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Effect of Gene actA on the Invasion Efficiency of Listeria monocytogenes, as Observed in Healthy and Senescent Intestinal Epithelial Cells

  • Ha, Jimyeong (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Oh, Hyemin (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Kim, Sejeong (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Lee, Jeeyeon (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Lee, Soomin (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Lee, Heeyoung (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Choi, Yukyung (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Moon, Sung Sil (Sunjin Meat & Processing Research Center) ;
  • Choi, Kyoung-Hee (Department of Oral Microbiology, College of Dentistry, Wonkwang University) ;
  • Yoon, Yohan (Department of Food and Nutrition, Sookmyung Women's University)
  • Received : 2017.10.20
  • Accepted : 2017.11.06
  • Published : 2018.01.28

Abstract

Listeria monocytogenes can asymptomatically inhabit the human intestine as a commensal bacterium. However, the mechanism by which L. monocytogenes is able to inhabit the intestine without pathogenic symptoms remains unclear. We compared the invasion efficiency of L. monocytogenes strains with the 268- and 385-bp-long actA gene. Clinical strains SMFM-CI-3 and SMFM-CI-6 with 268-bp actA isolated from patients with listeriosis, and strains SMFM-SI-1 and SMFM-SI-2 with the 385-bp gene isolated from carcasses, were used for inoculum preparation. The invasion efficiency of these strains was evaluated using Caco-2 cells (intestinal epithelial cell line), prepared as normal and healthy cells with tightened tight junctions and senescent cells with loose tight junctions that were loosened by adriamycin treatment. The invasion efficiency of L. monocytogenes strains with the 268-bp-long actA gene was 1.1-2.6-times lower than that of the strains with the 385-bp-long gene in normal and healthy cells. However, the invasion efficiency of both types of strains did not differ in senescent cells. Thus, L. monocytogenes strains with the 268-bp-long actA gene can inhabit the intestine asymptomatically as a commensal bacterium, but they may invade the intestinal epithelial cells and cause listeriosis in senescent cells.

Keywords

References

  1. Hansen CH, Vogel BF, Gram L. 2006. Prevalence and survival of Listeria monocytogenes in Danish aquatic and fishprocessing environments. J. Food Protect. 69: 2113-2122. https://doi.org/10.4315/0362-028X-69.9.2113
  2. Muhterem-Uyar M, Dalmasso M, Bolocan AS, Hernandez M, Kapetanakou AE, Kuchta T, et al. 2015. Environmental sampling for Listeria monocytogenes control in food processing facilities reveals three contamination scenarios. Food Control 51: 94-107. https://doi.org/10.1016/j.foodcont.2014.10.042
  3. Coroneo V, C arraro V , Aissani N, S anna A , Ru ggeri A, Succa S, et al. 2016. Detection of virulence genes and growth potential in Listeria monocytogenes strains isolated from ricotta salata cheese. J. Food Sci. 81: M114-M120. https://doi.org/10.1111/1750-3841.13173
  4. Kaufmann SH, Dorhoi A. 2016. Molecular determinants in phagocyte-bacteria interactions. Immunity 44: 476-491.
  5. Mengaud J, Ohayon H, Gounon P, Mege RM, Cossart P. 1996. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84: 923-932.
  6. Shen Y, Naujokas M, Park M, Ireton K. 2000. InlBdependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103: 501-510.
  7. Cossart P, Vicente MF, Mengaud J, Baquero F, Perez-Diaz JC, Berche P. 1989. Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect. Immun. 57: 3629-3636.
  8. Smith GA, Marquis H, Jones S, Johnston NC, Portnoy DA, Goldfine H. 1995. The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Infect. Immun. 63: 4231-4237.
  9. Domann E, Wehland J, Rohde M, Pistor S, Hartl M, Goebel W, Chakraborty T. 1992. A novel bacterial virulence gene in Listeria monocytogenes required for host cell microfilament interaction with homology to the proline-rich region of vinculin. EMBO J. 11: 1981-1990.
  10. Kocks C, Gouin E, Tabouret M, Berche P, Ohayon H, Cossart P. 1992. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68: 521-531. https://doi.org/10.1016/0092-8674(92)90188-I
  11. Suarez M, Gonzalez-Zorn B, Vega Y, Chico-Calero I, Vazquez-Boland JA. 2001. A role for ActA in epithelial cell invasion by Listeria monocytogenes. Cell. Microbiol. 3: 853-864.
  12. Pizarro-Cerda J, Kuhbacher A, Cossart P. 2012. Entry of Listeria monocytogenes in mammalian epithelial cells: an updated view. Cold Spring Harb. Perspect. Med. 2: a010009.
  13. Appelberg R, Leal IS. 2000. Mutants of Listeria monocytogenes defective in in vitro invasion and cell-to-cell spreading still invade and proliferate in hepatocytes of neutropenic mice. Infect. Immun. 68: 912-914.
  14. Lasa I, David V, Gouin E, Marchand JB, Cossar P. 1995. The amino-terminal part of ActA is critical for the actin-based motility of Listeria monocytogenes; the central proline-rich region acts as a stimulator. Mol. Microbiol. 18: 425-436. https://doi.org/10.1111/j.1365-2958.1995.mmi_18030425.x
  15. Pistor S, Chakraborty T, Walter U, Wehland J. 1995. The bacterial actin nucleator protein ActA of Listeria monocytogenes contains multiple binding sites for host microfilament proteins. Curr. Biol. 5: 517-525. https://doi.org/10.1016/S0960-9822(95)00104-7
  16. Conter M, Vergara A, Di Ciccio P, Zanardi E, Ghidini S, Ianieri A. 2010. Polymorphism of actA gene is not related to in vitro virulence of Listeria monocytogenes. Int J. Food Microbiol. 137: 100-105. https://doi.org/10.1016/j.ijfoodmicro.2009.10.019
  17. Jiang L L, X u JJ, C hen N, Shu ai J B, F ang WH. 2006. Virulence phenotyping and molecular characterization of a low-pathogenicity isolate of Listeria monocytogenes from cow's milk. Acta Biochim. Biophys. Sin. 38: 262-270. https://doi.org/10.1111/j.1745-7270.2006.00161.x
  18. Schwartz B, Hexter D, Broome CV, Hightower AW, Hirschhorn RB, Porter JD, et al. 1989. Investigation of an outbreak of listeriosis: new hypotheses for the etiology of epidemic Listeria monocytogenes infections. J. Infect. Dis. 159: 680-685. https://doi.org/10.1093/infdis/159.4.680
  19. Farber JM, Peterkin PI. 1991. Listeria monocytogenes, a foodborne pathogen. Microbiol. Mol. Biol. Rev. 55: 476-511.
  20. Ren W Y, W u KF, L i X, L uo M, L iu HC, Z hang S C, et al. 2014. Age-related changes in small intestinal mucosa epithelium architecture and epithelial tight junction in rat models. Aging Clin. Exp. Res. 26: 183-191. https://doi.org/10.1007/s40520-013-0148-0
  21. Oh HM. 2017. Prevalence and genetic characteristics of Listeria monocytogenes isolates from slaughterhouses, farms, and humans in South Korea. MD dissertation, Sookmyung Women's University, South Korea.
  22. Travier L, Guadagnini S, Gouin E, Dufour A, Chenal-Francisque V, Cossart P, et al. 2013. ActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage. PLoS Pathog. 9: e1003131.
  23. Peters WH, Roelofs HM. 1992. Biochemical characterization of resistance to mitoxantrone and adriamycin in Caco-2 human colon adenocarcinoma cells: a possible role for glutathione S-transferases. Cancer Res. 52: 1886-1890.
  24. Kwak ES. 2013. Exploration of plant extracts to induce cellular senescence in cancer cells. Ph. D. Thesis, Yeungnam University, South Korea
  25. Kim JW, Kim SH, Lee JH. 2008. Effect of hydrogen peroxide-induced oxidative stress on the senescence of trabecular meshwork cells. J. Korean Ophthalmol. Soc. 49: 1665-1670. https://doi.org/10.3341/jkos.2008.49.10.1665
  26. DeRisi JL, Lyer VR, Brown P.O. 1997. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278: 680-686. https://doi.org/10.1126/science.278.5338.680
  27. Hsu SH, Wang B, Kutay H, Bid H, Shreve J, Zhang X, et al. 2013. Hepatic loss of miR-122 predisposes mice to hepatobiliary cyst and hepatocellular carcinoma upon diethylnitrosamine exposure. Am. J. Pathol. 183: 1719-1730. https://doi.org/10.1016/j.ajpath.2013.08.004
  28. De Lisle RC. 2014. Disrupted tight junctions in the small intestine of cystic fibrosis mice. Cell Tissue Res. 355: 131-142.
  29. Garner MR, James KE, Callahan MC, Wiedmann M, Boor KJ. 2006. Exposure to salt and organic acids increases the ability of Listeria monocytogenes to invade Caco-2 cells but decreases its ability to survive gastric stress. Appl. Environ. Microbiol. 72: 5384-5395. https://doi.org/10.1128/AEM.00764-06
  30. Debacq-Chainiaux F, Erusalimsky JD, Campisi J, Toussaint O. 2009. Protocols to detect senescence-associated beta-galactosidase (SA-${\beta}gal$) activity, a biomarker of senescent cells in culture and in vivo. Nat. Protoc. 4: 1798-1806.
  31. Balda MS, Whitney JA, Flores C, Gonzalez S, Cereijido M, Matter K. 1996. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J. Cell Biol. 134: 1031-1049. https://doi.org/10.1083/jcb.134.4.1031
  32. Fanning AS, Jameson BJ, Jesaitis LA, Anderson JM. 1998. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J. Biol. Chem. 273: 29745-29753. https://doi.org/10.1074/jbc.273.45.29745
  33. Furuse M, Sasaki H, Fujimoto K, Tsukita S. 1998. A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J. Cell Biol. 143: 391-401. https://doi.org/10.1083/jcb.143.2.391
  34. Lipetz J, Cristofalo VJ. 1972. Ultrastructural changes accompanying the aging of human diploid cells in culture. J. Ultrastruct. Res. 39: 43-56. https://doi.org/10.1016/S0022-5320(72)80005-4
  35. He S, Sharpless NE. 2017. Senescence in health and disease. Cell 169: 1000-1011. https://doi.org/10.1016/j.cell.2017.05.015

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