The recombinant C-terminal fragment of tetanus toxin protects against cholinotoxicity by intraseptal injection of β-amyloid peptide (25-35) in rats

Neuroscience

Volumn 315, Issue , 2016, Pages 18-30

  Patricio Martinez A ^a   Mendieta, L ^a,b   Martinez I ^a   Aguilera, J ^c,d   Limon I D ^a  

^a BENEMÉRITA UNIVERSIDAD AUTÓNOMA DE PUEBLA   (Mexico)

^b INSTITUTO CAJAL   (Spain)

^c INSTITUT DE NEUROCIÈNCIES   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Acetylcholinesterase; Amyloid (25 35); Choline acetyltransferase; Hc TeTx; Medial septum; Spatial memory

Indexed keywords

ACETYLCHOLINESTERASE; AMYLOID BETA PROTEIN[25-35]; CASPASE 3; CHOLINE ACETYLTRANSFERASE; TETANUS TOXIN; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (25-35); CASP3 PROTEIN, RAT; NEUROPROTECTIVE AGENT; NOOTROPIC AGENT; PEPTIDE FRAGMENT;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHOLINOTOXICITY; CONTROLLED STUDY; ENZYME ACTIVATION; EXECUTIVE FUNCTION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; MALE; MAZE TEST; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPATIAL LEARNING; SPATIAL MEMORY; TOXICITY; TOXICITY TESTING; ANIMAL; DRUG EFFECTS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; PHYSIOLOGY; RANDOMIZATION; SEPTUM PELLUCIDUM; WISTAR RAT;

ACETYLCHOLINESTERASE; AMYLOID BETA-PEPTIDES; ANIMALS; CASPASE 3; CHOLINE O-ACETYLTRANSFERASE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MAZE LEARNING; NEUROPROTECTIVE AGENTS; NOOTROPIC AGENTS; PEPTIDE FRAGMENTS; RANDOM ALLOCATION; RATS, WISTAR; SEPTUM OF BRAIN; SPATIAL MEMORY; TETANUS TOXIN;

EID: 84951056866     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.11.066     Document Type: Article

References (63)

1. Abe E., Casamenti F., Giovannelli L., Scali C., Pepeu G. Administration of amyloid b-peptides into the medial septum of rats decreases acetylcholine release from hippocampus in vivo. Brain Res 1994, 636(1):162-164.
2. Amaral D.G., Kurz J. An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J Comp Neurol 1985, 240(1):37-59.
3. Auld D.S., Kornecook T.J., Bastianetto S., Quirion R. Alzheimer's disease and the basal forebrain cholinergic system: relations to β-amyloid peptides, cognition, and treatment strategies. Progr Neurobiol 2002, 68(3):209-245.
4. Baxter M.G., Bucci D.J., Gorman L.K., Wiley R.G., Gallagher M. Selective immunotoxic lesions of basal forebrain cholinergic cells: effects on learning and memory in rats. Behav Neurosci 1995, 109(4):714-722.
5. Cahill J.F., Baxter M.G. Cholinergic and noncholinergic septal neurons modulate strategy selection in spatial learning. Eur J Neurosci 2001, 14(11):1856-1864.
6. Calvo A.C., Moreno-Igoa M., Mancuso R., Manzano R., Oliván S., Muñoz M.J., Penas C., Zaragoza P., Navarro X., Osta R. Lack of a synergistic effect of a non-viral ALS gene therapy based on BDNF and a TTC fusion molecule. Orphanet J Rare Dis 2011, 6(10). 10.1186/1750-1172-6-10.
7. Calvo A.C., Oliván S., Manzano R., Zaragoza P., Aguilera J., Osta R. Fragment C of tetanus toxin: new insights into its neuronal signaling pathway. Int J Mol Sci 2012, 13(6):6883-6901.
8. Chaib-Oukadour I., Gil C., Aguilera J. The C-terminal domain of the heavy chain of tetanus toxin rescues cerebellar granule neurones from apoptotic death: involvement of phosphatidylinositol 3-kinase and mitogen-activated protein kinase pathways. J Neurochem 2004, 90(5):1227-1236.
9. + toxicity. Mol Cell Neurosci 2009, 41(3):297-303.
10. Chen G., Chen P., Tan H., Ma D., Dou F., Feng J., Yan Z. Regulation of the NMDA receptor-mediated synaptic response by acetylcholinesterase inhibitors and it's impairment it an animal model of Alzheimer's disease. Neurobiol Aging 2007, 29(12):1795-1804.
11. Ciriza J., Moreno-Igoa M., Calvo A.C., Yagüe G., Palacio J., Miana-Mena F.J., Muñoz M.J., Zaragoza P., BrÛlet P., Osta R. A genetic fusion GDNF-C fragment of tetanus toxin prolongs survival in a symptomatic mouse ALS model. Restor Neurol Neurosci 2008, 26(6):459-465.
12. Colom L.V., Castañeda M.T., Bañuelos C., Puras G., García-Hernández A., Hernandez S., Mounsey S., Benavidez J., Lehker C. Medial septal beta-amyloid 1-40 injections alter septo-hippocampal anatomy and function. Neurobiol Aging 2010, 31(1):46-57.
13. Conner J.M., Franks K.M., Titterness A.K., Russell K., Merrill D.A., Christie B.R., Sejnowski T.J., Tuszynski M.H. NGF is essential for hippocampal plasticity and learning. J Neurosci 2009, 29(35):10883-10889.
14. de Olmos J.S., Beltramino C.A., de Olmos S. An amino-cupricsilver method for the early detection of degenerative and regressive changes in neuronal perikarya, dendrites, stem-axons and axon terminals caused by neurotoxicants and hypoxia. Neurotoxicol Teratol 1994, 16:545-561.
15. DeKosky S.T., Harbaugh R.E., Schmitt F.A., Bakay R.A., Chui H.C., Knopman D.S., Reeder T.M., Shetter A.G., Senter H.J., Markesbery W.R. Cortical biopsy in Alzheimer's disease: diagnostic accuracy and neurochemical, neuropathological, and cognitive correlations. Intraventricular Bethanecol Study Group. Ann Neurol 1992, 32(5):625-632.
16. Díaz A., Limón I.D., Chávez R., Zenteno E., Guevara J. Aβ25-35 injection into the temporal cortex induces chronic inflammation that contributes to neurodegeneration and spatial memory impairment in rats. J Alzheimers Dis 2012, 30(3):505-522.
17. Dobransky T., Davis W.L., Rylett R.J. Functional characterization of phosphorylation of 69-kDa human choline acetyltransferase at serine 440 by protein kinase C. J Biol Chem 2001, 276(25):22244-22250.
18. Figueiredo D.M., Hallewell R.A., Chen L.L., Fairweather N.F., Dougan G., Savitt J.M., Parks D.A., Fishman P.S. Delivery of recombinant tetanus-superoxide dismutase proteins to central nervous system neurons by retrograde axonal transport. Exp Neurol 1997, 145(2 Pt 1):546-554.
19. García J.H., Liu K.F., Ho K.L. Neuronal necrosis after middle cerebral artery occlusion in Wistar rats progresses at different time intervals in the caudoputamen and the cortex. Stroke 1995, 26(4):636-642.
20. Gil C., Chaib I., Pelliccioni P., Aguilera J. Activation of signal transduction pathways involving TrkA, PLCγ-1, PKC isoforms and ERK-1/2 by tetanus toxin. FEBS Lett 2000, 481(2):177-182.
21. Gil C., Chaib-Oukadour I., Aguilera J. C-terminal fragment of tetanus toxin heavy chain activates Akt and MEK/ERK signalling pathways in a Trk receptor-dependent manner in cultured cortical neurons. Biochem J 2003, 373(Pt 2):613-620.
22. Gil C., Chaib-Oukadour I., Blasi J., Aguilera J. HC fragment (C-terminal portion of the heavy chain) of tetanus toxin activates protein kinase C isoforms and phosphoproteins involved in signal transduction. Biochem J 2001, 356(Pt 1):97-103.
23. Giovannelli L., Casamenti F., Scali C., Bartolini L., Pepeu G. Differential effects of amyloid peptides β-(1-40) and β-(25-35) injections into the rat nucleus basalis. Neuroscience 1995, 66(4):781-792.
24. Hagan J.J., Salamone J.D., Simpson J., Iversen S.D., Morris R.G.M. Place navigation in rats is impaired by lesions of medial septum and diagonal band but not nucleus basalis magnocellularis. Behav Brain Res 1988, 27:9-20.
25. Harkany T., Lengyel Z., Soo's K., Penke B., Luiten P.G.M., Gulya K. Cholinotoxic effects of β-amyloid(1-42) peptide on cortical projections of the rat nucleus basalis magnocellularis. Brain Res 1995, 695(1):71-75.
26. Herrando-Grabulosa M., Casas C., Aguilera J. The C-terminal domain of tetanus toxin protects motoneurons against acute excitotoxic damage on spinal cord organotypic cultures. J Neurochem 2013, 124:36-44.
27. Holtzman D.M., Kilbridge J., Li Y., Cunningham E.T., Lenn N.J., Clary D.O., Reichardt L.F., Mobley W.C. TrkA expression in the CNS: evidence for the existence of several novel NGF-responsive CNS neurons. J Neurosci 1995, 15(2):1567-1576.
28. Inserte J., Najib A., Pelliccioni P., Gil C., Aguilera J. Inhibition by tetanus toxin of sodium-dependent, high-affinity [3H]5-hydroxytryptamine uptake in rat synaptosomes. Biochem Pharmacol 1999, 57(1):111-120.
29. Kar S., Quirion R. Amyloid beta peptides and central cholinergic neurons: functional interrelationship and relevance to Alzheimer's disease pathology. Prog Brain Res 2004, 145:261-274.
30. Kar S., Slowikowski S.P., Westaway D. Interactions between beta-amyloid and central cholinergic neurons: implications for Alzheimer's disease. J Psychiatry Neurosci 2004, 29(6):427-441.
31. Kissa K., Mordelet E., Soudais C., Kremer E.J., Demeneix B.A., BrÛlet P., Coen L. In vivo neuronal tracing with GFP-TTC gene delivery. Mol Cell Neurosci 2002, 20(4):627-637.
32. Larsen K.E., Benn S.C., Ay I., Chian R.J., Celia S.A., Remington M.P., Bejarano M., Liu M., Ross J., Carmillo P., Sah D., Phillips K.A., Sulzer D., Pepinsky R.B., Fishman P.S., Brown R.H., Francis J.W. A glial cell line-derived neurotrophic factor (GDNF): tetanus toxin fragment C protein conjugate improves delivery of GDNF to spinal cord motor neurons in mice. Brain Res 2006, 1120(1):1-12.
33. Limón I.D., Diaz A., Mendieta L., Chamorro G., Espinosa B., Zenteno E., Guevara J. Amyloid-beta (25-35) impairs memory and increases NO in the temporal cortex of rats. Neurosci Res 2009, 63(2):129-137.
34. Limón I.D., Ramírez E., Díaz A., Mendieta L., Mayoral M.A., Espinosa B., Guevara J., Zenteno E. Alteration of the sialylation pattern and memory deficits by injection of Aβ (25-35) into the hippocampus of rats. Neurosci Lett 2011, 495(1):11-16.
35. Maccioni R.B., Muñoz J.P., Barbeito L. The molecular bases of Alzheimer's disease and other neurodegenerative disorders. Arch Med Res 2001, 32(5):367-381.
36. Maurice T., Lockhart B.P., Privat A. Amnesia induced in mice by centrally administered β-amyloid peptides involves cholinergic dysfunction. Brain Res 1996, 706(2):181-193.
37. Mendieta L., Venegas B., Moreno N., Patricio A., Martínez I., Aguilera J., Limón I.D. The carboxyl-terminal domain of the heavy chain of tetanus toxin prevents dopaminergic degeneration and improves motor behaviour in rats with striatal MPP+-lesions. Neurosci Res 2009, 65(1):98-106.
38. Mendieta L., Bautista E., Sánchez A., Guevara J., Herrando-Grabulosa M., Moran J., Martínez R., Aguilera J., Limón I.D. The C-terminal domain of the heavy chain of tetanus toxin given by intramuscular injection causes neuroprotection and improves the motor behavior in rats treated with 6-hydroxydopamine. Neurosci Res 2012, 74(2):156-167.
39. Mesulam M. The cholinergic lesion of Alzheimer's disease: pivotal factor or side show. Learn Mem 2004, 11(1):43-49.
40. Moreno-Igoa M., Calvo A.C., Ciriza J., Muñoz M.J., Zaragoza P., Osta R. Non-viral gene delivery of the GDNF, either alone or fused to the C-fragment of tetanus toxin protein, prolongs survival in a mouse ALS model. Restor Neurol Neurosci 2012, 30(1):69-80.
41. Mufson E.J., Ginsberg S.D., Ikonomovic M.D. Human cholinergic basal forebrain: chemoanatomy and neurologic dysfunction. J Chem Neuroanat 2003, 26:233-242.
42. Najib A., Pelliccioni P., Gil C., Aguilera J. Clostridium neurotoxins influence serotonin uptake and release differently in rat brain synaptosomes. J Neurochem 1999, 72(5):1991-1998.
43. Niewiadomska G., Mietelska-Porowska A., Mazurkiewicz M. The cholinergic system, nerve growth factor and the cytoskeleton. Behav Brain Res 2011, 221(2):515-526.
44. Oosawa H., Fujii T., Kawashima K. Nerve growth factor increases the synthesis and release of acetylcholine and the expression of vesicular acetylcholine transporter in primary cultured rat embryonic septal cells. J Neurosci Res 1999, 57(3):381-387.
45. Ortega L., Calvillo M., Luna F., Pérez-Severiano F., Rubio-Osornio M., Guevara J., Limón I.D. 17-AAG improves cognitive process and increases heat shock protein response in a model lesion with Aβ25-35. Neuropeptides 2014, 48(4):221-232.
46. 1-42=10:1) into rat medial septum impairs memory retention without inducing hippocampal apoptosis. Neurol Resc 2013, 35(8):798-803.
47. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic press. 4th ed.
48. Pike C.J., Walencewicz-Wasserman A.J., Kosmoski J., Cribbs D.H., Glabe C.G., Cotman C.W. Structure-activity analyses of beta-amyloid peptides: contributions of the beta 25-35 region to aggregation and neurotoxicity. J Neurochem 1995, 64(1):253-265.
49. Radenovic L., Selakovic V., Olivan S., Calvo A.C., Rando A., Janac B., Osta R. Neuroprotective efficiency of tetanus toxin C fragment in model of global cerebral ischemia in Mongolian gerbils. Brain Res Bull 2014, 101:37-44.
50. Sánchez-González A., Mendieta L., Palafox V., Candalija A., Luna F., Aguilera J., Limón I.D. The restorative effect of intramuscular injection of tetanus toxin C-fragment in hemiparkinsonian rats. Neurosci Res 2014, 84:1-9.
51. Selkoe D.J. The molecular pathology of Alzheimer's disease. Neuron 1991, 6(4):487-498.
52. Sofroniew M.V., Howe C.L., Mobley W.C. Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 2001, 24:1217-1281.
53. Stepanichev M., Lazareva N., Tukhbatova G., Salozhin S., Gulyaeva N. Transient disturbances in contextual fear memory induced by Aβ(25-35) in rats are accompanied by cholinergic dysfunction. Behav Brain Res 2014, 1(259):152-157.
54. Szutowicz A., Madziar B., Pawelczyk T., Tomaszewicz M., Bielarczyk H. Effects of NGF on acetylcholine, acetyl-CoA metabolism, and viability of differentiated and non-differentiated cholinergic neuroblastoma cells. J Neurochem 2004, 90(4):952-961.
55. Tian Q., Lin Z.Q., Wang X.C., Chen J., Wang Q., Gong C.X., Wang J.Z. Injection of okadaic acid into the meynert basalis of rat brain induces decreased acetylcholine level and spatial memory deficit. Neuroscience 2004, 126(2):277-284.
56. Toivonen J.M., Oliván S., Osta R. Tetanus toxin C-fragment: the courier and the cure?. Toxins 2010, 2(11):2622-2644.
57. Urschel B.A., Hulsebosch C.E. Distribution and relative density of p75 nerve growth factor receptors in the rat brain as a function of age and treatment with antibodies to nerve growth factor. Brain Res 1992, 591(2):223-238.
58. Vazquez M.E., Ebendal T. Messenger RNAs for trk and the low-affinity NGF receptor in rat basal forebrain. Neuroreport 1991, 2(10):593-596.
59. Winter J.C., Petti D.T. The effects of 8-hydroxy-2-(di-n-propylamino)tetralin and other serotonergic agonists on performance in a radial maze: a possible role for 5-HT1A receptors in memory. Pharmacol Biochem Behav 1987, 27(4):625-628.
60. Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., DeLong M.R. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 1981, 215(4537):1237-1239.
61. Woolf N.J., Milov A.M., Schweitzer E.S., Roghani A. Elevation of nerve growth factor and antisense knockdown of TrkA receptor during contextual memory consolidation. J Neurosci 2001, 21(3):1047-1055.
62. Yamaguchi Y., Kawashima S. Effects of amyloid-beta-(25-35) on passive avoidance, radial-arm maze learning and choline acetyltransferase activity in the rat. Eur J Pharmacol 2001, 412(3):265-272.
63. Zussy C., Brureau A., Keller E., Marchal S., Blayo C., Delair B., Ixart G., Maurice T., Givalois L. Alzheimer's disease related markers, cellular toxicity and behavioral deficits induced six weeks after oligomeric amyloid-β peptide injection in rats. PLoS One 2013, 8(1):e53117.