CREB-activity and NMNAT2 transcription are down-regulated prior to neurodegeneration, while NMNAT2 over-expression is neuroprotective, in a mouse model of human tauopathy

Human Molecular Genetics

Volumn 21, Issue 2, 2012, Pages 251-267

  Ljungberg, M Cecilia ^a,b   Ali, Yousuf O ^c   Zhu, Jie ^a,b   Wu, Chia Shan ^a,b   Oka, Kazuhiro ^b   Zhai, R Grace ^c   Lu, Hui Chen ^a,b  

^a TEXAS CHILDREN S HOSPITAL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; NEUROFILAMENT M PROTEIN; NICOTINAMIDE MONONUCLEOTIDE ADENYLYLTRANSFERASE 2; NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; RENILLA LUCIFERIN 2 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; BRAIN REGION; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TAUOPATHY;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CREB-BINDING PROTEIN; DISEASE MODELS, ANIMAL; DNA PRIMERS; DOWN-REGULATION; FLUORESCENT ANTIBODY TECHNIQUE; HIPPOCAMPUS; HUMANS; MICE; MICE, TRANSGENIC; NICOTINAMIDE-NUCLEOTIDE ADENYLYLTRANSFERASE; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; TAUOPATHIES; TRANSCRIPTION, GENETIC;

MAMMALIA; MUS;

EID: 84855389519     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr492     Document Type: Article

References (101)

1. Lee, V.M., Goedert, M. and Trojanowski, J.Q. (2001) Neurodegenerative tauopathies. Annu. Rev. Neurosci., 24, 1121-1159.
2. Hutton, M. (2000) Molecular genetics of chromosome 17 tauopathies. Ann. N. Y. Acad. Sci., 920, 63-73.
3. Spillantini, M.G. and Goedert, M. (1998) Tau protein pathology in neurodegenerative diseases. Trends Neurosci., 21, 428-433.
4. Sperfeld, A.D., Collatz, M.B., Baier, H., Palmbach, M., Storch, A., Schwarz, J., Tatsch, K., Reske, S., Joosse, M., Heutink, P. et al. (1999) FTDP-17: an early-onset phenotype with parkinsonism and epileptic seizures caused by a novel mutation. Ann. Neurol., 46, 708-715.
5. Bugiani, O., Murrell, J.R., Giaccone, G., Hasegawa, M., Ghigo, G., Tabaton, M., Morbin, M., Primavera, A., Carella, F., Solaro, C. et al. (1999) Frontotemporal dementia and corticobasal degeneration in a family with a P301S mutation in tau. J. Neuropathol. Exp. Neurol., 58, 667-677.
6. Poorkaj, P., Grossman, M., Steinbart, E., Payami, H., Sadovnick, A., Nochlin, D., Tabira, T., Trojanowski, J.Q., Borson, S., Galasko, D. et al. (2001) Frequency of tau gene mutations in familial and sporadic cases of non-Alzheimer dementia. Arch. Neurol., 58, 383-387.
7. Goedert, M. and Jakes, R. (2005) Mutations causing neurodegenerative tauopathies. Biochim. Biophys. Acta, 1739, 240-250.
8. Gotz, J., Chen, F., Barmettler, R. and Nitsch, R.M. (2001) Tau filament formation in transgenic mice expressing P301L tau. J. Biol. Chem., 276, 529-534.
9. Lewis, J., McGowan, E., Rockwood, J., Melrose, H., Nacharaju, P., Van Slegtenhorst, M., Gwinn-Hardy, K., Paul Murphy, M., Baker, M., Yu, X. et al. (2000) Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat. Genet., 25, 402-405.
10. Andorfer, C., Kress, Y., Espinoza, M., de Silva, R., Tucker, K.L., Barde, Y.A., Duff, K. and Davies, P. (2003) Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J. Neurochem., 86, 582-590.
11. Yoshiyama, Y., Higuchi, M., Zhang, B., Huang, S.M., Iwata, N., Saido, T.C., Maeda, J., Suhara, T., Trojanowski, J.Q. and Lee, V.M. (2007) Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron, 53, 337-351.
12. Wittmann, C.W., Wszolek, M.F., Shulman, J.M., Salvaterra, P.M., Lewis, J., Hutton, M. and Feany, M.B. (2001) Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science, 293, 711-714.
13. Andorfer, C., Acker, C.M., Kress, Y., Hof, P.R., Duff, K. and Davies, P. (2005) Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. J. Neurosci., 25, 5446-5454.
14. Spires, T.L., Orne, J.D., SantaCruz, K., Pitstick, R., Carlson, G.A., Ashe, K.H. and Hyman, B.T. (2006) Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Am. J. Pathol., 168, 1598-1607.
15. Gamblin, T.C., Chen, F., Zambrano, A., Abraha, A., Lagalwar, S., Guillozet, A.L., Lu, M., Fu, Y., Garcia-Sierra, F., LaPointe, N. et al. (2003) Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc. Natl Acad. Sci. USA, 100, 10032-10037.
16. Rissman, R.A., Poon, W.W., Blurton-Jones, M., Oddo, S., Torp, R., Vitek, M.P., LaFerla, F.M., Rohn, T.T. and Cotman, C.W. (2004) Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J. Clin. Invest., 114, 121-130.
17. Lin, W.L., Lewis, J., Yen, S.H., Hutton, M. and Dickson, D.W. (2003) Ultrastructural neuronal pathology in transgenic mice expressing mutant (P301L) human tau. J. Neurocytol., 32, 1091-1105.
18. de Calignon, A., Fox, L.M., Pitstick, R., Carlson, G.A., Bacskai, B.J., Spires-Jones, T.L. and Hyman, B.T. (2010) Caspase activation precedes and leads to tangles. Nature, 464, 1201-1204.
19. Lau, C., Niere, M. and Ziegler, M. (2009) The NMN/NaMN adenylyltransferase (NMNAT) protein family. Front. Biosci., 14, 410-431.
20. Magni, G., Amici, A., Emanuelli, M., Orsomando, G., Raffaelli, N. and Ruggieri, S. (2004) Structure and function of nicotinamide mononucleotide adenylyltransferase. Curr. Med. Chem., 11, 873-885.
21. Zhai, R.G., Zhang, F., Hiesinger, P.R., Cao, Y., Haueter, C.M. and Bellen, H.J. (2008) NAD synthase NMNAT acts as a chaperone to protect against neurodegeneration. Nature, 452, 887-891.
22. + metabolism in health and disease. Trends Biochem. Sci., 32, 12-19.
23. Zhai, R.G., Cao, Y., Hiesinger, P.R., Zhou, Y., Mehta, S.Q., Schulze, K.L., Verstreken, P. and Bellen, H.J. (2006) Drosophila NMNAT maintains neural integrity independent of its NAD synthesis activity. PLoS Biol., 4, e416.
24. Emanuelli, M., Carnevali, F., Saccucci, F., Pierella, F., Amici, A., Raffaelli, N. and Magni, G. (2001) Molecular cloning, chromosomal localization, tissue mRNA levels, bacterial expression, and enzymatic properties of human NMN adenylyltransferase. J. Biol. Chem., 276, 406-412.
25. Raffaelli, N., Sorci, L., Amici, A., Emanuelli, M., Mazzola, F. and Magni, G. (2002) Identification of a novel human nicotinamide mononucleotide adenylyltransferase. Biochem. Biophys. Res. Commun., 297, 835-840.
26. Zhang, X., Kurnasov, O.V., Karthikeyan, S., Grishin, N.V., Osterman, A.L. and Zhang, H. (2003) Structural characterization of a human cytosolic NMN/NaMN adenylyltransferase and implication in human NAD biosynthesis. J. Biol. Chem., 278, 13503-13511.
27. Gilley, J. and Coleman, M.P. (2010) Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol., 8, e1000300.
28. Press, C. and Milbrandt, J. (2008) Nmnat delays axonal degeneration caused by mitochondrial and oxidative stress. J. Neurosci., 28, 4861-4871.
29. Araki, T., Sasaki, Y. and Milbrandt, J. (2004) Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science, 305, 1010-1013.
30. Wang, J., Zhai, Q., Chen, Y., Lin, E., Gu, W., McBurney, M.W. and He, Z. (2005) A local mechanism mediates NAD-dependent protection of axon degeneration. J. Cell Biol., 170, 349-355.
31. Sasaki, Y. and Milbrandt, J. (2010) Axonal degeneration is blocked by nicotinamide mononucleotide adenylyltransferase (NMNAT) protein transduction into transected axons. J. Biol. Chem., 285, 41211-41215.
32. Sasaki, Y., Vohra, B.P., Baloh, R.H. and Milbrandt, J. (2009) Transgenic mice expressing the Nmnat1 protein manifest robust delay in axonal degeneration in vivo. J. Neurosci., 29, 6526-6534.
33. Yahata, N., Yuasa, S. and Araki, T. (2009) Nicotinamide mononucleotide adenylyltransferase expression in mitochondrial matrix delays Wallerian degeneration. J. Neurosci., 29, 6276-6284.
34. Ramsden, M., Kotilinek, L., Forster, C., Paulson, J., McGowan, E., SantaCruz, K., Guimaraes, A., Yue, M., Lewis, J., Carlson, G. et al. (2005) Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J. Neurosci., 25, 10637-10647.
35. Santacruz, K., Lewis, J., Spires, T., Paulson, J., Kotilinek, L., Ingelsson, M., Guimaraes, A., DeTure, M., Ramsden, M., McGowan, E. et al. (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science, 309, 476-481.
36. Hutton, M., Lendon, C.L., Rizzu, P., Baker, M., Froelich, S., Houlden, H., Pickering-Brown, S., Chakraverty, S., Isaacs, A., Grover, A. et al. (1998) Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature, 393, 702-705.
37. Hoover, B.R., Reed, M.N., Su, J., Penrod, R.D., Kotilinek, L.A., Grant, M.K., Pitstick, R., Carlson, G.A., Lanier, L.M., Yuan, L.L. et al. (2010) Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron, 68, 1067-1081.
38. Lee, Y.S. and Silva, A.J. (2009) The molecular and cellular biology of enhanced cognition. Nat. Rev. Neurosci., 10, 126-140.
39. 2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science, 252, 1427-1430.
40. Mayr, B. and Montminy, M. (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol., 2, 599-609.
41. Dickey, C.A., Loring, J.F., Montgomery, J., Gordon, M.N., Eastman, P.S. and Morgan, D. (2003) Selectively reduced expression of synaptic plasticity-related genes in amyloid precursor protein + presenilin-1 transgenic mice. J. Neurosci., 23, 5219-5226.
42. Ma, Q.L., Harris-White, M.E., Ubeda, O.J., Simmons, M., Beech, W., Lim, G.P., Teter, B., Frautschy, S.A. and Cole, G.M. (2007) Evidence of Abeta- and transgene-dependent defects in ERK-CREB signaling in Alzheimer's models. J. Neurochem., 103, 1594-1607.
43. Palop, J.J., Chin, J., Bien-Ly, N., Massaro, C., Yeung, B.Z., Yu, G.Q. and Mucke, L. (2005) Vulnerability of dentate granule cells to disruption of arc expression in human amyloid precursor protein transgenic mice. J. Neurosci., 25, 9686-9693.
44. Palop, J.J., Jones, B., Kekonius, L., Chin, J., Yu, G.Q., Raber, J., Masliah, E. and Mucke, L. (2003) Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc. Natl Acad. Sci. USA, 100, 9572-9577.
45. Tong, L., Thornton, P.L., Balazs, R. and Cotman, C.W. (2001) Beta -amyloid-(1-42) impairs activity-dependent cAMP-response element-binding protein signaling in neurons at concentrations in which cell survival is not compromised. J. Biol. Chem., 276, 17301-17306.
46. Vitolo, O.V., Sant'Angelo, A., Costanzo, V., Battaglia, F., Arancio, O. and Shelanski, M. (2002) Amyloid beta -peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc. Natl Acad. Sci. USA, 99, 13217-13221.
47. Saura, C.A., Choi, S.Y., Beglopoulos, V., Malkani, S., Zhang, D., Shankaranarayana Rao, B.S., Chattarji, S., Kelleher, R.J. 3rd, Kandel, E.R., Duff, K. et al. (2004) Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron, 42, 23-36.
48. Caccamo, A., Maldonado, M.A., Bokov, A.F., Majumder, S. and Oddo, S. (2010) CBP gene transfer increases BDNF levels and ameliorates learning and memory deficits in a mouse model of Alzheimer's disease. Proc. Natl Acad. Sci. USA, 107, 22687-22692.
49. Oddo, S., Caccamo, A., Kitazawa, M., Tseng, B.P. and LaFerla, F.M. (2003) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol. Aging, 24, 1063-1070.
50. Oddo, S., Caccamo, A., Shepherd, J.D., Murphy, M.P., Golde, T.E., Kayed, R., Metherate, R., Mattson, M.P., Akbari, Y. and LaFerla, F.M. (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron, 39, 409-421.
51. Espana, J., Valero, J., Minano-Molina, A.J., Masgrau, R., Martin, E., Guardia-Laguarta, C., Lleo, A., Gimenez-Llort, L., Rodriguez-Alvarez, J. and Saura, C.A. (2010) beta-Amyloid disrupts activity-dependent gene transcription required for memory through the CREB coactivator CRTC1. J. Neurosci., 30, 9402-9410.
52. Flammer, J.R., Popova, K.N. and Pflum, M.K. (2006) Cyclic AMP response element-binding protein (CREB) and CAAT/enhancer-binding protein beta (C/EBPbeta) bind chimeric DNA sites with high affinity. Biochemistry, 45, 9615-9623.
53. Zhang, X., Odom, D.T., Koo, S.H., Conkright, M.D., Canettieri, G., Best, J., Chen, H., Jenner, R., Herbolsheimer, E., Jacobsen, E. et al. (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc. Natl Acad. Sci. USA, 102, 4459-4464.
54. Seamon, K.B., Padgett, W. and Daly, J.W. (1981) Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc. Natl Acad. Sci. USA, 78, 3363-3367.
55. Berger, F., Lau, C., Dahlmann, M. and Ziegler, M. (2005) Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. J. Biol. Chem., 280, 36334-36341.
56. Mayer, P.R., Huang, N., Dewey, C.M., Dries, D.R., Zhang, H. and Yu, G. (2010) Expression, localization, and biochemical characterization of nicotinamide mononucleotide adenylyltransferase 2. J. Biol. Chem., 285, 40387-40396.
57. Cruzalegui, F.H., Kapiloff, M.S., Morfin, J.P., Kemp, B.E., Rosenfeld, M.G. and Means, A.R. (1992) Regulation of intrasteric inhibition of the multifunctional calcium/calmodulin-dependent protein kinase. Proc. Natl Acad. Sci. USA, 89, 12127-12131.
58. McCarty, D.M., Young, S.M. Jr and Samulski, R.J. (2004) Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu. Rev. Genet., 38, 819-845.
59. Grieger, J.C., Choi, V.W. and Samulski, R.J. (2006) Production and characterization of adeno-associated viral vectors. Nat. Protoc., 1, 1412-1428.
60. Kugler, S., Hahnewald, R., Garrido, M. and Reiss, J. (2007) Long-term rescue of a lethal inherited disease by adeno-associated virus-mediated gene transfer in a mouse model of molybdenum-cofactor deficiency. Am. J. Hum. Genet., 80, 291-297.
61. Burger, C., Nash, K. and Mandel, R.J. (2005) Recombinant adeno-associated viral vectors in the nervous system. Hum. Gene Ther., 16, 781-791.
62. Tenenbaum, L., Chtarto, A., Lehtonen, E., Velu, T., Brotchi, J. and Levivier, M. (2004) Recombinant AAV-mediated gene delivery to the central nervous system. J Gene Med., 6(Suppl. 1), S212-S222.
63. Benito, E. and Barco, A. (2010) CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci., 33, 230-240.
64. Alberini, C.M. (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol. Rev., 89, 121-145.
65. Lonze, B.E. and Ginty, D.D. (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron, 35, 605-623.
66. 2+)/CREB/CBP-dependent gene regulation: a shared mechanism critical in long-term synaptic plasticity and neuronal survival. Cell Calcium, 34, 425-430.
67. Mantamadiotis, T., Lemberger, T., Bleckmann, S.C., Kern, H., Kretz, O., Martin Villalba, A., Tronche, F., Kellendonk, C., Gau, D., Kapfhammer, J. et al. (2002) Disruption of CREB function in brain leads to neurodegeneration. Nat. Genet., 31, 47-54.
68. Valor, L.M., Jancic, D., Lujan, R. and Barco, A. (2010) Ultrastructural and transcriptional profiling of neuropathological misregulation of CREB function. Cell Death Differ., 17, 1636-1644.
69. Impey, S., McCorkle, S.R., Cha-Molstad, H., Dwyer, J.M., Yochum, G.S., Boss, J.M., McWeeney, S., Dunn, J.J., Mandel, G. and Goodman, R.H. (2004) Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell, 119, 1041-1054.
70. Yamamoto-Sasaki, M., Ozawa, H., Saito, T., Rosler, M. and Riederer, P. (1999) Impaired phosphorylation of cyclic AMP response element binding protein in the hippocampus of dementia of the Alzheimer type. Brain Res., 824, 300-303.
71. Smith, D.L., Pozueta, J., Gong, B., Arancio, O. and Shelanski, M. (2009) Reversal of long-term dendritic spine alterations in Alzheimer disease models. Proc. Natl Acad. Sci. USA, 106, 16877-16882.
72. Gong, B., Cao, Z., Zheng, P., Vitolo, O.V., Liu, S., Staniszewski, A., Moolman, D., Zhang, H., Shelanski, M. and Arancio, O. (2006) Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell, 126, 775-788.
73. Martin-Loeches, M., Molina, V., Munoz, F., Hinojosa, J.A., Reig, S., Desco, M., Benito, C., Sanz, J., Gabiri, A., Sarramea, F. et al. (2001) P300 amplitude as a possible correlate of frontal degeneration in schizophrenia. Schizophr. Res., 49, 121-128.
74. Rouaux, C., Jokic, N., Mbebi, C., Boutillier, S., Loeffler, J.P. and Boutillier, A.L. (2003) Critical loss of CBP/p300 histone acetylase activity by caspase-6 during neurodegeneration. EMBO J., 22, 6537-6549.
75. Wu, H.Y., Hudry, E., Hashimoto, T., Kuchibhotla, K., Rozkalne, A., Fan, Z., Spires-Jones, T., Xie, H., Arbel-Ornath, M., Grosskreutz, C.L. et al. (2010) Amyloid beta induces the morphological neurodegenerative triad of spine loss, dendritic simplification, and neuritic dystrophies through calcineurin activation. J. Neurosci., 30, 2636-2649.
76. Kogel, D., Peters, M., Konig, H.G., Hashemi, S.M., Bui, N.T., Arolt, V., Rothermundt, M. and Prehn, J.H. (2004) S100B potently activates p65/c-Rel transcriptional complexes in hippocampal neurons: Clinical implications for the role of S100B in excitotoxic brain injury. Neuroscience, 127, 913-920.
77. Ittner, L.M., Ke, Y.D., Delerue, F., Bi, M., Gladbach, A., van Eersel, J., Wolfing, H., Chieng, B.C., Christie, M.J., Napier, I.A. et al. (2010) Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell, 142, 387-397.
78. 2+) elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J. Neurosci., 30, 11938-11950.
79. Thompson, L.T., Moskal, J.R. and Disterhoft, J.F. (1992) Hippocampus-dependent learning facilitated by a monoclonal antibody or D-cycloserine. Nature, 359, 638-641.
80. Flood, J.F., Morley, J.E. and Lanthorn, T.H. (1992) Effect on memory processing by D-cycloserine, an agonist of the NMDA/glycine receptor. Eur. J. Pharmacol., 221, 249-254.
81. Coleman, M.P. and Freeman, M.R. (2010) Wallerian degeneration, wld(s), and nmnat. Annu. Rev. Neurosci., 33, 245-267.
82. Lunn, E.R., Perry, V.H., Brown, M.C., Rosen, H. and Gordon, S. (1989) Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur. J. Neurosci., 1, 27-33.
83. Conforti, L., Tarlton, A., Mack, T.G., Mi, W., Buckmaster, E.A., Wagner, D., Perry, V.H. and Coleman, M.P. (2000) A Ufd2/D4Cole1e chimeric protein and overexpression of Rbp7 in the slow Wallerian degeneration (WldS) mouse. Proc. Natl Acad. Sci. USA, 97, 11377-11382.
84. Mack, T.G., Reiner, M., Beirowski, B., Mi, W., Emanuelli, M., Wagner, D., Thomson, D., Gillingwater, T., Court, F., Conforti, L. et al. (2001) Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci., 4, 1199-1206.
85. Gillingwater, T.H., Haley, J.E., Ribchester, R.R. and Horsburgh, K. (2004) Neuroprotection after transient global cerebral ischemia in Wld(s) mutant mice. J. Cereb. Blood Flow Metab., 24, 62-66.
86. Sajadi, A., Schneider, B.L. and Aebischer, P. (2004) Wlds-mediated protection of dopaminergic fibers in an animal model of Parkinson disease. Curr. Biol., 14, 326-330.
87. Mi, W., Beirowski, B., Gillingwater, T.H., Adalbert, R., Wagner, D., Grumme, D., Osaka, H., Conforti, L., Arnhold, S., Addicks, K. et al. (2005) The slow Wallerian degeneration gene, WldS, inhibits axonal spheroid pathology in gracile axonal dystrophy mice. Brain, 128, 405-416.
88. MacDonald, J.M., Beach, M.G., Porpiglia, E., Sheehan, A.E., Watts, R.J. and Freeman, M.R. (2006) The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron, 50, 869-881.
89. Zhai, R.G., Rizzi, M. and Garavaglia, S. (2009) Nicotinamide/nicotinic acid mononucleotide adenylyltransferase, new insights into an ancient enzyme. Cell Mol. Life Sci., 66, 2805-2818.
90. Yan, T., Feng, Y., Zheng, J., Ge, X., Zhang, Y., Wu, D., Zhao, J. and Zhai, Q. (2010) Nmnat2 delays axon degeneration in superior cervical ganglia dependent on its NAD synthesis activity. Neurochem. Int., 56, 101-106.
91. Pollak, N., Dolle, C. and Ziegler, M. (2007) The power to reduce: pyridine nucleotides-small molecules with a multitude of functions. Biochem. J., 402, 205-218.
92. David, D.C., Hauptmann, S., Scherping, I., Schuessel, K., Keil, U., Rizzu, P., Ravid, R., Drose, S., Brandt, U., Muller, W.E. et al. (2005) Proteomic and functional analyses reveal a mitochondrial dysfunction in P301L tau transgenic mice. J. Biol. Chem., 280, 23802-23814.
93. Rhein, V., Song, X., Wiesner, A., Ittner, L.M., Baysang, G., Meier, F., Ozmen, L., Bluethmann, H., Drose, S., Brandt, U. et al. (2009) Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice. Proc. Natl Acad. Sci. USA, 106, 20057-20062.
94. Perreault, S., Bousquet, O., Lauzon, M., Paiement, J. and Leclerc, N. (2009) Increased association between rough endoplasmic reticulum membranes and mitochondria in transgenic mice that express P301L tau. J. Neuropathol. Exp. Neurol., 68, 503-514.
95. Samulski, R.J., Chang, L.S. and Shenk, T. (1989) Helper-free stocks of recombinant adeno-associated viruses: normal integration does not require viral gene expression. J. Virol., 63, 3822-3828.
96. Philpott, N.J., Gomos, J., Berns, K.I. and Falck-Pedersen, E. (2002) A p5 integration efficiency element mediates Rep-dependent integration into AAVS1 at chromosome 19. Proc. Natl Acad. Sci. USA, 99, 12381-12385.
97. Grimm, D., Kay, M.A. and Kleinschmidt, J.A. (2003) Helper virus-free, optically controllable, and two-plasmid-based production of adeno-associated virus vectors of serotypes 1 to 6. Mol. Ther., 7, 839-850.
98. Zolotukhin, S., Byrne, B.J., Mason, E., Zolotukhin, I., Potter, M., Chesnut, K., Summerford, C., Samulski, R.J. and Muzyczka, N. (1999) Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther., 6, 973-985.
99. Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 25, 402-408.
100. Chen, C., Cheng, X., Dieter, M.Z., Tanaka, Y. and Klaassen, C.D. (2007) Activation of cAMP-dependent signaling pathway induces mouse organic anion transporting polypeptide 2 expression. Mol. Pharmacol., 71, 1159-1164.
101. Lee, T.I., Johnstone, S.E. and Young, R.A. (2006) Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc., 1, 729-748.