Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly

Neurobiology of Aging

Volumn 49, Issue , 2017, Pages 60-68

  Cattaneo, Annamaria ^a,b   Cattane, Nadia ^a   Galluzzi, Samantha ^a   Provasi, Stefania ^a   Lopizzo, Nicola ^a   Festari, Cristina ^a   Ferrari, Clarissa ^a   Guerra, Ugo Paolo ^c   Paghera, Barbara ^d   Muscio, Cristina ^a,e   Bianchetti, Angelo ^f   Volta, Giorgio Dalla ^g   Turla, Marinella ^h   Cotelli, Maria Sofia ^h   Gennuso, Michele ⁱ   Prelle, Alessandro ⁱ   Zanetti, Orazio ^a   Lussignoli, Giulia ^a   Mirabile, Dario ^e   Bellandi, Daniele ^j   Gentile, Simona ^k   Belotti, Gloria ^l   Villani, Daniele ^m   Harach, Taoufiq ⁿ   Bolmont, Tristan ^o   Padovani, Alessandro ^p   Boccardi, Marina ^a   Frisoni, Giovanni B ^a,q,r   more..

^a IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c Poliambulanza Foundation Hospital   (Italy)

^d SPEDALI CIVILI   (Italy)

^e Ospedale Briolini   (Italy)

^f Istituto Clinico Sant Anna Hospital   (Italy)

^g Neuroradiology Service   (Italy)

^h Neurology Unit   (Italy)

ⁱ MAGGIORE HOSPITAL   (Italy)

^j Istituto Ospedaliero di Sospiro   (Italy)

^k Istituto Ospedaliero di Sospiro ONLUS Foundation ^*  (Italy)

^l Santa Maria Ausiliatrice Foundation   (Italy)

^m Alzheimer Evaluation Unit   (Italy)

ⁿ EPFL   (Switzerland)

^o Stemedica International SA   (Switzerland)

^p UNIVERSITY OF BRESCIA   (Italy)

^q UNIVERSITY HOSPITAL   (Switzerland)

^r UNIVERSITY OF GENEVA   (Switzerland)

more..

Author keywords

Brain amyloidosis; Cognitive impairment; Gut microbiota; Inflammation; Neurodegeneration

Indexed keywords

CRYOPYRIN; CXCL2 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; TUMOR NECROSIS FACTOR; AMYLOID BETA PROTEIN; AUTACOID; CYTOKINE;

AGED; ALZHEIMER DISEASE; AMYLOIDOSIS; ARTICLE; BACTEROIDES FRAGILIS; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE ASSOCIATION; ESCHERICHIA; EUBACTERIUM; EUBACTERIUM HALLII; EUBACTERIUM RECTALE; FAECALIBACTERIUM PRAUSNITZII; FEMALE; GENE EXPRESSION; HUMAN; INTESTINE FLORA; MALE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; SHIGELLA; AMYLOID PLAQUE; BRAIN; INFLAMMATION; INTESTINE; METABOLISM; MICROBIOLOGY; MIDDLE AGED; PHYSIOLOGY;

AGED; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; BRAIN; COGNITION DISORDERS; CYTOKINES; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; INTESTINES; MALE; MIDDLE AGED; PLAQUE, AMYLOID;

EID: 84993945111     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2016.08.019     Document Type: Article

References (63)

1. Asti, A., Gioglio, L., Can a bacterial endotoxin be a key factor in the kinetics of amyloid fibril formation?. J. Alzheimers Dis. 39 (2014), 169–179.
2. Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K.D., Verdu, E.F., Collins, S.M., The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141 (2011), 599–609 609 e591-593.
3. Berer, K., Mues, M., Koutrolos, M., Rasbi, Z.A., Boziki, M., Johner, C., Wekerle, H., Krishnamoorthy, G., Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 479 (2011), 538–541.
4. Bruzzese, E., Callegari, M.L., Raia, V., Viscovo, S., Scotto, R., Ferrari, S., Morelli, L., Buccigrossi, V., Lo Vecchio, A., Ruberto, E., Guarino, A., Disrupted intestinal microbiota and intestinal inflammation in children with cystic fibrosis and its restoration with Lactobacillus GG: a randomised clinical trial. PLoS One, 9, 2014, e87796.
5. Cantarel, B.L., Waubant, E., Chehoud, C., Kuczynski, J., DeSantis, T.Z., Warrington, J., Venkatesan, A., Fraser, C.M., Mowry, E.M., Gut microbiota in multiple sclerosis: possible influence of immunomodulators. J. Investig. Med. 63 (2015), 729–734.
6. Cattaneo, A., Gennarelli, M., Uher, R., Aitchison, K.J., Craig, I.W., Anacker, C., Zunsztain, P.A., McGuffin, P., Pariante, C.M., Candidate genes expression profile associated with antidepressants response in the GENDEP study: differentiating between baseline ‘predictors’ and longitudinal ‘targets’. Neuropsychopharmacology 38 (2013), 377–385.
7. Chen, L., Na, R., Boldt, E., Ran, Q., NLRP3 inflammasome activation by mitochondrial reactive oxygen species plays a key role in long-term cognitive impairment induced by paraquat exposure. Neurobiol. Aging 36 (2015), 2533–2543.
8. Chorell, E., Andersson, E., Evans, M.L., Jain, N., Götheson, A., Åden, J., Chapman, M.R., Almqvist, F., Wittung-Stafshede, P., Bacterial chaperones CsgE and CsgC differentially modulate human α-synuclein amyloid formation via transient contacts. PLoS One, 10, 2015, e0140194.
9. Clark, C.M., Pontecorvo, M.J., Beach, T.G., Bedell, B.J., Coleman, R.E., Doraiswamy, P.M., Fleisher, A.S., Reiman, E.M., Sabbagh, M.N., Sadowsky, C.H., Schneider, J.A., Arora, A., Carpenter, A.P., Flitter, M.L., Joshi, A.D., Krautkramer, M.J., Lu, M., Mintun, M.A., Skovronsky, D.M., AV-45-A16 Study Group. Cerebral PET with florbetapir compared with neuropathology at autopsy for detection of neuritic amyloid-beta plaques: a prospective cohort study. Lancet Neurol 11 (2012), 669–678.
10. Clark, I.A., Vissel, B., Amyloid beta: one of three danger-associated molecules that are secondary inducers of the proinflammatory cytokines that mediate Alzheimer's disease. Br. J. Pharmacol. 172 (2015), 3714–3727.
11. Cleveland, W.S., Grosse, E., Shyu, W.M., Local regression models. Chambers, J.M., Hastie, T.J., (eds.) Statistical Models in S, 1992, Wadsworth & Brooks/Cole.
12. Cox, P.A., Banack, S.A., Murch, S.J., Rasmussen, U., Tien, G., Bidigare, R.R., Metcalf, J.S., Morrison, L.F., Codd, G.A., Bergman, B., Diverse taxa of cyanobacteria produce beta-N-methylamino-L-alanine, a neurotoxic amino acid. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 5074–5078.
13. Cryan, J.F., Dinan, T.G., Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13 (2012), 701–712.
14. De la Fuente, M., Franchi, L., Araya, D., Díaz-Jiménez, D., Olivares, M., Álvarez-Lobos, M., Golenbock, D., González, M.J., López-Kostner, F., Quera, R., Núñez, G., Vidal, R., Hermoso, M.A., Escherichia coli isolates from inflammatory bowel diseases patients survive in macrophages and activate NLRP3 inflammasome. Int. J. Med. Microbiol. 304 (2014), 384–392.
15. Del Tredici, K., Hawkes, C.H., Ghebremedhin, E., Braak, H., Lewy pathology in the submandibular gland of individuals with incidental Lewy body disease and sporadic Parkinson's disease. Acta Neuropathol. 119 (2010), 703–713.
16. Diaz Heijtz, R., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M.L., Forssberg, H., Pettersson, S., Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 3047–3052.
17. Doecke, J.D., Laws, S.M., Faux, N.G., Wilson, W., Burnham, S.C., Lam, C.P., Mondal, A., Bedo, J., Bush, A.I., Brown, B., De Ruyck, K., Ellis, K.A., Fowler, C., Gupta, V.B., Head, R., Macaulay, S.L., Pertile, K., Rowe, C.C., Rembach, A., Rodrigues, M., Rumble, R., Szoeke, C., Taddei, K., Taddei, T., Trounson, B., Ames, D., Masters, C.L., Martins, R.N., Alzheimer's Disease Neuroimaging Initiative; Australian Imaging Biomarker and Lifestyle Research Group. Blood-based protein biomarkers for diagnosis of Alzheimer disease. Arch. Neurol. 69 (2012), 1318–1325.
18. Erny, D., Hrabě de Angelis, A.L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., Schwierzeck, V., Utermöhlen, O., Chun, E., Garrett, W.S., McCoy, K.D., Diefenbach, A., Staeheli, P., Stecher, B., Amit, I., Prinz, M., Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 18 (2015), 965–977.
19. Evans, M.L., Chorell, E., Taylor, J.D., Åden, J., Götheson, A., Li, F., Koch, M., Sefer, L., Matthews, S.J., Wittung-Stafshede, P., Almqvist, F., Chapman, M.R., The bacterial curli system possesses a potent and selective inhibitor of amyloid formation. Mol Cell 57 (2015), 445–455.
20. Folstein, M.F., Folstein, S.E., McHugh, P.R., “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12 (1975), 189–198.
21. Forsyth, C.B., Shannon, K.M., Kordower, J.H., Voigt, R.M., Shaikh, M., Jaglin, J.A., Estes, J.D., Dodiya, H.B., Keshavarzian, A., Increased intestinal permeability correlates with sigmoid mucosa alpha-synuclein staining and endotoxin exposure markers in early Parkinson's disease. PLoS One, 6, 2011, e28032.
22. Forsythe, P., Kunze, W.A., Voices from within: gut microbes and the CNS. Cell Mol. Life Sci. 70 (2013), 55–69.
23. Friedland, R.P., Mechanisms of molecular mimicry involving the microbiota in neurodegeneration. J. Alzheimers Dis. 45 (2015), 349–362.
24. Goedert, M., Spillantini, M.G., Del Tredici, K., Braak, H., 100 years of Lewy pathology. Nat. Rev. Neurol. 9 (2013), 13–24.
25. 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-beta. Nat. Immunol. 9 (2008), 857–865.
26. Hasegawa, S., Goto, S., Tsuji, H., Okuno, T., Asahara, T., Nomoto, K., Shibata, A., Fujisawa, Y., Minato, T., Okamoto, A., Ohno, K., Hirayama, M., Intestinal dysbiosis and lowered serum lipopolysaccharide-binding protein in Parkinson's disease. PLoS One, 10, 2015, e0142164.
27. Heneka, M.T., Golenbock, D.T., Latz, E., Innate immunity in Alzheimer's disease. Nat. Immunol. 16 (2015), 229–236.
28. Heneka, M.T., Kummer, M.P., Stutz, A., Delekate, A., Schwartz, S., Vieira-Saecker, A., Griep, A., Axt, D., Remus, A., Tzeng, T.C., Gelpi, E., Halle, A., Korte, M., Latz, E., Golenbock, D.T., NLRP3 is activated in Alzheimer's disease and contributes to pathology in APP/PS1 mice. Nature 493 (2013), 674–678.
29. Heppner, F.L., Ransohoff, R.M., Becher, B., Immune attack: the role of inflammation in Alzheimer disease. Nat. Rev. Neurosci. 16 (2015), 358–372.
30. Holmes, E., Li, J.V., Marchesi, J.R., Nicholson, J.K., Gut microbiota composition and activity in relation to host metabolic phenotype and disease risk. Cell Metab. 16 (2012), 559–564.
31. Huang, Y.L., Chassard, C., Hausmann, M., von Itzstein, M., Hennet, T., Sialic acid catabolism drives intestinal inflammation and microbial dysbiosis in mice. Nat. Commun., 6, 2015, 8141.
32. Jack, C.R. Jr., Barrio, J.R., Kepe, V., Cerebral amyloid PET imaging in Alzheimer's disease. Acta Neuropathol. 126 (2013), 643–657.
33. Kamer, A.R., Fortea, J.O., Videla, S., Mayoral, A., Janal, M., Carmona-Iragui, M., Benejam, B., Craig, R.G., Saxena, D., Corby, P., Glodzik, L., Annam, K.R., Robbins, M., de Leon, M.J., Periodontal disease's contribution to Alzheimer's disease progression in Down syndrome. Alzheimers Dement (Amst) 2 (2016), 49–57.
34. Kauwe, J.S., Bailey, M.H., Ridge, P.G., Perry, R., Wadsworth, M.E., Hoyt, K.L., Staley, L.A., Karch, C.M., Harari, O., Cruchaga, C., Ainscough, B.J., Bales, K., Pickering, E.H., Bertelsen, S. Alzheimer's Disease Neuroimaging Initiative, Fagan, A.M., Holtzman, D.M., Morris, J.C., Goate, A.M., Genome-wide association study of CSF levels of 59 Alzheimer's disease candidate proteins: significant associations with proteins involved in amyloid processing and inflammation. PLoS Genet., 10, 2014, e1004758.
35. Keshavarzian, A., Green, S.J., Engen, P.A., Voigt, R.M., Naqib, A., Forsyth, C.B., Mutlu, E., Shannon, K.M., Colonic bacterial composition in Parkinson's disease. Mov. Disord. 30 (2015), 1351–1360.
36. Kolho, K.L., Korpela, K., Jaakkola, T., Pichai, M.V., Zoetendal, E.G., Salonen, A., de Vos, W.M., Fecal microbiota in pediatric inflammatory bowel disease and its relation to inflammation. Am. J. Gastroenterol. 110 (2015), 921–930.
37. Latta, C.H., Brothers, H.M., Wilcock, D.M., Neuroinflammation in Alzheimer's disease; a source of heterogeneity and target for personalized therapy. Neuroscience 302 (2015), 103–111.
38. Lebouvier, T., Neunlist, M., Bruley des Varannes, S., Coron, E., Drouard, A., N'Guyen, J.M., Chaumette, T., Tasselli, M., Paillusson, S., Flamand, M., Galmiche, J.P., Damier, P., Derkinderen, P., Colonic biopsies to assess the neuropathology of Parkinson's disease and its relationship with symptoms. PLoS One, 5, 2010, e12728.
39. Lee, Y.K., Menezes, J.S., Umesaki, Y., Mazmanian, S.K., Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 4615–4622.
40. Leung, R., Proitsi, P., Simmons, A., Lunnon, K., Güntert, A., Kronenberg, D., Pritchard, M., Tsolaki, M., Mecocci, P., Kloszewska, I., Vellas, B., Soininen, H., Wahlund, L.O., Lovestone, S., Inflammatory proteins in plasma are associated with severity of Alzheimer's disease. PLoS One, 8, 2013, e64971.
41. Li, M., Zhou, H., Hua, W., Wang, B., Wang, S., Zhao, G., Li, L., Zhao, L., Pang, X., Molecular diversity of bacteroides spp. in human fecal microbiota as determined by group-specific 16S rRNA gene clone library analysis. Syst. Appl. Microbiol. 32 (2009), 193–200.
42. Luo, J., Wang, T., Liang, S., Hu, X., Li, W., Jin, F., Ingestion of Lactobacillus strain reduces anxiety and improves cognitive function in the hyperammonemia rat. Sci China Life Science 57 (2014), 327–335.
43. Martinon, F., Mayor, A., Tschopp, J., The inflammasomes: guardians of the body. Annu. Rev. Immunol. 27 (2009), 229–265.
44. Monson, N.L., Ireland, S.J., Ligocki, A.J., Chen, D., Rounds, W.H., Li, M., Huebinger, R.M., Munro Cullum, C., Greenberg, B.M., Stowe, A.M., Zhang, R., Elevated CNS inflammation in patients with preclinical Alzheimer's disease. J. Cereb. Blood Flow Metab. 34 (2014), 30–33.
45. Morgan, K.L., Infection, illness, and fenugreek seeds: was illness a good enough proxy for infection in the 2011 outbreak of shiga toxin-producing Escherichia coli O104:H4 in France?. Clin. Infect. Dis. 56 (2013), 1055–1056.
46. Nascimento, C.M., Pereira, J.R., de Andrade, L.P., Garuffi, M., Talib, L.L., Forlenza, O.V., Cancela, J.M., Cominetti, M.R., Stella, F., Physical exercise in MCI elderly promotes reduction of pro-inflammatory cytokines and improvements on cognition and BDNF peripheral levels. Curr. Alzheimer Res. 11 (2014), 799–805.
47. Olanow, C.W., Wakeman, D.R., Kordower, J.H., Peripheral alpha-synuclein and Parkinson's disease. Mov. Disord. 29 (2014), 963–966.
48. Palm, N.W., de Zoete, M.R., Flavell, R.A., Immune-microbiota interactions in health and disease. Clin. Immunol. 159 (2015), 122–127.
49. Petra, A.I., Panagiotidou, S., Hatziagelaki, E., Stewart, J.M., Conti, P., Theoharides, T.C., Gut-microbiota-brain axis and its effect on neuropsychiatric disorders with suspected immune dysregulation. Clin. Ther. 37 (2015), 984–995.
50. Pryde, S.E., Duncan, S.H., Hold, G.L., Stewart, C.S., Flint, H.J., The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 217 (2002), 133–139.
51. Ray, S., Britschgi, M., Herbert, C., Takeda-Uchimura, Y., Boxer, A., Blennow, K., Friedman, L.F., Galasko, D.R., Jutel, M., Karydas, A., Kaye, J.A., Leszek, J., Miller, B.L., Minthon, L., Quinn, J.F., Rabinovici, G.D., Robinson, W.H., Sabbagh, M.N., So, Y.T., Sparks, D.L., Tabaton, M., Tinklenberg, J., Yesavage, J.A., Tibshirani, R., Wyss-Coray, T., Classification and prediction of clinical Alzheimer's diagnosis based on plasma signaling proteins. Nat. Med. 13 (2007), 1359–1362.
52. Scheltens, P., Barkhof, F., Leys, D., Pruvo, J.P., Nauta, J.J., Vermersch, P., Steinling, M., Valk, J., A semiquantative rating scale for the assessment of signal hyperintensities on magnetic resonance imaging. J. Neurol. Sci. 114 (1993), 7–12.
53. Scheperjans, F., Aho, V., Pereira, P.A., Koskinen, K., Paulin, L., Pekkonen, E., Haapaniemi, E., Kaakkola, S., Eerola-Rautio, J., Pohja, M., Kinnunen, E., Murros, K., Auvinen, P., Gut microbiota are related to Parkinson's disease and clinical phenotype. Mov. Disord. 30 (2015), 350–358.
54. Schmittgen, T.D., Livak, K.J., Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3 (2008), 1101–1108.
55. Schwartz, A., What's next for Alzheimer treatment? While Abeta isn't out of the picture yet, several other therapeutic routes are being explored. Ann. Neurol. 73 (2013), A7–A9.
56. Small, C.L., Reid-Yu, S.A., McPhee, J.B., Coombes, B.K., Persistent infection with Crohn's disease-associated adherent-invasive Escherichia coli leads to chronic inflammation and intestinal fibrosis. Nat. Commun., 4, 2013, 1957.
57. Soares, D.M., Figueiredo, M.J., Martins, J.M., Machado, R.R., Sorgi, C., Faciolli, L.H., Alves-Filho, J.C., Cunha, F.Q., Souza, G.E., A crucial role for IL-6 in the CNS of rats during fever induced by the injection of live E. coli. Med. Microbiol. Immunol. 201 (2012), 47–60.
58. Soares, H.D., Potter, W.Z., Pickering, E., Kuhn, M., Immermann, F.W., Shera, D.M., Ferm, M., Dean, R.A., Simon, A.J., Swenson, F., Siuciak, J.A., Kaplow, J., Thambisetty, M., Zagouras, P., Koroshetz, W.J., Wan, H.I., Trojanowski, J.Q., Shaw, L.M., Biomarkers Consortium Alzheimer's Disease Plasma Proteomics Project. Plasma biomarkers associated with the apolipoprotein E genotype and Alzheimer disease. Arch. Neurol. 69 (2012), 1310–1317.
59. Stoeck, K., Schmitz, M., Ebert, E., Schmidt, C., Zerr, I., Immune responses in rapidly progressive dementia: a comparative study of neuroinflammatory markers in Creutzfeldt-Jakob disease, Alzheimer's disease and multiple sclerosis. J. Neuroinflammation, 11, 2014, 170.
60. Tan, M.S., Yu, J.T., Jiang, T., Tan, L., The NLRP3 inflammasome in Alzheimer's disease. Mol. Neurobiol. 48 (2013), 875–882.
61. Toumi, R., Soufli, I., Rafa, H., Belkhelfa, M., Biad, A., Touil-Boukoffa, C., Probiotic bacteria lactobacillus and bifidobacterium attenuate inflammation in dextran sulfate sodium-induced experimental colitis in mice. Int J Immunopathol Pharmacol 27 (2014), 615–627.
62. Wahlund, L.O., Barkhof, F., Fazekas, F., Bronge, L., Augustin, M., Sjögren, M., Wallin, A., Ader, H., Leys, D., Pantoni, L., Pasquier, F., Erkinjuntti, T., Scheltens, P., European Task Force on Age-Related White Matter Changes. A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke 32 (2001), 1318–1322.
63. Vom Berg, J., Prokop, S., Miller, K.R., Obst, J., Kälin, R.E., Lopategui-Cabezas, I., Wegner, A., Mair, F., Schipke, C.G., Peters, O., Winter, Y., Becher, B., Heppner, F.L., Inhibition of IL-12/IL-23 signaling reduces Alzheimer's disease-like pathology and cognitive decline. Nat. Med. 18 (2012), 1812–1819.