THE MOLECULAR MECHANISMS OF NEURODEGENERATION
gail_johnsonvoll@urmc.rochester.edu

Our laboratory has a longstanding interest in the pathogenic processes in Alzheimer disease and Huntington disease, and more recently in stroke. For our studies we use a wide variety of different approaches from in vitro enzyme assays with purified proteins, to studies in whole animals. This broad-based approach allows us to translate what we learn about a process or signaling pathway at the molecular level to the in vivo situation. Each of the 3 areas of research that are ongoing in our lab is discussed briefly below.
Two hallmarks of the Alzheimer's disease brain are the intracellular neurofibrillary tangles composed primarily of the protein tau in a pathologically modified state and the extracellular senile plaques composed primarily of the Abeta peptide. There is compelling evidence that aberrant posttranslational processing of tau is central to the disease process. Nonetheless, the mechanisms by which pathological changes in tau result in impaired neuronal function and contribute to cell death processes in Alzheimer disease have not been fully elucidated. A major focus in our lab is on understanding the cellular targets of Alzheimer disease relevant forms of tau. Currently we are investigating how tau that is abnormally phosphorylated and/or proteolytically processed impacts mitochondrial dynamics and function. We and others have exciting new data suggesting that the mitochondria may be a crucial downstream target of pathological tau and contribute to the neurodegenerative processes.
Our lab has a well-established and longstanding interest in understanding the regulation and function of transglutaminase 2 (TG2) in neuronal cell death and survival. Recently we found that TG2 in its capacity as a scaffold protein binds HIF1beta, attenuates HIF signaling, attenuates the expression of specific HIF responsive pro-apoptotic genes and protects neurons from ischemia-induced cell death. In addition, we have found that exogenous expression of TG2 in neurons in a mouse is protective against stroke damage. Therefore we are investigating the mechanisms by which TG2 attenuates HIF signaling and protects against ischemia-induced cell death.

Huntington disease is an autosomal dominant neurodegenerative disease caused by a pathological expansion of the polyglutamine domain in the huntingtin protein. There is convincing evidence that both transcriptional dysregulation and mitochondrial dysfunction play pivotal roles in the pathogenesis of Huntington disease. In recent studies we have found that mitochondria from mutant huntingtin expressing striatal cells take up significantly less calcium than mitochondria from wild type cells and are significantly more sensitive to calcium-induced decreases in respiration. We have also found that the expression of specific mitochondrial and anti-oxidant genes are downregulated in Huntington disease cell models. Therefore we are now investigating: (1) whether mutant huntingtin impairs the ability of mitochondria to appropriately maintain pH and regulate redox status and if this contributes to the calcium handling defects that result in respiratory deficits and increased sensitivity to calcium-induced permeability transition pore opening, (2) whether a decrease in the transcriptional activity PPARgamma by mutant huntingtin compromises mitochondrial metabolism and function and (3) whether activation of PPARgamma ameliorates mitochondrial dysfunction in mouse Huntington's disease models.

• Jin YN, Chen PC, Watson JA, Walters BJ, Phillips SE, Green K, Schmidt R, Wilson JA, Johnson GV, Roberson ED, Dobrunz LE, Wilson SM. Usp14 Deficiency Increases Tau Phosphorylation without Altering Tau Degradation or Causing Tau-Dependent Deficits. PLoS One. 2012; 7(10):e47884.
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• Gundemir S, Colak G, Feola J, Blouin R, Johnson GV. Transglutaminase 2 facilitates or ameliorates HIF signaling and ischemic cell death depending on its conformation and localization. Biochim Biophys Acta. 2013 Jan; 1833(1):1-10.
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• Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, Al-Zeer MA, Albert ML, Albin RL, Alegre-Abarrategui J, Aleo MF, Alirezaei M, Almasan A, Almonte-Becerril M, Amano A, Amaravadi R, Amarnath S, Amer AO, Andrieu-Abadie N, Anantharam V, Ann DK, Anoopkumar-Dukie S, Aoki H, Apostolova N, Auberger P, Baba M, Backues SK, Baehrecke EH, Bahr BA, Bai XY, Bailly Y, Baiocchi R, Baldini G, Balduini W, Ballabio A, Bamber BA, Bampton ET, Bánhegyi G, Bartholomew CR, Bassham DC, Bast RC, Batoko H, Bay BH, Beau I, Béchet DM, Begley TJ, Behl C, Behrends C, Bekri S, Bellaire B, Bendall LJ, Benetti L, Berliocchi L, Bernardi H, Bernassola F, Besteiro S, Bhatia-Kissova I, Bi X, Biard-Piechaczyk M, Blum JS, Boise LH, Bonaldo P, Boone DL, Bornhauser BC, Bortoluci KR, Bossis I, Bost F, Bourquin JP, Boya P, Boyer-Guittaut M, Bozhkov PV, Brady NR, Brancolini C, Brech A, Brenman JE, Brennand A, Bresnick EH, Brest P, Bridges D, Bristol ML, Brookes PS, Brown EJ, Brumell JH, Brunetti-Pierri N, Brunk UT, Bulman DE, Bultman SJ, Bultynck G, Burbulla LF, Bursch W, Butchar JP, Buzgariu W, Bydlowski SP, Cadwell K, Cahová M, Cai D, Cai J, Cai Q, Calabretta B, Calvo-Garrido J, Camougrand N, Campanella M, Campos-Salinas J, Candi E, Cao L, Caplan AB, Carding SR, Cardoso SM, Carew JS, Carlin CR, Carmignac V, Carneiro LA, Carra S, Caruso RA, Casari G, Casas C, Castino R, Cebollero E, Cecconi F, Celli J, Chaachouay H, Chae HJ, Chai CY, Chan DC, Chan EY, Chang RC, Che CM, Chen CC, Chen GC, Chen GQ, Chen M, Chen Q, Chen SS, Chen W, Chen X, Chen X, Chen X, Chen YG, Chen Y, Chen Y, Chen YJ, Chen Z, Cheng A, Cheng CH, Cheng Y, Cheong H, Cheong JH, Cherry S, Chess-Williams R, Cheung ZH, Chevet E, Chiang HL, Chiarelli R, Chiba T, Chin LS, Chiou SH, Chisari FV, Cho CH, Cho DH, Choi AM, Choi D, Choi KS, Choi ME, Chouaib S, Choubey D, Choubey V, Chu CT, Chuang TH, Chueh SH, Chun T, Chwae YJ, Chye ML, Ciarcia R, Ciriolo MR, Clague MJ, Clark RS, Clarke PG, Clarke R, Codogno P, Coller HA, Colombo MI, Comincini S, Condello M, Condorelli F, Cookson MR, Coombs GH, Coppens I, Corbalan R, Cossart P, Costelli P, Costes S, Coto-Montes A, Couve E, Coxon FP, Cregg JM, Crespo JL, Cronjé MJ, Cuervo AM, Cullen JJ, Czaja MJ, D'Amelio M, Darfeuille-Michaud A, Davids LM, Davies FE, De Felici M, de Groot JF, de Haan CA, De Martino L, De Milito A, De Tata V, Debnath J, Degterev A, Dehay B, Delbridge LM, Demarchi F, Deng YZ, Dengjel J, Dent P, Denton D, Deretic V, Desai SD, Devenish RJ, Di Gioacchino M, Di Paolo G, Di Pietro C, Díaz-Araya G, Díaz-Laviada I, Diaz-Meco MT, Diaz-Nido J, Dikic I, Dinesh-Kumar SP, Ding WX, Distelhorst CW, Diwan A, Djavaheri-Mergny M, Dokudovskaya S, Dong Z, Dorsey FC, Dosenko V, Dowling JJ, Doxsey S, Dreux M, Drew ME, Duan Q, Duchosal MA, Duff K, Dugail I, Durbeej M, Duszenko M, Edelstein CL, Edinger AL, Egea G, Eichinger L, Eissa NT, Ekmekcioglu S, El-Deiry WS, Elazar Z, Elgendy M, Ellerby LM, Eng KE, Engelbrecht AM, Engelender S, Erenpreisa J, Escalante R, Esclatine A, Eskelinen EL, Espert L, Espina V, Fan H, Fan J, Fan QW, Fan Z, Fang S, Fang Y, Fanto M, Fanzani A, Farkas T, Farré JC, Faure M, Fechheimer M, Feng CG, Feng J, Feng Q, Feng Y, Fésüs L, Feuer R, Figueiredo-Pereira ME, Fimia GM, Fingar DC, Finkbeiner S, Finkel T, Finley KD, Fiorito F, Fisher EA, Fisher PB, Flajolet M, Florez-McClure ML, Florio S, Fon EA, Fornai F, Fortunato F, Fotedar R, Fowler DH, Fox HS, Franco R, Frankel LB, Fransen M, Fuentes JM, Fueyo J, Fujii J, Fujisaki K, Fujita E, Fukuda M, Furukawa RH, Gaestel M, Gailly P, Gajewska M, Galliot B, Galy V, Ganesh S, Ganetzky B, Ganley IG, Gao FB, Gao GF, Gao J, Garcia L, Garcia-Manero G, Garcia-Marcos M, Garmyn M, Gartel AL, Gatti E, Gautel M, Gawriluk TR, Gegg ME, Geng J, Germain M, Gestwicki JE, Gewirtz DA, Ghavami S, Ghosh P, Giammarioli AM, Giatromanolaki AN, Gibson SB, Gilkerson RW, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012 Apr; 8(4):445-544.
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• Johnson KB, Petersen-Jones H, Thompson JM, Hitomi K, Itoh M, Bakker EN, Johnson GV, Colak G, Watts SW. Vena cava and aortic smooth muscle cells express transglutaminases 1 and 4 in addition to transglutaminase 2. Am J Physiol Heart Circ Physiol. 2012 Apr; 302(7):H1355-66.
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• Jin YN, Hwang WY, Jo C, Johnson GV. Metabolic State Determines Sensitivity to Cellular Stress in Huntington Disease: Normalization by Activation of PPAR?. PLoS One. 2012; 7(1):e30406.
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• Colak G, Johnson GV. Complete transglutaminase 2 ablation results in reduced stroke volumes and astrocytes that exhibit increased survival in response to ischemia. Neurobiol Dis. 2012 Mar; 45(3):1042-50.
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• Gundemir S, Colak G, Tucholski J, Johnson GV. Transglutaminase 2: A molecular Swiss army knife. Biochim Biophys Acta. 2012 Feb; 1823(2):406-19.
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• Dolan PJ, Jin YN, Hwang W, Johnson GV. Decreases in valosin-containing protein result in increased levels of tau phosphorylated at Ser262/356. FEBS Lett. 2011 Nov 4; 585(21):3424-9.
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• Pritchard SM, Dolan PJ, Vitkus A, Johnson GV. The toxicity of tau in Alzheimer disease: turnover, targets and potential therapeutics. J Cell Mol Med. 2011 Aug; 15(8):1621-35.
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• Colak G, Filiano AJ, Johnson GV. The application of permanent middle cerebral artery ligation in the mouse. J Vis Exp. 2011; (53).
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• Olsen KC, Sapinoro RE, Kottmann RM, Kulkarni AA, Iismaa SE, Johnson GV, Thatcher TH, Phipps RP, Sime PJ. Transglutaminase 2 and its role in pulmonary fibrosis. Am J Respir Crit Care Med. 2011 Sep 15; 184(6):699-707.
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• Quintanilla RA, Dolan PJ, Jin YN, Johnson GV. Truncated tau and Aß cooperatively impair mitochondria in primary neurons. Neurobiol Aging. 2012 Mar; 33(3):619.e25-35.
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• Colak G, Keillor JW, Johnson GV. Cytosolic guanine nucledotide binding deficient form of transglutaminase 2 (R580a) potentiates cell death in oxygen glucose deprivation. PLoS One. 2011; 6(1):e16665.
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• Chun W, Waldo GS, Johnson GV. Split GFP complementation assay for quantitative measurement of tau aggregation in situ. Methods Mol Biol. 2011; 670:109-23.
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• Beagle B, Johnson GV. AES/GRG5: more than just a dominant-negative TLE/GRG family member. Dev Dyn. 2010 Nov; 239(11):2795-805.
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• Dolan PJ, Johnson GV. The role of tau kinases in Alzheimer's disease. Curr Opin Drug Discov Devel. 2010 Sep; 13(5):595-603.
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• Beagle B, Johnson GV. Differential modulation of TCF/LEF-1 activity by the soluble LRP6-ICD. PLoS One. 2010; 5(7):e11821.
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• Jin YN, Johnson GV. The interrelationship between mitochondrial dysfunction and transcriptional dysregulation in Huntington disease. J Bioenerg Biomembr. 2010 Jun; 42(3):199-205.
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• Dolan PJ, Johnson GV. A caspase cleaved form of tau is preferentially degraded through the autophagy pathway. J Biol Chem. 2010 Jul 16; 285(29):21978-87.
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• Filiano AJ, Tucholski J, Dolan PJ, Colak G, Johnson GV. Transglutaminase 2 protects against ischemic stroke. Neurobiol Dis. 2010 Sep; 39(3):334-43.
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• Beagle B, Mi K, Johnson GV. Phosphorylation of PPP(S/T)P motif of the free LRP6 intracellular domain is not required to activate the Wnt/beta-catenin pathway and attenuate GSK3beta activity. J Cell Biochem. 2009 Nov 1; 108(4):886-95.
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• Quintanilla RA, Johnson GV. Role of mitochondrial dysfunction in the pathogenesis of Huntington's disease. Brain Res Bull. 2009 Oct 28; 80(4-5):242-7.
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• Gundemir S, Johnson GV. Intracellular localization and conformational state of transglutaminase 2: implications for cell death. PLoS One. 2009; 4(7):e6123.
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• Quintanilla RA, Matthews-Roberson TA, Dolan PJ, Johnson GV. Caspase-cleaved tau expression induces mitochondrial dysfunction in immortalized cortical neurons: implications for the pathogenesis of Alzheimer disease. J Biol Chem. 2009 Jul 10; 284(28):18754-66.
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• Matthews-Roberson TA, Quintanilla RA, Ding H, Johnson GV. Immortalized cortical neurons expressing caspase-cleaved tau are sensitized to endoplasmic reticulum stress induced cell death. Brain Res. 2008 Oct 9; 1234:206-12.
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• Kong PJ, Kil MO, Lee H, Kim SS, Johnson GV, Chun W. Increased expression of Bim contributes to the potentiation of serum deprivation-induced apoptotic cell death in Huntington's disease knock-in striatal cell line. Neurol Res. 2009 Feb; 31(1):77-83.
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• Ding H, Johnson GV. The last tangle of tau. J Alzheimers Dis. 2008 Aug; 14(4):441-7.
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• Quintanilla RA, Jin YN, Fuenzalida K, Bronfman M, Johnson GV. Rosiglitazone treatment prevents mitochondrial dysfunction in mutant huntingtin-expressing cells: possible role of peroxisome proliferator-activated receptor-gamma (PPARgamma) in the pathogenesis of Huntington disease. J Biol Chem. 2008 Sep 12; 283(37):25628-37.
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• Ding H, Dolan PJ, Johnson GV. Histone deacetylase 6 interacts with the microtubule-associated protein tau. J Neurochem. 2008 Sep; 106(5):2119-30.
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• Ding H, Johnson GV. New application of beta-galactosidase complementation to monitor tau self-association. J Neurochem. 2008 Aug; 106(4):1545-51.
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• Filiano AJ, Bailey CD, Tucholski J, Gundemir S, Johnson GV. Transglutaminase 2 protects against ischemic insult, interacts with HIF1beta, and attenuates HIF1 signaling. FASEB J. 2008 Aug; 22(8):2662-75.
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• Chun W, Waldo GS, Johnson GV. Split GFP complementation assay: a novel approach to quantitatively measure aggregation of tau in situ: effects of GSK3beta activation and caspase 3 cleavage. J Neurochem. 2007 Dec; 103(6):2529-39.
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• Mookherjee P, Quintanilla R, Roh MS, Zmijewska AA, Jope RS, Johnson GV. Mitochondrial-targeted active Akt protects SH-SY5Y neuroblastoma cells from staurosporine-induced apoptotic cell death. J Cell Biochem. 2007 Sep 1; 102(1):196-210.
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• Chun W, Johnson GV. Activation of glycogen synthase kinase 3beta promotes the intermolecular association of tau. The use of fluorescence resonance energy transfer microscopy. J Biol Chem. 2007 Aug 10; 282(32):23410-7.
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• Hunter JM, Lesort M, Johnson GV. Ubiquitin-proteasome system alterations in a striatal cell model of Huntington's disease. J Neurosci Res. 2007 Jun; 85(8):1774-88.
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• Ruan Q, Quintanilla RA, Johnson GV. Type 2 transglutaminase differentially modulates striatal cell death in the presence of wild type or mutant huntingtin. J Neurochem. 2007 Jul; 102(1):25-36.
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• Mi K, Johnson GV. Regulated proteolytic processing of LRP6 results in release of its intracellular domain. J Neurochem. 2007 Apr; 101(2):517-29.
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• Chun W, Johnson GV. The role of tau phosphorylation and cleavage in neuronal cell death. Front Biosci. 2007; 12:733-56.
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• Ruan Q, Johnson GV. Transglutaminase 2 in neurodegenerative disorders. Front Biosci. 2007; 12:891-904.
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• Clodfelder-Miller BJ, Zmijewska AA, Johnson GV, Jope RS. Tau is hyperphosphorylated at multiple sites in mouse brain in vivo after streptozotocin-induced insulin deficiency. Diabetes. 2006 Dec; 55(12):3320-5.
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• Mi K, Johnson GV. The role of tau phosphorylation in the pathogenesis of Alzheimer's disease. Curr Alzheimer Res. 2006 Dec; 3(5):449-63.
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• Milakovic T, Quintanilla RA, Johnson GV. Mutant huntingtin expression induces mitochondrial calcium handling defects in clonal striatal cells: functional consequences. J Biol Chem. 2006 Nov 17; 281(46):34785-95.
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• Oestreich K, Jester A, Ohlbauer M, Schröter B, Germann G, Pelzer M. [Survival strategy of burn centers in the context of the German DRG system: reimbursement]. Unfallchirurg. 2006 Jun; 109(6):505-10.
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• Bailey CD, Johnson GV. The protective effects of cystamine in the R6/2 Huntington's disease mouse involve mechanisms other than the inhibition of tissue transglutaminase. Neurobiol Aging. 2006 Jun; 27(6):871-9.
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• Ding H, Matthews TA, Johnson GV. Site-specific phosphorylation and caspase cleavage differentially impact tau-microtubule interactions and tau aggregation. J Biol Chem. 2006 Jul 14; 281(28):19107-14.
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• Germann G, Sauerbier M, Unglaub F. [Abdominal hernias resulting from abdominal flap harvest]. Chirurg. 2006 May; 77(5):424-31.
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• Tucholski J, Roth KA, Johnson GV. Tissue transglutaminase overexpression in the brain potentiates calcium-induced hippocampal damage. J Neurochem. 2006 Apr; 97(2):582-94.
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• Johnson GV. Tau phosphorylation and proteolysis: insights and perspectives. J Alzheimers Dis. 2006; 9(3 Suppl):243-50.
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• Mi K, Dolan PJ, Johnson GV. The low density lipoprotein receptor-related protein 6 interacts with glycogen synthase kinase 3 and attenuates activity. J Biol Chem. 2006 Feb 24; 281(8):4787-94.
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• Van Raamsdonk JM, Pearson J, Bailey CD, Rogers DA, Johnson GV, Hayden MR, Leavitt BR. Cystamine treatment is neuroprotective in the YAC128 mouse model of Huntington disease. J Neurochem. 2005 Oct; 95(1):210-20.
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• Choo YS, Mao Z, Johnson GV, Lesort M. Increased glutathione levels in cortical and striatal mitochondria of the R6/2 Huntington's disease mouse model. Neurosci Lett. 2005 Sep 23; 386(1):63-8.
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• Matthews TA, Johnson GV. 14-3-3Zeta does not increase GSK3beta-mediated tau phosphorylation in cell culture models. Neurosci Lett. 2005 Aug 26; 384(3):211-6.
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• Milakovic T, Johnson GV. Mitochondrial respiration and ATP production are significantly impaired in striatal cells expressing mutant huntingtin. J Biol Chem. 2005 Sep 2; 280(35):30773-82.
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• Mi K, Johnson GV. Role of the intracellular domains of LRP5 and LRP6 in activating the Wnt canonical pathway. J Cell Biochem. 2005 May 15; 95(2):328-38.
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• Stoothoff WH, Johnson GV. Tau phosphorylation: physiological and pathological consequences. Biochim Biophys Acta. 2005 Jan 3; 1739(2-3):280-97.
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• Bailey CD, Johnson GV. Tissue transglutaminase contributes to disease progression in the R6/2 Huntington's disease mouse model via aggregate-independent mechanisms. J Neurochem. 2005 Jan; 92(1):83-92.
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• Bailey CD, Tucholski J, Johnson GV. Transglutaminases in neurodegenerative disorders. Prog Exp Tumor Res. 2005; 38:139-57.
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• Bailey CD, Johnson GV. Developmental regulation of tissue transglutaminase in the mouse forebrain. J Neurochem. 2004 Dec; 91(6):1369-79.
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• Hunter JM, Crouse AB, Lesort M, Johnson GV, Detloff PJ. Verification of somatic CAG repeat expansion by pre-PCR fractionation. J Neurosci Methods. 2005 May 15; 144(1):11-7.
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• Johnson GV, Stoothoff WH. Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci. 2004 Nov 15; 117(Pt 24):5721-9.
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• Stoothoff WH, Cho JH, McDonald RP, Johnson GV. FRAT-2 preferentially increases glycogen synthase kinase 3 beta-mediated phosphorylation of primed sites, which results in enhanced tau phosphorylation. J Biol Chem. 2005 Jan 7; 280(1):270-6.
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• Cho JH, Johnson GV. Glycogen synthase kinase 3 beta induces caspase-cleaved tau aggregation in situ. J Biol Chem. 2004 Dec 24; 279(52):54716-23.
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• Suh MD, Park CH, Kim SS, Kil MO, Lee GH, Johnson GV, Chun W. Tissue transglutaminase is not involved in the aggregate formation of stably expressed alpha-synuclein in SH-SY5Y human neuroblastoma cells. Arch Pharm Res. 2004 Aug; 27(8):850-6.
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• Choo YS, Johnson GV, MacDonald M, Detloff PJ, Lesort M. Mutant huntingtin directly increases susceptibility of mitochondria to the calcium-induced permeability transition and cytochrome c release. Hum Mol Genet. 2004 Jul 15; 13(14):1407-20.
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• Robitaille K, Daviau A, Tucholski J, Johnson GV, Rancourt C, Blouin R. Tissue transglutaminase triggers oligomerization and activation of dual leucine zipper-bearing kinase in calphostin C-treated cells to facilitate apoptosis. Cell Death Differ. 2004 May; 11(5):542-9.
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• Johnson GV, LeShoure R. Immunoblot analysis reveals that isopeptide antibodies do not specifically recognize the epsilon-(gamma-glutamyl)lysine bonds formed by transglutaminase activity. J Neurosci Methods. 2004 Apr 30; 134(2):151-8.
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• Shelton SB, Krishnamurthy P, Johnson GV. Effects of cyclin-dependent kinase-5 activity on apoptosis and tau phosphorylation in immortalized mouse brain cortical cells. J Neurosci Res. 2004 Apr 1; 76(1):110-20.
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• Bailey CD, Graham RM, Nanda N, Davies PJ, Johnson GV. Validity of mouse models for the study of tissue transglutaminase in neurodegenerative diseases. Mol Cell Neurosci. 2004 Mar; 25(3):493-503.
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• Shelton SB, Johnson GV. Cyclin-dependent kinase-5 in neurodegeneration. J Neurochem. 2004 Mar; 88(6):1313-26.
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• Ruan Q, Lesort M, MacDonald ME, Johnson GV. Striatal cells from mutant huntingtin knock-in mice are selectively vulnerable to mitochondrial complex II inhibitor-induced cell death through a non-apoptotic pathway. Hum Mol Genet. 2004 Apr 1; 13(7):669-81.
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• Jope RS, Johnson GV. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci. 2004 Feb; 29(2):95-102.
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• Cho JH, Johnson GV. Primed phosphorylation of tau at Thr231 by glycogen synthase kinase 3beta (GSK3beta) plays a critical role in regulating tau's ability to bind and stabilize microtubules. J Neurochem. 2004 Jan; 88(2):349-58.
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• Milakovic T, Tucholski J, McCoy E, Johnson GV. Intracellular localization and activity state of tissue transglutaminase differentially impacts cell death. J Biol Chem. 2004 Mar 5; 279(10):8715-22.
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• Krishnamurthy PK, Johnson GV. Mutant (R406W) human tau is hyperphosphorylated and does not efficiently bind microtubules in a neuronal cortical cell model. J Biol Chem. 2004 Feb 27; 279(9):7893-900.
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• Johnson GV, Bailey CD. The p38 MAP kinase signaling pathway in Alzheimer's disease. Exp Neurol. 2003 Oct; 183(2):263-8.
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• Tucholski J, Johnson GV. Tissue transglutaminase directly regulates adenylyl cyclase resulting in enhanced cAMP-response element-binding protein (CREB) activation. J Biol Chem. 2003 Jul 18; 278(29):26838-43.
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• Chun W, Lesort M, Lee M, Johnson GV. Transient osmotic stress facilitates mutant huntingtin aggregation. Neuroreport. 2002 Dec 20; 13(18):2543-6.
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• Lesort M, Lee M, Tucholski J, Johnson GV. Cystamine inhibits caspase activity. Implications for the treatment of polyglutamine disorders. J Biol Chem. 2003 Feb 7; 278(6):3825-30.
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• Stoothoff WH, Bailey CD, Mi K, Lin SC, Johnson GV. Axin negatively affects tau phosphorylation by glycogen synthase kinase 3beta. J Neurochem. 2002 Nov; 83(4):904-13.
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• Cho JH, Johnson GV. Glycogen synthase kinase 3beta phosphorylates tau at both primed and unprimed sites. Differential impact on microtubule binding. J Biol Chem. 2003 Jan 3; 278(1):187-93.
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• Johnson GV, Bailey CD. Tau, where are we now? J Alzheimers Dis. 2002 Oct; 4(5):375-98.
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• Zhang J, Luan CH, Chou KC, Johnson GV. Identification of the N-terminal functional domains of Cdk5 by molecular truncation and computer modeling. Proteins. 2002 Aug 15; 48(3):447-53.
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• Watcharasit P, Bijur GN, Zmijewski JW, Song L, Zmijewska A, Chen X, Johnson GV, Jope RS. Direct, activating interaction between glycogen synthase kinase-3beta and p53 after DNA damage. Proc Natl Acad Sci U S A. 2002 Jun 11; 99(12):7951-5.
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• Tucholski J, Johnson GV. Tissue transglutaminase differentially modulates apoptosis in a stimuli-dependent manner. J Neurochem. 2002 May; 81(4):780-91.
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• Zhang J, Krishnamurthy PK, Johnson GV. Cdk5 phosphorylates p53 and regulates its activity. J Neurochem. 2002 Apr; 81(2):307-13.
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• Chun W, Lesort M, Lee M, Johnson GV. Mutant huntingtin aggregates do not sensitize cells to apoptotic stressors. FEBS Lett. 2002 Mar 27; 515(1-3):61-5.
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• Lesort M, Chun W, Tucholski J, Johnson GV. Does tissue transglutaminase play a role in Huntington's disease? Neurochem Int. 2002 Jan; 40(1):37-52.
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• Mookherjee P, Johnson GV. Tau phosphorylation during apoptosis of human SH-SY5Y neuroblastoma cells. Brain Res. 2001 Dec 7; 921(1-2):31-43.
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• Shelton SB, Johnson GV. Tau and HMW tau phosphorylation and compartmentalization in apoptotic neuronal PC12 cells. J Neurosci Res. 2001 Oct 15; 66(2):203-13.
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• Stoothoff WH, Johnson GV. Hyperosmotic stress-induced apoptosis and tau phosphorylation in human neuroblastoma cells. J Neurosci Res. 2001 Sep 15; 65(6):573-82.
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• Shen Y, Lue L, Yang L, Roher A, Kuo Y, Strohmeyer R, Goux WJ, Lee V, Johnson GV, Webster SD, Cooper NR, Bradt B, Rogers J. Complement activation by neurofibrillary tangles in Alzheimer's disease. Neurosci Lett. 2001 Jun 15; 305(3):165-8.
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• De Sarno P, Lesort M, Bijur GN, Johnson GV, Jope RS. Cholinergic- and stress-induced signaling activities in cells overexpressing wild-type and mutant presenilin-1. Brain Res. 2001 Jun 8; 903(1-2):226-30.
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• Hartigan JA, Xiong WC, Johnson GV. Glycogen synthase kinase 3beta is tyrosine phosphorylated by PYK2. Biochem Biophys Res Commun. 2001 Jun 8; 284(2):485-9.
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• Chun W, Lesort M, Tucholski J, Faber PW, MacDonald ME, Ross CA, Johnson GV. Tissue transglutaminase selectively modifies proteins associated with truncated mutant huntingtin in intact cells. Neurobiol Dis. 2001 Jun; 8(3):391-404.
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• Chun W, Lesort M, Tucholski J, Ross CA, Johnson GV. Tissue transglutaminase does not contribute to the formation of mutant huntingtin aggregates. J Cell Biol. 2001 Apr 2; 153(1):25-34.
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• Grierson AJ, Johnson GV, Miller CC. Three different human tau isoforms and rat neurofilament light, middle and heavy chain proteins are cellular substrates for transglutaminase. Neurosci Lett. 2001 Jan 26; 298(1):9-12.
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• Tucholski J, Lesort M, Johnson GV. Tissue transglutaminase is essential for neurite outgrowth in human neuroblastoma SH-SY5Y cells. Neuroscience. 2001; 102(2):481-91.
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• Zhang J, Johnson GV. Tau protein is hyperphosphorylated in a site-specific manner in apoptotic neuronal PC12 cells. J Neurochem. 2000 Dec; 75(6):2346-57.
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• Lesort M, Tucholski J, Zhang J, Johnson GV. Impaired mitochondrial function results in increased tissue transglutaminase activity in situ. J Neurochem. 2000 Nov; 75(5):1951-61.
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• Krishnamurthy PK, Mays JL, Bijur GN, Johnson GV. Transient oxidative stress in SH-SY5Y human neuroblastoma cells results in caspase dependent and independent cell death and tau proteolysis. J Neurosci Res. 2000 Sep 1; 61(5):515-23.
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• Lesort M, Tucholski J, Miller ML, Johnson GV. Tissue transglutaminase: a possible role in neurodegenerative diseases. Prog Neurobiol. 2000 Aug; 61(5):439-63.
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• Jenkins SM, Johnson GV. Microtubule/MAP-affinity regulating kinase (MARK) is activated by phenylarsine oxide in situ and phosphorylates tau within its microtubule-binding domain. J Neurochem. 2000 Apr; 74(4):1463-8.
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• Jenkins SM, Zinnerman M, Garner C, Johnson GV. Modulation of tau phosphorylation and intracellular localization by cellular stress. Biochem J. 2000 Jan 15; 345 Pt 2:263-70.
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• Lesort M, Johnson GV. Insulin-like growth factor-1 and insulin mediate transient site-selective increases in tau phosphorylation in primary cortical neurons. Neuroscience. 2000; 99(2):305-16.
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• Guttmann RP, Johnson GV. Measurement of calpain activity in vitro and in situ using a fluorescent compound and tau as substrates. Methods Mol Biol. 2000; 144:143-50.
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• Davis PK, Johnson GV. The microtubule binding of Tau and high molecular weight Tau in apoptotic PC12 cells is impaired because of altered phosphorylation. J Biol Chem. 1999 Dec 10; 274(50):35686-92.
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• Lesort M, Chun W, Johnson GV, Ferrante RJ. Tissue transglutaminase is increased in Huntington's disease brain. J Neurochem. 1999 Nov; 73(5):2018-27.
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• Johnson GV, Jenkins SM. Tau protein in normal and Alzheimer's disease brain. J Alzheimers Dis. 1999 Nov; 1(4-5):307-28.
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• Tucholski J, Kuret J, Johnson GV. Tau is modified by tissue transglutaminase in situ: possible functional and metabolic effects of polyamination. J Neurochem. 1999 Nov; 73(5):1871-80.
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• Johnson GV, Hartigan JA. Tau protein in normal and Alzheimer's disease brain: an update. J Alzheimers Dis. 1999 Nov; 1(4-5):329-51.
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• Zhang J, Tucholski J, Lesort M, Jope RS, Johnson GV. Novel bimodal effects of the G-protein tissue transglutaminase on adrenoreceptor signalling. Biochem J. 1999 Nov 1; 343 Pt 3:541-9.
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• Jenkins SM, Johnson GV. Modulation of tau phosphorylation within its microtubule-binding domain by cellular thiols. J Neurochem. 1999 Nov; 73(5):1843-50.
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• Miller ML, Johnson GV. Rapid, single-step procedure for the identification of transglutaminase-mediated isopeptide crosslinks in amino acid digests. J Chromatogr B Biomed Sci Appl. 1999 Sep 10; 732(1):65-72.
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• Hartigan JA, Johnson GV. Transient increases in intracellular calcium result in prolonged site-selective increases in Tau phosphorylation through a glycogen synthase kinase 3beta-dependent pathway. J Biol Chem. 1999 Jul 23; 274(30):21395-401.
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• Davis PK, Johnson GV. Energy metabolism and protein phosphorylation during apoptosis: a phosphorylation study of tau and high-molecular-weight tau in differentiated PC12 cells. Biochem J. 1999 May 15; 340 ( Pt 1):51-8.
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• Hensley K, Floyd RA, Zheng NY, Nael R, Robinson KA, Nguyen X, Pye QN, Stewart CA, Geddes J, Markesbery WR, Patel E, Johnson GV, Bing G. p38 kinase is activated in the Alzheimer's disease brain. J Neurochem. 1999 May; 72(5):2053-8.
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• Mashburn NA, Unlap MT, Runquist J, Alderman A, Johnson GV, Bell PD. Altered protein kinase C activation of Na+/Ca2+ exchange in mesangial cells from salt-sensitive rats. Am J Physiol. 1999 Apr; 276(4 Pt 2):F574-80.
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• Woolf NJ, Zinnerman MD, Johnson GV. Hippocampal microtubule-associated protein-2 alterations with contextual memory. Brain Res. 1999 Mar 6; 821(1):241-9.
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• Lesort M, Jope RS, Johnson GV. Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3beta and Fyn tyrosine kinase. J Neurochem. 1999 Feb; 72(2):576-84.
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• Lesort M, Greendorfer A, Stockmeier C, Johnson GV, Jope RS. Glycogen synthase kinase-3beta, beta-catenin, and tau in postmortem bipolar brain. J Neural Transm. 1999; 106(11-12):1217-22.
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• Spear N, Estévez AG, Johnson GV, Bredesen DE, Thompson JA, Beckman JS. Enhancement of peroxynitrite-induced apoptosis in PC12 cells by fibroblast growth factor-1 and nerve growth factor requires p21Ras activation and is suppressed by Bcl-2. Arch Biochem Biophys. 1998 Aug 1; 356(1):41-5.
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• Xie HQ, Johnson GV. Calcineurin inhibition prevents calpain-mediated proteolysis of tau in differentiated PC12 cells. J Neurosci Res. 1998 Jul 15; 53(2):153-64.
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• Xie H, Litersky JM, Hartigan JA, Jope RS, Johnson GV. The interrelationship between selective tau phosphorylation and microtubule association. Brain Res. 1998 Jul 6; 798(1-2):173-83.
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• Zhang J, Guttmann RP, Johnson GV. Tissue transglutaminase is an in situ substrate of calpain: regulation of activity. J Neurochem. 1998 Jul; 71(1):240-7.
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• Guttmann RP, Johnson GV. Oxidative stress inhibits calpain activity in situ. J Biol Chem. 1998 May 22; 273(21):13331-8.
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• Lesort M, Attanavanich K, Zhang J, Johnson GV. Distinct nuclear localization and activity of tissue transglutaminase. J Biol Chem. 1998 May 15; 273(20):11991-4.
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• Zhang J, Lesort M, Guttmann RP, Johnson GV. Modulation of the in situ activity of tissue transglutaminase by calcium and GTP. J Biol Chem. 1998 Jan 23; 273(4):2288-95.
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• Jenkins SM, Johnson GV. Tau complexes with phospholipase C-gamma in situ. Neuroreport. 1998 Jan 5; 9(1):67-71.
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• Johnson GV, Guttmann RP. Calpains: intact and active? Bioessays. 1997 Nov; 19(11):1011-8.
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• Jenkins SM, Johnson GV. Phosphorylation of microtubule-associated protein tau on Ser 262 by an embryonic 100 kDa protein kinase. Brain Res. 1997 Sep 5; 767(2):305-13.
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• Xie H, Johnson GV. Ceramide selectively decreases tau levels in differentiated PC12 cells through modulation of calpain I. J Neurochem. 1997 Sep; 69(3):1020-30.
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• Spear N, Estévez AG, Barbeito L, Beckman JS, Johnson GV. Nerve growth factor protects PC12 cells against peroxynitrite-induced apoptosis via a mechanism dependent on phosphatidylinositol 3-kinase. J Neurochem. 1997 Jul; 69(1):53-9.
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• Davis PK, Dudek SM, Johnson GV. Select alterations in protein kinases and phosphatases during apoptosis of differentiated PC12 cells. J Neurochem. 1997 Jun; 68(6):2338-47.
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• Johnson GV, Cox TM, Lockhart JP, Zinnerman MD, Miller ML, Powers RE. Transglutaminase activity is increased in Alzheimer's disease brain. Brain Res. 1997 Mar 21; 751(2):323-9.
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• Guttmann RP, Elce JS, Bell PD, Isbell JC, Johnson GV. Oxidation inhibits substrate proteolysis by calpain I but not autolysis. J Biol Chem. 1997 Jan 17; 272(3):2005-12.
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• Johnson GV, Seubert P, Cox TM, Motter R, Brown JP, Galasko D. The tau protein in human cerebrospinal fluid in Alzheimer's disease consists of proteolytically derived fragments. J Neurochem. 1997 Jan; 68(1):430-3.
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• Arnold CS, Johnson GV, Cole RN, Dong DL, Lee M, Hart GW. The microtubule-associated protein tau is extensively modified with O-linked N-acetylglucosamine. J Biol Chem. 1996 Nov 15; 271(46):28741-4.
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• Litersky JM, Johnson GV, Jakes R, Goedert M, Lee M, Seubert P. Tau protein is phosphorylated by cyclic AMP-dependent protein kinase and calcium/calmodulin-dependent protein kinase II within its microtubule-binding domains at Ser-262 and Ser-356. Biochem J. 1996 Jun 1; 316 ( Pt 2):655-60.
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• Fleming LM, Weisgraber KH, Strittmatter WJ, Troncoso JC, Johnson GV. Differential binding of apolipoprotein E isoforms to tau and other cytoskeletal proteins. Exp Neurol. 1996 Apr; 138(2):252-60.
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• Dudek SM, Johnson GV. Postnatal changes in serine/threonine protein phosphatases and their association with the microtubules. Brain Res Dev Brain Res. 1995 Dec 21; 90(1-2):54-61.
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• Miller ML, Johnson GV. Transglutaminase cross-linking of the tau protein. J Neurochem. 1995 Oct; 65(4):1760-70.
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• Greenwood JA, Johnson GV. Localization and in situ phosphorylation state of nuclear tau. Exp Cell Res. 1995 Oct; 220(2):332-7.
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• Seubert P, Mawal-Dewan M, Barbour R, Jakes R, Goedert M, Johnson GV, Litersky JM, Schenk D, Lieberburg I, Trojanowski JQ, et al. Detection of phosphorylated Ser262 in fetal tau, adult tau, and paired helical filament tau. J Biol Chem. 1995 Aug 11; 270(32):18917-22.
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• Litersky JM, Johnson GV. Phosphorylation of tau in situ: inhibition of calcium-dependent proteolysis. J Neurochem. 1995 Aug; 65(2):903-11.
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• Fleming LM, Johnson GV. Modulation of the phosphorylation state of tau in situ: the roles of calcium and cyclic AMP. Biochem J. 1995 Jul 1; 309 ( Pt 1):41-7.
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• Troncoso JC, Costello AC, Kim JH, Johnson GV. Metal-catalyzed oxidation of bovine neurofilaments in vitro. Free Radic Biol Med. 1995 May; 18(5):891-9.
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• Guttmann RP, Erickson AC, Johnson GV. Tau self-association: stabilization with a chemical cross-linker and modulation by phosphorylation and oxidation state. J Neurochem. 1995 Mar; 64(3):1209-15.
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• Davis PK, Johnson GV. Monoclonal antibody Alz-50 reacts with bovine and human serum albumin. J Neurosci Res. 1994 Dec 1; 39(5):589-94.
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• Norman SG, Johnson GV. Compromised mitochondrial function results in dephosphorylation of tau through a calcium-dependent process in rat brain cerebral cortical slices. Neurochem Res. 1994 Sep; 19(9):1151-8.
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• Dudek SM, Johnson GV. Transglutaminase facilitates the formation of polymers of the beta-amyloid peptide. Brain Res. 1994 Jul 18; 651(1-2):129-33.
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• Woolf NJ, Young SL, Johnson GV, Fanselow MS. Pavlovian conditioning alters cortical microtubule-associated protein-2. Neuroreport. 1994 May 9; 5(9):1045-8.
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• Greenwood JA, Scott CW, Spreen RC, Caputo CB, Johnson GV. Casein kinase II preferentially phosphorylates human tau isoforms containing an amino-terminal insert. Identification of threonine 39 as the primary phosphate acceptor. J Biol Chem. 1994 Feb 11; 269(6):4373-80.
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• Dudek SM, Johnson GV. Transglutaminase catalyzes the formation of sodium dodecyl sulfate-insoluble, Alz-50-reactive polymers of tau. J Neurochem. 1993 Sep; 61(3):1159-62.
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• Greenwood JA, Troncoso JC, Costello AC, Johnson GV. Phosphorylation modulates calpain-mediated proteolysis and calmodulin binding of the 200-kDa and 160-kDa neurofilament proteins. J Neurochem. 1993 Jul; 61(1):191-9.
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• Troncoso JC, Costello A, Watson AL, Johnson GV. In vitro polymerization of oxidized tau into filaments. Brain Res. 1993 Jun 11; 613(2):313-6.
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• Johnson GV, Foley VG. Calpain-mediated proteolysis of microtubule-associated protein 2 (MAP-2) is inhibited by phosphorylation by cAMP-dependent protein kinase, but not by Ca2+/calmodulin-dependent protein kinase II. J Neurosci Res. 1993 Apr 15; 34(6):642-7.
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• Erickson AC, Johnson GV. Metal (Fe3+) affinity chromatography: differential adsorption of tau phosphoproteins. J Neurosci Methods. 1993 Mar; 46(3):245-9.
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• Litersky JM, Scott CW, Johnson GV. Phosphorylation, calpain proteolysis and tubulin binding of recombinant human tau isoforms. Brain Res. 1993 Feb 26; 604(1-2):32-40.
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• Johnson GV, Jope RS. The role of microtubule-associated protein 2 (MAP-2) in neuronal growth, plasticity, and degeneration. J Neurosci Res. 1992 Dec; 33(4):505-12.
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• Johnson GV. Differential phosphorylation of tau by cyclic AMP-dependent protein kinase and Ca2+/calmodulin-dependent protein kinase II: metabolic and functional consequences. J Neurochem. 1992 Dec; 59(6):2056-62.
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• Khilko S, Greenwood JA, Johnson GV. Brain casein kinase 2: affinity purification procedure using immobilized polyethylenimine. Protein Expr Purif. 1992 Oct; 3(5):355-61.
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• Litersky JM, Johnson GV. Phosphorylation by cAMP-dependent protein kinase inhibits the degradation of tau by calpain. J Biol Chem. 1992 Jan 25; 267(3):1563-8.
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• Johnson GV, Watson AL, Lartius R, Uemura E, Jope RS. Dietary aluminum selectively decreases MAP-2 in brains of developing and adult rats. Neurotoxicology. 1992; 13(2):463-74.
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• Kolasa K, Jope RS, Baird MS, Johnson GV. Alterations of choline acetyltransferase, phosphoinositide hydrolysis, and cytoskeletal proteins in rat brain in response to colchicine administration. Exp Brain Res. 1992; 89(3):496-500.
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• Jope RS, Johnson GV. Neurotoxic effects of dietary aluminium. Ciba Found Symp. 1992; 169:254-62; discussion 262-7.
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• Johnson GV, Litersky JM, Whitaker JN. Proteolysis of microtubule-associated protein 2 and tubulin by cathepsin D. J Neurochem. 1991 Nov; 57(5):1577-83.
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• Jope RS, Johnson GV, Baird MS. Seizure-induced protein tyrosine phosphorylation in rat brain regions. Epilepsia. 1991 Nov-Dec; 32(6):755-60.
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• Johnson GV, Greenwood JA, Costello AC, Troncoso JC. The regulatory role of calmodulin in the proteolysis of individual neurofilament proteins by calpain. Neurochem Res. 1991 Aug; 16(8):869-73.
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• Johnson GV, Litersky JM, Jope RS. Degradation of microtubule-associated protein 2 and brain spectrin by calpain: a comparative study. J Neurochem. 1991 May; 56(5):1630-8.
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• Johnson GV, Cogdill KW, Jope RS. Oral aluminum alters in vitro protein phosphorylation and kinase activities in rat brain. Neurobiol Aging. 1990 May-Jun; 11(3):209-16.
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• Johnson GV, Jope RS, Binder LI. Proteolysis of tau by calpain. Biochem Biophys Res Commun. 1989 Sep 29; 163(3):1505-11.
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• Johnson GV, Li XH, Jope RS. Aluminum increases agonist-stimulated cyclic AMP production in rat cerebral cortical slices. J Neurochem. 1989 Jul; 53(1):258-63.
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• Johnson GV. The effects of aluminum on agonist-induced alterations in cyclic AMP and cyclic GMP concentrations in rat brain regions in vivo. Toxicology. 1988 Oct; 51(2-3):299-308.
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• Johnson GV, Simonato M, Jope RS. Dose- and time-dependent hippocampal cholinergic lesions induced by ethylcholine mustard aziridinium ion: effects of nerve growth factor, GM1 ganglioside, and vitamin E. Neurochem Res. 1988 Aug; 13(8):685-92.
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• Johnson GV, Jope RS. Phosphorylation of rat brain cytoskeletal proteins is increased after orally administered aluminum. Brain Res. 1988 Jul 19; 456(1):95-103.
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• Jope RS, Casebolt TL, Johnson GV. Modulation of carbachol-stimulated inositol phospholipid hydrolysis in rat cerebral cortex. Neurochem Res. 1987 Aug; 12(8):693-700.
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• Stanton TL, Johnson GV. In vitro measurements of cholinergic activity in brain regions of hibernating ground squirrels. Brain Res Bull. 1987 May; 18(5):663-7.
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• Johnson GV, Jope RS. Aluminum alters cyclic AMP and cyclic GMP levels but not presynaptic cholinergic markers in rat brain in vivo. Brain Res. 1987 Feb 10; 403(1):1-6.
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• Johnson GV, Jope RS. Aluminum increases cyclic AMP in rat cerebral cortex in vivo. Life Sci. 1986 Oct 6; 39(14):1301-5.
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• Johnson GV, Jope RS. Aluminum impairs glucose utilization and cholinergic activity in rat brain in vitro. Toxicology. 1986 Jul; 40(1):93-102.
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• Freerksen DL, Schroedl NA, Johnson GV, Hartzell CR. Increased aerobic glucose oxidation by cAMP in cultured regenerated skeletal myotubes. Am J Physiol. 1986 May; 250(5 Pt 1):C713-9.
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• Jope RS, Johnson GV. Quinacrine and 2-(4-phenylpiperidino)cyclohexanol (AH5183) inhibit acetylcholine release and synthesis in rat brain slices. Mol Pharmacol. 1986 Jan; 29(1):45-51.
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• Johnson GV, Hartzell CR. Halothane-induced alterations of glucose and pyruvate metabolism in rat cerebra synaptosomes. J Neurochem. 1985 Jun; 44(6):1838-44.
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• Johnson GV, Hartzell CR. Choline uptake, acetylcholine synthesis and release, and halothane effects in synaptosomes. Anesth Analg. 1985 Apr; 64(4):395-9.
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• Hartzell CR, Johnson GV. In vivo MAC values and in vitro experimentation. Anesth Analg. 1985 Apr; 64(4):386-7.
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