Synaptic plasticity and PDGF signaling defects underlie clinical progression in multiple sclerosis

Journal of Neuroscience

Volumn 33, Issue 49, 2013, Pages 19112-19119

  Mori, Francesco ^a,b   Rossi, Silvia ^a,b   Piccinin, Sonia ^c,d   Motta, Caterina ^a,b   Mango, Dalila ^a,b   Kusayanagi, Hajime ^a,b   Bergami, Alessandra ^a,b   Studer, Valeria ^e   Nicoletti, Carolina G ^a,b   Buttari, Fabio ^a,b   Barbieri, Francesca ^a,b   Mercuri, Nicola B ^a,b   Martino, Gianvito ^e   Furlan, Roberto ^e   Nisticò, Robert ^a,c   Centonze, Diego ^a,b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^e SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PLATELET DERIVED GROWTH FACTOR;

ADULT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ELECTROPHYSIOLOGY; FEMALE; HIPPOCAMPUS; HUMAN; LONG TERM POTENTIATION; MAJOR CLINICAL STUDY; MALE; MOUSE; MULTIPLE SCLEROSIS; NERVE CELL PLASTICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; ANIMALS; BRAIN; CEREBRAL CORTEX; DISEASE PROGRESSION; ELECTRIC STIMULATION; ELECTROPHYSIOLOGICAL PROCESSES; EVOKED POTENTIALS; FEMALE; HUMANS; LONG-TERM POTENTIATION; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; NEURONAL PLASTICITY; PLATELET-DERIVED GROWTH FACTOR; SIGNAL TRANSDUCTION; SYNAPSES; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84889069571     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2536-13.2013     Document Type: Article

References (68)

1. Baroncelli L, Braschi C, Spolidoro M, Begenisic T, Maffei L, Sale A (2011) Brain plasticity and disease: a matter of inhibition. Neural Plast 2011: 286073. CrossRef Medline
2. Bartlett TE, Wang YT (2013) The intersections of NMDAR-dependent synaptic plasticity and cell survival. Neuropharmacology 74:59-68. CrossRef Medline
3. Benveniste H, Drejer J, Schousboe A, Diemer NH (1984) Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J Neurochem 43:1369-1374. CrossRef Medline
4. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331-356. Medline
5. Caramia MD, Palmieri MG, Desiato MT, Boffa L, Galizia P, Rossini PM, Centonze D, Bernardi G (2004) Brain excitability changes in the relapsing and remitting phases of multiple sclerosis: a study with transcranial magnetic stimulation. Clin Neurophysiol 115:956-965. CrossRef Medline
6. Cenci MA, Konradi C (2010) Maladaptive striatal plasticity in L-DOPAinduced dyskinesia. Prog Brain Res 183:209-233. CrossRef Medline
7. Centonze D, Rossi S, Tortiglione A, Picconi B, Prosperetti C, De Chiara V, Bernardi G, Calabresi P (2007) Synaptic plasticity during recovery from permanent occlusion of the middle cerebral artery. Neurobiol Dis 27:44-53. CrossRef Medline
8. Chapman CA, Perez Y, Lacaille JC (1998) Effects of GABA(A) inhibition on the expression of long-term potentiation in CA1 pyramidal cells are dependent on tetanization parameters. Hippocampus 8:289-298. CrossRef Medline
9. Cheng B, Mattson MP (1995) PDGFs protect hippocampal neurons against energy deprivation and oxidative injury: evidence for induction of antioxidant pathways. J Neurosci 15:7095-7104. Medline
10. Collin C, Miyaguchi K, Segal M (1997) Dendritic spine density and LTP induction in cultured hippocampal slices. J Neurophysiol 77:1614-1623. Medline
11. Compston A, Coles A (2008) Multiple sclerosis. Lancet 372:1502-1517. CrossRef Medline
12. Conte A, Belvisi D, Bologna M, Ottaviani D, Fabbrini G, Colosimo C, Williams DR, Berardelli A (2012) Abnormal cortical synaptic plasticity in primary motor area in progressive supranuclear palsy. Cereb Cortex 22: 693-700. CrossRef Medline
13. Di Lazzaro V, Restuccia D, Oliviero A, Profice P, Ferrara L, Insola A, Mazzone P, Tonali P, Rothwell JC (1998) Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. J Physiol 508:625-633. CrossRef Medline
14. Di Lazzaro V, Pilato F, Saturno E, Oliviero A, Dileone M, Mazzone P, Insola A, Tonali PA, Ranieri F, Huang YZ, Rothwell JC (2005) Theta-burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J Physiol 565:945-950. CrossRef Medline
15. Di Lazzaro V, Profice P, Pilato F, Capone F, Ranieri F, Pasqualetti P, Colosimo C, Pravatà E, Cianfoni A, Dileone M (2010) Motor cortex plasticity predicits recovery in acute stroke. Cereb Cortex 20:1523-1528. CrossRef Medline
16. Egawa-Tsuzuki T, Ohno M, Tanaka N, Takeuchi Y, Uramoto H, Faigle R, Funa K, Ishii Y, Sasahara M (2004) The PDGF B-chain is involved in the ontogenic susceptibility of the developing rat brain to NMDA toxicity. Exp Neurol 186:89-98. CrossRef Medline
17. Erlandsson A, Enarsson M, Forsberg-Nilsson K (2001) Immature neurons from CNS stem cells proliferate in response to platelet-derived growth factor. J Neurosci 21:3483-3491. Medline
18. Errico F, Nisticò R, Palma G, Federici M, Affuso A, Brilli E, Topo E, Centonze D, Bernardi G, Bozzi Y, D'Aniello A, Di Lauro R, Mercuri NB, Usiello A (2008) Increased levels of D-aspartate in the hippocampus enhance LTP but do not facilitate cognitive flexibility. Mol Cell Neurosci 37:236-246. CrossRef Medline
19. Gentner R, Wankerl K, Reinsberger C, Zeller D, Classen J (2008) Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb Cortex 18:2046-2053. CrossRef Medline
20. Gozal D, Simakajornboon N, Czapla MA, Xue YD, Gozal E, Vlasic V, Lasky JA, Liu JY (2000) Brainstem activation of platelet-derived growth factor-beta receptor modulates the late phase of the hypoxic ventilatory response. J Neurochem 74:310-319. CrossRef Medline
21. Grover LM, Yan C (1999) Blockade of GABAA receptors facilitates induction of NMDA receptor-independent long-term potentiation. J Neurophysiol 81:2814-2822. Medline
22. Haji N, Mandolesi G, Gentile A, Sacchetti L, Fresegna D, Rossi S, Musella A, Sepman H, Motta C, Studer V, De Chiara V, Bernardi G, Strata P, Centonze D (2012) TNF-α-mediated anxiety in a mouse model of multiple sclerosis. Exp Neurol 237:296-303. CrossRef Medline
23. Harirchian MH, Tekieh AH, Modabbernia A, Aghamollaii V, Tafakhori A, Ghaffarpour M, Sahraian MA, Naji M, Yazdanbakhsh M (2012) Serum and CSF PDGF-AA and FGF-2 in relapsing-remitting multiple sclerosis: a case-control study. Eur J Neurol 19:241-247. CrossRef Medline
24. Hess G, Donoghue JP (1996) Long-term depression of horizontal connections in rat motor cortex. Eur J Neurosci 8:658-665. CrossRef Medline
25. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201-206. CrossRef Medline
26. Huang YZ, Rothwell JC, Chen RS, Lu CS, Chuang WL (2011) The theoretical model of theta burst form of repetitive transcranial magnetic stimulation. Clin Neurophysiol 122:1011-1018. CrossRef Medline
27. Iezzi E, Conte A, Suppa A, Agostino R, Dinapoli L, Scontrini A, Berardelli A (2008) Phasic voluntary movements reverse the aftereffects of subsequent theta-burst stimulation in humans. J Neurophysiol 100:2070-2076. CrossRef Medline
28. Imbrosci B, Mittmann T (2011) Functional consequences of the disturbances in the GABA-mediated inhibition induced by injuries in the cerebral cortex. Neural Plast 2011:614329. CrossRef Medline
29. Kerschensteiner M, Stadelmann C, Dechant G, Wekerle H, Hohlfeld R (2003) Neurotrophic cross-talk between the nervous and immune systems: implications for neurological diseases. Ann Neurol 53:292-304. CrossRef Medline
30. Koehler NK, Roebbert M, Dehghani K, Ballmaier M, Claus P, von Hoersten S, Shing M, Odin P, Strehlau J, Heidenreich F (2008) Up-regulation of platelet-derived growth factor by peripheral-blood leukocytes during experimental allergic encephalomyelitis. J Neurosci Res 86:392-402. CrossRef Medline
31. Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33:1444-1452. CrossRef Medline
32. Levkovitz Y, Avignone E, Groner Y, Segal M (1999) Upregulation of GABA neurotransmission suppresses hippocampal excitability and prevents longterm potentiation in transgenic superoxide dismutase-overexpressing mice. J Neurosci 19:10977-10984. Medline
33. Lu YM, Mansuy IM, Kandel ER, Roder J (2000) Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP. Neuron 26:197-205. CrossRef Medline
34. Mariorenzi R, Zarola F, Caramia MD, Paradiso C, Rossini PM (1991) Noninvasive evaluation of central motor tract excitability changes following peripheral nerve stimulation in healthy humans. Electroencephalogr Clin Neurophysiol 81:90-101. CrossRef Medline
35. Martin LJ, Zurek AA, MacDonald JF, Roder JC, Jackson MF, Orser BA (2010) Alpha5GABAA receptor activity sets the threshold for long-term potentiation and constrains hippocampus-dependent memory. J Neurosci 30:5269-5282. CrossRef Medline
36. McAllister CJ, Rönnqvist KC, Stanford IM, Woodhall GL, Furlong PL, Hall SD (2013) Oscillatory beta activity mediates neuroplastic effects of motor cortex stimulation in humans. J Neurosci 33:7919-7927. CrossRef Medline
37. 2+ exchanger (NCX3) knock-out mice display an impairment in hippocampal long-term potentiation and spatial learning and memory. J Neurosci 31:7312-7321. CrossRef Medline
38. Mori F, Codecà C, Kusayanagi H, Monteleone F, Boffa L, Rimano A, Bernardi G, Koch G, Centonze D (2010) Effects of intermittent theta burst stimulation on spasticity in patients with multiple sclerosis. Eur J Neurol 17:295-300. CrossRef Medline
39. Mori F, Rossi S, Sancesario G, Codecà C, Mataluni G, Monteleone F, Buttari F, Kusayanagi H, Castelli M, Motta C, Studer V, Bernardi G, Koch G, Bernardini S, Centonze D (2011) Cognitive and cortical plasticity deficits correlate with altered amyloid-βCSF levels in multiple sclerosis. Neuropsychopharmacology 36:559-568. CrossRef Medline
40. Mori F, Nisticò R, Mandolesi G, Piccinin S, Mango D, Kusayanagi H, Berretta N, Bergami A, Gentile A, Musella A, Nicoletti CG, Nicoletti F, Buttari F, Mercuri NB, Martino G, Furlan R, Centonze D (2013) Interleukin-1β promotes long-term potentiation in patients with multiple sclerosis. Neuromolecular Med. Advance online publication. Retrieved July 28, 2013. doi: 10.1007/s12017-013-8249-7. CrossRef Medline
41. Nisticò R, Mango D, Mandolesi G, Piccinin S, Berretta N, Pignatelli M, Feligioni M, Musella A, Gentile A, Mori F, Bernardi G, Nicoletti F, Mercuri NB, Centonze D (2013) Inflammation subverts hippocampal synaptic plasticity in experimental multiple sclerosis. PLoS One 8:e54666. CrossRef Medline
42. Peng F, Dhillon N, Callen S, Yao H, Bokhari S, Zhu X, Baydoun HH, Buch S (2008) Platelet-derived growth factor protects neurons against gp120- mediated toxicity. J Neurovirol 14:62-72. CrossRef Medline
43. Peng F, Yao H, Bai X, Zhu X, Reiner BC, Beazely M, Funa K, Xiong H, Buch S (2010) Platelet-derived growth factor-mediated induction of the synaptic plasticity gene Arc/Arg3.1. J Biol Chem 285:21615-21624. CrossRef Medline
44. Picconi B, Tortiglione A, Barone I, Centonze D, Gardoni F, Gubellini P, Bonsi P, Pisani A, Bernardi G, Di Luca M, Calabresi P (2006) NR2B subunit exerts a critical role in post ischemic synaptic plasticity. Stroke 37:1895-1901. CrossRef Medline
45. Pickering M, Cumiskey D, O'Connor JJ (2005) Actions of TNF-alpha on glutamatergic synaptic transmission in the central nervous system. Exp Physiol 90:663-670. CrossRef Medline
46. Polman CH, Reingold SC, Edan G, Filippi M, Hartung HP, Kappos L, Lublin FD, Metz LM, McFarland HF, O'Connor PW, Sandberg-Wollheim M, Thompson AJ, Weinshenker BG, Wolinsky JS (2005) Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria." Ann Neurol 58:840-846. CrossRef Medline
47. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, Lublin FD, Montalban X, O'Connor P, Sandberg-Wollheim M, Thompson AJ, Waubant E, Weinshenker B, Wolinsky JS (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69:292-302. CrossRef Medline
48. Quartarone A, Bagnato S, Rizzo V, Siebner HR, Dattola V, Scalfari A, Morgante F, Battaglia F, Romano M, Girlanda P (2003) Abnormal associative plasticity of the human motor cortex in writer's cramp. Brain 126: 2586-2596. CrossRef Medline
49. Rossi S, Furlan R, De Chiara V, Motta C, Studer V, Mori F, Musella A, Bergami A, Muzio L, Bernardi G, Battistini L, Martino G, Centonze D (2012) Interleukin-1α causes synaptic hyperexcitability in multiple sclerosis. Ann Neurol 71:76-83. CrossRef Medline
50. Sasahara M, Fries JW, Raines EW, Gown AM, Westrum LE, Frosch MP, Bonthron DT, Ross R, Collins T (1991) PDGF B-chain in neurons of the central nervous system, posterior pituitary, and in a transgenic model. Cell 64:217-227. CrossRef Medline
51. Schirmer L, Merkler D, König FB, Bruck W, Stadelmann C (2013) Neuroaxonal regeneration is more pronounced in early multiple sclerosis than in traumatic brain injury lesions. Brain Pathol 23:2-12. CrossRef Medline
52. Schwartz M, Cohen I, Lazarov-Spiegler O, Moalem G, Yoles E (1999) The remedy may lie in ourselves: prospects for immune cell therapy in central nervous system protection and repair. J Mol Med 77:713-717. CrossRef Medline
53. Schwenkreis P, Witscher K, Janssen F, Addo A, Dertwinkel R, Zenz M, Malin JP, Tegenthoff M (1999) Influence of the N-methyl-D-aspartate antagonist memantine on human motor cortex excitability. Neurosci Lett 270: 137-140. CrossRef Medline
54. Singer BH, Gamelli AE, Fuller CL, Temme SJ, Parent JM, Murphy GG (2011) Compensatory network changes in the dentate gyrus restore long-term potentiation following ablation of neurogenesis in young-adult mice. Proc Natl Acad Sci U S A 108:5437-5442. CrossRef Medline
55. Stagg CJ, Wylezinska M, Matthews PM, Johansen-Berg H, Jezzard P, Rothwell JC, Bestmann S (2009) Neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy. J Neurophysiol 101: 2872-2877. CrossRef Medline
56. Staubli U, Scafidi J, Chun D (1999) GABAB receptor antagonism: facilitatory effects on memory parallel those on LTP induced by TBS but not HFS. J Neurosci 19:4609-4615. Medline
57. Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123:572-584. CrossRef Medline
58. Tan AM, Chakrabarty S, Kimura H, Martin JH (2012) Selective corticospinal tract injury in the rat induces primary afferent fiber sprouting in the spinal cord and hyperreflexia. J Neurosci 32:12896-12908. CrossRef Medline
59. Teo JT, Terranova C, Swayne O, Greenwood RJ, Rothwell JC (2009) Differing effects of intracortical circuits on plasticity. Exp Brain Res 193:555-563. CrossRef Medline
60. Tiberio M, Chard DT, Altmann DR, Davies G, Griffin CM, Rashid W, Sastre- Garriga J, Thompson AJ, Miller DH (2005) Gray and white matter volume changes in early RRMS: a 2-year longitudinal study. Neurology 64: 1001-1007. CrossRef Medline
61. Vana AC, Flint NC, Harwood NE, Le TQ, Fruttiger M, Armstrong RC (2007) Platelet-derived growth factor promotes repair of chronically demyelinated white matter. J Neuropathol Exp Neurol 66:975-988. CrossRef Medline
62. Vernet M, Bashir S, Yoo WK, Perez JM, Najib U, Pascual-Leone A (2013) Insights on the neural basis of motor plasticity induced by theta burst stimulation from TMS-EEG. Eur J Neurosci 37:598-606. CrossRef Medline
63. Wigström H, Gustafsson B (1983) Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature 301:603-604. CrossRef Medline
64. Williams BP, Park JK, Alberta JA, Muhlebach SG, Hwang GY, Roberts TM, Stiles CD (1997) A PDGF-regulated immediate early gene response initiates neuronal differentiation in ventricular zone progenitor cells. Neuron 18:553-562. CrossRef Medline
65. Yoshiike Y, Kimura T, Yamashita S, Furudate H, Mizoroki T, Murayama M, Takashima A (2008) GABA(A) receptor-mediated acceleration of aging-associated memory decline in APP/PS1 mice and its pharmacological treatment by picrotoxin. PLoS One 3:e3029. CrossRef Medline
66. Zapallow CM, Asmussen MJ, Bolton DA, Lee KG, Jacobs MF, Nelson AJ (2012) Theta burst repetitive transcranial magnetic stimulation attenuates somatosensory evoked potentials from the lower limb. BMC Neurosci 13:133. CrossRef Medline
67. Zepeda A, Aguilar-Arredondo A, Michel G, Ramos-Languren LE, Escobar ML, Arias C (2013) Functional recovery of the dentate gyrus after a focal lesion is accompanied by structural reorganization in the adult rat. Brain Struct Funct 218:437-453. CrossRef Medline
68. Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W (1996) The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res 109:127-135. Medline