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Cheng              F, Zhao              J, Wang              Y, Lu              W, Liu              Z, Zhou              Y, et            al. Comprehensive characterization of            protein-protein interactions perturbed by disease mutations. Nat            Genet. 2021; 53:            342\u2013353.","DOI":"10.1038\/s41588-020-00774-y"},{"key":"2","doi-asserted-by":"crossref","unstructured":"2. Greenblatt              JF, Alberts              BM, Krogan              NJ. Discovery            and significance of protein-protein interactions in health and disease.            Cell. 2024; 187:            6501\u20136517.","DOI":"10.1016\/j.cell.2024.10.038"},{"key":"3","doi-asserted-by":"crossref","unstructured":"3. Roux              KJ, Kim              DI, Raida              M, Burke              B. A            promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in            mammalian cells. J Cell Biol. 2012;            196: 801\u2013810.","DOI":"10.1083\/jcb.201112098"},{"key":"4","doi-asserted-by":"crossref","unstructured":"4. Li              P, Li              J, Wang              L, Di              L. Proximity labeling of          interacting proteins: application of BioID as a discovery tool. Proteomics.            2017; 17: pmic.201700002.","DOI":"10.1002\/pmic.201700002"},{"key":"5","doi-asserted-by":"crossref","unstructured":"5. Uezu              A, Kanak              DJ, Bradshaw              TWA,                Soderblom              EJ, Catavero              CM, Burette              AC, et            al. Identification of an elaborate complex mediating            postsynaptic inhibition. Science. 2016;            353: 1123\u20131129.","DOI":"10.1126\/science.aag0821"},{"key":"6","doi-asserted-by":"crossref","unstructured":"6. Spence              EF, Dube              S, Uezu              A, Locke              M, Soderblom              EJ, Soderling              SH. In vivo            proximity proteomics of nascent synapses reveals a novel regulator of            cytoskeleton-mediated synaptic maturation. Nat Commun.            2019; 10: 386.","DOI":"10.1038\/s41467-019-08288-w"},{"key":"7","doi-asserted-by":"crossref","unstructured":"7. Oura              S, Ninomiya              A, Sugihara              F, Matzuk              MM, Ikawa              M.            Proximity-dependent biotin labeling in testicular germ cells identified            TESMIN-associated proteins. Sci Rep. 2022;            12: 22198.","DOI":"10.1038\/s41598-022-26501-7"},{"key":"8","doi-asserted-by":"crossref","unstructured":"8. Feng              W, Liu              C, Spinozzi              S, Wang              L, Evans              SM, Chen              J. Identifying            the cardiac dyad proteome in vivo by a BioID2 knock-in strategy.            Circulation. 2020; 141:            940\u2013942.","DOI":"10.1161\/CIRCULATIONAHA.119.043434"},{"key":"9","doi-asserted-by":"crossref","unstructured":"9. Rudolph              F, Fink              C,                H\u00fcttemeister              J, Kirchner              M, Radke              MH, Lopez                Carballo              J, et            al. Deconstructing sarcomeric structure-function            relations in titin-BioID knock-in mice. Nat Commun.            2020; 11: 3133\u20133138.","DOI":"10.1038\/s41467-020-16929-8"},{"key":"10","doi-asserted-by":"crossref","unstructured":"10. Gerlach              GF, Imseis              ZH, Cooper              SL, Santos              AN, O\u2019Brien              LL. Mapping of            the podocin proximity-dependent proteome reveals novel components of the kidney podocyte            foot process. Front Cell Dev Biol. 2023;            11: 1195037.","DOI":"10.3389\/fcell.2023.1195037"},{"key":"11","doi-asserted-by":"crossref","unstructured":"11. Branon              TC, Bosch              JA, Sanchez              AD, Udeshi              ND, Svinkina              T, Carr              SA, et            al. Efficient proximity labeling in living cells and            organisms with TurboID. Nat Biotechnol.            2018; 36: 880\u2013887.","DOI":"10.1038\/nbt.4201"},{"key":"12","doi-asserted-by":"crossref","unstructured":"12. Kubitz              L, Bitsch              S, Zhao              X, Schmitt              K, Deweid              L, Roehrig              A, et            al. Engineering of ultraID, a compact and            hyperactive enzyme for proximity-dependent biotinylation in living          cells. Commun Biol. 2022;          5: 657.","DOI":"10.1038\/s42003-022-03604-5"},{"key":"13","doi-asserted-by":"crossref","unstructured":"13. Johnson              BS, Chafin              L, Farkas              D, Adair              J, Elhance              A, Farkas              L, et            al. MicroID2: A novel biotin ligase enables rapid            proximity-dependent proteomics. Mol Cell Proteomics.            2022; 21: 100256.","DOI":"10.1016\/j.mcpro.2022.100256"},{"key":"14","doi-asserted-by":"crossref","unstructured":"14. Yin              J, Schoeffler              AJ, Wickliffe              K, Newton              K,                Starovasnik              MA, Dueber              EC, et            al. Structural insights into WD-repeat 48 activation            of ubiquitin-specific protease 46. Structure.            2015; 23: 2043\u20132054.","DOI":"10.1016\/j.str.2015.08.010"},{"key":"15","doi-asserted-by":"crossref","unstructured":"15. Zhu              H, Zhang              T, Wang              F, Yang              J, Ding              J. Structural            insights into the activation of USP46 by WDR48 and WDR20. Cell            Discov. 2019; 5: 34.","DOI":"10.1038\/s41421-019-0102-1"},{"key":"16","doi-asserted-by":"crossref","unstructured":"16. Tomida              S, Mamiya              T, Sakamaki              H, Miura              M, Aosaki              T, Masuda              M, et            al. Usp46 is a quantitative trait gene regulating            mouse immobile behavior in the tail suspension and forced swimming          tests. Nat Genet. 2009; 41:            688\u2013695.","DOI":"10.1038\/ng.344"},{"key":"17","doi-asserted-by":"crossref","unstructured":"17. Huo              Y, Khatri              N, Hou              Q, Gilbert              J, Wang              G, Man              HY. The            deubiquitinating enzyme USP46 regulates AMPA receptor ubiquitination and            trafficking. J Neurochem. 2015;            134: 1067\u20131080.","DOI":"10.1111\/jnc.13194"},{"key":"18","doi-asserted-by":"crossref","unstructured":"18. Kiran              S, Dar              A, Singh              SK, Lee              KY, Dutta              A. The            Deubiquitinase USP46 is essential for proliferation and tumor growth of HPV-transformed            cancers. Mol Cell. 2018;            72: 823\u2013835.e5.","DOI":"10.1016\/j.molcel.2018.09.019"},{"key":"19","doi-asserted-by":"crossref","unstructured":"19. Mu              C, Yu              D, Li              A, Yu              Y, Liang              Z. USP46            regulates glycolysis in the process of cardiac hypertrophy through the HIF-1\u03b1            pathway. Pathol Res Pract. 2025;            270: 155980.","DOI":"10.1016\/j.prp.2025.155980"},{"key":"20","doi-asserted-by":"crossref","unstructured":"20. Imai              S, Kano              M, Nonoyama              K, Ebihara              S. Behavioral            characteristics of ubiquitin-specific peptidase 46-deficient mice.            PLoS One. 2013; 8: e58566.","DOI":"10.1371\/journal.pone.0058566"},{"key":"21","doi-asserted-by":"publisher","unstructured":"21. Mizuno-Iijima              S, Ayabe              S, Kato              K, Matoba              S, Ikeda              Y, Dinh              TTH, et            al. Efficient production of large deletion and gene            fragment knock-in mice mediated by genome editing with Cas9-mouse Cdt1 in mouse            zygotes. Methods. 2021;            191: 23\u201331.","DOI":"10.1016\/j.ymeth.2020.04.007"},{"key":"22","doi-asserted-by":"crossref","unstructured":"22. Tanimoto              Y, Mikami              N, Ishida              M, Iki              N, Kato              K, Sugiyama              F, et            al. Zygote microinjection for creating gene cassette            knock-in and flox alleles in mice. J Vis Exp.            2022; 184: 64161.","DOI":"10.3791\/64161-v"},{"key":"23","doi-asserted-by":"crossref","unstructured":"23. Murata              K, Mimura              A, Suzuki              H, Mikami              N, Hamada              Y, Kato              K, et            al. Efficient induction of proximity-dependent            labelling by biotin feeding in BMAL1-BioID knock-in mice. J            Biochem. 2021; 170:            453\u2013461.","DOI":"10.1093\/jb\/mvab059"},{"key":"24","doi-asserted-by":"publisher","unstructured":"24. Yoshioka              K, Nakagawa              R, Nguyen              CLK, Suzuki              H, Ishigaki              K, Mizuno              S, et            al. Proximity-dependent biotinylation reveals an            interaction between ubiquitin-specific peptidase 46 and centrosome-related            proteins. FEBS Open Bio. 2025;            15: 151\u2013164.","DOI":"10.1002\/2211-5463.13918"},{"key":"25","doi-asserted-by":"crossref","unstructured":"25. Szklarczyk              D, Kirsch              R, Koutrouli              M, Nastou              K, Mehryary              F, Hachilif              R, et            al. The STRING database in 2023: protein-protein            association networks and functional enrichment analyses for any sequenced genome of            interest. Nucleic Acids Res. 2023;            51:(D1):            D638\u2013D646.","DOI":"10.1093\/nar\/gkac1000"},{"key":"26","doi-asserted-by":"crossref","unstructured":"26. Ge              SX, Jung              D, Yao              R. ShinyGO: a            graphical gene-set enrichment tool for animals and plants.            Bioinformatics. 2020; 36:            2628\u20132629.","DOI":"10.1093\/bioinformatics\/btz931"},{"key":"27","doi-asserted-by":"crossref","unstructured":"27. Dumanis              SB, Cha              HJ, Song              JM, Trotter              JH, Spitzer              M, Lee              JY, et            al. ApoE receptor 2 regulates synapse and dendritic            spine formation. PLoS One. 2011;            6: e17203.","DOI":"10.1371\/journal.pone.0017203"},{"key":"28","doi-asserted-by":"crossref","unstructured":"28. Reemst              K, Noctor              SC, Lucassen              PJ, Hol              EM. The            indispensable roles of microglia and astrocytes during brain          development. Front Hum Neurosci. 2016;            10: 566.","DOI":"10.3389\/fnhum.2016.00566"},{"key":"29","doi-asserted-by":"crossref","unstructured":"29. Umemura              S, Imai              S, Mimura              A, Fujiwara              M, Ebihara              S. Impaired            maternal behavior in Usp46 mutant mice: a model for trans-generational transmission of            maternal care. PLoS One. 2015;            10: e0136016.","DOI":"10.1371\/journal.pone.0136016"},{"key":"30","doi-asserted-by":"crossref","unstructured":"30. Li              X, Stevens              PD, Yang              H, Gulhati              P, Wang              W, Evers              BM, et            al. The deubiquitination enzyme USP46 functions as a            tumor suppressor by controlling PHLPP-dependent attenuation of Akt signaling in colon            cancer. Oncogene. 2013;            32: 471\u2013478.","DOI":"10.1038\/onc.2012.66"},{"key":"31","doi-asserted-by":"crossref","unstructured":"31. Willim              J, Woike              D, Greene              D, Das              S, Pfeifer              K, Yuan              W, et            al. Undiagnosed Diseases Network.            Variants in LRRC7 lead to intellectual disability, autism, aggression and            abnormal eating behaviors. Nat Commun.            2024; 15: 7909.","DOI":"10.1038\/s41467-024-52095-x"},{"key":"32","doi-asserted-by":"crossref","unstructured":"32. Wagner              W, Lippmann              K, Heisler              FF, Gromova              KV, Lombino              FL, Roesler              MK, et            al. Myosin VI drives clathrin-mediated AMPA receptor            endocytosis to facilitate cerebellar long-term depression. Cell            Rep. 2019; 28:            11\u201320.e9.","DOI":"10.1016\/j.celrep.2019.06.005"},{"key":"33","doi-asserted-by":"crossref","unstructured":"33. Murtaza              N, Cheng              AA, Brown              CO, Meka              DP, Hong              S, Uy              JA, et            al. Neuron-specific protein network mapping of            autism risk genes identifies shared biological mechanisms and disease-relevant            pathologies. Cell Rep. 2022;            41: 111678.","DOI":"10.1016\/j.celrep.2022.111678"},{"key":"34","doi-asserted-by":"crossref","unstructured":"34. Majewski              \u0141, Maci\u0105g              F,                Boguszewski              PM,                Wasilewska              I, Wiera              G, W\u00f3jtowicz              T, et            al. Overexpression of STIM1 in neurons in mouse            brain improves contextual learning and impairs long-term depression.            Biochim Biophys Acta Mol Cell Res. 2017;            1864: 1071\u20131087.","DOI":"10.1016\/j.bbamcr.2016.11.025"},{"key":"35","doi-asserted-by":"crossref","unstructured":"35. L\u00f3pez-Ju\u00e1rez              A,                Morales-L\u00e1zaro              S,                S\u00e1nchez-S\u00e1nchez              R, Sunkara              M, Lomel\u00ed              H, Velasco              I, et            al. Expression of LPP3 in Bergmann glia is required            for proper cerebellar sphingosine-1-phosphate metabolism\/signaling and            development. Glia. 2011;            59: 577\u2013589.","DOI":"10.1002\/glia.21126"},{"key":"36","doi-asserted-by":"crossref","unstructured":"36. Busnelli              M, Manzini              S, Parolini              C,                Escalante-Alcalde              D, Chiesa              G. Lipid            phosphate phosphatase 3 in vascular pathophysiology.            Atherosclerosis. 2018; 271:            156\u2013165.","DOI":"10.1016\/j.atherosclerosis.2018.02.025"},{"key":"37","doi-asserted-by":"crossref","unstructured":"37. Panchatcharam              M, Salous              AK, Brandon              J, Miriyala              S, Wheeler              J, Patil              P, et            al. Mice with targeted inactivation of ppap2b in            endothelial and hematopoietic cells display enhanced vascular inflammation and            permeability. Arterioscler Thromb Vasc Biol.            2014; 34: 837\u2013845.","DOI":"10.1161\/ATVBAHA.113.302335"},{"key":"38","doi-asserted-by":"crossref","unstructured":"38. Busnelli              M, Manzini              S, Hilvo              M, Parolini              C, Ganzetti              GS, Dellera              F, et            al. Liver-specific deletion of the Plpp3 gene alters            plasma lipid composition and worsens atherosclerosis in apoE<sup>-\/-<\/sup>            mice. Sci Rep. 2017; 7:            44503.","DOI":"10.1038\/srep44503"},{"key":"39","doi-asserted-by":"crossref","unstructured":"39. Chandra              M,                Escalante-Alcalde              D, Bhuiyan              MS, Orr              AW, Kevil              C, Morris              AJ, et            al. Cardiac-specific inactivation of LPP3 in mice            leads to myocardial dysfunction and heart failure. Redox            Biol. 2018; 14:            261\u2013271.","DOI":"10.1016\/j.redox.2017.09.015"},{"key":"40","doi-asserted-by":"crossref","unstructured":"40. Wagner              SA, Beli              P, Weinert              BT, Sch\u00f6lz              C, Kelstrup              CD, Young              C, et            al. Proteomic analyses reveal divergent            ubiquitylation site patterns in murine tissues. Mol Cell            Proteomics. 2012; 11:            1578\u20131585.","DOI":"10.1074\/mcp.M112.017905"},{"key":"41","doi-asserted-by":"crossref","unstructured":"41. Liu              S, Li              S, Yang              Y, Li              W. Termini            restraining of small membrane proteins enables structure determination at near-atomic            resolution. Sci Adv. 2020;            6: eabe3717.","DOI":"10.1126\/sciadv.abe3717"},{"key":"42","doi-asserted-by":"crossref","unstructured":"42. May              DG, Scott              KL, Campos              AR, Roux              KJ. Comparative            application of BioID and TurboID for protein-proximity biotinylation.            Cells. 2020; 9: 1070.","DOI":"10.3390\/cells9051070"},{"key":"43","doi-asserted-by":"crossref","unstructured":"43. G\u00f3mez-L\u00f3pez              S,                Mart\u00ednez-Silva              AV, Montiel              T,                Osorio-G\u00f3mez              D,                Berm\u00fadez-Rattoni              F, Massieu              L, et            al. Neural ablation of the PARK10 candidate Plpp3            leads to dopaminergic transmission deficits without neurodegeneration.            Sci Rep. 2016; 6: 24028.","DOI":"10.1038\/srep24028"},{"key":"44","doi-asserted-by":"crossref","unstructured":"44. Esaki              K, Balan              S, Iwayama              Y,                Shimamoto-Mitsuyama              C,                Hirabayashi              Y, Dean              B, et            al. Evidence for altered metabolism of            sphingosine-1-phosphate in the corpus callosum of patients with            schizophrenia. 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