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Utilities of Isolated Nerve Terminals in Ex Vivo Analyses of Protein Translation in (Patho)physiological Brain States: Focus on Alzheimer’s Disease

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Abstract

Synapses are the cellular substrates of higher-order brain functions, and their dysfunction is an early and primary pathogenic mechanism across several neurological disorders. In particular, Alzheimer’s disease (AD) is categorized by prodromal structural and functional synaptic deficits, prior to the advent of classical behavioral and pathological features. Recent research has shown that the development, maintenance, and plasticity of synapses depend on localized protein translation. Synaptosomes and synaptoneurosomes are biochemically isolated synaptic terminal preparations which have long been used to examine a variety of synaptic processes ex vivo in both healthy and pathological conditions. These ex vivo preparations preserve the mRNA species and the protein translational machinery. Hence, they are excellent in organello tools for the study of alterations in mRNA levels and protein translation in neuropathologies. Evaluation of synapse-specific basal and activity-driven de novo protein translation activity can be conveniently performed in synaptosomal/synaptoneurosomal preparations from both rodent and human brain tissue samples. This review gives a quick overview of the methods for isolating synaptosomes and synaptoneurosomes before discussing the studies that have utilized these preparations to study localized synapse-specific protein translation in (patho)physiological situations, with an emphasis on AD. While the review is not an exhaustive accumulation of all the studies evaluating synaptic protein translation using the synaptosomal model, the aim is to assemble the most relevant studies that have done so. The hope is to provide a suitable research platform to aid neuroscientists to utilize the synaptosomal/synaptoneurosomal models to evaluate the molecular mechanisms of synaptic dysfunction within the specific confines of mRNA localization and protein translation research.

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References

  1. Lepeta K, Lourenco MV, Schweitzer BC et al (2016) Synaptopathies: synaptic dysfunction in neurological disorders - a review from students to students. J Neurochem 138:785–805. https://doi.org/10.1111/jnc.13713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. van Spronsen M, Hoogenraad CC (2010) Synapse pathology in psychiatric and neurologic disease. Curr Neurol Neurosci Rep 10:207–214. https://doi.org/10.1007/s11910-010-0104-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Harris KP, Littleton JT (2015) Transmission, development, and plasticity of synapses. Genetics 201:345–375. https://doi.org/10.1534/genetics.115.176529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Ahmad F, Haque S, Chavda V, Ashraf GM (2021) Recent advances in synaptosomal proteomics in Alzheimer’s disease. Curr Protein Pept Sci 22:479–492. https://doi.org/10.2174/1389203722666210618110233

    Article  CAS  PubMed  Google Scholar 

  5. Murphy KM (2018) Synaptosomes. Springer New York, New York

    Book  Google Scholar 

  6. Ahmad F, Liu P (2020) Synaptosome as a tool in Alzheimer’s disease research. Brain Res 1746:147009. https://doi.org/10.1016/j.brainres.2020.147009

    Article  CAS  PubMed  Google Scholar 

  7. Jhou J-F, Tai H-C (2017) The study of postmortem human synaptosomes for understanding Alzheimer’s Disease and other neurological disorders: a review. Neurol Ther 6:57–68. https://doi.org/10.1007/s40120-017-0070-z

    Article  PubMed  PubMed Central  Google Scholar 

  8. Crispino M, Chun JT, Cefaliello C et al (2014) Local gene expression in nerve endings. Dev Neurobiol 74:279–291. https://doi.org/10.1002/dneu.22109

    Article  CAS  PubMed  Google Scholar 

  9. Kuzniewska B, Chojnacka M, Milek J, Dziembowska M (2018) Preparation of polysomal fractions from mouse brain synaptoneurosomes and analysis of polysomal-bound mRNAs. J Neurosci Methods 293:226–233. https://doi.org/10.1016/j.jneumeth.2017.10.006

    Article  CAS  PubMed  Google Scholar 

  10. Jeong S (2017) Molecular and cellular basis of neurodegeneration in Alzheimer’s disease. Mol Cells 40:613–620. https://doi.org/10.14348/molcells.2017.0096

  11. Wang J, Jin C, Zhou J et al (2023) PET molecular imaging for pathophysiological visualization in Alzheimer’s disease. Eur J Nucl Med Mol Imaging 50:765–783. https://doi.org/10.1007/s00259-022-05999-z

    Article  PubMed  Google Scholar 

  12. Hane FT, Robinson M, Lee BY et al (2017) Recent progress in Alzheimer’s disease research, part 3: diagnosis and treatment. J Alzheimer’s Dis 57:645–665. https://doi.org/10.3233/JAD-160907

    Article  Google Scholar 

  13. John A, Reddy PH (2021) Synaptic basis of Alzheimer’s disease: focus on synaptic amyloid beta. P-tau and mitochondria. Ageing Res Rev 65:101208. https://doi.org/10.1016/j.arr.2020.101208

    Article  CAS  PubMed  Google Scholar 

  14. Selkoe DJ (2002) Alzheimer’s disease is a synaptic failure. Science (80- ) 298:789–791. https://doi.org/10.1126/science.1074069

  15. Lin JQ, van Tartwijk FW, Holt CE (2021) Axonal mRNA translation in neurological disorders. RNA Biol 18:936–961. https://doi.org/10.1080/15476286.2020.1822638

    Article  CAS  PubMed  Google Scholar 

  16. Holt CE, Martin KC, Schuman EM (2019) Local translation in neurons: visualization and function. Nat Struct Mol Biol 26:557–566. https://doi.org/10.1038/s41594-019-0263-5

    Article  CAS  PubMed  Google Scholar 

  17. Gamarra M, de la Cruz A, Blanco-Urrejola M, Baleriola J (2021) Local translation in nervous system pathologies. Front Integr Neurosci 15:479–492. https://doi.org/10.3389/fnint.2021.689208

    Article  CAS  Google Scholar 

  18. Khalil B, Morderer D, Price PL et al (2018) mRNP assembly, axonal transport, and local translation in neurodegenerative diseases. Brain Res 1693:75–91. https://doi.org/10.1016/j.brainres.2018.02.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Steward O, Schuman EM (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24:299–325. https://doi.org/10.1146/annurev.neuro.24.1.299

    Article  CAS  PubMed  Google Scholar 

  20. Biever A, Donlin-Asp PG, Schuman EM (2019) Local translation in neuronal processes. Curr Opin Neurobiol 57:141–148. https://doi.org/10.1016/j.conb.2019.02.008

    Article  CAS  PubMed  Google Scholar 

  21. Rangaraju V, tom Dieck S, Schuman EM (2017) Local translation in neuronal compartments: how local is local? EMBO Rep 18:693–711. https://doi.org/10.15252/embr.201744045

  22. Joo Y, Benavides DR (2021) Local protein translation and RNA processing of synaptic proteins in autism spectrum disorder. Int J Mol Sci 22:2811. https://doi.org/10.3390/ijms22062811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Verity MA, Brown WJ, Cheung M (1980) Isolation of ribosome containing synaptosome subpopulation with active in vitro protein synthesis. J Neurosci Res 5:143–153. https://doi.org/10.1002/jnr.490050206

    Article  CAS  PubMed  Google Scholar 

  24. Weiler IJ, Hawrylak N, Greenough WT (1995) Morphogenesis in memory formation: synaptic and cellular mechanisms. Behav Brain Res 66:1–6. https://doi.org/10.1016/0166-4328(94)00116-W

    Article  CAS  PubMed  Google Scholar 

  25. Gharami K, Das S (2014) BDNF local translation in viable synaptosomes: implication in spine maturation. Neurochem Int 69:28–34. https://doi.org/10.1016/j.neuint.2014.02.009

    Article  CAS  PubMed  Google Scholar 

  26. Iliff AJ, Renoux AJ, Krans A et al (2013) Impaired activity-dependent FMRP translation and enhanced mGluR-dependent LTD in fragile X premutation mice. Hum Mol Genet 22:1180–1192. https://doi.org/10.1093/hmg/dds525

    Article  CAS  PubMed  Google Scholar 

  27. Takei N, Inamura N, Kawamura M et al (2004) Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J Neurosci 24:9760–9769. https://doi.org/10.1523/JNEUROSCI.1427-04.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Claasen AM, Guévremont D, Mason-Parker SE et al (2009) Secreted amyloid precursor protein-α upregulates synaptic protein synthesis by a protein kinase G-dependent mechanism. Neurosci Lett 460:92–96. https://doi.org/10.1016/j.neulet.2009.05.040

    Article  CAS  PubMed  Google Scholar 

  29. Bernard C, Exposito-Alonso D, Selten M, et al. (2022) Cortical wiring by synapse type–specific control of local protein synthesis. Science (80- ) 378:eabm7466. https://doi.org/10.1126/science.abm7466

  30. Hegde AN, Smith SG (2019) Recent developments in transcriptional and translational regulation underlying long-term synaptic plasticity and memory. Learn Mem 26:307–317. https://doi.org/10.1101/lm.048769.118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Sutton MA, Schuman EM (2006) Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127:49–58. https://doi.org/10.1016/j.cell.2006.09.014

    Article  CAS  PubMed  Google Scholar 

  32. Choe HK, Cho J (2020) Comprehensive genome-wide approaches to activity-dependent translational control in neurons. Int J Mol Sci 21:1592. https://doi.org/10.3390/ijms21051592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ahmad F, Singh K, Das D et al (2017) Reactive oxygen species-mediated loss of synaptic Akt1 signaling leads to deficient activity-dependent protein translation early in Alzheimer’s disease. Antioxid Redox Signal 27:1269–1280. https://doi.org/10.1089/ars.2016.6860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ahmad F, Salahuddin M, Alsamman K et al (2018) Developmental lead (Pb)-induced deficits in hippocampal protein translation at the synapses are ameliorated by ascorbate supplementation. Neuropsychiatr Dis Treat 14:3289–3298. https://doi.org/10.2147/NDT.S174083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Ahmad F, Salahuddin M, Alsamman K, et al. (2018) Neonatal maternal deprivation impairs localized de novo activity-induced protein translation at the synapse in the rat hippocampus. Biosci Rep 38. https://doi.org/10.1042/BSR20180118

  36. Whittaker VP (1988) Synaptosome preparations. J Neurochem 50:324–325. https://doi.org/10.1111/j.1471-4159.1988.tb13270.x

    Article  CAS  PubMed  Google Scholar 

  37. Chang JW, Arnold MM, Rozenbaum A et al (2012) Synaptoneurosome micromethod for fractionation of mouse and human brain, and primary neuronal cultures. J Neurosci Methods 211:289–295. https://doi.org/10.1016/j.jneumeth.2012.09.005

    Article  PubMed  Google Scholar 

  38. Johnson MW, Chotiner JK, Watson JB (1997) Isolation and characterization of synaptoneurosomes from single rat hippocampal slices. J Neurosci Methods 77:151–156. https://doi.org/10.1016/S0165-0270(97)00120-9

    Article  CAS  PubMed  Google Scholar 

  39. Villasana LE, Klann E, Tejada-Simon MV (2006) Rapid isolation of synaptoneurosomes and postsynaptic densities from adult mouse hippocampus. J Neurosci Methods 158:30–36. https://doi.org/10.1016/j.jneumeth.2006.05.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Cefaliello C, Eyman M, Melck D et al (2014) Brain synaptosomes harbor more than one cytoplasmic system of protein synthesis. J Neurosci Res 92:1573–1580. https://doi.org/10.1002/jnr.23435

    Article  CAS  PubMed  Google Scholar 

  41. Troca-Marín JA, Alves-Sampaio A, Tejedor FJ, Montesinos ML (2010) Local translation of dendritic RhoA revealed by an improved synaptoneurosome preparation. Mol Cell Neurosci 43:308–314. https://doi.org/10.1016/j.mcn.2009.12.004

    Article  CAS  PubMed  Google Scholar 

  42. Williams C, MehrianShai R, Wu Y et al (2009) Transcriptome analysis of synaptoneurosomes identifies neuroplasticity genes overexpressed in incipient Alzheimer’s disease. PLoS One 4:e4936. https://doi.org/10.1371/journal.pone.0004936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Schmidt EK, Clavarino G, Ceppi M, Pierre P (2009) SUnSET, a nonradioactive method to monitor protein synthesis. Nat Methods 6:275–277. https://doi.org/10.1038/nmeth.1314

    Article  CAS  PubMed  Google Scholar 

  44. Pasciuto E, Ahmed T, Wahle T et al (2015) Dysregulated ADAM10-mediated processing of APP during a critical time window leads to synaptic deficits in fragile X syndrome. Neuron 87:382–398. https://doi.org/10.1016/j.neuron.2015.06.032

    Article  CAS  PubMed  Google Scholar 

  45. Aviner R, Geiger T, Elroy-Stein O (2014) Genome-wide identification and quantification of protein synthesis in cultured cells and whole tissues by puromycin-associated nascent chain proteomics (PUNCH-P). Nat Protoc 9:751–760. https://doi.org/10.1038/nprot.2014.051

    Article  CAS  PubMed  Google Scholar 

  46. Shi H, Zhang X, Weng Y-L et al (2018) m6A facilitates hippocampus-dependent learning and memory through YTHDF1. Nature 563:249–253. https://doi.org/10.1038/s41586-018-0666-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Wang W, Wang L, Lu J et al (2016) The inhibition of TDP-43 mitochondrial localization blocks its neuronal toxicity. Nat Med 22:869–878. https://doi.org/10.1038/nm.4130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Cefaliello C, Penna E, Barbato C et al (2020) Deregulated local protein synthesis in the brain synaptosomes of a mouse model for Alzheimer’s disease. Mol Neurobiol 57:1529–1541. https://doi.org/10.1007/s12035-019-01835-y

    Article  CAS  PubMed  Google Scholar 

  49. Goldberg MA (1970) Protein synthesis in isolated nerve endings and brain mitochondria. Neurology 20:404. https://doi.org/10.1038/s41598-018-31073-6

    Article  CAS  PubMed  Google Scholar 

  50. Deanin GG, Gordon MW (1973) Chloramphenicol- and cycloheximide-sensitive protein synthetic systems in brain mitochondrial and nerve-ending preparations. J Neurochem 20:55–68. https://doi.org/10.1111/j.1471-4159.1973.tb12104.x

    Article  CAS  PubMed  Google Scholar 

  51. Hernández AG (1974) Protein synthesis by synaptosomes from rat brain. Contribution by the intraterminal mitochondria. Biochem J 142:7–17. https://doi.org/10.1042/bj1420007

    Article  PubMed  PubMed Central  Google Scholar 

  52. Martin R, Vaida B, Bleher R et al (1998) Protein synthesizing units in presynaptic and postsynaptic domains of squid neurons. J Cell Sci 111:3157–3166. https://doi.org/10.1242/jcs.111.21.3157

    Article  CAS  PubMed  Google Scholar 

  53. Crispino M, Castigli E, Perrone Capano C et al (1993) Protein synthesis in a synaptosomal fraction from squid brain. Mol Cell Neurosci 4:366–374. https://doi.org/10.1006/mcne.1993.1046

    Article  CAS  PubMed  Google Scholar 

  54. Huang YS, Richter JD (2007) Analysis of mRNA translation in cultured hippocampal neurons. Methods Enzymol 431:143–62. https://doi.org/10.1016/S0076-6879(07)31008-2

    Article  CAS  PubMed  Google Scholar 

  55. Claudio Benech J, Crispino M, Kaplan BB, Giuditta A (1999) Protein synthesis in presynaptic endings from squid brain: modulation by calcium ions. J Neurosci Res 55:776–781. https://doi.org/10.1002/(SICI)1097-4547(19990315)55:6%3c776::AID-JNR12%3e3.0.CO;2-1

    Article  Google Scholar 

  56. Gioio AE, Eyman M, Zhang H et al (2001) Local synthesis of nuclear-encoded mitochondrial proteins in the presynaptic nerve terminal. J Neurosci Res 64:447–453. https://doi.org/10.1002/jnr.1096

    Article  CAS  PubMed  Google Scholar 

  57. Gioio AE, Lavina ZS, Jurkovicova D et al (2004) Nerve terminals of squid photoreceptor neurons contain a heterogeneous population of mRNAs and translate a transfected reporter mRNA. Eur J Neurosci 20:865–872. https://doi.org/10.1111/j.1460-9568.2004.03538.x

    Article  PubMed  Google Scholar 

  58. Eyman M, Cefaliello C, Bruno A et al (2012) Synaptosomal protein synthesis in P2 and Ficoll purified fractions. J Neurosci Methods 203:335–337. https://doi.org/10.1016/j.jneumeth.2011.10.007

    Article  CAS  PubMed  Google Scholar 

  59. Eyman M, Cefaliello C, Ferrara E et al (2007) Synaptosomal protein synthesis is selectively modulated by learning. Brain Res 1132:148–157. https://doi.org/10.1016/j.brainres.2006.11.025

    Article  CAS  PubMed  Google Scholar 

  60. Eyman M, Cefaliello C, Mandile P, Piscopo S, Crispino M, Giuditta A (2013) Training old rats selectively modulates synaptosomal protein synthesis. J Neurosci Res. 91(1):20–9. https://doi.org/10.1002/jnr.23133

    Article  CAS  PubMed  Google Scholar 

  61. Ferrara E, Cefaliello C, Eyman M et al (2009) Synaptic mRNAs are modulated by learning. J Neurosci Res 87:1960–1968. https://doi.org/10.1002/jnr.22037

    Article  CAS  PubMed  Google Scholar 

  62. Leski ML, Steward O (1996) Protein synthesis within dendrites: ionic and neurotransmitter modulation of synthesis of particular polypeptides characterized by gel electrophoresis. Neurochem Res 21:681–690. https://doi.org/10.1007/BF02527725

    Article  CAS  PubMed  Google Scholar 

  63. Rao A, Steward O (1991) Evidence that protein constituents of postsynaptic membrane specializations are locally synthesized: analysis of proteins synthesized within synaptosomes. J Neurosci 11:2881–2895. https://doi.org/10.1523/JNEUROSCI.11-09-02881.1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Villanueva S, Steward O (2001) Protein synthesis at the synapse: developmental changes, subcellular localization and regional distribution of polypeptides synthesized in isolated dendritic fragments. Mol Brain Res 91:148–153. https://doi.org/10.1016/S0169-328X(01)00131-0

    Article  CAS  PubMed  Google Scholar 

  65. Villanueva S, Steward O (2001) Glycoprotein synthesis at the synapse: fractionation of polypeptides synthesized within isolated dendritic fragments by concanavalin A affinity chromatography. Mol Brain Res 91:137–147. https://doi.org/10.1016/S0169-328X(01)00132-2

    Article  CAS  PubMed  Google Scholar 

  66. Steward O, Pollack A, Rao A (1991) Evidence that protein constituents of postsynaptic membrane specializations are locally synthesized: time course of appearance of recently synthesized proteins in synaptic junctions. J Neurosci Res 30:649–660. https://doi.org/10.1002/jnr.490300408

    Article  CAS  PubMed  Google Scholar 

  67. Bagni C, Mannucci L, Dotti CG, Amaldi F (2000) Chemical stimulation of synaptosomes modulates α-Ca 2+/calmodulin-dependent protein kinase II mRNA association to polysomes. J Neurosci 20:RC76–RC76. https://doi.org/10.1523/JNEUROSCI.20-10-j0004.2000

  68. Scheetz AJ, Nairn AC, Constantine-Paton M (2000) NMDA receptor-mediated control of protein synthesis at developing synapses. Nat Neurosci 3:211–216. https://doi.org/10.1038/72915

    Article  CAS  PubMed  Google Scholar 

  69. Jin C, Lee Y, Kang H et al (2021) Increased ribosomal protein levels and protein synthesis in the striatal synaptosome of Shank3-overexpressing transgenic mice. Mol Brain 14:39. https://doi.org/10.1186/s13041-021-00756-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Jiménez CR, Eyman M, Lavina ZS et al (2002) Protein synthesis in synaptosomes: a proteomics analysis. J Neurochem 81:735–744. https://doi.org/10.1046/j.1471-4159.2002.00873.x

    Article  PubMed  Google Scholar 

  71. Chicurel M, Terrian D, Potter H (1993) mRNA at the synapse: analysis of a synaptosomal preparation enriched in hippocampal dendritic spines. J Neurosci 13:4054–4063. https://doi.org/10.1523/JNEUROSCI.13-09-04054.1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Simbriger K, Amorim IS, Chalkiadaki K et al (2020) Monitoring translation in synaptic fractions using a ribosome profiling strategy. J Neurosci Methods 329:108456. https://doi.org/10.1016/j.jneumeth.2019.108456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Muddashetty RS, Kelić S, Gross C et al (2007) Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of fragile X syndrome. J Neurosci 27:5338–5348. https://doi.org/10.1523/JNEUROSCI.0937-07.2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Kuzniewska B, Cysewski D, Wasilewski M et al. (2020) Mitochondrial protein biogenesis in the synapse is supported by local translation. EMBO Rep 21. https://doi.org/10.15252/embr.201948882

  75. Mariucci G, Tantucci M, Giuditta A, Ambrosini MV (2007) Permanent brain ischemia induces marked increments in hsp72 expression and local protein synthesis in synapses of the ischemic hemisphere. Neurosci Lett 415:77–80. https://doi.org/10.1016/j.neulet.2006.12.047

    Article  CAS  PubMed  Google Scholar 

  76. Muddashetty RS, Nalavadi VC, Gross C et al (2011) Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol Cell 42:673–688. https://doi.org/10.1016/j.molcel.2011.05.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Kommaddi RP, Gowaikar R, Singh K et al (2023) Down regulation of Akt/mTOR signaling pathway proteins in hippocampus of Alzheimer’s disease mouse model. Alzheimer’s Dement 19:e064101. https://doi.org/10.1002/alz.064101

    Article  Google Scholar 

  78. Kommaddi RP, Diwakar L, Gowaikar R et al (2022) Sex-specific differences in cognitive functions and synaptic dysfunction in an Alzheimer’s disease mouse model. Alzheimer’s Dement 17:e052825. https://doi.org/10.1002/alz.064101

    Article  Google Scholar 

  79. Borreca A, Gironi K, Amadoro G, Ammassari-Teule M (2016) Opposite dysregulation of fragile-X mental retardation protein and heteronuclear ribonucleoprotein C protein associates with enhanced APP translation in Alzheimer disease. Mol Neurobiol 53:3227–3234. https://doi.org/10.1007/s12035-015-9229-8

    Article  CAS  PubMed  Google Scholar 

  80. Perrone-Capano C, Volpicelli F, Penna E et al (2021) Presynaptic protein synthesis and brain plasticity: from physiology to neuropathology. Prog Neurobiol 202:102051. https://doi.org/10.1016/j.pneurobio.2021.102051

    Article  CAS  PubMed  Google Scholar 

  81. Sidorov MS, Auerbach BD, Bear MF (2013) Fragile X mental retardation protein and synaptic plasticity. Mol Brain 6:15. https://doi.org/10.1186/1756-6606-6-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Laguesse S, Ron D (2020) Protein translation and psychiatric disorders. Neurosci 26:21–42. https://doi.org/10.1177/1073858419853236

    Article  Google Scholar 

  83. Borreca A, Latina V, Corsetti V et al (2018) AD-related N-terminal truncated tau is sufficient to recapitulate in vivo the early perturbations of human neuropathology: implications for immunotherapy. Mol Neurobiol 55:8124–8153. https://doi.org/10.1007/s12035-018-0974-3

    Article  CAS  PubMed  Google Scholar 

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Funding

The author FA thanks Vellore Institute of Technology, Vellore, for providing “VIT SEED Grant–RGEMS Fund (Sanction Order No. SG20220054)” for carrying out this research work.

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Authors and Affiliations

  1. Department of Biotechnology, Vellore Institute of Technology, Vellore, Tamil Nadu, India, 632014

    Mohammad Jasim Ibrahim, Viswanath Baiju, Shivam Sen, Pranav Prathapa Chandran & Faraz Ahmad

  2. University of Sharjah, College of Health Sciences, and Research Institute for Medical and Health Sciences, Department of Medical Laboratory Sciences, University City, 27272, Sharjah, United Arab Emirates

    Ghulam Md Ashraf

  3. Research and Scientific Studies Unit, College of Nursing and Allied Health Sciences, Jazan University, 45142, Jazan, Saudi Arabia

    Shafiul Haque

  4. Gilbert and Rose-Marie Chagoury School of Medicine, Lebanese American University, Beirut, Lebanon

    Shafiul Haque

  5. Centre of Medical and Bio-Allied Health Sciences Research, Ajman University, Ajman, United Arab Emirates

    Shafiul Haque

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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Ghulam Md. Ashraf, Shafiul Haque, and Faraz Ahmad. The first draft of the manuscript was written by Mohammad Jasim Ibrahim, Viswanath Baiju, Shivam Sen, and Pranav Prathapa Chandran, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Ibrahim, M.J., Baiju, V., Sen, S. et al. Utilities of Isolated Nerve Terminals in Ex Vivo Analyses of Protein Translation in (Patho)physiological Brain States: Focus on Alzheimer’s Disease. Mol Neurobiol 61, 91–103 (2024). https://doi.org/10.1007/s12035-023-03562-x

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