p140Cap regulates memory and synaptic plasticity through src-mediated and citron-N-mediated actin reorganization

Journal of Neuroscience

Volumn 34, Issue 4, 2014, Pages 1542-1553

  Repetto, Daniele ^a,f   Camera, Paola ^a   Melani, Riccardo ^b,c   Morello, Noemi ^a   Russo, Isabella ^a   Calcagno, Eleonora ^a,d   Tomasoni, Romana ^e   Bianchi, Federico ^a   Berto, Gaia ^a   Giustetto, Maurizio ^a   Berardi, Nicoletta ^b,c   Pizzorusso, Tommaso ^b,c   Matteoli, Michela ^e   Di Stefano, Paola ^a   Missler, Markus ^f   Turco, Emilia ^a   Di Cunto, Ferdinando ^a   Defilippi, Paola ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

^d National Institute of Neuroscience   (Italy)

^e UNIVERSITY OF MILAN   (Italy)

^f UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Actin cytoskeleton; Cit N; p140Cap; Rho GTPase; Src; Synapses

Indexed keywords

ACTIN CYTOSKELETON; CIT-N; P140CAP; RHO GTPASE; SRC; SYNAPSES;

ACTINS; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BLOTTING, WESTERN; DENDRITIC SPINES; EXCITATORY POSTSYNAPTIC POTENTIALS; FLUORESCENT ANTIBODY TECHNIQUE; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LEARNING; MEMORY; MICE; MICE, KNOCKOUT; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PROTEIN-SERINE-THREONINE KINASES; RATS; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; SYNAPTIC TRANSMISSION;

EID: 84892685277     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2341-13.2014     Document Type: Article

References (49)

1. Arellano JI, Benavides-Piccione R, Defelipe J, Yuste R (2007) Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front Neurosci 1:131-143. CrossRef Medline
2. Arthur WT, Petch LA, Burridge K (2000) Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr Biol 10:719-722. CrossRef Medline
3. Banker G, Goslin K (1988) Developments in neuronal cell culture. Nature 336:185-186. CrossRef Medline
4. Brouns MR, Matheson SF, Settleman J (2001) p190 RhoGAP is the principal Src substrate in brain and regulates axon outgrowth, guidance and fasciculation. Nat Cell Biol 3:361-367. CrossRef Medline
5. Brown MW, Aggleton JP (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2:51-61. CrossRef Medline
6. Cabodi S, del Pilar Camacho-Leal M, Di Stefano P, Defilippi P (2010) Integrin signalling adaptors: not only figurants in the cancer story. Nat Rev Cancer 10:858-870. CrossRef Medline
7. Camera P, da Silva JS, Griffiths G, Giuffrida MG, Ferrara L, Schubert V, Imarisio S, Silengo L, Dotti CG, Di Cunto F (2003) Citron-N is a neuronal Rho-associated protein involved in Golgi organization through actin cytoskeleton regulation. Nat Cell Biol 5:1071-1078. CrossRef Medline
8. Camera P, Schubert V, Pellegrino M, Berto G, Vercelli A, Muzzi P, Hirsch E, Altruda F, Dotti CG, Di Cunto F (2008) The RhoA-associated protein Citron-N controls dendritic spine maintenance by interacting with spineassociated Golgi compartments. EMBO Rep 9:384-392. CrossRef Medline
9. Chapleau CA, Boggio EM, Calfa G, Percy AK, Giustetto M, Pozzo-Miller L (2012) Hippocampal CA1 pyramidal neurons of Mecp2 mutant mice show a dendritic spine phenotype only in the presymptomatic stage. Neural Plast 2012:976164. CrossRef Medline
10. Cho K, Kemp N, Noel J, Aggleton JP, Brown MW, Bashir ZI (2000) A new form of long-term depression in the perirhinal cortex. Nat Neurosci 3:150-156. CrossRef Medline
11. Damiano L, Di Stefano P, Camacho Leal MP, Barba M, Mainiero F, Cabodi S, Tordella L, Sapino A, Castellano I, Canel M, Frame M, Turco E, Defilippi P (2010) p140Cap dual regulation of E-cadherin/EGFR cross-talk and Ras signalling in tumour cell scatter and proliferation. Oncogene 29: 3677-3690. CrossRef Medline
12. Damiano L, Le Dévédec SE, Di Stefano P, Repetto D, Lalai R, Truong H, Xiong JL, Danen EH, Yan K, Verbeek FJ, De Luca E, Attanasio F, Buccione R, Turco E, van de Water B, Defilippi P (2012) p140Cap suppresses the invasive properties of highly metastatic MTLn3-EGFR cells via impaired cortactin phosphorylation. Oncogene 31:624-633. CrossRef Medline
13. Di Stefano P, Cabodi S, Boeri Erba E, Margaria V, Bergatto E, Giuffrida MG, Silengo L, Tarone G, Turco E, Defilippi P (2004) P130Cas-associated protein (p140Cap) as a new tyrosine-phosphorylated protein involved in cell spreading. Mol Biol Cell 15:787-800. Medline
14. Di Stefano P, Damiano L, Cabodi S, Aramu S, Tordella L, Praduroux A, Piva R, Cavallo F, Forni G, Silengo L, Tarone G, Turco E, Defilippi P (2007) p140Cap protein suppresses tumour cell properties, regulating Csk and Src kinase activity. EMBO J 26:2843-2855. CrossRef Medline
15. Furuyashiki T, Fujisawa K, Fujita A, Madaule P, Uchino S, Mishina M, Bito H, Narumiya S (1999) Citron, a Rho-target, interacts with PSD-95/SAP-90 at glutamatergic synapses in the thalamus. J Neurosci 19:109-118. Medline
16. Hanley JG (2008) AMPA receptor trafficking pathways and links to dendritic spine morphogenesis. Cell Adh Migr 2:276-282. CrossRef Medline
17. Hering H, ShengM (2001) Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2:880-888. CrossRef Medline
18. Holtmaat A, Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10:647-658. CrossRef Medline
19. Hotulainen P, Hoogenraad CC (2010) Actin in dendritic spines: connecting dynamics to function. J Cell Biol 189:619-629. CrossRef Medline
20. Hu X, Ballo L, Pietila L, Viesselmann C, Ballweg J, Lumbard D, Stevenson M, Merriam E, DentEW (2011) BDNF-induced increase of PSD-95 in dendritic spines requires dynamic microtubule invasions. J Neurosci 31: 15597-15603. CrossRef Medline
21. Ito H, Atsuzawa K, Sudo K, Di Stefano P, Iwamoto I, Morishita R, Takei S, Semba R, Defilippi P, Asano T, Usuda N, Nagata K (2008) Characterization of a multidomain adaptor protein, p140Cap, as part of a pre-synaptic complex. J Neurochem 107:61-72. CrossRef Medline
22. Jaworski J, Kapitein LC, Gouveia SM, Dortland BR, Wulf PS, Grigoriev I, Camera P, Spangler SA, Di Stefano P, Demmers J, Krugers H, Defilippi P, Akhmanova A, Hoogenraad CC (2009) Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61:85-100. CrossRef Medline
23. Kimura K, Tsuji T, Takada Y, Miki T, Narumiya S (2000) Accumulation of GTP-bound RhoA during cytokinesis and a critical role of ECT2 in this accumulation. J Biol Chem 275:17233-17236. CrossRef Medline
24. Kopec CD, Real E, Kessels HW, Malinow R (2007) GluR1 links structural and functional plasticity at excitatory synapses. J Neurosci 27:13706-13718. CrossRef Medline
25. Lemieux M, Labrecque S, Tardif C, Labrie-Dion É, Lebel É, De Koninck P (2012) Translocation of CaMKII to dendritic microtubules supports the plasticity of local synapses. J Cell Biol 198:1055-1073. CrossRef Medline
26. Lin WH, Webb DJ (2009) Actin and actin-binding proteins: masters of dendritic spine formation, morphology, and function. Open Neurosci J 3:54-66. CrossRef Medline
27. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766. CrossRef Medline
28. Merriam EB, Lumbard DC, Viesselmann C, Ballweg J, Stevenson M, Pietila L, Hu X, Dent EW (2011) Dynamic microtubules promote synaptic NMDA receptor-dependent spine enlargement. PLoS One 6:e27688. CrossRef Medline
29. Murakoshi H, Wang H, Yasuda R (2011) Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 472:100-104. CrossRef Medline
30. 2+ signaling in dendrites. Neuron 46:609-622. CrossRef Medline
31. Ohashi K, Nagata K, Maekawa M, Ishizaki T, Narumiya S, Mizuno K (2000) Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J Biol Chem 275:3577-3582. CrossRef Medline
32. Oser M, Yamaguchi H, Mader CC, Bravo-Cordero JJ, Arias M, Chen X, Desmarais V, van Rheenen J, Koleske AJ, Condeelis J (2009) Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J Cell Biol 186:571-587. CrossRef Medline
33. Pavlowsky A, Gianfelice A, Pallotto M, Zanchi A, Vara H, Khelfaoui M, Valnegri P, Rezai X, Bassani S, Brambilla D, Kumpost J, Blahos J, Roux MJ, Humeau Y, Chelly J, Passafaro M, Giustetto M, Billuart P, Sala C (2010) A postsynaptic signaling pathway that may account for the cognitive defect due to IL1RAPL1 mutation. Curr Biol 20:103-115. CrossRef Medline
34. Pontrello CG, Ethell IM (2009) Accelerators, brakes, and gears of actin dynamics in dendritic spines. Open Neurosci J 3:67-86. CrossRef Medline
35. Pontrello CG, Sun MY, Lin A, Fiacco TA, DeFea KA, Ethell IM (2012) Cofilin under control of beta-arrestin-2 in NMDA-dependent dendritic spine plasticity, long-term depression (LTD), and learning. Proc Natl Acad Sci U S A 109:E442-E451. CrossRef Medline
36. Repetto D, Aramu S, Boeri Erba E, Sharma N, Grasso S, Russo I, Jensen ON, Cabodi S, Turco E, Di Stefano P, Defilippi P (2013) Mapping of p140Cap phosphorylation sites: the EPLYA and EGLYA motifs have a key role in tyrosine phosphorylation and Csk binding, and are substrates of the Abl kinase. PLoS One 8:e54931. CrossRef Medline
37. Rex CS, Chen LY, Sharma A, Liu J, Babayan AH, Gall CM, Lynch G (2009) Different Rho GTPase-dependent signaling pathways initiate sequential steps in the consolidation of long-term potentiation. J Cell Biol 186:85-97. CrossRef Medline
38. Schubert V, Da Silva JS, Dotti CG (2006) Localized recruitment and activation of RhoA underlies dendritic spine morphology in a glutamate receptor-dependent manner. J Cell Biol 172:453-467. CrossRef Medline
39. Sfakianos MK, Eisman A, Gourley SL, Bradley WD, Scheetz AJ, Settleman J, Taylor JR, Greer CA, Williamson A, Koleske AJ (2007) Inhibition of Rho via Arg and p190RhoGAP in the postnatal mouse hippocampus regulates dendritic spine maturation, synapse and dendrite stability, and behavior. J Neurosci 27:10982-10992. CrossRef Medline
40. Shi Y, Pontrello CG, DeFea KA, Reichardt LF, Ethell IM (2009) Focal adhesion kinase acts downstream of EphB receptors to maintain mature dendritic spines by regulating cofilin activity. J Neurosci 29:8129-8142. CrossRef Medline
41. Star EN, Kwiatkowski DJ, Murthy VN (2002) Rapid turnover of actin in dendritic spines and its regulation by activity. Nat Neurosci 5:239-246. CrossRef Medline
42. Tada T, ShengM (2006) Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol 16:95-101. CrossRef Medline
43. Tamura H, Fukada M, Fujikawa A, Noda M (2006) Protein tyrosine phosphatase receptor type Z is involved in hippocampus-dependent memory formation through dephosphorylation at Y1105 on p190 RhoGAP. Neurosci Lett 399:33-38. CrossRef Medline
44. van Spronsen M, Hoogenraad CC (2010) Synapse pathology in psychiatric and neurologic disease. Curr Neurol Neurosci Rep 10:207-214. CrossRef Medline
45. Xie Z, Srivastava DP, Photowala H, Kai L, Cahill ME, Woolfrey KM, Shum CY, Surmeier DJ, Penzes P (2007) Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 56:640-656. CrossRef Medline
46. Yang N, Higuchi O, Ohashi K, Nagata K, Wada A, Kangawa K, Nishida E, Mizuno K (1998) Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393:809-812. CrossRef Medline
47. Yoshihara Y, De Roo M, Muller D (2009) Dendritic spine formation and stabilization. Curr Opin Neurobiol 19:146-153. CrossRef Medline
48. Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelfinger ED, Ziv NE, Garner CC (2001) Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 29:131-143. CrossRef Medline
49. Zhang W, Benson DL (2006) Targeting and clustering citron to synapses. Mol Cell Neurosci 31:26-36. CrossRef Medline