C-terminal region of teneurin-1 co-localizes with dystroglycan and modulates cytoskeletal organization through an extracellular signal-regulated kinase-dependent stathmin- and filamin A-mediated mechanism in hippocampal cells

Neuroscience

Volumn 219, Issue , 2012, Pages 255-270

  Chand, D ^a   Song, L ^a   Delannoy, L ^a   Barsyte Lovejoy, D ^a,b   Ackloo, S ^c   Boutros, P C ^d   Evans, K ^c   Belsham, D D ^e   Lovejoy, D A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b Structural Genomics Consortium MaRS Centre   (Canada)

^c MaRS Centre   (Canada)

^d ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cytoskeleton; Dystroglycan; Hippocampus; Neuropeptide; Stress; Teneurin

Indexed keywords

BETA DYSTROGLYCAN; FILAMIN A; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUROPEPTIDE; SERINE; STATHMIN; TENEURIN 1; TENEURIN C TERMINAL ASSOCIATED PEPTIDE 1; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; DENTATE GYRUS; EMBRYO; FILOPODIUM; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; MICROTUBULE ASSEMBLY; MOUSE; NERVE CELL MEMBRANE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PYRAMIDAL NERVE CELL;

ANIMALS; BLOTTING, WESTERN; CONTRACTILE PROTEINS; CYTOSKELETON; DYSTROGLYCANS; FLUORESCENT ANTIBODY TECHNIQUE; HIPPOCAMPUS; MAP KINASE SIGNALING SYSTEM; MICE; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; NEUROGENESIS; PYRAMIDAL CELLS; STATHMIN; TENASCIN;

EID: 84864002990     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.05.069     Document Type: Article

References (57)

1. Al Chawaf A., St.Amant K., Belsham D.D., Lovejoy D.A. Regulation of neurite outgrowth in immortalized hypothalamic cells and hippocampal primary cultures by teneurin C-terminal associate peptide-1 (TCAP-1). Neuroscience 2007, 144:1241-1254.
2. Al Chawaf A., Xu K., Tan L., Vaccarino F.J., Lovejoy D.A., Rotzinger S. Corticotropin-releasing factor (CRF)-induced behaviors are modulated by intravenous administration of teneurin C-terminal associated peptide-1 (TCAP-1). Peptides 2007, 28:1406-1415.
3. Baumgartner S., Martin D., Hagios C., Chiquet-Ehrismann R. Tenm, a Drosophila gene related to tenascin is a new pair-rule gene. EMBO J 1994, 13:3728-3740.
4. Ben-Zur T., Feige E., Motro B., Wides R. The mammalian Odz gene family: homologs of a Drosophila pair-rule gene with expression implying distinct yet overlapping developmental roles. Dev Biol 2000, 217:107-120.
5. Beretta L., Dobransky T., Sobel A. Multiple phosphorylation of stathmin. J Biol Chem 1993, 268:20076-20084.
6. Bohil A.B., Robertson B.W., Cheney R.E. Myosin-X is a molecular motor that functions in filopodia formation. Proc Natl Acad Sci USA 2006, 103:12411-12416.
7. Cassimeris L. The oncoprotein 18/stathmin family of microtubule destabilizers. Curr Opin Cell Biol 2002, 14:18-24.
8. Cavaldesi M., Macchia G., Barca S., Defilippi P., Tarone G., Petrucci T.C. Association of the dystroglycan complex isolated from bovine brain synaptosomes with proteins involved in signal transduction. J Neurochem 1999, 72:1648-1655.
9. Chen Y.J., Spence H.J., Cameron J.M., Jess T., Ilsley J.L., Winder S.J. Direct interaction of beta-dystroglycan with F-actin. Biochem J 2003, 375:329-337.
10. Curmi P.A., Gavet O., Charbaut E., Ozon S., Lachkar-Colmerauer S., Manceau V., Siavoshian S., Maucuer A., Sobel A. Stathmin and its phosphoprotein family: general properties, biochemical and functional interaction with tubulin. Cell Struct Funct 1999, 24:345-357.
11. DiPaolo G., Pellier V., Catsicas M., Antonsson B., Catsicas S., Grenningloh G. The phosphoprotein stathmin is essential for nerve growth factor-stimulated differentiation. J Cell Biol 1996, 133:1383-1390.
12. Doye V., Boutterin M.C., Sobel A. Phosphorylation of stathmin and other proteins related to nerve growth factor-induced regulation of PC12 cells. J Biol Chem 1990, 265:11650-11655.
13. Feng K., Zhou X.H., Oohashi T., Morgelin M., Lustig A., Hirakawa S., Ninomiya Y., Engel J., Rauch U., Fassler R. All four members of the ten-m/Odz family of transmembrane proteins form dimers. J Biol Chem 2002, 277:26128-26135.
14. Gavet O., Pines J. Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev Cell 2010, 18:533-543.
15. Gingerich S., Kim G.L., Chalmers J.A., Koletar M.M., Wang X., Wang Y., Belsham D.D. Estrogen receptor α and G-protein coupled receptor 30 mediate the neuroprotective effects of 17β-estradiol in novel murine hippocampal cell models. Neuroscience 2010, 170:54-66.
16. Grutzendler J., Kasthuri N., Gan W.B. Long-term dendritic spine stability in the adult cortex. Nature 2002, 420:812-816.
17. Gu J., Firestein B.L., Zheng J.Q. Microtubules in dendritic spine development. J Neurosci 2008, 28:12120-12124.
18. Hailat N., Strahler J., Melhem R., Zhu X.X., Brodeur G., Seeger R.C., Reynolds C.P., Hanash S. N-myc gene amplification in neuroblastoma is associated with altered phosphorylation of a proliferation related polypeptide (Op18). Oncogene 1990, 5:1615-1618.
19. Hotulainen P., Hoogenraad C.C. Actin in dendritic spines: connecting dynamics to function. J Cell Biol 2010, 189:619-629.
20. Johnston S.A., Bramble J.P., Yeung C.L., Mendes P.M., Machesky L.M. Arp2/3 complex activity in filopodia of spreading cells. BMC Cell Biol 2008, 9:65.
21. Kater S.B., Rehder V. The sensory-motor role of growth cone filopodia. Curr Opin Neurobiol 1995, 5:68-74.
22. Kenzelmann D., Chiquet-Ehrismann R., Leachman N.T., Tucker R.P. Teneurin-1 is expressed in interconnected regions of the developing brain and is processed in vivo. BMC Dev Biol 2008, 8:30.
23. Kenzelmann D., Chiquet-Ehrismann R., Tucker R.P. Teneurins, a transmembrane protein family involved in cell communication during neuronal development. Cell Mol Life Sci 2007, 64:1452-1456.
24. Kupferschmidt D.A., Lovejoy D.A., Rotzinger S., Erb S. Teneurin C-terminal associated peptide (TCAP)-1 blocks the effects of corticotropin-releasing factor on reinstatement of cocaine seeking and on cocaine-induced behavioural sensitization. Br J Pharmacol 2011, 162:574-583.
25. Leamey C.A., Merlin S., Lattouf P., Sawatari A., Zhou X., Demel N., Glendining K.A., Oohashi T., Sur M., Fassler R. Ten-m3 regulates eye-specific patterning in the mammalian visual pathway and is required for binocular vision. PLoS Biol 2007, 5:e241.
26. Leighton I.A., Curmi P., Campbell D.G., Cohen P., Sobel A. The phosphorylation of stathmin by MAP kinase. Mol Cell Biochem 1993, 127-128:151-156.
27. Levine A., Bashan-Ahrend A., Budai-Hadrian O., Gartenberg D., Menasherow S., Wides R. Odd Oz: a novel Drosophila pair-rule gene. Cell 1994, 77:587-598.
28. Lin C.H., Espreafico E.M., Mooseker M.S., Forscher P. Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 1996, 16:769-782.
29. Lossie A.C., Nakamura H., Thomas S.E., Justice M.J. Mutation of l7Rn3 shows that Odz4 is required for mouse gastrulation. Genetics 2005, 169:285-299.
30. Manna T., Thrower D.A., Honnappa S., Steinmetz M.O., Wilson L. Regulation of microtubule dynamic instability in vitro by differentially phosphorylated stathmin. J Biol Chem 2009, 284:15640-15649.
31. Matsumoto-Miyai K., Sokolowska E., Zurlinden A., Gee C.E., Lüscher D., Hettwer S., Wölfel J., Ladner A.P., Ster J., Gerber U., Rülicke T., Kunz B., Sonderegger P. Coincident pre- and postsynaptic activation induces dendritic filopodia via neurotrypsin-dependent agrin cleavage. Cell 2009, 136:1161-1171.
32. Minet A.D., Rubin B.P., Tucker R.P., Baumgartner S., Chiquet-Ehrismann R. Teneurin-1, a vertebrate homologue of the Drosophila pair-rule gene ten-m, is a neuronal protein with a novel type of heparin-binding domain. J Cell Sci 1999, 112:2019-2032.
33. Ng D.C., Zhao T.T., Yeap Y.Y., Ngoei K.R., Bogoyevitch M.A. C-Jun N-terminal kinase phosphorylation of stathmin confers protection against cellular stress. J Biol Chem 2010, 285:29001-29013.
34. Nunes S.M., Ferralli J., Choi K., Brown-Luedi M., Minet A.D., Chiquet-Ehrismann R. The intracellular domain of teneurin-1 interacts with MBD1 and CAP/ponsin resulting in subcellular codistribution and translocation to the nuclear matrix. Exp Cell Res 2005, 305:122-132.
35. O'Leary D.D.M., Fawcett J.W., Cowan W.M. Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death. J Neurosci 1986, 6:3692-3705.
36. Palazzo A.F., Eng C.H., Schlaepfer D.D., Marcantonio E.E., Gundersen G.G. Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science 2004, 303:836-839.
37. Qian X., Barsyte-Lovejoy D., Wang L., Chewpoy B., Gautam N., Al Chawaf A., Lovejoy D.A. Cloning and characterization of teneurin C-terminus associated peptide (TCAP)-3 from the hypothalamus of an adult rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 2004, 137:205-216.
38. Rubin B.P., Tucker R.P., Brown-Luedi M., Martin D., Chiquet-Ehrismann R. Teneurin 2 is expressed by the neurons of the thalamofugal visual system in situ and promotes homophilic cell-cell adhesion in vitro. Development 2002, 129:4697-4705.
39. Rubin B.P., Tucker R.P., Martin D., Chiquet-Ehrismann R. Teneurins: a novel family of neuronal cell surface proteins in vertebrates, homologous to the Drosophila pair-rule gene product Ten-m. Dev Biol 1999, 216:195-209.
40. Smalheiser N.R., Schwartz N.B. Cranin: a laminin-binding protein of cell membranes. Proc Natl Acad Sci USA 1987, 84:6457-6461.
41. Spence H.J., Dhillon A.S., James M., Winder S.J. Dystroglycan, a scaffold for the ERK-MAP kinase cascade. EMBO Rep 2004, 5:484-489.
42. Stossel T.P., Condeelis J., Cooley L., Hartwig J.H., Noegel A., Schleicher M., Shapiro S.S. Filamins as integrators of cell mechanics and signalling. Nat Rev Mol Cell Biol 2001, 2:138-145.
43. Sydor A.M., Su A.L., Wang F.S., Xu A., Jay D.G. Talin and vinculin play distinct roles in filopodial motility in the neuronal growth cone. J Cell Biol 1996, 134:1197-1207.
44. Tada T., Sheng M. Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol 2006, 16:95-101.
45. Tan L.A., Al Chawaf A., Vaccarino F.J., Boutros P.C., Lovejoy D.A. Teneurin C-terminal associated peptide (TCAP)-1 modulates dendritic morphology in hippocampal neurons and decreases anxiety-like behaviors in rats. Physiol Behav 2011, 104:199-204.
46. Tan L.A., Xu K., Vaccarino F.J., Lovejoy D.A., Rotzinger S. Repeated intracerebral teneurin C-terminal associated peptide (TCAP)-1 injections produce enduring changes in behavioral responses to corticotropin-releasing factor (CRF) in rat models of anxiety. Behav Brain Res 2008, 188:195-200.
47. Tan L.A., Xu K., Vaccarino F.J., Lovejoy D.A., Rotzinger S. Teneurin C-terminal associated peptide (TCAP)-1 attenuates corticotropin-releasing factor (CRF)-induced c-Fos expression in the limbic system and modulates anxiety behavior in male Wistar rats. Behav Brain Res 2009, 201:198-206.
48. Trzebiatowska A., Topf U., Sauder U., Drabikowski K., Chiquet-Ehrismann R. Caenorhabditis elegans teneurin, ten-1, is required for gonadal and pharyngeal basement membrane integrity and acts redundantly with integrin ina-1 and dystroglycan dgn-1. Mol Biol Cell 2008, 19:3898-3908.
49. Tucker R.P., Kenzelmann D., Trzebiatowska A., Chiquet-Ehrismann R. Teneurins: transmembrane proteins with fundamental roles in development. Int J Biochem Cell Biol 2007, 39:292-297.
50. Ujike H., Takaki M., Kodama M., Kuroda S. Gene expression related to synaptogenesis, neuritogenesis, and MAP kinase in behavioral sensitization to psychostimulants. Ann NY Acad Sci 2002, 965:55-67.
51. Wang L., Rotzinger S., Barsyte-Lovejoy D., Qian X., Elias C.F., Bittencourt J.C., De Cristofaro A., Wang N.C., Belsham D., Vaccarino F., Lovejoy D.A. Teneurin proteins possess a carboxy terminal corticotropin-releasing factor-like sequence that modulates emotionality and neuronal growth. Mol Brain Res 2005, 133:253-265.
52. Winder S.J. The complexities of dystroglycan. Trends Biochem Sci 2001, 26:118-124.
53. Woo M.S., Ohta Y., Rabinovitz I., Stossel T.P., Blenis J. Ribosomal S6 kinase (RSK) regulates phosphorylation of filamin A on an important regulatory site. Mol Cell Biol 2004, 24:3025-3035.
54. Wood W., Martin P. Structures in focus-filopodia. Int J Biochem Cell Biol 2002, 34:726-730.
55. Zaccaria M.L., Di Tommaso F., Brancaccio A., Paggi P., Petrucci T.C. Dystroglycan distribution in adult mouse brain: a light and electron microscopy study. Neuroscience 2001, 104:311-324.
56. Zhang W., Wu Y., Du L., Tang D.D., Gunst S.J. Activation of the Arp2/3 complex by N-WASp is required for actin polymerization and contraction in smooth muscle. Am J Physiol Cell Physiol 2005, 288:1145-1160.
57. Zhou X.H., Brandau O., Feng K., Oohashi T., Ninomiya Y., Rauch U., Fässler R. The murine Ten-m/Odz genes show distinct but overlapping expression patterns during development and in adult brain. Gene Expr Patterns 2003, 3:397-405.