Bioavailability of transgenic microRNAs in genetically modified plants

Genes and Nutrition

Volumn 12, Issue 1, 2017, Pages

  Yang, Jian ^a   Primo, Cecilia ^a   Elbaz Younes, Ismail ^a   Hirschi, Kendal D ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Bioavailability; Dietary microRNAs; Digestive stability; Genetically modified organisms; Mice; MIR2911

Indexed keywords

MICRORNA;

ANIMAL EXPERIMENT; ARABIDOPSIS; ARTICLE; BIOAVAILABILITY; CONTROLLED STUDY; FOOD INTAKE; GENE TARGETING; GENETIC ENGINEERING; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PILOT STUDY; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA DEGRADATION; RNA STABILITY; SMALL INTESTINE; TRANSGENIC PLANT;

EID: 85029845312     PISSN: 15558932     EISSN: 18653499     Source Type: Journal    
DOI: 10.1186/s12263-017-0563-5     Document Type: Article

References (46)

1. James C. A global overview of biotech (GM) crops: adoption, impact and future prospects. GM Crops. 2010;1:8-12.
2. Sakakibara K, Saito K. Review: genetically modified plants for the promotion of human health. Biotechnol Lett. 2006;28:1983-91.
3. Gartland KMA, Bruschi F, Dundar M, Gahan PB, et al. Progress towards the ‘Golden Age’ of biotechnology. Curr Opin Biotechnol. 2013;24 Suppl 1:S6-13.
4. Kuiper HA, Kleter GA, Noteborn HP, Kok EJ. Assessment of the food safety issues related to genetically modified foods. Plant J. 2001;27:503-28.
5. Varzakas TH, Chryssochoidis G, Argyropoulos D. Approaches in the risk assessment of genetically modified foods by the Hellenic Food Safety Authority. Food Chem Toxicol. 2007;45:530-42.
6. Ramon M, Devos Y, Lanzoni A, Liu Y, et al. RNAi-based GM plants: food for thought for risk assessors. Plant Biotechnol J. 2014;12:1271-3.
7. Levine E, Zhang Z, Kuhlman T, Hwa T. Quantitative characteristics of gene regulation by small RNA. PLoS Biol. 2007;5:e229.
8. Dickinson B, Zhang Y, Petrick JS, Heck G, et al. Lack of detectable oral bioavailability of plant microRNAs after feeding in mice. Nat Biotechnol. 2013;31:965-7.
9. Witwer KW, McAlexander MA, Queen SE, Adams RJ. Real-time quantitative PCR and droplet digital PCR for plant miRNAs in mammalian blood provide little evidence for general uptake of dietary miRNAs: limited evidence for general uptake of dietary plant xenomiRs. RNA Biol. 2013;10:1080-6.
10. 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;66:167-76.
11. Petrick JS, Moore WM, Heydens WF, Koch MS, Sherman JH. 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;71:8-23.
12. 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;49:53-62.
13. Snow JW, Hale AE, Isaacs SK, Baggish AL, Chan SY. Ineffective delivery of diet-derived microRNAs to recipient animal organisms. RNA Biol. 2013;10:1107-16.
14. Yang J, Farmer LM, Agyekum AAA, Elbaz-Younes I, Hirschi KD. Detection of an abundant plant-based small RNA in healthy consumers. PLoS One. 2015;10:e0137516. p. 0137511-0137514.
15. Chin AR, Fong MY, Somlo G, Wu J, et al. Cross-kingdom inhibition of breast cancer growth by plant miR159. Cell Res. 2016;20(2):217-28.
16. Zhou Z, Li X, Liu J, Dong L, et al. Honeysuckle-encoded atypical microRNA2911 directly targets influenza A viruses. Cell Res. 2015;25:39-49.
17. Zhang L, Hou D, Chen X, Li D, et al. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res. 2012;22:107-26.
18. Zempleni J, Baier SR, Hirschi KD. Diet-responsive MicroRNAs are likely exogenous. J Biol Chem. 2015;290:25197.
19. Baier SR, Nguyen C, Xie F, Wood JR, Zempleni J. MicroRNAs are absorbed in biologically meaningful amounts from nutritionally relevant doses of cow milk and affect gene expression in peripheral blood mononuclear cells, HEK-293 kidney cell cultures, and mouse livers. J Nutr. 2014;144:1495-500.
20. Witwer KW, Hirschi KD. Transfer and functional consequences of dietary microRNAs in vertebrates: concepts in search of corroboration: negative results challenge the hypothesis that dietary xenomiRs cross the gut and regulate genes in ingesting vertebrates, but important questions persist. Bioessays. 2014;36:394-406.
21. Yang J, Hirschi KD, Farmer LM. Dietary RNAs: new stories regarding oral delivery. Nutrients. 2015;7:3184-99.
22. Mlotshwa S, Pruss GJ, MacArthur JL, Endres MW, et al. A novel chemopreventive strategy based on therapeutic microRNAs produced in plants. Cell Res. 2015;25:521-4.
23. Pastrello C, Tsay M, McQuaid R, Abovsky M, et al. Circulating plant miRNAs can regulate human gene expression in vitro. Sci Rep. 2016;6:32773.
24. Witwer KW. Diet-responsive mammalian miRNAs are likely endogenous. J Nutr. 2014;144:1880-1.
25. Bagci C, Allmer J. One step forward, two steps back; xeno-microRNAs reported in breast milk are artifacts. PLoS One. 2016;11:e0145065.
26. Auerbach A, Vyas G, Li A, Halushka M, Witwer K. Uptake of dietary milk miRNAs by adult humans: a validation study. F1000Res. 2016;5:721.
27. Yang J, Hotz T, Broadnax L, Yarmarkovich M, et al. Anomalous uptake and circulatory characteristics of the plant-based small RNA MIR2911. Sci Rep. 2016;6:1-9.
28. Yang J, Farmer LM, Agyekum AAA, Hirschi KD. Detection of dietary plant-based small RNAs in animals. Cell Res. 2015;25:517-20.
29. Zhang X, Yuan YR, Pei Y, Lin SS, et al. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 2006;20:3255-68.
30. 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;20:1320-7.
31. Yang et al. Mol Nutr Food Res. http://onlinelibrary.wiley.com/doi/10.1002/mnfr.201600974/abstract;jsessionid=123206D8B1EA5E15E9516E804C2927AC.f04t04.
32. Chen X, Liang H, Guan D, Wang C, 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:e79652.
33. Philip A, Ferro VA, Tate RJ. Determination of the potential bioavailability of plant microRNAs using a simulated human digestion process. Mol Nutr Food Res. 2015;59:1962-72.
34. Minekus M, Alminger M, Alvito P, Ballance S, et al. A standardised static in vitro digestion method suitable for food-an international consensus. Food Funct. 2014;5:1113-24.
35. Huala E, Dickerman AW, Garcia-Hernandez M, Weems D, et al. The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucleic Acids Res. 2001;29:102-5.
36. Dai Y, Jia P, Fang Y, Liu H, et al. miR-146a is essential for lipopolysaccharide (LPS)-induced cross-tolerance against kidney ischemia/reperfusion injury in mice. Sci Rep. 2016;6:1-12.
37. Mu J, Zhuang X, Wang Q, Jiang H, et al. Interspecies communication between plant and mouse gut host cells through edible plant derived exosome-like nanoparticles. Mol Nutr Food Res. 2014;58:1561-73.
38. Krehl WA. Factors affecting utilization and requirements. Vitamins and minerals. Am J Clin Nutr. 1962;11:389-99.
39. Hotz C, Gibson RS. Traditional food-processing and preparation practices to enhance the bioavailability of micronutrients in plant-based diets. J Nutr. 2007;137:1097-100.
40. Schiborr C, Kocher A, Behnam D, Jandasek J, et al. The oral bioavailability of curcumin from micronized powder and liquid micelles is significantly increased in healthy humans and differs between sexes. Mol Nutr Food Res. 2014;58:516-27.
41. Bryniarski K, Ptak W, Martin E, Nazimek K, et al. Free extracellular miRNA functionally targets cells by transfecting exosomes from their companion cells. PLoS One. 2015;10:1-22.
42. Fabbri M, Paone A, Calore F, Galli R, et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci U S A. 2012;109:E2110-6.
43. Galli R, Paone A, Fabbri M, Zanesi N, et al. Toll-like receptor 3 (TLR3) activation induces microRNA-dependent reexpression of functional RARβ and tumor regression. Proc Natl Acad Sci U S A. 2013;110:9812-7.
44. Cavalieri D, Rizzetto L, Tocci N, Rivero D, et al. Plant microRNAs as novel immunomodulatory agents. Sci Rep. 2016;6:25761.
45. Title AC, Denzler R, Stoffel M. Uptake and function studies of maternal milk-derived microRNAs. J Biol Chem. 2015;290:23680-91.
46. Chan SY, Snow JW. Uptake and impact of natural diet-derived small RNA in invertebrates: implications for ecology and agriculture. RNA Biol. 2016;14(4):402-14.