#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

CAMDI interacts with the human memory-associated protein KIBRA and regulates AMPAR cell surface expression and cognition


Autoři: Toshifumi Fukuda aff001;  Shun Nagashima aff001;  Ryoko Inatome aff001;  Shigeru Yanagi aff001
Působiště autorů: Laboratory of Molecular Biochemistry, School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Hachioji, Tokyo, Japan aff001
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224967

Souhrn

Little is known about the molecular mechanisms of cognitive deficits in psychiatric disorders. CAMDI is a psychiatric disorder-related factor, the deficiency of which in mice results in delayed neuronal migration and psychiatrically abnormal behaviors. Here, we found that CAMDI-deficient mice exhibited impaired recognition memory and spatial reference memory. Knockdown of CAMDI in hippocampal neurons increased the amount of internalized alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor (AMPAR) and attenuated the chemical long-term potentiation (LTP)-dependent cell surface expression of AMPAR. KIBRA was identified as a novel CAMDI-binding protein that retains AMPAR in the cytosol after internalization. KIBRA inhibited CAMDI-dependent Rab11 activation, thereby attenuating AMPAR cell surface expression. These results suggest that CAMDI regulates AMPAR cell surface expression during LTP. CAMDI dysfunction may partly explain the mechanism underlying cognitive deficits in psychiatric diseases.

Klíčová slova:

Cognitive impairment – Immunoprecipitation – Learning and memory – Memory – Mice – Neuronal dendrites – Neurons – Two-hybrid screening


Zdroje

1. Lu W, Man H, Ju W, Trimble WS, MacDonald JF, Wang YT. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron. 2001;29(1):243–54. doi: 10.1016/s0896-6273(01)00194-5 11182095.

2. Petrini EM, Lu J, Cognet L, Lounis B, Ehlers MD, Choquet D. Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron. 2009;63(1):92–105. doi: 10.1016/j.neuron.2009.05.025 19607795.

3. Lee SH, Simonetta A, Sheng M. Subunit rules governing the sorting of internalized AMPA receptors in hippocampal neurons. Neuron. 2004;43(2):221–36. doi: 10.1016/j.neuron.2004.06.015 15260958.

4. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD. Recycling endosomes supply AMPA receptors for LTP. Science. 2004;305(5692):1972–5. doi: 10.1126/science.1102026 15448273.

5. Hanley JG. Endosomal sorting of AMPA receptors in hippocampal neurons. Biochem Soc Trans. 2010;38(2):460–5. doi: 10.1042/BST0380460 20298203.

6. Lu J, Helton TD, Blanpied TA, Racz B, Newpher TM, Weinberg RJ, et al. Postsynaptic positioning of endocytic zones and AMPA receptor cycling by physical coupling of dynamin-3 to Homer. Neuron. 2007;55(6):874–89. doi: 10.1016/j.neuron.2007.06.041 17880892.

7. Braithwaite SP, Xia H, Malenka RC. Differential roles for NSF and GRIP/ABP in AMPA receptor cycling. Proc Natl Acad Sci USA. 2002;99(10):7096–101. doi: 10.1073/pnas.102156099 12011465.

8. Lu W, Ziff EB. PICK1 interacts with ABP/GRIP to regulate AMPA receptor trafficking. Neuron. 2005;47(3):407–21. doi: 10.1016/j.neuron.2005.07.006 16055064.

9. Mao L, Takamiya K, Thomas G, Lin DT, Huganir RL. GRIP1 and 2 regulate activity-dependent AMPA receptor recycling via exocyst complex interactions. Proc Natl Acad Sci USA. 2010;107(44):19038–43. doi: 10.1073/pnas.1013494107 20956289.

10. Traer CJ, Rutherford AC, Palmer KJ, Wassmer T, Oakley J, Attar N, et al. SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment. Nat Cell Biol. 2007;9(12):1370–80. doi: 10.1038/ncb1656 17994011.

11. Makuch L, Volk L, Anggono V, Johnson RC, Yu Y, Duning K, et al. Regulation of AMPA receptor function by the human memory-associated gene KIBRA. Neuron. 2011;71(6):1022–9. doi: 10.1016/j.neuron.2011.08.017 21943600.

12. Blanque A, Repetto D, Rohlmann A, Brockhaus J, Duning K, Pavenstadt H, et al. Deletion of KIBRA, protein expressed in kidney and brain, increases filopodial-like long dendritic spines in neocortical and hippocampal neurons in vivo and in vitro. Front Neuroanat. 2015;9:13. doi: 10.3389/fnana.2015.00013 25750616.

13. Fukuda T, Sugita S, Inatome R, Yanagi S. CAMDI, a novel disrupted in Schizophrenia 1 (DISC1)-binding protein, is required for radial migration. J Biol Chem. 2010;285(52):40554–61. Epub 2010/10/20. doi: 10.1074/jbc.M110.179481 20956536.

14. Fukuda T, Yanagi S. Psychiatric behaviors associated with cytoskeletal defects in radial neuronal migration. Cell Mol Life Sci. 2017;74(19):3533–52. doi: 10.1007/s00018-017-2539-4 28516224.

15. Fukuda T, Nagashima S, Abe T, Kiyonari H, Inatome R, Yanagi S. Rescue of CAMDI deletion-induced delayed radial migration and psychiatric behaviors by HDAC6 inhibitor. EMBO Rep. 2016;17(12):1785–98. doi: 10.15252/embr.201642416 27737934.

16. Tomppo L, Ekelund J, Lichtermann D, Veijola J, Jarvelin MR, Hennah W. DISC1 conditioned GWAS for psychosis proneness in a large Finnish birth cohort. PLoS One. 2012;7(2):e30643. Epub 2012/03/01. doi: 10.1371/journal.pone.0030643 22363459.

17. Ortega-Alonso A, Ekelund J, Sarin AP, Miettunen J, Veijola J, Jarvelin MR, et al. Genome-Wide Association Study of Psychosis Proneness in the Finnish Population. Schizophr Bull. 2017;43(6):1304–14. doi: 10.1093/schbul/sbx006 28525603.

18. Millan MJ, Agid Y, Brune M, Bullmore ET, Carter CS, Clayton NS, et al. Cognitive dysfunction in psychiatric disorders: characteristics, causes and the quest for improved therapy. Nat Rev Drug Discov. 2012;11(2):141–68. doi: 10.1038/nrd3628 22293568.

19. Amador-Arjona A, Elliott J, Miller A, Ginbey A, Pazour GJ, Enikolopov G, et al. Primary cilia regulate proliferation of amplifying progenitors in adult hippocampus: implications for learning and memory. J Neurosci. 2011;31(27):9933–44. doi: 10.1523/JNEUROSCI.1062-11.2011 21734285.

20. Ehlers MD. Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron. 2000;28(2):511–25. doi: 10.1016/s0896-6273(00)00129-x 11144360.

21. Casanova JE, Wang X, Kumar R, Bhartur SG, Navarre J, Woodrum JE, et al. Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol Biol Cell. 1999;10(1):47–61. doi: 10.1091/mbc.10.1.47 9880326.

22. Hammond JC, McCullumsmith RE, Funk AJ, Haroutunian V, Meador-Woodruff JH. Evidence for abnormal forward trafficking of AMPA receptors in frontal cortex of elderly patients with schizophrenia. Neuropsychopharmacology. 2010;35(10):2110–9. doi: 10.1038/npp.2010.87 20571483.

23. Kos MZ, Carless MA, Peralta J, Blackburn A, Almeida M, Roalf D, et al. Exome Sequence Data From Multigenerational Families Implicate AMPA Receptor Trafficking in Neurocognitive Impairment and Schizophrenia Risk. Schizophr Bull. 2016;42(2):288–300. doi: 10.1093/schbul/sbv135 26405221.

24. Heitz FD, Farinelli M, Mohanna S, Kahn M, Duning K, Frey MC, et al. The memory gene KIBRA is a bidirectional regulator of synaptic and structural plasticity in the adult brain. Neurobiol Learn Mem. 2016;135:100–14. doi: 10.1016/j.nlm.2016.07.028 27498008.

25. Rubio MD, Johnson R, Miller CA, Huganir RL, Rumbaugh G. Regulation of synapse structure and function by distinct myosin II motors. J Neurosci. 2011;31(4):1448–60. doi: 10.1523/JNEUROSCI.3294-10.2011 21273429.

26. Hanley JG. Actin-dependent mechanisms in AMPA receptor trafficking. Front Cell Neurosci. 2014;8:381. doi: 10.3389/fncel.2014.00381 25429259.

27. Papassotiropoulos A, Stephan DA, Huentelman MJ, Hoerndli FJ, Craig DW, Pearson JV, et al. Common Kibra alleles are associated with human memory performance. Science. 2006;314(5798):475–8. doi: 10.1126/science.1129837 17053149.

28. Lin DT, Huganir RL. PICK1 and phosphorylation of the glutamate receptor 2 (GluR2) AMPA receptor subunit regulates GluR2 recycling after NMDA receptor-induced internalization. J Neurosci. 2007;27(50):13903–8. doi: 10.1523/JNEUROSCI.1750-07.2007 18077702.

29. Citri A, Bhattacharyya S, Ma C, Morishita W, Fang S, Rizo J, et al. Calcium binding to PICK1 is essential for the intracellular retention of AMPA receptors underlying long-term depression. J Neurosci. 2010;30(49):16437–52. doi: 10.1523/JNEUROSCI.4478-10.2010 21147983.

30. Ling DS, Benardo LS, Sacktor TC. Protein kinase Mzeta enhances excitatory synaptic transmission by increasing the number of active postsynaptic AMPA receptors. Hippocampus. 2006;16(5):443–52. doi: 10.1002/hipo.20171 16463388.

31. Yao Y, Kelly MT, Sajikumar S, Serrano P, Tian D, Bergold PJ, et al. PKM zeta maintains late long-term potentiation by N-ethylmaleimide-sensitive factor/GluR2-dependent trafficking of postsynaptic AMPA receptors. J Neurosci. 2008;28(31):7820–7. doi: 10.1523/JNEUROSCI.0223-08.2008 18667614.

32. Buther K, Plaas C, Barnekow A, Kremerskothen J. KIBRA is a novel substrate for protein kinase Czeta. Biochem Biophys Res Commun. 2004;317(3):703–7. doi: 10.1016/j.bbrc.2004.03.107 15081397.


Článek vyšel v časopise

PLOS One


2019 Číslo 11
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#