Genetic deletion of TNFRII gene enhances the Alzheimer-like pathology in an APP transgenic mouse model via reduction of phosphorylated IκBα

Human Molecular Genetics

Volumn 23, Issue 18, 2014, Pages 4906-4918

  Jiang, Hong ^a,b   He, Ping ^a,d   Xie, Junxia ^b   Staufenbiel, Matthias ^c   Li, Rena ^d   Shen, Yong ^a,b,d  

^a SUN HEALTH RESEARCH INSTITUTE   (United States)

^b QINGDAO UNIVERSITY MEDICAL COLLEGE   (China)

^c NOVARTIS PHARMA AG   (Switzerland)

^d ROSKAMP INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; ASPARTIC PROTEINASE; BACE1 PROTEIN, HUMAN; I KAPPA B; NF-KAPPAB INHIBITOR ALPHA; SECRETASE; TUMOR NECROSIS FACTOR RECEPTOR 2;

ALZHEIMER DISEASE; ANIMAL; BINDING SITE; DISEASE MODEL; GENE DELETION; GENE TARGETING; GENETICS; HUMAN; METABOLISM; MICROGLIA; MOUSE; PATHOLOGY; PHOSPHORYLATION; PROCEDURES; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; BINDING SITES; DISEASE MODELS, ANIMAL; GENE DELETION; GENE TARGETING; HUMANS; I-KAPPA B PROTEINS; MICE; MICE, TRANSGENIC; MICROGLIA; PHOSPHORYLATION; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II;

EID: 84906841220     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu206     Document Type: Article

References (52)

1. Sinha, S., Anderson, J.P., Barbour, R., Basi, G.S., Caccavello, R., Davis, D., Doan, M., Dovey, H.F., Frigon, N., Hong, J. et al. (1999) Purification and cloning of amyloid precursor protein beta-secretase from human brain. Nature, 402, 537-540.
2. Sinha, S. and Lieberburg, I. (1999) Cellular mechanisms of beta-amyloid production and secretion. Proc. Natl. Acad. Sci. USA, 96, 11049-11053.
3. Vassar, R., Bennett, B.D., Babu-Khan, S., Kahn, S., Mendiaz, E.A., Denis, P., Teplow, D.B., Ross, S., Amarante, P., Loeloff, R. et al. (1999) Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science, 286, 735-741.
4. Yan, R., Bienkowski, M.J., Shuck, M.E., Miao, H., Tory, M.C., Pauley, A.M., Brashier, J.R., Stratman, N.C., Mathews, W.R., Buhl, A.E. et al. (1999) Membrane-anchored aspartyl protease with Alzheimer's disease beta-secretase activity. Nature, 402, 533-537.
5. Cai, H., Wang, Y., McCarthy, D., Wen, H., Borchelt, D.R., Price, D.L. and Wong, P.C. (2001) BACE1 is the major beta-secretase for generation of Abeta peptides by neurons. Nat. Neurosci., 4, 233-234.
6. Rossner, S., Sastre, M., Bourne, K. and Lichtenthaler, S.F. (2006) Transcriptional and translational regulation of BACE1 expression-implications for Alzheimer's disease. Prog. Neurobiol., 79, 95-111.
7. Vassar, R. (2004) BACE1: the beta-secretase enzyme in Alzheimer's disease. J. Mol. Neurosci., 23, 105-114.
8. Xia, W., Zhang, J., Ostaszewski, B.L., Kimberly, W.T., Seubert, P., Koo, E.H., Shen, J. and Selkoe, D.J. (1998) Presenilin 1 regulates the processing of beta-amyloid precursor protein C-terminal fragments and the generation of amyloid beta-protein in endoplasmic reticulum and Golgi. Biochemistry, 37, 16465-16471.
9. Akiyama, H., Barger, S., Barnum, S., Bradt, B., Bauer, J., Cole, G.M., Cooper, N.R., Eikelenboom, P., Emmerling, M., Fiebich, B.L. et al. (2000) Inflammation and Alzheimer's disease. Neurobiol. Aging, 21, 383-421.
10. Shen, Y. and Meri, S. (2003) Yin and Yang: complement activation and regulation in Alzheimer's disease. Prog. Neurobiol., 70, 463-472.
11. Shen, Y., Sullivan, T., Lee, C.M., Meri, S., Shiosaki, K. and Lin, C.W. (1998) Induced expression of neuronal membrane attack complex and cell death by Alzheimer's beta-amyloid peptide. Brain. Res., 796, 187-197.
12. Wyss-Coray, T. and Mucke, L. (2002) Inflammation in neurodegenerative disease-a double-edged sword. Neuron, 35, 419-432.
13. Yang, L.B., Li, R., Meri, S., Rogers, J. and Shen, Y. (2000) Deficiency of complement defense protein CD59 may contribute to neurodegeneration in Alzheimer's disease. J. Neurosci., 20, 7505-7509.
14. Heneka, M.T. and O'Banion, M.K. (2007) Inflammatory processes in Alzheimer's disease. J. Neuroimmunol., 184, 69-91.
15. McAlpine, F.E., Lee, J.K., Harms, A.S., Ruhn, K.A., Blurton-Jones, M., Hong, J., Das, P., Golde, T.E., LaFerla, F.M., Oddo, S., Blesch, A. and Tansey, M.G. (2009) Inhibition of soluble TNF signaling in a mouse model of Alzheimer's disease prevents pre-plaque amyloid-associated neuropathology. Neurobiol. Dis., 34, 163-177.
16. Tan, Z.S., Beiser, A.S., Vasan, R.S., Roubenoff, R., Dinarello, C.A., Harris, T.B., Benjamin, E.J., Au, R., Kiel, D.P., Wolf, P.A. and Seshadri, S. (2007) Inflammatory markers and the risk of Alzheimer disease: the Framingham Study. Neurology, 68, 1902-1908.
17. Tripathy, D., Thirumangalakudi, L. and Grammas, P. (2007) Expression of macrophage inflammatory protein 1-alpha is elevated in Alzheimer's vessels and is regulated by oxidative stress. J. Alzheimers. Dis., 11, 447-455.
18. He, P., Zhong, Z., Lindholm, K., Berning, L., Lee, W., Lemere, C., Staufenbiel, M., Li, R. and Shen, Y. (2007) Deletion of tumor necrosis factor death receptor inhibits amyloid {beta} generation and prevents learning and memory deficits in Alzheimer's mice. J. Cell Biol., 178, 829-841.
19. Cheng, X., Yang, L., He, P., Li, R. andShen, Y. (2010)Differential activationof tumor necrosis factor receptors distinguishes between brains from Alzheimer's disease and non-demented patients. J. Alzheimers Dis., 19, 621-630.
20. Sommer, B. and Staufenbiel, M. (1998) A beta peptide deposition in the brains of transgenic mice: evidence for a key event in Alzheimer's disease pathogenesis. Mol. Psychiatry, 3, 284-286, 282-283.
21. Peschon, J.J., Torrance, D.S., Stocking, K.L., Glaccum, M.B., Otten, C., Willis, C.R., Charrier, K., Morrissey, P.J., Ware, C.B. and Mohler, K.M. (1998)TNFreceptor-deficient mice reveal divergent roles for p55 and p75 in several models of inflammation. J. Immunol., 160, 943-952.
22. VanDooren, T., Muyllaert, D., Borghgraef, P., Cresens, A., Devijver, H., Van derAuwera, I., Wera, S., Dewachter, I. and VanLeuven, F. (2006) Neuronal or glial expression of human apolipoprotein e4 affects parenchymal and vascular amyloid pathology differentially in different brain regions of double-and triple-transgenic mice. Am. J. Pathol., 168, 245-260.
23. Simard, A.R., Soulet, D., Gowing, G., Julien, J.P. and Rivest, S. (2006) Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron, 49, 489-502.
24. Wilcock, D.M., Rojiani, A., Rosenthal, A., Levkowitz, G., Subbarao, S., Alamed, J., Wilson, D., Wilson, N., Freeman, M.J., Gordon, M.N. and Morgan, D. (2004) Passive amyloid immunotherapy clears amyloid and transiently activates microglia in a transgenic mouse model of amyloid deposition. J. Neurosci., 24, 6144-6151.
25. Yan, Q., Zhang, J., Liu, H., Babu-Khan, S., Vassar, R., Biere, A.L., Citron, M. and Landreth, G. (2003) Anti-inflammatory drug therapy alters beta-amyloid processing and deposition in an animal model of Alzheimer's disease. J. Neurosci., 23, 7504-7509.
26. Wilcock, D.M., DiCarlo, G., Henderson, D., Jackson, J., Clarke, K., Ugen, K.E., Gordon, M.N. and Morgan, D. (2003) Intracranially administered anti-Abeta antibodies reduce beta-amyloid deposition by mechanisms both independent of and associated with microglial activation. J. Neurosci., 23, 3745-3751.
27. Selkoe, D.J. (1998) The cell biology of beta-amyloid precursor protein and presenilin in Alzheimer's disease. Trends Cell Biol., 8, 447-453.
28. Younkin, S.G. (1995) Evidence that A beta 42 is the real culprit in Alzheimer's disease. Ann. Neurol., 37, 287-288.
29. Li, R., Lindholm, K., Yang, L.B., Yue, X., Citron, M., Yan, R., Beach, T., Sue, L., Sabbagh, M., Cai, H. et al. (2004) Amyloid beta peptide load is correlated with increased beta-secretase activity in sporadic Alzheimer's disease patients. Proc. Natl. Acad. Sci. USA, 101, 3632-3637.
30. Yang, L.B., Lindholm, K., Yan, R., Citron, M., Xia, W., Yang, X.L., Beach, T., Sue, L., Wong, P., Price, D., Li, R. and Shen, Y. (2003) Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat. Med., 9, 3-4.
31. Zhong, Z., Ewers, M., Teipel, S., Burger, K., Wallin, A., Blennow, K., He, P., McAllister, C., Hampel, H. and Shen, Y. (2007) Levels of beta-secretase (BACE1) in cerebrospinal fluid as a predictor of risk in mild cognitive impairment. Arch. Gen. Psychiatry. (JAMA Psychiatry), 64, 718-726.
32. Christensen, M.A., Zhou, W., Qing, H., Lehman, A., Philipsen, S. and Song, W.(2004) Transcriptional regulation of BACE1, the beta-amyloid precursor protein beta-secretase, by Sp1. Mol. Cell Biol., 24, 865-874.
33. Sambamurti, K., Kinsey, R., Maloney, B., Ge, Y.W. and Lahiri, D.K. (2004) Gene structure and organization of the human beta-secretase (BACE) promoter. FASEB J., 18, 1034-1036.
34. McFarlane, S.M., Pashmi, G., Connell, M.C., Littlejohn, A.F., Tucker, S.J., Vandenabeele, P. and MacEwan, D.J. (2002) Differential activation of nuclear factor-kappaB by tumour necrosis factor receptor subtypes. TNFR1 predominates whereas TNFR2 activates transcription poorly. FEBS Lett., 515, 119-126.
35. Rothe, M., Sarma, V., Dixit, V.M. and Goeddel, D.V. (1995) TRAF2-mediated activation of NF-kappa B by TNF receptor 2 and CD40. Science, 269, 1424-1427.
36. Rothe, M., Wong, S.C., Henzel, W.J. and Goeddel, D.V. (1994) A novel family of putative signal transducers associated with the cytoplasmic domain of the 75 kDa tumor necrosis factor receptor. Cell, 78, 681-692.
37. Bourne, K.Z., Ferrari, D.C., Lange-Dohna, C., Rossner, S., Wood, T.G. and Perez-Polo, J.R. (2007) Differential regulation of BACE1 promoter activity by nuclear factor-kappaB in neurons and glia upon exposure to beta-amyloid peptides. J. Neurosci. Res., 85, 1194-1204.
38. Dohmen, R.J. (2004) SUMO protein modification. Biochim. Biophys. Acta, 1695, 113-131.
39. Hay, R.T. (2005) SUMO: a history of modification. Mol. Cell, 18, 1-12.
40. Mabb, A.M. and Miyamoto, S. (2007)SUMOand NF-kappaB ties. Cell Mol. Life Sci., 64, 1979-1996.
41. Schwartz, D.C. and Hochstrasser, M. (2003) A superfamily of protein tags: ubiquitin, SUMOand related modifiers. Trends Biochem. Sci., 28, 321-328.
42. Desterro, J.M., Rodriguez, M.S. and Hay, R.T. (1998) SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol. Cell, 2, 233-239.
43. Guo, D., Li, M., Zhang, Y., Yang, P., Eckenrode, S., Hopkins, D., Zheng, W., Purohit, S., Podolsky, R.H., Muir, A. et al. (2004) A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes. Nat. Genet., 36, 837-841.
44. Wang, C.Y., Yang, P., Li, M. and Gong, F. (2009) Characterization of a negative feedback network between SUMO4 expression and NFkappaB transcriptional activity. Biochem. Biophys. Res. Commun., 381, 477-481.
45. Old, L.J. (1988) Tumor necrosis factor. Sci. Am., 258, 59-60, 69-75.
46. Thommesen, L. and Laegreid, A. (2005) Distinct differences between TNF receptor 1-and TNF receptor 2-mediated activation of NFkappaB. J. Biochem. Mol. Biol., 38, 281-289.
47. Brink, R. and Lodish, H.F. (1998) Tumor necrosis factor receptor (TNFR)-associated factor 2A (TRAF2A), a TRAF2 splice variant with an extended RING finger domain that inhibits TNFR2-mediated NF-kappaB activation. J. Biol. Chem., 273, 4129-4134.
48. Takeuchi, M., Rothe, M. and Goeddel, D.V. (1996) Anatomy of TRAF2. Distinct domains for nuclear factor-kappaB activation and association with tumor necrosis factor signaling proteins. J. Biol. Chem., 271, 19935-19942.
49. Botto, M., Dell'Agnola, C., Bygrave, A.E., Thompson, E.M., Cook, H.T., Petry, F., Loos, M., Pandolfi, P.P. and Walport, M.J. (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet., 19, 56-59.
50. Matsuoka, Y., Picciano, M., Malester, B., LaFrancois, J., Zehr, C., Daeschner, J.M., Olschowka, J.A., Fonseca, M.I., O'Banion, M.K., Tenner, A.J., Lemere, C.A. and Duff, K. (2001) Inflammatory responses to amyloidosis in a transgenic mouse model of Alzheimer's disease. Am. J. Pathol., 158, 1345-1354.
51. Casas, C., Sergeant, N., Itier, J.M., Blanchard, V., Wirths, O., van der Kolk, N., Vingtdeux, V., van de Steeg, E., Ret, G., Canton, T. et al. (2004) Massive CA1/2 neuronal loss with intraneuronal and N-terminal truncated Abeta42 accumulation in a novel Alzheimer transgenic model. Am. J. Pathol., 165, 1289-1300.
52. Schmitz, C., Rutten, B.P., Pielen, A., Schafer, S., Wirths, O., Tremp, G., Czech, C., Blanchard, V., Multhaup, G., Rezaie, P. et al. (2004) Hippocampal neuron loss exceeds amyloid plaque load in a transgenic mouse model of Alzheimer's disease. Am. J. Pathol., 164, 1495-1502.