Gut microbiota influences Alzheimer's disease pathogenesis by regulating acetate in Drosophila model

Future Microbiology

Volumn 13, Issue 10, 2018, Pages 1117-1128

  Kong, Yan ^a   Jiang, Baichun ^b   Luo, Xuancai ^c  

^a MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

^b Shandong Key Laboratory of Digital Human and Clinical Anatomy   (China)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

16S rRNA gene sequencing; acetate; Alzheimer's disease; Drosophila; GC MS; microbiota; SCFA

Indexed keywords

ACETIC ACID; AMYLOID PROTEIN; BACTERIAL DNA; BACTERIAL RNA; BUTYRIC ACID; ISOBUTYRIC ACID; ISOVALERIC ACID; PROPIONIC ACID; RNA 16S; SHORT CHAIN FATTY ACID;

ACETOBACTER; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FRUIT FLY MODEL; INTESTINE FLORA; LACTOBACILLUS; MALE; NONHUMAN; PATHOGENESIS; PREVOTELLA; PRIORITY JOURNAL; RNA SEQUENCE; ANIMAL; BACTERIUM; BIODIVERSITY; CLASSIFICATION; DISEASE MODEL; DROSOPHILA; GENETICS; METABOLISM; METABOLOME; MICROBIOLOGY; PHENOTYPE; PHYSIOLOGY;

ACETATES; ALZHEIMER DISEASE; ANIMALS; BACTERIA; BIODIVERSITY; DISEASE MODELS, ANIMAL; DROSOPHILA; GASTROINTESTINAL MICROBIOME; METABOLOME; PHENOTYPE; RNA, RIBOSOMAL, 16S;

EID: 85053243169     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb-2018-0185     Document Type: Article

References (59)

1. Ferri CP, Prince M, Brayne C et al. Global prevalence of dementia: A Delphi consensus study. Lancet 366(9503), 2112-2117 (2005).
2. Ittner LM, Götze J. Amyloid-β and tau: A toxic pas de deux in Alzheimers disease. Nat. Rev. Neurosci. 12(2), 65-72 (2011).
3. Karran E, Mercken M, De Strooper B. The amyloid cascade hypothesis for Alzheimers disease: An appraisal for the development of therapeutics. Nat. Rev. Drug Discov. 10(9), 698-712 (2011).
4. Lian H, Litvinchuk A, Chiang AC, Aithmitti N, Jankowsky JL, Zheng H. Astrocyte-microglia cross-Talk through complement activation modulates amyloid pathology in mouse models of Alzheimers disease. J. Neurosci. 36(2), 577-589 (2016).
5. Polanco JC, Li C, Bodea LG, Martinez-Marmol R, Meunier FA, Götz J. Amyloid-β and tau complexity: Toward improved biomarkers and targeted therapies. Nat. Rev. Neurol. 14(1), 22-39 (2018).
6. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science 307(5717), 1915-1920 (2005).
7. Thursby E, Juge N. Introduction to the human gut microbiota. Biochem. J. 474(11), 1823-1836 (2017).
8. OToole PW, Jeffery IB. Gut microbiota and aging. Science 350(6525), 1214-1215 (2015).
9. Fukami H, Kobayashi S, Tachimoto H et al. Effect of continuous ingestion of acetic acid bacteria on memory retention and the synaptic function in aged rats. Biosci Biotechnol. Biochem. 74(7), 1498-500 (2010).
10. Fukami H, Tachimoto H, Kishi M et al. Continuous ingestion of acetic acid bacteria: effect on cognitive function in healthy middle-Aged and elderly persons. Antiaging Med. 6(7), 60-65 (2009).
11. Athari Nik Azm S, Djazayeri A, Safa M et al. Lactobacillus and Bifidobacterium ameliorate memory and learning deficits and oxidative stress in Aβ (1-42) injected rats. Appl. Physiol. Nutr. Metab. 20, 1-9 (2018).
12. Akbari E, Asemi Z, Daneshvar Kakhaki R et al. Effect of probiotic supplementation on cognitive function and metabolic status in Alzheimers disease: A randomized, double-blind and controlled trial. Front Aging Neurosci. 8, 256 (2016).
13. Dinan TG, Cryan JF. Gut-brain axis in 2016: Brain-gut microbiota axis: mood, metabolism and behavior. Nat. Rev. Gastroenterol. Hepatol. 14(2), 69-70 (2017).
14. Bhattacharjee S, Lukiw WJ. Alzheimers disease and the microbiome. Front. Cell. Neurosci. 7, 153 (2013).
15. Pistollato F, Sumalla Cano S, Elio I et al. Role of gut microbiota and nutrients in amyloid formation and pathogenesis of Alzheimer disease. Nutr. Rev. 74(10), 624-634 (2016).
16. Lei E, Vacy K, Boon WC. Fatty acids and their therapeutic potential in neurological disorders. Neurochem. Int. 95, 75-84 (2016).
17. Chen X, Bisschops MMM, Agarwal NR, Ji B, Shanmugavel KP, Petranovic D. Interplay of energetics and ER stress exacerbates Alzheimers amyloid-β (Aβ) toxicity in yeast. Front. Mol. Neurosci. 10, 232 (2017).
18. Sorrentino V, Romani M, Mouchiroud L et al. Enhancing mitochondrial proteostasis reduces amyloid-β proteotoxicity. Nature 552(7684), 187-193 (2017).
19. Fernandez-Funez P, de Mena L, Rincon-Limas DE. Modeling the complex pathology of Alzheimers disease in Drosophila. Exp. Neurol. 274(Pt A), 58-71 (2015).
20. Jankowsky JL, Zheng H. Practical considerations for choosing a mouse model of Alzheimers disease.Mol. Neurodegener. 12(1), 89 (2017).
21. Cohen RM, Rezai-Zadeh K, Weitz TM et al. A transgenic Alzheimer rat with plaques, tau pathology, behavioral impairment, oligomeric Aβ and frank neuronal loss. J. Neurosci. 33(15), 6245-6256 (2013).
22. Van Dam D, De Deyn PP. Nonhuman primate models for Alzheimers disease-related research and drug discovery. Expert Opin. Drug Discov. 12(2), 187-200 (2017).
23. Iijima K, Liu HP, Chiang AS et al. Dissecting the pathological effects of human Abeta40 and Abeta42 in Drosophila: A potential model for Alzheimers disease. Proc. Natl Acad. Sci. USA 101(17), 6623-6628 (2004).
24. Ray A, Speese SD, Logan MA. Glial draper rescues Aβ toxicity in a Drosophila model of Alzheimers disease. J. Neurosci. 37(49), 11881-11893 (2017).
25. Marcora MS, Belfiori-Carrasco LF, Bocai NI, Morelli L, Castano EM. Amyloid-β42 clearance and neuroprotection mediated by X-box-binding protein 1 signaling decline with aging in the Drosophila brain. Neurobiol. Aging 60, 57-70 (2017).
26. Kong Y, Li K, Fu T et al. Quercetin ameliorates Aβ toxicity in Drosophila AD model by modulating cell cycle-related protein expression. Oncotarget 7(42), 67716-67731 (2016).
27. Johnson AA, Sarthi J, Pirooznia SK. Increasing Tip60 HAT levels rescues axonal transport defects and associated behavioral phenotypes in a Drosophila Alzheimers disease model. J. Neurosci. 33(17), 7535-7547 (2013).
28. Hong YK, Lee S, Park SH et al. Inhibition of JNK/dFOXO pathway and caspases rescues neurological impairments in Drosophila Alzheimers disease model. Biochem. Biophys. Res. Commun. 419(1), 49-53 (2012).
29. Casas-Tinto S, Zhang Y, Sanchez-Garcia J, Gomez-Velazquez M, Rincon-Limas DE, Fernandez-Funez P. The ER stress factor XBP1s prevents amyloid-β neurotoxicity. Hum. Mol. Genet. 20(11), 2144-2160 (2011).
30. Sofola O, Kerr F, Rogers I et al. Inhibition of GSK-3 ameliorates Abeta pathology in an adult-onset Drosophila model of Alzheimers disease. PLoS Genet. 6(9), e1001087 (2010).
31. Clark RI, Walker DW. Role of gut microbiota in aging-related health decline: insights from invertebrate models. Cell Mol. Life Sci. 75(1), 93-101 (2018).
32. Broderick NA, Lemaitre B. Gut-Associated microbes of Drosophila melanogaster. Gut Microbes 3(4), 307-321 (2012).
33. Shin SC, Kim SH, You H et al. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334(6056), 670-674 (2011).
34. Erkosar B, Defaye A, Bozonnet N, Puthier D, Royet J, Leulier F. Drosophila microbiota modulates host metabolic gene expression via IMD/NF-κB signaling. PLoS ONE 9(4), e94729 (2014).
35. Clark RI, Salazar A, Yamada R et al. Distinct shifts in microbiota composition during Drosophila aging impair intestinal function and drive mortality. Cell Rep. 12(10), 1656-1567 (2015).
36. Yamada R, Deshpande SA, Bruce KD, Mak EM, Ja WW. Microbes promote amino acid harvest to rescue undernutrition in Drosophila. Cell Rep. 10, 865-872 (2015).
37. Singh N, Arioli S, Wang A et al. Impact of Bifidobacterium bifidum MIMBb75 on mouse intestinal microorganisms. FEMS Microbiol. Ecol. 85(2), 369-375 (2013).
38. Walters W, Hyde ER, Berg-Lyons D et al. Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1(1), E00009-E000015 (2015).
39. Fernando WMADB, Rainey-Smith SR, Martins IJ, Martins RN. In vitro study to assess the potential of short chain fatty acids (SCFA) as therapeutic agents for Alzheimers disease. Alzheimers & Dementia 10(4), 626 (2014).
40. Carabotti M, Scirocco A, Maselli MA, Severi C. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann. Gastroenterol. 28(2), 203-209 (2015).
41. Cryan JF, Dinan TG. Mind-Altering microorganisms: The impact of the gut microbiota on brain and behavior. Nat. Rev. Neurosci. 13(10), 701-712 (2012).
42. Braniste V, Al-Asmakh M, Kowal C et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci. Transl. Med. 6(263), 263ra158 (2014).
43. Fukami H, Tachimoto H, Kishi M, Kaga T, Tanaka Y. Acetic acid bacterial lipids improve cognitive function in dementia model rats. J. Agric. Food Chem. 58(7), 4084-4089 (2010).
44. Park JY, Choi J, Lee Y et al. Metagenome analysis of bodily microbiota in a mouse model of Alzheimer disease using bacteria-derived membrane vesicles in blood. Exp. Neurobiol. 26(6), 369-379 (2017).
45. Lee WJ, Hase K. Gut microbiota-generated metabolites in animal health and disease. Nat. Chem. Biol. 10(6), 416-424 (2014).
46. Frost G, Sleeth ML, Sahuri-Arisoylu M et al. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat. Commun. 5, 3611 (2014).
47. Perry RJ, Peng L, Barry NA et al. Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome. Nature 534(7606), 213-217 (2016).
48. Burokas A, Arboleya S, Moloney RD et al. Targeting the microbiota gut-grain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol. Psychiatry 82(7), 472-487 (2017).
49. Unger MM, Spiegel J, Dillmann KU et al. Short chain fatty acids and gut microbiota differ between patients with Parkinsons disease and age-matched controls. Parkinsonism Relat. Disord. 32, 66-72 (2016).
50. Nankova BB, Agarwal R, MacFabe DF, La Gamma EF. Enteric bacterial metabolites propionic and butyric acid modulate gene expression, including CREB-dependent catecholaminergic neurotransmission, in PC12 cells: possible relevance to autism spectrum disorders. PLoS ONE 9(8), e103740 (2014).
51. MacFabe DF. Enteric short-chain fatty acids: microbial messengers of metabolism, mitochondria and mind: implications in autism spectrum disorders. Microb. Ecol. Health Dis. 26, 28177 (2015).
52. Lei E, Vacy K, Boon WC. Fatty acids and their therapeutic potential in neurological disorders. Neurochem. Int. 95, 75-84 (2016).
53. Joseph J, Depp C, Shih PB, Cadenhead KS, Schmid-Schönbein G. Modified mediterranean diet for enrichment of short-chain fatty acids: potential adjunctive therapeutic to target immune and metabolic dysfunction in schizophrenia? Front. Neurosci. 11, 155 (2017).
54. Brandscheid C, Schuck F, Reinhardt S et al. Altered gut microbiome composition and tryptic activity of the 5 FAD Alzheimers mouse model. J. Alzheimers Dis. 56(2), 775-788 (2017).
55. Shen L, Liu L, Ji HF. Alzheimers disease histological and behavioral manifestations in transgenic mice correlate with specific gut microbiome state. J. Alzheimers Dis. 56(1), 385-390 (2017).
56. Cattaneo A, Cattane N, Galluzzi S. Association of brain amyloidosis with proinflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol. Aging 49, 60-68 (2017).
57. Cox CR, Gilmore MS. Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infect. Immun. 75(4), 1565-76 (2007).
58. Deshpande SA, Yamada R, Mak CM. Acidic food pH increases palatability and consumption and extends Drosophila lifespan. J. Nutr. 145(12), 2789-96 (2015).
59. Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 107(46), 20051-20056 (2010).