Diversification of behavior and postsynaptic properties by netrin-G presynaptic adhesion family proteins

Molecular Brain

Volumn 9, Issue 1, 2016, Pages

  Zhang, Qi ^a   Goto, Hiromichi ^a   Akiyoshi Nishimura, Sachiko ^a   Prosselkov, Pavel ^a   Sano, Chie ^a   Matsukawa, Hiroshi ^a   Yaguchi, Kunio ^a   Nakashiba, Toshiaki ^a   Itohara, Shigeyoshi ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Cognitive diversification; GPI protein; Molecular evolution; Netrin G2; Netrtin G1; Postsynapse; Presynapse

Indexed keywords

NETRIN; NETRIN G1; NETRIN G2; POSTSYNAPTIC DENSITY PROTEIN 95; UNCLASSIFIED DRUG; DLGH4 PROTEIN, MOUSE; GUANYLATE KINASE; MEMBRANE PROTEIN; NERVE PROTEIN; NETRIN-G1; NTNG2 PROTEIN, MOUSE;

ADAPTIVE BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; ATTENTION; COGNITION; CONTROLLED STUDY; GENETIC ANALYSIS; IMPULSIVENESS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SENSORIMOTOR FUNCTION; TASK PERFORMANCE; WORKING MEMORY; ANIMAL; ANIMAL BEHAVIOR; BRAIN; C57BL MOUSE; EMOTION; KNOCKOUT MOUSE; MEMORY; METABOLISM; NERVE CELL NETWORK; NERVE ENDING; PHENOTYPE; SENSORIMOTOR CORTEX; SYNAPSE;

ANIMALS; ATTENTION; BEHAVIOR, ANIMAL; BRAIN; EMOTIONS; GUANYLATE KINASES; MEMBRANE PROTEINS; MEMORY; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE NET; NERVE TISSUE PROTEINS; PHENOTYPE; PRESYNAPTIC TERMINALS; SENSORIMOTOR CORTEX; SYNAPSES;

EID: 84954118616     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/s13041-016-0187-5     Document Type: Article

References (87)

1. Brown D, Waneck GL. Glycosyl-phosphatidylinositol-anchored membrane proteins. J Am Soc Nephrol. 1992;3:895-906
2. Ikezawa H. Glycosylphosphatidylinositol (GPI)-anchored proteins. Biol Pharm Bull. 2002;25:409-17
3. Taylor DR, Hooper NM. GPI-anchored proteins in health and disease. In Post-translational modifications in health and disease. Volume 13 of the series of Protein Reviews. Edited by Vidal CJ: New York: Springer Science + Business Media; 2011. p. 39-55
4. Mani A, Singh S, Dwivedi M, Tripathi V, Gupta DK. An evolutionary account of GPI anchored proteins. Eur J Exp Biol. 2011;1:148-55
5. Walsh FS, Doherty P. Glycosylphosphatidylinositol anchored recognition molecules that function in axonal fasciculation, growth and guidance in the nervous system. Cell Biol Int Rep. 1991;15:1151-66
6. Hattori M, Osterfield M, Flanagan JG. Regulated cleavage of a contact-mediated axon repellent. Science. 2000;289:1360-5
7. Karagogeos D. Neural GPI-anchored cell adhesion molecules. Front Biosci. 2003;1:s1304-1320
8. Labasque M, Faivre-Sarrailh C. GPI-anchored proteins at the node of Ranvier. FEBS Lett. 2010;584:1787-92
9. Hruska M, Dalva MB. Ephrin regulation of synapse formation, function and plasticity. Mol Cell Neurosci. 2012;50:35-44
10. Brennaman LH, Zhang X, Guan H, Triplett JW, Brown A, Demyanenko GP, et al. Polysialylated NCAM and ephrinA/EphA regulate synaptic development of GABAergic interneurons in prefrontal cortex. Cereb Cortex. 2013;23:162-77
11. Nosten-Bertrand M, Errington ML, Murphy KP, Tokugawa Y, Barboni E, Kozlova E, et al. Normal spatial learning despite regional inhibition of LTP in mice lacking Thy-1. Nature. 1996;379:826-9
12. Murai KK, Misner D, Ranscht B. Contactin supports synaptic plasticity associated with hippocampal long-term depression but not potentiation. Curr Biol. 2002;12:181-90
13. Innos J, Philips MA, Leidmaa E, Heinla I, Raud S, Reemann P, et al. Lower anxiety and a decrease in agonistic behaviour in Lsamp-deficient mice. Behav Brain Res. 2011;217:21-31
14. Prachumwat A, Li WH. Gene number expansion and contraction in vertebrate genomes with respect to invertebrate genomes. Genome Res. 2008;18:221-32
15. Nithianantharajah J, Komiyama NH, McKechanie A, Johnstone M, Blackwood DH, St Clair D, et al. Synaptic scaffold evolution generated components of vertebrate cognitive complexity. Nat Neurosci. 2013;16:16-24
16. Ryan TJ, Kopanitsa MV, Indersmitten T, Nithianantharajah J, Afinowi NO, Pettit C, et al. Evolution of GluN2A/B cytoplasmic domains diversified vertebrate synaptic plasticity and behavior. Nat Neurosci. 2013;16:25-32
17. Nakashiba T, Ikeda T, Nishimura S, Tashiro K, Honjo T, Culotti JG, et al. Netrin-G1: a novel glycosyl phosphatidylinositol-linked mammalian netrin that is functionally divergent from classical netrins. J Neurosci. 2000;20:6540-50
18. Nakashiba T, Nishimura S, Ikeda T, Itohara S. Complementary expression and neurite outgrowth activity of netrin-G subfamily members. Mech Dev. 2002;111:47-60
19. Yin Y, Miner JH, Sanes JR. Laminets: laminin- and netrin-related genes expressed in distinct neuronal subsets. Mol Cell Neurosci. 2002;19:344-58
20. Guthrie S. Axon guidance: netrin receptors are revealed. Curr Biol. 1997;7:R6-9
21. Braisted JE, Catalano SM, Stimac R, Kennedy TE, Tessier-Lavigne M, Shatz CJ, et al. Netrin-1 promotes thalamic axon growth and is required for proper development of the thalamocortical projection. J Neurosci. 2000;20:5792-801
22. Nishimura-Akiyoshi S, Niimi K, Nakashiba T, Itohara S. Axonal netrin-Gs transneuronally determine lamina-specific subdendritic segments. Proc Natl Acad Sci U S A. 2007;104:14801-6
23. Zhang W, Rajan I, Savelieva KV, Wang CY, Vogel P, Kelly M, et al. Netrin-G2 and netrin-G2 ligand are both required for normal auditory responsiveness. Genes Brain Behav. 2008;7:385-92
24. Lin JC, Ho WH, Gurney A, Rosenthal A. The netrin-G1 ligand NGL-1 promotes the outgrowth of thalamocortical axons. Nat Neurosci. 2003;6:1270-6
25. Kim S, Burette A, Chung HS, Kwon SK, Woo J, Lee HW, et al. NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci. 2006;9:1294-301
26. Brasch J, Harrison OJ, Ahlsen G, Liu Q, Shapiro L. Crystal structure of the ligand binding domain of netrin G2. J Mol Biol. 2011;414:723-34
27. Seiradake E, Coles CH, Perestenko PV, Harlos K, McIlhinney RA, Aricescu AR, et al. Structural basis for cell surface patterning through NetrinG-NGL interactions. EMBO J. 2011;30:4479-88
28. Fukasawa M, Aoki M, Yamada K, Iwayama-Shigeno Y, Takao H, Meerabux J, et al. Case-control association study of human netrin G1 gene in Japanese schizophrenia. J Med Dent Sci. 2004;51:121-8
29. Aoki-Suzuki M, Yamada K, Meerabux J, Iwayama-Shigeno Y, Ohba H, Iwamoto K, et al. A family-based association study and gene expression analyses of netrin-G1 and -G2 genes in schizophrenia. Biol Psychiatry. 2005;57:382-93
30. Bisgaard AM, Rasmussen LN, Moller HU, Kirchhoff M, Bryndorf T. Interstitial deletion of the short arm of chromosome 1 (1p13.1p21.1) in a girl with mental retardation, short stature and colobomata. Clin Dysmorphol. 2007;16:109-12
31. Eastwood SL, Harrison PJ. Decreased mRNA expression of netrin-G1 and netrin-G2 in the temporal lobe in schizophrenia and bipolar disorder. Neuropsychopharmacology. 2008;33:933-45
32. Ohtsuki T, Horiuchi Y, Koga M, Ishiguro H, Inada T, Iwata N, et al. Association of polymorphisms in the haplotype block spanning the alternatively spliced exons of the NTNG1 gene at 1p13.3 with schizophrenia in Japanese populations. Neurosci Lett. 2008;435:194-7
33. Yaguchi K, Nishimura-Akiyoshi S, Kuroki S, Onodera T, Itohara S. Identification of transcriptional regulatory elements for Ntng1 and Ntng2 genes in mice. Mol Brain. 2014;7:19
34. Matsukawa H, Akiyoshi-Nishimura S, Zhang Q, Lujan R, Yamaguchi K, Goto H, et al. Netrin-G/NGL Complexes Encode Functional Synaptic Diversification. J Neurosci. 2014;34:15779-92
35. Glickfeld LL, Histed MH, Maunsell JH. Mouse primary visual cortex is used to detect both orientation and contrast changes. J Neurosci. 2013;33:19416-22
36. Scholl B, Burge J, Priebe NJ. Binocular integration and disparity selectivity in mouse primary visual cortex. J Neurophysiol. 2013;109:3013-24
37. Soto F, Watkins KL, Johnson RE, Schottler F, Kerschensteiner D. NGL-2 regulates pathway-specific neurite growth and lamination, synapse formation, and signal transmission in the retina. J Neurosci. 2013;33:11949-59
38. Henry KR. Auditory brainstem volume-conducted responses: origins in the laboratory mouse. J Am Aud Soc. 1979;4:173-8
39. Doya K. Complementary roles of basal ganglia and cerebellum in learning and motor control. Curr Opin Neurobiol. 2000;10:732-9
40. Ito M. Mechanisms of motor learning in the cerebellum. Brain Res. 2000;886:237-45
41. Coura RS, Cressant A, Xia J, de Chaumont F, Olivo-Marin JC, Pelloux Y, et al. Nonaggressive and adapted social cognition is controlled by the interplay between noradrenergic and nicotinic receptor mechanisms in the prefrontal cortex. FASEB J. 2013;27:4343-54
42. Kim JJ, Fanselow MS. Modality-specific retrograde amnesia of fear. Science. 1992;256:675-7
43. Morris RG, Garrud P, Rawlins JN, O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 1982;297:681-3
44. Dudchenko PA. An overview of the tasks used to test working memory in rodents. Neurosci Biobehav Rev. 2004;28:699-709
45. Olton DS, Samuelson RJ. Remembrance of places passed - spatial memory in rats. J Exp Psych-Anim Behav Proc. 1976;2:97-116
46. van Asselen M, Kessels RP, Neggers SF, Kappelle LJ, Frijns CJ, Postma A. Brain areas involved in spatial working memory. Neuropsychologia. 2006;44:1185-94
47. Niewoehner B, Single FN, Hvalby Ø, Jensen V, Meyer zum Alten Borgloh S, Seeburg PH, et al. Impaired spatial working memory but spared spatial reference memory following functional loss of NMDA receptors in the dentate gyrus. Eur J Neurosci. 2007;25:837-46
48. Petersen SE, Posner MI. The attention system of the human brain: 20 years after. Annu Rev Neurosci. 2012;35:73-89
49. Aspide R, Fresiello A, de Filippis G, Gironi Carnevale UA, Sadile AG. Non-selective attention in a rat model of hyperactivity and attention deficit: subchronic methylphenydate and nitric oxide synthesis inhibitor treatment. Neurosci Biobehav Rev. 2000;24:59-71
50. Robbins TW. The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berl). 2002;163:362-80
51. Kobayashi Y, Sano Y, Vannoni E, Goto H, Suzuki H, Oba A, et al. Genetic dissection of medial habenula-interpeduncular nucleus pathway function in mice. Front Behav Neurosci. 2013;7:17
52. Fineberg NA, Potenza MN, Chamberlain SR, Berlin HA, Menzies L, Bechara A, et al. Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review. Neuropsychopharmacology. 2010;35:591-604
53. Hollingsworth EB, McNeal ET, Burton JL, Williams RJ, Daly JW, Creveling CR. Biochemical characterization of a filtered synaptoneurosome preparation from guinea pig cerebral cortex: cyclic adenosine 3':5'-monophosphate-generating systems, receptors, and enzymes. J Neurosci. 1985;5:2240-53
54. Ricciardi S, Ungaro F, Hambrock M, Rademacher N, Stefanelli G, Brambilla D, et al. CDKL5 ensures excitatory synapse stability by reinforcing NGL-1-PSD95 interaction in the postsynaptic compartment and is impaired in patient iPSC-derived neurons. Nature Cell Biol. 2012;14:911-23
55. Zhang Y, Matt L, Patriarchi T, Malik ZA, Chowdhury D, Park DK, et al. Capping of the N-terminus of PSD-95 by calmodulin triggers its postsynaptic release. EMBO J. 2014;33:1341-53
56. Augustine GJ, Santamaria F, Tanaka K. Local calcium signaling in neurons. Neuron. 2003;40:331-46
57. Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R. Activation of CaMKII in single dendritic spines during long-term potentiation. Nature. 2009;458:299-304
58. Emes RD, Pocklington AJ, Anderson CN, Bayes A, Collins MO, Vickers CA, et al. Evolutionary expansion and anatomical specialization of synapse proteome complexity. Nat Neurosci. 2008;11:799-806
59. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron. 1994;12:529-40
60. Sakimura K, Kutsuwada T, Ito I, Manabe T, Takayama C, Kushiya E, et al. Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor epsilon 1 subunit. Nature. 1995;373:151-5
61. Kutsuwada T, Sakimura K, Manabe T, Takayama C, Katakura N, Kushiya E, et al. Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor epsilon 2 subunit mutant mice. Neuron. 1996;16:333-44
62. Sprengel R, Suchanek B, Amico C, Brusa R, Burnashev N, Rozov A, et al. Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell. 1998;92:279-89
63. Cuthbert PC, Stanford LE, Coba MP, Ainge JA, Fink AE, Opazo P, et al. Synapse-associated protein 102/dlgh3 couples the NMDA receptor to specific plasticity pathways and learning strategies. J Neurosci. 2007;27:2673-82
64. Endele S, Rosenberger G, Geider K, Popp B, Tamer C, Stefanova I, et al. Mutations in GRIN2A and GRIN2B encoding regulatory subunits of NMDA receptors cause variable neurodevelopmental phenotypes. Nat Genet. 2010;42:1021-6
65. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature. 1998;396:433-9
66. Carlisle HJ, Fink AE, Grant SG, O'Dell TJ. Opposing effects of PSD-93 and PSD-95 on long-term potentiation and spike timing-dependent plasticity. J Physiol. 2008;586:5885-900
67. Fremeau Jr RT, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, et al. Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science. 2004;304:1815-9
68. Fremeau Jr RT, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, et al. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron. 2001;31:247-60
69. Fremeau Jr RT, Voglmaier S, Seal RP, Edwards RH. VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci. 2004;27:98-103
70. Crawley JN: What's wrong with my mouse?: behavioral phenotyping of transgenic and knockout mice. New Jersey: John Wiley & Sons; 2007
71. Prusky GT, Alam NM, Douglas RM. Enhancement of vision by monocular deprivation in adult mice. J Neurosci. 2006;26:11554-61
72. Fox MW. The visual cliff test for the study of visual depth perception in the mouse. Anim Behav. 1965;13:232-3
73. Kurt S, Groszer M, Fisher SE, Ehret G. Modified sound-evoked brainstem potentials in Foxp2 mutant mice. Brain Res. 2009;1289:30-6
74. Koch M, Schnitzler HU. The acoustic startle response in rats - circuits mediating evocation, inhibition and potentiation. Behav Brain Res. 1997;89:35-49
75. Shibuki K, Gomi H, Chen L, Bao S, Kim JJ, Wakatsuki H, et al. Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice. Neuron. 1996;16:587-99
76. Bearzatto B, Servais L, Cheron G, Schiffmann SN. Age dependence of strain determinant on mice motor coordination. Brain Res. 2005;1039:37-42
77. Sano Y, Ornthanalai VG, Yamada K, Homma C, Suzuki H, Suzuki T, et al. X11-like protein deficiency is associated with impaired conflict resolution in mice. J Neurosci. 2009;29:5884-96
78. Dere E, Huston JP, De Souza Silva MA. The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci Biobehav Rev. 2007;31:673-704
79. Pellow S, Chopin P, File SE, Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods. 1985;14:149-67
80. Porsolt RD, Le Pichon M, Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature. 1977;266:730-2
81. Araya R, Noguchi T, Yuhki M, Kitamura N, Higuchi M, Saido TC, et al. Loss of M5 muscarinic acetylcholine receptors leads to cerebrovascular and neuronal abnormalities and cognitive deficits in mice. Neurobiol Dis. 2006;24:334-44
82. Sarter M, Bodewitz G, Stephens DN. Attenuation of scopolamine-induced impairment of spontaneous alteration behaviour by antagonist but not inverse agonist and agonist beta-carbolines. Psychopharmacology (Berl). 1988;94:491-5
83. 2+ signals are required for the functional integrity of tripartite synapses. Mol Brain. 2013;6:6
84. Kim JJ, Rison RA, Fanselow MS. Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behav Neurosci. 1993;107:1093-8
85. Lee K, Kobayashi Y, Seo H, Kwak JH, Masuda A, Lim CS, et al. Involvement of cAMP-guanine nucleotide exchange factor II in hippocampal long-term depression and behavioral flexibility. Mol Brain. 2015;8:38
86. Floresco SB, Seamans JK, Phillips AG. Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J Neurosci. 1997;17:1880-90
87. Moore SW, Tessier-Lavigne M, Kennedy TE. Netrins and their receptors. Adv Exp Med Biol. 2007;621:17-31