Neuronal glycoprotein M6a induces filopodia formation via association with cholesterol-rich lipid rafts

Journal of Neurochemistry

Volumn 119, Issue 3, 2011, Pages 521-531

  Scorticati, Camila ^a   Formoso, Karina ^a   Frasch, Alberto C ^a  

^a INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

Author keywords

filopodia formation; lipid membrane microdomains; methyl cyclodextrin; mitogen activated protein kinase; proteolipid protein family; Src kinases

Indexed keywords

CHOLESTEROL; MEMBRANE PROTEIN; MESSENGER RNA; METHYL BETA CYCLODEXTRIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN M6A; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME INHIBITION; FILOPODIUM; HIPPOCAMPUS; LIPID RAFT; NERVE CELL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CHOLESTEROL; COS CELLS; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE MICRODOMAINS; NERVE TISSUE PROTEINS; NEURONS; PROTEIN BINDING; PSEUDOPODIA; RATS; RATS, SPRAGUE-DAWLEY;

ANIMALIA; RATTUS;

EID: 80054065715     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07252.x     Document Type: Article

References (51)

1. Alfonso J., Fernandez M. E., Cooper B., Flugge G., and, Frasch A. C., (2005a) The stress-regulated protein M6a is a key modulator for neurite outgrowth and filopodium/spine formation. Proc. Natl Acad. Sci. USA 102, 17196-17201. (Pubitemid 41692706)
2. Alfonso J., Frasch A. C., and, Flugge G., (2005b) Chronic stress, depression and antidepressants: effects on gene transcription in the hippocampus. Rev. Neurosci. 16, 43-56. (Pubitemid 40444829)
3. Alfonso J., Frick L. R., Silberman D. M., Palumbo M. L., Genaro A. M., and, Frasch A. C., (2006) Regulation of hippocampal gene expression is conserved in two species subjected to different stressors and antidepressant treatments. Biol. Psychiatry 59, 244-251. (Pubitemid 43208971)
4. Bari M., Oddi S., De Simone C., Spagnolo P., Gasperi V., Battista N., Centonze D., and, Maccarrone M., (2008) Type-1 cannabinoid receptors colocalize with caveolin-1 in neuronal cells. Neuropharmacology 54, 45-50. (Pubitemid 350299413)
5. Baumrind N. L., Parkinson D., Wayne D. B., Heuser J. E., and, Pearlman A. L., (1992) EMA: a developmentally regulated cell-surface glycoprotein of CNS neurons that is concentrated at the leading edge of growth cones. Dev. Dyn. 194, 311-325. (Pubitemid 23015686)
6. Brocco M., Pollevick G. D., and, Frasch A. C., (2003) Differential regulation of polysialyltransferase expression during hippocampus development: implications for neuronal survival. J. Neurosci. Res. 74, 744-753. (Pubitemid 37475454)
7. Brocco M. A., Fernandez M. E., and, Frasch A. C., (2010) Filopodial protrusions induced by glycoprotein M6a exhibit high motility and aids synapse formation. Eur. J. Neurosci. 31, 195-202.
8. Cooper B., Werner H. B., and, Flugge G., (2008) Glycoprotein M6a is present in glutamatergic axons in adult rat forebrain and cerebellum. Brain Res. 1197, 1-12.
9. de Diesbach P., Medts T., Carpentier S., et al. (2008) Differential subcellular membrane recruitment of Src may specify its downstream signalling. Exp. Cell Res. 314, 1465-1479.
10. Duncan M. J., Li G., Shin J. S., Carson J. L., and, Abraham S. N., (2004) Bacterial penetration of bladder epithelium through lipid rafts. J. Biol. Chem. 279, 18944-18951. (Pubitemid 38623323)
11. Elyassaki W., and, Wu S., (2006) Lipid rafts mediate ultraviolet light-induced Fas aggregation in M624 melanoma cells. Photochem. Photobiol. 82, 787-792. (Pubitemid 44032802)
12. Fernandez M. E., Alfonso J., Brocco M. A., and, Frasch A. C., (2010) Conserved cellular function and stress-mediated regulation among members of the proteolipid protein family. J. Neurosci. Res. 88, 1298-1308.
13. Fuchsova B., Fernandez M. E., Alfonso J., and, Frasch A. C., (2009) Cysteine residues in the large extracellular loop (EC2) are essential for the function of the stress-regulated glycoprotein M6a. J. Biol. Chem. 284, 32075-32088.
14. Ge X., Qiu Y., Loh H. H., and, Law P. Y., (2009) GRIN1 regulates micro-opioid receptor activities by tethering the receptor and G protein in the lipid raft. J. Biol. Chem. 284, 36521-36534.
15. Gerits N., Shiryaev A., Kostenko S., Klenow H., Shiryaeva O., Johannessen M., and, Moens U., (2009) The transcriptional regulation and cell-specific expression of the MAPK-activated protein kinase MK5. Cell Mol. Biol. Lett. 14, 548-574.
16. Hering H., Lin C. C., and, Sheng M., (2003) Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci. 23, 3262-3271. (Pubitemid 36531967)
17. Hou Q., Huang Y., Amato S., Snyder S. H., Huganir R. L., and, Man H. Y., (2008) Regulation of AMPA receptor localization in lipid rafts. Mol. Cell. Neurosci. 38, 213-223.
18. Huang P., Xu W., Yoon S. I., Chen C., Chong P. L., and, Liu-Chen L. Y., (2007) Cholesterol reduction by methyl-beta-cyclodextrin attenuates the delta opioid receptor-mediated signaling in neuronal cells but enhances it in non-neuronal cells. Biochem. Pharmacol. 73, 534-549. (Pubitemid 46038858)
19. Klinghoffer R. A., Sachsenmaier C., Cooper J. A., and, Soriano P., (1999) Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J. 18, 2459-2471. (Pubitemid 29213279)
20. Kramer-Albers E. M., Gehrig-Burger K., Thiele C., Trotter J., and, Nave K. A., (2006) Perturbed interactions of mutant proteolipid protein/DM20 with cholesterol and lipid rafts in oligodendroglia: implications for dysmyelination in spastic paraplegia. J. Neurosci. 26, 11743-11752. (Pubitemid 44772145)
21. Lagenaur C., Kunemund V., Fischer G., Fushiki S., and, Schachner M., (1992) Monoclonal M6 antibody interferes with neurite extension of cultured neurons. J. Neurobiol. 23, 71-88.
22. Lee Y. C., Huang C. F., Murshed M., et al. (2010) Src family kinase/abl inhibitor dasatinib suppresses proliferation and enhances differentiation of osteoblasts. Oncogene 29, 3196-3207.
23. Liang Y. J., Wu D. F., Stumm R., Hollt V., and, Koch T., (2008) Membrane glycoprotein M6A promotes mu-opioid receptor endocytosis and facilitates receptor sorting into the recycling pathway. Cell Res. 18, 768-779. (Pubitemid 351948228)
24. Ligeza A., Wawrzczak-Bargiela A., Kaminska D., Korostynski M., and, Przewlocki R., (2008) Regulation of ERK1/2 phosphorylation by acute and chronic morphine-implications for the role of cAMP-responsive element binding factor (CREB)-dependent and Ets-like protein-1 (Elk-1)-dependent transcription; small interfering RNA-based strategy. FEBS J. 275, 3836-3849. (Pubitemid 351990949)
25. Mathew S., George S. P., Wang Y., Siddiqui M. R., Srinivasan K., Tan L., and, Khurana S., (2008) Potential molecular mechanism for c-Src kinase-mediated regulation of intestinal cell migration. J. Biol. Chem. 283, 22709-22722.
26. Meloche S., and, Pouyssegur J., (2007) The ERK1/2 mitogen-activated protein kinase pathway as a master regulator of the G1- to S-phase transition. Oncogene 26, 3227-3239. (Pubitemid 46763017)
27. Michibata H., Okuno T., Konishi N., et al. (2008) Inhibition of mouse GPM6A expression leads to decreased differentiation of neurons derived from mouse embryonic stem cells. Stem Cells Dev. 17, 641-651.
28. Michibata H., Okuno T., Konishi N., et al. (2009) Human GPM6A is associated with differentiation and neuronal migration of neurons derived from human embryonic stem cells. Stem Cells Dev. 18, 629-639.
29. Mobius W., Patzig J., Nave K. A., and, Werner H. B., (2008) Phylogeny of proteolipid proteins: divergence, constraints, and the evolution of novel functions in myelination and neuroprotection. Neuron Glia Biol. 4, 111-127.
30. Mukobata S., Hibino T., Sugiyama A., Urano Y., Inatomi A., Kanai Y., Endo H., and, Tashiro F., (2002) M6a acts as a nerve growth factor-gated Ca(2+) channel in neuronal differentiation. Biochem. Biophys. Res. Commun. 297, 722-728. (Pubitemid 35230310)
31. Nunez E., Alonso-Torres P., Fornes A., Aragon C., and, Lopez-Corcuera B., (2008) The neuronal glycine transporter GLYT2 associates with membrane rafts: functional modulation by lipid environment. J. Neurochem. 105, 2080-2090. (Pubitemid 351782243)
32. Ohvo H., and, Slotte J. P., (1996) Cyclodextrin-mediated removal of sterols from monolayers: effects of sterol structure and phospholipids on desorption rate. Biochemistry 35, 8018-8024. (Pubitemid 26202544)
33. Prinetti A., Iwabuchi K., and, Hakomori S., (1999) Glycosphingolipid- enriched signaling domain in mouse neuroblastoma Neuro2a cells. Mechanism of ganglioside-dependent neuritogenesis. J. Biol. Chem. 274, 20916-20924.
34. Ramseger R., White R., and, Kroger S., (2009) Transmembrane form agrin-induced process formation requires lipid rafts and the activation of Fyn and MAPK. J. Biol. Chem. 284, 7697-7705.
35. Rimmerman N., Hughes H. V., Bradshaw H. B., Pazos M. X., Mackie K., Prieto A. L., and, Walker J. M., (2008) Compartmentalization of endocannabinoids into lipid rafts in a dorsal root ganglion cell line. Br. J. Pharmacol. 153, 380-389.
36. Robin P., Boulven I., Desmyter C., Harbon S., and, Leiber D., (2002) ET-1 stimulates ERK signaling pathway through sequential activation of PKC and Src in rat myometrial cells. Am. J. Physiol. Cell Physiol. 283, C251-C260. (Pubitemid 34670569)
37. Roussel G., Trifilieff E., Lagenaur C., and, Nussbaum J. L., (1998) Immunoelectron microscopic localization of the M6a antigen in rat brain. J. Neurocytol. 27, 695-703. (Pubitemid 29230043)
38. Sanchez-Wandelmer J., Davalos A., de la Pena G., et al. (2010) Haloperidol disrupts lipid rafts and impairs insulin signaling in SH-SY5Y cells. Neuroscience 167, 143-153.
39. Schroeder F., Gallegos A. M., Atshaves B. P., et al. (2001) Recent advances in membrane microdomains: rafts, caveolae, and intracellular cholesterol trafficking. Exp. Biol. Med. (Maywood) 226, 873-890.
40. Sheetz M. P., Baumrind N. L., Wayne D. B., and, Pearlman A. L., (1990) Concentration of membrane antigens by forward transport and trapping in neuronal growth cones. Cell 61, 231-241.
41. Simons K., and, Ikonen E., (1997) Functional rafts in cell membranes. Nature 387, 569-572. (Pubitemid 27248754)
42. Simons K., and, Toomre D., (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39.
43. Simons M., Kramer E. M., Thiele C., Stoffel W., and, Trotter J., (2000) Assembly of myelin by association of proteolipid protein with cholesterol- and galactosylceramide-rich membrane domains. J. Cell Biol. 151, 143-154.
44. Simons M., Kramer E. M., Macchi P., Rathke-Hartlieb S., Trotter J., Nave K. A., and, Schulz J. B., (2002) Overexpression of the myelin proteolipid protein leads to accumulation of cholesterol and proteolipid protein in endosomes/lysosomes: implications for Pelizaeus-Merzbacher disease. J. Cell Biol. 157, 327-336. (Pubitemid 34839828)
45. Waheed A. A., Shimada Y., Heijnen H. F., Nakamura M., Inomata M., Hayashi M., Iwashita S., Slot J. W., and, Ohno-Iwashita Y., (2001) Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts). Proc. Natl Acad. Sci. USA 98, 4926-4931. (Pubitemid 32397059)
46. Wu D. F., Koch T., Liang Y. J., Stumm R., Schulz S., Schroder H., and, Hollt V., (2007) Membrane glycoprotein M6a interacts with the micro-opioid receptor and facilitates receptor endocytosis and recycling. J. Biol. Chem. 282, 22239-22247. (Pubitemid 47195768)
47. Yan Y., Lagenaur C., and, Narayanan V., (1993) Molecular cloning of M6: identification of a PLP/DM20 gene family. Neuron 11, 423-431. (Pubitemid 23287070)
48. Yanez-Mo M., Barreiro O., Gordon-Alonso M., Sala-Valdes M., and, Sanchez-Madrid F., (2009) Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol. 19, 434-446.
49. Zhao J., Iida A., Ouchi Y., Satoh S., and, Watanabe S., (2008) M6a is expressed in the murine neural retina and regulates neurite extension. Mol. Vis. 14, 1623-1630.
50. Zhao H., Cao X., Wu G., Loh H. H., and, Law P. Y., (2009) Neurite outgrowth is dependent on the association of c-Src and lipid rafts. Neurochem. Res. 34, 2197-2205.
51. Zhu D., Xiong W. C., and, Mei L., (2006) Lipid rafts serve as a signaling platform for nicotinic acetylcholine receptor clustering. J. Neurosci. 26, 4841-4851. (Pubitemid 44315325)