Journal of Food Hygiene and Safety (한국식품위생안전성학회지)

The Korean Society of Food Hygiene and Safety (한국식품위생안전성학회)
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Extracellular RNAs and Extracellular Vesicles: Inception, Current Explorations, and Future Applications

  • Perumal, Ayyappasamy Sudalaiyadum (Department of Bioengineering, McGill University) ;
  • Chelliah, Ramachandran (Department of Food Science and Biotechnology, College of Agriculture and Life Science, Kangwon National University) ;
  • Datta, Saptashwa (Department of Genetic Engineering, School of Bioengineering, SRM Institute of Science and Technology) ;
  • Krishna, Jayachandran (Centre for Biotechnology, Anna University) ;
  • Samuel, Melvin S. (School of Environmental Science and Engineering, Indian Institute of Technology) ;
  • Ethiraj, Selvarajan (Department of Genetic Engineering, School of Bioengineering, SRM Institute of Science and Technology) ;
  • Park, Chae Rin (Department of Food Science and Biotechnology, College of Agriculture and Life Science, Kangwon National University)
  • Received : 2020.12.01
  • Accepted : 2020.12.14
  • Published : 2020.12.30
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Abstract

In addition to the ubiquitous roles of cellular RNA in genetic regulations, gene expression and phenotypic variations in response to environmental cues and chemotactic signals, the regulatory roles of a new type of RNA called extracellular RNAs (exRNAs) are an up-and-coming area of research interest. exRNA is transported outside the cell through membrane blebs known as membrane vesicles or extracellular vesicles (EVs). EV formation is predominant and conserved among all microbial forms, including prokaryotes, eukaryotes, and archaea. This review will focus on the three major topics concerning bacterially derived exRNAs, i.e., 1) the discovery of exRNA and influence of extraneous RNA over bacterial gene regulations, 2) the known secretion mechanism for the release of exRNA, and 3) the possible applications that can be devised with these exRNA secreted by different gram-negative and gram-positive bacteria. Further, this review will also provide an opinion on exRNA- and EV-derived applications such as the species-specific exRNA markers for diagnostics and the possible roles of exRNA in probiotics and the epigenetic regulations of the gut microbiome.

유전적 조절, 유전자 발현 그리고 환경적 단서, 화학적 신호에 대응하는 표현형 변이에서 세포 RNA는 ubiquitous 역할 이외에도 세포 외 RNA(exRNA)라 하는 새로운 형태의 RNA는 추후 연구의 방향을 제시한다. exRNA는 membrane vesicles 또는 세포 외 소포체(EV)로 알려진 membrane blebs를 통해 세포 외부로 운반된다. EV의 형성은 원핵생물, 진핵생물, 고세균을 포함한 모든 미생물군에 우세하게 보존되어있다. 본 리뷰는 세균 유래 exRNA에 관해 세가지 주제에 초점을 두었다. exRNA의 발견과 박테리아 유전자 배열에 대한 외부 RNA의 영향, b. exRNA의 분비기작을 통한 방출, c. 다른 그람음성 및 그람양성균에 의해 분비되는 exRNA로 고안될 수 있는 응용 가능분야이다. 본 리뷰에서 장내 미생물군의 probiotics 및 후성유전학적 규제에서 본 exRNA와 exRNA마커와 같은 EV파생 응용프로그램에 대한 의견을 제공할 것이다.

Keywords

References

  1. Buckingham, S.D., Esmaeili, B., Wood, M., Sattelle, D.B., RNA interference: from model organisms towards therapy for neural and neuromuscular disorders. Hum. Mol. Genet., 13(2), R275-R288 (2004). https://doi.org/10.1093/hmg/ddh224
  2. Cooper, T.A., Wan, L., Dreyfuss, G., RNA and disease. Cell, 136(4), 777-793 (2009). https://doi.org/10.1016/j.cell.2009.02.011
  3. Gottesman, S., Stealth regulation: biological circuits with small RNA switches. Genes & Dev., 16(22), 2829-2842 (2002). https://doi.org/10.1101/gad.1030302
  4. Grosshans, H., Slack, F.J., Micro-RNAs: small is plentiful. J. Cell. Biol., 156(1), 17-22 (2002). https://doi.org/10.1083/jcb.200111033
  5. Masse, E., Majdalani, N., Gottesman, S., Regulatory roles for small RNAs in bacteria. Curr. Opin. Microbiol., 6(2), 120-124 (2003). https://doi.org/10.1016/S1369-5274(03)00027-4
  6. Wassarman, K.M., Small RNAs in bacteria: diverse regulators of gene expression in response to environmental changes. Cell, 109(2), 141-144 (2002). https://doi.org/10.1016/S0092-8674(02)00717-1
  7. Paudel, D.B., Ghoshal, B., Jossey, S., Ludman, M., Fatyol, K., Sanfacon, H., Expression and antiviral function of ARGONAUTE 2 in Nicotiana benthamiana plants infected with two isolates of tomato ringspot virus with varying degrees of virulence. Virology, 524, 127-139 (2018). https://doi.org/10.1016/j.virol.2018.08.016
  8. Kim, T.K., Hemberg, M., Gray, J.M., Enhancer RNAs: a class of long noncoding RNAs synthesized at enhancers. Cold. Spring. Harb. Perspect. Biol., 7(1), a018622 (2015). https://doi.org/10.1101/cshperspect.a018622
  9. Tsatsaronis, J.A., Franch-Arroyo, S., Resch, U., Charpentier, E., Extracellular vesicle RNA: a universal mediator of microbial communication?. Trends. Microbiol., 26(5), 401-410 (2018). https://doi.org/10.1016/j.tim.2018.02.009
  10. Whitchurch, A.K., Gene expression microarrays. IEEE Potentials, 21(1), 30-34 (2002). https://doi.org/10.1109/45.985325
  11. Pinchuk, I.V., Morris, K.T., Nofchissey, R.A., Earley, R.B., Wu, J.Y., Ma, T.Y., Beswick, E.J., Stromal cells induce Th17 during Helicobacter pylori infection and in the gastric tumor microenvironment. PLoS One, 8(1), e53798 (2013). https://doi.org/10.1371/journal.pone.0053798
  12. Montanaro, L., Trere, D., Derenzini, M., The emerging role of RNA polymerase I transcription machinery in human malignancy: a clinical perspective. Oncotarget., 6, 909 (2013)
  13. Pavankumar, A.R., Ayyappasamy, S.P., Sankaran, K., Small RNA fragments in complex culture media cause alterations in protein profiles of three species of bacteria. Biotechniques, 52(3), 167-172 (2012). https://doi.org/10.2144/000113819
  14. Vlassov, V.V., Laktionov, P.P., Rykova, E.Y., Extracellular nucleic acids. Bioessays, 29(7), 654-667 (2007). https://doi.org/10.1002/bies.20604
  15. Vunjak-Novakovic, G., Altman, G., Horan, R., Kaplan, D.L., Tissue engineering of ligaments. Annu. Rev. Biomed. Eng., 6, 131-156 (2004). https://doi.org/10.1146/annurev.bioeng.6.040803.140037
  16. Eigenbrod, T., Dalpke, A.H., Bacterial RNA: an underestimated stimulus for innate immune responses. J. Immunol., 195(2), 411-418 (2015). https://doi.org/10.4049/jimmunol.1500530
  17. Vanaja, S.K., Rathinam, V.A., Atianand, M.K., Kalantari, P., Skehan, B., Fitzgerald, K.A., Leong, J.M., Bacterial RNA: DNA hybrids are activators of the NLRP3 inflammasome. Proc of the Nat. Aca. Sci., 111(21), 7765-7770 (2014). https://doi.org/10.1073/pnas.1400075111
  18. Sander, L.E., Davis, M.J., Boekschoten, M.V., Amsen, D., Dascher, C.C., Ryffel, B., ... & Blander, J.M., Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature, 474(7351), 385-389 (2011). https://doi.org/10.1038/nature10072
  19. Dorward, D.W., Garon, C.F., Judd, R.C., Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J. Bacteriol., 171(5), 2499-2505 (1989). https://doi.org/10.1128/jb.171.5.2499-2505.1989
  20. Nishimura, K., Hirokawa, Y.S., Mizutani, H., Shiraishi, T., Reduced heterochromatin protein 1-beta (HP1β) expression is correlated with increased invasive activity in human melanoma cells. Anticancer. Res., 26(6B), 4349-4356(2006).
  21. Ando, T., Screening effect and impurity scattering in monolayer graphene. J. Phys. Soc. Jpn., 75(7), 074716-074716 (2006). https://doi.org/10.1143/JPSJ.75.074716
  22. Renelli, M., Matias, V., Lo, R.Y., Beveridge, T.J., DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology, 150(7), 2161-2169 (2004). https://doi.org/10.1099/mic.0.26841-0
  23. Obregon-Henao, A., Duque-Correa, M.A., Rojas, M., Garcia, L.F., Brennan, P.J., Ortiz, B.L., Belisle, J.T., Stable extracellular RNA fragments of Mycobacterium tuberculosis induce early apoptosis in human monocytes via a caspase-8 dependent mechanism. PLoS One, 7(1), e29970 (2012). https://doi.org/10.1371/journal.pone.0029970
  24. Biller, S.J., Berube, P.M., Berta-Thompson, J.W., Kelly, L., Roggensack, S.E., Awad, L., ...& Moore, L.R., Genomes of diverse isolates of the marine cyanobacterium Prochlorococcus. Sci. Data., 1(1), 1-11. (2014)
  25. Ghosal, A., Upadhyaya, B.B., Fritz, J.V., Heintz?Buschart, A., Desai, M.S., Yusuf, D., Wilmes, P., The extracellular RNA complement of Escherichia coli. Microbiologyopen, 4(2), 252-266 (2015). https://doi.org/10.1002/mbo3.235
  26. Grohmann, E., Christie, P.J., Waksman, G., Backert, S., Type IV secretion in Gram-negative and Gram?positive bacteria. Mol. mic., 107(4), 455-471 (2018). https://doi.org/10.1111/mmi.13896
  27. Han, Y., Wang, F., Shao, L., Huang, P., Xu, Y., LncRNA TUG1 mediates lipopolysaccharide-induced proliferative inhibition and apoptosis of human periodontal ligament cells by sponging miR-132. Acta. Biochim. Biophys. Sin., 51(12), 1208-1215 (2019).
  28. Paudel, D.B., Ghoshal, B., Jossey, S., Ludman, M., Fatyol, K., Sanfacon, H., Expression and antiviral function of ARGONAUTE 2 in Nicotiana benthamiana plants infected with two isolates of tomato ringspot virus with varying degrees of virulence. Virology, 524, 127-139. (2018) https://doi.org/10.1016/j.virol.2018.08.016
  29. Habier, J., May, P., Heintz-Buschart, A., Ghosal, A., Wienecke-Baldacchino, A.K., Nolte, E.N., Paul, W., Fritz, J.V., 2018. Extraction and analysis of RNA isolated from pure bacteria-derived outer membrane vesicles. In Bacterial Regulatory RNA. Humana Press, New York, NY, USA, pp. 213-230.
  30. Yu, J., Xu, Q.G., Wang, Z.G., Yang, Y., Zhang, L., Ma, J.Z., Sun, S.H., Yang, F., Zhou, W.P. Circular RNA cSMARCA5 inhibits growth and metastasis in hepatocellular carcinoma. J. of hep., 68(6), 1214-1227 (2018). https://doi.org/10.1016/j.jhep.2018.01.012
  31. Kuehn, M.J., Kesty, N.C., Bacterial outer membrane vesicles and the host-pathogen interaction. Genes. Dev., 19(22), 2645-2655 (2005). https://doi.org/10.1101/gad.1299905
  32. Dubnau, D., DNA uptake in bacteria. Annu. Rev. Microbiol., 53(1), 217-244 (1999). https://doi.org/10.1146/annurev.micro.53.1.217
  33. Nayak, M., Perumal, A.S., Nicolau, D.V., van Delft, F.C., Bacterial motility behaviour in sub-ten micron wide geometries. In 2018 16th IEEE International New Circuits and Systems Conference (NEWCAS) (pp. 382-384) (2018).
  34. Holmqvist, E., Vogel, J., RNA-binding proteins in bacteria. Nat. Rev. Microbio., 16, 601-615 https://doi.org/10.1038/s41579-018-0049-5 (2018).
  35. Kuipers, M.E., Hokke, C.H., Smits, H.H., Pathogen-derived extracellular vesicle-associated molecules that affect the host immune system: an overview. Front. Microbiol., 9, 2182 (2018). https://doi.org/10.3389/fmicb.2018.02182
  36. Mug-Opstelten, D., Witholt, B., Preferential release of new outer membrane fragments by exponentially growing Escherichia coli. Biochimica et Biophysica Acta (BBA)-Biomembranes, 508(2), 287-295 (1978). https://doi.org/10.1016/0005-2736(78)90331-0
  37. Yaganza, E.S., Rioux, D., Simard, M., Arul, J., Tweddell, R.J., Ultrastructural alterations of Erwinia carotovora subsp. atroseptica caused by treatment with aluminum chloride and sodium metabisulfite. J. Appl. Environ., 70(11), 6800-6808 (2004). https://doi.org/10.1128/AEM.70.11.6800-6808.2004
  38. Zhou, K., Doyle, J.C., Essentials of robust control (104). Upper Saddle River, NJ: Prentice hall (1998).
  39. Hoekstra, D., van der Laan, J.W., de Leij, L., Witholt, B., Release of outer membrane fragments from normally growing Escherichia coli. Biochim. Biophys. Acta. (BBA)-Biomembr., 455(3), 889-899 (1976). https://doi.org/10.1016/0005-2736(76)90058-4
  40. Gamazo, C., Moriyon, I., Release of outer membrane fragments by exponentially growing Brucella melitensis cells. Infect. Immun., 55(3), 609-615 (1987). https://doi.org/10.1128/IAI.55.3.609-615.1987
  41. Horstman, A.L., Kuehn, M.J., Bacterial surface association of heat-labile enterotoxin through lipopolysaccharide after secretion via the general secretory pathway. J. Biol. Chem., 277(36), 32538-32545 (2002). https://doi.org/10.1074/jbc.M203740200
  42. Dorward, D.W., Garon, C.F., Judd, R.C., Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J. Bacteriol., 171(5), 2499-2505 (1989). https://doi.org/10.1128/jb.171.5.2499-2505.1989
  43. Kolling, G.L., Matthews, K.R., Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli O157: H7. Appl. Environ. Microbiol., 65(5), 1843-1848 (1999). https://doi.org/10.1128/aem.65.5.1843-1848.1999
  44. Yaron, S., Kolling, G.L., Simon, L., Matthews, K.R., VesicleMediated Transfer of Virulence Genes fromEscherichia coli O157: H7 to Other Enteric Bacteria. Appl. Environ. Micro-biol., 66(10), 4414-4420 (2000). https://doi.org/10.1128/AEM.66.10.4414-4420.2000
  45. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M. Lee, J.J., Lotvall, J.O., Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell. Biol., 9, 654-659 (2007). https://doi.org/10.1038/ncb1596
  46. MacDonald, I.A., Kuehn, M.J., Offense and defense: microbial membrane vesicles play both ways. Res in microbial., 163(9-10), 607-618 (2012). https://doi.org/10.1016/j.resmic.2012.10.020
  47. Choi, J.W., Kim, S.C., Hong, S.H., Lee, H.J., Secretable small RNAs via outer membrane vesicles in periodontal pathogens. J. Dent. Res., 96(4), 458-466 (2017). https://doi.org/10.1177/0022034516685071
  48. Peng, L.H., Wang, M.Z., Chu, Y., Zhang, L., Niu, J., Shao, H.T., Yuan, T.J., Jiang, Z.H., Gao, J.Q., Ning, X.H., Engineering bacterial outer membrane vesicles as transdermal nanoplatforms for photo-TRAIL-programmed therapy against melanoma. Science advances, 6(27), eaba2735 (2020). https://doi.org/10.1126/sciadv.aba2735
  49. Hampton, T.H., Koeppen, K., Bashor, L., Stanton, B.A., Selection of Reference Genes for Quantitative PCR: Identifying Reference Genes for Airway Epithelial Cells Exposed to Pseudomonas aeruginosa. Am. J. Physiol. Lung. Cell. Mol. Physiol., 319(2), L256-L265 (2020). https://doi.org/10.1152/ajplung.00158.2020
  50. Yau, W.L., Lambertz, U., Colineau, L., Pescher, P., MacDonald, A., Zander, D., Retzlaff, S., Eick, J., Reiner, N., Clos, J., Spath, G.F., Phenotypic characterization of a Leishmania donovani cyclophilin 40 null mutant. J. Eukaryot Microbiol., 63(6), 823-833 (2016). https://doi.org/10.1111/jeu.12329
  51. Yue, Y., Liu, X., Xu, M., Ren, D., Liu, Q., Epidemiological dynamics of dengue fever in mainland China, 2014-2018. Int. J. Infect. Dis., 86, 82-93 (2019). https://doi.org/10.1016/j.ijid.2019.06.015
  52. Lenz, D.H., Mok, K.C., Lilley, B.N., Kulkarni, R.V., Wingreen, N.S., Bassler, B.L., The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell, 118(1), 69-82 (2004). https://doi.org/10.1016/j.cell.2004.06.009
  53. Storz, G., Vogel, J., Wassarman, K.M., Regulation by small RNAs in bacteria: expanding frontiers. Molecular cell, 43(6), 880-891 (2011). https://doi.org/10.1016/j.molcel.2011.08.022
  54. Gelsinger, D.R., Uritskiy, G., Reddy, R., Munn, A., Farney, K., DiRuggiero, J. Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community. Msystems, 5(1) (2020).
  55. MacDonald, I.A., Kuehn, M.J., Offense and defense: microbial membrane vesicles play both ways. Res. Microbiol., 163(9-10), 607-618 (2012). https://doi.org/10.1016/j.resmic.2012.10.020
  56. Begic, M., Josic, D., Biofilm formation and extracellular microvesicles-The way of foodborne pathogens toward resistance. Electrophoresis, 41(20), 1718-1739 (2020). https://doi.org/10.1002/elps.202000106
  57. Lee, H.J., Microbe-Host Communication by Small RNAs in Extracellular Vesicles: Vehicles for Transkingdom RNA Transportation. Int. J. Mol. Sci, 20(6), 1487. https://doi.org/10.3390/ijms20061487 (2019).
  58. Novakovic, S., Hocevar, M., Zgajnar, J., Besic, N., Stegel, V., Detection of telomerase RNA in the plasma of patients with breast cancer, malignant melanoma or thyroid cancer. Oncology reports, 11(1), 245-252 (2004).
  59. Liu, J., Perumal, A.S., Doucet, F.R., Rifai, K., Ozcan, L. Kheireddine, S., Wachsmann-Hogiu, S., A flexible and portable nanocomposite-based substrate for electrochemical biosensing (Conference Presentation). Nanoscale Imaging, Sensing, and Actuation for Biomedical Applications XVI 10891, 108910E (2019).
  60. Liu, J., Moakhar, R.S., Perumal, A.S., Roman, H.N., Mahshid, S., Wachsmann-Hogiu, S., An AgNP-deposited commercial electrochemistry test strip as a platform for urea detection. Scientific Reports, 10(1), 1-11 (2020). https://doi.org/10.1038/s41598-019-56847-4
  61. Zhao, X., Li, M., Liu, Y., Microfluidic-Based Approaches for Foodborne Pathogen Detection. Microorganisms, 7(10), 381 (2019). https://doi.org/10.3390/microorganisms7100381