Differential pathways for interleukin-1β production activated by chromogranin A and amyloid β in microglia

Neurobiology of Aging

Volumn 34, Issue 12, 2013, Pages 2715-2725

  Wu, Zhou ^a   Sun, Li ^a   Hashioka, Sadayuki ^b,c   Yu, Sheng ^b   Schwab, Claudia ^b   Okada, Ryo ^a   Hayashi, Yoshinori ^a   McGeer, Patrick L ^b   Nakanishi, Hiroshi ^a,d  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c SHIMANE UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Alzheimer's disease; Amyloid protein; Cathepsin B; Chromogranin A; Interleukin 1 ; Microglia; Nuclear factor B; Toll like receptor 4

Indexed keywords

AMYLOID BETA PROTEIN; CATHEPSIN B; CHROMOGRANIN A; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA; SMALL INTERFERING RNA;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; GENE; IMMUNOREACTIVITY; INTRACELLULAR SIGNALING; MICROGLIA; MOUSE; NERVE CELL CULTURE; NERVE CELL LESION; NERVOUS SYSTEM INFLAMMATION; NEUROFILAMENT; NEUROPATHOLOGY; NLRP GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

ALZHEIMER'S DISEASE; AMYLOID Β PROTEIN; CATHEPSIN B; CHROMOGRANIN A; INTERLEUKIN-1Β; MICROGLIA; NUCLEAR FACTOR-ΚB; TOLL-LIKE RECEPTOR 4;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; CARRIER PROTEINS; CASPASE 1; CATHEPSIN B; CELLS, CULTURED; CHROMOGRANIN A; CYTOSOL; INFLAMMASOMES; INTERLEUKIN-1BETA; MICE; MICE, INBRED C57BL; MICROGLIA; NF-KAPPA B; PLAQUE, AMYLOID; SIGNAL TRANSDUCTION;

EID: 84884163207     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.05.018     Document Type: Article

References (63)

1. Akiyama H., Barger S., Barnum S., Bradt B., Bauer J., Cole G.M., Cooper N.R., Eikelenboom P., Emmerling M., Fiebich B.L., Finch C.E., Frautschy S., Griffin W.S., Hampel H., Hull M., Landreth G., Lue L., Mrak R., Mackenzie I.R., McGeer P.L., O'Banion M.K., Pachter J., Pasinetti G., Plata-Salaman C., Rogers J., Rydel R., Shen, Y., Streit W., Strohmeyer R., Tooyoma I., Van Muiswinkel F.L., Veerhuis R., Walker D., Webster S., Wegrzyniak B., Wenk G., Wyss-Coray T. Inflammation and Alzheimer disease. Neurobiol. Aging 2000, 21:383-421.
2. Bamberger M.E., Harris M.E., McDonald D.R., Husemann J., Landreth G.E. Acell surface receptor complex for fibrillar β-amyloid mediates microglial activation. J.Neurosci. 2003, 23:2665-2674.
3. Barrientos R.M., Frank M.G., Hein A.M., Higgins E.A., Watkins L.R., Rudy J.W., Maier S.F. Time course of hippocampal IL-1β and memory consolidation impairments in aging rats following peripheral infection. Brain Behav. Immun. 2009, 23:46-54.
4. Betmouni S., Perry V.H., Gordon J.L. Evidence for an early inflammatory response in the central nervous system of mice with scrapie. Neuroscience 1996, 74:1-5.
5. Bien S., Ritter C.A., Gratz M., Sperker B., Sonnemann J., Beck J.F., Kroemer H.K. Nuclear factor-κB mediates up-regulation of cathepsin B by doxorubicin in tumor cells. Mol. Pharmacol. 2004, 65:1092-1102.
6. Cechetto D.F., Hachinski V., Whitehead S.N. Vascular risk factors and Alzheimer's disease. Expert Rev. Neurother. 2008, 8:743-750.
7. Combrinck M.I., Perry V.H., Cunningham C. Peripheral infection evokes exaggerated sickness behavior in pre-clinical murine prion disease. Neuroscience 2002, 112:7-11.
8. Cunningham C., Konsman J.P., Cartmell T. Cytokines and the ageing brain. Trends Neurosci. 2002, 25:546-557.
9. Dinarello C.A. Asignal for the caspase-1 inflammasome free of TLR. Immunity 2007, 26:383-385.
10. Duewell P., Kono H., Rayner K.J., Sirois C.M., Valdimer G., Bauerfeind F.G., Abela G.S., Franchi L., Nuñez G., Schnurr M., Espevik T., Lien E., Fitzgerald K.A., Rock K.L., Moore K.J., Wright S.D., Hornung V., Latz E. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010, 464:1357-1361.
11. Geula C., Wu C.K., Saoff D., Lorenzo A., Yuan M., Yanker B.A. Aging renders the brain vulnerable to amyloid β-protein neurotoxicity. Nat. Med. 1998, 4:827-831.
12. Ghosh C.C., Ramaswami S., Juvekar A., Vu H.Y., Galdieri L., Davidson D., Vancurova I. Gene-specific repression of proinflammatory cytokines in stimulated human macrophages by nuclear IκBα. J.Immunol. 2010, 185:3685-3693.
13. Goto M., Katayama K.I., Shirakawa F., Tanaka I. Involvement of NF-κB p50/p60 heterodimer in activation of the human pro-interleukin-1βgene at two subregion of the upstream enhancer element. Cytokine 1999, 11:16-28.
14. Griffin W.S.T., Yeralan O., Boop F., Rovnaghi C.R., Sheng J.G., Mrak R.E., Van Eldik L.J. Overexpression of the neurotrophic cytokine S100βin human temporal lobe epilepsy. J.Neurochem. 1995, 65:228-233.
15. Griffin W.S.T., Nicoll J.A., Grimaldi L.M., Sheng J.G., Mrak R.E. The pervasiveness of interleukin-1 an Alzheimer pathogenesis: a role for specific polymorphisms in disease risk. Exp. Gerontol. 2000, 35:481-487.
16. Halle A., Hornung V., Petzold G.C., Stewart C.R., Monks B.G., Reinheckel T., Fitzgerald K.A., Latz E., Moore K.J., Golenbock D.T. The NALP3 inflammasome is involved in the innate immune response to amyloid-β. Nat. Immunol. 2008, 9:857-865.
17. Hayashi Y., Yoshida M., Yamato M., Ide T., Wu Z., Ochi-Shindou M., Kanki T., Kang D., Sunagawa K., Tsutsui H., Nakanishi H. Reverse of age-dependent memory impairment and mitochondrial DNA damage in microglia by an overexpression of human mitochondrial transcription factor A in mice. J.Neurosci. 2008, 28:8624-8634.
18. Heneka M.T., O'Banion M.K., Terwel D., Kummer M.P. Neuroinflammatory processes in Alzheimer's disease. J.Neural Transm. 2010, 117:919-947.
19. Hook V.Y., Toneff T., Aaron W., Yasothornsrikul S., Bundey R., Reisine T. β-amyloid peptide in regulated secretory vesicles of chromaffin cells: evidence for multiple cysteine proteolytic activities in distinct pathways for β-secretase activity in chromaffin vesicles. J.Neurochem. 2002, 81:237-256.
20. Hook V.Y., Kindy M., Hook G. Inhibitors of cathepsin B improves memory and reduce β-amyloid in transgenic Alzheimer disease mice expressing the wild-type, but not Swedish mutant, β-secretase site of the amyloid precursor. J.Biol. Chem. 2008, 283:7745-7753.
21. Hook V.Y., Kindy M., Reinheckel T., Peters C., Hook G. Genetic cathepsin B deficiency reduces β-amyloid in transgenic mice expressing human wild-type amyloid precursor protein. Biochem. Biophys. Res. Commun. 2008, 386:284-288.
22. Hook G., Hook V., Kindy M. The cysteine protease inhibitor, E64d, reduces brain amyloid-β and improves memory deficits in Alzheimer's disease animal models by inhibiting cathepsin B, but not BACE1, β-secretase activity. J.Alzheimers Dis. 2011, 26:387-408.
23. Hooper C., Fry V.A.H., Sevastou I.G., Pocock J.M. Scavenger receptor control of chromogranin A-induced microglial stress and neurotoxic cascades. FEBS Lett. 2009, 583:3461-3466.
24. Hornung V., Bauernfeind F., Halle A., Samstad E.O., Kono H., Rock K.L., Fitzgerald K.A., Latz E. Silica crystals and aluminium salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 2008, 9:847-856.
25. Jana M., Palencia C.A., Pahan K. Fibrillar amyloid-β peptides activate microglia via TLR2: implications for Alzheimer's disease. J.Immunol. 2008, 181:7254-7262.
26. Kamer A.R., Dasanayake A.P., Craig R.G., Glodzik-Sobanska L., Bry M., de Leon M.J. Altzheimer's disease and peripheral infections: the possible contribution from periodontal infections, model and hypothesis. J.Alzheimers Dis. 2008, 13:437-449.
27. Klegeris A., Walker D.G., McGeer P.L. Activation of macrophages by Alzheimer β amyloid peptide. Biochem. Biophys. Res. Commun. 1994, 199:984-991.
28. Kodl C.T., Seaquist E.R. Cognitive dysfunction and diabetes mellitus. Endocr. Rev. 2008, 29:494-511.
29. Lechner T., Adlassnig C., Humpel C., Kaufmann W.A., Maier H., Reinstadler Kramer K., Hinterhölzl J., Mahata S.K., Jellinger K.A., Marksteiner J. Chromogranin peptide in Alzheimer's disease. Exp. Gerontol. 2004, 39:101-113.
30. Licastro F., Pedrini S., Caputo L., Annoni G., Davis L.J., Ferri C., Casadei V., Grimaldi L.M. Increased plasma levels of interleukin-1, interleukin-6 and α-1-antichymotrypsin in patients with Alzheimer's disease: peripheral inflammation or signals from brain?. J.Neuroimmunol. 2000, 103:97-102.
31. Li Y., Liu L., Kang J., Sheng J.G., Barger S.W., Mrak R.E., Griffin W.S. Neuronal-glial interactions mediated by interleukin-1 enhance neuronal acetylcholineesterase activity and mRNA expression. J.Neurosci. 2000, 20:149-155.
32. Liu X., Wu Z., Hayashi Y., Nakanishi H. Age-dependent neuroinflammatory responses and deficits in long-term potentiation in the hippocampus during systemic inflammation. Neuroscience 2012, 216:133-142.
33. Liu Y., Walter S., Stagi M., Cherny D., Letiembre M., Schulz-Schaeffer W., Heine H., Penke B., Neumann H., Fassbender K. LPS receptor (CD14): a receptor for phagocytosis of Alzheimer's amyloid peptide. Brain 2005, 128:1778-1789.
34. Luchsinger J.A., Gustafson D.R. Adiposity and Alzheimer's disease. Curr. Opin. Clin. Nutr. Metab. Care 2009, 12:15-21.
35. Marsland A.E., Gianaros P.J., Abramowitch S.M., Manuck S.B., Hariri A.R. Interleukin-6 covaries inversely with hippocampal grey matter volume in middle-aged adults. Biol. Psychiatry 2008, 64:484-490.
36. McGeer P.L., Akiyama H., Kawamata T., Yamada T., Walker D.G., Ishii T. Immunohistochemical localization of β-amyloid precursor protein sequences in Alzheimer and normal brain tissue by light and electron microscopy. J.Neurosci. Res. 1992, 31:428-442.
37. McGeer P.L., McGeer E.G. Inflammation, autotoxicity and Alzheimer disease. Neurobiol. Aging 2001, 22:799-809.
38. McGeer P.L., Rogers J., McGeer E.G. Inflammation, anti-inflammatory agents and Alzheimer disease: the last 12 years. J.Alzheimer Dis. 2006, 9:271-276.
39. Mrak R.E., Sheng J.G., Griffin W.S. Glial cytokines in Alzheimer's disease: review and pathogenic implications. Hum. Pathol. 1995, 26:816-823.
40. Nakamichi K., Saiki M., Kitani H., Kuboyama Y., Morimoto K., Takayama-Ito M., Kurane I. Suppressive effect of simvastatin on interferon-β-induced expression of CC chemokine ligand 5 in microglia. Neurosci. Lett. 2006, 407:205-210.
41. Nakanishi H., Wu Z. Microglia-aging: roles of microglial lysosome- and mitochondria-derived reactive oxygen species in brain aging. Behav. Brain Res. 2009, 201:1-7.
42. Nakanishi H., Hayashi Y., Wu Z. The role of microglial mtDNA damage in age-dependent prolonged LPS-induced sickness behavior. Neuron Glia Biol. 2011, 7:17-23.
43. Nishimura M., Tomimoto H., Suenaga T., Nakamura S., Namba Y., Ikeda K., Akiguchi I., Kimura K. Synaptophysin and chromogranin A immunoreactivities of Lewy bodies in Parkinson's disease brains. Brain Res. 1994, 634:339-344.
44. Perry H.V., Matyszak M.K., Fearn S. Altered antigen expression of microglia in the aged rodent CNS. Glia 1993, 7:60-67.
45. Perry H.V., Newman T.A., Cunningham C. The impact of systemic infectionon the progression of neurodegenerative disease. Nat. Rev. Neurosci. 2003, 4:103-112.
46. Perry H.V. The influence of systemic inflammation on inflammation in the brain: implication for chronic neurodegenerative disease. Brain Behav. Immun. 2004, 18:407-413.
47. Perry H.V., Cunningham C., Holmes C. Systemic infection and inflammation affect chronic neurodegeneration. Nat. Rev. Immunol. 2007, 28:161-167.
48. Rangon C.M., Haïk S., Faucheux B.A., Metz-Boutigue M.H., Fierville F., Fuchs J.P., Hauw J.J., Aunis D. Different chromogranin immunoreactivity between prion and Aβ amyloid plaque. Neuroreport 2003, 14:755-758.
49. 1-42and delay the cognitive decline in a mouse model of Alzheimer's disease. J.Neurosci. 2008, 28:5784-5793.
50. Shaftel S.S., Griffin W.S., O'Banion M.K. The role of interleukin-1 in neuroinflammation and Alzheimer disease: an evolving perspective. J.Neuroinflammation 2008, 5:7.
51. Shao D.Z., Lin M. Platonin inhibits LPS-induced NF-κB by preventing activation of Ark and IKKβ in human PBMC. Inflamm. Res. 2008, 57:601-606.
52. Sun L., Wu Z., Hayashi Y., Peters C., Tsuda M., Inoue K., Nakanishi H. Microglial cathepsin B contributes to the initiation of peripheral inflammation -induced chronic pain. J.Neurosci. 2012, 32:11330-11342.
53. 7 nucleotide receptors on mouse microglial cell line. Biochim. Biophys. Acta 2005, 1726:177-186.
54. Terada K., Yamada J., Hayashi Y., Wu Z., Uchiyama Y., Peters C., Nakanishi H. Involvement of cathepsin B in the processing and secretion of interleukin-1β in chromogranin A-stimulated microglia. Glia 2010, 58:114-124.
55. Triantafilou M., Brandenburg K., Kusumoto S., Fukase K., Mackie A., Seydel U., Triantafilou K. Combinational clustering of receptors following stimulation by bacterial products determines lipopolysaccharide responses. Biochem. J. 2004, 381:527-536.
56. Walsh D.T., Betmouni S., Perry V.H. Absence of detectable IL-1βproduction in murine prion disease: a model of chronic neurodegeneration. J.Neuropathol. Exp. Neurol. 2001, 60:173-182.
57. Walter S., Letiembre M., Liu Y., Heine H., Penke B., Hao W., Bode B., Manietta N., Walter J., Schulz-Schuffer W., Fassbender K. Role of the toll-like receptor 4 in neuroinflammation in Alzheimer's disease. Cell. Physiol. Biochem. 2007, 20:947-956.
58. Wu Z., Tokuda Y., Zhang X.W., Nakanishi H. Age-dependent responses of glial cells and leptomeninges during systemic inflammation. Neurobiol. Dis. 2008, 32:543-551.
59. Yasuhara O., Akiguchi I., Nakamura S., Kinoshita A., Ikemoto A., Kawamoto Y., Kimura J., Funakoshi A., Tateishi K., McGeer P.L. Pancreastatin-like immunoreactivity in globular dystrophic neuritis of senile plaques in brains of patients with Alzheimer's disease. Neurosci. Lett. 1996, 208:167-170.
60. Yasuhara O., Kawamata T., Aimi Y., McGeer E.G., McGeer P.L. Expression of chromogranin A in lesions in the central nervous system from patients with neurological diseases. Neurosci. Lett. 1994, 170:13-16.
61. Yaffe K., Kanaya A., Lindquist K., Simonsick E.M., Harris T., Shorr R.I., Tylavsky F.A., Newman A.B. The metabolic syndrome, inflammation, and risk of cognitive decline. JAMA 2004, 292:2237-2242.
62. Zhang R., Yamada J., Hayashi Y., Wu Z., Koyama S., Nakanishi H. Inhibition of NMDA-induced outward currents by interleulin-1β in hippocampal neurons. Biochem. Biophys. Res. Commun. 2008, 372:816-820.
63. Zhang R., Sun L., Hayashi Y., Liu X., Koyama S., Wu Z., Nakanishi H. Acute p38-mediated inhibition of NMDA-induced outward currents in hippocampal CA1 neurons by interleukin-1β. Neurobiol. Dis. 2010, 38:68-77.