Dietary impact of a plant-derived microRNA on the gut microbiome

ExRNA - Tập 2 - Trang 1-11 - 2020
Jennifer K. Spinler1,2, Numan Oezguen1,2, Jessica K. Runge1,2, Ruth Ann Luna1,2, Vivekanudeep Karri3, Jian Yang4, Kendal D. Hirschi4
1Texas Children’s Microbiome Center, Department of Pathology, Texas Children’s Hospital, Houston, USA
2Department of Pathology & Immunology, Baylor College of Medicine, Houston, USA
3Rice University, Houston, USA
4Pediatrics-Nutrition, Children’s Nutrition Research, Baylor College of Medicine, Houston, USA

Tóm tắt

Global estimations of 4 billion people living on plant-based diets signify tremendous diversity in plant consumption and their assorted miRNAs, which presents a challenging model to experimentally address how plant-based miRNAs impact the microbiome. Here we establish baseline gut microbiome composition for a mouse model deficient in the specific mammalian miR-146a shown to alter gut microbiomes. We then asses the effect on the gut microbiome when miR-146a-deficient mice are fed a transgenic plant-based diet expressing the murine-derived miR-146a. Mice deficient in miR-146a were maintained either on a baseline diet until 7 weeks of age (day 0) and then fed either vector or miR-146a-expressing plant-based diets for 21 days. The gut microbiomes of mice were examined by comparing the V4 region of 16S rRNA gene sequences of DNA isolated from fecal samples at days 0 (baseline diet) and 21 (vector or miR-146a expressing plant-based diets). Beta-diversity analysis demonstrated that the transition from baseline chow to a plant-based diet resulted in significant longitudinal shifts in microbial community structure attributable to increased fiber intake. Bipartite network analysis suggests that miR-146a-deficient mice fed a plant diet rich in miR-146a have a microbiome population modestly different than mice fed an isogenic control plant diet deficient in miR-146a. A mouse diet composed of a transgenic plant expressing a mouse miR-146a may fine tune microbial communities but does not appear to have global effects on microbiome structure and composition.

Tài liệu tham khảo

Derrien M, Veiga P. Rethinking diet to aid human-microbe symbiosis. Trends Microbiol. 2017;25(2):100–12. Wong MW, Yi CH, Liu TT, Lei WY, Hung JS, Lin CL, et al. Impact of vegan diets on gut microbiota: an update on the clinical implications. Ci Ji Yi Xue Za Zhi. 2018;30(4):200–3. Witwer KW, et al. F1000Res. 2018;7:244. Knudsen I, Poulsen M. Comparative safety testing of genetically modified foods in a 90-day rat feeding study design allowing the distinction between primary and secondary effects of the new genetic event. Regul Toxicol Pharmacol. 2007;49(1):53–62. Petrick JS, Brower-Toland B, Jackson AL, Kier LD. Safety assessment of food and feed from biotechnology-derived crops employing RNA-mediated gene regulation to achieve desired traits: a scientific review. Regul Toxicol Pharmacol. 2013;66(2):167–76. Petrick JS, Moore WM, Heydens WF, Koch MS, Sherman JH, Lemke SL. A 28-day oral toxicity evaluation of small interfering RNAs and a long double-stranded RNA targeting vacuolar ATPase in mice. Regul Toxicol Pharmacol. 2015;71(1):8–23. Snow JW, Hale AE, Isaacs SK, Baggish AL, Chan SY. Ineffective delivery of diet-derived microRNAs to recipient animal organisms. RNA Biol. 2013;10(7):1107–16. Dickinson B, Zhang Y, Petrick JS, Heck G, Ivashuta S, Marshall WS. Lack of detectable oral bioavailability of plant microRNAs after feeding in mice. Nat Biotechnol. 2013;31(11):965–7. Teng Y, Ren Y, Sayed M, Hu X, Lei C, Kumar A, et al. Plant-derived Exosomal MicroRNAs shape the gut Micobiota. Cell Host Microbe. 2018;24:1–16. Liu S, da Cunha AP, Rezende RM, Cialic R, Wei Z, Bry L, et al. The host shapes the gut microbiota via fecal MicroRNA. Cell Host Microbe. 2016;19(1):32–43. Kane AV, Dinh DM, Ward HD. Childhood malnutrition and the intestinal microbiome. Pediatr Res. 2015;77(1–2):256–62. Thaxton GE, Melby PC, Manary MJ, Preidis GA. New insights into the pathogenesis and treatment of malnutrition. Gastroenterol Clin N Am. 2018;47(4):813–27. Tomova A, Bukovsky I, Rembert E, Yonas W, Alwarith J, Barnard ND, et al. The effects of vegetarian and vegan diets on gut microbiota. Front Nutr. 2019;6:47. Teng Y, Ren Y, Sayed M, Hu X, Lei C, Kumar A, et al. Plant-derived exosomal MicroRNAs shape the gut microbiota. Cell Host Microbe. 2018;24(5):637–52 e8. Runtsch MC, Hu R, Alexander M, Wallace J, Kagele D, Petersen C, et al. MicroRNA-146a constrains multiple parameters of intestinal immunity and increases susceptibility to DSS colitis. Oncotarget. 2015;6(30):28556–72. Rusca N, Monticelli S. MiR-146a in immunity and disease. Mol Biol Int. 2011;2011:437301. Sun T, Li X, Song H, Gao F, Zhou G, Li X, et al. MiR-146a aggravates LPS-induced inflammatory injury by targeting CXCR4 in the articular chondrocytes. Cell Physiol Biochem. 2017;44(4):1282–94. Du CT, Gao W, Ma K, Yu SX, Li N, Yan SQ, et al. MicroRNA-146a deficiency protects against Listeria monocytogenes infection by modulating the gut microbiota. Int J Mol Sci. 2018;19(4):993. Kakeshpour T, Tamang TM, Park WD, Manohar M, Yang J, Hirschi KD, et al. Expression of mouse small interfering RNAs in lettuce using artificial microRNA technology. Biotechniques. 2020;68(4):214–8. Giles K, Guan C, Jagoe TR, Mazurak V. Diet composition as a source of variation in experimental animal models of cancer cachexia. J Cachexia Sarcopenia Muscle. 2016;7(2):110–25. Riffo-Campos AL, Riquelme I, Brebi-Mieville P. Tools for sequence-based miRNA target prediction: what to choose? Int J Mol Sci. 2016;17(12):1987. Mullany LE, Wolff RK, Slattery ML. Effectiveness and usability of bioinformatics tools to analyze pathways associated with miRNA expression. Cancer Informat. 2015;14:121–30. Yang J, Primo C, Elbaz-Younes I, Hirschi KD. Bioavailability of transgenic microRNAs in genetically modified plants. Genes Nutr. 2017;12:17. Yang J, Elbaz-Younes I, Primo C, Murungi D, Hirschi KD. Intestinal permeability, digestive stability and oral bioavailability of dietary small RNAs. Sci Rep. 2018;8(1):10253. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107(33):14691–6. Baldrich P, Rutter BD, Karimi HZ, Podicheti R, Meyers BC, Innes RW. Plant extracellular vesicles contain diverse small RNA species and are enriched in 10- to 17-nucleotide “tiny” RNAs. Plant Cell. 2019;31(2):315–24. Yang J, Kongchan N, Primo Planta C, Neilson JR, Hirschi KD. The atypical genesis and bioavailability of the plant-based small RNA MIR2911: bulking up while breaking down. Mol Nutr Food Res. 2017;61(9):10.1002/mnfr.201600974. Yang J, Hotz T, Broadnax L, Yarmarkovich M, Elbaz-Younes I, Hirschi KD. Anomalous uptake and circulatory characteristics of the plant-based small RNA MIR2911. Sci Rep. 2016;6(26834):1–9. Matijasic BB, Obermajer T, Lipoglavsek L, Grabnar I, Avgustin G, Rogelj I. Association of dietary type with fecal microbiota in vegetarians and omnivores in Slovenia. Eur J Nutr. 2014;53(4):1051–64. Perge P, Nagy Z, Decmann A, Igaz I, Igaz P. Potential relevance of microRNAs in inter-species epigenetic communication, and implications for disease pathogenesis. RNA Biol. 2016;14:391–401 Epub Ahead of Print (12–08-16), LK:1–11. Title AC, Denzler R, Stoffel M. Uptake and function studies of maternal milk-derived MicroRNAs. J Biol Chem. 2015;290(39):23680–91. Zempleni J, Baier SR, Hirschi KD. Diet-responsive MicroRNAs are likely exogenous. J Biol Chem. 2015;290(41):25197. Youngblut ND, Reischer GH, Walters W, Schuster N, Walzer C, Stalder G, et al. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat Commun. 2019;10(1):2200. Hills RD Jr, Pontefract BA, Mishcon HR, Black CA, Sutton SC, Theberge CR. Gut microbiome: profound implications for diet and disease. Nutrients. 2019;11(7):1613. Chan SY, Snow JW. Formidable challenges to the notion of biologically important roles for dietary small RNAs in ingesting mammals. Genes Nutr. 2017;12:13. Rutter BD, Innes RW. Extracellular vesicles as key mediators of plant-microbe interactions. Curr Opin Plant Biol. 2018;44:16–22. Zhang X, Yuan YR, Pei Y, Lin SS, Tuschl T, Patel DJ, et al. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 2006;20(23):3255–68. Tsuzuki M, Takeda A, Watanabe Y. Recovery of dicer-like 1-late flowering phenotype by miR172 expressed by the noncanonical DCL4-dependent biogenesis pathway. RNA. 2014;20(8):1320–7. Chen X, Liang H, Guan D, Wang C, Hu X, Cui L, et al. A combination of let-7d, let-7g and let-7i serves as a stable reference for normalization of serum microRNAs. PLoS One. 2013;8(11):e79652. Bertolet G, Kongchan N, Miller R, Patel RK, Jain A, Choi JM, et al. MiR-146a wild-type 3′ sequence identity is dispensable for proper innate immune function in vivo. Life Sci Alliance. 2019;2(1):e201800249. Yang J, Farmer LM, Agyekum AA, Elbaz-Younes I, Hirschi KD. Detection of an abundant plant-based small RNA in healthy consumers. PLoS One. 2015;10(9):e0137516. Yang J, Farmer LM, Agyekum AA, Hirschi KD. Detection of dietary plant-based small RNAs in animals. Cell Res. 2015;25(4):517–20. Aagaard K, Petrosino J, Keitel W, Watson M, Katancik J, Garcia N, et al. The human microbiome project strategy for comprehensive sampling of the human microbiome and why it matters. FASEB J. 2013;27(3):1012–22. Hildebrand F, Tadeo R, Voigt AY, Bork P, Raes J. LotuS: an efficient and user-friendly OTU processing pipeline. Microbiome. 2014;2(1):30. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10(10):996–8. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(Database issue):D590–6. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75(23):7537–41. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498–504.