3,053
Views
14
CrossRef citations to date
0
Altmetric
Review Articles

Spatial organization of palmitoyl acyl transferases governs substrate localization and function

ORCID Icon & ORCID Icon
Pages 60-75 | Received 24 Sep 2019, Accepted 19 Dec 2019, Published online: 22 Jan 2020

References

  • Abrami L, Kunz B, Iacovache I, van der Goot FG. 2008. Palmitoylation and ubiquitination regulate exit of the Wnt signaling protein LRP6 from the endoplasmic reticulum. Proc Natl Acad Sci USA 105:5384–5389.
  • Babu P, Deschenes RJ, Robinson LC. 2004. Akr1p-dependent palmitoylation of Yck2p yeast casein kinase 1 is necessary and sufficient for plasma membrane targeting. J Biol Chem 279:27138–27147.
  • Baker K, Astle DE, Scerif G, Barnes J, Smith J, Moffat G, et al. 2015. Epilepsy, cognitive deficits and neuroanatomy in males with ZDHHC9 mutations. Ann Clin Transl Neurol 2:559–569.
  • Bartels DJ, Mitchell DA, Dong X, Deschenes RJ. 1999. Erf2, a novel gene product that affects the localization and palmitoylation of Ras2 in Saccharomyces cerevisiae. Mol Cell Biol 19:6775–6787.
  • Blanc M, David F, Abrami L, Migliozzi D, Armand F, Bürgi J, et al. 2015. SwissPalm: protein palmitoylation database. F1000Res 4:261.
  • Blaskovic S, Blanc M, van der Goot FG. 2013. What does S-palmitoylation do to membrane proteins? Febs J 280:2766–2774.
  • Brigidi GS, Santyr B, Shimell J, Jovellar B, Bamji SX. 2015. Activity-regulated trafficking of the palmitoyl-acyl transferase DHHC5. Nat Commun 6:8200.
  • Brigidi GS, Sun Y, Beccano-Kelly D, Pitman K, Mobasser M, Borgland SL, et al. 2014. Palmitoylation of delta-catenin by DHHC5 mediates activity-induced synapse plasticity. Nat Neurosci 17:522–532.
  • Chen X, Nelson CD, Li X, Winters CA, Azzam R, Sousa AA, et al. 2011. PSD-95 is required to sustain the molecular organization of the postsynaptic density. J Neurosci 31:6329–6338.
  • El-Husseini AE-D, Schnell E, Dakoji S, Sweeney N, Zhou Q, Prange O, et al. 2002. Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108:849–863.
  • Ernst AM, Syed SA, Zaki O, Bottanelli F, Zheng H, Hacke M, et al. 2018. S-palmitoylation sorts membrane cargo for anterograde transport in the Golgi. Dev Cell 47:479–493 e7.
  • Ernst AM, Toomre D, Bogan JS. 2019. Acylation – a new means to control traffic through the Golgi. Front Cell Dev Biol 7:109.
  • Fairbank M, Huang K, El-Husseini A, Nabi IR. 2012. RING finger palmitoylation of the endoplasmic reticulum Gp78 E3 ubiquitin ligase. FEBS Lett 586:2488–2493.
  • Fallin MD, Lasseter VK, Wolyniec PS, McGrath JA, Nestadt G, Valle D, et al. 2004. Genomewide linkage scan for bipolar-disorder susceptibility loci among Ashkenazi Jewish families. Am J Hum Genet 75:204–219.
  • Feng W, Zhang M. 2009. Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density. Nat Rev Neurosci 10:87–99.
  • Fernandez-Hernando C, et al. 2006. Identification of Golgi-localized acyl transferases that palmitoylate and regulate endothelial nitric oxide synthase. J Cell Biol 174:369–377.
  • Fredericks GJ, Hoffmann FW, Rose AH, Osterheld HJ, Hess FM, Mercier F, et al. 2014. Stable expression and function of the inositol 1,4,5-triphosphate receptor requires palmitoylation by a DHHC6/selenoprotein K complex. Proc Natl Acad Sci USA 111:16478–16483.
  • Fromer M, Pocklington AJ, Kavanagh DH, Williams HJ, Dwyer S, Gormley P, et al. 2014. De novo mutations in schizophrenia implicate synaptic networks. Nature 506:179–184.
  • Fukata M, Fukata Y, Adesnik H, Nicoll RA, Bredt DS. 2004. Identification of PSD-95 palmitoylating enzymes. Neuron 44:987–996.
  • Fukata Y, Dimitrov A, Boncompain G, Vielemeyer O, Perez F, Fukata M, et al. 2013. Local palmitoylation cycles define activity-regulated postsynaptic subdomains. J Cell Biol 202:145–161.
  • Fukata Y, Fukata M. 2010. Protein palmitoylation in neuronal development and synaptic plasticity. Nat Rev Neurosci 11:161–175.
  • Globa AK, Bamji SX. 2017. Protein palmitoylation in the development and plasticity of neuronal connections. Curr Opin Neurobiol 45:210–220.
  • Gold MG, Stengel F, Nygren PJ, Weisbrod CR, Bruce JE, Robinson CV, et al. 2011. Architecture and dynamics of an A-kinase anchoring protein 79 (AKAP79) signaling complex. Proc Natl Acad Sci USA 108:6426–6431.
  • Gorleku OA, Barns A-M, Prescott GR, Greaves J, Chamberlain LH. 2011. Endoplasmic reticulum localization of DHHC palmitoyltransferases mediated by lysine-based sorting signals. J Biol Chem 286:39573–39584.
  • Greaves J, Carmichael JA, Chamberlain LH. 2011. The palmitoyl transferase DHHC2 targets a dynamic membrane cycling pathway: regulation by a C-terminal domain. Mol Biol Cell 22:1887–1895.
  • Greaves J, Chamberlain LH. 2007. Palmitoylation-dependent protein sorting. J Cell Biol 176:249–254.
  • Greaves J, Chamberlain LH. 2014. New links between S-acylation and cancer. J Pathol 233:4–6.
  • Greaves J, Gorleku OA, Salaun C, Chamberlain LH. 2010. Palmitoylation of the SNAP25 protein family: specificity and regulation by DHHC palmitoyl transferases. J Biol Chem 285:24629–24638.
  • Greaves J, Salaun C, Fukata Y, Fukata M, Chamberlain LH. 2008. Palmitoylation and membrane interactions of the neuroprotective chaperone cysteine-string protein. J Biol Chem 283:25014–25026.
  • Guan X, Fierke CA. 2011. Understanding protein palmitoylation: biological significance and enzymology. Sci China Chem 54:1888–1897.
  • Han JY, Lee IG, Shin S, Kim M, Jang JH, Park J, et al. 2017. The first patient with sporadic X-linked intellectual disability with de novo ZDHHC9 mutation identified by targeted next-generation sequencing. Eur J Med Genet 60:499–503.
  • Hata Y, Nakanishi H, Takai Y. 1998. Synaptic PDZ domain-containing proteins. Neurosci Res 32:1–7.
  • Hayashi T, Rumbaugh G, Huganir RL. 2005. Differential regulation of AMPA receptor subunit trafficking by palmitoylation of two distinct sites. Neuron 47:709–723.
  • He M, Abdi KM, Bennett V. 2014. Ankyrin-G palmitoylation and betaII-spectrin binding to phosphoinositide lipids drive lateral membrane assembly. J Cell Biol 206:273–288.
  • He M, Jenkins P, Bennett V. 2012. Cysteine 70 of ankyrin-G is S-palmitoylated and is required for function of ankyrin-G in membrane domain assembly. J Biol Chem 287:43995–44005.
  • Holland SM, Thomas GM. 2017. Roles of palmitoylation in axon growth, degeneration and regeneration. J Neurosci Res 95:1528–1539.
  • Hou H, John Peter AT, Meiringer C, Subramanian K, Ungermann C. 2009. Analysis of DHHC acyltransferases implies overlapping substrate specificity and a two-step reaction mechanism. Traffic 10:1061–1073.
  • Hou H, Subramanian K, LaGrassa TJ, Markgraf D, Dietrich LEP, Urban J, et al. 2005. The DHHC protein Pfa3 affects vacuole-associated palmitoylation of the fusion factor Vac8. Proc Natl Acad Sci USA 102:17366–17371.
  • Howie J, Reilly L, Fraser NJ, Vlachaki Walker JM, Wypijewski KJ, Ashford MLJ, et al. 2014. Substrate recognition by the cell surface palmitoyl transferase DHHC5. Proc Natl Acad Sci USA 111:17534–17539.,
  • Huang K, Sanders S, Singaraja R, Orban P, Cijsouw T, Arstikaitis P, et al. 2009. Neuronal palmitoyl acyl transferases exhibit distinct substrate specificity. Faseb J 23:2605–2615.
  • Iwanaga T, Tsutsumi R, Noritake J, Fukata Y, Fukata M. 2009. Dynamic protein palmitoylation in cellular signaling. Prog Lipid Res 48:117–127.
  • Jenkins PM, He M, Bennett V. 2015. Dynamic spectrin/ankyrin-G microdomains promote lateral membrane assembly by opposing endocytosis. Sci Adv 1:e1500301.
  • Jeyifous O, Lin EI, Chen X, Antinone SE, Mastro R, Drisdel R, et al. 2016. Palmitoylation regulates glutamate receptor distributions in postsynaptic densities through control of PSD95 conformation and orientation. Proc Natl Acad Sci USA 113:E8482–E8491.,
  • Jurado S, Biou V, Malenka RC. 2010. A calcineurin/AKAP complex is required for NMDA receptor-dependent long-term depression. Nat Neurosci 13:1053–1055.
  • Kanaani J, El-Husseini AE-D, Aguilera-Moreno A, Diacovo JM, Bredt DS, Baekkeskov S, et al. 2002. A combination of three distinct trafficking signals mediates axonal targeting and presynaptic clustering of GAD65. J Cell Biol 158:1229–1238.
  • Kanaani J, Patterson G, Schaufele F, Lippincott-Schwartz J, Baekkeskov S. 2008. A palmitoylation cycle dynamically regulates partitioning of the GABA-synthesizing enzyme GAD65 between ER-Golgi and post-Golgi membranes. J Cell Sci 121:437–449.
  • Keith DJ, Sanderson JL, Gibson ES, Woolfrey KM, Robertson HR, Olszewski K, et al. 2012. Palmitoylation of A-kinase anchoring protein 79/150 regulates dendritic endosomal targeting and synaptic plasticity mechanisms. J Neurosci 32:7119–7136.
  • Kim E, Sheng M. 2004. PDZ domain proteins of synapses. Nat Rev Neurosci 5:771–781.
  • Lakkaraju AKK, Abrami L, Lemmin T, Blaskovic S, Kunz B, Kihara A, et al. 2012. Palmitoylated calnexin is a key component of the ribosome-translocon complex. Embo J 31:1823–1835.
  • Lam KKY, Davey M, Sun B, Roth AF, Davis NG, Conibear E, et al. 2006. Palmitoylation by the DHHC protein Pfa4 regulates the ER exit of Chs3. J Cell Biol 174:19–25.
  • Lemonidis K, Gorleku OA, Sanchez-Perez MC, Grefen C, Chamberlain LH. 2014. The Golgi S-acylation machinery comprises zDHHC enzymes with major differences in substrate affinity and S-acylation activity. Mol Biol Cell 25:3870–3883.
  • Lemonidis K, Salaun C, Kouskou M, Diez-Ardanuy C, Chamberlain LH, Greaves J, et al. 2017. Substrate selectivity in the zDHHC family of S-acyltransferases. Biochem Soc Trans 45:751–758.
  • Lemonidis K, Sanchez-Perez MC, Chamberlain LH. 2015. Identification of a novel sequence motif recognized by the ankyrin repeat domain of zDHHC17/13 S-acyltransferases. J Biol Chem 290:21939–21950.
  • Lievens PM-J, Kuznetsova T, Kochlamazashvili G, Cesca F, Gorinski N, Galil DA, et al. 2016. ZDHHC3 tyrosine phosphorylation regulates neural cell adhesion molecule palmitoylation. Mol Cell Biol 36:2208–2225.
  • Lin M-J, Fine M, Lu J-Y, Hofmann SL, Frazier G, Hilgemann DW, et al. 2013. Massive palmitoylation-dependent endocytosis during reoxygenation of anoxic cardiac muscle. Elife 2:e01295.
  • Linder ME, Deschenes RJ. 2007. Palmitoylation: policing protein stability and traffic. Nat Rev Mol Cell Biol 8:74–84.
  • Lobo S, Greentree WK, Linder ME, Deschenes RJ. 2002. Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J Biol Chem 277:41268–41273.
  • Lundby A, Andersen MN, Steffensen AB, Horn H, Kelstrup CD, Francavilla C, et al. 2013. In vivo phosphoproteomics analysis reveals the cardiac targets of beta-adrenergic receptor signaling. Sci Signal 6:rs11–rs11.
  • Masurel-Paulet A, Kalscheuer VM, Lebrun N, Hu H, Levy F, Thauvin-Robinet C, et al. 2014. Expanding the clinical phenotype of patients with a ZDHHC9 mutation. Am J Med Genet A 164:789–795.
  • Mitchell DA, Hamel LD, Reddy KD, Farh L, Rettew LM, Sanchez PR, et al. 2014. Mutations in the X-linked intellectual disability gene, zDHHC9, alter autopalmitoylation activity by distinct mechanisms. J Biol Chem 289:18582–18592.
  • Mitchell DA, Mitchell G, Ling Y, Budde C, Deschenes RJ. 2010. Mutational analysis of Saccharomyces cerevisiae Erf2 reveals a two-step reaction mechanism for protein palmitoylation by DHHC enzymes. J Biol Chem 285:38104–38114.
  • Mitchell DA, Vasudevan A, Linder ME, Deschenes RJ. 2006. Protein palmitoylation by a family of DHHC protein S-acyltransferases. J Lipid Res 47:1118–1127.
  • Moutin E, Nikonenko I, Stefanelli T, Wirth A, Ponimaskin E, De Roo M, et al. 2017. Palmitoylation of cdc42 promotes spine stabilization and rescues spine density deficit in a mouse model of 22q11.2 deletion syndrome. Cereb Cortex 27:3618–3629.
  • Mukai J, Dhilla A, Drew LJ, Stark KL, Cao L, MacDermott AB, et al. 2008. Palmitoylation-dependent neurodevelopmental deficits in a mouse model of 22q11 microdeletion. Nat Neurosci 11:1302–1310.
  • Mukai J, Liu H, Burt RA, Swor DE, Lai W-S, Karayiorgou M, et al. 2004. Evidence that the gene encoding ZDHHC8 contributes to the risk of schizophrenia. Nat Genet 36:725–731.
  • Mukai J, Tamura M, Fénelon K, Rosen AM, Spellman TJ, Kang R, et al. 2015. Molecular substrates of altered axonal growth and brain connectivity in a mouse model of schizophrenia. Neuron 86:680–695.
  • Nadolski MJ, Linder ME. 2007. Protein lipidation. Febs J 274:5202–5210.
  • Nadolski MJ, Linder ME. 2009. Molecular recognition of the palmitoylation substrate Vac8 by its palmitoyltransferase Pfa3. J Biol Chem 284:17720–17730.
  • Noritake J, Fukata Y, Iwanaga T, Hosomi N, Tsutsumi R, Matsuda N, et al. 2009. Mobile DHHC palmitoylating enzyme mediates activity-sensitive synaptic targeting of PSD-95. J Cell Biol 186:147–160.
  • Ohno Y, Kashio A, Ogata R, Ishitomi A, Yamazaki Y, Kihara A, et al. 2012. Analysis of substrate specificity of human DHHC protein acyltransferases using a yeast expression system. Mol Biol Cell 23:4543–4551.
  • Ohno Y, Kihara A, Sano T, Igarashi Y. 2006. Intracellular localization and tissue-specific distribution of human and yeast DHHC cysteine-rich domain-containing proteins. Biochim Biophys Acta 1761:474–483.
  • Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, Harris KM, et al. 2006. Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52:817–830.
  • Park M. 2004. Recycling endosomes supply AMPA receptors for LTP. Science 305:1972–1975.
  • Perrody E, Abrami L, Feldman M, Kunz B, Urbé S, van der Goot FG, et al. 2016. Ubiquitin-dependent folding of the Wnt signaling coreceptor LRP6. Elife 5:e19083.
  • Pinner AL, Tucholski J, Haroutunian V, McCullumsmith RE, Meador-Woodruff JH. 2016. Decreased protein S-palmitoylation in dorsolateral prefrontal cortex in schizophrenia. Schizophr Res 177:78–87.
  • Plain F, Congreve SD, Yee RSZ, Kennedy J, Howie J, Kuo C-W, et al. 2017. An amphipathic alpha-helix directs palmitoylation of the large intracellular loop of the sodium/calcium exchanger. J Biol Chem 292:10745–10752.
  • Politis EG, Roth AF, Davis NG. 2005. Transmembrane topology of the protein palmitoyl transferase Akr1. J Biol Chem 280:10156–10163.
  • Putilina T, Wong P, Gentleman S. 1999. The DHHC domain: a new highly conserved cysteine-rich motif. Mol Cell Biochem 195:219–226.
  • Rana MS, Lee CJ, Banerjee A. 2019. The molecular mechanism of DHHC protein acyltransferases. Biochem Soc Trans 47:157–167.
  • Raymond FL, Tarpey PS, Edkins S, Tofts C, O’Meara S, Teague J, et al. 2007. Mutations in ZDHHC9, which encodes a palmitoyltransferase of NRAS and HRAS, cause X-linked mental retardation associated with a Marfanoid habitus. Am J Hum Genet 80:982–987.
  • Rocks O, Gerauer M, Vartak N, Koch S, Huang Z-P, Pechlivanis M, et al. 2010. The palmitoylation machinery is a spatially organizing system for peripheral membrane proteins. Cell 141:458–471.
  • Rocks O, Peyker A, Kahms M, Verveer PJ, Koerner C, Lumbierres M, et al. 2005. An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307:1746–1752.
  • Rodenburg RNP, Snijder J, van de Waterbeemd M, Schouten A, Granneman J, Heck AJR, et al. 2017. Stochastic palmitoylation of accessible cysteines in membrane proteins revealed by native mass spectrometry. Nat Commun 8:1280.
  • Roth AF, Feng Y, Chen L, Davis NG. 2002. The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. J Cell Biol 159:23–28.
  • Roth AF, Wan J, Bailey AO, Sun B, Kuchar JA, Green WN, et al. 2006. Global analysis of protein palmitoylation in yeast. Cell 125:1003–1013.
  • Rush DB, Leon RT, McCollum MH, Treu RW, Wei J. 2012. Palmitoylation and trafficking of GAD65 are impaired in a cellular model of Huntington's disease. Biochem J 442:39–48.
  • Salaun C, Greaves J, Chamberlain LH. 2010. The intracellular dynamic of protein palmitoylation. J Cell Biol 191:1229–1238.
  • Salaun C, Ritchie L, Greaves J, Bushell TJ, Chamberlain LH. 2017. The C-terminal domain of zDHHC2 contains distinct sorting signals that regulate intracellular localisation in neurons and neuroendocrine cells. Mol Cell Neurosci 85:235–246.
  • Sanders SS, Martin DDO, Butland SL, Lavallée-Adam M, Calzolari D, Kay C, et al. 2015. Curation of the mammalian palmitoylome indicates a pivotal role for palmitoylation in diseases and disorders of the nervous system and cancers. PLoS Comput Biol 11:e1004405.
  • Sanderson JL, Dell'Acqua ML. 2011. AKAP signaling complexes in regulation of excitatory synaptic plasticity. Neuroscientist 17:321–336.
  • Sanderson JL, Gorski JA, Gibson ES, Lam P, Freund RK, Chick WS, et al. 2012. AKAP150-anchored calcineurin regulates synaptic plasticity by limiting synaptic incorporation of Ca2+-permeable AMPA receptors. J Neurosci 32:15036–15052.
  • Schizophrenia Working Group of the Psychiatric Genomics Consortium. 2014. Biological insights from 108 schizophrenia-associated genetic loci. Nature 511:421–427.
  • Setou M, Seog D-H, Tanaka Y, Kanai Y, Takei Y, Kawagishi M, et al. 2002. Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 417:83–87.
  • Shimell JJ, Shah BS, Cain SM, Thouta S, Kuhlmann N, Tatarnikov I, et al. 2019. The X-linked intellectual disability gene Zdhhc9 is essential for dendrite outgrowth and inhibitory synapse formation. Cell Rep 29:2422–2437 e8.
  • Shmueli A, Segal M, Sapir T, Tsutsumi R, Noritake J, Bar A, et al. 2010. Ndel1 palmitoylation: a new mean to regulate cytoplasmic dynein activity. Embo J 29:107–119.
  • Siddoway B, Hou H, Yang H, Petralia R, Xia H. 2014. Synaptic activity bidirectionally regulates a novel sequence-specific S-Q phosphoproteome in neurons. J Neurochem 128:841–851.
  • Smith KE, Gibson ES, Dell'Acqua ML. 2006. cAMP-dependent protein kinase postsynaptic localization regulated by NMDA receptor activation through translocation of an A-kinase anchoring protein scaffold protein. J Neurosci 26:2391–2402.
  • Smotrys JE, Schoenfish MJ, Stutz MA, Linder ME. 2005. The vacuolar DHHC-CRD protein Pfa3p is a protein acyltransferase for Vac8p. J Cell Biol 170:1091–1099.
  • Sobocinska J, Roszczenko-Jasińska P, Ciesielska A, Kwiatkowska K. 2017. Protein palmitoylation and its role in bacterial and viral infections. Front Immunol 8:2003.
  • Sutton LM, Sanders SS, Butland SL, Singaraja RR, Franciosi S, Southwell AL, et al. 2013. Hip14l-deficient mice develop neuropathological and behavioural features of Huntington disease. Hum Mol Genet 22:452–465.
  • Swarthout JT, Lobo S, Farh L, Croke MR, Greentree WK, Deschenes RJ, et al. 2005. DHHC9 and GCP16 constitute a human protein fatty acyltransferase with specificity for H- and N-Ras. J Biol Chem 280:31141–31148.
  • Tavalin SJ, Colledge M, Hell JW, Langeberg LK, Huganir RL, Scott JD, et al. 2002. Regulation of GluR1 by the A-kinase anchoring protein 79 (AKAP79) signaling complex shares properties with long-term depression. J Neurosci 22:3044–3051.
  • Thomas GM, Hayashi T, Chiu S-L, Chen C-M, Huganir RL. 2012. Palmitoylation by DHHC5/8 targets GRIP1 to dendritic endosomes to regulate AMPA-R trafficking. Neuron 73:482–496.
  • Thomas GM, Hayashi T, Huganir RL, Linden DJ. 2013. DHHC8-dependent PICK1 palmitoylation is required for induction of cerebellar long-term synaptic depression. J Neurosci 33:15401–15407.
  • Tian L, McClafferty H, Jeffries O, Shipston MJ. 2010. Multiple palmitoyltransferases are required for palmitoylation-dependent regulation of large conductance calcium- and voltage-activated potassium channels. J Biol Chem 285:23954–23962.
  • Traub LM, Bonifacino JS. 2013. Cargo recognition in clathrin-mediated endocytosis. Cold Spring Harb Perspect Biol 5:a016790–a016790.
  • Tsutsumi R, Fukata Y, Noritake J, Iwanaga T, Perez F, Fukata M, et al. 2009. Identification of G protein alpha subunit-palmitoylating enzyme. Mol Cell Biol 29:435–447.
  • Tulloch LB, Howie J, Wypijewski KJ, Wilson CR, Bernard WG, Shattock MJ, et al. 2011. The inhibitory effect of phospholemman on the sodium pump requires its palmitoylation. J Biol Chem 286:36020–36031.
  • Tzschach A, Grasshoff U, Beck-Woedl S, Dufke C, Bauer C, Kehrer M, et al. 2015. Next-generation sequencing in X-linked intellectual disability. Eur J Hum Genet 23:1513–1518.
  • Valdez-Taubas J, Pelham H. 2005. Swf1-dependent palmitoylation of the SNARE Tlg1 prevents its ubiquitination and degradation. Embo J 24:2524–2532.
  • Woodin M, Wang PP, Aleman D, McDonald-McGinn D, Zackai E, Moss E, et al. 2001. Neuropsychological profile of children and adolescents with the 22q11.2 microdeletion. Genet Med 3:34–39.
  • Woolfrey KM, Sanderson JL, Dell'Acqua ML. 2015. The palmitoyl acyltransferase DHHC2 regulates recycling endosome exocytosis and synaptic potentiation through palmitoylation of AKAP79/150. J Neurosci 35:442–456.
  • Yuan L, Seong E, Beuscher JL, Arikkath J. 2015. Delta-catenin regulates spine architecture via cadherin and PDZ-dependent interactions. J Biol Chem 290:10947–10957.