Teneurin-4 promotes cellular protrusion formation and neurite outgrowth through focal adhesion kinase signaling

FASEB Journal

Volumn 28, Issue 3, 2014, Pages 1386-1397

  Suzuki, Nobuharu ^a,b   Numakawa, Tadahiro ^c   Chou, Joshua ^b   De Vega, Susana ^b,d   Mizuniwa, Chihiro ^a   Sekimoto, Kaori ^a   Adachi, Naoki ^c   Kunugi, Hiroshi ^c   Arikawa Hirasawa, Eri ^d   Yamada, Yoshihiko ^b   Akazawa, Chihiro ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^d JUNTENDO UNIVERSITY   (Japan)

Author keywords

Cytoskeleton; Neuronal differentiation

Indexed keywords

FOCAL ADHESION KINASE; MEMBRANE PROTEIN; MESSENGER RNA; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PROTEIN CDC42; RAC1 PROTEIN; SMALL INTERFERING RNA; TENEURIN 4; UNCLASSIFIED DRUG; ODZ4 PROTEIN, MOUSE; PRIMER DNA;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELLULAR PROTRUSION FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; GROWTH CONE; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEURITE; NEUROBLASTOMA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CYTOSKELETON; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

CYTOSKELETON; NEURONAL DIFFERENTIATION;

ANIMALS; BASE SEQUENCE; DNA PRIMERS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; MEMBRANE PROTEINS; MICE; NEURITES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84899549628     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-241034     Document Type: Article

References (33)

1. Tucker, R. P., and Chiquet-Ehrismann, R. (2006) Teneurins: a conserved family of transmembrane proteins involved in intercellular signaling during development. Dev. Biol. 290, 237-245
2. Levine, A., Bashan-Ahrend, A., Budai-Hadrian, O., Gartenberg, D., Menasherow, S., and Wides, R. (1994) Odd Oz: a novel Drosophila pair rule gene. Cell 77, 587-598
3. Zheng, L., Michelson, Y., Freger, V., Avraham, Z., Venken, K. J., Bellen, H. J., Justice, M. J., and Wides, R. (2011) Drosophila Ten-m and filamin affect motor neuron growth cone guidance. PLoS One 6, e22956
4. Mosca, T. J., Hong, W., Dani, V. S., Favaloro, V., and Luo, L. (2012) Trans-synaptic Teneurin signalling in neuromuscular synapse organization and target choice. Nature 484, 237-241
5. Hong, W., Mosca, T. J., and Luo, L. (2012) Teneurins instruct synaptic partner matching in an olfactory map. Nature 484, 201-207
6. Morck, C., Vivekanand, V., Jafari, G., and Pilon, M. (2010) C. elegans ten-1 is synthetic lethal with mutations in cytoskeleton regulators, and enhances many axon guidance defective mutants. BMC Dev. Biol. 10, 55
7. Rubin, B. P., Tucker, R. P., Brown-Luedi, M., Martin, D., and Chiquet-Ehrismann, R. (2002) Teneurin 2 is expressed by the neurons of the thalamofugal visual system in situ and promotes homophilic cell-cell adhesion in vitro. Development 129, 4697-4705
8. Li, H., Bishop, K. M., and O'Leary, D. D. (2006) Potential target genes of EMX2 include Odz/Ten-M and other gene families with implications for cortical patterning. Mol. Cell. Neurosci. 33, 136-149
9. Leamey, C. A., Merlin, S., Lattouf, P., Sawatari, A., Zhou, X., Demel, N., Glendining, K. A., Oohashi, T., Sur, M., and Fassler, R. (2007) Ten-m3 regulates eye-specific patterning in the mammalian visual pathway and is required for binocular vision. PLoS Biol. 5, e241
10. Minet, A. D., Rubin, B. P., Tucker, R. P., Baumgartner, S., and Chiquet-Ehrismann, R. (1999) 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. 112, 2019-2032
11. Rubin, B. P., Tucker, R. P., Martin, D., and Chiquet-Ehrismann, R. (1999) Teneurins: a novel family of neuronal cell surface proteins in vertebrates, homologous to the Drosophila pair-rule gene product Ten-m. Dev. Biol. 216, 195-209
12. Young, T. R., Bourke, M., Zhou, X., Oohashi, T., Sawatari, A., Fassler, R., and Leamey, C. A. (2013) Ten-m2 is required for the generation of binocular visual circuits. J. Neurosci. 33, 12490-12509
13. Suzuki, N., Fukushi, M., Kosaki, K., Doyle, A. D., de Vega, S., Yoshizaki, K., Akazawa, C., Arikawa-Hirasawa, E., and Yamada, Y. (2012) Teneurin-4 is a novel regulator of oligodendrocyte differentiation and myelination of small-diameter axons in the CNS. J. Neurosci. 32, 11586-11599
14. Sklar, P., Ripke, S., Scott, L. J., Andreassen, O. A., Cichon, S., Craddock, N., Edenberg, H. J., Nurnberger, J. I., Jr., Rietschel, M., Blackwood, D., Corvin, A., Flickinger, M., Guan, W., Mattingsdal, M., McQuillin, A., Kwan, P., Wienker, T. F., Daly, M., Dudbridge, F., Holmans, P. A., Lin, D., Burmeister, M., Greenwood, T. A., Hamshere, M. L., Muglia, P., Smith, E. N., Zandi, P. P., Nievergelt, C. M., McKinney, R., Shilling, P. D., Schork, N. J., Bloss, C. S., Foroud, T., Koller, D. L., Gershon, E. S., Liu, C., Badner, J. A., Scheftner, W. A., Lawson, W. B., Nwulia, E. A., Hipolito, M., Coryell, W., Rice, J., Byerley, W., McMahon, F. J., Schulze, T. G., Berrettini, W., Lohoff, F. W., Potash, J. B., Mahon, P. B., McInnis, M. G., Zollner, S., Zhang, P., Craig, D. W., Szelinger, S., Barrett, T. B., Breuer, R., Meier, S., Strohmaier, J., Witt, S. H., Tozzi, F., Farmer, A., McGuffin, P., Strauss, J., Xu, W., Kennedy, J. L., Vincent, J. B., Matthews, K., Day, R., Ferreira, M. A., O'Dushlaine, C., Perlis, R., Raychaudhuri, S., Ruderfer, D., Hyoun, P. L., Smoller, J. W., Li, J., Absher, D., Thompson, R. C., Meng, F. G., Schatzberg, A. F., Bunney, W. E., Barchas, J. D., Jones, E. G., Watson, S. J., Myers, R. M., Akil, H., Boehnke, M., Chambert, K., Moran, J., Scolnick, E., Djurovic, S., Melle, I., Morken, G., Gill, M., Morris, D., Quinn, E., Muhleisen, T. W., Degenhardt, F. A., Mattheisen, M., Schumacher, J., Maier, W., Steffens, M., Propping, P., Nothen, M. M., Anjorin, A., Bass, N., Gurling, H., Kandaswamy, R., Lawrence, J., McGhee, K., McIntosh, A., McLean, A. W., Muir, W. J., Pickard, B. S., Breen, G., St Clair, D., Caesar, S., Gordon-Smith, K., Jones, L., Fraser, C., Green, E. K., Grozeva, D., Jones, I. R., Kirov, G., Moskvina, V., Nikolov, I., O'Donovan, M. C., Owen, M. J., Collier, D. A., Elkin, A., Williamson, R., Young, A. H., Ferrier, I. N., Stefansson, K., Stefansson, H., Thornorgeirsson, T., Steinberg, S., Gustafsson, O., Bergen, S. E., Nimgaonkar, V., Hultman, C., Landen, M., Lichtenstein, P., Sullivan, P., Schalling, M., Osby, U., Backlund, L., Frisen, L., Langstrom, N., Jamain, S., Leboyer, M., Etain, B., Bellivier, F., Petursson, H., Sigur Sson, E., Muller-Mysok, B., Lucae, S., Schwarz, M., Schofield, P. R., Martin, N., Montgomery, G. W., Lathrop, M., Oskarsson, H., Bauer, M., Wright, A., Mitchell, P. B., Hautzinger, M., Reif, A., Kelsoe, J. R., and Purcell, S. M. (2011) Large-scale genome-wide association analysis of bipolar disorder identifies a new susceptibility locus near ODZ4. Nat. Genet. 43, 977-983
15. Mattila, P. K., and Lappalainen, P. (2008) Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9, 446-454
16. Chacon, M. R., and Fazzari, P. (2011) FAK: dynamic integration of guidance signals at the growth cone. Cell Adh. Migr. 5, 52-55
17. Chacon, M. R., Navarro, A. I., Cuesto, G., del Pino, I., Scott, R., Morales, M., and Rico, B. (2012) Focal adhesion kinase regulates actin nucleation and neuronal filopodia formation during axonal growth. Development 139, 3200-3210
18. Myers, J. P., Robles, E., Ducharme-Smith, A., and Gomez, T. M. (2012) Focal adhesion kinase modulates Cdc42 activity downstream of positive and negative axon guidance cues. J. Cell Sci. 125, 2918-2929
19. Miyazaki, H., Oyama, F., Wong, H. K., Kaneko, K., Sakurai, T., Tamaoka, A., and Nukina, N. (2007) BACE1 modulates filopodia-like protrusions induced by sodium channel beta4 subunit. Biochem. Biophys. Res. Commun. 361, 43-48
20. Katz, B. Z., Miyamoto, S., Teramoto, H., Zohar, M., Krylov, D., Vinson, C., Gutkind, J. S., and Yamada, K. M. (2002) Direct transmembrane clustering and cytoplasmic dimerization of fo-cal adhesion kinase initiates its tyrosine phosphorylation. Biochim. Biophys. Acta 1592, 141-152
21. Greene, L. A., and Tischler, A. S. (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. U. S. A. 73, 2424-2428
22. Wu, G., Fang, Y., Lu, Z. H., and Ledeen, R. W. (1998) Induction of axon-like and dendrite-like processes in neuroblastoma cells. J. Neurocytol. 27, 1-14
23. Seong, J., Ouyang, M., Kim, T., Sun, J., Wen, P. C., Lu, S., Zhuo, Y., Llewellyn, N. M., Schlaepfer, D. D., Guan, J. L., Chien, S., and Wang, Y. (2011) Detection of focal adhesion kinase activation at membrane microdomains by fluorescence resonance energy transfer. Nat. Commun. 2, 406
24. Crespi, A., Ferrari, I., Lonati, P., Disanza, A., Fornasari, D., Scita, G., Padovano, V., and Pietrini, G. (2012) LIN7 regulates the filopodium-And neurite-promoting activity of IRSp53. J. Cell Sci. 125, 4543-4554
25. Shekarabi, M., Moore, S. W., Tritsch, N. X., Morris, S. J., Bouchard, J. F., and Kennedy, T. E. (2005) Deleted in colorectal cancer binding netrin-1 mediates cell substrate adhesion and recruits Cdc42, Rac1, Pak1, and N-WASP into an intracellular signaling complex that promotes growth cone expansion. J. Neurosci. 25, 3132-3141
26. Chen, C., Wirth, A., and Ponimaskin, E. (2012) Cdc42: an important regulator of neuronal morphology. Int. J. Biochem. Cell Biol. 44, 447-451
27. Tanaka, M., Ohashi, R., Nakamura, R., Shinmura, K., Kamo, T., Sakai, R., and Sugimura, H. (2004) Tiam1 mediates neurite outgrowth induced by ephrin-B1 and EphA2. EMBO J. 23, 1075-1088
28. Silva, J. P., Lelianova, V. G., Ermolyuk, Y. S., Vysokov, N., Hitchen, P. G., Berninghausen, O., Rahman, M. A., Zangrandi, A., Fidalgo, S., Tonevitsky, A. G., Dell, A., Volynski, K. E., and Ushkaryov, Y. A. (2011) Latrophilin 1 and its endogenous ligand Lasso/teneurin-2 form a high-Affinity transsynaptic receptor pair with signaling capabilities. Proc. Natl. Acad. Sci. U. S. A. 108, 12113-12118
29. Mahon, K., Burdick, K. E., and Szeszko, P. R. (2010) A role for white matter abnormalities in the pathophysiology of bipolar disorder. Neurosci. Biobehav. Rev. 34, 533-554
30. Kuramoto, K., Negishi, M., and Katoh, H. (2009) Regulation of dendrite growth by the Cdc42 activator Zizimin1/Dock9 in hippocampal neurons. J. Neurosci. Res. 87, 1794-1805
31. Detera-Wadleigh, S. D., Liu, C. Y., Maheshwari, M., Cardona, I., Corona, W., Akula, N., Steele, C. J., Badner, J. A., Kundu, M., Kassem, L., Potash, J. B., Gibbs, R., Gershon, E. S., and McMahon, F. J. (2007) Sequence variation in DOCK9 and heterogeneity in bipolar disorder. Psychiatr. Genet. 17, 274-286
32. Ginsberg, S. D., Hemby, S. E., and Smiley, J. F. (2012) Expression profiling in neuropsychiatric disorders: emphasis on glutamate receptors in bipolar disorder. Pharmacol. Biochem. Behav. 100, 705-711
33. Menna, E., Fossati, G., Scita, G., and Matteoli, M. (2011) From filopodia to synapses: the role of actin-capping and anti-capping proteins. Eur. J. Neurosci. 34, 1655-1662