Neurochemical mapping of the human hippocampus reveals perisynaptic matrix around functional synapses in Alzheimer's disease

Acta Neuropathologica

Volumn 125, Issue 2, 2013, Pages 215-229

  Lendvai, Dávid ^a   Morawski, Markus ^b,c   Négyessy, László ^d   Gáti, Georgina ^a   Jäger, Carsten ^b   Baksa, Gábor ^a   Glasz, Tibor ^a   Attems, Johannes ^e   Tanila, Heikki ^f,g   Arendt, Thomas ^b   Harkany, Tibor ^h,i   Alpár, Alán ^a,h,i  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c State University of New York Upstate Medical University: College of Medicine   (United States)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^e NEWCASTLE UNIVERSITY   (United Kingdom)

^f UNIVERSITY OF EASTERN FINLAND   (Finland)

^g KUOPIO UNIVERSITY HOSPITAL   (Finland)

^h UNIVERSITY OF ABERDEEN   (United Kingdom)

ⁱ KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Ageing; Ca2+ binding protein; Human cortex; Interneuron; Neurodegeneration; Neuroprotection; Synaptic plasticity

Indexed keywords

AGGRECAN; AMYLOID BETA PROTEIN; BREVICAN; CALBINDIN; CALRETININ; CARTILAGE LINK PROTEIN 1; EPITOPE; LINK PROTEIN; MOLECULAR SCAFFOLD; PARVALBUMIN; PROTEOCHONDROITIN SULFATE; TAU PROTEIN; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ALZHEIMER DISEASE; ARTICLE; AXONAL COAT; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENTATE GYRUS; ENTORHINAL CORTEX; EXTRACELLULAR MATRIX; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; MALE; MOLECULAR PATHOLOGY; MOUSE; NERVE ENDING; NERVE FIBER; NEUROCHEMISTRY; NEUROTRANSMITTER RELEASE; NONHUMAN; PEPTIDE MAPPING; PERINEURONAL MATRIX; PERISYNAPTIC MATRIX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; PYRAMIDAL NERVE CELL; SYNAPTOSOME;

AGGRECANS; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; AXONS; BLOTTING, WESTERN; BRAIN MAPPING; BREVICAN; CALCIUM-BINDING PROTEINS; COHORT STUDIES; DENDRITES; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FEMALE; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; PROTEOGLYCANS; SYNAPSES; TAU PROTEINS; VESICULAR NEUROTRANSMITTER TRANSPORT PROTEINS;

EID: 84875627668     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-012-1042-0     Document Type: Article

References (73)

1. Adams I, Brauer K, Arelin C, Härtig W, Fine A, Mader M, Arendt T, Brückner G (2001) Perineuronal nets in the rhesus monkey and human basal forebrain including basal ganglia. Neuroscience 108:285-298
2. Amet LE, Lauri SE, Hienola A, Croll SD, Lu Y, Levorse JM, Prabhakaran B, Taira T, Rauvala H, Vogt TF (2001) Enhanced hippocampal long-term potentiation in mice lacking heparin-binding growth-associated molecule. Mol Cell Neurosci 17:1014-1024
3. Baig S, Wilcock GK, Love S (2005) Loss of perineuronal net N-acetylgalactosamine in Alzheimer's disease. Acta Neuropathol 110:393-401
4. Berardi N, Pizzorusso T, Ratto GM, Maffei L (2003) Molecular basis of plasticity in the visual cortex. Trends Neurosci 26:369-378
5. Bertolotto A, Rocca G, Canavese G, Migheli A, Schiffer D (1991) Chondroitin sulfate proteoglycan surrounds a subset of human and rat CNS neurons. J Neurosci Res 29:225-234
6. Braak H, Braak E (1992) The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases. Neurosci Res 15:6-31
7. Brakebusch C, Seidenbecher CI, Asztely F, Rauch U, Matthies H, Meyer H, Krug M, Bockers TM, Zhou X, Kreutz MR, Montag D, Gundelfinger ED, Fassler R (2002) Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol Cell Biol 22:7417-7427
8. Brückner G, Brauer K, Härtig W, Wolff JR, Rickmann MJ, Derouiche A, Delpech B, Girard N, Oertel WH, Reichenbach A (1993) Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 8:183-200
9. Brückner G, Grosche J, Hartlage-Rübsamen M, Schmidt S, Schachner M (2003) Region and lamina-specific distribution of extracellular matrix proteoglycans, hyaluronan and tenascin-R in the mouse hippocampal formation. J Chem Neuroanat 26:37-50
10. Brückner G, Hausen D, Härtig W, Drlicek M, Arendt T, Brauer K (1999) Cortical areas abundant in extracellular matrix chondroitin sulphate proteoglycans are less affected by cytoskeletal changes in Alzheimer's disease. Neuroscience 92:791-805
11. Brückner G, Morawski M, Arendt T (2008) Aggrecan-based extracellular matrix is an integral part of the human basal ganglia circuit. Neuroscience 151:489-504
12. Brückner G, Seeger G, Brauer K, Härtig W, Kacza J, Bigl V (1994) Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat. Brain Res 658:67-86
13. Brückner G, Szeoke S, Pavlica S, Grosche J, Kacza J (2006) Axon initial segment ensheathed by extracellular matrix in perineuronal nets. Neuroscience 138:365-375
14. Carulli D, Pizzorusso T, Kwok JC, Putignano E, Poli A, Forostyak S, Andrews MR, Deepa SS, Glant TT, Fawcett JW (2010) Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133:2331-2347
15. Carulli D, Rhodes KE, Fawcett JW (2007) Upregulation of aggrecan, link protein 1, and hyaluronan synthases during formation of perineuronal nets in the rat cerebellum. J Comp Neurol 501:83-94
16. Celio MR (1993) Perineuronal nets of extracellular matrix around parvalbumin-containing neurons of the hippocampus. Hippocampus 3 Spec No:55-60
17. Celio MR, Spreafico R, De BS, Vitellaro-Zuccarello L (1998) Perineuronal nets: past and present. Trends Neurosci 21:510-515
18. Crews L, Masliah E (2010) Molecular mechanisms of neurodegeneration in Alzheimer's disease. Hum Mol Genet 19:R12-R20
19. de CA, Polydoro M, Suarez-Calvet M, William C, Adamowicz DH, Kopeikina KJ, Pitstick R, Sahara N, Ashe KH, Carlson GA, Spires-Jones TL, Hyman BT (2012) Propagation of tau pathology in a model of early Alzheimer's disease. Neuron 73:685-697
20. Dityatev A, Fellin T (2008) Extracellular matrix in plasticity and epileptogenesis. Neuron Glia Biol 4:235-247
21. Dityatev A, Seidenbecher CI, Schachner M (2010) Compartmentalization from the outside: the extracellular matrix and functional microdomains in the brain. Trends Neurosci 33:503-512
22. Drake CT, Mulligan KA, Wimpey TL, Hendrickson A, Chavkin C (1991) Characterization of Vicia villosa agglutinin-labeled GABAergic interneurons in the hippocampal formation and in acutely dissociated hippocampus. Brain Res 554:176-185
23. Ferhat L, Chevassus-Au-Louis N, Khrestchatisky M, Ben-Ari Y, Represa A (1996) Seizures induce tenascin-C mRNA expression in neurons. J Neurocytol 25:535-546
24. Fitch MT, Silver J (2008) CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp Neurol 209:294-301
25. Franklin SL, Love S, Greene JR, Betmouni S (2008) Loss of perineuronal net in ME7 prion disease. J Neuropathol Exp Neurol 67:189-199
26. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470
27. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, Gundelfinger ED (2009) Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 12:897-904
28. Giamanco KA, Morawski M, Matthews RT (2010) Perineuronal net formation and structure in aggrecan knockout mice. Neuroscience 170:1314-1327
29. Härtig W, Brauer K, Bigl V, Brückner G (1994) Chondroitin sulfate proteoglycan-immunoreactivity of lectin-labeled perineuronal nets around parvalbumin-containing neurons. Brain Res 635:307-311
30. Härtig W, Derouiche A, Welt K, Brauer K, Grosche J, Mäder M, Reichenbach A, Brückner G (1999) Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations. Brain Res 842:15-29
31. Hockfield S, McKay RD (1983) A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. Proc Natl Acad Sci USA 80:5758-5761
32. Ida M, Shuo T, Hirano K, Tokita Y, Nakanishi K, Matsui F, Aono S, Fujita H, Fujiwara Y, Kaji T, Oohira A (2006) Identification and functions of chondroitin sulfate in the milieu of neural stem cells. J Biol Chem 281:5982-5991
33. Jankowsky JL, Slunt HH, Gonzales V, Jenkins NA, Copeland NG, Borchelt DR (2004) APP processing and amyloid deposition in mice haplo-insufficient for presenilin 1. Neurobiol Aging 25:885-892
34. Jaworski DM, Kelly GM, Hockfield S (1995) The CNS-specific hyaluronan-binding protein BEHAB is expressed in ventricular zones coincident with gliogenesis. J Neurosci 15:1352-1362
35. Jenkins HG, Bachelard HS (1988) Glycosaminoglycans in cortical autopsy samples from Alzheimer brain. J Neurochem 51:1641-1645
36. Kaas JH, Qi HX, Burish MJ, Gharbawie OA, Onifer SM, Massey JM (2008) Cortical and subcortical plasticity in the brains of humans, primates, and rats after damage to sensory afferents in the dorsal columns of the spinal cord. Exp Neurol 209:407-416
37. Katsumaru H, Kosaka T, Heizmann CW, Hama K (1988) Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp Brain Res 72:347-362
38. Kobayashi K, Emson PC, Mountjoy CQ (1989) Vicia villosa lectin-positive neurones in human cerebral cortex. Loss in Alzheimer-type dementia. Brain Res 498:170-174
39. Kocherhans S, Madhusudan A, Doehner J, Breu KS, Nitsch RM, Fritschy JM, Knuesel I (2010) Reduced Reelin expression accelerates amyloid-beta plaque formation and tau pathology in transgenic Alzheimer's disease mice. J Neurosci 30:9228-9240
40. Koyama R, Yamada MK, Fujisawa S, Katoh-Semba R, Matsuki N, Ikegaya Y (2004) Brain-derived neurotrophic factor induces hyperexcitable reentrant circuits in the dentate gyrus. J Neurosci 24:7215-7224
41. Kurazono S, Okamoto M, Sakiyama J, Mori S, Nakata Y, Fukuoka J, Amano S, Oohira A, Matsui H (2001) Expression of brain specific chondroitin sulfate proteoglycans, neurocan and phosphacan, in the developing and adult hippocampus of Ihara's epileptic rats. Brain Res 898:36-48
42. Kusakabe M, Mangiarini L, Laywell ED, Bates GP, Yoshiki A, Hiraiwa N, Inoue J, Steindler DA (2001) Loss of cortical and thalamic neuronal tenascin-C expression in a transgenic mouse expressing exon 1 of the human Huntington disease gene. J Comp Neurol 430:485-500
43. Lander C, Zhang H, Hockfield S (1998) Neurons produce a neuronal cell surface-associated chondroitin sulfate proteoglycan. J Neurosci 18:174-183
44. Lendvai D, Morawski M, Brückner G, Négyessy L, Baksa G, Glasz T, Patonay L, Matthews RT, Arendt T, Alpár A (2012) Perisynaptic aggrecan-based extracellular matrix coats in the human lateral geniculate body devoid of perineuronal nets. J Neurosci Res 90:376-387
45. Matthews RT, Gary SC, Zerillo C, Pratta M, Solomon K, Arner EC, Hockfield S (2000) Brain-enriched hyaluronan binding (BEHAB)/brevican cleavage in a glioma cell line is mediated by a disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS) family member. J Biol Chem 275:22695-22703
46. Matthews RT, Kelly GM, Zerillo CA, Gray G, Tiemeyer M, Hockfield S (2002) Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J Neurosci 22:7536-7547
47. McEwen BS (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22:105-122
48. McGuire PK, Hockfield S, Goldman-Rakic PS (1989) Distribution of cat-301 immunoreactivity in the frontal and parietal lobes of the macaque monkey. J Comp Neurol 288:280-296
49. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM (1997) Identification and characterization of the vesicular GABA transporter. Nature 389:870-876
50. McRae PA, Baranov E, Sarode S, Brooks-Kayal AR, Porter BE (2010) Aggrecan expression, a component of the inhibitory interneuron perineuronal net, is altered following an early-life seizure. Neurobiol Dis 39:439-448
51. Morawski M, Alpár A, Brückner G, Fiedler A, Jäger C, Gáti G, Stieler JT, Arendt T (2009) Chondroitin sulfate proteoglycan-based extracellular matrix in chicken (Gallus domesticus) brain. Brain Res 1275:10-23
52. Morawski M, Brückner G, Arendt T, Matthews RT (2012) Aggrecan: beyond cartilage and into the brain. Int J Biochem Cell Biol 44:690-693
53. Morawski M, Brückner G, Jäger C, Seeger G, Arendt T (2010) Neurons associated with aggrecan-based perineuronal nets are protected against tau pathology in subcortical regions in Alzheimer's disease. Neuroscience 169:1347-1363
54. Morawski M, Brückner G, Jäger C, Seeger G, Matthews R, Arendt T (2012) Involvement of perineuronal and perisynaptic extracellular matrix in Alzheimer's disease neuropathology. Brain Pathol 22:547-561
55. Morawski M, Brückner MK, Riederer P, Brückner G, Arendt T (2004) Perineuronal nets potentially protect against oxidative stress. Exp Neurol 188:309-315
56. Morawski M, Pavlica S, Seeger G, Grosche J, Kouznetsova E, Schliebs R, Brückner G, Arendt T (2010) Perineuronal nets are largely unaffected in Alzheimer model Tg2576 mice. Neurobiol Aging 31:1254-1256
57. Mulder J, Zilberter M, Pasquare SJ, Alpár A, Schulte G, Ferreira SG, Kofalvi A, Martin-Moreno AM, Keimpema E, Tanila H, Watanabe M, Mackie K, Hortobagyi T, de Ceballos ML, Harkany T (2011) Molecular reorganization of endocannabinoid signalling in Alzheimer's disease. Brain 134:1041-1060
58. O'Callaghan P, Sandwall E, Li JP, Yu H, Ravid R, Guan ZZ, van Kuppevelt TH, Nilsson LN, Ingelsson M, Hyman BT, Kalimo H, Lindahl U, Lannfelt L, Zhang X (2008) Heparan sulfate accumulation with Abeta deposits in Alzheimer's disease and Tg2576 mice is contributed by glial cells. Brain Pathol 18:548-561
59. Ojima H, Sakai M, Ohyama J (1998) Molecular heterogeneity of Vicia villosa-recognized perineuronal nets surrounding pyramidal and nonpyramidal neurons in the guinea pig cerebral cortex. Brain Res 786:274-280
60. Palop JJ, Mucke L (2009) Epilepsy and cognitive impairments in Alzheimer disease. Arch Neurol 66:435-440
61. Pavlov I, Rauvala H, Taira T (2006) Enhanced hippocampal GABAergic inhibition in mice overexpressing heparin-binding growth-associated molecule. Neuroscience 139:505-511
62. Perosa SR, Porcionatto MA, Cukiert A, Martins JR, Amado D, Nader HB, Cavalheiro EA, Leite JP, Naffah-Mazzacoratti MG (2002) Extracellular matrix components are altered in the hippocampus, cortex, and cerebrospinal fluid of patients with mesial temporal lobe epilepsy. Epilepsia 43(Suppl 5):159-161
63. Perosa SR, Porcionatto MA, Cukiert A, Martins JR, Passeroti CC, Amado D, Matas SL, Nader HB, Cavalheiro EA, Leite JP, Naffah-Mazzacoratti MG (2002) Glycosaminoglycan levels and proteoglycan expression are altered in the hippocampus of patients with mesial temporal lobe epilepsy. Brain Res Bull 58:509-516
64. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248-1251
65. Schnell SA, Staines WA, Wessendorf MW (1999) Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J Histochem Cytochem 47:719-730
66. Schüppel K, Brauer K, Härtig W, Grosche J, Earley B, Leonard BE, Brückner G (2002) Perineuronal nets of extracellular matrix around hippocampal interneurons resist destruction by activated microglia in trimethyltin-treated rats. Brain Res 958:448-453
67. Suzuki K, Katzman R, Korey SR (1965) Chemical studies on Alzheimer's disease. J Neuropathol Exp Neurol 24:211-224
68. Vidal E, Bolea R, Tortosa R, Costa C, Domenech A, Monleon E, Vargas A, Badiola JJ, Pumarola M (2006) Assessment of calcium-binding proteins (parvalbumin and calbindin D-28K) and perineuronal nets in normal and scrapie-affected adult sheep brains. J Virol Methods 136:137-146
69. Watanabe H, Kimata K, Line S, Strong D, Gao LY, Kozak CA, Yamada Y (1994) Mouse cartilage matrix deficiency (cmd) caused by a 7 bp deletion in the aggrecan gene. Nat Genet 7:154-157
70. Wegner F, Härtig W, Bringmann A, Grosche J, Wohlfarth K, Zuschratter W, Brückner G (2003) Diffuse perineuronal nets and modified pyramidal cells immunoreactive for glutamate and the GABA(A) receptor alpha1 subunit form a unique entity in rat cerebral cortex. Exp Neurol 184:705-714
71. Wu Y, Wu J, Lee DY, Yee A, Cao L, Zhang Y, Kiani C, Yang BB (2005) Versican protects cells from oxidative stress-induced apoptosis. Matrix Biol 24:3-13
72. Yamada H, Fredette B, Shitara K, Hagihara K, Miura R, Ranscht B, Stallcup WB, Yamaguchi Y (1997) The brain chondroitin sulfate proteoglycan brevican associates with astrocytes ensheathing cerebellar glomeruli and inhibits neurite outgrowth from granule neurons. J Neurosci 17:7784-7795
73. Yamaguchi Y (2000) Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 57:276-289