Glial fibrillary acidic protein isoform expression in plaque related astrogliosis in Alzheimer's disease

Neurobiology of Aging

Volumn 35, Issue 3, 2014, Pages 492-510

  Kamphuis, Willem ^a   Middeldorp, Jinte ^a,b   Kooijman, Lieneke ^a   Sluijs, Jacqueline A ^a   Kooi, Evert Jan ^a,c   Moeton, Martina ^a   Freriks, Michel ^a   Mizee, Mark R ^a,c   Hol, Elly M ^a,d,e  

^a ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Alzheimer's disease; Astrocytes; GFAP; Glial fibrillary acidic protein; Gliosis; Hippocampus; Intermediate filaments; Isoforms; Nestin; Plaques; Synemin; Vimentin

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN ALPHA; GLIAL FIBRILLARY ACIDIC PROTEIN BETA; GLIAL FIBRILLARY ACIDIC PROTEIN DELTA; GLIAL FIBRILLARY ACIDIC PROTEIN GAMMA; GLIAL FIBRILLARY ACIDIC PROTEIN KAPPA; GLIAL FIBRILLARY ACIDIC PROTEIN ZETA; RNA; UNCLASSIFIED DRUG;

ADULT; AGED; ALZHEIMER DISEASE; AMYLOID PLAQUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; AUTOPSY; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GENETIC TRANSFECTION; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; VERY ELDERLY; WESTERN BLOTTING;

ALZHEIMER'S DISEASE; ASTROCYTES; GFAP; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; HIPPOCAMPUS; INTERMEDIATE FILAMENTS; ISOFORMS; NESTIN; PLAQUES; SYNEMIN; VIMENTIN;

ALZHEIMER DISEASE; ASTROCYTES; CELLS, CULTURED; DISEASE PROGRESSION; GENE EXPRESSION; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; HUMANS; PLAQUE, AMYLOID; PROTEIN ISOFORMS; SEVERITY OF ILLNESS INDEX; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84889582306     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.09.035     Document Type: Article

References (74)

1. Allaman I., Gavillet M., Belanger M., Laroche T., Viertl D., Lashuel H.A., Magistretti P.J. Amyloid-beta aggregates cause alterations of astrocytic metabolic phenotype: impact on neuronal viability. J.Neurosci. 2010, 30:3326-3338.
2. Apelt J., Ach K., Schliebs R. Aging-related down-regulation of neprilysin, a putative beta-amyloid-degrading enzyme, in transgenic Tg2576 Alzheimer-like mouse brain is accompanied by an astroglial upregulation in the vicinity of beta-amyloid plaques. Neurosci. Lett. 2003, 339:183-186.
3. Bai X., Saab A.S., Huang W., Hoberg I.K., Kirchhoff F., Scheller A. Genetic background affects human glial fibrillary acidic protein promoter activity. PLoS One 2013, 8:e66873.
4. Blechingberg J., Holm I.E., Nielsen K.B., Jensen T.H., Jorgensen A.L., Nielsen A.L. Identification and characterization of GFAPkappa, a novel glial fibrillary acidic protein isoform. Glia 2007, 55:497-507.
5. Boer K., Middeldorp J., Spliet W.G., Razavi F., van Rijen P.C., Baayen J.C., Hol E.M., Aronica E. Immunohistochemical characterization of the out-of frame splice variants GFAP Delta164/Deltaexon 6 in focal lesions associated with chronic epilepsy. Epilepsy Res. 2010, 90:99-109.
6. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
7. Busuttil R.A., Garcia A.M., Reddick R.L., Dolle M.E., Calder R.B., Nelson J.F., Vijg J. Intra-organ variation in age-related mutation accumulation in the mouse. PLoS One 2007, 2:e876.
8. Carter S.F., Scholl M., Almkvist O., Wall A., Engler H., Langstrom B., Nordberg A. Evidence for astrocytosis in prodromal Alzheimer disease provided by 11C-deuterium-L-deprenyl: a multitracer PET paradigm combining 11C-Pittsburgh compound B and 18F-FDG. J.Nucl. Med. 2012, 53:37-46.
9. Chafekar S.M., Hoozemans J.J., Zwart R., Baas F., Scheper W. Abeta 1-42 induces mild endoplasmic reticulum stress in an aggregation state-dependent manner. Antioxid. Redox. Signal 2007, 9:2245-2254.
10. Chakrabarty P., Ceballos-Diaz C., Beccard A., Janus C., Dickson D., Golde T.E., Das P. IFN-gamma promotes complement expression and attenuates amyloid plaque deposition in amyloid beta precursor protein transgenic mice. J.Immunol. 2010, 184:5333-5343.
11. Condorelli D.F., Nicoletti V.G., Barresi V., Conticello S.G., Caruso A., Tendi E.A., Giuffrida Stella A.M. Structural features of the rat GFAP gene and identification of a novel alternative transcript. J.Neurosci. Res. 1999, 56:219-228.
12. Condorelli D.F., Nicoletti V.G., Dell'Albani P., Barresi V., Caruso A., Conticello S.G., Belluardo N., Giuffrida Stella A.M. GFAPbeta mRNA expression in the normal rat brain and after neuronal injury. Neurochem. Res. 1999, 24:709-714.
13. Datki Z., Papp R., Zadori D., Soos K., Fulop L., Juhasz A., Laskay G., Hetenyi C., Mihalik E., Zarandi M., Penke B. Invitro model of neurotoxicity of Abeta 1-42 and neuroprotection by a pentapeptide: irreversible events during the first hour. Neurobiol. Dis. 2004, 17:507-515.
14. Durrenberger P.F., Fernando F.S., Magliozzi R., Kashefi S.N., Bonnert T.P., Ferrer I., Seilhean D., Nait-Oumesmar B., Schmitt A., Gebicke-Haerter P.J., Falkai P., Grunblatt E., Palkovits M., Parchi P., Capellari S., Arzberger T., Kretzschmar H., Roncaroli F., Dexter D.T., Reynolds R. Selection of novel reference genes for use in the human central nervous system: a BrainNet Europe Study. Acta Neuropathol. 2012, 124:893-903.
15. Elobeid A., Bongcam-Rudloff E., Westermark B., Nister M. Effects of inducible glial fibrillary acidic protein on glioma cell motility and proliferation. J.Neurosci. Res. 2000, 60:245-256.
16. Feinstein D.L., Weinmaster G.A., Milner R.J. Isolation of cDNA clones encoding rat glial fibrillary acidic protein: expression in astrocytes and in Schwann cells. J.Neurosci. Res. 1992, 32:1-14.
17. Fleige S., Pfaffl M.W. RNA integrity and the effect on the real-time qRT-PCR performance. Mol. Aspects Med. 2006, 27:126-139.
18. Furman J.L., Sama D.M., Gant J.C., Beckett T.L., Murphy M.P., Bachstetter A.D., Van Eldik L.J., Norris C.M. Targeting astrocytes ameliorates neurologic changes in a mouse model of Alzheimer's disease. J.Neurosci. 2012, 32:16129-16140.
19. Gomez-Isla T., Hollister R., West H., Mui S., Growdon J.H., Petersen R.C., Parisi J.E., Hyman B.T. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann. Neurol. 1997, 41:17-24.
20. Halassa M.M., Haydon P.G. Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu. Rev. Physiol. 2010, 72:335-355.
21. Hanzel D.K., Trojanowski J.Q., Johnston R.F., Loring J.F. High-throughput quantitative histological analysis of Alzheimer's disease pathology using a confocal digital microscanner. Nat. Biotechnol. 1999, 17:53-57.
22. Hol E.M., Roelofs R.F., Moraal E., Sonnemans M.A., Sluijs J.A., Proper E.A., de Graan P.N., Fischer D.F., van Leeuwen F.W. Neuronal expression of GFAP in patients with Alzheimer pathology and identification of novel GFAP splice forms. Mol. Psychiatry 2003, 8:786-796.
23. Hu J., Akama K.T., Krafft G.A., Chromy B.A., Van Eldik L.J. Amyloid-beta peptide activates cultured astrocytes: morphological alterations, cytokine induction and nitric oxide release. Brain Res. 1998, 785:195-206.
24. Jiang S.X., Slinn J., Aylsworth A., Hou S.T. Vimentin participates in microgliaactivation and neurotoxicity in cerebral ischemia. J.Neurochem. 2012, 122:764-774.
25. Jing R., Wilhelmsson U., Goodwill W., Li L., Pan Y., Pekny M., Skalli O. Synemin is expressed in reactive astrocytes in neurotrauma and interacts differentially with vimentin and GFAP intermediate filament networks. J.Cell Sci. 2007, 120:1267-1277.
26. Kamphuis W., Mamber C., Moeton M., Kooijman L., Sluijs J.A., Jansen A.H., Verveer M., de Groot L.R., Smith V.D., Rangarajan S., Rodriguez J.J., Orre M., Hol E.M. GFAP isoforms in adult mouse brain with a focus on neurogenic astrocytes and reactive astrogliosis in mouse models of Alzheimer disease. PLoS. One 2012, 7:e42823.
27. Kanski, R., Van Strien, M.E., Van Tijn, P., Hol, E.M. A star is born: insights into the mechanism of astrogenesis. Cell. Mol. Life Sci., in press. http://www.ncbi.nlm.nih.gov/pubmed/23907612?dopt=Citation.
28. Kato S., Gondo T., Hoshii Y., Takahashi M., Yamada M., Ishihara T. Confocal observation of senile plaques in Alzheimer's disease: senile plaque morphology and relationship between senile plaques and astrocytes. Pathol. Int. 1998, 48:332-340.
29. Kim S., Coulombe P.A. Emerging role for the cytoskeleton as an organizer and regulator of translation. Nat. Rev. Mol. Cell Biol. 2010, 11:75-81.
30. Kraft A.W., Hu X., Yoon H., Yan P., Xiao Q., Wang Y., Gil S.C., Brown J., Wilhelmsson U., Restivo J.L., Cirrito J.R., Holtzman D.M., Kim J., Pekny M., Lee J.M. Attenuating astrocyte activation accelerates plaque pathogenesis in APP/PS1 mice. FASEB J. 2012, 27:187-198.
31. Lee H.U., Yamazaki Y., Tanaka K.F., Furuya K., Sokabe M., Hida H., Takao K., Miyakawa T., Fujii S., Ikenaka K. Increased astrocytic ATP release results in enhanced excitability of the hippocampus. Glia 2012, 61:210-224.
32. Lepekhin E.A., Eliasson C., Berthold C.H., Berezin V., Bock E., Pekny M. Intermediate filaments regulate astrocyte motility. J.Neurochem. 2001, 79:617-625.
33. Li L., Lundkvist A., Andersson D., Wilhelmsson U., Nagai N., Pardo A.C., Nodin C., Stahlberg A., Aprico K., Larsson K., Yabe T., Moons L., Fotheringham A., Davies I., Carmeliet P., Schwartz J.P., Pekna M., Kubista M., Blomstrand F., Maragakis N., Nilsson M., Pekny M. Protective role of reactive astrocytes in brain ischemia. J.Cereb. Blood Flow Metab. 2008, 28:468-481.
34. Li W., Vijg J. Measuring genome instability in aging - a mini-review. Gerontology 2012, 58:129-138.
35. Lu Y.B., Iandiev I., Hollborn M., Korber N., Ulbricht E., Hirrlinger P.G., Pannicke T., Wei E.Q., Bringmann A., Wolburg H., Wilhelmsson U., Pekny M., Wiedemann P., Reichenbach A., Kas J.A. Reactive glial cells: increased stiffness correlates with increased intermediate filament expression. FASEB J. 2011, 25:624-631.
36. Luco R.F., Allo M., Schor I.E., Kornblihtt A.R., Misteli T. Epigenetics in alternative pre-mRNA splicing. Cell 2011, 144:16-26.
37. Middeldorp J., Hol E.M. GFAP in health and disease. Prog. Neurobiol. 2011, 93:421-443.
38. Middeldorp J., Kamphuis W., Sluijs J.A., Achoui D., Leenaars C.H., Feenstra M.G., van T.P., Fischer D.F., Berkers C., Ovaa H., Quinlan R.A., Hol E.M. Intermediate filament transcription in astrocytes is repressed by proteasome inhibition. FASEB J. 2009, 23:2710-2726.
39. Middeldorp J., van den Berge S.A., Aronica E., Speijer D., Hol E.M. Specific human astrocyte subtype revealed by affinity purified GFAP antibody; unpurified serum cross-reacts with neurofilament-L in Alzheimer. PLoS. One 2009, 4:e7663.
40. Muramori F., Kobayashi K., Nakamura I. Aquantitative study of neurofibrillary tangles, senile plaques and astrocytes in the hippocampal subdivisions and entorhinal cortex in Alzheimer's disease, normal controls and non-Alzheimer neuropsychiatric diseases. Psychiatry Clin. Neurosci. 1998, 52:593-599.
41. Nawashiro H., Brenner M., Fukui S., Shima K., Hallenbeck J.M. High susceptibility to cerebral ischemia in GFAP-null mice. J.Cereb. Blood Flow Metab. 2000, 20:1040-1044.
42. Nawashiro H., Messing A., Azzam N., Brenner M. Mice lacking GFAP arehypersensitive to traumatic cerebrospinal injury. Neuroreport 1998, 9:1691-1696.
43. Nielsen A.L., Holm I.E., Johansen M., Bonven B., Jorgensen P., Jorgensen A.L. Anew splice variant of glial fibrillary acidic protein, GFAP epsilon, interacts with the presenilin proteins. J.Biol. Chem. 2002, 277:29983-29991.
44. Nielsen H.M., Veerhuis R., Holmqvist B., Janciauskiene S. Binding and uptake of A beta1-42 by primary human astrocytes invitro. Glia 2009, 57:978-988.
45. Oberheim N.A., Takano T., Han X., He W., Lin J.H., Wang F., Xu Q., Wyatt J.D., Pilcher W., Ojemann J.G., Ransom B.R., Goldman S.A., Nedergaard M. Uniquely hominid features of adult human astrocytes. J.Neurosci. 2009, 29:3276-3287.
46. Otani N., Nawashiro H., Fukui S., Ooigawa H., Ohsumi A., Toyooka T., Shima K., Gomi H., Brenner M. Enhanced hippocampal neurodegeneration after traumatic or kainate excitotoxicity in GFAP-null mice. J.Clin. Neurosci. 2006, 13:934-938.
47. Pallari H.M., Eriksson J.E. Intermediate filaments as signaling platforms. Sci. STKE 2006, 2006:e53.
48. Pekny M., Nilsson M. Astrocyte activation and reactive gliosis. Glia 2005, 50:427-434.
49. Perng M.D., Wen S.F., Gibbon T., Middeldorp J., Sluijs J., Hol E.M., Quinlan R.A. Glial fibrillary acidic protein filaments can tolerate the incorporation of assembly-compromised GFAP-delta, but with consequences for filament organization and alphaB-crystallin association. Mol. Biol. Cell 2008, 19:4521-4533.
50. Pihlaja R., Koistinaho J., Kauppinen R., Sandholm J., Tanila H., Koistinaho M. Multiple cellular and molecular mechanisms are involved in human Abeta clearance by transplanted adult astrocytes. Glia 2011, 59:1643-1657.
51. Pihlaja R., Koistinaho J., Malm T., Sikkila H., Vainio S., Koistinaho M. Transplanted astrocytes internalize deposited beta-amyloid peptides in a transgenic mouse model of Alzheimer's disease. Glia 2008, 56:154-163.
52. Potokar M., Kreft M., Li L., Daniel A.J., Pangrsic T., Chowdhury H.H., Pekny M., Zorec R. Cytoskeleton and vesicle mobility in astrocytes. Traffic 2007, 8:12-20.
53. Potokar M., Stenovec M., Gabrijel M., Li L., Kreft M., Grilc S., Pekny M., Zorec R. Intermediate filaments attenuate stimulation-dependent mobility of endosomes/lysosomes in astrocytes. Glia 2010, 58:1208-1219.
54. Roelofs R.F., Fischer D.F., Houtman S.H., Sluijs J.A., Van Haren W., van Leeuwen F.W., Hol E.M. Adult human subventricular, subgranular, and subpial zones contain astrocytes with a specialized intermediate filament cytoskeleton. Glia 2005, 52:289-300.
55. Salinero O., Moreno-Flores M.T., Ceballos M.L., Wandosell F. beta-amyloid peptide induced cytoskeletal reorganization in cultured astrocytes. J.Neurosci. Res. 1997, 47:216-223.
56. Sarria A.J., Lieber J.G., Nordeen S.K., Evans R.M. The presence or absence of a vimentin-type intermediate filament network affects the shape of the nucleus in human SW-13 cells. J. Cell Sci. 1994, 107:1593-1607.
57. Seth P., Koul N. Astrocyte, the star avatar: redefined. J.Biosci. 2008, 33:405-421.
58. Simpson J.E., Ince P.G., Lace G., Forster G., Shaw P.J., Matthews F., Savva G., Brayne C., Wharton S.B. Astrocyte phenotype in relation to Alzheimer-type pathology in the ageing brain. Neurobiol. Aging 2008, 31:578-590.
59. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol. 2010, 119:7-35.
60. Takizawa T., Gudla P.R., Guo L., Lockett S., Misteli T. Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. Genes Dev. 2008, 22:489-498.
61. Thal D.R., Rub U., Schultz C., Sassin I., Ghebremedhin E., Del T.K., Braak E., Braak H. Sequence of Abeta-protein deposition in the human medial temporal lobe. J.Neuropathol. Exp. Neurol. 2000, 59:733-748.
62. Thal D.R., Schultz C., Dehghani F., Yamaguchi H., Braak H., Braak E. Amyloid beta-protein (Abeta)-containing astrocytes are located preferentially near N-terminal-truncated Abeta deposits in the human entorhinal cortex. Acta Neuropathol. 2000, 100:608-617.
63. van den Berge S.A., Middeldorp J., Zhang C.E., Curtis M.A., Leonard B.W., Mastroeni D., Voorn P., van de Berg W.D., Huitinga I., Hol E.M. Longterm quiescent cells in the aged human subventricular neurogenic system specifically express GFAP-delta. Aging Cell 2010, 9:313-326.
64. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., DePaepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple interval control genes. Genome Biol. 2002, 3:0034.1-0034.11.
65. Vehmas A.K., Kawas C.H., Stewart W.F., Troncoso J.C. Immune reactive cells in senile plaques and cognitive decline in Alzheimer's disease. Neurobiol. Aging 2003, 24:321-331.
66. Verkhratsky A., Olabarria M., Noristani H.N., Yeh C.Y., Rodriguez J.J. Astrocytes in Alzheimer's disease. Neurotherapeutics 2010, 7:399-412.
67. Vincent A.J., Gasperini R., Foa L., Small D.H. Astrocytes in Alzheimer's disease: emerging roles in calcium dysregulation and synaptic plasticity. J.Alzheimers Dis. 2010, 22:699-714.
68. Wang Q., Ishikawa T., Michiue T., Zhu B.L., Guan D.W., Maeda H. Stability of endogenous reference genes in postmortem human brains for normalization of quantitative real-time PCR data: comprehensive evaluation using geNorm, NormFinder, and BestKeeper. Int. J. Legal Med. 2012, 126:943-952.
69. Wilhelmsson U., Li L., Pekna M., Berthold C.H., Blom S., Eliasson C., Renner O., Bushong E., Ellisman M., Morgan T.E., Pekny M. Absence of glialfibrillary acidic protein and vimentin prevents hypertrophy of astrocytic processes and improves post-traumatic regeneration. J.Neurosci. 2004, 24:5016-5021.
70. Wisniewski H.M., Wegiel J. Spatial relationships between astrocytes and classical plaque components. Neurobiol. Aging 1991, 12:593-600.
71. Wyss-Coray T., Loike J.D., Brionne T.C., Lu E., Anankov R., Yan F., Silverstein S.C., Husemann J. Adult mouse astrocytes degrade amyloid-beta invitro and in situ. Nat. Med. 2003, 9:453-457.
72. Xu K., Malouf A.T., Messing A., Silver J. Glial fibrillary acidic protein is necessary for mature astrocytes to react to beta-amyloid. Glia 1999, 25:390-403.
73. Yoshida T., Tomozawa Y., Arisato T., Okamoto Y., Hirano H., Nakagawa M. The functional alteration of mutant GFAP depends on the location of the domain: morphological and functional studies using astrocytoma-derived cells. J.Hum. Genet. 2007, 52:362-369.
74. Zelenika D., Grima B., Brenner M., Pessac B. Anovel glial fibrillary acidic protein mRNA lacking exon 1. Brain Res. Mol. Brain Res. 1995, 30:251-258.