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A novel effect of PDLIM5 in α7 nicotinic acetylcholine receptor upregulation and surface expression

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Abstract

Nicotinic acetylcholine receptors (nAChRs) are widespread throughout the central nervous system. Signaling through nAChRs contributes to numerous higher-order functions, including memory and cognition, as well as abnormalities such as nicotine addiction and neurodegenerative disorders. Although recent studies indicate that the PDZ-containing proteins comprising PSD-95 family co-localize with nicotinic acetylcholine receptors and mediate downstream signaling in the neurons, the mechanisms by which α7nAChRs are regulated remain unclear. Here, we show that the PDZ-LIM domain family protein PDLIM5 binds to α7nAChRs and plays a role in nicotine-induced α7nAChRs upregulation and surface expression. We find that chronic exposure to 1 μM nicotine upregulated α7, β2-contained nAChRs and PDLIM5 in cultured hippocampal neurons, and the upregulation of α7nAChRs and PDLIM5 is increased more on the cell membrane than the cytoplasm. Interestingly, in primary hippocampal neurons, α7nAChRs and β2nAChRs display distinct patterns of expression, with α7nAChRs colocalized more with PDLIM5. Furthermore, PDLIM5 interacts with α7nAChRs, but not β2nAChRs in native brain neurons. Knocking down of PDLIM5 in SH-SY5Y abolishes nicotine-induced upregulation of α7nAChRs. In primary hippocampal neurons, using shRNA against PDLIM5 decreased both surface clustering of α7nAChRs and α7nAChRs-mediated currents. Proteomics analysis and isothermal titration calorimetry (ITC) results show that PDLIM5 interacts with α7nAChRs through the PDZ domain, and the interaction between PDLIM5 and α7nAChRs can be promoted by nicotine. Collectively, our data suggest a novel cellular role of PDLIM5 in the regulation of α7nAChRs, which may be relevant to plastic changes in the nervous system.

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References

  1. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89(1):73–120. https://doi.org/10.1152/physrev.00015.2008

    Article  CAS  PubMed  Google Scholar 

  2. Miwa JM, Freedman R, Lester HA (2011) Neural systems governed by nicotinic acetylcholine receptors: emerging hypotheses. Neuron 70(1):20–33. https://doi.org/10.1016/j.neuron.2011.03.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Stokes C, Treinin M, Papke RL (2015) Looking below the surface of nicotinic acetylcholine receptors. Trends Pharmacol Sci 36(8):514–523. https://doi.org/10.1016/j.tips.2015.05.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Picciotto MR, Kenny PJ (2021) Mechanisms of Nicotine Addiction. Cold Spring Harb Perspect Med. https://doi.org/10.1101/cshperspect.a039610

    Article  PubMed  Google Scholar 

  5. Gotti C, Zoli M, Clementi F (2006) Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmacol Sci 27(9):482–491. https://doi.org/10.1016/j.tips.2006.07.004

    Article  CAS  PubMed  Google Scholar 

  6. Kutlu MG, Gould TJ (2015) Nicotinic receptors, memory, and hippocampus. Curr Top Behav Neurosci 23:137–163. https://doi.org/10.1007/978-3-319-13665-3_6

    Article  CAS  PubMed  Google Scholar 

  7. Ambrose V, Miller JH, Dickson SJ, Hampton S, Truman P, Lea RA, Fowles J (2007) Tobacco particulate matter is more potent than nicotine at upregulating nicotinic receptors on SH-SY5Y cells. Nicotine Tob Res 9(8):793–799. https://doi.org/10.1080/14622200701485117

    Article  CAS  PubMed  Google Scholar 

  8. Besson M, Granon S, Mameli-Engvall M, Cloez-Tayarani I, Maubourguet N, Cormier A, Cazala P, David V, Changeux JP, Faure P (2007) Long-term effects of chronic nicotine exposure on brain nicotinic receptors. Proc Natl Acad Sci USA 104(19):8155–8160. https://doi.org/10.1073/pnas.0702698104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cano M, Reynaga DD, Belluzzi JD, Loughlin SE, Leslie F (2020) Chronic exposure to cigarette smoke extract upregulates nicotinic receptor binding in adult and adolescent rats. Neuropharmacology 181:108308. https://doi.org/10.1016/j.neuropharm.2020.108308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Teaktong T, Graham AJ, Johnson M, Court JA, Perry EK (2004) Selective changes in nicotinic acetylcholine receptor subtypes related to tobacco smoking: an immunohistochemical study. Neuropathol Appl Neurobiol 30(3):243–254. https://doi.org/10.1046/j.0305-1846.2003.00528.x

    Article  CAS  PubMed  Google Scholar 

  11. Donde C, Brunelin J, Mondino M, Cellard C, Rolland B, Haesebaert F (2020) The effects of acute nicotine administration on cognitive and early sensory processes in schizophrenia: a systematic review. Neurosci Biobehav Rev 118:121–133. https://doi.org/10.1016/j.neubiorev.2020.07.035

    Article  CAS  PubMed  Google Scholar 

  12. Mineur YS, Picciotto MR (2010) Nicotine receptors and depression: revisiting and revising the cholinergic hypothesis. Trends Pharmacol Sci 31(12):580–586. https://doi.org/10.1016/j.tips.2010.09.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Benowitz NL (2010) Nicotine addiction. N Engl J Med 362(24):2295–2303. https://doi.org/10.1056/NEJMra0809890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Changeux JP (2010) Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat Rev Neurosci 11(6):389–401. https://doi.org/10.1038/nrn2849

    Article  CAS  PubMed  Google Scholar 

  15. Colombo SF, Mazzo F, Pistillo F, Gotti C (2013) Biogenesis, trafficking and up-regulation of nicotinic ACh receptors. Biochem Pharmacol 86(8):1063–1073. https://doi.org/10.1016/j.bcp.2013.06.023

    Article  CAS  PubMed  Google Scholar 

  16. Fox-Loe AM, Moonschi FH, Richards CI (2017) Organelle-specific single-molecule imaging of alpha4beta2 nicotinic receptors reveals the effect of nicotine on receptor assembly and cell-surface trafficking. J Biol Chem 292(51):21159–21169. https://doi.org/10.1074/jbc.M117.801431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Govind AP, Vezina P, Green WN (2009) Nicotine-induced upregulation of nicotinic receptors: underlying mechanisms and relevance to nicotine addiction. Biochem Pharmacol 78(7):756–765. https://doi.org/10.1016/j.bcp.2009.06.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Conroy WG, Liu Z, Nai Q, Coggan JS, Berg DK (2003) PDZ-containing proteins provide a functional postsynaptic scaffold for nicotinic receptors in neurons. Neuron 38(5):759–771. https://doi.org/10.1016/s0896-6273(03)00324-6

    Article  CAS  PubMed  Google Scholar 

  19. Parker MJ, Zhao SL, Bredt DS, Sanes JR, Feng GP (2004) PSD93 regulates synaptic stability at neuronal cholinergic synapses. J Neurosci 24(2):378–388. https://doi.org/10.1523/Jneurosci.3865-03.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gomez-Varela D, Schmidt M, Schoellerman J, Peters EC, Berg DK (2012) PMCA2 via PSD-95 controls calcium signaling by alpha7-containing nicotinic acetylcholine receptors on aspiny interneurons. J Neurosci 32(20):6894–6905. https://doi.org/10.1523/JNEUROSCI.5972-11.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Baer K, Burli T, Huh KH, Wiesner A, Erb-Vogtli S, Gockeritz-Dujmovic D, Moransard M, Nishimune A, Rees MI, Henley JM, Fritschy JM, Fuhrer C (2007) PICK1 interacts with alpha7 neuronal nicotinic acetylcholine receptors and controls their clustering. Mol Cell Neurosci 35(2):339–355. https://doi.org/10.1016/j.mcn.2007.03.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Huang X, Qu R, Ouyang J, Zhong S, Dai J (2020) An overview of the cytoskeleton-associated role of PDLIM5. Front Physiol 11:975. https://doi.org/10.3389/fphys.2020.00975

    Article  PubMed  PubMed Central  Google Scholar 

  23. Kuroda S, Tokunaga C, Kiyohara Y, Higuchi O, Konishi H, Mizuno K, Gill GN, Kikkawa U (1996) Protein-protein interaction of zinc finger LIM domains with protein kinase C. J Biol Chem 271(49):31029–31032. https://doi.org/10.1074/jbc.271.49.31029

    Article  CAS  PubMed  Google Scholar 

  24. Horiuchi Y, Arai M, Niizato K, Iritani S, Noguchi E, Ohtsuki T, Koga M, Kato T, Itokawa M, Arinami T (2006) A polymorphism in the PDLIM5 gene associated with gene expression and schizophrenia. Biol Psychiatry 59(5):434–439. https://doi.org/10.1016/j.biopsych.2005.07.041

    Article  CAS  PubMed  Google Scholar 

  25. Liu Z, Liu W, Xiao Z, Wang G, Yin S, Zhu F, Wang H, Cheng J, Wang X, He X, Li W (2008) A major single nucleotide polymorphism of the PDLIM5 gene associated with recurrent major depressive disorder. J Psychiatry Neurosci 33(1):43–46

    PubMed  PubMed Central  Google Scholar 

  26. Zhao T, Liu Y, Wang P, Li S, Zhou DZ, Zhang D, Chen Z, Wang T, Xu H, Feng GY, He L, Yu L (2009) Positive association between the PDLIM5 gene and bipolar disorder in the Chinese Han population. J Psychiatr Neurosci 34(3):199–204

    Google Scholar 

  27. Maeno-Hikichi Y, Chang S, Matsumura K, Lai M, Lin H, Nakagawa N, Kuroda S, Zhang JF (2003) A PKC epsilon-ENH-channel complex specifically modulates N-type Ca2+ channels. Nat Neurosci 6(5):468–475. https://doi.org/10.1038/nn1041

    Article  CAS  PubMed  Google Scholar 

  28. Herrick S, Evers DM, Lee JY, Udagawa N, Pak DT (2010) Postsynaptic PDLIM5/Enigma Homolog binds SPAR and causes dendritic spine shrinkage. Mol Cell Neurosci 43(2):188–200. https://doi.org/10.1016/j.mcn.2009.10.009

    Article  CAS  PubMed  Google Scholar 

  29. Ren B, Li X, Zhang J, Fan J, Duan J, Chen Y (2015) PDLIM5 mediates PKCepsilon translocation in PMA-induced growth cone collapse. Cell Signal 27(3):424–435. https://doi.org/10.1016/j.cellsig.2014.12.005

    Article  CAS  PubMed  Google Scholar 

  30. Baumert R, Ji H, Paulucci-Holthauzen A, Wolfe A, Sagum C, Hodgson L, Arikkath J, Chen X, Bedford MT, Waxham MN, McCrea PD (2020) Novel phospho-switch function of delta-catenin in dendrite development. J Cell Biol 219(11):10. https://doi.org/10.1083/jcb.201909166

    Article  CAS  Google Scholar 

  31. Duan JJ, Pandey S, Li TM, Castellano D, Cu XL, Li J, Tian QJ, Lu W (2019) Genetic deletion of GABA(A) receptors reveals distinct requirements of neurotransmitter receptors for GABAergic and glutamatergic synapse development. Front Cell Neurosci. https://doi.org/10.3389/fncel.2019.00217

    Article  PubMed  PubMed Central  Google Scholar 

  32. Puddifoot CA, Wu M, Sung RJ, Joiner WJ (2015) Ly6h regulates trafficking of alpha7 nicotinic acetylcholine receptors and nicotine-induced potentiation of glutamatergic signaling. J Neurosci 35(8):3420–3430. https://doi.org/10.1523/JNEUROSCI.3630-14.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rose JE, Mukhin AG, Lokitz SJ, Turkington TG, Herskovic J, Behm FM, Garg S, Garg PK (2010) Kinetics of brain nicotine accumulation in dependent and nondependent smokers assessed with PET and cigarettes containing 11C-nicotine. Proc Natl Acad Sci USA 107(11):5190–5195. https://doi.org/10.1073/pnas.0909184107

    Article  PubMed  PubMed Central  Google Scholar 

  34. Marks MJ, Whiteaker P, Calcaterra J, Stitzel JA, Bullock AE, Grady SR, Picciotto MR, Changeux JP, Collins AC (1999) Two pharmacologically distinct components of nicotinic receptor-mediated rubidium efflux in mouse brain require the beta2 subunit. J Pharmacol Exp Ther 289(2):1090–1103

    CAS  PubMed  Google Scholar 

  35. Daly JW (2005) Nicotinic agonists, antagonists, and modulators from natural sources. Cell Mol Neurobiol 25(3–4):513–552. https://doi.org/10.1007/s10571-005-3968-4

    Article  CAS  PubMed  Google Scholar 

  36. Fabian-Fine R, Skehel P, Errington ML, Davies HA, Sher E, Stewart MG, Fine A (2001) Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci 21(20):7993–8003

    Article  CAS  Google Scholar 

  37. Chen Y, Lai M, Maeno-Hikichi Y, Zhang JF (2006) Essential role of the LIM domain in the formation of the PKCepsilon-ENH-N-type Ca2+ channel complex. Cell Signal 18(2):215–224. https://doi.org/10.1016/j.cellsig.2005.04.007

    Article  CAS  PubMed  Google Scholar 

  38. Gardezi SR, Weber AM, Li Q, Wong FK, Stanley EF (2009) PDLIM5 is not a neuronal CaV2.2 adaptor protein. Nat Neurosci 12(8):957–958. https://doi.org/10.1038/nn0809-957a (author reply 958)

    Article  CAS  PubMed  Google Scholar 

  39. Alkondon M, Albuquerque EX (1993) Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. I. Pharmacological and functional evidence for distinct structural subtypes. J Pharmacol Exp Ther 265(3):1455–1473

    CAS  PubMed  Google Scholar 

  40. John D, Shelukhina I, Yanagawa Y, Deuchars J, Henderson Z (2015) Functional alpha7 nicotinic receptors are expressed on immature granule cells of the postnatal dentate gyrus. Brain Res 1601:15–30. https://doi.org/10.1016/j.brainres.2014.12.041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Yamauchi JG, Nemecz A, Nguyen QT, Muller A, Schroeder LF, Talley TT, Lindstrom J, Kleinfeld D, Taylor P (2011) Characterizing ligand-gated ion channel receptors with genetically encoded Ca2++ sensors. PLoS ONE 6(1):e16519. https://doi.org/10.1371/journal.pone.0016519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Young GT, Zwart R, Walker AS, Sher E, Millar NS (2008) Potentiation of alpha7 nicotinic acetylcholine receptors via an allosteric transmembrane site. Proc Natl Acad Sci USA 105(38):14686–14691. https://doi.org/10.1073/pnas.0804372105

    Article  PubMed  PubMed Central  Google Scholar 

  43. Kim E, Sheng M (2004) PDZ domain proteins of synapses. Nat Rev Neurosci 5(10):771–781. https://doi.org/10.1038/nrn1517

    Article  CAS  PubMed  Google Scholar 

  44. Dani JA, Ji D, Zhou FM (2001) Synaptic plasticity and nicotine addiction. Neuron 31(3):349–352. https://doi.org/10.1016/s0896-6273(01)00379-8

    Article  CAS  PubMed  Google Scholar 

  45. Kobayashi Y, Tomoshige S, Imakado K, Sekino Y, Koganezawa N, Shirao T, Diniz GB, Miyamoto T, Saito Y (2021) Ciliary GPCR-based transcriptome as a key regulator of cilia length control. FASEB Bioadv 3(9):744–767. https://doi.org/10.1096/fba.2021-00029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Murakami K, Ishikawa Y, Sato F (2013) Localization of alpha 7 nicotinic acetylcholine receptor immunoreactivity on gabaergic interneurons in layers I-III of the rat retrosplenial granular cortex. Neuroscience 252:443–459. https://doi.org/10.1016/j.neuroscience.2013.08.024

    Article  CAS  PubMed  Google Scholar 

  47. Ge S, Dani JA (2005) Nicotinic acetylcholine receptors at glutamate synapses facilitate long-term depression or potentiation. J Neurosci 25(26):6084–6091. https://doi.org/10.1523/JNEUROSCI.0542-05.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Ji D, Lape R, Dani JA (2001) Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31(1):131–141. https://doi.org/10.1016/s0896-6273(01)00332-4

    Article  CAS  PubMed  Google Scholar 

  49. McGehee DS, Heath MJ, Gelber S, Devay P, Role LW (1995) Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269(5231):1692–1696. https://doi.org/10.1126/science.7569895

    Article  CAS  Google Scholar 

  50. Herber DL, Severance EG, Cuevas J, Morgan D, Gordon MN (2004) Biochemical and histochemical evidence of nonspecific binding of alpha7nAChR antibodies to mouse brain tissue. J Histochem Cytochem 52(10):1367–1376. https://doi.org/10.1177/002215540405201013

    Article  CAS  PubMed  Google Scholar 

  51. Jones IW, Wonnacott S (2005) Why doesn’t nicotinic ACh receptor immunoreactivity knock out? Trends Neurosci 28(7):343–345. https://doi.org/10.1016/j.tins.2005.04.010

    Article  CAS  PubMed  Google Scholar 

  52. Xu J, Zhu Y, Heinemann SF (2006) Identification of sequence motifs that target neuronal nicotinic receptors to dendrites and axons. J Neurosci 26(38):9780–9793. https://doi.org/10.1523/JNEUROSCI.0840-06.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Dajas-Bailador FA, Soliakov L, Wonnacott S (2002) Nicotine activates the extracellular signal-regulated kinase 1/2 via the alpha7 nicotinic acetylcholine receptor and protein kinase A, in SH-SY5Y cells and hippocampal neurones. J Neurochem 80(3):520–530. https://doi.org/10.1046/j.0022-3042.2001.00725.x

    Article  CAS  PubMed  Google Scholar 

  54. Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13(2):596–604

    Article  CAS  Google Scholar 

  55. Barrantes GE, Rogers AT, Lindstrom J, Wonnacott S (1995) alpha-Bungarotoxin binding sites in rat hippocampal and cortical cultures: initial characterisation, colocalisation with alpha 7 subunits and up-regulation by chronic nicotine treatment. Brain Res 672(1–2):228–236. https://doi.org/10.1016/0006-8993(94)01386-v

    Article  CAS  PubMed  Google Scholar 

  56. Ridley DL, Rogers A, Wonnacott S (2001) Differential effects of chronic drug treatment on alpha3* and alpha7 nicotinic receptor binding sites, in hippocampal neurones and SH-SY5Y cells. Br J Pharmacol 133(8):1286–1295. https://doi.org/10.1038/sj.bjp.0704207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Lukas RJ, Norman SA, Lucero L (1993) Characterization of nicotinic acetylcholine receptors expressed by cells of the SH-SY5Y human neuroblastoma clonal line. Mol Cell Neurosci 4(1):1–12. https://doi.org/10.1006/mcne.1993.1001

    Article  CAS  PubMed  Google Scholar 

  58. Ridley DL, Pakkanen J, Wonnacott S (2002) Effects of chronic drug treatments on increases in intracellular calcium mediated by nicotinic acetylcholine receptors in SH-SY5Y cells. Br J Pharmacol 135(4):1051–1059. https://doi.org/10.1038/sj.bjp.0704508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Vijayaraghavan S, Pugh PC, Zhang ZW, Rathouz MM, Berg DK (1992) Nicotinic receptors that bind alpha-bungarotoxin on neurons raise intracellular free Ca2+. Neuron 8(2):353–362. https://doi.org/10.1016/0896-6273(92)90301-s

    Article  CAS  PubMed  Google Scholar 

  60. Kuryatov A, Luo J, Cooper J, Lindstrom J (2005) Nicotine acts as a pharmacological chaperone to up-regulate human alpha4beta2 acetylcholine receptors. Mol Pharmacol 68(6):1839–1851. https://doi.org/10.1124/mol.105.012419

    Article  CAS  PubMed  Google Scholar 

  61. Richards CI, Srinivasan R, Xiao C, Mackey ED, Miwa JM, Lester HA (2011) Trafficking of alpha4* nicotinic receptors revealed by superecliptic phluorin: effects of a beta4 amyotrophic lateral sclerosis-associated mutation and chronic exposure to nicotine. J Biol Chem 286(36):31241–31249. https://doi.org/10.1074/jbc.M111.256024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Srinivasan R, Pantoja R, Moss FJ, Mackey ED, Son CD, Miwa J, Lester HA (2011) Nicotine up-regulates alpha4beta2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning. J Gen Physiol 137(1):59–79. https://doi.org/10.1085/jgp.201010532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Manjunath GP, Ramanujam PL, Galande S (2018) Structure function relations in PDZ-domain-containing proteins: Implications for protein networks in cellular signalling. J Biosci 43(1):155–171

    Article  CAS  Google Scholar 

  64. Christensen NR, Calyseva J, Fernandes EFA, Luchow S, Clemmensen LS, Haugaard-Kedstrom LM, Stromgaard K (2019) PDZ domains as drug targets. Adv Ther. https://doi.org/10.1002/adtp.201800143

    Article  Google Scholar 

  65. Su Y, Hiemstra TF, Yan YH, Li J, Karet HI, Rosen L, Moreno P, Frankl FEK (2017) PDLIM5 links kidney anion exchanger 1 (kAE1) to ILK and is required for membrane targeting of kAE1. Sci Rep. https://doi.org/10.1038/srep39701

    Article  PubMed  PubMed Central  Google Scholar 

  66. Drenan RM, Nashmi R, Imoukhuede P, Just H, McKinney S, Lester HA (2008) Subcellular trafficking, pentameric assembly, and subunit stoichiometry of neuronal nicotinic acetylcholine receptors containing fluorescently labeled alpha6 and beta3 subunits. Mol Pharmacol 73(1):27–41. https://doi.org/10.1124/mol.107.039180

    Article  CAS  PubMed  Google Scholar 

  67. Duffy AM, Fitzgerald ML, Chan J, Robinson DC, Milner TA, Mackie K, Pickel VM (2011) Acetylcholine alpha7 nicotinic and dopamine D2 receptors are targeted to many of the same postsynaptic dendrites and astrocytes in the rodent prefrontal cortex. Synapse 65(12):1350–1367. https://doi.org/10.1002/syn.20977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Millar NS, Harkness PC (2008) Assembly and trafficking of nicotinic acetylcholine receptors (Review). Mol Membr Biol 25(4):279–292. https://doi.org/10.1080/09687680802035675

    Article  CAS  PubMed  Google Scholar 

  69. Fanning AS, Anderson JM (1999) PDZ domains: fundamental building blocks in the organization of protein complexes at the plasma membrane. J Clin Invest 103(6):767–772. https://doi.org/10.1172/JCI6509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Farias GG, Valles AS, Colombres M, Godoy JA, Toledo EM, Lukas RJ, Barrantes FJ, Inestrosa NC (2007) Wnt-7a induces presynaptic colocalization of alpha 7-nicotinic acetylcholine receptors and adenomatous polyposis coli in hippocampal neurons. J Neurosci 27(20):5313–5325. https://doi.org/10.1523/JNEUROSCI.3934-06.2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Zoli M, Pucci S, Vilella A, Gotti C (2018) Neuronal and extraneuronal nicotinic acetylcholine receptors. Curr Neuropharmacol 16(4):338–349. https://doi.org/10.2174/1570159X15666170912110450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Fernandes CC, Berg DK, Gomez-Varela D (2010) Lateral mobility of nicotinic acetylcholine receptors on neurons is determined by receptor composition, local domain, and cell type. J Neurosci 30(26):8841–8851. https://doi.org/10.1523/JNEUROSCI.6236-09.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Revah F, Bertrand D, Galzi JL, Devillers-Thiery A, Mulle C, Hussy N, Bertrand S, Ballivet M, Changeux JP (1991) Mutations in the channel domain alter desensitization of a neuronal nicotinic receptor. Nature 353(6347):846–849. https://doi.org/10.1038/353846a0

    Article  CAS  PubMed  Google Scholar 

  74. Gay EA, Giniatullin R, Skorinkin A, Yakel JL (2008) Aromatic residues at position 55 of rat alpha7 nicotinic acetylcholine receptors are critical for maintaining rapid desensitization. J Physiol 586(4):1105–1115. https://doi.org/10.1113/jphysiol.2007.149492

    Article  CAS  PubMed  Google Scholar 

  75. Peng X, Katz M, Gerzanich V, Anand R, Lindstrom J (1994) Human alpha 7 acetylcholine receptor: cloning of the alpha 7 subunit from the SH-SY5Y cell line and determination of pharmacological properties of native receptors and functional alpha 7 homomers expressed in Xenopus oocytes. Mol Pharmacol 45(3):546–554

    CAS  PubMed  Google Scholar 

  76. Gu S, Matta JA, Lord B, Harrington AW, Sutton SW, Davini WB, Bredt DS (2016) Brain alpha7 Nicotinic Acetylcholine Receptor Assembly Requires NACHO. Neuron 89(5):948–955. https://doi.org/10.1016/j.neuron.2016.01.018

    Article  CAS  PubMed  Google Scholar 

  77. Williams ME, Burton B, Urrutia A, Shcherbatko A, Chavez-Noriega LE, Cohen CJ, Aiyar J (2005) Ric-3 promotes functional expression of the nicotinic acetylcholine receptor alpha7 subunit in mammalian cells. J Biol Chem 280(2):1257–1263. https://doi.org/10.1074/jbc.M410039200

    Article  CAS  PubMed  Google Scholar 

  78. Gopalakrishnan M, Buisson B, Touma E, Giordano T, Campbell JE, Hu IC, Donnelly-Roberts D, Arneric SP, Bertrand D, Sullivan JP (1995) Stable expression and pharmacological properties of the human alpha 7 nicotinic acetylcholine receptor. Eur J Pharmacol 290(3):237–246. https://doi.org/10.1016/0922-4106(95)00083-6

    Article  CAS  PubMed  Google Scholar 

  79. Cecon E, Dam J, Luka M, Gautier C, Chollet AM, Delagrange P, Danober L, Jockers R (2019) Quantitative assessment of oligomeric amyloid beta peptide binding to alpha7 nicotinic receptor. Br J Pharmacol 176(18):3475–3488. https://doi.org/10.1111/bph.14688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Nashmi R, Dickinson ME, McKinney S, Jareb M, Labarca C, Fraser SE, Lester HA (2003) Assembly of alpha4beta2 nicotinic acetylcholine receptors assessed with functional fluorescently labeled subunits: effects of localization, trafficking, and nicotine-induced upregulation in clonal mammalian cells and in cultured midbrain neurons. J Neurosci 23(37):11554–11567

    Article  CAS  Google Scholar 

  81. Nuutinen S, Ekokoski E, Lahdensuo E, Tuominen RK (2006) Nicotine-induced upregulation of human neuronal nicotinic alpha7-receptors is potentiated by modulation of cAMP and PKC in SH-EP1-halpha7 cells. Eur J Pharmacol 544(1–3):21–30. https://doi.org/10.1016/j.ejphar.2006.06.038

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was funded by Guangdong Nature Science Foundation (2019A1515011309), Shenzhen Science and Technology Program (JCYJ20190807155615170), and The Key Scientific and Technology Project of Guangdong Province (2018B030335001)

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  1. Neurobiology Research Center, School of Medicine, Shenzhen Campus of Sun Yat-Sen University, No. 66, Gongchang Road, Guangming District, Shenzhen, 518107, Guangdong, People’s Republic of China

    Zi-Lin Li, Wen-Hui Wang, Yu Cui & Yuan Chen

  2. Department of Anatomy and Neurobiology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzho, 510080, Guangdong, People’s Republic of China

    Chen-Yu Gou, Yuan Li & Jing-Jing Duan

  3. Guangdong Province Key Laboratory of Brain Function and Disease, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou, 510080, Guangdong, People’s Republic of China

    Jing-Jing Duan

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  1. Zi-Lin Li
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  2. Chen-Yu Gou
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  3. Wen-Hui Wang
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  4. Yuan Li
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  5. Yu Cui
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  6. Jing-Jing Duan
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  7. Yuan Chen
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Correspondence to Jing-Jing Duan or Yuan Chen.

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Li, ZL., Gou, CY., Wang, WH. et al. A novel effect of PDLIM5 in α7 nicotinic acetylcholine receptor upregulation and surface expression. Cell. Mol. Life Sci. 79, 64 (2022). https://doi.org/10.1007/s00018-021-04115-y

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  • DOI: https://doi.org/10.1007/s00018-021-04115-y

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