Cognitive and cortical plasticity deficits correlate with altered amyloid-Β CSF levels in multiple sclerosis

Neuropsychopharmacology

Volumn 36, Issue 3, 2011, Pages 559-568

  Mori, Francesco ^a,b   Rossi, Silvia ^a,b   Sancesario, Giulia ^c,d   Codecá, Claudia ^a,b   Mataluni, Giorgia ^a,b   Monteleone, Fabrizia ^a,b   Buttari, Fabio ^a,b   Kusayanagi, Hajime ^a,b   Castelli, Maura ^a,b   Motta, Caterina ^a,b   Studer, Valeria ^a,b   Bernardi, Giorgio ^a,b   Koch, Giacomo ^a,b   Bernardini, Sergio ^c,d   Centonze, Diego ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d TOR VERGATA UNIVERSITY HOSPITAL   (Italy)

Author keywords

cognition; inflammation; LTP; t protein; transcranial magnetic stimulation

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; GADOLINIUM; TAU PROTEIN;

ADULT; AMYLOID PLAQUE; ARTICLE; BRAIN CORTEX; CLINICAL ARTICLE; COGNITION; COGNITIVE DEFECT; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; HUMAN; LONG TERM POTENTIATION; MALE; MULTIPLE SCLEROSIS; NERVE CELL PLASTICITY; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN CEREBROSPINAL FLUID LEVEL;

ADULT; AMYLOID BETA-PEPTIDES; CEREBRAL CORTEX; COGNITION DISORDERS; EVOKED POTENTIALS, MOTOR; FEMALE; FUNCTIONAL LATERALITY; GADOLINIUM; HUMANS; LONG-TERM POTENTIATION; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; MUSCLE, SKELETAL; NEURONAL PLASTICITY; NEURONS; NEUROPSYCHOLOGICAL TESTS; PEPTIDE FRAGMENTS; STATISTICS AS TOPIC; TAU PROTEINS; TIME FACTORS; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 78651411152     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2010.187     Document Type: Article

References (71)

1. Amato MP, Bartolozzi ML, Zipoli V, Portaccio E, Mortilla M, Guidi L et al (2004). Neocortical volume decrease in relapsing-remitting MS patients with mild cognitive impairment. Neurology 63: 89-93.
2. Amato MP, Zipoli V, Goretti B, Portaccio E, De Caro MF, Ricchiuti L et al (2006a). Benign multiple sclerosis: cognitive, psychological and social aspects in a clinical cohort. J Neurol 253: 1054-1059.
3. Amato MP, Portaccio E, Goretti B, Zipoli V, Ricchiuti L, De Caro MF et al (2006b). The Rao's brief repeatable battery and stroop test: normative values with age, education and gender corrections in an Italian population. Mult Scler 12: 787-793.
4. Amato MP, Zipoli V, Portaccio E (2008a). Cognitive changes in multiple sclerosis. Expert Rev Neurother 8: 1585-1596.
5. Amato MP, Portaccio E, Stromillo ML, Goretti B, Zipoli V, Siracusa G et al (2008b). Cognitive assessment and quantitative magnetic resonance metrics can help to identify benign multiple sclerosis. Neurology 71: 632-638.
6. Andreasson U, Portelius E, Andersson ME, Blennow K, Zetterberg H Aspects of beta-amyloid as a biomarker for Alzheimer's disease. Biomark Med, 2007 1: 59-78.
7. Battaglia F, Wang HY, Ghilardi MF, Gashi E, Quartarone A, Friedman E et al (2007). Cortical plasticity in Alzheimer's disease in humans and rodents. Biol Psychiatry 62: 1405-1412.
8. Bellmann-Strobl J, Wuerfel J, Aktas O, Dörr J, Wernecke KD, Zipp F et al (2009). Poor PASAT performance correlates with MRI contrast enhancement in multiple sclerosis. Neurology 73: 1624-1627.
9. Bliss TV, Collingridge GL (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39.
10. Calabrese M, Agosta F, Rinaldi F, Mattisi I, Grossi P, Favaretto A et al (2009). Cortical lesions and atrophy associated with cognitive impairment in relapsing-remitting multiple sclerosis. Arch Neurol 66: 1144-1150.
11. Calabrese M, Rinaldi F, Mattisi I, Grossi P, Favaretto A, Atzori M et al (2010). Widespread cortical thinning characterizes patients with MS with mild cognitive impairment. Neurology 74: 318-321.
12. Caramia MD, Palmieri MG, Desiato MT, Boffa L, Galizia P, Rossini PM et al (2004). Brain excitability changes in the relapsing and remitting phases of multiple sclerosis: a study with transcranial magnetic stimulation. Clin Neurophysiol 115: 956-965.
13. Centonze D, Bari M, Rossi S, Prosperetti C, Furlan R, Fezza F et al (2007). The endocannabinoid system is dysregulated in multiple sclerosis and in experimental autoimmune encephalomyelitis. Brain 130: 2543-2553.
14. Chiaravalloti ND, DeLuca J (2008). Cognitive impairment in multiple sclerosis. Lancet Neurol 7: 1139-1151.
15. Conte A, Lenzi D, Frasca V, Gilio F, Giacomelli E, Gabriele M et al (2009). Intracortical excitability in patients with relapsing-remitting and secondary progressive multiple sclerosis. J Neurol 256: 933-938.
16. Cooke SF, Bliss TV (2006). Plasticity in the human central nervous system. Brain 129: 1659-1673.
17. Di Lazzaro V, Pilato F, Dileone M, Profice P, Oliviero A, Mazzone P et al (2008). The physiological basis of the effects of intermittent theta burst stimulation of the human motor cortex. J Physiol 586: 3871-3879.
18. Englund H, Degerman Gunnarsson M, Brundin RM, Hedlund M, Kilander L, Lannfelt L et al (2009). Oligomerization partially explains the lowering of Abeta42 in Alzheimer's disease cerebrospinal fluid. Neurodegener Dis 6: 139-147.
19. Fan LW, Mitchell HJ, Tien LT, Rhodes PG, Cai Z (2009). Interleukin-1beta-induced brain injury in the neonatal rat can be ameliorated by alpha-phenyl-n-tert-butyl-nitrone. Exp Neurol 220: 143-153.
20. Feldman DE (2009). Synaptic mechanisms for plasticity in neocortex. Annu Rev Neurosci 32: 33-55.
21. Foong J, Rozewicz L, Quaghebeur G, Thompson AJ, Miller DH, Ron MA (1998). Neuropsychological deficits in multiple sclerosis after acute relapse. J Neurol Neurosurg Psychiatry 64: 529-532.
22. Gandy S, Simon AJ, Steele JW, Lublin AL, Lah JJ, Walker LC et al (2010). Days to criterion as an indicator of toxicity associated with human Alzheimer amyloid-beta oligomers. Ann Neurol 68: 220-230.
23. Genova HM, Sumowski JF, Chiaravalloti N, Voelbel GT, Deluca J (2009). Cognition in multiple sclerosis: a review of neuropsy-chological and fMRI research. Front Biosci 14: 1730-1744.
24. Ghoshal N, Garća-Sierra F, Wuu J, Leurgans S, Bennett DA, Berry RW et al (2002). Tau conformational changes correspond to impairments of episodic memory in mild cognitive impairment and Alzheimer's disease. Exp Neurol 177: 475-493.
25. Gong N, Li Y, Cai GQ, Niu RF, Fang Q, Wu K et al (2009). GABA transporter-1 activity modulates hippocampal theta oscillation and theta burst stimulation-induced long-term potentiation. J Neurosci 29: 15836-15845.
26. Griffin WS, Liu L, Li Y, Mrak RE, Barger SW (2006). Interleukin-1 mediates Alzheimer and Lewy body pathologies. J Neuroin-flammation 3: 5.
27. Hanajima R, Ugawa Y, Terao Y, Enomoto H, Shiio Y, Mochizuki H et al (2002). Mechanisms of intracortical I-wave facilitation elicited with paired-pulse magnetic stimulation in humans. J Physiol 538: 253-261.
28. Hickman SE, Allison EK, El Khoury J (2008). Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice. J Neurosci 28: 8354-8360.
29. Hong HS, Hwang EM, Sim HJ, Cho HJ, Boo JH, Oh SS et al (2003). Interferon gamma stimulates beta-secretase expression and sAPPbeta production in astrocytes. Biochem Biophys Res Commun 307: 922-927.
30. Hu NW, Smith IM, Walsh DM, Rowan MJ (2008). Soluble amyloid-beta peptides potently disrupt hippocampal synaptic plasticity in the absence of cerebrovascular dysfunction in vivo. Brain 131: 2414-2424.
31. Hu X, Hicks CW, He W, Wong P, Macklin WB, Trapp BD et al (2006). Bace1 modulates myelination in the central and peripheral nervous system. Nat Neurosci 9: 1520-1525.
32. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005). Theta burst stimulation of the human motor cortex. Neuron 45: 201-206.
33. Inghilleri M, Conte A, Frasca V, Scaldaferri N, Gilio F, Santini M et al (2006). Altered response to rTMS in patients with Alzheimer's disease. Clin Neurophysiol 117: 103-109.
34. Kessels HW, Malinow R (2009). Synaptic AMPA receptor plasticity and behavior. Neuron 61: 340-350.
35. Klyubin I, Walsh DM, Lemere CA, Cullen WK, Shankar GM, Betts V et al (2005). Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat Med 11: 556-561.
36. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A et al (1993). Corticocortical inhibition in human motor cortex. J Physiol 471: 501-519.
37. Liepert J, Mingers D, Heesen C, Bäumer T, Weiller C (2005). Motor cortex excitability and fatigue in multiple sclerosis: a transcra-nial magnetic stimulation study. Mult Scler 11: 316-321.
38. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L et al (1999). Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155: 853-862.
39. Malenka RC (2003). The long-term potential of LTP. Nat Rev Neurosci 4: 923-926.
40. Matsuyama S, Taniguchi T, Kadoyama K, Matsumoto A (2008). Long-term potentiation-like facilitation through GABAA receptor blockade in the mouse dentate gyrus in vivo. Neuroreport 19: 1809-1813.
41. Mattsson N, Axelsson M, Haghighi S, Malmeström C, Wu G, Anckarsäter R et al (2009). Reduced cerebrospinal fluid BACE1 activity in multiple sclerosis. Mult Scler 15: 448-454.
42. McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, Lublin FD et al (2001). Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol 50: 121-127.
43. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K et al (1999). Soluble pool of A beta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46: 860-866.
44. Minichiello L (2009). TrkB signalling pathways in LTP and learning. Nat Rev Neurosci 10: 850-860.
45. Mulder SD, van der Flier WM, Verheijen JH, Mulder C, Scheltens P, Blankenstein MA et al (2010). BACE1 activity in cerebrospinal fluid and its relation to markers of AD pathology. J Alzheimers Dis 20: 253-260.
46. Nygaard HB, Strittmatter SM (2009). Cellular prion protein mediates the toxicity of beta-amyloid oligomers: implications for Alzheimer disease. Arch Neurol 66: 1325-1328.
47. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R et al (2003). Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39: 409-421.
48. Ozturk A, Smith SA, Gordon-Lipkin EM, Harrison DM, Shiee N, Pham DL et al (2010). MRI of the corpus callosum in multiple sclerosis: association with disability. Mult Scler 16: 166-177.
49. Pan BX, Dong Y, Ito W, Yanagawa Y, Shigemoto R, Morozov A (2009). Selective gating of glutamatergic inputs to excitatory neurons of amygdala by presynaptic GABAb receptor. Neuron 61: 917-929.
50. Peretti CS (1998). Anxiety and cognition disorders. Encephale 24: 256-259.
51. Polman CH, Reingold SC, Edan G, Filippi M, Hartung HP, Kappos L et al (2005). Diagnostic criteria for multiple sclerosis: 2005 revisions to the 'McDonald Criteria'. Ann Neurol 58: 840-846.
52. Polydoro M, Acker CM, Duff K, Castillo PE, Davies P (2009). Age-dependent impairment of cognitive and synaptic function in the htau mouse model of tau pathology. J Neurosci 29: 10741-10749.
53. Rao S (1990). A Manual for the Brief Repeatable Battery of Neuropsychological Tests in Multiple Sclerosis. Medical College of Wisconsin: Milwaukee.
54. Rosenmann H, Grigoriadis N, Eldar-Levy H, Avital A, Rozenstein L, Touloumi O et al (2008). A novel transgenic mouse expressing double mutant tau driven by its natural promoter exhibits tauopathy characteristics. Exp Neurol 212: 71-84.
55. Rothwell JC (1997). Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Methods 74: 113-122.
56. Sancesario GM, Esposito Z, Nuccetelli M, Bernardini S, Sorge R, Martorana A et al (2010). Abeta1-42 detection in CSF of Alzheimer's disease is influenced by temperature: indication of reversible Abeta1-42 aggregation? Exp Neurol 223: 371-376.
57. Selkoe DJ (2008). Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav Brain Res 192: 106-113.
58. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I et al (2008). Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-842.
59. Schmidt J, Barthel K, Wrede A, Salajegheh M, Bähr M, Dalakas MC (2008). Interrelation of inflammation and APP in sIBM: IL-1 beta induces accumulation of beta-amyloid in skeletal muscle. Brain 131: 1228-1240.
60. Shimizu E, Kawahara K, Kajizono M, Sawada M, Nakayama H (2008). IL-4-induced selective clearance of oligomeric beta-amyloid peptide(1-42) by rat primary type 2 microglia. J Immunol 181: 6503-6513.
61. Staff NP, Lucchinetti CF, Keegan BM (2009). Multiple sclerosis with predominant, severe cognitive impairment. Arch Neurol 66: 1139-1143.
62. Terry RD (1996). The pathogenesis of Alzheimer disease: an alternative to the amyloid hypothesis. J Neuropathol Exp Neurol 55: 1023-1025.
63. Tiemann L, Penner IK, Haupts M, Schlegel U, Calabrese P (2009). Cognitive decline in multiple sclerosis: impact of topographic lesion distribution on differential cognitive deficit patterns. Mult Scler 15: 1164-1174.
64. Tombaugh TN (2006). A comprehensive review of the paced auditory serial addition test (PASAT). Arch Clin Neuropsychol 21: 53-76.
65. Townsend M, Qu Y, Gray A, Wu Z, Seto T, Hutton M et al (2010). Oral treatment with a {gamma}-secretase inhibitor improves long-term potentiation in a mouse model of Alzheimer's disease. J Pharmacol Exp Ther 333: 110-119.
66. Valls-Solé J, Pascual-Leone A, Wassermann EM, Hallett M (1992). Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalogr Clin Neurophysiol 85: 355-364.
67. Vemuri P, Wiste HJ, Weigand SD, Shaw KM, Trojanowski JQ, Weiner MW, et al, On behalf of the Alzheimer's Disease Neuroimaging Initiative (2009). MRI and CSF biomarkers in normal, MCI, and AD subjects. Diagnostic discrimination and cognitive correlations. Neurology 73: 287-293.
68. Walther T, Albrecht D, Becker M, Schubert M, Kouznetsova E, Wiesner B et al (2009). Improved learning and memory in aged mice deficient in amyloid beta-degrading neutral endopeptidase. PLoS One 4: e4590.
69. Zeller D, Kampe K, Biller A, Stefan K, Gentner R, Schütz A et al (2010). Rapid-onset central motor plasticity in multiple sclerosis. Neurology 74: 728-735.
70. Ziemann U (2004). TMS induced plasticity in human cortex. Rev Neurosci 15: 253-266.
71. Ziemann U, Tergau F, Wischer S, Hildebrandt J, Paulus W (1998). Pharmacological control of facilitatory I-wave interaction in the human motor cortex. A paired transcranial magnetic stimulation study. Electroencephalogr Clin Neurophysiol 109: 321-330.