Burkholderia pseudomallei survival in lung epithelial cells benefits from miRNA-mediated suppression of ATG10

Autophagy

Volumn 11, Issue 8, 2015, Pages 1293-1307

  Li, Qian ^a   Fang, Yao ^a   Zhu, Pan ^a   Ren, Chun Yan ^a   Chen, Hai ^b   Gu, Jiang ^a   Jia, Yin Ping ^a   Wang, Kun ^a   Tong, Wen de ^a   Zhang, Wei jun ^a   Pan, Jing ^a   Lu, Dong shui ^a   Tang, Bin ^a,c   Mao, Xu hu ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b Respiratory Department   (China)

^c Emei Sanatorium of Chengdu Military Region ^*  (China)

Author keywords

ATG10; Autophagy; Burkholderia pseudomallei; DNA methylation; MIR4458; MIR4667 5p; MIR4668 5p

Indexed keywords

ATG10 PROTEIN; MICRORNA; PROTEIN; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; ATG10 PROTEIN, HUMAN; AUTOPHAGY RELATED PROTEIN; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; MIRN-4458 MICRORNA, HUMAN; MIRN4667 MICRORNA, HUMAN; MIRN4668 MICRORNA, HUMAN; VESICULAR TRANSPORT PROTEIN;

3' UNTRANSLATED REGION; ARTICLE; AUTOPHAGY; BACTERIAL SURVIVAL; BURKHOLDERIA PSEUDOMALLEI; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM; MELIOIDOSIS; METHYLATION; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; SURVIVAL RATE; UPREGULATION; CELL LINE; CELL SURVIVAL; CONFOCAL MICROSCOPY; CYTOLOGY; DNA METHYLATION; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; LUNG; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PATHOLOGY; PLASMID; TRANSMISSION ELECTRON MICROSCOPY; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; AUTOPHAGY-RELATED PROTEINS; BASE SEQUENCE; BURKHOLDERIA PSEUDOMALLEI; CELL LINE; CELL LINE, TUMOR; CELL SURVIVAL; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HUMANS; LUNG; MICRORNAS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMIDS; PROMOTER REGIONS, GENETIC; UP-REGULATION; VESICULAR TRANSPORT PROTEINS;

EID: 84943801536     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1058474     Document Type: Article

References (39)

1. Wiersinga WJ, Currie BJ, Peacock SJ. Melioidosis. N Engl J Med 2012; 367: 1035-44; PMID: 22970946; http://dx. doi. org/10. 1056/NEJMra1204699.
2. Cheng AC, Currie BJ. Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 2005; 18: 383-416; PMID: 15831829; http://dx. doi. org/10. 1128/CMR. 18. 2. 383-416. 2005.
3. Currie BJ, Dance DA, Cheng AC. The global distribution of Burkholderia pseudomallei and melioidosis: an update. Trans R Soc Trop Med Hyg 2008; 102 1: S1-4; PMID: 19121666; http://dx. doi. org/10. 1016/S0035-9203(08)70002-6.
4. Jones AL, Beveridge TJ, Woods DE. Intracellular survival of Burkholderia pseudomallei. Infect Immun 1996; 64: 782-90; PMID: 8641782.
5. Allwood EM, Devenish RJ, Prescott M, Adler B, Boyce JD. Strategies for intracellular survival of burkholderia pseudomallei. Front Microbiol 2011; 2: 170; PMID: 22007185; http://dx. doi. org/10. 3389/fmicb. 2011. 00170.
6. Baxt LA, Garza-Mayers AC, Goldberg MB. Bacterial subversion of host innate immune pathways. Science 2013; 340: 697-701; PMID: 23661751; http://dx. doi. org/10. 1126/science. 1235771.
7. Deretic V. Autophagy in immunity and cell-autonomous defense against intracellular microbes. Immunol Rev 2011; 240: 92-104; PMID: 21349088; http://dx. doi. org/10. 1111/j. 1600-065X. 2010. 00995. x.
8. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C. Escape of intracellular shigella from autophagy. Science 2005; 307: 727-31; PMID: 15576571; http://dx. doi. org/10. 1126/science. 1106036.
9. McGourty K, Thurston TL, Matthews SA, Pinaud L, Mota LJ, Holden DW. Salmonella inhibits retrograde trafficking of mannose-6-phosphate receptors and lysosome function. Science 2012; 338: 963-7; PMID: 23162002; http://dx. doi. org/10. 1126/science. 1227037.
10. Shin DM, Jeon BY, Lee HM, Jin HS, Yuk JM, Song CH, Lee SH, Lee ZW, Cho SN, Kim JM, et al. Mycobacterium tuberculosis eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog 2010; 6: e1001230; PMID: 21187903; http://dx. doi. org/10. 1371/journal. ppat. 1001230.
11. Beale R, Wise H, Stuart A, Ravenhill BJ, Digard P, Randow F. A LC3-interacting motif in the influenza A virus M2 protein is required to subvert autophagy and maintain virion stability. Cell Host Microbe 2014; 15: 239-47; PMID: 24528869; http://dx. doi. org/10. 1016/j. chom. 2014. 01. 006.
12. Cullinane M, Gong L, Li X, Lazar-Adler N, Tra T, Wolvetang E, Prescott M, Boyce JD, Devenish RJ, Adler B. Stimulation of autophagy suppresses the intracellular survival of Burkholderia pseudomallei in mammalian cell lines. Autophagy 2008; 4: 744-53; PMID: 18483470; http://dx. doi. org/10. 4161/auto. 6246.
13. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-97; PMID: 14744438; http://dx. doi. org/10. 1016/S0092-8674(04)00045-5.
14. Nguyen HT, Dalmasso G, Muller S, Carriere J, Seibold F, Darfeuille-Michaud A. Crohn's disease-associated adherent invasive Escherichia coli modulate levels of microRNAs in intestinal epithelial cells to reduce autophagy. Gastroenterology 2014; 146: 508-19; PMID: 24148619; http://dx. doi. org/10. 1053/j. gastro. 2013. 10. 021.
15. Lu C, Chen J, Xu HG, Zhou X, He Q, Li YL, Jiang G, Shan Y, Xue B, Zhao RX, et al. MIR106B and MIR93 prevent removal of bacteria from epithelial cells by disrupting ATG16L1-mediated autophagy. Gastroenterology 2014; 146: 188-99; PMID: 24036151; http://dx. doi. org/10. 1053/j. gastro. 2013. 09. 006.
16. Tang B, Li N, Gu J, Zhuang Y, Li Q, Wang HG, Fang Y, Yu B, Zhang JY, Xie QH, et al. Compromised autophagy by MIR30B benefits the intracellular survival of Helicobacter pylori. Autophagy 2012; 8: 1045-57; PMID: 22647547; http://dx. doi. org/10. 4161/auto. 20159.
17. Zheng K, Chen DS, Wu YQ, Xu XJ, Zhang H, Chen CF, Chen HC, Liu ZF. MicroRNA expression profile in RAW264. 7 cells in response to Brucella melitensis infection. Int J Biol Sci 2012; 8: 1013-22; PMID: 22904669; http://dx. doi. org/10. 7150/ijbs. 3836.
18. Kespichayawattana W, Rattanachetkul S, Wanun T, Utaisincharoen P, Sirisinha S. Burkholderia pseudomallei induces cell fusion and actin-associated membrane protrusion: a possible mechanism for cell-to-cell spreading. Infect Immun 2000; 68: 5377-84; PMID: 10948167; http://dx. doi. org/10. 1128/IAI. 68. 9. 5377-5384. 2000.
19. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544; PMID: 22966490; http://dx. doi. org/10. 4161/auto. 19496.
20. Kangaspeska S, Stride B, Metivier R, Polycarpou-Schwarz M, Ibberson D, Carmouche RP, Benes V, Gannon F, Reid G. Transient cyclical methylation of promoter DNA. Nature 2008; 452: 112-5; PMID: 18322535; http://dx. doi. org/10. 1038/nature06640.
21. Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, Carmouche RP, Ibberson D, Barath P, Demay F, Reid G, et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008; 452: 45-50; PMID: 18322525; http://dx. doi. org/10. 1038/nature06544.
22. Gong L, Cullinane M, Treerat P, Ramm G, Prescott M, Adler B, Boyce JD, Devenish RJ. The Burkholderia pseudomallei type III secretion system and BopA are required for evasion of LC3-associated phagocytosis. PLoS One 2011; 6: e17852; PMID: 21412437; http://dx. doi. org/10. 1371/journal. pone. 0017852.
23. Xu J, Wang Y, Tan X, Jing H. MicroRNAs in autophagy and their emerging roles in crosstalk with apoptosis. Autophagy 2012; 8: 873-82; PMID: 22441107; http://dx. doi. org/10. 4161/auto. 19629.
24. Zhai H, Fesler A, Ju J. MicroRNA: a third dimension in autophagy. Cell Cycle 2013; 12: 246-50; PMID: 23255136; http://dx. doi. org/10. 4161/cc. 23273.
25. Wang J, Yang K, Zhou L, Minhaowu, Wu Y, Zhu M, Lai X, Chen T, Feng L, Li M, et al. MicroRNA-155 promotes autophagy to eliminate intracellular mycobacteria by targeting Rheb. PLoS Pathog 2013; 9: e1003697; PMID: 24130493; http://dx. doi. org/10. 1371/journal. ppat. 1003697.
26. Xu J, Li CX, Li YS, Lv JY, Ma Y, Shao TT, Xu LD, Wang YY, Du L, Zhang YP, et al. MiRNA-miRNA synergistic network: construction via co-regulating functional modules and disease miRNA topological features. Nucleic Acids Res 2011; 39: 825-36; PMID: 20929877; http://dx. doi. org/10. 1093/nar/gkq832.
27. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, et al. Combinatorial microRNA target predictions. Nat Genet 2005; 37: 495-500; PMID: 15806104; http://dx. doi. org/10. 1038/ng1536.
28. Utaisincharoen P, Anuntagool N, Arjcharoen S, Lengwehasatit I, Limposuwan K, Chaisuriya P, Sirisinha S. Burkholderia pseudomallei stimulates low interleukin-8 production in the human lung epithelial cell line A549. Clin Exp Immunol 2004; 138: 61-5; PMID: 15373906; http://dx. doi. org/10. 1111/j. 1365-2249. 2004. 02601. x.
29. Utaisincharoen P, Arjcharoen S, Lengwehasatit I, Limposuwan K, Sirisinha S. Burkholderia pseudomallei invasion and activation of epithelial cells requires activation of p38 mitogen-activated protein kinase. Microb Pathog 2005; 38: 107-12; PMID: 15748812; http://dx. doi. org/10. 1016/j. micpath. 2004. 12. 006.
30. Cui J, Yao Q, Li S, Ding X, Lu Q, Mao H, Liu L, Zheng N, Chen S, Shao F. Glutamine deamidation and dysfunction of ubiquitin/NEDD8 induced by a bacterial effector family. Science 2010; 329: 1215-8; PMID: 20688984; http://dx. doi. org/10. 1126/science. 1193844.
31. Bierne H, Hamon M, Cossart P. Epigenetics and bacterial infections. Cold Spring Harb Perspect Med 2012; 2: a010272; PMID: 23209181; http://dx. doi. org/10. 1101/cshperspect. a010272.
32. Li W, Sun W, Liu L, Yang F, Li Y, Chen Y, et al. IL-32: a host proinflammatory factor against influenza viral replication is upregulated by aberrant epigenetic modifications during influenza A virus infection. J Immunol 2010; 185: 5056-65; PMID: 20889550; http://dx. doi. org/10. 4049/jimmunol. 0902667.
33. Tang B, Zhao R, Sun Y, Zhu Y, Zhong J, Zhao G, Zhu N. Interleukin-6 expression was regulated by epigenetic mechanisms in response to influenza virus infection or dsRNA treatment. Mol Immunol 2011; 48: 1001-8; PMID: 21353307; http://dx. doi. org/10. 1016/j. molimm. 2011. 01. 003.
34. Pero R, Peluso S, Angrisano T, Tuccillo C, Sacchetti S, Keller S, Tomaiuolo R, Bruni CB, Lembo F, Chiariotti L. et al. Chromatin and DNA methylation dynamics of Helicobacter pylori-induced COX-2 activation. Int J Med Microbiol 2011; 301: 140-9; PMID: 20934379; http://dx. doi. org/10. 1016/j. ijmm. 2010. 06. 009.
35. Ando T, Yoshida T, Enomoto S, Asada K, Tatematsu M, Ichinose M, Sugiyama T, Ushijima T. DNA methylation of microRNA genes in gastric mucosae of gastric cancer patients: its possible involvement in the formation of epigenetic field defect. Int J Cancer 2009; 124: 2367-74; PMID: 19165869; http://dx. doi. org/10. 1002/ijc. 24219.
36. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002; 16: 6-21; PMID: 11782440; http://dx. doi. org/10. 1101/gad. 947102.
37. Fang Y, Huang Y, Li Q, Chen H, Yao Z, Pan J, Gu J, Tang B, Wang HG, Yu B, et al. First genome sequence of a Burkholderia pseudomallei Isolate in China, strain BPC006, obtained from a melioidosis patient in Hainan. J Bacteriol 2012; 194: 6604-5; PMID: 23144371; http://dx. doi. org/10. 1128/JB. 01577-12.
38. Whitlock GC, Lukaszewski RA, Judy BM, Paessler S, Torres AG, Estes DM. Host immunity in the protective response to vaccination with heat-killed Burkholderia mallei. BMC Immunol 2008; 9: 55; PMID: 18823549; http://dx. doi. org/10. 1186/1471-2172-9-55.
39. Elsinghorst EA. Measurement of invasion by gentamicin resistance. Methods Enzymol 1994; 236: 405-20; PMID: 7968625.