In vitro treatments with ceftriaxone promote elimination of mutant glial fibrillary acidic protein and transcription down-regulation

Experimental Cell Research

Volumn 316, Issue 13, 2010, Pages 2152-2165

  Bachetti, Tiziana ^a   Di Zanni, Eleonora ^a   Balbi, Pietro ^b   Bocca, Paola ^a   Prigione, Ignazia ^a   Deiana, Giovanni A ^c   Rezzani, Antonella ^b   Ceccherini, Isabella ^a   Sechi, GianPietro ^c  

^a G GASLINI INSTITUTE   (Italy)

^b IRCCS   (Italy)

^c UNIVERSITY OF SASSARI   (Italy)

Author keywords

Alexander disease; Ceftriaxone; Glial fibrillary acidic protein; Small heat shock proteins; Transcriptional regulation; Ubiquitin proteasome system

Indexed keywords

ALPHA CRYSTALLIN; BETA CRYSTALLIN; CEFTRIAXONE; GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT SHOCK PROTEIN 27; MUTANT PROTEIN; PROTEASOME;

ALEXANDER DISEASE; ARTICLE; ASTROCYTE; AUTOPHAGY; CONTROLLED STUDY; DEGENERATIVE DISEASE; DOWN REGULATION; DRUG MECHANISM; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; NEUROPROTECTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN AGGREGATION; TRANSCRIPTION REGULATION; UBIQUITINATION; UPREGULATION;

ANIMALIA; MUS;

EID: 77953812401     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.05.005     Document Type: Article

References (49)

1. Alexander W.-S. Progressive fibrinoid degeneration of fibrillary astrocytes associated with mental retardation in hydrocephalic infant. Brain 1949, 72:373-381.
2. Brenner M., Goldman J.E., Quinlan R.A., Messing A. Alexander disease: a genetic disorder of astrocytes. Astrocytes in (patho)physiology of the nervous system 2009, 591-648. Springer. V. Parpura, P. Haydon (Eds.).
3. Haed M.W., Corbin E., Goldman J.E. Overexpression and abnormal modification of the stress alpha B-crystallin anf HSP27 in Alexander disease. Am. J. Pathol. 1993, 143:1743-1753.
4. Iwaki T., Kume-Iwaki A., Liem R.K., Goldman J.E. Alpha B-crystallin is expressed in non-lenticular tissues and accumulates in Alexander's disease brain. Cell 1989, 57:71-78.
5. Tomokane N., Iwaki T., Tateishi J., Iwaki A., Goldman J.E. Rosenthal fibers share epitopes with alpha B-crystallin, glial fibrillary acidic protein, and ubiquitin, but not with vimentin: immunoelectron microscopy with colloidal gold. Am. J. Pathol. 1991, 138:875-885.
6. Brenner M., Johnson A.B., Boespflug-Tangury O., Rodriguez D., Goldman J., Messing A. Mutations in GFAP, encoding glial fibrillary acidic protein, are associated with Alexander disease. Nat. Genet. 2001, 27:117-120.
7. Caroli F., Biancheri R., Seri M., Rossi A., Pessagno A., Corsolini F., Savasta S., Romano S., Antonelli C., Romano A., Pareyson D., Gambero P., Uziel G., Ravazzolo R., Ceccherini I., Filocamo M. GFAP mutations and polymorphisms in 13 unrelated Italian patients affected by Alexander disease. Clin. Genet. 2007, 72:427-433.
8. Li R., Johnson A.B., Salomons G., Goldman J.E., Naidu S., Quinlan R., Cree B., Ruyle S.Z., Banwell B., D'Hooghe M., Siebert J.R., Rolf C.M., Cox H., Reddy A., Gutierrez-Solana L.G., Collins A., Weller R.O., Messing A., Van der Knaap M.S., Brenner M. Glial fibrillary acidic protein mutations in infantile, juvenile and adult forms of Alexander disease. Ann. Neurol. 2005, 57:310-325.
9. Rodriguez D., Gauthier F., Bertini E., Bugiani M., N'guyen S., Goizet C., Gelot A., Surtees R., Pedespan J.M., Hernandorena X., Troncoso M., Uziel G., Messing A., Ponsot G., Pham-Dinh D., Dautigny A., Boespflug-Tanguy O. Infantile Alexander disease: spectrum of GFAP mutations and genotype-phenotype correlation. Am. J. Hum. Genet. 2001, 69:1134-1140.
10. Bachetti T., Caroli F., Bocca P., Prigione I., Balbi P., Biancheri R., Filocamo M., Mariotti C., Pareyson D., Ravazzolo R., Ceccherini I. Mild functional effects of a novel GFAP mutant allele identified in a familial case of adult onset Alexander disease. Eur. J. Hum. Genet. 2008, 16:462-470.
11. Eliasson C., Sahlgren C., Berthold C.-H., Stakenberg J., Celis J.E., Betsholtz C., Eiksson J.E., Pekny M. Intermediate filaments protein partnership in astrocytes. J. Biol. Chem. 1999, 34:23996-24006.
12. Hsiao V.C., Tian R., Long H., Perng M.D., Brenner M., Quinlan R.A., Goldman J.E. Alexander-disease mutation of GFAP causes filament disorganization and decreased solubility of GFAP. J. Cell Sci. 2005, 118:2057-2065.
13. Tang G., Xu Z., Goldman J.E. Synergistic effects of the SAPK/JNK & the proteasome pathways on GFAP accumulation in Alexander disease. J. Biol. Chem. 2006, 281:38634-38643.
14. Messing A., Head M.W., Galles K., Galbreath E.J., Goldman J.E., Brenner M. Fatal encephalopathy with astrocytes inclusions in GFAP transgenic mice. Am. J. Pathol. 1998, 152:391-398.
15. Cho W., Messing A. Properties of astrocytes cultured from GFAP over-expressing and GFAP mutant mice. Exp. Cell Res. 2009, 315:1260-1272.
16. Koyama Y., Goldman J. Formation of GFAP cytoplasmic inclusions in astrocytes and their disaggregation by aB-crystallin. Am. J. Pathol. 1999, 154:1563-1572.
17. Hagemann T.L., Boelens W.C., Wawrousek E.F., Messing A. Suppression of GFAP toxicity by alphaB-crystallin in mouse models of Alexander disease. Hum. Mol. Genet. 2009, 18:1190-1199.
18. Perng M.D., Cairns L., van den Ijsse P., Prescott A., Hutcheson A.M., Quinlan R.A. Intermediate filament interactions can be altered by HSP27 and alphaB-crystallin. J. Cell Sci. 1999, 112:2099-2112.
19. Wyttenbach A., Sauvageot O., Carmichael J., Diaz-Latoud C., Arrigo A.P., Rubinsztein D.C. Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin. Hum. Mol. Genet. 2002, 11:1137-1151.
20. Zourlidou A., Payne Smith M.D., Latchman D.S. HSP27 but not HSP70 has a potent protective effect against alpha-synuclein-induced cell death in mammalian neuronal cells. J. Neurochem. 2004, 88:1439-1448.
21. Perrin V., Régulier E., Abbas-Terki T., Hassig R., Brouillet E., Aebischer P., Luthi-Carter R., Déglon N. Neuroprotection by Hsp104 and Hsp27 in lentiviral-based rat models of Huntington's disease. Mol. Ther. 2007, 15:903-911.
22. Zhai J., Lin H., Julien J.P., Schlaepfer W.W. Disruption of neurofilament network with aggregation of light neurofilament protein: a common pathway leading to motor neuron degeneration due to Charcot-Marie-Tooth disease-linked mutations in NFL and HSPB1. Hum. Mol. Genet. 2007, 16:3103-3116.
23. Goldbaum O., Riedel M., Stahnke T., Richter-Landsberg C. The small heat shock protein HSP25 protects astrocytes against stress induced by proteasomal inhibition. Glia 2009, 57:1566-1577.
24. Mignot C., Delarasse C., Escaich S., Della Gaspera B., Noé E., Colucci-Guyon E., Babinet C., Pekny M., Vicart P., Boespflug-Tanguy O., Dautigny A., Rodriguez D., Pham-Dinh D. Dynamics of mutated GFAP aggregates revealed by real-time imaging of an astrocyte model of Alexander disease. Exp. Cell Res. 2007, 313:2766-2779.
25. Chu K., Lee S.T., Sinn D.I., Ko S.Y., Kim E.H., Kim J.M., Kim D.J., Park D.K., Joung K.H., Song E.C., Lee S.K., Kim M., Roh J.K. Pharmacological induction of ischemic tolerance by glutamate transporter-1 (EAAT2) upregulation. Stroke 2007, 38:177-182.
26. Lipski J., Wan C.K., Bai J.Z., Pi R., Li D., Donnely D. Neuroprotective potential of ceftriaxone in in vitro models of stroke. Neuroscience 2007, 146:617-629.
27. Melzer N., Meuth S.G., Torres-Salazar D., Bittner S., Zozulya A.L., Weidenfeller C., Kotsiari A., Stangel M., Fahlke C., Wiendl H. A ?-lactam antibiotic dampens excitotoxic inflammatory CNS damage in a mouse model of multiple sclerosis. PLoS ONE 2008, 3:e3149.
28. Miller B.R., Dorner J.L., Shou M., Sari Y., Barton S.J., Sengelaub D.R., Kennedy R.T., Rebec G.V. Up-regulation of GLT1 expression increases glutamate uptake and attenuates the Huntington's disease phenotype in the R6/2 mouse. Neuroscience 2008, 153:329-337.
29. Ouyang Y.B., Voloboueva L.A., Xu L.J., Giffard R.G. Selective dysfunction of hippocampal CA1 astrocytes contributes to delayed neuronal damage after transient forebrain ischemia. J. Neurosci. 2007, 27:4253-4260.
30. Rothstein J.D., Patel S., Regan M.R., Haenggeli C., Huang Y.H., Bergles D.E., Jin L., Dykes Hoberg M., Vidensky S., Chung D.S., Toan S.V., Bruijn L.I., Su Z.Z., Gupta P., Fisher P.B. ?-Lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 2005, 433:73-77.
31. Rumbaugh J.A., Li G., Rothstein J., Nath A. Ceftriaxone protects against the neurotoxicity of human immunodeficiency virus proteins. J. Neurovirol. 2007, 13:168-172.
32. Lee S.G., Su Z.Z., Emdad L., Gupta P., Sarkar D., Borjabad A., Volsky D.J., Fisher P.B. Mechanism of ceftriaxone induction of excitatory amino acid transporter- expression and glutamate uptake in primary human astrocytes. J. Biol. Chem. 2008, 283:13116-13123.
33. Lewerenz J., Albrecht P., Tran Tine M.-L., Henke P., Karumbayaram S., Kornblum H.I., Wiedau-Pazos M., Schubert D., Maher P., Methner A. Induction of Nrf2 and xCT are involved in the action of the neuroprotective antibiotic ceftriaxone in vitro. J. Neurochem. 2009, 111:332-343.
34. Sechi G.P., Balbi P., Bachetti T., Matta M., Serra A., Deiana G.A., Di Zanni E., Ceccherini I. Ceftriaxone has a therapeutic role in Alexander disease. Prog. Neuropsychopharmacol. Biol. Psychiatry 2010, 34:416-417.
35. Bryantsev A.L., Kurchashova S.Y., Golyshev S.A., Polyakov V.Y., Wunderink H.F., Kanon B., Budagova K.R., Kabakov A.E., Kampinga H.H. Regulation of stress-induced intracellular sorting and chaperone function of Hsp27 (HspB1) in mammalian cells. Biochem. J. 2007, 407:407-417.
36. Perng M.D., Su M., Wen S.F., Li R., Gibbon T., Prescott A.R., Brenner M., Quinlan R.A. The Alexander disease-causing glial fibrillary acidic protein mutant, R416W, accumulates into Rosenthal fibers by a pathway that involves filament aggregation and the association of ?B-crystallin and HSP27. Am. J. Hum. Genet. 2006, 79:197-213.
37. Carratelli Romano C., Benedetto N., Catania M.R., Rizzo A., Gallè F., Losi E., Hasty D.L., Rossano F. Commonly used antibiotics induce expression of Hsp27 and Hsp 60 and protect human lymphocytes from apoptosis. Int. Immunopharmacol. 2004, 4:1067-1073.
38. Parcellier A., Schmitt E., Gurbuxani S., Seigneurin-Berny D., Pance A., Chantôme A., Plenchette S., Khochbin S., Solary E., Garrido C. HSP27 is a ubiquitin-binding protein involved in I-?B? proteasomal degradation. Mol. Cell. Biol. 2003, 23:5790-5802.
39. Parcellier A., Brunet M., Schmitt E., Col E., Didelot C., Hammann A., Nakayama K., Khochbin S., Solary E., Garrido C. HSP27 favors ubiquitination and proteasomal degradation of p27Kip1 and helps S-phase re-entry in stressed cells. FASEB J. 2006, 20:1179-1193.
40. Tang G., Yue Z., Talloczy Z., Goldman J.E. Adaptive autophagy in Alexander disease-affected astrocytes. Autophagy 2008, 4:701-703.
41. Wu J., Dang Y., Su W., Liu C., Ma H., Shan Y., Pei Y., Wan B., Guo J., Yu L. Molecular cloning and characterization of rat LC3A and LC3B-two novel markers of autophagosome. Biochem. Biophys. Res. Commun. 2006, 339:437-442.
42. Middeldorp J., Kamphius W., Sluijs J.A., Achoui D., Leenaars C.H., Feenstra M.G., van Tijn P., Fisher D.F., Beckers C., Ovaa H., Quinlan R.A., Hol E.M. Intermediated filament transcription in astrocytes is repressed by proteasome inhibition. FASEB J. 2009, 23:2710-2726.
43. Bae M.K., Kim S.R., Lee H.J., Wee H.J., Yoo M.A., Ock Oh S., Baek S.Y., Kim B.S., Kim J.B., Yoon S., Bae S.K. Aspirin-induced blockade of NF-kappaB activity restrains up-regulation of glial fibrillary acidic protein in human astroglial cells. Biochem. Biophys. Acta 2006, 1763:282-289.
44. Yoshida T., Sasayama H., Nakagawa M. The process of inducing GFAP aggregates in astrocytoma-derived cells is different between R239C and R416W mutant GFAP, A time-lapse recording study. Neurosci. Lett. 2009, 458:11-14.
45. Nau R., Prange H.W., Muth P., Mahr G., Menck S., Kolenda H., Sörgel F. Passage of cefotaxime and ceftriaxone into cerebrospinal fluid of patients with uninflamed meninges. Antimicrob. Agents Chemother. 1993, 37:1518-1524.
46. Read D.E., Gorman A.M. Heat shoch protein 27 in neuronal survival and neurite outgrowth. Biochem. Biophys. Res. Commun. 2009, 382:6-8.
47. Kwak M.K., Itoh K., Yamamoto M., Kensler T.W. Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Mol. Cell. Biol. 2002, 22:2883-2892.
48. Tang G., Perng M.D., Wilk S., Quinlan R., Goldman J.E. Oligomers of mutant glial fibrillary acidic protein (GFAP) inhibit the proteasome system in Alexander disease astrocytes, and the small heat shock protein alphaB-crystallin reverses the inhibition. J. Biol. Chem. 2010, 285:10527-10537.
49. Tang G., Yue Z., Talloczy Z., Hagemann T., Cho W., Messing A., Sulzer D.L., Goldman J.E. Autophagy induced by Alexander disease-mutant GFAP accumulation is regulated by p38/MAPK and mTOR signaling pathways. Hum. Mol. Genet. 2008, 17:1540-1555.