1,707
Views
0
CrossRef citations to date
0
Altmetric
In vitro and animal studies

Long-term supplementation with anthocyanin-rich or -poor Rubus idaeus berries does not influence microvascular architecture nor cognitive outcome in the APP/PS-1 mouse model of Alzheimer’s disease

, , ORCID Icon, , ORCID Icon, , , , , , ORCID Icon & ORCID Icon show all
Pages 33-50 | Received 26 Sep 2022, Accepted 25 Oct 2022, Published online: 30 Nov 2022

References

  • Ackermann M, Konerding M. 2015. Vascular casting for the study of vascular morphogenesis. Methods Mol Biol (Clifton, N.J.). 1214:49–66.
  • Adelman R, Saul RL, Ames BN. 1988. Oxidative damage to DNA: relation to species metabolic rate and life span. Proc Natl Acad Sci USA. 85(8):2706–2708.
  • Allwood JW, Weber RJM, Zhou J, He S, Viant MR, Dunn WB. 2013. CASMI-the small molecule identification process from a Birmingham perspective. Metabolites. 3(2):397–411.
  • Beckmann N, Schuler A, Mueggler T, Meyer E, Wiederhold K, Staufenbiel M, Krucker T. 2003. Age-dependent cerebrovascular abnormalities and blood flow disturbances in APP23 mice modeling Alzheimer’s disease. J Neurosci. 23(24):8453–8459.
  • Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Series B (Methodological). 57(1):289–300.
  • Berendsen AM, Kang JH, Feskens EJM, de Groot CPGM, Grodstein F, van de Rest O. 2018. Association of long-term adherence to the MIND Diet with cognitive function and cognitive decline in American women. J Nutr Health Aging. 22(2):222–229.
  • Bookheimer SY, Strojwas MH, Cohen MS, Saunders AM, Pericak-Vance MA, Mazziotta JC, Small GW. 2000. Patterns of brain activation in people at risk for Alzheimer’s disease. N Engl J Med. 343(7):450–456.
  • Brown M, Wedge DC, Goodacre R, Kell DB, Baker PN, Kenny LC, Mamas MA, Neyses L, Dunn WB. 2011. Automated workflows for accurate mass-based putative metabolite identification in LC/MS-derived metabolomic datasets. Bioinformatics. 27(8):1108–1112.
  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 13(7):581–583.
  • Cao J, Amakye WK, Qi C, Liu X, Ma J, Ren J. 2021. Bifidobacterium Lactis Probio-M8 regulates gut microbiota to alleviate Alzheimer’s disease in the APP/PS1 mouse model. Eur J Nutr. 60(7):3757–3769.
  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 7(5):335–336.
  • Dal-Pan A, Dudonné S, Bourassa P, Bourdoulous M, Tremblay C, Desjardins Y, Calon F, on behalf of the Neurophenols consortium 2016. Cognitive-enhancing effects of a polyphenols-rich extract from fruits without changes in neuropathology in an animal model of Alzheimer’s disease. JAD. 55(1):115–135.
  • El Gaamouch F, Liu K, Lin H, Wu C, Wang J. 2021. Development of grape polyphenols as multi-targeting strategies for Alzheimer’s disease. Neurochem Int. 147:105046.
  • Elmaleh DR, Downey MA, Kundakovic L, Wilkinson JE, Neeman Z, Segal E. 2021. New approaches to profile the microbiome for treatment of neurodegenerative disease. J Alzheimers Dis. 82(4):1373–1401.
  • Fan X, Liu B, Zhou J, Gu X, Zhou Y, Yang Y, Guo F, Wei X, Wang H, Si N, et al. 2021. High-fat diet alleviates neuroinflammation and metabolic disorders of APP/PS1 mice and the intervention with chinese medicine. Front Aging Neurosci. 13:658376.
  • Farkas E, Luiten PGM. 2001. Cerebral microvascular pathology in aging and Alzheimer’s disease. Prog Neurobiol. 64(6):575–611.
  • Ghosh S, Whitley CS, Haribabu B, Jala VR. 2021. Regulation of intestinal barrier function by microbial metabolites. Cell Mol Gastroenterol Hepatol. 11(5):1463–1482.
  • Gildawie KR, Galli RL, Shukitt-Hale B, Carey AN. 2018. Protective effects of foods containing flavonoids on age-related cognitive decline. Curr Nutr Rep. 7(2):39–48.
  • Go J, Chang D, Ryu Y, Park H, Lee I, Noh J, Hwang DY, Kim B, Kim K, Lee C. 2021. Human gut microbiota Agathobaculum butyriciproducens improves cognitive impairment in LPS-induced and APP/PS1 mouse models of Alzheimer’s disease. Nutr Res. 86:96–108.
  • Han D, Li Z, Liu T, Yang N, Li Y, He J, Qian M, Kuang Z, Zhang W, Ni C, et al. 2020. Prebiotics regulation of intestinal microbiota attenuates cognitive dysfunction induced by surgery stimulation in APP/PS1 mice. Aging Dis. 11(5):1029–1045.
  • Hendrickx JO, Martinet W, Van Dam D, De Meyer , Guido RY. 2021. Inflammation, nitro-oxidative stress, impaired autophagy, and insulin resistance as a mechanistic convergence between arterial stiffness and Alzheimer’s disease. Front Mol Biosci. 8:651215.
  • Herring WL, Gould IG, Fillit H, Lindgren P, Forrestal F, Thompson R, Pemberton-Ross P. 2021. Predicted lifetime health outcomes for aducanumab in patients with early Alzheimer’s disease. Neurol Ther. 10(2):919–940.
  • Hoyles L, Snelling T, Umlai U, Nicholson JK, Carding SR, Glen RC, McArthur S. 2018. Microbiome-host systems interactions: protective effects of propionate upon the blood-brain barrier. Microbiome. 6(1):55.
  • Jawhar S, Wirths O, Bayer TA. 2011. Pyroglutamate amyloid-β (Aβ): a hatchet man in Alzheimer disease. J Biol Chem. 286(45):38825–38832.
  • Jefferies WA, Price KA, Biron KE, Fenninger F, Pfeifer CG, Dickstein DL. 2013. Adjusting the compass: new insights into the role of angiogenesis in Alzheimer’s disease. Alzheimers Res Ther. 5(6):64.
  • Joshua M, Okere C, Sylvester OP, Yahaya M, Precious O, Dluya T, Um J, Neksumi M, Boyd J, Vincent-Tyndall J, et al. 2017. Disruption of angiogenesis by anthocyanin-rich extracts of Hibiscus sabdariffa. Int J Sci Eng Res. 8(2):299–307.
  • Kay CD, Mazza G, Holub BJ, Wang J. 2004. Anthocyanin metabolites in human urine and serum. Br J Nutr. 91(6):933–942.
  • Kelly P, Denver P, Satchell SC, Ackermann M, Konerding MA, Mitchell CA. 2017. Microvascular ultrastructural changes precede cognitive impairment in the murine APPswe/PS1dE9 model of Alzheimer’s disease. Angiogenesis. 20(4):567–580.
  • Kelly P, McClean PL, Ackermann M, Konerding MA, Hölscher C, Mitchell CA. 2015. Restoration of cerebral and systemic microvascular architecture in APP/PS1 transgenic mice following treatment with Liraglutide™. Microcirculation. 22(2):133–145.
  • Khan A, Kalaria RN, Corbett A, Ballard C. 2016. Update on vascular dementia. J Geriatr Psychiatry Neurol. 29(5):281–301.
  • Kiray H. 2015. Identification of astrocytic factors that could play a role in myelination. University of Glasgow. https://eleanor.lib.gla.ac.uk/record=b3120656.
  • Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO. 2013. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41(1):e1.
  • Knopman DS, Roberts R. 2010. Vascular risk factors: imaging and neuropathologic correlates. J Alzheimers Dis. 20(3):699–709.
  • Lamar M, Boots EA, Arfanakis K, Barnes LL, Schneider JA. 2020. Common brain structural alterations associated with cardiovascular disease risk factors and Alzheimer’s dementia: future directions and implications. Neuropsychol Rev. 30(4):546–557.
  • Lamport DJ, Williams CM. 2021. Polyphenols and cognition in humans: an overview of current evidence from recent systematic reviews and meta-analyses. Brain Plast. 6(2):139–153.
  • Lee J, Choi J, Wong GW, Wolfgang MJ. 2016. Neurometabolic roles of ApoE and Ldl-R in mouse brain. J Bioenerg Biomembr. 48(1):13–21.
  • Lee Y, Lai D, Huang H, Lee-Chen G, Chang C, Hsieh-Li HM, Lee G. 2021. Prebiotic lactulose ameliorates the cognitive deficit in Alzheimer’s disease mouse model through macroautophagy and chaperone-mediated autophagy pathways. J Agric Food Chem. 69(8):2422–2437.
  • Liang Q, Liu H, Zhang T, Jiang Y, Xing H, Zhang A. 2015. Metabolomics-based screening of salivary biomarkers for early diagnosis of Alzheimer’s disease. RSC Adv. 5(116):96074–96079.
  • Liu D, Du D. 2020. Mulberry fruit extract alleviates cognitive impairment by promoting the clearance of amyloid-β and inhibiting neuroinflammation in Alzheimer’s disease mice. Neurochem Res. 45(9):2009–2019.
  • Lyras L, Cairns NJ, Jenner A, Jenner P, Halliwell B. 1997. An assessment of oxidative damage to proteins, lipids, and DNA in brain from patients with Alzheimer’s disease. J Neurochem. 68(5):2061–2069.
  • McDougall GJ, Allwood JW, Pereira-Caro G, Brown EM, Verrall S, Stewart D, Latimer C, McMullan G, Lawther R, O'Connor G, et al. 2017. Novel colon-available triterpenoids identified in raspberry fruits exhibit antigenotoxic activities in vitro. Mol Nutr Food Res. 61(2):1600327.
  • Meyer EP, Ulmann-Schuler A, Staufenbiel M, Krucker T. 2008. Altered morphology and 3D architecture of brain vasculature in a mouse model for Alzheimer’s disease. Proc Natl Acad Sci U S A. 105(9):3587–3592.
  • Miller MG, Hamilton DA, Joseph JA, Shukitt-Hale B. 2018. Dietary blueberry improves cognition among older adults in a randomized, double-blind, placebo-controlled trial. Eur J Nutr. 57(3):1169–1180.
  • Morris MC, Tangney CC, Wang Y, Sacks FM, Barnes LL, Bennett DA, Aggarwal NT. 2015. MIND diet slows cognitive decline with aging. Alzheimers Dement. 11(9):1015–1022.
  • Nation DA, Sweeney MD, Montagne A, Sagare AP, D'Orazio LM, Pachicano M, Sepehrband F, Nelson AR, Buennagel DP, Harrington MG, et al. 2019. Blood-brain barrier breakdown is an early biomarker of human cognitive dysfunction. Nat Med. 25(2):270–276.
  • Niwa K, Kazama K, Younkin SG, Carlson GA, Iadecola C. 2002. Alterations in cerebral blood flow and glucose utilisation in mice overexpressing the amyloid precursor protein. Neurobiol Dis. 9(1):61–68.
  • Ou Z, Deng L, Lu Z, Wu F, Liu W, Huang D, Peng Y. 2020. Protective effects of Akkermansia muciniphila on cognitive deficits and amyloid pathology in a mouse model of Alzheimer’s disease. Nutr Diabetes. 10(1):12.
  • Pfeifer LA, White LR, Ross GW, Petrovitch H, Launer LJ. 2002. Cerebral amyloid angiopathy and cognitive function: the HAAS autopsy study. Neurology. 58(11):1629–1634.
  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41(Database issue), 590.
  • Román GC, Jackson RE, Gadhia R, Román AN, Reis J. 2019. Mediterranean diet: the role of long-chain ω-3 fatty acids in fish; polyphenols in fruits, vegetables, cereals, coffee, tea, cacao and wine; probiotics and vitamins in prevention of stroke, age-related cognitive decline, and Alzheimer disease. Rev Neurol (Paris). 175(10):724–741.
  • Rutledge GA, Sandhu AK, Miller MG, Edirisinghe I, Burton-Freeman BB, Shukitt-Hale B. 2021. Blueberry phenolics are associated with cognitive enhancement in supplemented healthy older adults. Food Funct. 12(1):107–118.
  • Rutsch A, Kantsjö JB, Ronchi F. 2020. The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology. Front Immunol. 11:604179.
  • Saito S, Yamamoto Y, Maki T, Hattori Y, Ito H, Mizuno K, Harada-Shiba M, Kalaria RN, Fukushima M, Takahashi R, et al. 2017. Taxifolin inhibits amyloid-β oligomer formation and fully restores vascular integrity and memory in cerebral amyloid angiopathy. Acta Neuropathol Commun. 5(1):26.
  • Serrano-Pozo A, Frosch MP, Masliah E, Hyman BT. 2011. Neuropathological alterations in Alzheimer disease. Cold Spring Harb Perspect Med. 1(1):a006189.
  • Shishtar E, Rogers GT, Blumberg JB, Au R, Jacques PF. 2020. Long-term dietary flavonoid intake and risk of Alzheimer disease and related dementias in the Framingham Offspring Cohort. Am J Clin Nutr. 112(2):343–353.
  • Srivastava S, Ahmad R, Khare SK. 2021. Alzheimer’s disease and its treatment by different approaches: a review. Eur J Med Chem. 216:113320.
  • Steinman J, Sun H, Feng Z. 2020. Microvascular alterations in Alzheimer’s Disease. Front Cell Neurosci. 14:618986.
  • Sun J, Liu S, Ling Z, Wang F, Ling Y, Gong T, Fang N, Ye S, Si J, Liu J. 2019. Fructooligosaccharides ameliorating cognitive deficits and neurodegeneration in APP/PS1 transgenic mice through modulating gut microbiota. J Agric Food Chem. 67(10):3006–3017.
  • Sun J, Xu J, Yang B, Chen K, Kong Y, Fang N, Gong T, Wang F, Ling Z, Liu J. 2020. Effect of Clostridium butyricum against microglia-mediated neuroinflammation in Alzheimer’s disease via regulating gut microbiota and metabolites butyrate. Mol Nutr Food Res. 64(2):e1900636.
  • Szu JI, Obenaus A. 2021. Cerebrovascular phenotypes in mouse models of Alzheimer’s disease. J Cereb Blood Flow Metab. 41(8):1821–1841.
  • Tan L, Yang H, Pang W, Li H, Liu W, Sun S, Song N, Zhang W, Jiang Y. 2017. Investigation on the role of BDNF in the benefits of blueberry extracts for the improvement of learning and memory in Alzheimer’s disease mouse model. J Alzheimers Dis. 56(2):629–640.
  • Tsakiroglou P, VandenAkker NE, Bo’ CD, Riso P, Klimis-Zacas D. 2019. Role of berry anthocyanins and phenolic acids on cell migration and angiogenesis: an updated overview. Nutrients. 11(5):1075.
  • Vardarajan B, Kalia V, Manly J, Brickman A, Reyes Dumeyer D, Lantigua R, Ionita Laza I, Jones DP, Miller GW, Mayeux R, et al. 2020. Differences in plasma metabolites related to Alzheimer’s disease, APOE ε4 status, and ethnicity. Alzheimer’s & Dementia. Alzheimers Dement (NY). 6(1):e12025.
  • Vepsäläinen S, Koivisto H, Pekkarinen E, Mäkinen P, Dobson G, McDougall GJ, Stewart D, Haapasalo A, Karjalainen RO, Tanila H, et al. 2013. Anthocyanin-enriched bilberry and blackcurrant extracts modulate amyloid precursor protein processing and alleviate behavioral abnormalities in the APP/PS1 mouse model of Alzheimer’s disease. J Nutr Biochem. 24(1):360–370.
  • Wang Y, Lim Y, He Z, Wong W, Lai W. 2021. Dietary phytochemicals that influence gut microbiota: roles and actions as anti-Alzheimer agents. Crit Rev Food Sci Nutr. 62(19):1–27.
  • Wang F, Xu T, Zhang Y, Zheng T, He Y, He F, Jiang Y. 2020. Long-term combined administration of Bifidobacterium bifidum TMC3115 and Lactobacillus plantarum 45 alleviates spatial memory impairment and gut dysbiosis in APP/PS1 mice. FEMS Microbiology Letters. 367(7):fnaa048.
  • Wimo A, Guerchet M, Ali G, Wu Y, Prina AM, Winblad B, Jönsson L, Liu Z, Prince M. 2017. The worldwide costs of dementia 2015 and comparisons with 2010. Alzheimers Dement. 13(1):1–7.
  • Wu Q, Li Q, Zhang X, Ntim M, Wu X, Li M, Wang L, Zhao J, Li S. 2020. Treatment with Bifidobacteria can suppress Aβ accumulation and neuroinflammation in APP/PS1 mice. PeerJ. 8:e10262.
  • Xian Y, Fan R, Shao J, Mulcahy Toney A, Chung S, Ramer-Tait AE. 2021. Polyphenolic fractions isolated from red raspberry whole fruit, pulp, and seed differentially alter the gut microbiota of mice with diet-induced obesity. J Funct Foods. 76:104288.
  • Zhu G, Zhao J, Zhang H, Chen W, Wang G. 2021. Administration of Bifidobacterium breve improves the brain function of Aβ1-42-treated mice via the modulation of the gut microbiome. Nutrients. 13(5):1602.