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Defects in syntabulin-mediated synaptic cargo transport associate with autism-like synaptic dysfunction and social behavioral traits

Molecular Psychiatry volume 26, pages 1472–1490 (2021)Cite this article

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Abstract

The formation and maintenance of synapses require long-distance delivery of newly synthesized synaptic proteins from the soma to distal synapses, raising the fundamental question of whether impaired transport is associated with neurodevelopmental disorders such as autism. We previously revealed that syntabulin acts as a motor adapter linking kinesin-1 motor and presynaptic cargos. Here, we report that defects in syntabulin-mediated transport and thus reduced formation and maturation of synapses are one of core synaptic mechanisms underlying autism-like synaptic dysfunction and social behavioral abnormalities. Syntabulin expression in the mouse brain peaks during the first 2 weeks of postnatal development and progressively declines during brain maturation. Neurons from conditional syntabulin−/− mice (stb cKO) display impaired transport of presynaptic cargos, reduced synapse density and active zones, and altered synaptic transmission and long-term plasticity. Intriguingly, stb cKO mice exhibit core autism-like traits, including defective social recognition and communication, increased stereotypic behavior, and impaired spatial learning and memory. These phenotypes establish a new mechanistic link between reduced transport of synaptic cargos and impaired maintenance of synaptic transmission and plasticity, contributing to autism-associated behavioral abnormalities. This notion is further confirmed by the human missense variant STB-R178Q, which is found in an autism patient and loses its adapter capacity for binding kinesin-1 motors. Expressing STB-R178Q fails to rescue reduced synapse formation and impaired synaptic transmission and plasticity in stb cKO neurons. Altogether, our study suggests that defects in syntabulin-mediated transport mechanisms underlie the synaptic dysfunction and behavioral abnormalities that bear similarities to autism.

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Fig. 1: stb cKO neurons display impaired axonal transport of presynaptic cargos, reduced density of synapses and spines, and altered structures of AZs.
Fig. 2: The human autism-linked STB missense variant is a loss-of-function mutant.
Fig. 3: Stb cKO mice exhibit deficits in synaptic transmission and long-term plasticity.
Fig. 4: The human autism-associated STB variant fails to rescue synaptic dysfunction in cKO neurons.
Fig. 5: Stb cKO mice exhibit core autistic traits.

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References

  1. Goda Y, Davis GW. Mechanisms of synapse assembly and disassembly. Neuron. 2003;40:243–64.

    CAS  PubMed  Google Scholar 

  2. Chia PH, Li PP, Shen K. Cellular and molecular mechanisms underlying presynapse formation. J Cell Biol. 2013;203:11–22.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Ziv NE, Garner CC. Cellular and molecular mechanisms of presynaptic assembly. Nat Rev Neurosci. 2004;5:385–99.

    CAS  PubMed  Google Scholar 

  4. Nakata T, Terada S, Hirokawa N. Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons. J Cell Biol. 1998;140:659–74.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Jin Y, Garner CC. Molecular mechanisms of presynaptic differentiation. Annu Rev Cell Dev Biol. 2008;24:237–62.

    CAS  PubMed  Google Scholar 

  6. Gundelfinger ED, Fejtova A. Molecular organization and plasticity of the cytomatrix at the active zone. Curr Opin Neurobiol. 2012;22:423–30.

    CAS  PubMed  Google Scholar 

  7. Fenster SD, Chung WJ, Zhai R, Cases-Langhoff C, Voss B, Garner AM, et al. Piccolo, a presynaptic zinc finger protein structurally related to bassoon. Neuron. 2000;25:203–14.

    CAS  PubMed  Google Scholar 

  8. Gundelfinger ED, Reissner C, Garner CC. Role of Bassoon and Piccolo in assembly and molecular organization of the active zone. Front Synaptic Neurosci. 2015;7:19.

    PubMed  Google Scholar 

  9. Altrock WD, tom Dieck S, Sokolov M, Meyer AC, Sigler A, Brakebusch C, et al. Functional inactivation of a fraction of excitatory synapses in mice deficient for the active zone protein bassoon. Neuron. 2003;37:787–800.

    CAS  PubMed  Google Scholar 

  10. Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelfinger ED, Ziv NE, et al. Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron. 2001;29:131–43.

    CAS  PubMed  Google Scholar 

  11. Lord C, Risi S, Lambrecht L, Cook EH, Leventhal BL, DiLavore PC, et al. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord. 2000;30:205–23.

    CAS  PubMed  Google Scholar 

  12. Miles JH. Autism spectrum disorders-a genetics review. Genet Med. 2011;13:278–94.

    PubMed  Google Scholar 

  13. Yuen RK, Thiruvahindrapuram B, Merico D, Walker S, Tammimies K, Hoang N, et al. Whole-genome sequencing of quartet families with autism spectrum disorder. Nat Med. 2015;21:185–91.

    CAS  PubMed  Google Scholar 

  14. Sanders SJ, Murtha MT, Gupta AR, Murdoch JD, Raubeson MJ, Willsey AJ, et al. De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature. 2012;485:237–41.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Iossifov I, O’Roak BJ, Sanders SJ, Ronemus M, Krumm N, Levy D, et al. The contribution of de novo coding mutations to autism spectrum disorder. Nature. 2014;515:216–21.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Tabuchi K, Blundell J, Etherton MR, Hammer RE, Liu X, Powell CM, et al. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science. 2007;318:71–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Peca J, Feliciano C, Ting JT, Wang WT, Wells MF, Venkatraman TN, et al. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature. 2011;472:437–U534.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Tsai NP, Wilkerson JR, Guo WR, Maksimova MA, DeMartino GN, Cowan CW, et al. Multiple autism-linked genes mediate synapse elimination via proteasomal degradation of a synaptic scaffold PSD-95. Cell. 2012;151:1581–94.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Ebert DH, Greenberg ME. Activity-dependent neuronal signalling and autism spectrum disorder. Nature. 2013;493:327–37.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Davenport EC, Szulc BR, Drew J, Taylor J, Morgan T, Higgs NF, et al. Autism and Schizophrenia-Associated CYFIP1 Regulates the Balance of Synaptic Excitation and Inhibition. Cell Rep. 2019;26:2037–51. e2036.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Zoghbi HY. Postnatal neurodevelopmental disorders: meeting at the synapse? Science. 2003;302:826–30.

    CAS  PubMed  Google Scholar 

  22. Bourgeron T. A synaptic trek to autism. Curr Opin Neurobiol. 2009;19:231–4.

    CAS  PubMed  Google Scholar 

  23. Su QN, Cai Q, Gerwin C, Smith CL, Sheng ZH. Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat Cell Biol. 2004;6:941–53.

    CAS  PubMed  Google Scholar 

  24. Ylisaukko-oja T, Alarcon M, Cantor RM, Auranen M, Vanhala R, Kempas E, et al. Search for autism loci by combined analysis of autism genetic resource exchange and finnish families. Ann Neurol. 2006;59:145–55.

    PubMed  Google Scholar 

  25. Delgado MS, Camprubi C, Tumer Z, Martinez F, Mila M, Monk D. Screening individuals with intellectual disability, autism and Tourette’s syndrome for KCNK9 mutations and aberrant DNA methylation within the 8q24 imprinted cluster. Am J Med Genet B. 2014;165:472–8.

    CAS  Google Scholar 

  26. Chen CH, Chen HI, Chien WH, Li LH, Wu YY, Chiu YN, et al. High resolution analysis of rare copy number variants in patients with autism spectrum disorder from Taiwan. Sci Rep. 2017;7:11919.

    PubMed  PubMed Central  Google Scholar 

  27. Herman GE, Hansen-Kiss E, Sadee W, Barrie E. A collaborative translational autism research program for the military. 2016 https://apps.dtic.mil/dtic/tr/fulltext/u2/a631878.pdf.

  28. Perlson E, Jeong GB, Ross JL, Dixit R, Wallace KE, Kalb RG, et al. A switch in retrograde signaling from survival to stress in rapid-onset neurodegeneration. J Neurosci. 2009;29:9903–17.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Cohen-Cory S. The developing synapse: Construction and modulation of synaptic structures and circuits. Science. 2002;298:770–6.

    CAS  PubMed  Google Scholar 

  30. Wong ROL, Ghosh A. Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci. 2002;3:803–12.

    CAS  PubMed  Google Scholar 

  31. Isshiki M, Tanaka S, Kuriu T, Tabuchi K, Takumi T, Okabe S. Enhanced synapse remodelling as a common phenotype in mouse models of autism. Nat Commun. 2014;5:4742.

    CAS  PubMed  Google Scholar 

  32. Knaus P, Betz H, Rehm H. Expression of synaptophysin during postnatal-development of the mouse brain. J Neurochem. 1986;47:1302–4.

    CAS  PubMed  Google Scholar 

  33. Watson RE, DeSesso JM, Hurtt ME, Cappon GD. Postnatal growth and morphological development of the brain: a species comparison. Birth Defects Res B Dev Reprod Toxicol. 2006;77:471–84.

    CAS  PubMed  Google Scholar 

  34. Xu J, Wang N, Luo JH, Xia J. Syntabulin regulates the trafficking of PICK1-containing vesicles in neurons. Sci Rep. 2016;6:20924.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Xia J, Zhang XQ, Staudinger J, Huganir RL. Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron. 1999;22:179–87.

    CAS  PubMed  Google Scholar 

  36. Terashima A, Pelkey KA, Rah JC, Suh YH, Roche KW, Collingridge GL, et al. An essential role for PICK1 in NMDA receptor-dependent bidirectional synaptic plasticity. Neuron. 2008;57:872–82.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Volk L, Kim CH, Takamiya K, Yu YL, Huganir RL. Developmental regulation of protein interacting with C kinase 1 (PICK1) function in hippocampal synaptic plasticity and learning. Proc Natl Acad Sci USA. 2010;107:21784–9.

    PubMed  Google Scholar 

  38. Cai Q, Gerwin C, Sheng ZH. Syntabulin-mediated anterograde transport of mitochondria along neuronal processes. J Cell Biol. 2005;170:959–69.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Sheng ZH. The interplay of axonal energy homeostasis and mitochondrial trafficking and anchoring. Trends Cell Biol. 2017;27:403–16.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Phelps SM, Campbell P, Zheng DJ, Ophir AG. Beating the boojum: comparative approaches to the neurobiology of social behavior. Neuropharmacology. 2010;58:17–28.

    CAS  PubMed  Google Scholar 

  41. Etherton M, Foldy C, Sharma M, Tabuchi K, Liu XR, Shamloo M, et al. Autism-linked neuroligin-3 R451C mutation differentially alters hippocampal and cortical synaptic function. Proc Natl Acad Sci USA. 2011;108:13764–9.

    CAS  PubMed  Google Scholar 

  42. Won H, Lee HR, Gee HY, Mah W, Kim JI, Lee J, et al. Autistic-like social behaviour in Shank2-mutant mice improved by restoring NMDA receptor function. Nature. 2012;486:261–5.

    CAS  PubMed  Google Scholar 

  43. Citri A, Malenka RC. Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology. 2008;33:18–41.

    PubMed  Google Scholar 

  44. Luscher C, Malenka RC. NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol. 2012;4:a005710.

    PubMed  PubMed Central  Google Scholar 

  45. Beattie EC, Carroll RC, Yu X, Morishita W, Yasuda H, von Zastrow M, et al. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat Neurosci. 2000;3:1291–300.

    CAS  PubMed  Google Scholar 

  46. Hanley JG. Molecular mechanisms for regulation of AMPAR trafficking by PICK1. Biochem Soc Trans. 2006;34:931–5.

    CAS  PubMed  Google Scholar 

  47. Rocca DL, Martin S, Jenkins EL, Hanley JG. Inhibition of Arp2/3-mediated actin polymerization by PICK1 regulates neuronal morphology and AMPA receptor endocytosis. Nat Cell Biol. 2008;10:259–U257.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Fiuza M, Rostosky CM, Parkinson GT, Bygrave AM, Halemani N, Baptista M, et al. PICK1 regulates AMPA receptor endocytosis via direct interactions with AP2 alpha-appendage and dynamin. J Cell Biol. 2017;216:3323–38.

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Asrican B, Lisman J, Otmakhov N. Synaptic strength of individual spines correlates with bound Ca2+-calmodulin-dependent kinase II. J Neurosci. 2007;27:14007–11.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci. 2001;4:1086–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Segal M. Dendritic spines and long-term plasticity. Nat Rev Neurosci. 2005;6:277–84.

    CAS  PubMed  Google Scholar 

  52. Zhou Q, Homma KJ, Poo MM. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron. 2004;44:749–57.

    CAS  PubMed  Google Scholar 

  53. Nagerl UV, Eberhorn N, Cambridge SB, Bonhoeffer T. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron. 2004;44:759–67.

    PubMed  Google Scholar 

  54. Xu-Friedman MA, Regehr WG. Probing fundamental aspects of synaptic transmission with strontium. J Neurosci. 2000;20:4414–22.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Hagler DJ, Goda Y. Properties of synchronous and asynchronous release during pulse train depression in cultured hippocampal neurons. J Neurophysiol. 2001;85:2324–34.

    CAS  PubMed  Google Scholar 

  56. Moy SS, Nadler JJ, Perez A, Barbaro RP, Johns JM, Magnuson TR, et al. Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav. 2004;3:287–302.

    CAS  PubMed  Google Scholar 

  57. Thor DH, Holloway WR. Social memory of the male laboratory rat. J Comp Physiol Psychol. 1982;96:1000–6.

    Google Scholar 

  58. Mody M, Belliveau JW. Speech and language impairments in autism: Insights from behavior and neuroimaging. N Am J Med Sci. 2013;5:157–61.

    Google Scholar 

  59. Chung W, Choi SY, Lee E, Park H, Kang J, Park H, et al. Social deficits in IRSp53 mutant mice improved by NMDAR and mGluR5 suppression. Nat Neurosci. 2015;18:435–43.

    CAS  PubMed  Google Scholar 

  60. Maggio JC, Maggio JH, Whitney G. Experience-based vocalization of male-mice to female chemosignals. Physiol Behav. 1983;31:269–72.

    CAS  PubMed  Google Scholar 

  61. Devor M, Murphy MR. The effect of peripheral olfactory blockade on the social behavior of the male golden hamster. Behav Biol. 1973;9:31–42.

    CAS  PubMed  Google Scholar 

  62. Dong Z, Bai Y, Wu X, Li H, Gong B, Howland JG, et al. Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze. Neuropharmacology. 2013;64:65–73.

    CAS  PubMed  Google Scholar 

  63. Nicholls RE, Alarcon JM, Malleret G, Carroll RC, Grody M, Vronskaya S, et al. Transgenic mice lacking NMDAR-dependent LTD exhibit deficits in behavioral flexibility. Neuron. 2008;58:104–17.

    CAS  PubMed  Google Scholar 

  64. Baudouin SJ, Gaudias J, Gerharz S, Hatstatt L, Zhou KK, Punnakkal P, et al. Shared synaptic pathophysiology in syndromic and nonsyndromic rodent models of autism. Science. 2012;338:128–32.

    CAS  PubMed  Google Scholar 

  65. Zoghbi HY, Bear MF. Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb Perspect Biol. 2012;4:a009886.

  66. Lee E, Lee J, Kim E. Excitation/inhibition imbalance in animal models of autism spectrum disorders. Biol Psychiat. 2017;81:838–47.

    PubMed  Google Scholar 

  67. Hines RM, Wu LJ, Hines DJ, Steenland H, Mansour S, Dahlhaus R, et al. Synaptic imbalance, stereotypies, and impaired social interactions in mice with altered neuroligin 2 expression. J Neurosci. 2008;28:6055–67.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Wang X, McCoy PA, Rodriguiz RM, Pan Y, Je HS, Roberts AC, et al. Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3. Hum Mol Genet. 2011;20:3093–108.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Hung AY, Futai K, Sala C, Valtschanoff JG, Ryu J, Woodworth MA, et al. Smaller dendritic spines, weaker synaptic transmission, but enhanced spatial learning in mice lacking Shank1. J Neurosci. 2008;28:1697–708.

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Matz J, Gilyan A, Kolar A, McCarvill T, Krueger SR. Rapid structural alterations of the active zone lead to sustained changes in neurotransmitter release. Proc Natl Acad Sci USA. 2010;107:8836–41.

    CAS  PubMed  Google Scholar 

  71. Hallermann S, Fejtova A, Schmidt H, Weyhersmuller A, Silver RA, Gundelfinger ED, et al. Bassoon speeds vesicle reloading at a central excitatory synapse. Neuron. 2010;68:710–23.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Yin X, Takei Y, Kido MA, Hirokawa N. Molecular motor KIF17 is fundamental for memory and learning via differential support of synaptic NR2A/2B levels. Neuron. 2011;70:310–25.

    CAS  PubMed  Google Scholar 

  73. Alsabban AH, Morikawa M, Tanaka Y, Takei Y, Hirokawa N. Kinesin Kif3b mutation reduces NMDAR subunit NR2A trafficking and causes schizophrenia-like phenotypes in mice. EMBO J. 2020;39:e101090.

    CAS  PubMed  Google Scholar 

  74. Morikawa M, Tanaka Y, Cho HS, Yoshihara M, Hirokawa N. The molecular motor KIF21B mediates synaptic plasticity and fear extinction by terminating Rac1 activation. Cell Rep. 2018;23:3864–77.

    CAS  PubMed  Google Scholar 

  75. Belger A, Carpenter KL, Yucel GH, Cleary KM, Donkers FC. The neural circuitry of autism. Neurotox Res. 2011;20:201–14.

    PubMed  PubMed Central  Google Scholar 

  76. Amodio DM, Frith CD. Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci. 2006;7:268–77.

    CAS  PubMed  Google Scholar 

  77. Felix-Ortiz AC, Tye KM. Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior. J Neurosci. 2014;34:586–95.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Kogan JH, Frankland PW, Silva AJ. Long-term memory underlying hippocampus- dependent social recognition in mice. Hippocampus. 2000;10:47–56.

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank members of the Sheng lab for technical assistance and constructive discussion, Zezhi Li for assistance in analyzing human sequence data, Eckart Gundelfinger for EGFP-Bassoon, Richard Youle for pCMV-DsRed-Mito, Jun Xia for YFP-PICK1, the NIH/NICHD rodent behavioral core facility and Daniel Tadese Abebe for assistance in animal behavioral tests, the NINDS Electron Microscopy Facility and Susan Cheng for assistance in TEM analysis, and Kelly Chamberlain and Joseph Roney for critical reading/editing.

Funding

This work was supported by the Intramural Research Program of NINDS, NIH ZIA NS003029, and ZIA NS002946 (Z-H.S).

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  1. Synaptic Function Section, The Porter Neuroscience Research Center, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Room 2B-215, 35 Convent Drive, Bethesda, MD, 20892-3706, USA

    Gui-Jing Xiong, Xiu-Tang Cheng, Tao Sun, Yuxiang Xie, Ning Huang, Sunan Li, Mei-Yao Lin & Zu-Hang Sheng

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Contributions

G-J.X and Z-H.S designed the project, G-J.X performed synaptic physiological and behavioral studies and analyzed data, X-T.C, TS, YX, SL, NH, and M-Y.L performed biochemical and cell biological experiments, Z-H.S is the senior author who conceived and directed the project; G-J.X and Z-H.S wrote the manuscript.

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Correspondence to Zu-Hang Sheng.

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Xiong, GJ., Cheng, XT., Sun, T. et al. Defects in syntabulin-mediated synaptic cargo transport associate with autism-like synaptic dysfunction and social behavioral traits. Mol Psychiatry 26, 1472–1490 (2021). https://doi.org/10.1038/s41380-020-0713-9

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