臺灣博碩士論文加值系統

思覺失調症是一種伴隨許多嚴重症狀的神經發育疾病，包括視覺迴路的異常；已知Dysbindin為一重要的思覺失調症易感蛋白，但Dysbindin在視覺迴路的發育中所扮演的角色迄今未明。視覺迴路的發育需要視網膜波 (一種模式化的神經自發性放電現象)；以出生後一週的大鼠視網膜為例，星狀無軸突細胞 (SACs)會自發性產生神經衝動，分泌乙醯膽鹼和GABA並至周圍其他SACs和視網膜神經節細胞 (RGCs)，產生第二期視網膜波。研究已經證實，第二期視網膜波在調控視覺迴路的發育當中扮演著重要的角色。然而，目前仍為未知Dysbindin是否參與在調控第二期視網膜波的機制當中。實驗室先前利用不具細胞專一性的分子擾動技術，發現大鼠視網膜中Dysbindin的表現量會調控第二期視網膜波的時空性質，但作用機制則需更深入的研究；因此，本研究深入探討Dysbindin調控第二期視網膜波的細胞與分子機制。首先，我們發現在大鼠視網膜中，Dysbindin的蛋白表現量在第二期視網膜波時期較高。利用免疫螢光染色，發現Dysbindin主要分布於視網膜的內部叢狀層和神經節細胞層，並表現於SACs和RGCs中。我們進一步利用SAC和RGC的專一引子，在SACs和RGCs中分別過量或消耗表現Dysbindin，再用鈣離子實像錄影並分析第二期視網膜波的時空性質。結果發現，Dysbindin在SACs中的表現量並不會影響第二期視網膜波的時空性質；然而，在RGCs中，過量表現Dysbindin降低了第二期視網膜波的頻率、波的大小、和同步性；而消耗Dysbindin的表現量則僅降低第二期視網膜波的大小。為了深入研究Dysbindin調控第二期視網膜波的分子機制，我們進一步分析視網膜中與胞吐作用相關的蛋白表現量是否會受到分子擾動Dysbindin的影響。結果發現在視網膜的層級中無法看出Dysbindin和其他蛋白表現量的變化；但在單一細胞的層級中，我們發現了Dysbindin在SACs或RGCs中過量或消耗表現的證據。此外，在RGCs中，隨著Dysbindin的表現量增加或減少，SNAP-25的表現量會同步變化。另外，我們也發現在RGCs中過量表現Dysbindin，會降低SACs中Dysbindin和 SNAP-25的表現量，表示RGCs中的Dysbindin可能存在著逆向調控SACs的作用機制。最後，我們利用Mirror Tree蛋白交互作用預測法輔以免疫共沉澱實驗，發現在發育的大鼠視網膜中，Dysbindin會和SNAP-25有交互作用；表示Dysbindin可能是透過與SNAP-25的交互作用，來調控第二期視網膜波。綜合以上結果，我們發現Dysbindin主要透過RGCs調控第二期視網膜波，並且會調控視網膜細胞中SNAP-25的表現量。因此，本研究發現Dysbindin參與神經迴路發育的作用機制，為未來研究思覺失調症的致病分子機制，提供一個新的方向。

Schizophrenia (SCZ) is a neurodevelopmental disease with several symptoms including visual circuit defects. One of the major SCZ susceptibility proteins is Dystrobrevin-binding protein (Dysbindin), but how Dysbindin involves in the development of visual circuits remains unknown. During the first postnatal week, developing rat retinas display the patterned spontaneous activity, termed stage II retinal waves, which are initiated by starburst amacrine cells (SACs) spontaneously releasing acetylcholine (ACh) and -amino butyric acid (GABA) to neighboring SACs and retinal ganglion cells (RGCs), further propagating to central brain. Stage II retinal waves play a critical role in establishing the precise visual circuits. However, the role of Dysbindin in regulating stage II retinal waves remains unclear. By using non-cell-type-specific molecular perturbation, we found that changing the Dysbindin levels in the developing rat retina regulates the spatiotemporal properties of stage II retinal waves. However, the underlying mechanisms are not clear. Here, we aimed to identify the cellular and molecular mechanisms for Dysbindin to regulate stage II retinal waves. First, we found that the expression levels of Dysbindin in rat retinas were relatively high during the stage II wave period compared to adulthood. With immunofluorescence, we found that Dysbindin was localized to the inner plexiform layer (IPL) and ganglion cell layer (GCL), particularly in SACs and RGCs. To identify whether Dysbindin may regulate stage II retinal waves in SACs or RGCs, we combined the cell-type-specific molecular perturbation (the Brn3b promoter for RGCs and the mGluR2 promoter for SACs, respectively) and live Ca2+ imaging to analyze the wave spatiotemporal properties. We showed that overexpressing Dysbindin in RGCs, but not in SACs, dramatically down-regulates the wave spatiotemporal properties, suggesting that Dysbindin regulates stage II retinal waves via RGCs. Furthermore, using immunofluorescence on dissociated cells, we found that the protein levels of SNAP-25 were proportionally changed with the Dysbindin levels in RGCs. Moreover, overexpressing Dysbindin in RGCs decreased the levels of Dysbindin and SNAP-25 in SACs, suggesting a retrograde signal may counter balance the presynaptic levels of Dysbindin and SNAP-25 through the RGC-SAC synapses. Finally, using the Mirror Tree prediction and immunoprecipitation, we found that Dysbindin may interact with SNAP-25, previously shown to regulate the properties of stage II retinal waves, suggesting that Dysbindin may regulate stage II retinal waves via modulating the SNAP-25 level and/or via interacting with SNAP-25. Therefore, our results revealed a role of Dysbindin in regulating retinal waves, providing a new direction for studying visual circuit defects in SCZ.

國立臺灣大學碩士學位論文口試委員會審定書 i
Acknowledgments ii
中文摘要 iii
Abstract v
Abbreviations vii
Chapter I: Introduction 1
1.1 Neurodevelopment 1
1.2 Patterned spontaneous activity 2
1.3 The retinal structure and retinal waves 3
1.4 Stage II retinal waves 4
1.5 The link between neural circuit refinement and neurodevelopmental diseases 5
1.6 Schizophrenia 6
1.7 Schizophrenia and the impaired visual system 7
1.8 Dysbindin 8
1.9 Previous work 10
1.10 Objectives in this study 12
Chapter II: Materials and Methods 15
2.1 Animals 15
2.2 Western blot 15
2.3 Transcardiac perfusion and cryosection of eyeballs 16
2.4 Dissociation of retinal neurons 17
2.5 Immunofluorescence staining 18
2.6 Plasmid 20
2.7 Primary culture of retinal explants 20
2.8 Ex vivo electroporation 21
2.9 Live Ca2+ imaging 21
2.10 Prediction of protein-protein interaction by the Mirror Tree software 24
2.11 Co-immunoprecipitation 25
2.12 Statistics 27
Chapter III: Results 28
3.1 Dysbindin was highly expressed in rat retinas during the period of stage II retinal waves. 28
3.2 Dysbindin was localized to the IPL and GCL of rat retinas. 29
3.3 Dysbindin was expressed in the developing SACs and RGCs. 30
3.4 The temporal properties of spontaneous Ca2+ transients remained similar by overexpressing or depleting Dysbindin in SACs. 31
3.5 Overexpressing Dysbindin in RGCs increased the interval and decreased the frequency of spontaneous Ca2+ transients. 32
3.6 Overexpressing or depleting Dysbindin in RGCs decreased the duration and intensity of spontaneous Ca2+ transients. 32
3.7 The spike time tiling coefficient (STTC) and correlation activity of spontaneous Ca2+ transients remained similar by overexpressing or depleting Dysbindin in SACs. 33
3.8 Dysbindin overexpressing in RGCs decreased the STTC and correlation activity of spontaneous Ca2+ transients. 34
3.9 The ex vivo transfection did not change the expression levels of exocytotic proteins in the whole retinas. 35
3.10 The mGluR2-drived constructs successfully overexpressed and depleted the Dysbindin level in SACs. 36
3.11 The Brn3b-drived constructs successfully overexpressed and depleted the Dysbindin level in RGCs. 36
3.12 The level of SNAP-25 was changed with the altering level of Dysbindin in RGCs. 37
3.13 Overexpressing Dysbindin in RGCs decreased the level of Dysbindin and SNAP-25 in SACs. 38
3.14 Dysbindin interacted with SNAP-25 in the developing rat retina. 39
Chapter IV: Discussion 42
4.1 Dysbindin regulates the spatiotemporal properties of stage II retinal waves via RGCs. 44
4.2 The correlation between Dysbindin-regulated-stage II retinal waves and SCZ. 46
4.3 The level of Dysbindin modulates the level of SNAP-25. 49
4.4 The interaction between Dysbindin and GluA2. 51
Chapter V: Conclusion 54
Chapter VI: References 55
Figure 1. The mature rodent retinas. 63
Figure 2. The retinal waves. 65
Figure 3. The visual map in mature rodent. 67
Figure 4. Dysbindin was highly expressed in the developing rat retina during stage II retinal waves period. 69
Figure 5. Dysbindin was localized to IPL and GCL in the developing rat retina. 71
Figure 6. Dysbindin was localized to RGCs in the developing rat retina. 73
Figure 7. Dysbindin was expressed in RGCs and SACs in the developing rat retina. 75
Figure 8. The interval and frequency of spontaneous Ca2+ transients remained similar after overexpression or depletion of Dysbindin in SACs. 77
Figure 9. The duration and intensity of spontaneous Ca2+ transients remained similar after overexpression or depletion of Dysbindin in SACs. 79
Figure 10. The interval of spontaneous Ca2+ transients was increased and the frequency of spontaneous Ca2+ transients was decreased after overexpression of Dysbindin in RGCs. 81
Figure 11. The duration and intensity of spontaneous Ca2+ transients were decreased after overexpression of Dysbindin in RGCs. 83
Figure 12. The spike time tiling coefficient (STTC) and the correlation activity of spontaneous Ca2+ transients remained similar after overexpression or depletion of Dysbindin in SACs. 85
Figure 13. The STTC and the correlation activity of spontaneous Ca2+ transients were decreased after overexpression of Dysbindin in RGCs. 87
Figure 14. Expression of retinal exocytotic proteins remained similar after overexpression or depletion of Dysbindin in SACs or RGCs. 89
Figure 15. Evidence of overexpressing or depleting Dysbindin in SACs. 91
Figure 16. Evidence of overexpressing or depleting Dysbindin in RGCs. 93
Figure 17. The immunoreactivity level of SNAP-25 was increased after overexpressing Dysbindin in RGCs and was decreased after depleting Dysbindin in RGCs. 95
Figure 18. The immunoreactivity level of Dysbindin and SNAP-25 was decreased in SACs after overexpressing Dysbindin in RGCs. 97
Figure 19. Dysbindin interacted with SNAP-25, but not Synaptobrevin 2 in the developing rat retina. 99
Figure 20. The summary of the results. 101
Appendix 102
Appendix 1. Co-immunoprecipitation of Dysbindin with GluA2 or CSP in the P2 intact retinas. 102
Appendix 2. The Abstract and Poster for the Society of Neuroscience (SfN) 2019 104
Appendix 3. The Abstract and Poster for the Graduate Competition in the Institute of Molecular and Cellular Biology (IMCB) 2020 107

Agliardi, C., F. R. Guerini, M. Zanzottera, G. Riboldazzi, R. Zangaglia, A. Sturchio, C. Casali, C. Di Lorenzo, B. Minafra, R. Nemni, and M. Clerici. 2019. 'SNAP25 Gene Polymorphisms Protect Against Parkinson's Disease and Modulate Disease Severity in Patients', Mol Neurobiol, 56: 4455-63.
Al-Shammari, Abeer R., Sanjeev K. Bhardwaj, Ksenia Musaelyan, Lalit K. Srivastava, and Francis G. Szele. 2018. 'Schizophrenia-related dysbindin-1 gene is required for innate immune response and homeostasis in the developing subventricular zone', NPJ schizophrenia, 4: 15-15.
Albert, Frank W., Sebastian Treusch, Arthur H. Shockley, Joshua S. Bloom, and Leonid Kruglyak. 2014. 'Genetics of single-cell protein abundance variation in large yeast populations', Nature, 506: 494-97.
Balu, D. T. 2016. 'The NMDA Receptor and Schizophrenia: From Pathophysiology to Treatment', Adv Pharmacol, 76: 351-82.
Bear, Mark F., Barry W. Connors, and Michael A. Paradiso. 2007. Neuroscience: Exploring the brain, 3rd ed (Lippincott Williams & Wilkins Publishers: Philadelphia, PA, US).
Blankenship, Aaron G., and Marla B. Feller. 2010. 'Mechanisms underlying spontaneous patterned activity in developing neural circuits', Nature reviews. Neuroscience, 11: 18-29.
Brown, A. S. 2006. 'Prenatal infection as a risk factor for schizophrenia', Schizophr Bull, 32: 200-2.
Brzustowicz, L. M., K. A. Hodgkinson, E. W. Chow, W. G. Honer, and A. S. Bassett. 2000. 'Location of a major susceptibility locus for familial schizophrenia on chromosome 1q21-q22', Science (New York, N.Y.), 288: 678-82.
Chang, E. H., K. Fernando, L. W. E. Yeung, K. Barbari, T. S. Chandon, and A. K. Malhotra. 2018. 'Single point mutation on the gene encoding dysbindin results in recognition deficits', Genes Brain Behav, 17: e12449.
Cheah, S. Y., B. R. Lawford, R. M. Young, C. P. Morris, and J. Voisey. 2015. 'Dysbindin (DTNBP1) variants are associated with hallucinations in schizophrenia', European Psychiatry, 30: 486-91.
Chiang, Ning, Yu-Tien Hsiao, Hui-Ju Yang, Yu-Chun Lin, Juu-Chin Lu, and Chih-Tien Wang. 2014. 'Phosphomimetic Mutation of Cysteine String Protein-α Increases the Rate of Regulated Exocytosis by Modulating Fusion Pore Dynamics in PC12 Cells', PLoS One, 9: e99180.
Demas, Jay, Stephen J. Eglen, and Rachel O. L. Wong. 2003. 'Developmental loss of synchronous spontaneous activity in the mouse retina is independent of visual experience', The Journal of neuroscience : the official journal of the Society for Neuroscience, 23: 2851-60.
Dickman, D. K., and G. W. Davis. 2009. 'The schizophrenia susceptibility gene dysbindin controls synaptic homeostasis', Science, 326: 1127-30.
Dickman, Dion K., Amy Tong, and Graeme W. Davis. 2012. 'Snapin is critical for presynaptic homeostatic plasticity', The Journal of neuroscience : the official journal of the Society for Neuroscience, 32: 8716-24.
Elward, K., and P. Gasque. 2003. '"Eat me" and "don't eat me" signals govern the innate immune response and tissue repair in the CNS: emphasis on the critical role of the complement system', Mol Immunol, 40: 85-94.
Estes, M. L., and A. K. McAllister. 2015. 'Immune mediators in the brain and peripheral tissues in autism spectrum disorder', Nat Rev Neurosci, 16: 469-86.
Failor, Samuel, Barbara Chapman, and Hwai-Jong Cheng. 2015. 'Retinal waves regulate afferent terminal targeting in the early visual pathway', Proceedings of the National Academy of Sciences, 112: E2957.
Fatemi, S. H., J. Earle, R. Kanodia, D. Kist, E. S. Emamian, P. H. Patterson, L. Shi, and R. Sidwell. 2002. 'Prenatal viral infection leads to pyramidal cell atrophy and macrocephaly in adulthood: implications for genesis of autism and schizophrenia', Cell Mol Neurobiol, 22: 25-33.
Feller, Marla B. 1999. 'Spontaneous Correlated Activity in Developing Neural Circuits', Neuron, 22: 653-56.
Feller, Marla B., David P. Wellis, David Stellwagen, Frank S. Werblin, and Carla J. Shatz. 1996. 'Requirement for Cholinergic Synaptic Transmission in the Propagation of Spontaneous Retinal Waves', Science, 272: 1182.
Firl, Alana, Georgeann S. Sack, Zachary L. Newman, Hiroaki Tani, and Marla B. Feller. 2013. 'Extrasynaptic glutamate and inhibitory neurotransmission modulate ganglion cell participation during glutamatergic retinal waves', Journal of neurophysiology, 109: 1969-78.
Folsom, David P., William Hawthorne, Laurie Lindamer, Todd Gilmer, Anne Bailey, Shahrokh Golshan, Piedad Garcia, Jürgen Unützer, Richard Hough, and Dilip V. Jeste. 2005. 'Prevalence and Risk Factors for Homelessness and Utilization of Mental Health Services Among 10,340 Patients With Serious Mental Illness in a Large Public Mental Health System', American Journal of Psychiatry, 162: 370-76.
Foss, E. J., D. Radulovic, S. A. Shaffer, D. M. Ruderfer, A. Bedalov, D. R. Goodlett, and L. Kruglyak. 2007. 'Genetic basis of proteome variation in yeast', Nat Genet, 39: 1369-75.
Ghosh, W., S. Mallick, and S. K. DasGupta. 2009. 'Origin of the Sox multienzyme complex system in ancient thermophilic bacteria and coevolution of its constituent proteins', Res Microbiol, 160: 409-20.
Gokhale, Avanti, Ariana P. Mullin, Stephanie A. Zlatic, Charles A. th Easley, Megan E. Merritt, Nisha Raj, Jennifer Larimore, David E. Gordon, Andrew A. Peden, Subhabrata Sanyal, and Victor Faundez. 2015. 'The N-ethylmaleimide-sensitive factor and dysbindin interact to modulate synaptic plasticity', The Journal of neuroscience : the official journal of the Society for Neuroscience, 35: 7643-53.
'Hebb, D. O. Organization of behavior. New York: Wiley, 1949, pp. 335, $4.00'. 1950. Journal of Clinical Psychology, 6: 307-07.
Holzman, Philip S., Leonard R. Proctor, and Dominic W. Hughes. 1973. 'Eye-Tracking Patterns in Schizophrenia', Science, 181: 179.
Hsiao, Yu-Tien, Wen-Chi Shu, Pin-Chun Chen, Hui-Ju Yang, Hsin-Yo Chen, Sheng-Ping Hsu, Yi-Ting Huang, Cheng-Chang Yang, Yen-Ju Chen, Ni-Yen Yu, Shih-Yuan Liou, Ning Chiang, Chien-Ting Huang, Tzu-Lin Cheng, Lam-Yan Cheung, Yu-Chun Lin, Juu-Chin Lu, and Chih-Tien Wang. 2019. 'Presynaptic SNAP-25 regulates retinal waves and retinogeniculate projection via phosphorylation', Proc Natl Acad Sci U S A, 116: 3262-67.
Huang, Cathy C. Y., Kevin J. Muszynski, Vadim Y. Bolshakov, and Darrick T. Balu. 2019. 'Deletion of Dtnbp1 in mice impairs threat memory consolidation and is associated with enhanced inhibitory drive in the amygdala', Translational psychiatry, 9: 132-32.
Huberman, Andrew D., Marla B. Feller, and Barbara Chapman. 2008. 'Mechanisms underlying development of visual maps and receptive fields', Annual Review of Neuroscience, 31: 479-509.
Insel, Thomas R. 2010. 'Rethinking schizophrenia', Nature, 468: 187-93.
Isaac, John T. R., Michael C. Ashby, and Chris J. McBain. 2007. 'The Role of the GluR2 Subunit in AMPA Receptor Function and Synaptic Plasticity', Neuron, 54: 859-71.
Ito, H., R. Morishita, T. Shinoda, I. Iwamoto, K. Sudo, K. Okamoto, and K. Nagata. 2010. 'Dysbindin-1, WAVE2 and Abi-1 form a complex that regulates dendritic spine formation', Molecular Psychiatry, 15: 976-86.
Ito, Hidenori, Rika Morishita, and Koh-ichi Nagata. 2016. 'Schizophrenia susceptibility gene product dysbindin-1 regulates the homeostasis of cyclin D1', Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 1862: 1383-91.
Jeong, Y. H., J. H. Choi, D. Lee, S. Kim, and K. T. Kim. 2018. 'Vaccinia-related kinase 2 modulates role of dysbindin by regulating protein stability', J Neurochem, 147: 609-25.
Kang, Seung-Gul, Ik-Seung Chee, Hun Soo Chang, Kyoung-Sae Na, Kwanghun Lee, and Jonghun Lee. 2017. 'Polymorphism of the SNAP25 gene is associated with symptom improvement in schizophrenic patients treated with amisulpride', Neuroscience Letters, 661: 46-50.
Kety, Seymour S., David Rosenthal, Paul H. Wender, and Fini Schulsinger. 1971. 'Mental Illness in the Biological and Adoptive Families of Adopted Schizophrenics', American Journal of Psychiatry, 128: 302-06.
Kogata, Tomohiro, and Tetsuya Iidaka. 2018. 'A review of impaired visual processing and the daily visual world in patients with schizophrenia', Nagoya journal of medical science, 80: 317-28.
Larimore, Jennifer, Pearl V. Ryder, Kun-Yong Kim, L. Alex Ambrose, Christopher Chapleau, Gaston Calfa, Christina Gross, Gary J. Bassell, Lucas Pozzo-Miller, Yoland Smith, Konrad Talbot, In-Hyun Park, and Victor Faundez. 2013. 'MeCP2 regulates the synaptic expression of a Dysbindin-BLOC-1 network component in mouse brain and human induced pluripotent stem cell-derived neurons', PLoS One, 8: e65069-e69.
Larimore, Jennifer, Stephanie A. Zlatic, Avanti Gokhale, Karine Tornieri, Kaela S. Singleton, Ariana P. Mullin, Junxia Tang, Konrad Talbot, and Victor Faundez. 2014. 'Mutations in the BLOC-1 subunits dysbindin and muted generate divergent and dosage-dependent phenotypes', J Biol Chem, 289: 14291-300.
Lee, Seol-Ae, Seong-Mo Kim, Bo Kyoung Suh, Hwa-Young Sun, Young-Un Park, Ji-Ho Hong, Cana Park, Minh Dang Nguyen, Koh-Ichi Nagata, Joo-Yeon Yoo, and Sang Ki Park. 2015. 'Disrupted-in-schizophrenia 1 (DISC1) regulates dysbindin function by enhancing its stability', J Biol Chem, 290: 7087-96.
Lehrman, Emily K., Daniel K. Wilton, Elizabeth Y. Litvina, Christina A. Welsh, Stephen T. Chang, Arnaud Frouin, Alec J. Walker, Molly D. Heller, Hisashi Umemori, Chinfei Chen, and Beth Stevens. 2018. 'CD47 Protects Synapses from Excess Microglia-Mediated Pruning during Development', Neuron, 100: 120-34.e6.
Ma, X., E. Fei, C. Fu, H. Ren, and G. Wang. 2011. 'Dysbindin-1, a schizophrenia-related protein, facilitates neurite outgrowth by promoting the transcriptional activity of p53', Mol Psychiatry, 16: 1105-16.
Mahanty, Nishith K., and Pankaj Sah. 1998. 'Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala', Nature, 394: 683-87.
Marwaha, Steven, Sonia Johnson, Paul Bebbington, Mai Stafford, Matthias C. Angermeyer, Traolach Brugha, Jean-Michel Azorin, Reinhold Kilian, Karina Hansen, and Mondher Toumi. 2007. 'Rates and correlates of employment in people with schizophrenia in the UK, France and Germany', British Journal of Psychiatry, 191: 30-37.
Matteucci, Andrea, Lucia Gaddini, Gianfranco Macchia, Monica Varano, Tamara C. Petrucci, Pompeo Macioce, Fiorella Malchiodi-Albedi, and Marina Ceccarini. 2013. 'Developmental expression of dysbindin in Muller cells of rat retina', Experimental Eye Research, 116: 1-8.
Menke, A., and H. Jockusch. 1991. 'Decreased osmotic stability of dystrophin-less muscle cells from the mdx mouse', Nature, 349: 69-71.
Monyer, H., P. H. Seeburg, and W. Wisden. 1991. 'Glutamate-operated channels: Developmentally early and mature forms arise by alternative splicing', Neuron, 6: 799-810.
Owen, Michael J., Nigel M. Williams, and Michael C. O'Donovan. 2004. 'Dysbindin-1 and schizophrenia: from genetics to neuropathology', The Journal of clinical investigation, 113: 1255-57.
Paolicelli, R. C., G. Bolasco, F. Pagani, L. Maggi, M. Scianni, P. Panzanelli, M. Giustetto, T. A. Ferreira, E. Guiducci, L. Dumas, D. Ragozzino, and C. T. Gross. 2011. 'Synaptic pruning by microglia is necessary for normal brain development', Science, 333: 1456-8.
Peinado, Alejandro, and Charles K. Abrams. 2015. 'Patterns of Spontaneous Local Network Activity in Developing Cerebral Cortex: Relationship to Adult Cognitive Function', PLoS One, 10: e0131259-e59.
Pulver, Ann E. 2000. 'Search for schizophrenia susceptibility genes', Biological Psychiatry, 47: 221-30.
Ramos-Miguel, A., K. Gicas, J. Alamri, C. L. Beasley, A. J. Dwork, J. J. Mann, G. Rosoklija, F. Cai, W. Song, A. M. Barr, and W. G. Honer. 2019. 'Reduced SNAP25 Protein Fragmentation Contributes to SNARE Complex Dysregulation in Schizophrenia Postmortem Brain', Neuroscience, 420: 112-28.
Robinson, Delbert G., Margaret G. Woerner, Marjorie McMeniman, Alan Mendelowitz, and Robert M. Bilder. 2004. 'Symptomatic and Functional Recovery From a First Episode of Schizophrenia or Schizoaffective Disorder', American Journal of Psychiatry, 161: 473-79.
Söllner, T., M. K. Bennett, S. W. Whiteheart, R. H. Scheller, and J. E. Rothman. 1993. 'A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion', Cell, 75: 409-18.
Sharma, M., J. Burré, and T. C. Südhof. 2011. 'CSPα promotes SNARE-complex assembly by chaperoning SNAP-25 during synaptic activity', Nat Cell Biol, 13: 30-9.
Shatz, C. J., and M. P. Stryker. 1988. 'Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents', Science, 242: 87-9.
Shirafuji, Toshihiko, Takehiko Ueyama, Naoko Adachi, Ken-Ichi Yoshino, Yusuke Sotomaru, Junsuke Uwada, Azumi Kaneoka, Taro Ueda, Shigeru Tanaka, Izumi Hide, Naoaki Saito, and Norio Sakai. 2018. 'The Role of Cysteine String Protein α Phosphorylation at Serine 10 and 34 by Protein Kinase Cγ for Presynaptic Maintenance', The Journal of neuroscience : the official journal of the Society for Neuroscience, 38: 278-90.
Shuwairi, Sarah M., Alice Cronin-Golomb, Robert W. McCarley, and Brian F. O'Donnell. 2002. 'Color discrimination in schizophrenia', Schizophrenia Research, 55: 197-204.
Silverstein, Steven M., Ilona Kovács, Rodney Corry, and Carolyn Valone. 2000. 'Perceptual organization, the disorganization syndrome, and context processing in chronic schizophrenia', Schizophrenia Research, 43: 11-20.
Smith, S. E., J. Li, K. Garbett, K. Mirnics, and P. H. Patterson. 2007. 'Maternal immune activation alters fetal brain development through interleukin-6', J Neurosci, 27: 10695-702.
Stuve, T. A., L. Friedman, J. A. Jesberger, G. C. Gilmore, M. E. Strauss, and H. Y. Meltzer. 1997. 'The relationship between smooth pursuit performance, motion perception and sustained visual attention in patients with schizophrenia and normal controls', Psychological Medicine, 27: 143-52.
Susser, E., R. Neugebauer, H. W. Hoek, A. S. Brown, S. Lin, D. Labovitz, and J. M. Gorman. 1996. 'Schizophrenia after prenatal famine. Further evidence', Arch Gen Psychiatry, 53: 25-31.
Syed, Mohsin Md, Seunghoon Lee, Jijian Zheng, and Z. Jimmy Zhou. 2004. 'Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina', The Journal of physiology, 560: 533-49.
Syken, Josh, Tadzia GrandPre, Patrick O. Kanold, and Carla J. Shatz. 2006. 'PirB Restricts Ocular-Dominance Plasticity in Visual Cortex', Science, 313: 1795.
Talbot, Konrad, Wess L. Eidem, Caroline L. Tinsley, Matthew A. Benson, Edward W. Thompson, Rachel J. Smith, Chang-Gyu Hahn, Steven J. Siegel, John Q. Trojanowski, Raquel E. Gur, Derek J. Blake, and Steven E. Arnold. 2004. 'Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia', The Journal of clinical investigation, 113: 1353-63.
Tang, Junxia, Robert P. LeGros, Natalia Louneva, Lilly Yeh, Julia W. Cohen, Chang-Gyu Hahn, Derek J. Blake, Steven E. Arnold, and Konrad Talbot. 2009. 'Dysbindin-1 in dorsolateral prefrontal cortex of schizophrenia cases is reduced in an isoform-specific manner unrelated to dysbindin-1 mRNA expression', Hum Mol Genet, 18: 3851-63.
Wang, Haitao, Mohd Farhan, Jiangping Xu, Philip Lazarovici, and Wenhua Zheng. 2017. 'The involvement of DARPP-32 in the pathophysiology of schizophrenia', Oncotarget, 8: 53791-803.
Wang, X., Y. Liu, M. Jia, X. Sun, N. Wang, Y. Li, and C. Cui. 2018. 'Phosphorylated SNAP25 in the CA1 regulates morphine-associated contextual memory retrieval via increasing GluN2B-NMDAR surface localization', Addict Biol, 23: 1067-78.
Washbourne, P., P. M. Thompson, M. Carta, E. T. Costa, J. R. Mathews, G. Lopez-Benditó, Z. Molnár, M. W. Becher, C. F. Valenzuela, L. D. Partridge, and M. C. Wilson. 2002. 'Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis', Nat Neurosci, 5: 19-26.
Weickert, Cynthia Shannon, Richard E. Straub, Benjamin W. McClintock, Mitsuyuki Matsumoto, Ryota Hashimoto, Thomas M. Hyde, Mary M. Herman, Daniel R. Weinberger, and Joel E. Kleinman. 2004. 'Human Dysbindin (DTNBP1) Gene Expression inNormal Brain and in Schizophrenic Prefrontal Cortex and Midbrain', Archives of General Psychiatry, 61: 544-55.
Weinberger, Daniel R. 1987. 'Implications of Normal Brain Development for the Pathogenesis of Schizophrenia', Archives of General Psychiatry, 44: 660-69.
Wong, Rachel O. L. 1999. 'RETINAL WAVES AND VISUAL SYSTEM DEVELOPMENT', Annual Review of Neuroscience, 22: 29-47.
Wong, W. T., J. R. Sanes, and R. O. Wong. 1998. 'Developmentally regulated spontaneous activity in the embryonic chick retina', The Journal of neuroscience : the official journal of the Society for Neuroscience, 18: 8839-52.
Zheng, W., H. Wang, Z. Zeng, J. Lin, P. J. Little, L. K. Srivastava, and R. Quirion. 2012. 'The possible role of the Akt signaling pathway in schizophrenia', Brain Res, 1470: 145-58.