa K, Rasband MN, Yuki N. 2007. Gangliosides contribute to stability of paranodal junctions and ion channel clusters in myelinated nerve fibers. Glia. 55:746-757.
36. Svennerholm, L. 1963. Chromatographic separation of human brain gangliosides. J Neurochem. 10:455-463.
37. Takamiya K, Yamamoto A, Furukawa K, Yamashiro, S, Shin M, Okada M, Fukumoto S, Haraguchi M, Takeda N, Fujimura K, et al. 1996. Mice with disrupted GM2/GD2 synthase gene lack complex gangliosides but exhibit only subtle defects in their nervous system. Proc Natl Acad Sci USA 93:10662-10667.
38. Tsujino H, Mansur K, Kiryu-Seo S, Namikawa. K, Kitahara T, Tanabe K, Ochi T, Kiyama H. 1999. Discordant expression of c-Ret and glial cell fine-derived neurotrophic factor receptor alpha-1 mRNAs in response to motor nerve injury in neonate rats. Brain Res Mol Brain Res. 70:298-303.
39. Tuszynski MU, Mafong E, Meyer S. 1996. Central infusions of brain-derived neurotrophic factor and neurotrophin-4/5, but not nerve growth factor and neurotrophin-3, prevent loss of the cholinergic phenotype in injured adult motor neurons. Neuroscience. 71:761-771.
40. Wang W, Salvaterra PM, Loera S, Chiu AY. 1997. Brain-derived neurotrophic factor spares choline acetyltransferase mRNA following axotomy of motor neurons in vivo. J Neurosci Res. 47:134-143.
41. Wiegandt H. 1985. Gangliosisdes. In: Wiegandt H, editor. Glycolipids Amsterdam: Elsevier. p. 199-260.
42. Yamashita T, Wu YP, Sandhoff R, Werth N, Mizukami H, Ellis JM, Dupree JL, Geyer R, Sandhoff K, Proia, RL. 2005. Interruption of ganglioside synthesis produces central nervous system degeneration and altered axon-glial interactions. Proc Natl Acad Sci USA. 102:2725-2730.
43. Zhang J, Lineaweaver WC, Oswald T, Chen Z, Chen Z, Zhang F. 2004. Ciliary neurotrophic factor for acceleration of peripheral nerve regeneration: An experimental study. J Reconstr Microsurg. 20:323-327.