Gangliosides are essential in the protection of inflammation and neurodegeneration via maintenance of lipid rafts: Elucidation by a series of ganglioside-deficient mutant mice

Journal of Neurochemistry

Volumn 116, Issue 5, 2011, Pages 926-935

  Ohmi, Yuhsuke ^a   Tajima, Orie ^a,b   Ohkawa, Yuki ^a   Yamauchi, Yoshio ^a   Sugiura, Yasuo ^a   Furukawa, Keiko ^a,b   Furukawa, Koichi ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b CHUBU UNIVERSITY   (Japan)

Author keywords

complement; ganglioside; inflammation; knockout; neurodegeneration; raft

Indexed keywords

CAVEOLIN 1; CELL ADHESION MOLECULE; CHOLESTEROL; COMPLEMENT COMPONENT C1Q; FLOTILLIN 1; GANGLIOSIDE; INTERLEUKIN 1BETA; PHOSPHOLIPID; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL ADHESION; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; ENCEPHALITIS; GENE EXPRESSION; IMMUNOBLOTTING; LIPID COMPOSITION; LIPID RAFT; MICROGLIA; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; UPREGULATION;

AGE FACTORS; ANIMALS; ASTROCYTES; CELL PROLIFERATION; CEREBELLUM; CHOLESTEROL; CHROMATOGRAPHY, THIN LAYER; DISEASE MODELS, ANIMAL; GANGLIOSIDES; INFLAMMATION; INTERLEUKIN-1BETA; MEMBRANE MICRODOMAINS; MICE; MICE, KNOCKOUT; N-ACETYLGALACTOSAMINYLTRANSFERASES; NEURODEGENERATIVE DISEASES; RNA, MESSENGER; SIALYLTRANSFERASES; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

MUS;

EID: 79851474972     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.07067.x     Document Type: Article

References (47)

1. Barnum S. R., (2002) Complement in central nervous system inflammation. Immunol. Res. 26, 7-13. (Pubitemid 35177479)
2. Bénard M., Gonzalez B. J., Schouft M. T., Falluel-Morel A., Vaudry D., Chan P., Vaudry H., and, Fontaine M., (2004) Characterization of C3a and C5a receptors in rat cerebellar granule neurons during maturation: neuroprotective effect of C5a against apoptotic cell death. J. Biol. Chem. 279, 43487-43496. (Pubitemid 39390648)
3. Chen H. H., Fukumoto S., Furukawa K., Nakao A., Akiyama S., Urano T., and, Furukawa K., (2003) Suppression of lung metastasis of mouse Lewis lung cancer P29 with transfection of the ganglioside GM2/GD2 synthase gene. Int. J. Cancer 103, 169-176. (Pubitemid 35461508)
4. Clark J. D., Gebhart G. F., Gonder J. C., Keeling M. E., and, Kohn D. F., (1997) The 1996 guide for the care and use of laboratory animals. ILAR J. 38, 41-48.
5. Farkas I., Takahashi M., Fukuda A., et al. (2003) Complement C5a receptor-mediated signaling may be involved in neurodegeneration in Alzheimer's disease. J. Immunol. 170, 5764-5771. (Pubitemid 36617870)
6. Folch J., Lees M., and, Sloane-Stanley G. H., (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509.
7. Furukawa K., Clausen H., Hakomori S., Sakamoto J., Look K., Lundblad A., Mattes M. J., and, Lloyd K. O., (1985) Analysis of the specificity of five murine anti-blood group A monoclonal antibodies, including one that identifies type 3 and type 4 determinants. Biochemistry 24, 7820-7826. (Pubitemid 16140520)
8. Furukawa K., Tajima O., Okuda T., Tokuda N., and, Furukawa K., (2007) Knockout mice and glycolipids, in Comprehensive Glycoscience. From Chemistry to Systems Biology (, Kamerling J. P., Boons G. J., Lee Y. C., Suzuki A., Taniguchi N., and, Voragen A. G. J., eds), pp. 149-157. Elsevier, Oxford.
9. Gasque P., Dean Y. D., McGreal E. P., VanBeek J., and, Morgan B. P., (2000) Complement components of the innate immune system in health and disease in the CNS. Immuno-pharmacology 49, 171-186. (Pubitemid 30445228)
10. Inoue M., Fujii Y., Furukawa K., Okada M., Okumura K., Hayakawa T., Furukawa K., and, Sugiura Y., (2002) Refractory skin injury in the complex knock-out mice expressing only GM3 ganglioside. J. Biol. Chem. 277, 29881-29888.
11. Jennemann R., Sandhoff R., Wang S., et al. (2005) Cell-specific deletion of glucosyl- ceramide synthase in brain leads to severe neural defects after birth. Proc. Natl Acad. Sci. USA 102, 12459-12464. (Pubitemid 41266381)
12. Kinoshita T., Fujita M., and, Maeda Y., (2008) Biosynthesis, remodelling and functions of mammalian GPI-anchored proteins: recent progress. J. Biochem. 144, 287-294.
13. Kittaka D., Itoh M., Ohmi Y., Kondo Y., Fukumoto S., Urano T., Tajima O., Furukawa K., and, Furukawa K., (2008) Impaired hypoglossal nerve regeneration in complex ganglioside-lacking mutant mice: down-regulation of neurotrophic factors and receptors as possible mechanisms. Glycobiology 18, 509-516. (Pubitemid 351865831)
14. Li Q., Zhang Q., Zhang M., Wang C., Zhu Z., Li N., and, Li J., (2008) Effect of n-3 polyunsaturated fatty acids on membrane microdomain localization of tight junction proteins in experimental colitis. FEBS J. 275, 411-420.
15. Lin F., Salant D. J., Meyerson H., Emancipator S., Morgan B. P., and, Medof M. E., (2004) Respective roles of decay-accelerating factor and CD59 in circumventing glomerular injury in acute nephrotoxic serum nephritis. J. Immunol. 172, 2636-2642. (Pubitemid 38185803)
16. Mason J. C., Yarwood H., Sugars K., Morgan B. P., Davies K. A., and, Haskard D. O., (1999) Induction of decay-accelerating factor by cytokines or the membrane-attack complex protects vascular endothelial cells against complement deposition. Blood 94, 1673-1682. (Pubitemid 29411317)
17. McGeer E. G., and, McGeer P. L., (1998) The importance of inflammatory mechanisms in Alzheimer disease. Exp. Gerontol. 33, 371-378. (Pubitemid 28354931)
18. Michel V., and, Bakovic M., (2007) Lipid rafts in health and disease. Biol. Cell 99, 129-140. (Pubitemid 46380925)
19. Mitsuda T., Furukawa K., Fukumoto S., Miyazaki H., Urano T., and, Furukawa K., (2002) Over-expression of ganglioside GM1 results in the dispersion of platelet derived growth factor receptor from glycolipid-enriched microdomains and in the suppression of cell growth signals. J. Biol. Chem. 277, 11239-11246. (Pubitemid 34952887)
20. Morgan B. P., Chamberlain-Banoub J., Neal J. W., Song W., Mizuno M., and, Harris C. L., (2006) The membrane attack pathway of complement drives pathology in passively induced experimental autoimmune myasthenia gravis in mice. Clin. Exp. Immunol. 146, 294-302. (Pubitemid 44581345)
21. Nishio M., Fukumoto S., Furukawa K., Ichimura A., Miyazaki H., Kusunoki S., Urano T., and, Furukawa K., (2004) Overexpressed GM1 suppresses nerve growth factor (NGF) signals by modulating the intracellular localization of NGF receptors and membrane fluidity in PC12 cells. J. Biol. Chem. 279, 33368-33378. (Pubitemid 39062985)
22. Ohmi Y., Tajima O., Ohkawa Y., Mori A., Sugiura Y., Furukawa K., and, Furukawa K., (2009) Gangliosides play pivotal roles in the regulation of complement systems and in the maintenance of integrity in nerve tissues. Proc. Natl Acad. Sci. USA 106, 22405-22410.
23. Okada M., Itoh Mi M., Haraguchi M., et al. (2002) b-series Ganglioside deficiency exhibits no definite changes in the neurogenesis and the sensitivity to Fas-mediated apoptosis, but impairs regeneration of the lesioned hypoglossal nerve. J Biol Chem 277, 1633-1636. (Pubitemid 34968730)
24. Pike L. J., (2006) Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 47, 1597-1598. (Pubitemid 44079915)
25. Rahpeymai Y., Hietala M. A., Wilhelmsson U., et al. (2006) Complement: a novel factor in basal and ischemia-induced neurogenesis. EMBO J. 25, 1364-1374.
26. Rodemer C., Thai T. P., Brugger B., Kaercher T., Werner H., Nave K. A., Wieland F., Gorgas K., and, Just W. W., (2003) Inactivation of ether lipid biosynthesis causes male infertility, defects in eye development and optic nerve hypoplasia in mice. Hum. Mol. Genet. 12, 1881-1895. (Pubitemid 36944142)
27. Rogers J., and, Shen Y., (2000) A perspective on inflammation in Alzheimer's disease. Ann. N Y Acad. Sci. 924, 132-135. (Pubitemid 32050194)
28. Rogers J., Cooper N. R., Webster S., et al. (1992) Complement activation by beta-amyloid in Alzheimer disease. Proc. Natl Acad. Sci. USA 89, 10016-10020.
29. Schengrund C. L., (1990) The roles of gangliosides in neural differentiation and repair: a perspective. Brain Res. Bull. 24, 131-141.
30. Sheikh K. A., Sun J., Liu Y., Kawai H., Crawford T. O., Proia R. L., Griffin J. W., and, Schnaar R. L., (1999) Mice lacking complex gangliosides develop Wallerian degeneration and myelination defects. Proc. Natl Acad. Sci. USA 96, 7532-7537. (Pubitemid 29299696)
31. Shen Y., Lue L., Yang L., et al. (2001) Complement activation by neurofibrillary tangles in Alzheimer's disease. Neurosci. Lett. 305, 165-168. (Pubitemid 32525831)
32. Simons K., and, Ikonen E., (1997) Functional rafts in cell membranes. Nature 387, 569-572. (Pubitemid 27248754)
33. Stevens B., Allen N. J., Vazquez L. E., et al. (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131, 1164-1178. (Pubitemid 350235022)
34. Sugiura Y., Furukawa K., Tajima O., Mii S., Honda T., and, Furukawa K., (2005) Sensory nerve-dominant nerve degeneration and remodeling in the mutant mice lacking complex gangliosides. Neuroscience 135, 1167-1178. (Pubitemid 41416679)
35. Tajima O., Egashira N., Ohmi Y., et al. (2009) Reduced motor and sensory functions and emotional response in GM3-only mice: emergence from early stage of life and exacerbation with aging. Behav. Brain Res. 198, 74-82.
36. Takamiya K., Yamamoto A., Furukawa 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. (Pubitemid 26333045)
37. Tenner A. J., (2001) Complement in Alzheimer's disease: opportunities for modulating protective and pathogenic events. Neurobiol. Aging 22, 849-861. (Pubitemid 34066552)
38. Terai K., Walker D. G., McGeer E. G., and, McGeer P. L., (1997) Neurons express proteins of the classical complement pathway in Alzheimer disease. Brain Res. 769, 385-390. (Pubitemid 27461477)
39. Toledo M. S., Suzuki E., Handa K., and, Hakomori S., (2005) Effect of ganglioside and tetraspanins in microdomains on interaction of integrins with fibroblast growth factor receptor. J. Biol. Chem. 280, 16227-16234. (Pubitemid 40616749)
40. Truedsson L., Bengtsson A. A., and, Sturfelt G., (2007) Complement deficiencies and systemic lupus erythematosus. Autoimmunity 40, 560-566. (Pubitemid 350302182)
41. White A. B., Givogri M. I., Lopez-Rosas A., Cao H., van Breemen R., Thinakaran G., and, Bongarzone E. R., (2009) Psychosine accumulates in membrane microdomains in the brain of krabbe patients, disrupting the raft architecture. J. Neurosci. 29, 6068-6077.
42. Wyss-Coray T., Yan F., Lin A. H., Lambris J. D., Alexander J. J., Quigg R. J., and, Masliah E., (2002) Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice. Proc. Natl Acad. Sci. USA 99, 10837-10842.
43. Yamada K., Miwa T., Liu J., Nangaku M., and, Song W. C., (2004) Critical protection from renal ischemia reperfusion injury by CD55 and CD59. J. Immunol. 172, 3869-3875. (Pubitemid 38337974)
44. Yamashita T., Wada R., Sasaki T., Deng C., Bierfreund U., Sandhoff K., and, Proia R. L., (1999) A vital role for glycosphingolipid synthesis during development and differentiation. Proc. Natl Acad. Sci. USA 96, 9142-9147. (Pubitemid 29374721)
45. Yang L. B., Li R., Meri S., Rogers J., and, Shen Y., (2000) Deficiency of complement defense protein CD59 may contribute to neurodegeneration in Alzheimer's disease. J. Neurosci. 20, 7505-7509.
46. Yasojima K., Schwab C., McGeer E. G., and, McGeer P. L., (1999) Up-regulated production and activation of the complement system in Alzheimer's disease brain. Am. J. Pathol. 154, 927-936. (Pubitemid 29122612)
47. Zhang Q., Furukawa K., Chen H. H., Sakakibara T., Urano T., and, Furukawa K., (2006) Metastatic potential of mouse Lewis lung cancer cells is regulated via ganglioside GM1 by modulating the matrix metalloprotease-9 localization in lipid rafts. J. Biol. Chem. 281, 18145-18155. (Pubitemid 44035614)