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SNX17 Mediates Dendritic Spine Maturation via p140Cap

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Abstract

Sorting nexin17 (SNX17) is a member of the sorting nexin family, which plays a crucial role in endosomal trafficking. Previous research has shown that SNX17 is involved in the recycling or degradation of various proteins associated with neurodevelopmental and neurological diseases in cell models. However, the significance of SNX17 in neurological function in the mouse brain has not been thoroughly investigated. In this study, we generated Snx17 knockout mice and observed that the homozygous deletion of Snx17 (Snx17−/−) resulted in lethality. On the other hand, heterozygous mutant mice (Snx17+/−) exhibited anxiety-like behavior with a reduced preference for social novelty. Furthermore, Snx17 haploinsufficiency led to impaired synaptic transmission and reduced maturation of dendritic spines. Through GST pulldown and interactome analysis, we identified the SRC kinase inhibitor, p140Cap, as a potential downstream target of SNX17. We also demonstrated that the interaction between p140Cap and SNX17 is crucial for dendritic spine maturation. Together, this study provides the first in vivo evidence highlighting the important role of SNX17 in maintaining neuronal function, as well as regulating social novelty and anxiety-like behaviors.

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Data Availability

The Snx17+/− mice and the data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Cullen PJ (2008) Endosomal sorting and signalling: an emerging role for sorting nexins. Nat Rev Mol Cell Biol 9(7):574–582. https://doi.org/10.1038/nrm2427

    Article  CAS  PubMed  Google Scholar 

  2. Carlton J, Bujny M, Rutherford A, Cullen P (2005) Sorting nexins–unifying trends and new perspectives. Traffic 6(2):75–82. https://doi.org/10.1111/j.1600-0854.2005.00260.x

    Article  CAS  PubMed  Google Scholar 

  3. Schobel S, Neumann S, Hertweck M, Dislich B, Kuhn PH, Kremmer E, Seed B, Baumeister R et al (2008) A novel sorting nexin modulates endocytic trafficking and alpha-secretase cleavage of the amyloid precursor protein. J Biol Chem 283(21):14257–14268. https://doi.org/10.1074/jbc.M801531200

    Article  CAS  PubMed  Google Scholar 

  4. Lee J, Retamal C, Cuitino L, Caruano-Yzermans A, Shin JE, van Kerkhof P, Marzolo MP, Bu G (2008) Adaptor protein sorting nexin 17 regulates amyloid precursor protein trafficking and processing in the early endosomes. J Biol Chem 283(17):11501–11508. https://doi.org/10.1074/jbc.M800642200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Zhao Y, Wang Y, Yang J, Wang X, Zhao Y, Zhang X, Zhang YW (2012) Sorting nexin 12 interacts with BACE1 and regulates BACE1-mediated APP processing. Mol Neurodegener 7:30. https://doi.org/10.1186/1750-1326-7-30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Zhang H, Huang T, Hong Y, Yang W, Zhang X, Luo H, Xu H, Wang X (2018) The retromer complex and sorting nexins in neurodegenerative diseases. Front Aging Neurosci 10:79. https://doi.org/10.3389/fnagi.2018.00079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Wang X, Zhao Y, Zhang X, Badie H, Zhou Y, Mu Y, Loo LS, Cai L et al (2013) Loss of sorting nexin 27 contributes to excitatory synaptic dysfunction by modulating glutamate receptor recycling in Down’s syndrome. Nat Med 19(4):473–480. https://doi.org/10.1038/nm.3117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Thomas AC, Williams H, Seto-Salvia N, Bacchelli C, Jenkins D, O’Sullivan M, Mengrelis K, Ishida M et al (2014) Mutations in SNX14 cause a distinctive autosomal-recessive cerebellar ataxia and intellectual disability syndrome. Am J Hum Genet 95(5):611–621. https://doi.org/10.1016/j.ajhg.2014.10.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ma L, Semick SA, Chen Q, Li C, Tao R, Price AJ, Shin JH, Jia Y et al (2020) Schizophrenia risk variants influence multiple classes of transcripts of sorting nexin 19 (SNX19). Mol Psychiatry 25(4):831–843. https://doi.org/10.1038/s41380-018-0293-0

    Article  CAS  PubMed  Google Scholar 

  10. Christophersen IE, Rienstra M, Roselli C, Yin X, Geelhoed B, Barnard J, Lin H, Arking DE et al (2017) Large-scale analyses of common and rare variants identify 12 new loci associated with atrial fibrillation. Nat Genet 49(6):946–952. https://doi.org/10.1038/ng.3843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Zhu Z, Zhang F, Hu H, Bakshi A, Robinson MR, Powell JE, Montgomery GW, Goddard ME et al (2016) Integration of summary data from GWAS and eQTL studies predicts complex trait gene targets. Nat Genet 48(5):481–487. https://doi.org/10.1038/ng.3538

    Article  CAS  PubMed  Google Scholar 

  12. Du Y, Zou Y, Yu W, Shi R, Zhang M, Yang W, Duan J, Deng Y et al (2013) Expression pattern of sorting Nexin 25 in temporal lobe epilepsy: a study on patients and pilocarpine-induced rats. Brain Res 1509:79–85. https://doi.org/10.1016/j.brainres.2013.03.005

    Article  CAS  PubMed  Google Scholar 

  13. Vieira N, Rito T, Correia-Neves M, Sousa N (2021) Sorting out sorting nexins functions in the nervous system in health and disease. Mol Neurobiol 58(8):4070–4106. https://doi.org/10.1007/s12035-021-02388-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ghai R, Mobli M, Norwood SJ, Bugarcic A, Teasdale RD, King GF, Collins BM (2011) Phox homology band 4.1/ezrin/radixin/moesin-like proteins function as molecular scaffolds that interact with cargo receptors and Ras GTPases. Proc Natl Acad Sci U S A 108(19):7763–7768. https://doi.org/10.1073/pnas.1017110108

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  15. Zhou C, Wu Z, Du W, Que H, Wang Y, Ouyang Q, Jian F, Yuan W et al (2022) Recycling of autophagosomal components from autolysosomes by the recycler complex. Nat Cell Biol 24(4):497–512. https://doi.org/10.1038/s41556-022-00861-8

    Article  CAS  PubMed  Google Scholar 

  16. Yong X, Zhao L, Hu W, Sun Q, Ham H, Liu Z, Ren J, Zhang Z, Zhou Y, Yang Q, Mo X, Hu J, Billadeau DD, Jia D (2021) SNX27-FERM-SNX1 complex structure rationalizes divergent trafficking pathways by SNX17 and SNX27. Proc Natl Acad Sci U S A 118(36). https://doi.org/10.1073/pnas.2105510118

  17. Cullen PJ, Korswagen HC (2011) Sorting nexins provide diversity for retromer-dependent trafficking events. Nat Cell Biol 14(1):29–37. https://doi.org/10.1038/ncb2374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Chandra M, Collins BM (2019) The Phox Homology (PX) Domain. Adv Exp Med Biol 1111:1–17. https://doi.org/10.1007/5584_2018_185

    Article  CAS  PubMed  Google Scholar 

  19. Czubayko M, Knauth P, Schluter T, Florian V, Bohnensack R (2006) Sorting nexin 17, a non-self-assembling and a PtdIns(3)P high class affinity protein, interacts with the cerebral cavernous malformation related protein KRIT1. Biochem Biophys Res Commun 345(3):1264–1272. https://doi.org/10.1016/j.bbrc.2006.04.129

    Article  CAS  PubMed  Google Scholar 

  20. Stiegler AL, Zhang R, Liu W, Boggon TJ (2014) Structural determinants for binding of sorting nexin 17 (SNX17) to the cytoplasmic adaptor protein Krev interaction trapped 1 (KRIT1). J Biol Chem 289(36):25362–25373. https://doi.org/10.1074/jbc.M114.584011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Seog DH, Han J (2008) Sorting nexin 17 interacts directly with kinesin superfamily KIF1Bbeta protein. Korean J Physiol Pharmacol 12(4):199–204. https://doi.org/10.4196/kjpp.2008.12.4.199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. McNally KE, Faulkner R, Steinberg F, Gallon M, Ghai R, Pim D, Langton P, Pearson N et al (2017) Retriever is a multiprotein complex for retromer-independent endosomal cargo recycling. Nat Cell Biol 19(10):1214–1225. https://doi.org/10.1038/ncb3610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Gallon M, Cullen PJ (2015) Retromer and sorting nexins in endosomal sorting. Biochem Soc Trans 43(1):33–47. https://doi.org/10.1042/BST20140290

    Article  CAS  PubMed  Google Scholar 

  24. Ghai R, Bugarcic A, Liu H, Norwood SJ, Skeldal S, Coulson EJ, Li SS, Teasdale RD et al (2013) Structural basis for endosomal trafficking of diverse transmembrane cargos by PX-FERM proteins. Proc Natl Acad Sci U S A 110(8):E643-652. https://doi.org/10.1073/pnas.1216229110

    Article  PubMed  PubMed Central  Google Scholar 

  25. van Kerkhof P, Lee J, McCormick L, Tetrault E, Lu W, Schoenfish M, Oorschot V, Strous GJ et al (2005) Sorting nexin 17 facilitates LRP recycling in the early endosome. EMBO J 24(16):2851–2861. https://doi.org/10.1038/sj.emboj.7600756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Yin W, Liu D, Liu N, Xu L, Li S, Lin S, Shu X, Pei D (2012) SNX17 regulates Notch pathway and pancreas development through the retromer-dependent recycling of Jag1. Cell Regen 1(1):4. https://doi.org/10.1186/2045-9769-1-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Sotelo P, Farfan P, Benitez ML, Bu G, Marzolo MP (2014) Sorting nexin 17 regulates ApoER2 recycling and reelin signaling. PLoS One 9(4):e93672. https://doi.org/10.1371/journal.pone.0093672

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  28. O’Brien RJ, Wong PC (2011) Amyloid precursor protein processing and Alzheimer’s disease. Annu Rev Neurosci 34:185–204. https://doi.org/10.1146/annurev-neuro-061010-113613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Jing W, Zhang T, Liu J, Huang X, Yu Q, Yu H, Zhang Q, Li H et al (2021) A circuit of COCH neurons encodes social-stress-induced anxiety via MTF1 activation of Cacna1h. Cell Rep 37(13):110177. https://doi.org/10.1016/j.celrep.2021.110177

    Article  CAS  PubMed  Google Scholar 

  30. Li X, Yu H, Zhang B, Li L, Chen W, Yu Q, Huang X, Ke X et al (2022) Molecularly defined and functionally distinct cholinergic subnetworks. Neuron 110(22):3774-3788 e3777. https://doi.org/10.1016/j.neuron.2022.08.025

    Article  CAS  PubMed  Google Scholar 

  31. Liu G, Yu Q, Tan B, Ke X, Zhang C, Li H, Zhang T, Lu Y (2022) Gut dysbiosis impairs hippocampal plasticity and behaviors by remodeling serum metabolome. Gut Microbes 14(1):2104089. https://doi.org/10.1080/19490976.2022.2104089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Gao Q, Tian R, Han H, Slone J, Wang C, Ke X, Zhang T, Li X et al (2022) PINK1-mediated Drp 1(S616) phosphorylation modulates synaptic development and plasticity via promoting mitochondrial fission. Signal Transduct Target Ther 7(1):103. https://doi.org/10.1038/s41392-022-00933-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Yang Y, Chen J, Chen X, Li D, He J, Wang S, Zhao S, Yang X, Deng S, Tong C, Wang D, Guo Z, Li D, Ma C, Liang X, Shi YS, Liu JJ (2021) Endophilin A1 drives acute structural plasticity of dendritic spines in response to Ca2+/calmodulin. J Cell Biol 220(6). https://doi.org/10.1083/jcb.202007172

  34. Zhu B, Jiang L, Huang T, Zhao Y, Liu T, Zhong Y, Li X, Campos A et al (2017) ER-associated degradation regulates Alzheimer’s amyloid pathology and memory function by modulating gamma-secretase activity. Nat Commun 8(1):1472. https://doi.org/10.1038/s41467-017-01799-4

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  35. Stupack J, Xiong XP, Jiang LL, Zhang T, Zhou L, Campos A, Ranscht B, Mobley W et al (2020) Soluble SORLA enhances neurite outgrowth and regeneration through activation of the EGF receptor/ERK signaling axis. J Neurosci 40(31):5908–5921. https://doi.org/10.1523/JNEUROSCI.0723-20.2020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zoghbi HY, Bear MF (2012) Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb Perspect Biol 4(3). https://doi.org/10.1101/cshperspect.a009886

  37. Hering H, Sheng M (2001) Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2(12):880–888. https://doi.org/10.1038/35104061

    Article  CAS  PubMed  Google Scholar 

  38. Repetto D, Camera P, Melani R, Morello N, Russo I, Calcagno E, Tomasoni R, Bianchi F et al (2014) p140Cap regulates memory and synaptic plasticity through Src-mediated and citron-N-mediated actin reorganization. J Neurosci 34(4):1542–1553. https://doi.org/10.1523/JNEUROSCI.2341-13.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Yang Y, Wei M, Xiong Y, Du X, Zhu S, Yang L, Zhang C, Liu JJ (2015) Endophilin A1 regulates dendritic spine morphogenesis and stability through interaction with p140Cap. Cell Res 25(4):496–516. https://doi.org/10.1038/cr.2015.31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Tomasoni R, Repetto D, Morini R, Elia C, Gardoni F, Di Luca M, Turco E, Defilippi P et al (2013) SNAP-25 regulates spine formation through postsynaptic binding to p140Cap. Nat Commun 4:2136. https://doi.org/10.1038/ncomms3136

    Article  ADS  CAS  PubMed  Google Scholar 

  41. Russo I, Gavello D, Menna E, Vandael D, Veglia C, Morello N, Corradini I, Focchi E et al (2019) p140Cap regulates GABAergic synaptogenesis and development of hippocampal inhibitory circuits. Cereb Cortex 29(1):91–105. https://doi.org/10.1093/cercor/bhx306

    Article  PubMed  Google Scholar 

  42. Ji Z, Li H, Yang Z, Huang X, Ke X, Ma S, Lin Z, Lu Y et al (2019) Kibra modulates learning and memory via binding to dendrin. Cell Rep 26(8):2064-2077 e2067. https://doi.org/10.1016/j.celrep.2019.01.097

    Article  CAS  PubMed  Google Scholar 

  43. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5(2):97–107. https://doi.org/10.1038/nrn1327

    Article  CAS  PubMed  Google Scholar 

  44. Glasgow SD, McPhedrain R, Madranges JF, Kennedy TE, Ruthazer ES (2019) Approaches and limitations in the investigation of synaptic transmission and plasticity. Front Synaptic Neurosci 11:20. https://doi.org/10.3389/fnsyn.2019.00020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Wu Y, Zhou Y, Huang J, Ma K, Yuan T, Jiang Y, Ye M, Li J (2021) The role of sorting nexin 17 in cardiac development. Front Cardiovasc Med 8:748891. https://doi.org/10.3389/fcvm.2021.748891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Geng L, Wang S, Zhang F, Xiong K, Huang J, Zhao T, Shi D, Lv F et al (2019) SNX17 (sorting nexin 17) mediates atrial fibrillation onset through endocytic trafficking of the Kv1.5 (potassium voltage-gated channel subfamily A member 5) channel. Circ Arrhythm Electrophysiol 12(4):e007097. https://doi.org/10.1161/CIRCEP.118.007097

    Article  CAS  PubMed  Google Scholar 

  47. Ito H, Atsuzawa K, Sudo K, Di Stefano P, Iwamoto I, Morishita R, Takei S, Semba R et al (2008) Characterization of a multidomain adaptor protein, p140Cap, as part of a pre-synaptic complex. J Neurochem 107(1):61–72. https://doi.org/10.1111/j.1471-4159.2008.05585.x

    Article  CAS  PubMed  Google Scholar 

  48. Chin LS, Nugent RD, Raynor MC, Vavalle JP, Li L (2000) SNIP, a novel SNAP-25-interacting protein implicated in regulated exocytosis. J Biol Chem 275(2):1191–1200. https://doi.org/10.1074/jbc.275.2.1191

    Article  CAS  PubMed  Google Scholar 

  49. Jaworski J, Kapitein LC, Gouveia SM, Dortland BR, Wulf PS, Grigoriev I, Camera P, Spangler SA et al (2009) Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61(1):85–100. https://doi.org/10.1016/j.neuron.2008.11.013

    Article  CAS  PubMed  Google Scholar 

  50. Di Stefano P, Cabodi S, Boeri Erba E, Margaria V, Bergatto E, Giuffrida MG, Silengo L, Tarone G et al (2004) P130Cas-associated protein (p140Cap) as a new tyrosine-phosphorylated protein involved in cell spreading. Mol Biol Cell 15(2):787–800. https://doi.org/10.1091/mbc.e03-09-0689

    Article  PubMed  PubMed Central  Google Scholar 

  51. Valdes JL, Tang J, McDermott MI, Kuo JC, Zimmerman SP, Wincovitch SM, Waterman CM, Milgram SL et al (2011) Sorting nexin 27 protein regulates trafficking of a p21-activated kinase (PAK) interacting exchange factor (beta-Pix)-G protein-coupled receptor kinase interacting protein (GIT) complex via a PDZ domain interaction. J Biol Chem 286(45):39403–39416. https://doi.org/10.1074/jbc.M111.260802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank Dr. Jia-Jia Liu (Chinese Academy of Sciences, Beijing, China) for kindly providing the p140Cap plasmids and antibody. The authors thank the Medical Sub-center of HUST Analytical & Testing Center for data acquisition.

Funding

This work was supported by the National Natural Science Foundation of China (Grants: 31721002 to Y.L.; 81920208014 to Y.L.; 31930051 to Y.L; 8180113 to TZ; 32200795 to HL) and Natural Science Foundation of Hubei Province (2022CFB608) to HL. The authors thank the Medical Sub-center of HUST Analytical & Testing Center for data acquisition.

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  1. Qiuyan Cui and Shiqi Liang made equal contributions to the work.

Authors and Affiliations

  1. The Institute for Brain Research, Collaborative Innovation Center for Brain Science, Huazhong University of Science and Technology, Wuhan, 430030, China

    Qiuyan Cui, Shiqi Liang, Hao Li, Yiqing Guo, Junkai Lv, Pengwei Qin, Youming Lu, Qing Tian & Tongmei Zhang

  2. Department of Pathophysiology, School of Basic Medicine and Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China

    Qiuyan Cui, Shiqi Liang, Hao Li, Yiqing Guo, Junkai Lv, Pengwei Qin, Youming Lu & Qing Tian

  3. Department of Pediatrics, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Chongqing, 400016, China

    Xinyuan Wang

  4. Institute for Brain Science and Disease, Chongqing Medical University, Chongqing, 400016, China

    Huaxi Xu

  5. Degenerative Diseases Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, 92037, USA

    Timothy Y. Huang

  6. Department of Histology and Embryology, School of Basic Medicine and Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China

    Tongmei Zhang

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Contributions

T. Zhang, Q. Tian, Y. Lu, and H. Xu designed the research. Q. Cui, S. Liang, H. Li, and J. Lv performed the experiments; Y. Guo, X. Wang, and P. Qin performed the critical techniques and analyzed the data; T. Zhang, Q Tian, Y. Lu, and T. Huang analyzed the data and wrote the manuscript. All authors contributed to the manuscript editing.

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Correspondence to Qing Tian or Tongmei Zhang.

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Mice were bred and reared under the same conditions following our institutional guidelines and the Animal Care and Use Committee of the Animal Core Facility at Huazhong University of Science and Technology. All efforts were made to minimize the number of animals and their suffering.

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Cui, Q., Liang, S., Li, H. et al. SNX17 Mediates Dendritic Spine Maturation via p140Cap. Mol Neurobiol 61, 1346–1362 (2024). https://doi.org/10.1007/s12035-023-03620-4

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