Hippocampal synaptic dysregulation of exo/endocytosis-associated proteins induced in a chronic mild-stressed rat model

Neuroscience

Volumn 230, Issue , 2013, Pages 1-12

  Hu, Y ^a,b   Zhou, J ^a   Fang, L ^a   Liu, H ^a   Zhan, Q ^c   Luo, D ^a   Zhou, C ^a   Chen, J ^a   Li, Q ^a   Xie, P ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

^b Third People's Hospital of Chengdu   (China)

^c The Fifth People's Hospital of Chongqing   (China)

Author keywords

Chronic mild stress; Hippocampus; Major depressive disorder; Proteomics; Synaptosome; Two dimensional gel electrophoresis

Indexed keywords

CELL PROTEIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC STRESS; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; DISEASE ASSOCIATION; DISEASE SEVERITY; DOWN REGULATION; ENDOCYTOSIS; EXOCYTOSIS; HIPPOCAMPUS; MAJOR DEPRESSION; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NERVE CELL PLASTICITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEOMICS; RAT; SYNAPTIC TRANSMISSION; SYNAPTOSOME; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION; VALIDATION PROCESS; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; DEPRESSION; DISEASE MODELS, ANIMAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENDOCYTOSIS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MALE; MEMBRANE PROTEINS; PROTEOMICS; QA-SNARE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STRESS, PSYCHOLOGICAL; SYNAPSES; SYNAPTOSOMES; TIME FACTORS;

EID: 84871359300     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.08.026     Document Type: Article

References (75)

1. Abul-Husn N.S., Bushlin I., Moron J.A., Jenkins S.L., Dolios G., Wang R., Iyengar R., Ma'ayan A., Devi L.A. Systems approach to explore components and interactions in the presynapse. Proteomics 2009, 9:3303-3315.
2. Ammon S., Mayer P., Riechert U., Tischmeyer H., Hollt V. Microarray analysis of genes expressed in the frontal cortex of rats chronically treated with morphine and after naloxone precipitated withdrawal. Brain Res Mol Brain Res 2003, 112:113-125.
3. Anisman H., Merali Z., Hayley S. Neurotransmitter, peptide and cytokine processes in relation to depressive disorder: comorbidity between depression and neurodegenerative disorders. Prog Neurobiol 2008, 85:1-74.
4. Beasley C.L., Pennington K., Behan A., Wait R., Dunn M.J., Cotter D. Proteomic analysis of the anterior cingulate cortex in the major psychiatric disorders: evidence for disease-associated changes. Proteomics 2006, 6:3414-3425.
5. Belmaker R.H., Agam G. Mechanisms of disease: major depressive disorder. N Engl J Med 2008, 358:55-68.
6. Bown C., Wang J.F., MacQueen G., Young L.T. Increased temporal cortex ER stress proteins in depressed subjects who died by suicide. Neuropsychopharmacology 2000, 22:327-332.
7. Brambilla P., Perez J., Barale F., Schettini G., Soares J.C. GABAergic dysfunction in mood disorders. Mol Psychiatry 2003, 8:721-737. 715.
8. Campbell S., Macqueen G. The role of the hippocampus in the pathophysiology of major depression. J Psychiatry Neurosci 2004, 29:417-426.
9. Carboni L., Piubelli C., Pozzato C., Astner H., Arban R., Righetti P.G., Hamddan M., Domenici E. Proteomic analysis of rat hippocampus after repeated psychosocial stress. Neuroscience 2006, 137:1237-1246.
10. Carlin R.K., Grab D.J., Cohen R.S., Siekevitz P. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol 1980, 86:831-845.
11. Carro E. Gelsolin as therapeutic target in Alzheimer's disease. Expert Opin Ther Targets 2010, 14:585-592.
12. Carroll R.C., Beattie E.C., Xia H., Luscher C., Altschuler Y., Nicoll R.A., Malenka R.C., von Z.M. Dynamin-dependent endocytosis of ionotropic glutamate receptors. Proc Natl Acad Sci U S A 1999, 96:14112-14117.
13. Carroll R.C., Beattie E.C., von Z.M., Malenka R.C. Role of AMPA receptor endocytosis in synaptic plasticity. Nat Rev Neurosci 2001, 2:315-324.
14. Chauhan V., Ji L., Chauhan A. Anti-amyloidogenic, anti-oxidant and anti-apoptotic role of gelsolin in Alzheimer's disease. Biogerontology 2008, 9:381-389.
15. Collingridge G.L., Isaac J.T., Wang Y.T. Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 2004, 5:952-962.
16. Collins M.O., Husi H., Yu L., Brandon J.M., Anderson C.N., Blackstock W.P., Choudhary J.S., Grant S.G. Molecular characterization and comparison of the components and multiprotein complexes in the postsynaptic proteome. J Neurochem 2006, 97(Suppl. 1):16-23.
17. Dickson T.C., Chuckowree J.A., Chuah M.I., West A.K., Vickers J.C. Alpha-internexin immunoreactivity reflects variable neuronal vulnerability in Alzheimer's disease and supports the role of the beta-amyloid plaques in inducing neuronal injury. Neurobiol Dis 2005, 18:286-295.
18. Elfving B., Bonefeld B.E., Rosenberg R., Wegener G. Differential expression of synaptic vesicle proteins after repeated electroconvulsive seizures in rat frontal cortex and hippocampus. Synapse 2008, 62:662-670.
19. Ertunc M., Sara Y., Chung C., Atasoy D., Virmani T., Kavalali E.T. Fast synaptic vesicle reuse slows the rate of synaptic depression in the CA1 region of hippocampus. J Neurosci 2007, 27:341-354.
20. Ferguson S.M., Brasnjo G., Hayashi M., Wolfel M., Collesi C., Giovedi S., Raimondi A., Gong L.W., Ariel P., Paradise S., O'toole E., Flavell R., Cremona O., Miesenbock G., Ryan T.A., De Camilli P. A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 2007, 316:570-574.
21. Fernandez E., Collins M.O., Uren R.T., Kopanitsa M.V., Komiyama N.H., Croning M.D.D., Zografos L., Armstrong J.D., Choudhary J.S., Grant S.G. Targeted tandem affinity purification of PSD-95 recovers core postsynaptic complexes and schizophrenia susceptibility proteins. Mol Syst Biol 2009, 5. 10.1038/msb.2009.27.
22. Gitler D., Cheng Q., Greengard P., Augustine G.J. Synapsin IIa controls the reserve pool of glutamatergic synaptic vesicles. J Neurosci 2008, 28:10835-10843.
23. Granseth B., Odermatt B., Royle S.J., Lagnado L. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 2006, 51:773-786.
24. Grippo A.J., Moffitt J.A., Johnson A.K. Cardiovascular alterations and autonomic imbalance in an experimental model of depression. Am J Physiol Regul Integr Comp Physiol 2002, 282:R1333-R1341.
25. Guix F.X., Ill-Raga G., Bravo R., Nakaya T., de Fabritiis G., Coma M., Miscione G.P., Villa-Freixa J., Suzuki T., Fernandez-Busquets X., Valverde M.A., de Strooper B., Munoz F.J. Amyloid-dependent triosephosphate isomerase nitrotyrosination induces glycation and tau fibrillation. Brain 2009, 132:1335-1345.
26. Haass C., Capell A., Citron M., Teplow D.B., Selkoe D.J. The vacuolar H(+)-ATPase inhibitor bafilomycin A1 differentially affects proteolytic processing of mutant and wild-type beta-amyloid precursor protein. J Biol Chem 1995, 270:6186-6192.
27. Holderbach R., Clark K., Moreau J.L., Bischofberger J., Normann C. Enhanced long-term synaptic depression in an animal model of depression. Biol Psychiatry 2007, 62:92-100.
28. Holm M.M., Nieto-Gonzalez J.L., Vardya I., Henningsen K., Jayatissa M.N., Wiborg O., Jensen K. Hippocampal GABAergic dysfunction in a rat chronic mild stress model of depression. Hippocampus 2011, 21:422-433.
29. Huang Y., Man H.Y., Sekine-Aizawa Y., Han Y., Juluri K., Luo H., Cheah J., Lowenstein C., Huganir R.L., Snyder S.H. S-Nitrosylation of N-ethylmaleimide sensitive factor mediates surface expression of AMPA receptors. Neuron 2005, 46:533-540.
30. Humeau Y., Doussau F., Vitiello F., Greengard P., Benfenati F., Poulain B. Synapsin controls both reserve and releasable synaptic vesicle pools during neuronal activity and short-term plasticity in Aplysia. J Neurosci 2001, 21:4195-4206.
31. Imai C., Sugai T., Iritani S., Niizato K., Nakamura R., Makifuchi T., Kakita A., Takahashi H., Nawa H. A quantitative study on the expression of synapsin II and N-ethylmaleimide-sensitive fusion protein in schizophrenic patients. Neurosci Lett 2001, 305:185-188.
32. Imaizumi K., Miyoshi K., Katayama T., Yoneda T., Taniguchi M., Kudo T., Tohyama M. The unfolded protein response and Alzheimer's disease. Biochim Biophys Acta 2001, 1536:85-96.
33. Johnston-Wilson N.L., Sims C.D., Hofmann J.P., Anderson L., Shore A.D., Torrey E.F., Yolken R.H. Disease-specific alterations in frontal cortex brain proteins in schizophrenia, bipolar disorder, and major depressive disorder. The Stanley Neuropathology Consortium. Mol Psychiatry 2000, 5:142-149.
34. Kakiuchi C., Ishiwata M., Nanko S., Kunugi H., Minabe Y., Nakamura K., Mori N., Fujii K., Umekage T., Tochigi M., Kohda K., Sasaki T., Yamada K., Yoshikawa T., Kato T. Association analysis of HSP90B1 with bipolar disorder. J Hum Genet 2007, 52:794-803.
35. Kawasaki F., Iyer J., Posey L.L., Sun C.E., Mammen S.E., Yan H., Ordway R.W. The DISABLED protein functions in CLATHRIN-mediated synaptic vesicle endocytosis and exoendocytic coupling at the active zone. Proc Natl Acad Sci U S A 2011, 108:E222-E229.
36. Kedracka-Krok S., Fic E., Jankowska U., Jaciuk M., Gruca P., Papp M., Kusmider M., Solich J., Debski J., Dadlez M., Dziedzicka-Wasylewska M. Effect of chronic mild stress and imipramine on the proteome of the rat dentate gyrus. J Neurochem 2010, 113:848-859.
37. Kelly B.L., Vassar R., Ferreira A. Beta-amyloid-induced dynamin 1 depletion in hippocampal neurons. A potential mechanism for early cognitive decline in Alzheimer disease. J Biol Chem 2005, 280:31746-31753.
38. Kim H.T., Russell R.L., Raina A.K., Harris P.L., Siedlak S.L., Zhu X., Petersen R.B., Shimohama S., Smith M.A., Perry G. Protein disulfide isomerase in Alzheimer disease. Antioxid Redox Signal 2000, 2:485-489.
39. Klaiman G., Petzke T.L., Hammond J., Leblanc A.C. Targets of caspase-6 activity in human neurons and Alzheimer disease. Mol Cell Proteomics 2008, 7:1541-1555.
40. Labudova O., Kitzmueller E., Rink H., Cairns N., Lubec G. Increased phosphoglycerate kinase in the brains of patients with Down's syndrome but not with Alzheimer's disease. Clin Sci (Lond) 1999, 96:279-285.
41. Lee J.H., Yu W.H., Kumar A., Lee S., Mohan P.S., Peterhoff C.M., Wolfe D.M., Martinez-Vicente M., Massey A.C., Sovak G., Uchiyama Y., Westaway D., Cuervo A.M., Nixon R.A. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 2010, 141:1146-1158.
42. Lewitus G.M., Wilf-Yarkoni A., Ziv Y., Shabat-Simon M., Gersner R., Zangen A., Schwartz M. Vaccination as a novel approach for treating depressive behavior. Biol Psychiatry 2009, 65:283-288.
43. Linden D.J. The return of the spike: postsynaptic action potentials and the induction of LTP and LTD. Neuron 1999, 22:661-666.
44. Liu J., Kaksonen M., Drubin D.G., Oster G. Endocytic vesicle scission by lipid phase boundary forces. Proc Natl Acad Sci U S A 2006, 103:10277-10282.
45. Mallei A., Giambelli R., Barbiero V.S., Musazzi L., El Khoury A., Gruber S.H., Mathè A.A., Racagni G., Popoli M. Synaptoproteomic analysis of a rat model of depression with gene-environment interaction. Eur Neuropsychopharmacol 2008, 18(Suppl. 1):S19-S20.
46. Mallei A., Giambelli R., Gass P., Racagni G., Mathe A.A., Vollmayr B., Popoli M. Synaptoproteomics of learned helpless rats involve energy metabolism and cellular remodeling pathways in depressive-like behavior and antidepressant response. Neuropharmacology 2011, 60:1243-1253.
47. Marais L., Hattingh S.M., Stein D.J., Daniels W.M. A proteomic analysis of the ventral hippocampus of rats subjected to maternal separation and escitalopram treatment. Metab Brain Dis 2009, 24:569-586.
48. Martins-de-Souza D., Gattaz W.F., Schmitt A., Novello J.C., Marangoni S., Turck C.W., Dias-Neto E. Proteome analysis of schizophrenia patients Wernicke's area reveals an energy metabolism dysregulation. BMC Psychiatry 2009, 9:17.
49. Morciano M., Beckhaus T., Karas M., Zimmermann H., Volknandt W. The proteome of the presynaptic active zone: from docked synaptic vesicles to adhesion molecules and maxi-channels. J Neurochem 2009, 108:662-675.
50. +ATPase. Biol Cell 2003, 95:453-457.
51. Moriyama Y., Maeda M., Futai M. The role of V-ATPase in neuronal and endocrine systems. J Exp Biol 1992, 172:171-178.
52. Moron J.A., Abul-Husn N.S., Rozenfeld R., Dolios G., Wang R., Devi L.A. Morphine administration alters the profile of hippocampal postsynaptic density-associated proteins: a proteomics study focusing on endocytic proteins. Mol Cell Proteomics 2007, 6:29-42.
53. Morton A.J., Faull R.L., Edwardson J.M. Abnormalities in the synaptic vesicle fusion machinery in Huntington's disease. Brain Res Bull 2001, 56:111-117.
54. Mu J., Xie P., Yang Z.S., Yang D.L., Lv F.J., Luo T.Y., Li Y. Neurogenesis and major depression: implications from proteomic analyses of hippocampal proteins in a rat depression model. Neurosci Lett 2007, 416:252-256.
55. Nakamura Y., Takeda M., Yoshimi K., Hattori H., Hariguchi S., Hashimoto S., Nishimura T. Involvement of clathrin light chains in the pathology of Pick's disease; implication for impairment of axonal transport. Neurosci Lett 1994, 180:25-28.
56. Nakamura Y., Takeda M., Yoshimi K., Hattori H., Hariguchi S., Kitajima S., Hashimoto S., Nishimura T. Involvement of clathrin light chains in the pathology of Alzheimer's disease. Acta Neuropathol 1994, 87:23-31.
57. Opii W.O., Joshi G., Head E., Milgram N.W., Muggenburg B.A., Klein J.B., Pierce W.M., Cotman C.W., Butterfield D.A. Proteomic identification of brain proteins in the canine model of human aging following a long-term treatment with antioxidants and a program of behavioral enrichment: relevance to Alzheimer's disease. Neurobiol Aging 2008, 29:51-70.
58. Phillips G.R., Florens L., Tanaka H., Khaing Z.Z., Fidler L., Yates J.R., Colman D.R. Proteomic comparison of two fractions derived from the transsynaptic scaffold. J Neurosci Res 2005, 81:762-775.
59. Popoli M., Gennarelli M., Racagni G. Modulation of synaptic plasticity by stress and antidepressants. Bipolar Disord 2002, 4:166-182.
60. Rosahl T.W., Spillane D., Missler M., Herz J., Selig D.K., Wolff J.R., Hammer R.E., Malenka R.C., Sudhof T.C. Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 1995, 375:488-493.
61. Sarter M., Bruno J.P., Parikh V. Abnormal neurotransmitter release underlying behavioral and cognitive disorders: toward concepts of dynamic and function-specific dysregulation. Neuropsychopharmacology 2007, 32:1452-1461.
62. Saviouk V., Moreau M.P., Tereshchenko I.V., Brzustowicz L.M. Association of synapsin 2 with schizophrenia in families of Northern European ancestry. Schizophr Res 2007, 96:100-111.
63. Spellmann I., Muller N., Musil R., Zill P., Douhet A., Dehning S., Cerovecki A., Bondy B., Moller H.J., Riedel M. Associations of SNAP-25 polymorphisms with cognitive dysfunctions in Caucasian patients with schizophrenia during a brief trail of treatment with atypical antipsychotics. Eur Arch Psychiatry Clin Neurosci 2008, 258:335-344.
64. Sudhof T.C. The synaptic vesicle cycle. Annu Rev Neurosci 2004, 27:509-547.
65. Sugie H., Sugie Y., Nishida M., Ito M., Tsurui S., Suzuki M., Miyamoto R., Igarashi Y. Recurrent myoglobinuria in a child with mental retardation: phosphoglycerate kinase deficiency. J Child Neurol 1989, 4:95-99.
66. Takamori S., Holt M., Stenius K., Lemke E.A., Gronborg M., Riedel D., Urlaub H., Schenck S., Brugger B., Ringler P., Muller S.A., Rammner B., Grater F., Hub J.S., De Groot B.L., Mieskes G., Moriyama Y., Klingauf J., Grubmuller H., Heuser J., Wieland F., Jahn R. Molecular anatomy of a trafficking organelle. Cell 2006, 127:831-846.
67. Tolar L.A., Pallanck L. NSF function in neurotransmitter release involves rearrangement of the SNARE complex downstream of synaptic vesicle docking. J Neurosci 1998, 18:10250-10256.
68. Vawter M.P., Thatcher L., Usen N., Hyde T.M., Kleinman J.E., Freed W.J. Reduction of synapsin in the hippocampus of patients with bipolar disorder and schizophrenia. Mol Psychiatry 2002, 7:571-578.
69. Vercauteren F.G., Flores G., Ma W., Chabot J.G., Geenen L., Clerens S., Fazel A., Bergeron J.J., Srivastava L.K., Arckens L., Quirion R. An organelle proteomic method to study neurotransmission-related proteins, applied to a neurodevelopmental model of schizophrenia. Proteomics 2007, 7:3569-3579.
70. Wang Y.T., Linden D.J. Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 2000, 25:635-647.
71. WHO The World Health Report 2001: Mental health: new understanding, new hope 2001, World Health Organization, Geneva, 169 p.
72. Xu Q., Huang W., Payne T.J., Ma J.Z., Li M.D.D. Detection of genetic association and a functional polymorphism of dynamin 1 gene with nicotine dependence in European and African Americans. Neuropsychopharmacology 2009, 34:1351-1359.
73. Yan J.X., Wait R., Berkelman T., Harry R.A., Westbrook J.A., Wheeler C.H., Dunn M.J. A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 2000, 21:3666-3672.
74. Yoo B.C., Krapfenbauer K., Cairns N., Belay G., Bajo M., Lubec G. Overexpressed protein disulfide isomerase in brains of patients with sporadic Creutzfeldt-Jakob disease. Neurosci Lett 2002, 334:196-200.
75. Zhou K., Yang Y., Gao L., He G., Li W., Tang K., Ji B., Zhang M., Li Y., Yang J., Sun L., Zhang Z., Zhu H., He L., Wan C. NMD: a receptor hypofunction induces dysfunctions of energy metabolism and semaphorin signaling in rats: A Synaptic Proteome Study. Schizophr Bull 2010, 10.1093/schbul/sbq132.