Synapsin III acts downstream of semaphorin 3A/CDK5 signaling to regulate radial migration and orientation of pyramidal neurons in vivo

Cell Reports

Volumn 11, Issue 2, 2015, Pages 234-248

  Perlini, Laura E ^a,b   Szczurkowska, Joanna ^a   Ballif, Bryan A ^c   Piccini, Alessandra ^b   Sacchetti, Silvio ^a   Giovedí, Silvia ^b   Benfenati, Fabio ^a,b   Cancedda, Laura ^a  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 5; SEMAPHORIN 3A; SYNAPSIN; SYNAPSIN III; UNCLASSIFIED DRUG; C REACTIVE PROTEIN; CDK5 PROTEIN, RAT; NERVE PROTEIN; NEURONAL PENTRAXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL MIGRATION; CELL MOTION; CELL ORIENTATION; CONTROLLED STUDY; DOWN REGULATION; GENE DELETION; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PYRAMIDAL NERVE CELL; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; BRAIN CORTEX; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; CYTOLOGY; DENDRITE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOSPHORYLATION; PRIMARY CELL CULTURE;

ANIMALS; C-REACTIVE PROTEIN; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; CEREBRAL CORTEX; COS CELLS; CYCLIN-DEPENDENT KINASE 5; DENDRITES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PRIMARY CELL CULTURE; PYRAMIDAL CELLS; RATS; SEMAPHORIN-3A; SIGNAL TRANSDUCTION; SYNAPSINS;

EID: 84929275660     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.03.022     Document Type: Article

References (55)

1. Arnold, S.E., Lee, V.M., Gur, R.E., and Trojanowski, J.Q. (1991). Abnormal expression of two microtubule-associated proteins (MAP2 and MAP5) in specific subfields of the hippocampal formation in schizophrenia. Proc. Natl. Acad. Sci. USA 88, 10850-10854.
2. Ayala, R., Shu, T., and Tsai, L.H. (2007). Trekking across the brain: the journey of neuronal migration. Cell 128, 29-43.
3. Bai, J., Ramos, R.L., Ackman, J.B., Thomas, A.M., Lee, R.V., and LoTurco, J.J. (2003). RNAi reveals doublecortin is required for radial migration in rat neocortex. Nat. Neurosci. 6, 1277-1283.
4. Ballif, B.A., Cao, Z., Schwartz, D., Carraway, K.L., 3rd, and Gygi, S.P. (2006). Identification of 14-3-3epsilon substrates from embryonic murine brain. J. Proteome Res. 5, 2372-2379.
5. Ballif, B.A., Carey, G.R., Sunyaev, S.R., and Gygi, S.P. (2008). Large-scale identification and evolution indexing of tyrosine phosphorylation sites from murine brain. J. Proteome Res. 7, 311-318.
6. Behar, O., Golden, J.A., Mashimo, H., Schoen, F.J., and Fishman, M.C. (1996). Semaphorin III is needed for normal patterning and growth of nerves, bones and heart. Nature 383, 525-528.
7. Benes, F.M., Sorensen, I., and Bird, E.D. (1991). Reduced neuronal size in posterior hippocampus of schizophrenic patients. Schizophr. Bull. 17, 597-608.
8. Benfenati, F., Bähler, M., Jahn, R., and Greengard, P. (1989a). Interactions of synapsin I with small synaptic vesicles: distinct sites in synapsin I bind to vesicle phospholipids and vesicle proteins. J. Cell Biol. 108, 1863-1872.
9. Benfenati, F., Valtorta, F., Bähler, M., and Greengard, P. (1989b). Synapsin I, a neuron-specific phosphoprotein interacting with small synaptic vesicles and F-actin. Cell Biol. Int. Rep. 13, 1007-1021.
10. Benfenati, F., Valtorta, F., Chieregatti, E., and Greengard, P. (1992). Interaction of free and synaptic vesicle-bound synapsin I with F-actin. Neuron 8, 377-386.
11. Bony, G., Szczurkowska, J., Tamagno, I., Shelly, M., Contestabile, A., and Cancedda, L. (2013). Non-hyperpolarizing GABAB receptor activation regulates neuronal migration and neurite growth and specification by cAMP/ LKB1. Nat. Commun. 4, 1800.
12. Buel, G.R., Rush, J., and Ballif, B.A. (2010). Fyn promotes phosphorylation of collapsin response mediator protein 1 at tyrosine 504, a novel, isoform-specific regulatory site. J. Cell. Biochem. 111, 20-28.
13. Candiani, S., Moronti, L., Pennati, R., De Bernardi, F., Benfenati, F., and Pestarino, M. (2010). The synapsin gene family in basal chordates: evolutionary perspectives in metazoans. BMC Evol. Biol. 10, 32.
14. Cesca, F., Baldelli, P., Valtorta, F., and Benfenati, F. (2010). The synapsins: key actors of synapse function and plasticity. Prog. Neurobiol. 91, 313-348.
15. Chae, T., Kwon, Y.T., Bronson, R., Dikkes, P., Li, E., and Tsai, L.H. (1997). Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 18, 29-42.
16. Chen, G., Sima, J., Jin, M., Wang, K.Y., Xue, X.J., Zheng, W., Ding, Y.Q., and Yuan, X.B. (2008). Semaphorin-3A guides radial migration of cortical neurons during development. Nat. Neurosci. 11, 36-44.
17. Chen, Q., Che, R., Wang, X., O'Neill, F.A., Walsh, D., Tang, W., Shi, Y., He, L., Kendler, K.S., and Chen, X. (2009). Association and expression study of synapsin III and schizophrenia. Neurosci. Lett. 465, 248-251.
18. Corbo, J.C., Deuel, T.A., Long, J.M., LaPorte, P., Tsai, E., Wynshaw-Boris, A., and Walsh, C.A. (2002). Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J. Neurosci. 22, 7548-7557.
19. dal Maschio, M., Ghezzi, D., Bony, G., Alabastri, A., Deidda, G., Brondi, M., Sato, S.S., Zaccaria, R.P., Di Fabrizio, E., Ratto, G.M., and Cancedda, L. (2012). High-performance and site-directed in utero electroporation by a triple-electrode probe. Nat. Commun. 3, 960.
20. De Paula, D., Bentley, M.V., and Mahato, R.I. (2007). Hydrophobization and bioconjugation for enhanced siRNA delivery and targeting. RNA 13, 431-456.
21. Eastwood, S.L., Law, A.J., Everall, I.P., and Harrison, P.J. (2003). The axonal chemorepellant semaphorin 3A is increased in the cerebellum in schizophrenia and may contribute to its synaptic pathology. Mol. Psychiatry 8, 148-155.
22. Elias, L.A., Wang, D.D., and Kriegstein, A.R. (2007). Gap junction adhesion is necessary for radial migration in the neocortex. Nature 448, 901-907.
23. Feng, J., Chi, P., Blanpied, T.A., Xu, Y., Magarinos, A.M., Ferreira, A., Takahashi, R.H., Kao, H.T., McEwen, B.S., Ryan, T.A., et al. (2002). Regulation of neurotransmitter release by synapsin III. J. Neurosci. 22, 4372-4380.
24. Ferreira, A., Kao, H.T., Feng, J., Rapoport, M., and Greengard, P. (2000). Synapsin III: developmental expression, subcellular localization, and role in axon formation. J. Neurosci. 20, 3736-3744.
25. Geyer, M.A., Krebs-Thomson, K., Braff, D.L., and Swerdlow, N.R. (2001). Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology (Berl.) 156, 117-154.
26. Glantz, L.A., Austin, M.C., and Lewis, D.A. (2000). Normal cellular levels of synaptophysin mRNA expression in the prefrontal cortex of subjects with schizophrenia. Biol. Psychiatry 48, 389-397.
27. Gupta, A., Sanada, K., Miyamoto, D.T., Rovelstad, S., Nadarajah, B., Pearlman, A.L., Brunstrom, J., and Tsai, L.H. (2003). Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat. Neurosci. 6, 1284-1291.
28. Hall, H., Lawyer, G., Sillén, A., Jönsson, E.G., Agartz, I., Terenius, L., and Arnborg, S. (2007). Potential genetic variants in schizophrenia: a Bayesian analysis. World J. Biol. Psychiatry 8, 12-22.
29. Itofusa, R., and Kamiguchi, H. (2011). Polarizing membrane dynamics and adhesion for growth cone navigation. Mol. Cell. Neurosci. 48, 332-338.
30. Jessberger, S., Aigner, S., Clemenson, G.D., Jr., Toni, N., Lie, D.C., Karalay, O., Overall, R., Kempermann, G., and Gage, F.H. (2008). Cdk5 regulates accurate maturation of newborn granule cells in the adult hippocampus. PLoS Biol. 6, e272.
31. Kao, H.T., Porton, B., Czernik, A.J., Feng, J., Yiu, G., Häring, M., Benfenati, F., and Greengard, P. (1998). A third member of the synapsin gene family. Proc. Natl. Acad. Sci. USA 95, 4667-4672.
32. Kao, H.T., Porton, B., Hilfiker, S., Stefani, G., Pieribone, V.A., DeSalle, R., and Greengard, P. (1999). Molecular evolution of the synapsin gene family. J. Exp. Zool. 285, 360-377.
33. Lachman, H.M., Stopkova, P., Rafael, M.A., and Saito, T. (2005). Association of schizophrenia in African Americans to polymorphismin synapsin III gene. Psychiatr. Genet. 15, 127-132.
34. Lee, K.F., Li, E., Huber, L.J., Landis, S.C., Sharpe, A.H., Chao, M.V., and Jaenisch, R. (1992). Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69, 737-749.
35. Mirnics, K., Middleton, F.A., Marquez, A., Lewis, D.A., and Levitt, P. (2000). Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron 28, 53-67.
36. Ohshima, T., Hirasawa, M., Tabata, H., Mutoh, T., Adachi, T., Suzuki, H., Saruta, K., Iwasato, T., Itohara, S., Hashimoto, M., et al. (2007). Cdk5 is required for multipolar-to-bipolar transition during radial neuronal migration and proper dendrite development of pyramidal neurons in the cerebral cortex. Development 134, 2273-2282.
37. Petrucci, T.C., and Morrow, J.S. (1991). Actin and tubulin binding domains of synapsins Ia and Ib. Biochemistry 30, 413-422.
38. Polleux, F., Giger, R.J., Ginty, D.D., Kolodkin, A.L., and Ghosh, A. (1998). Patterning of cortical efferent projections by semaphorin-neuropilin interactions. Science 282, 1904-1906.
39. Polleux, F., Morrow, T., and Ghosh, A. (2000). Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404, 567-573.
40. Porton, B., and Wetsel, W.C. (2007). Reduction of synapsin III in the prefrontal cortex of individuals with schizophrenia. Schizophr. Res. 94, 366-370.
41. Porton, B., Kao, H.T., and Greengard, P. (1999). Cloning of cDNAs encoding human synapsins IIa and IIb. DNA Seq. 10, 49-54.
42. Porton, B., Ferreira, A., DeLisi, L.E., and Kao, H.T. (2004). A rare polymorphism affects a mitogen-activated protein kinase site in synapsin III: possible relationship to schizophrenia. Biol. Psychiatry 55, 118-125.
43. Porton, B., Rodriguiz, R.M., Phillips, L.E., Gilbert, J.W., 4th, Feng, J., Greengard, P., Kao, H.T., and Wetsel, W.C. (2010). Mice lacking synapsin III show abnormalities in explicit memory and conditioned fear. Genes Brain Behav. 9, 257-268.
44. Rajkowska, G., Selemon, L.D., and Goldman-Rakic, P.S. (1998). Neuronal and glial somal size in the prefrontal cortex: a postmortem morphometric study of schizophrenia and Huntington disease. Arch. Gen. Psychiatry 55, 215-224.
45. Rivas, R.J., and Hatten, M.E. (1995). Motility and cytoskeletal organization of migrating cerebellar granule neurons. J. Neurosci. 15, 981-989.
46. Rosoklija, G., Toomayan, G., Ellis, S.P., Keilp, J., Mann, J.J., Latov, N., Hays, A.P., and Dwork, A.J. (2000). Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch. Gen. Psychiatry 57, 349-356.
47. Sanada, K., Gupta, A., and Tsai, L.H. (2004). Disabled-1-regulated adhesion of migrating neurons to radial glial fiber contributes to neuronal positioning during early corticogenesis. Neuron 42, 197-211.
48. Sasaki, Y., Cheng, C., Uchida, Y., Nakajima, O., Ohshima, T., Yagi, T., Taniguchi, M., Nakayama, T., Kishida, R., Kudo, Y., et al. (2002). Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron 35, 907-920.
49. Schuler, V., Lüscher, C., Blanchet, C., Klix, N., Sansig, G., Klebs, K., Schmutz, M., Heid, J., Gentry, C., Urban, L., et al. (2001). Epilepsy, hyperalgesia, impaired memory, and loss of pre-and postsynaptic GABA(B) responses in mice lacking GABA(B(1)). Neuron 31, 47-58.
50. Shelly, M., Cancedda, L., Lim, B.K., Popescu, A.T., Cheng, P.L., Gao, H., and Poo, M.M. (2011). Semaphorin3A regulates neuronal polarization by suppressing axon formation and promoting dendrite growth. Neuron 71, 433-446.
51. Solecki, D.J., Trivedi, N., Govek, E.E., Kerekes, R.A., Gleason, S.S., and Hatten, M.E. (2009). Myosin II motors and F-actin dynamics drive the coordinated movement of the centrosome and soma during CNS glial-guided neuronal migration. Neuron 63, 63-80.
52. Songyang, Z., Lu, K.P., Kwon, Y.T., Tsai, L.H., Filhol, O., Cochet, C., Brickey, D.A., Soderling, T.R., Bartleson, C., Graves, D.J., et al. (1996). A structural basis for substrate specificities of protein Ser/Thr kinases: primary sequence preference of casein kinases I and II, NIMA, phosphorylase kinase, calmodulin-dependent kinase II, CDK5, and Erk1. Mol. Cell. Biol. 16, 6486-6493.
53. Valiente, M., Ciceri, G., Rico, B., and Marín, O. (2011). Focal adhesion kinase modulates radial glia-dependent neuronal migration through connexin-26. J. Neurosci. 31, 11678-11691.
54. Zalesky, A., Fornito, A., Seal, M.L., Cocchi, L., Westin, C.F., Bullmore, E.T., Egan, G.F., and Pantelis, C. (2011). Disrupted axonal fiber connectivity in schizophrenia. Biol. Psychiatry 69, 80-89.
55. NTR specifies axons during development and adult neurogenesis. Cell Rep. 7, 138-152.