Activation of 5-HT7 receptor stimulates neurite elongation through mTOR, Cdc42 and actin filaments dynamics

Frontiers in Behavioral Neuroscience

Volumn 9, Issue , 2015, Pages

  Speranza, Luisa ^a,b   Giuliano, Teresa ^b   Volpicelli, Floriana ^a,b   De Stefano, M Egle ^c   Lombardi, Loredana ^c   Chambery, Angela ^d,e   Lacivita, Enza ^f   Leopoldo, Marcello ^f   Bellenchi, Gian C ^b   di Porzio, Umberto ^b   Crispino, Marianna ^a   Perrone Capano, Carla ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d SECOND UNIVERSITY OF NAPLES   (Italy)

^e IRCCS MULTIMEDICA   (Italy)

^f UNIVERSITY OF BARI   (Italy)

Author keywords

5 HT7 receptor; Actin dynamics; Axonal elongation; Cdc42; mTOR; Neurite outgrowth

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; COFILIN; CYCLIN DEPENDENT KINASE 5; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN CDC42; PROTEIN KINASE B; SEROTONIN 7 RECEPTOR;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DENDRITE; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; INTRACELLULAR SIGNALING; MOUSE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE ELONGATION; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; STRIATE CORTEX; WESTERN BLOTTING;

EID: 84939514534     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2015.00062     Document Type: Article

References (61)

1. Adriani, W., Leo, D., Guarino, M., Natoli, A., Di Consiglio, E., De Angelis, G., et al. (2006). Short-term effects of adolescent methylphenidate exposure on brain striatal gene expression and sexual/endocrine parameters in male rats. Ann. N.Y. Acad. Sci. 1074, 52-73. doi: 10.1196/annals.1369.005
2. Adriani, W., Travaglini, D., Lacivita, E., Saso, L., Leopoldo, M., and Laviola, G. (2012). Modulatory effects of two novel agonists for serotonin receptor 7 on emotion, motivation and circadian rhythm profiles in mice.Neuropharmacology 62, 833-842. doi: 10.1016/j.neuropharm.2011.09.012
3. Auer, M., Hausott, B., and Klimaschewski, L. (2011). Rho GTPases as regulators of morphological neuroplasticity.Ann. Anat. 193, 259-266. doi: 10.1016/j.aanat.2011.02.015
4. Bernstein, B. W., and Bamburg, J. R. (2010). ADF/cofilin:a functional node in cell biology. Trends Cell Biol. 20, 187-195. doi: 10.1016/j.tcb.2010.01.001
5. Bradke, F., and Dotti, C. G. (1999). The role of local actin instability in axon formation. Science 283, 1931-1934. doi: 10.1126/science.283.5409.1931
6. Bravo-Cordero, J. J., Magalhaes, M. A. O., Eddy, R. J., Hodgson, L., and Condeelis, J. (2013). Functions of cofilin in cell locomotion and invasion. Nat. Rev. Mol. Cell Biol. 14, 405-415. doi: 10.1038/nrm3609
7. Briz, V., and Baudry, M. (2014). Estrogen regulates protein synthesis and actin polymerization in hippocampal neurons through different molecular mechanisms. Front. Endocrinol. 5:22. doi: 10.3389/fendo.2014.00022
8. Burnett, P. E., Barrow, R. K., Cohen, N. A., Snyder, S. H., and Sabatini, D. M. (1998). RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc. Natl. Acad. Sci. U.S.A. 95, 1432-1437. doi: 10.1073/pnas.95.4.1432
9. Cates, L. N., Roberts, A. J., Huitron-Resendiz, S., and Hedlund, P. B. (2013). Effects of lurasidone in behavioral models of depression. Role of the 5-HT7 receptor subtype. Neuropharmacology 70, 211-217. doi: 10.1016/j.neuropharm.2013.01.023
10. Cheung, Z. H., Chin, W. H., Chen, Y., Ng, Y. P., and Ip, N. Y. (2007). Cdk5 is involved in BDNF-stimulated dendritic growth in hippocampal neurons. PLoS Biol. 5:e63. doi: 10.1371/journal.pbio.0050063
11. Colucci-D'Amato, L., Perrone-Capano, C., and di Porzio, U. (2003). Chronic activation of ERK and neurodegenerative diseases. Bioessays 25, 1085-1095. doi: 10.1002/bies.10355
12. Conti, A. M., Fischer, S. J., and Windebank, A. J. (1997). Inhibition of axonal growth from sensory neurons by excess nerve growth factor. Ann. Neurol. 42, 838-846. doi: 10.1002/ana.410420604
13. Costa, L., Spatuzza, M., D'Antoni, S., Bonaccorso, C. M., Trovato, C., Musumeci, S. A., et al. (2012). Activation of 5-HT7 serotonin receptors reverses metabotropic glutamate receptor-mediated synaptic plasticity in wild-type and Fmr1 knockout mice, a model of Fragile X syndrome. Biol. Psychiatry 72, 924-933. doi: 10.1016/j.biopsych.2012.06.008
14. Daubert, E. A., and Condron, B. G. (2010). Serotonin: a regulator of neuronal morphology and circuitry. Trends Neurosci. 33, 424-434. doi: 10.1016/j.tins.2010.05.005
15. De Filippis, B., Nativio, P., Fabbri, A., Ricceri, L., Adriani, W., Lacivita, E., et al. (2014). Pharmacological stimulation of the brain serotonin receptor 7 as a novel therapeutic approach for Rett Syndrome.Neuropsychopharmacology 39, 2506-2518. doi: 10.1038/npp.2014.105
16. Dotti, C. G., Sullivan, C. A., and Banker, G. A. (1988). The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468.
17. Duhr, F., Déléris, P., Raynaud, F., Séveno, M., Morisset-Lopez, S., Mannoury la Cour, C., et al. (2014). Cdk5 induces constitutive activation of 5-HT6 receptors to promote neurite growth. Nat. Chem. Biol. 10, 590-597. doi: 10.1038/nchembio.1547
18. Endo, M., Ohashi, K., and Mizuno, K. (2007). LIM kinase and slingshot are critical for neurite extension. J. Biol. Chem. 282, 13692-13702. doi: 10.1074/jbc.M610873200
19. Figge, C., Loers, G., Schachner, M., and Tilling, T. (2012). Neurite outgrowth triggered by the cell adhesion molecule L1 requires activation and inactivation of the cytoskeletal protein cofilin. Mol. Cell. Neurosci. 49, 196-204. doi: 10.1016/j.mcn.2011.10.002
20. Fiszman, M. L., Zuddas, A., Masana, M. I., Barker, J. L., and di Porzio, U. (1991). Dopamine synthesis precedes dopamine uptake in embryonic rat mesencephalic neurons. J. Neurochem. 56, 392-399. doi: 10.1111/j.1471-4159.1991.tb08164.x
21. Gallo, G., Yee, H. F. Jr., and Letourneau, P. C. (2002). Actin turnover is required to prevent axon retraction driven by endogenous actomyosin contractility. J. Cell Biol. 158, 1219-1228. doi: 10.1083/jcb.200204140
22. Garvalov, B. K., Flynn, K. C., Neukirchen, D., Meyn, L., Teusch, N., Wu, X., et al. (2007). Cdc42 regulates cofilin during the establishment of neuronal polarity. J. Neurosci. 27, 13117-13129. doi: 10.1523/JNEUROSCI.3322-07.2007
23. Gellynck, E., Heyninck, K., Andressen, K. W., Haegeman, G., Levy, F. O., Vanhoenacker, P., et al. (2013). The serotonin 5-HT7 receptors: two decades of research. Exp. Brain Res. 230, 555-568. doi: 10.1007/s00221-013-3694-y
24. Guo, W., Qian, L., Zhang, J., Zhang, W., Morrison, A., Hayes, P., et al. (2011). Sirt1 overexpression in neurons promotes neurite outgrowth and cell survival through inhibition of the mTOR signaling. J. Neurosci. Res. 89, 1723-1736. doi: 10.1002/jnr.22725
25. Hagan, J. J., Price, G. W., Jeffrey, P., Deeks, N. J., Stean, T., Piper, D., et al. (2000). Characterization of SB-269970-A, a selective 5-HT(7) receptor antagonist. Br. J. Pharmacol. 130, 539-548. doi: 10.1038/sj.bjp.0703357
26. Hannan, M. A., Kang, J. Y., Mohibbullah, M., Hong, Y. K., Lee, H., Choi, J. S., et al. (2014). Moringa oleifera with promising neuronal survival and neurite outgrowth promoting potentials. J. Ethnopharmacol. 152, 142-150. doi: 10.1016/j.jep.2013.12.036
27. He, Y., Li, D., Cook, S. L., Yoon, M. S., Kapoor, A., Rao, C. V., et al. (2013). Mammalian target of rapamycin and Rictor control neutrophil chemotaxis by regulating Rac/Cdc42 activity and the actin cytoskeleton. Mol. Biol. Cell24, 3369-3380. doi: 10.1091/mbc.E13-07-0405
28. Hedlund, P. B., Leopoldo, M., Caccia, S., Sarkisyan, G., Fracasso, C., Martelli, G., et al. (2010). LP-211 is a brain penetrant selective agonist for the serotonin 5-HT(7) receptor. Neurosci. Lett. 481, 12-16. doi: 10.1016/j.neulet.2010.06.036
29. Hoeffer, C. A., and Klann, E. (2010). mTOR signaling:at the crossroads of plasticity, memory and disease. Trends Neurosci. 33, 67-75. doi: 10.1016/j.tins.2009.11.003
30. Huang, T. Y., DerMardirossian, C., and Bokoch, G. M. (2006). Cofilin phosphatases and regulation of actin dynamics. Curr. Opin. Cell Biol. 18, 26-31. doi: 10.1016/j.ceb.2005.11.005
31. Huang, W., Zhu, P. J., Zhang, S., Zhou, H., Stoica, L., Galiano, M., et al. (2013). mTORC2 controls actin polymerization required for consolidation of long-term memory. Nat. Neurosci. 16, 441-448. doi: 10.1038/nn.3351
32. Jaffe, A. B., and Hall, A. (2005). Rho GTPases:biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269. doi: 10.1146/annurev.cellbio.21.020604.150721
33. Jaworski, J., and Sheng, M. (2006). The growing role of mTOR in neuronal development and plasticity. Mol. Neurobiol. 34, 205-219. doi: 10.1385/MN:34:3:205
34. Jessberger, S., Gage, F. H., Eisch, A. J., and Lagace, D. C. (2009). Making a neuron:Cdk5 in embryonic and adult neurogenesis. Trends Neurosci. 32, 575-582. doi: 10.1016/j.tins.2009.07.002
35. Jones, S. B., Lu, H. Y., and Lu, Q. (2004). Abl tyrosine kinase promotes dendrogenesis by inducing actin cytoskeletal rearrangements in cooperation with Rho family small GTPases in hippocampal neurons. J. Neurosci. 24, 8510-8521. doi: 10.1523/JNEUROSCI.1264-04.2004
36. Kobe, F., Guseva, D., Jensen, T. P., Wirth, A., Renner, U., Hess, D., et al. (2012). 5-HT7R/ G12 signaling regulates neuronal morphology and function in an age-dependent manner. J. Neurosci. 32, 2915-2930. doi: 10.1523/JNEUROSCI.2765-11.2012
37. Kvachnina, E., Liu, G., Dityatev, A., Renner, U., Dumuis, A., Richter, D. W., et al. (2005). 5-HT7 receptor is coupled to G alpha subunits of heterotrimeric G12-protein to regulate gene transcription and neuronal morphology. J. Neurosci. 25, 7821-7830. doi: 10.1523/JNEUROSCI.1790-05.2005
38. Laplante, M., and Sabatini, D. M. (2012). mTOR signaling in growth control and disease. Cell 149, 274-293. doi: 10.1016/j.cell.2012.03.017
39. Leo, D., Adriani, W., Cavaliere, C., Cirillo, G., Marco, E. M., Romano, E., et al. (2009). Methylphenidate to adolescent rats drives enduring changes of accumbal Htr7 expression: implications for impulsive behavior and neuronal morphology. Genes Brain Behav. 8, 356-368. doi: 10.1111/j.1601-183X.2009.00486.x
40. Leopoldo, M., Lacivita, E., Berardi, F., Perrone, R., and Hedlund, P. B. (2011). Serotonin 5-HT7 receptor agents: structure-activity relationships and potential therapeutic applications in central nervous system disorders.Pharmacol. Ther. 129, 120-148. doi: 10.1016/j.pharmthera.2010.08.013
41. Lesch, K. P., and Waider, J. (2012). Serotonin in the modulation of neural plasticity and networks: implications for neurodevelopmental disorders. Neuron 76, 175-191. doi: 10.1016/j.neuron.2012.09.013
42. Li, J., Gu, J., Wang, B., Xie, M., Huang, L., Liu, Y., et al. (2014). Activation of DOPamine D1 receptors regulates dendritic morphogenesis through Rac1 and RhoA in prefrontal cortex neurons. Mol Neurobiol. doi: 10.1007/s12035-014-8762-1. [Epub ahead of print].
43. Liu, Q., Chang, J. W., Wang, J., Kang, S. A., Thoreen, C. C., Markhard, A., et al. (2010). Discovery of 1-(4-(4-propionylpiperazin-1-yl)-3-(trifluoromethyl)phenyl)-9-(quinolin-3-yl)benz o[h][1,6]naphthyridin-2(1H)-one as a highly potent, selective mammalian target of rapamycin (mTOR) inhibitor for the treatment of cancer. J. Med. Chem. 53, 7146-7155. doi: 10.1021/jm101144f
44. Lu, Y., Belin, S., and He, Z. (2014). Signaling regulations of neuronal regenerative ability. Curr. Opin. Neurobiol. 27, 135-142. doi: 10.1016/j.conb.2014.03.007
45. Luo, L. (2000). Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 1, 173-180. doi: 10.1038/35044547
46. Matthys, A., Haegeman, G., Van Craenenbroeck, K., and Vanhoenacker, P. (2011). Role of the 5-HT7 receptor in the central nervous system:from current status to future perspectives. Mol. Neurobiol. 43, 228-253. doi: 10.1007/s12035-011-8175-3
47. Meffre, J., Chaumont-Dubel, S., Mannoury la Cour, C., Loiseau, F., Watson, D. J., Dekeyne, A., et al. (2012). 5-HT(6) receptor recruitment of mTOR as a mechanism for perturbed cognition in schizophrenia. EMBO Mol. Med. 4, 1043-1056. doi: 10.1002/emmm.201201410
48. Mizuno, K. (2013). Signaling mechanisms and functional roles of cofilin phosphorylation and dephosphorylation.Cell. Signal. 25, 457-469. doi: 10.1016/j.cellsig.2012.11.001
49. Park, J. W., Vahidi, B., Taylor, A. M., Rhee, S. W., and Jeon, N. L. (2006). Microfluidic culture platform for neuroscience research. Nat. Protoc. 1, 2128-2136. doi: 10.1038/nprot.2006.316
50. di Porzio, U., Daguet, M. C., Glowinski, J., and Prochiantz, A. (1980). Effect of striatal cells on in vitro maturation of mesencephalic dopaminergic neurones grown in serum-free conditions. Nature 288, 370-373. doi: 10.1038/288370a0
51. Pytliak, M., Vargová, V., Mechírová, V., and Felšöci, M. (2011). Serotonin receptors - from molecular biology to clinical applications. Physiol. Res. 60, 15-25.
52. Sarbassov, D. D., Guertin, D. A., Ali, S. M., and Sabatini, D. M. (2005). Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101. doi: 10.1126/science.1106148
53. Schaefer, A. W., Schoonderwoert, V. T. G., Ji, L., Mederios, N., Danuser, G., and Forscher, P. (2008). Coordination of actin filament and microtubule dynamics during neurite outgrowth. Dev. Cell 15, 146-162. doi: 10.1016/j.devcel.2008.05.003
54. Schmittgen, T. D., and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101-1108. doi: 10.1038/nprot.2008.73
55. Speranza, L., Chambery, A., Di Domenico, M., Crispino, M., Severino, V., Volpicelli, F., et al. (2013). The serotonin receptor 7 promotes neurite outgrowth via ERK and Cdk5 signaling pathways. Neuropharmacology 67, 155-167. doi: 10.1016/j.neuropharm.2012.10.026
56. Stern, S., Haverkamp, S., Sinske, D., Tedeschi, A., Naumann, U., Di Giovanni, S., et al. (2013). The transcription factor serum response factor stimulates axon regeneration through cytoplasmic localization and cofilin interaction. J. Neurosci. 33, 18836-18848. doi: 10.1523/JNEUROSCI.3029-13.2013
57. Tajiri, M., Hayata-Takano, A., Seiriki, K., Ogata, K., Hazama, K., Shintani, N., et al. (2012). Serotonin 5-HT(7) receptor blockade reverses behavioral abnormalities in PACAP-deficient mice and receptor activation promotes neurite extension in primary embryonic hippocampal neurons: therapeutic implications for psychiatric disorders.J. Mol. Neurosci. 48, 473-481. doi: 10.1007/s12031-012-9861-y
58. Takei, N., and Nawa, H. (2014). mTOR signaling and its roles in normal and abnormal brain development. Front. Mol. Neurosci. 7:28. doi: 10.3389/fnmol.2014.00028
59. Taylor, A. M., Blurton-Jones, M., Rhee, S. W., Cribbs, D. H., Cotman, C. W., and Jeon, N. L. (2005). A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat. Methods 2, 599-605. doi: 10.1038/nmeth777
60. Van Kesteren, R. E., and Spencer, G. E. (2003). The role of neurotransmitters in neurite outgrowth and synapse formation. Rev. Neurosci. 14, 217-231. doi: 10.1515/REVNEURO.2003.14.3.217
61. Volpicelli, F., Speranza, L., di Porzio, U., Crispino, M., and Perrone-Capano, C. (2014). The serotonin receptor 7 and the structural plasticity of brain circuits. Front. Behav. Neurosci. 8:318. doi: 10.3389/fnbeh.2014.00318