Intraneuronal protein aggregation as a trigger for inflammation and neurodegeneration in the aging brain

FASEB Journal

Volumn 31, Issue 1, 2017, Pages 5-10

  Currais, Antonio ^a   Fischer, Wolfgang ^a   Maher, Pamela ^a   Schubert, David ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Alzheimer's disease; Cell division; Neurodegenerative diseases

Indexed keywords

CELL PROTEIN; PROTEIN AGGREGATE;

AGING; ARTICLE; BRAIN NERVE CELL; BRAIN TOXICITY; DEGENERATIVE DISEASE; ENCEPHALITIS; HUMAN; LIFESPAN; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN MISFOLDING; ALZHEIMER DISEASE; BRAIN; INFLAMMATION; METABOLISM; NEURODEGENERATIVE DISEASES; PATHOLOGY; PHYSIOLOGY;

AGING; ALZHEIMER DISEASE; BRAIN; HUMANS; INFLAMMATION; NEURODEGENERATIVE DISEASES; PROTEIN AGGREGATES;

EID: 85009817021     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201601184     Document Type: Article

References (89)

1. Currais, A. (2015) Ageing and inflammation-a central role for mitochondria in brain health and disease. Ageing Res. Rev. 21, 30-42
2. Wyss-Coray, T., and Mucke, L. (2002) Inflammation in neurodegenerative disease-a double-edged sword. Neuron 35, 419-432
3. Wyss-Coray, T. (2006) Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat. Med. 12, 1005-1015
4. Glass, C. K., Saijo, K., Winner, B., Marchetto, M. C., and Gage, F. H. (2010) Mechanisms underlyinginflammationinneurodegeneration. Cell 140, 918-934
5. Lee, Y. J., Han, S. B., Nam, S. Y., Oh, K. W., and Hong, J. T. (2010) Inflammation and Alzheimer's disease. Arch. Pharm. Res. 33, 1539-1556
6. Gentile, M. T., Reccia, M. G., Sorrentino, P. P., Vitale, E., Sorrentino, G., Puca, A. A., and Colucci-D'Amato, L. (2012) Role of cytosolic calcium-dependent phospholipase A2 in Alzheimer's disease pathogenesis. Mol. Neurobiol. 45, 596-604
7. Wyss-Coray, T., and Rogers, J. (2012) Inflammation in Alzheimer disease-a brief reviewof the basic science and clinical literature. Cold Spring Harb. Perspect. Med. 2, a006346
8. Howcroft, T. K., Campisi, J., Louis, G. B., Smith, M. T., Wise, B., Wyss-Coray, T., Augustine, A. D., McElhaney, J. E., Kohanski, R., and Sierra, F. (2013) The role of inflammation in age-related disease. Aging (Albany, N.Y.) 5, 84-93
9. Franceschi, C., Capri, M., Monti, D., Giunta, S., Olivieri, F., Sevini, F., Panourgia, M. P., Invidia, L., Celani, L., Scurti, M., Cevenini, E., Castellani, G. C., and Salvioli, S. (2007) Inflammaging and antiinflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech. Ageing Dev. 128, 92-105
10. Chung, H. Y., Cesari, M., Anton, S., Marzetti, E., Giovannini, S., Seo, A. Y., Carter, C., Yu, B. P., and Leeuwenburgh, C. (2009) Molecular inflammation: underpinnings of aging and age-related diseases. Ageing Res. Rev. 8, 18-30
11. Pawelec, G., Goldeck, D., and Derhovanessian, E. (2014) Inflammation, ageing and chronic disease. Curr. Opin. Immunol. 29, 23-28
12. Wei, J., Xu, H., Davies, J. L., and Hemmings, G. P. (1992) Increase of plasma IL-6 concentration with age in healthy subjects. Life Sci. 51, 1953-1956
13. Brüünsgaard, H., and Pedersen, B. K. (2003) Age-related inflammatory cytokines and disease. Immunol. Allergy Clin. North Am. 23, 15-39
14. Shaw, A. C., Goldstein, D. R., and Montgomery, R. R. (2013) Agedependent dysregulation of innate immunity. Nat. Rev. Immunol. 13, 875-887
15. Campisi, J., and d'Adda di Fagagna, F. (2007) Cellular senescence: whenbadthingshappentogoodcells. Nat.Rev. Mol.CellBiol. 8, 729-740
16. Coppé, J. P., Desprez, P. Y., Krtolica, A., and Campisi, J. (2010) The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu. Rev. Pathol. 5, 99-118
17. Kregel, K. C., and Zhang, H. J. (2007) An integrated view of oxidative stress in aging: basicmechanisms, functional effects, and pathological considerations.Am. J. Physiol.Regul. Integr.Comp. Physiol. 292, R18-R36
18. Gill, R., Tsung, A., and Billiar, T. (2010) Linking oxidative stress to inflammation: Toll-like receptors. Free Radic. Biol. Med. 48, 1121-1132
19. Starr, M. E., and Saito, H. (2014) Sepsis in old age: review of human and animal studies. Aging Dis. 5, 126-136
20. Di Marzo, V., Stella, N., and Zimmer, A. (2015) Endocannabinoid signalling and the deteriorating brain. Nat. Rev. Neurosci. 16, 30-42
21. Tschopp, J. (2011) Mitochondria: sovereign of inflammation? Eur. J. Immunol. 41, 1196-1202
22. Green, D. R., Galluzzi, L., and Kroemer, G. (2011) Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 333, 1109-1112
23. López-Armada, M. J., Riveiro-Naveira, R. R., Vaamonde-García, C., and Valcárcel-Ares, M. N. (2013) Mitochondrial dysfunction and the inflammatory response. Mitochondrion 13, 106-118
24. Castello, M.A., and Soriano, S. (2013) Rational heterodoxy: cholesterol reformation of the amyloid doctrine. Ageing Res. Rev. 12, 282-288
25. Hermann, P. M., Watson, S. N., and Wildering, W. C. (2014) Phospholipase A2-nexus of aging, oxidative stress, neuronal excitability, and functional decline of the aging nervous system? Insights from a snail model system of neuronal aging and ageassociated memory impairment. Front. Genet. 5, 419
26. Currais, A., Quehenberger, Q., Armando, A., Daugherty, D., Maher, P., and Schubert, D. (2016) Amyloid proteotoxicity initiates an inflammatory response blocked by cannabinoids. NPJ Aging Mech. Dis. 2, 16012
27. Hanzel, C. E., Pichet-Binette, A., Pimentel, L. S., Iulita, M. F., Allard, S., Ducatenzeiler, A., Do Carmo, S., and Cuello, A. C. (2014) Neuronal driven pre-plaque inflammation in a transgenic rat model of Alzheimer's disease. Neurobiol. Aging 35, 2249-2262
28. López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M., and Kroemer, G. (2013) The hallmarks of aging. Cell 153, 1194-1217
29. Powers, E. T., Morimoto, R. I., Dillin, A., Kelly, J.W., and Balch, W. E. (2009) Biological and chemical approaches to diseases of proteostasis deficiency. Annu. Rev. Biochem. 78, 959-991
30. Orgel, L.E. (1963) Themaintenanceof theaccuracyofproteinsynthesis and its relevance to ageing. Proc. Natl. Acad. Sci. USA 49, 517-521
31. Gladyshev, V. N. (2013) The origin of aging: imperfectness-driven non-random damage defines the aging process and control of lifespan. Trends Genet. 29, 506-512
32. Evans, S.N., and Steinsaltz, D. (2007) Damage segregation at fissioning may increase growth rates: a superprocess model. Theor. Popul. Biol. 71, 473-490
33. Rang, C. U., Peng, A. Y., and Chao, L. (2011) Temporal dynamics of bacterial aging and rejuvenation. Curr. Biol. 21, 1813-1816
34. Nyström, T. (2007) A bacterial kind of aging. PLoS Genet. 3, e224
35. Steinkraus, K. A., Kaeberlein, M., and Kennedy, B. K. (2008) Replicative aging in yeast: the means to the end.Annu. Rev. CellDev.Biol. 24, 29-54
36. Nyström, T., and Liu, B. (2014) The mystery of aging and rejuvenation-a budding topic. Curr. Opin. Microbiol. 18, 61-67
37. Coelho, M., and Tolić, I.M. (2015) Asymmetric damage segregation at cell division via protein aggregate fusion and attachment to organelles. BioEssays 37, 740-747
38. Sinclair, D. A., and Guarente, L. (1997) Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 91, 1033-1042
39. Aguilaniu, H., Gustafsson, L., Rigoulet, M., and Nyström, T. (2003) Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299, 1751-1753
40. Johnston, J. A., Ward, C. L., and Kopito, R. R. (1998) Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 143, 1883-1898
41. Rujano, M.A., Bosveld, F., Salomons, F.A., Dijk, F., van Waarde, M.A., van der Want, J. J., de Vos, R. A., Brunt, E. R., Sibon, O. C., and Kampinga, H. H. (2006) Polarised asymmetric inheritance of accumulated protein damage in higher eukaryotes. PLoS Biol. 4, e417
42. Desnues, B., Cuny, C., Grégori, G., Dukan, S., Aguilaniu, H., and Nyström, T. (2003) Differential oxidative damage and expression of stress defence regulons in culturable and non-culturable Escherichia coli cells. EMBO Rep. 4, 400-404
43. Stewart, E. J., Madden, R., Paul, G., and Taddei, F. (2005) Aging and death in an organismthat reproduces bymorphologically symmetric division. PLoS Biol. 3, e45
44. Terman, A. (2001) Garbage catastrophe theory of aging: imperfect removal of oxidative damage? Redox Rep. 6, 15-26
45. Toyama, B. H., and Hetzer, M. W. (2013) Protein homeostasis: live long, won't prosper. Nat. Rev. Mol. Cell Biol. 14, 55-61
46. Toyama, B.H., Savas, J.N., Park, S.K., Harris, M.S., Ingolia, N.T., Yates III, J. R., and Hetzer, M. W. (2013) Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 154, 971-982
47. Ross, C. A., and Poirier, M. A. (2005) Opinion: What is the roleofprotein aggregation in neurodegeneration? Nat. Rev. Mol. Cell Biol. 6, 891-898
48. Chen, B., Retzlaff, M., Roos, T., and Frydman, J.(2011) Cellularstrategies of protein quality control. Cold Spring Harb. Perspect. Biol. 3, a004374
49. Tyedmers, J., Mogk, A., and Bukau, B. (2010) Cellular strategies for controlling protein aggregation. Nat. Rev. Mol. Cell Biol. 11, 777-788
50. Knowles, T. P., Vendruscolo, M., and Dobson, C. M. (2014) The amyloid state and its association with proteinmisfolding diseases. Nat. Rev. Mol. Cell Biol. 15, 384-396
51. Simonsen, A., Cumming, R. C., Brech, A., Isakson, P., Schubert, D. R., and Finley, K. D. (2008) Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy 4, 176-184
52. Cuervo, A. M., and Dice, J. F. (2000) Age-related decline in chaperone-mediated autophagy. J. Biol. Chem. 275, 31505-31513
53. Tonoki, A., Kuranaga, E., Tomioka, T., Hamazaki, J., Murata, S., Tanaka, K., and Miura, M. (2009) Genetic evidence linking agedependent attenuationof the 26S proteasome with the aging process. Mol. Cell. Biol. 29, 1095-1106
54. Valera, E., Dargusch, R., Maher, P. A., and Schubert, D. (2013) Modulation of 5-lipoxygenase in proteotoxicity and Alzheimer's disease. J. Neurosci. 33, 10512-10525
55. Li, F., Zhang, L., Craddock, J., Bruce-Keller, A. J., Dasuri, K., Nguyen, A., and Keller, J. N. (2008) Aging and dietary restriction effects on ubiquitination, sumoylation, and the proteasome in the heart. Mech. Ageing Dev. 129, 515-521
56. Bukau, B., Weissman, J., and Horwich, A. (2006) Molecular chaperones and protein quality control. Cell 125, 443-451
57. Cao, S. S., and Kaufman, R. J. (2012) Unfoldedproteinresponse.Curr. Biol. 22, R622-R626
58. Carrara, M., Prischi, F., Nowak, P.R., Kopp, M.C., and Ali, M.M.(2015) Noncanonical binding of BiP ATPase domain to Ire1 and Perk is dissociated by unfolded protein CH1 to initiate ER stress signaling. eLife 4, e03522
59. Sonenberg, N., and Hinnebusch, A. G. (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745
60. Pellegrino, M. W., Nargund, A. M., and Haynes, C. M. (2013) Signaling the mitochondrial unfolded protein response. Biochim. Biophys. Acta 1833, 410-416
61. Schneider, K., and Bertolotti, A. (2015) Surviving proteinquality control catastrophes-from cells to organisms. J. Cell Sci. 128, 3861-3869
62. Opattova, A., Cente, M., Novak, M., and Filipcik, P. (2015) The ubiquitin proteasome system as a potential therapeutic target for treatment of neurodegenerative diseases. Gen. Physiol. Biophys. 34, 337-352
63. Jung, C. H., Ro, S. H., Cao, J., Otto, N. M., and Kim, D. H. (2010) mTOR regulation of autophagy. FEBS Lett. 584, 1287-1295
64. Medzhitov, R. (2008) Origin and physiological roles of inflammation. Nature 454, 428-435
65. Chovatiya, R., and Medzhitov, R. (2014) Stress, inflammation, and defense of homeostasis. Mol. Cell 54, 281-288
66. Minter, M.R., Taylor, J.M., and Crack, P. J. (2016) The contributionof neuroinflammation to amyloid toxicity in Alzheimer's disease. J. Neurochem. 136, 457-474
67. Porhomayon, J., Kolesnikov, S., and Nader, N. D. (2014) The impact of stress hormones on post-traumatic stress disorders symptoms and memory in cardiac surgery patients. J. Cardiovasc. Thorac.Res. 6, 79-84
68. Fang, C., Wei, X., and Wei, Y. (2016) Mitochondrial DNA in the regulation of innate immune responses. Protein Cell 7, 11-16
69. Clark, I.A., and Vissel, B. (2015) Amyloidb: oneof threedanger-associated molecules that are secondary inducers of the proinflammatory cytokines thatmediateAlzheimer'sdisease. Br. J. Pharmacol. 172, 3714-3727
70. Reed-Geaghan, E. G., Savage, J. C., Hise, A. G., and Landreth, G. E. (2009) CD14 and Toll-like receptors 2 and 4 are required for fibrillar Abeta-stimulated microglial activation. J. Neurosci. 29, 11982-11992
71. Stewart, C. R., Stuart, L. M., Wilkinson, K., van Gils, J. M., Deng, J., Halle, A., Rayner, K. J., Boyer, L., Zhong, R., Frazier, W. A., Lacy-Hulbert, A., El Khoury, J., Golenbock, D. T., and Moore, K. J. (2010) CD36 ligands promote sterile inflammationthrough assembly of aToll-like receptor 4 and6 heterodimer.Nat. Immunol. 11, 155-161
72. Vollmar, P., Kullmann, J. S., Thilo, B., Claussen, M. C., Rothhammer, V., Jacobi, H., Sellner, J., Nessler, S., Korn, T., and Hemmer, B. (2010) Active immunization with amyloid-beta 1-42 impairs memory performance through TLR2/4-dependent activation of the innate immune system. J. Immunol. 185, 6338-6347
73. Chiti, F., and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366
74. Marin, I., and Kipnis, J. (2013) Learning and memory and the immune system. Learn. Mem. 20, 601-606
75. Morris, G. P., Clark, I. A., and Vissel, B. (2014) Inconsistencies and controversies surrounding the amyloid hypothesis of Alzheimer's disease. Acta Neuropathol. Commun. 2, 135
76. Bayer, T. A., and Wirths, O. (2010) Intracellular accumulation of amyloid-Beta-a predictor for synaptic dysfunction and neuron loss in Alzheimer's disease. Front. Aging Neurosci. 2, 8
77. Lauritzen, I., Pardossi-Piquard, R., Bauer, C., Brigham, E., Abraham, J. D., Ranaldi, S., Fraser, P., St-George-Hyslop, P., LeThuc, O., Espin, V., Chami, L., Dunys, J., and Checler, F. (2012) The b-secretasederived C-terminal fragment of bAPP, C99, but not Ab, is a key contributor to early intraneuronal lesions in triple-transgenic mouse hippocampus. J. Neurosci. 32, 16243-16255
78. Gouras, G. K., Almeida, C.G., and Takahashi, R.H. (2005) Intraneuronal Abeta accumulation and origin of plaques in Alzheimer's disease. Neurobiol. Aging 26, 1235-1244
79. Baker-Nigh, A., Vahedi, S., Davis, E. G., Weintraub, S., Bigio, E. H., Klein, W. L., and Geula, C. (2015) Neuronal amyloid-b accumulation within cholinergic basal forebrain in ageing and Alzheimer's disease. Brain 138, 1722-1737
80. Chui, D. H., Tanahashi, H., Ozawa, K., Ikeda, S., Checler, F., Ueda, O., Suzuki, H., Araki, W., Inoue, H., Shirotani, K., Takahashi, K., Gallyas, F., and Tabira, T. (1999) TransgenicmicewithAlzheimer presenilin 1 mutations show accelerated neurodegeneration without amyloid plaque formation. Nat. Med. 5, 560-564
81. Billings, L.M., Oddo, S., Green, K.N., McGaugh, J. L., and LaFerla, F.M. (2005) Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45, 675-688
82. Oakley, H., Cole, S. L., Logan, S., Maus, E., Shao, P., Craft, J., Guillozet-Bongaarts, A., Ohno, M., Disterhoft, J., Van Eldik, L., Berry, R., and Vassar, R. (2006) Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J. Neurosci. 26, 10129-10140
83. Tampellini, D., Capetillo-Zarate, E., Dumont, M., Huang, Z., Yu, F., Lin, M. T., and Gouras, G. K. (2010) Effects of synaptic modulation on beta-amyloid, synaptophysin, and memory performance in Alzheimer's disease transgenic mice. J. Neurosci. 30, 14299-14304
84. Wirths, O., Multhaup, G., Czech, C., Blanchard, V., Moussaoui, S., Tremp, G., Pradier, L., Beyreuther, K., and Bayer, T. A. (2001) Intraneuronal Abeta accumulation precedes plaque formation in beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci. Lett. 306, 116-120
85. Oddo, S., Caccamo, A., Tran, L., Lambert, M. P., Glabe, C. G., Klein, W. L., and LaFerla, F. M. (2006) Temporal profile of amyloid-beta (Abeta) oligomerization in an in vivo model of Alzheimer disease. A link between Abeta and tau pathology. J. Biol. Chem. 281, 1599-1604
86. Himeno, E., Ohyagi, Y., Ma, L., Nakamura, N., Miyoshi, K., Sakae, N., Motomura, K., Soejima, N., Yamasaki, R., Hashimoto, T., Tabira, T., LaFerla, F. M., and Kira, J. (2011) Apomorphinetreatment inAlzheimer mice promoting amyloid-b degradation. Ann. Neurol. 69, 248-256
87. Chiti, F., and Dobson, C. M. (2009) Amyloid formation by globular proteins under native conditions. Nat. Chem. Biol. 5, 15-22
88. Goldschmidt, L., Teng, P. K., Riek, R., and Eisenberg, D. (2010) Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proc.Natl. Acad. Sci. USA 107, 3487-3492
89. Craig-Schapiro, R., Fagan, A. M., and Holtzman, D. M. (2009) Biomarkers of Alzheimer's disease. Neurobiol. Dis. 35, 128-140