Impaired dendritic development and memory in sorbs2 knock-out mice

Journal of Neuroscience

Volumn 36, Issue 7, 2016, Pages 2247-2260

  Zhang, Qiangge ^a,c   Gao, Xian ^a,b,c   Li, Chenchen ^a,c   Feliciano, Catia ^d   Wang, Dongqing ^a   Zhou, Dingxi ^a,e   Mei, Yuan ^a   Monteiro, Patricia ^a,c   Anand, Michelle ^a   Itohara, Shigeyoshi ^f   Dong, Xiaowei ^b   Fu, Zhanyan ^a,c   Feng, Guoping ^a,b,c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b B326 Science Building   (China)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d CHAMPALIMAUD CENTRE FOR THE UNKNOWN   (Portugal)

^e PEKING UNIVERSITY   (China)

^f RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Dendrites; Dentate gyrus; Intellectual disability; Learning and memory; NArgBP2; Sorbs2

Indexed keywords

CALRETININ; F ACTIN; GEPHYRIN; NETRIN; NEURON SPECIFIC NUCLEAR PROTEIN; PROTEIN; SORBS2 PROTEIN; SYNAPSIN I; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; DNA; SORBS2 PROTEIN, MOUSE;

ACOUSTIC STARTLE THRESHOLD AND PREPULSE INHIBITION TEST; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN REGION; CONTROLLED STUDY; DENDRITIC CELL; ELEVATED ZERO MAZE TEST; EXPERIMENTAL BEHAVIORAL TEST; FEAR CONDITIONING TEST; FEMALE; GENE DELETION; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; INTELLECTUAL IMPAIRMENT; MALE; MEMORY; MORRIS WATER MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; NUCLEOTIDE SEQUENCE; OPEN FIELD BEHAVIOR; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SYNAPTIC TRANSMISSION; ANIMAL; ANIMAL BEHAVIOR; BRAIN; C57BL MOUSE; DENDRITE; DENDRITIC SPINE; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; GROWTH CONE; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; LONG TERM MEMORY; MOTOR ACTIVITY; PATHOLOGY; PHYSIOLOGY; RECOGNITION; STARTLE REFLEX;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; DENDRITES; DENDRITIC SPINES; DNA; EXCITATORY POSTSYNAPTIC POTENTIALS; GROWTH CONES; INTELLECTUAL DISABILITY; MEMORY; MEMORY, LONG-TERM; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MOTOR ACTIVITY; RECOGNITION (PSYCHOLOGY); REFLEX, STARTLE;

EID: 84958743695     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2528-15.2016     Document Type: Article

References (63)

1. American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th Ed. Washington, DC: American Psychiatric Association.
2. Anagnostaras SG, Wood SC, Shuman T, Cai DJ, LeDuc AD, Zurn KR, Zurn JB, Sage JR, Herrera GM (2010) Automated assessment of Pavlovian conditioned freezing and shock reactivity in mice using the VideoFreeze system. Front Behav Neurosci 4:pii158. CrossRef Medline.
3. Anekal PV, Yong J, Manser E (2015) Arg kinase binding protein 2 (ArgBP2) interaction with alpha-actinin and actin stress fibres inhibits cell migration. J Biol Chem 290:2112-2125. CrossRef Medline.
4. Antunes M, Biala G (2012) The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 13:93-110. CrossRef Medline.
5. Barak B, Okun E, Ben-Simon Y, Lavi A, Shapira R, Madar R, Wang Y, Norman E, Sheinin A, Pita MA, Yizhar O, Mughal MR, Stuenkel E, van Praag H, Mattson MP, Ashery U (2013) Neuron-specific expression of tomosyn1 in the mouse hippocampal dentate gyrus impairs spatial learning and memory. Neuromol Med 15:351-363. CrossRef Medline.
6. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39. CrossRef Medline.
7. Cai D, Cohen KB, Luo T, Lichtman JW, Sanes JR (2013) Improved tools for the Brainbow toolbox. Nat Methods 10:540-547. CrossRef Medline.
8. Castellani CA, Melka MG, Gui JL, O’Reilly RL, Singh SM (2015) Integration of DNA sequence and DNA methylation changes in monozygotic twin pairs discordant for schizophrenia. Schizophr Res 169:433-440. CrossRef Medline.
9. Cestra G, Toomre D, Chang S, De Camilli P (2005) The Abl/Arg substrate ArgBP2/nArgBP2 coordinates the function of multiple regulatory mechanisms converging on the actin cytoskeleton. Proc Natl Acad Sci U S A 102:1731-1736. CrossRef Medline.
10. Chen CY, Tsai MS, Lin CY, Yu IS, Chen YT, Lin SR, Juan LW, Chen YT, Hsu HM, Lee LJ, Lin SW (2012) Rescue of the genetically engineered Cul4b mutant mouse as a potential model for human X-linked mental retardation. Hum Mol Genet 21:4270-4285. CrossRef Medline.
11. Dang V, Medina B, Das D, Moghadam S, Martin KJ, Lin B, Naik P, Patel D, Nosheny R, Wesson Ashford J, Salehi A (2014) Formoterol, a longacting beta2 adrenergic agonist, improves cognitive function and promotes dendritic complexity in a mouse model of Down syndrome. Biol Psychiatry 75:179-188. CrossRef Medline.
12. Deakin NO, Turner CE (2008) Paxillin comes of age. J Cell Sci 121:2435-2444. CrossRef Medline.
13. Förster E, Zhao S, Frotscher M (2006) Laminating the hippocampus. Nat Rev Neurosci 7:259-267. CrossRef Medline.
14. Foust KD, Nurre E, Montgomery CL, Hernandez A, Chan CM, Kaspar BK (2009) Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 27:59-65. CrossRef Medline.
15. Fromer M, Pocklington AJ, Kavanagh DH, Williams HJ, Dwyer S, Gormley P, Georgieva L, Rees E, Palta P, Ruderfer DM, Carrera N, Humphreys I, Johnson JS, Roussos P, Barker DD, Banks E, Milanova V, Grant SG, Hannon E, Rose SA, et al. (2014) De novo mutations in schizophrenia implicate synaptic networks. Nature 506:179-184. CrossRef Medline.
16. Geng J, Picker J, Zheng Z, Zhang X, Wang J, Hisama F, Brown DW, Mullen MP, Harris D, Stoler J, Seman A, Miller DT, Fu Q, Roberts AE, Shen Y (2014) Chromosome microarray testing for patients with congenital heart defects reveals novel disease causing loci and high diagnostic yield. BMC Genomics 15:1127. CrossRef Medline.
17. Glover CP, Bienemann AS, Heywood DJ, Cosgrave AS, Uney JB (2002) Adenoviral-mediated, high-level, cell-specific transgene expression: a SYN1-WPRE cassette mediates increased transgene expression with no loss of neuron specificity. Mol Ther 5:509-516. CrossRef Medline.
18. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K (2009) Optical deconstruction of parkinsonian neural circuitry. Science 324: 354-359. CrossRef Medline.
19. Grover LM, Kim E, Cooke JD, Holmes WR (2009) LTP in hippocampal area CA1 is induced by burst stimulation over a broad frequency range centered around delta. Learn Mem 16:69-81. CrossRef Medline.
20. Gunaydin LA, Yizhar O, Berndt A, Sohal VS, Deisseroth K, Hegemann P (2010) Ultrafast optogenetic control. Nat Neurosci 13:387-392. CrossRef Medline.
21. Haglund K, Ivankovic-Dikic I, Shimokawa N, Kruh GD, Dikic I (2004) Recruitment of Pyk2 and Cbl to lipid rafts mediates signals important for actin reorganization in growing neurites. J Cell Sci 117:2557-2568. CrossRef Medline.
22. Hancock JF, Cadwallader K, Paterson H, Marshall CJ (1991) A CAAX or a CAAL motif and a 2nd signal are sufficient for plasma-membrane targeting of Ras proteins. EMBO J 10:4033-4039. Medline.
23. Heyer MP, Pani AK, Smeyne RJ, Kenny PJ, Feng G (2012) Normal midbrain dopaminergic neuron development and function in miR-133b mutant mice. J Neurosci 32:10887-10894. CrossRef Medline.
24. Jasnow AM, Schulkin J, Pfaff DW (2006) Estrogen facilitates fear conditioning and increases corticotropin-releasing hormone mRNA expression in the central amygdala in female mice. Horm Behav 49:197-205. CrossRef Medline.
25. Kaech S, Banker G (2006) Culturing hippocampal neurons. Nat Protoc 1:2406-2415. CrossRef Medline.
26. Kawabe H, Hata Y, Takeuchi M, Ide N, Mizoguchi A, Takai Y (1999) nArgBP2, a novel neural member of ponsin/ArgBP2/vinexin family that interacts with synapse-associated protein 90/postsynaptic density-95-associated protein (SAPAP). J Biol Chem 274:30914-30918. CrossRef Medline.
27. Kervestin S, Jacobson A (2012) NMD: a multifaceted response to premature translational termination. Nat Rev Mol Cell Bio 13:700-712. CrossRef Medline.
28. Kim IH, Racz B, Wang H, Burianek L, Weinberg R, Yasuda R, Wetsel WC, Soderling SH (2013) Disruption of Arp2/3 results in asymmetric structural plasticity of dendritic spines and progressive synaptic and behavioral abnormalities. J Neurosci 33:6081-6092. CrossRef Medline.
29. Kim JH, Lee SR, Li LH, Park HJ, Park JH, Lee KY, Kim MK, Shin BA, Choi SY (2011) High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLoS One 6:e18556. CrossRef Medline.
30. Kioka N, Ueda K, Amachi T (2002) Vinexin, CAP/ponsin, ArgBP2: a novel adaptor protein family regulating cytoskeletal organization and signal transduction. Cell Struct Funct 27:1-7. CrossRef Medline.
31. Krueger DD, Osterweil EK, Chen SP, Tye LD, Bear MF (2011) Cognitive dysfunction and prefrontal synaptic abnormalities in a mouse model of fragile X syndrome. Proc Natl Acad Sci U S A 108:2587-2592. CrossRef Medline.
32. Laplagne DA, Esposito MS, Piatti VC, Morgenstern NA, Zhao CM, van Praag H, Gage FH, Schinder AF (2006) Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol 4:2349-2360. CrossRef Medline.
33. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868-872. CrossRef Medline.
34. Luo L (2002) Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu Rev Cell Dev Biol 18:601-635. CrossRef Medline.
35. Maren S, Phan KL, Liberzon I (2013) The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14:417-428. CrossRef Medline.
36. Markus EJ, Zecevic M (1997) Sex differences and estrous cycle changes in hippocampus-dependent fear conditioning. Psychobiology 25:246-252.
37. Martin M, Geudens I, Bruyr J, Potente M, Bleuart A, Lebrun M, Simonis N, Deroanne C, Twizere JC, Soubeyran P, Peixoto P, Mottet D, Janssens V, Hofmann WK, Claes F, Carmeliet P, Kettmann R, Gerhardt H, Dequiedt F (2013) PP2A regulatory subunit Balpha controls endothelial contractility and vessel lumen integrity via regulation of HDAC7. EMBO J 32: 2491-2503. CrossRef Medline.
38. Murase K, Ito H, Kanoh H, Sudo K, Iwamoto I, Morishita R, Soubeyran P, Seishima M, Nagata K (2012) Cell biological characterization of a multidomain adaptor protein, ArgBP2, in epithelialNMuMGcells, and identification of a novel short isoform. Med Mol Morphol 45:22-28. CrossRef Medline.
39. Negishi M, Katoh H (2005) Rho family GTPases and dendrite plasticity. Neuroscientist 11:187-191. CrossRef Medline.
40. Nishimura-Akiyoshi S, Niimi K, Nakashiba T, Itohara S (2007) Axonal netrin-Gs transneuronally determine lamina-specific subdendritic segments. Proc Natl Acad Sci U S A 104:14801-14806. CrossRef Medline.
41. Osumi N, Guo N, Matsumata M, Yoshizaki K (2015) Neurogenesis and sensorimotor gating: bridging a microphenotype and an endophenotype. Curr Mol Med 15:129-137. CrossRef Medline.
42. Pavlowsky A, Chelly J, Billuart P (2012) Emerging major synaptic signaling pathways involved in intellectual disability. Mol Psychiatry 17:682-693. CrossRef Medline.
43. Peça J, Feliciano C, Ting JT, Wang WT, Wells MF, Venkatraman TN, Lascola CD, Fu ZY, Feng GP (2011) Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 472:437-442. CrossRef Medline.
44. Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106:274-285. CrossRef Medline.
45. Powell AD, Gill KK, Saintot PP, Jiruska P, Chelly J, Billuart P, Jefferys JG (2012) Rapid reversal of impaired inhibitory and excitatory transmission but not spine dysgenesis in a mouse model of mental retardation. J Physiol 590:763-776. CrossRef Medline.
46. Rahimi O, Claiborne BJ (2007) Morphological development and maturation of granule neuron dendrites in the rat dentate gyrus. Prog Brain Res 163:167-181. CrossRef Medline.
47. Rodriguez A, Ehlenberger DB, Dickstein DL, Hof PR, Wearne SL (2008) Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS One 3:e1997. CrossRef Medline.
48. Roignot J, Soubeyran P (2009) ArgBP2 and theSoHofamily of adapter proteins in oncogenic diseases. Cell Adh Migr 3:167-170. CrossRef Medline.
49. Rönty M, Taivainen A, Moza M, Kruh GD, Ehler E, Carpen O (2005) Involvement of palladin and alpha-actinin in targeting of the Abl/Arg kinase adaptor ArgBP2 to the actin cytoskeleton. Exp Cell Res 310:88-98. CrossRef Medline.
50. Rossi MR, DiMaio MS, Xiang B, Lu K, Kaymakcalan H, Seashore M, Mahoney MJ, Li P (2009) Clinical and genomic characterization of distal duplications and deletions of chromosome 4q: study of two cases and review of the literature. Am J Med Genet A 149A:2788-2794. CrossRef Medline.
51. Scaife RM, Courtneidge SA, Langdon WY (2003) The multi-adaptor protooncoprotein Cbl is a key regulator of Rac and actin assembly. J Cell Sci 116:463-473. CrossRef Medline.
52. 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.
53. Vadodaria KC, Brakebusch C, Suter U, Jessberger S (2013) Stage-specific functions of the small rho GTPases Cdc42 and Rac1 for adult hippocampal neurogenesis. J Neurosci 33:1179-1189. CrossRef Medline.
54. van BokhovenH (2011) Genetic and epigenetic networks in intellectual disabilities. Annu Rev Genet 45:81-104. CrossRef Medline.
55. van Goethem NP, Rutten K, van der Staay FJ, Jans LA, Akkerman S, Steinbusch HW, Blokland A, van’t Klooster J, Prickaerts J (2012) Object recognition testing: rodent species, strains, housing conditions, and estrous cycle. Behav Brain Res 232:323-334. CrossRef Medline.
56. Vorhees CV, Williams MT (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1:848-858. CrossRef Medline.
57. Wang B, Golemis EA, Kruh GD (1997) ArgBP2, a multiple Src homology 3 domain-containing, Arg/Abl-interacting protein, is phosphorylated in v-Abl-transformed cells and localized in stress fibers and cardiocyte Z-disks. J Biol Chem 272:17542-17550. CrossRef Medline.
58. Welch JM, Wang D, Feng G (2004) Differential mRNA expression and protein localization of the SAP90/PSD-95-associated proteins (SAPAPs) in the nervous system of the mouse. J Comp Neurol 472:24-39. CrossRef Medline.
59. Welch JM, Lu J, Rodriguiz RM, Trotta NC, Peça J, Ding JD, Feliciano C, Chen M, Adams JP, Luo J, Dudek SM, Weinberg RJ, Calakos N, Wetsel WC, Feng G (2007) Cortico-striatal synaptic defects and OCD-like behaviours in Sapap3-mutant mice. Nature 448:894-900. CrossRef Medline.
60. Witter MP (2007) The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog Brain Res 163:43-61. CrossRef Medline.
61. Yardeni T, Eckhaus M, Morris HD, Huizing M, Hoogstraten-Miller S (2011) Retro-orbital injections in mice. Lab Anim (NT) 40:155-160. CrossRef Medline.
62. Yuan ZQ, Kim D, Kaneko S, Sussman M, Bokoch GM, Kruh GD, Nicosia SV, Testa JR, Cheng JQ (2005) ArgBP2gamma interacts with Akt and p21-activated kinase-1 and promotes cell survival. J Biol Chem 280:21483-21490. CrossRef Medline.
63. Zhang Q, Wang F, Cao J, Shen Y, Huang Q, Bao L, Zhu X (2009) Nudel promotes axonal lysosome clearance and endo-lysosome formation via dynein-mediated transport. Traffic 10:1337-1349. CrossRef Medline.