The neuronal extracellular matrix restricts distribution and internalization of aggregated Tau-protein

Neuroscience

Volumn 313, Issue , 2016, Pages 225-235

  Suttkus, A ^a   Holzer, M ^a   Morawski, M ^a   Arendt, T ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Alzheimer's disease; Extracellular matrix; Neuroprotection; Perineuronal nets; Spreading; Tau

Indexed keywords

AGGRECAN; CELL PROTEIN; PROTEIN HAPLN1; TAU PROTEIN; TENASCIN; TENASCIN R; UNCLASSIFIED DRUG; LINK PROTEIN; MAPT PROTEIN, HUMAN; MAPT PROTEIN, MOUSE; PROTEOGLYCAN; RECOMBINANT PROTEIN; SCLEROPROTEIN;

ADULT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; INTERNALIZATION; MALE; MOUSE; NONHUMAN; PERINEURONAL NET; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; ANIMAL; C57BL MOUSE; ESCHERICHIA COLI; GENETICS; HUMAN; INTRACELLULAR SPACE; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PHYSIOLOGY; PROTEIN MULTIMERIZATION; SOMATOSENSORY CORTEX; TISSUE CULTURE TECHNIQUE;

AGGRECANS; ANIMALS; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FEMALE; HUMANS; INTRACELLULAR SPACE; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; PROTEIN MULTIMERIZATION; PROTEOGLYCANS; RECOMBINANT PROTEINS; SOMATOSENSORY CORTEX; TAU PROTEINS; TENASCIN; TISSUE CULTURE TECHNIQUES;

EID: 84949293137     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.11.040     Document Type: Article

References (43)

1. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991, 82:239-259.
2. Braak H., Del Tredici K., Rub U., de Vos R.A., Jansen Steur E.N., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003, 24:197-211.
3. Bramblett G.T., Goedert M., Jakes R., Merrick S.E., Trojanowski J.Q., Lee V.M. Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 1993, 10:1089-1099.
4. Bruckner G., Grosche J. Perineuronal nets show intrinsic patterns of extracellular matrix differentiation in organotypic slice cultures. Exp Brain Res 2001, 137:83-93.
5. Bruckner G., Hausen D., Hartig W., Drlicek M., Arendt T., Brauer K. Cortical areas abundant in extracellular matrix chondroitin sulphate proteoglycans are less affected by cytoskeletal changes in Alzheimer's disease. Neuroscience 1999, 92:791-805.
6. Bruckner G., Grosche J., Schmidt S., Hartig W., Margolis R.U., Delpech B., Seidenbecher C.I., Czaniera R., Schachner M. Postnatal development of perineuronal nets in wild-type mice and in a mutant deficient in tenascin-R. J Comp Neurol 2000, 428:616-629.
7. Carulli D., Pizzorusso T., Kwok J.C., Putignano E., Poli A., Forostyak S., Andrews M.R., Deepa S.S., Glant T.T., Fawcett J.W. Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 2010, 133:2331-2347.
8. Chandran P.L., Horkay F. Aggrecan, an unusual polyelectrolyte: review of solution behavior and physiological implications. Acta Biomater 2012, 8:3-12.
9. Chow V.W., Mattson M.P., Wong P.C., Gleichmann M. An overview of APP processing enzymes and products. NeuroMol Med 2010, 12:1-12.
10. Clavaguera F., Bolmont T., Crowther R.A., Abramowski D., Frank S., Probst A., Fraser G., Stalder A.K., Beibel M., Staufenbiel M., Jucker M., Goedert M., Tolnay M. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 2009, 11:909-913.
11. Czipri M., Otto J.M., Cs-Szabo G., Kamath R.V., Vermes C., Firneisz G., Kolman K.J., Watanabe H., Li Y., Roughley P.J., Yamada Y., Olsen B.R., Glant T.T. Genetic rescue of chondrodysplasia and the perinatal lethal effect of cartilage link protein deficiency. J Biol Chem 2003, 278:39214-39223.
12. Flach K., Hilbrich I., Schiffmann A., Gartner U., Kruger M., Leonhardt M., Waschipky H., Wick L., Arendt T., Holzer M. Tau oligomers impair artificial membrane integrity and cellular viability. J Biol Chem 2012, 287:43223-43233.
13. Frischknecht R., Heine M., Perrais D., Seidenbecher C.I., Choquet D., Gundelfinger E.D. Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 2009, 12:897-904.
14. Frost B., Jacks R.L., Diamond M.I. Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 2009, 284:12845-12852.
15. Giamanco K.A., Matthews R.T. Deconstructing the perineuronal net: cellular contributions and molecular composition of the neuronal extracellular matrix. Neuroscience 2012, 218:367-384.
16. Giamanco K.A., Morawski M., Matthews R.T. Perineuronal net formation and structure in aggrecan knockout mice. Neuroscience 2010, 170:1314-1327.
17. Hartig W., Derouiche A., Welt K., Brauer K., Grosche J., Mader M., Reichenbach A., Bruckner G. 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 1999, 842:15-29.
18. Hockfield S., Kalb R.G., Zaremba S., Fryer H. Expression of neural proteoglycans correlates with the acquisition of mature neuronal properties in the mammalian brain. Cold Spring Harb Symp Quant Biol 1990, 55:505-514.
19. Holmes B.B., DeVos S.L., Kfoury N., Li M., Jacks R., Yanamandra K., Ouidja M.O., Brodsky F.M., Marasa J., Bagchi D.P., Kotzbauer P.T., Miller T.M., Papy-Garcia D., Diamond M.I. Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc Natl Acad Sci USA 2013, 110:E3138-3147.
20. Hrabetova S., Masri D., Tao L., Xiao F., Nicholson C. Calcium diffusion enhanced after cleavage of negatively charged components of brain extracellular matrix by chondroitinase ABC. J Physiol 2009, 587:4029-4049.
21. Jucker M., Walker L.C. Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders. Ann Neurol 2011, 70:532-540.
22. Kfoury N., Holmes B.B., Jiang H., Holtzman D.M., Diamond M.I. Trans-cellular propagation of Tau aggregation by fibrillar species. J Biol Chem 2012, 287:19440-19451.
23. McRae P.A., Rocco M.M., Kelly G., Brumberg J.C., Matthews R.T. Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J Neurosci 2007, 27:5405-5413.
24. Medina M., Avila J. The role of extracellular Tau in the spreading of neurofibrillary pathology. Front Cell Neurosci 2014, 8:113.
25. Miyata S., Nishimura Y., Nakashima T. Perineuronal nets protect against amyloid beta-protein neurotoxicity in cultured cortical neurons. Brain Res 2007, 1150:200-206.
26. Morawski M., Bruckner M.K., Riederer P., Bruckner G., Arendt T. Perineuronal nets potentially protect against oxidative stress. Exp Neurol 2004, 188:309-315.
27. Morawski M., Bruckner G., Jager C., Seeger G., Arendt T. Neurons associated with aggrecan-based perineuronal nets are protected against tau pathology in subcortical regions in Alzheimer's disease. Neuroscience 2010, 169:1347-1363.
28. Morawski M., Bruckner G., Jager C., Seeger G., Matthews R.T., Arendt T. Involvement of perineuronal and perisynaptic extracellular matrix in Alzheimer's disease neuropathology. Brain Pathol 2012, 22:547-561.
29. Morawski M., Dityatev A., Hartlage-Rubsamen M., Blosa M., Holzer M., Flach K., Pavlica S., Dityateva G., Grosche J., Bruckner G., Schachner M. Tenascin-R promotes assembly of the extracellular matrix of perineuronal nets via clustering of aggrecan. Philos Trans R Soc Lond B Biol Sci 2014, 369.
30. Nowicka D., Soulsby S., Skangiel-Kramska J., Glazewski S. Parvalbumin-containing neurons, perineuronal nets and experience-dependent plasticity in murine barrel cortex. Eur J Neurosci 2009, 30:2053-2063.
31. Selkoe D.J. Toward a comprehensive theory for Alzheimer's disease. Hypothesis: Alzheimer's disease is caused by the cerebral accumulation and cytotoxicity of amyloid beta-protein. Ann N Y Acad Sci 2000, 924:17-25.
32. Selkoe D.J. Folding proteins in fatal ways. Nature 2003, 426:900-904.
33. Stoppini L., Buchs P.A., Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 1991, 37:173-182.
34. Suttkus A., Rohn S., Jäger C., Arendt T., Morawski M. Neuroprotection against iron-induced cell death by perineuronal nets - an in vivo analysis of oxidative stress. Am J Neurodegener Dis 2012, 1:122-129.
35. Suttkus A., Rohn S., Weigel S., Glockner P., Arendt T., Morawski M. Aggrecan, link protein and tenascin-R are essential components of the perineuronal net to protect neurons against iron-induced oxidative stress. Cell Death Dis 2014, 5:e1119.
36. Sykova E., Nicholson C. Diffusion in brain extracellular space. Physiol Rev 2008, 88:1277-1340.
37. Sykova E., Jendelova P., Herynek V. MR tracking of stem cells in living recipients. Methods Mol Biol 2009, 549:197-215.
38. Tomassy G.S., Berger D.R., Chen H.H., Kasthuri N., Hayworth K.J., Vercelli A., Seung H.S., Lichtman J.W., Arlotta P. Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex. Science 2014, 344:319-324.
39. Vogt C., Vogt O. Importance of neuroanatomy in the field of neuropathology. Neurology 1951, 1:205-218.
40. Watanabe H., Nakata K., Kimata K., Nakanishi I., Yamada Y. Dwarfism and age-associated spinal degeneration of heterozygote cmd mice defective in aggrecan. Proc Natl Acad Sci USA 1997, 94:6943-6947.
41. Weber P., Bartsch U., Rasband M.N., Czaniera R., Lang Y., Bluethmann H., Margolis R.U., Levinson S.R., Shrager P., Montag D., Schachner M. Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J Neurosci 1999, 19:4245-4262.
42. Wu Y., Wu J., Lee D.Y., Yee A., Cao L., Zhang Y., Kiani C., Yang B.B. Versican protects cells from oxidative stress-induced apoptosis. Matrix Biol 2005, 24:3-13.
43. Yamaguchi Y. Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 2000, 57:276-289.