Current Microbiology

, Volume 76, Issue 5, pp 637–643 | Cite as

Association of Listeria monocytogenes LIPI-1 and LIPI-3 marker llsX with invasiveness

  • Rodolfo Erik Vilchis-Rangel
  • María del Rosario Espinoza-MelladoEmail author
  • Irving Jesús Salinas-Jaramillo
  • Marcos Daniel Martinez-Peña
  • Oscar Rodolfo Rodas-Suárez


Listeria monocytogenes is an opportunistic pathogen that is widely distributed in the environment. The evolution of its genome has exhibited differences in virulence among strains of the same species. Listeria monocytogenes LIPI-3 (Listeria Pathogenicity Island 3) and LIPI-1 (Listeria Pathogenicity Island 1) are considered responsible for the increased virulence in some strains. The aim of this study was to detect LIPI-1 genes and the llsX gene belonging to LIPI-3 in invasive strains of L. monocytogenes and to establish whether there is a relationship among the invasiveness, presence of the llsX and LIPI-1 genes, and the source of the strains. The results showed that 70% of the strains were invasive, and all these strains except one possessed LIPI-1, which suggests that although there is a correlation between LIPI-1 and invasiveness, the independent mechanisms of LIPI-1 may contribute to invasiveness. In contrast, 35% of the total strains were positive for llsX and were invasive; thus, the results revealed that there is a strong association between llsX and the invasiveness of L. monocytogenes in HEp-2 cells (HeLa contaminant/epithelial in origin). In addition, there is no other association with any other variable in this study. Moreover, the authors found that LIPI-1 and llsX are more frequently found in fresh than in frozen vegetables. Together, the findings provide an approximation for the better understanding of Listeriolysin S (LLS) and its role in the pathogenesis of L. monocytogenes, and a possible relation between virulence factors and food-storage temperature.



REV-R was a recipient of a scholarship from BEIFI-México in 2013–2014. ORR-S is the recipient of COFAA and EDI fellowships. MRE-M is the recipient of SNI and EDI fellowships.


This work was supported by the SIP-IPN (Grants 20131379, 20141510, 20151345, 20161199, 20170749, 20181268).


  1. 1.
    Akya A, Najafi F, Moradi J et al (2013) Prevalence of food contamination with Listeria spp. in Kermanshah, Islamic Republic of Iran. East Mediterr Health J 19:474–477CrossRefGoogle Scholar
  2. 2.
    Ariza-Miguel J, Fernández-Natal M, Soriano F et al (2015) Molecular epidemiology of invasive listeriosis due to Listeria monocytogenes in a Spanish hospital over a nine-year study period. 2006–2014. BioMed Res Int 2015:191409. CrossRefGoogle Scholar
  3. 3.
    Bouayad L, Hamdi M, Naim M et al (2015) Prevalence of Listeria spp. and molecular characterization of Listeria monocytogenes isolates from broilers at the abattoir. Foodborne Pathog Dis 12:606–611. CrossRefGoogle Scholar
  4. 4.
    Clayton EM, Hill C, Cotter PD et al (2011) Real-time PCR assay to differentiate Listeriolysin S-positive and negative strains of Listeria monocytogenes.. Appl Environ Microbiol 77:163–171. CrossRefGoogle Scholar
  5. 5.
    Clayton EM, Daly KM, Guinane CM et al (2014) Atypical Listeria innocua strains possess an intact LIPI-3. BMC Microbiol 14:58. CrossRefGoogle Scholar
  6. 6.
    Cossart P, Lecuit M (1998) Interactions of Listeria monocytogenes with mammalian cells during entry and actin-based movement: bacterial factors, cellular ligands and signaling. EMBO J 17:3797–3806. CrossRefGoogle Scholar
  7. 7.
    Cotter PD, Draper LA, Lawton EM et al (2008) Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes. PLoS Pathog 4:e1000144. CrossRefGoogle Scholar
  8. 8.
    Dramsi S, Cossart P (2003) Listeriolysin O-mediated calcium influx potentiates entry of Listeria monocytogenes into the human Hep-2 epithelial cell line. Infect lmmun 71:3614–3618. CrossRefGoogle Scholar
  9. 9.
    Du XJ, Zhang X, Wang XY et al (2017) Isolation and characterization of Listeria monocytogenes in Chinese food obtained from the central area of China. Food Control 74:9–16. CrossRefGoogle Scholar
  10. 10.
    Favaro M, Sarmati L, Sancesario G et al (2014) First case of Listeria innocua meningitis in a patient on steroids and eternecept. JMM Case Rep Google Scholar
  11. 11.
    Francis MS, Thomas CJ (1996) Effect of multiplicity of infection on Listeria monocytogenes pathogenicity for HeLa and Caco-2 cell lines. J Med Microbiol 45:323–330. CrossRefGoogle Scholar
  12. 12.
    Gebretsadik S, Kassa T, Alemayehu H et al (2011) Isolation and characterization of Listeria monocytogenes and other Listeria species in foods of animal origin in Addis Ababa, Ethiopia. J Infect Public Health 4:22–29. CrossRefGoogle Scholar
  13. 13.
    Hitchens AD (1995) Listeria monocytogenes. In: FDA bacteriological analytical manual, 8th edn. AOAC International, Arlington, pp 10.1–10.13Google Scholar
  14. 14.
    Hmaïed F, Helel S, Le berre V et al (2013) Prevalence, identification by a DNA microarray-based assay of human and food isolates Listeria spp. from Tunisia. Pathol Biol 62:24–29. CrossRefGoogle Scholar
  15. 15.
    Johnson JR, Kuskowski MA, Smith K et al (2005) Antimicrobial-resistant and extraintestinal pathogenic Escherichia coli in retail foods. J Infect Dis 191:1040–1049. CrossRefGoogle Scholar
  16. 16.
    Klein P, Juneja V (1997) Sensitive detection of viable Listeria monocytogenes by reverse transcription PCR. Appl Environ Microbiol 63:4441–4448Google Scholar
  17. 17.
    Kocaman N, Sarimehmetoğlu B (2016) Stress responses of Listeria monocytogenes. Ankara Üniv Vet Fak Derg 63:421–427CrossRefGoogle Scholar
  18. 18.
    Komora N, Bruschi C, Magalhães R, Ferreira et al (2017) Survival of Listeria monocytogenes with different antibiotic resistance patterns to food-associated stresses. Int J Food Microbiol 245:79–87. CrossRefGoogle Scholar
  19. 19.
    Li Z, Pérez-Osorio A, Wang Y et al (2017) Whole genome sequencing analyses of Listeria monocytogenes that persisted in a milkshake machine for a year and caused illnesses in Washington State. BMC Microbiol 17:1–11. CrossRefGoogle Scholar
  20. 20.
    Perrin M, Bemer M, Delamare C (2003) Fatal case of Listeria innocua bacteremia. J Clin Microbiol 41:5308–5309. CrossRefGoogle Scholar
  21. 21.
    Portnoy DA, Chakraborty T, Goebel W et al (1992) Molecular determinants of Listeria monocytogenes pathogenesis. Infect Immun 60:1263–1267Google Scholar
  22. 22.
    Quereda JJ, Dussurget O, Nahori M-A et al (2016) Bacteriocin from epidemic Listeria strains alters the host intestinal microbiota to favor infection. Proc Natl Acad Sci USA 113:5706–5711. CrossRefGoogle Scholar
  23. 23.
    Quereda JJ, Meza-Torres J, Cossart P et al (2017) Listeriolysin S: a bacteriocin from epidemic Listeria monocytogenes strains that targets the gut microbiota. Gut Microbes 8:384–391. CrossRefGoogle Scholar
  24. 24.
    Rohlf FJ (1998) NTSYS-pc Numerical taxonomy and multivariate analysis system, version 2.21q. EXETER software, Setauket, New York, USAGoogle Scholar
  25. 25.
    Sansano S, Rivas A, Piña-Pérez MC et al (2017) Stevia rebaudiana Bertoni effect on the hemolytic potential of Listeria monocytogenes. Int J Food Microbiol 250:7–11. CrossRefGoogle Scholar
  26. 26.
    Söderqvist K, Lambertz ST, Vågsholm I et al (2017) Fate of Listeria monocytogenes, pathogenic Yersinia enterocolitica, and Escherichia coli O157:H7 gfp+ in ready-to-eat salad during cold storage: what is the risk to consumers? J Food Prot 80:204–212. CrossRefGoogle Scholar
  27. 27.
    Stea E, Purdue L, Jamieson R et al (2015) Comparison of the prevalences and diversities of Listeria species and Listeria monocytogenes in an urban and a rural agricultural watershed. Appl Environ Microbiol 81:3812–3822. CrossRefGoogle Scholar
  28. 28.
    Tao T, Chen Q, Bie X et al (2017) Investigation on prevalence of Listeria spp. and Listeria monocytogenes in animal-derived foods by multiplex PCR assay targeting novel genes. Food Control 73:704–711. CrossRefGoogle Scholar
  29. 29.
    Vallim D, Hofer C, Lisboa R et al (2015) Twenty years of Listeria in Brazil: occurrence of Listeria species and Listeria monocytogenes serovars in food samples in Brazil between 1990 and 2012. Biomed Res Int 2015:540204. CrossRefGoogle Scholar
  30. 30.
    Vázquez-Boland JA, Kuhn M, Berche P et al (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14:584–640. CrossRefGoogle Scholar
  31. 31.
    Wałecka-Zacharska E, Kosek-Paszkowska K, Bania J et al (2013) Salt stress-induced invasiveness of major Listeria monocytogenes serotypes. Lett Appl Microbiol 56:216–221. CrossRefGoogle Scholar
  32. 32.
    Zoz F, Grandvalet C, Lang E et al (2017) Listeria monocytogenes ability to survive desiccation: influence of serotype, origin, virulence, and genotype. Int J Food Microbiol 248:82–89. CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Rodolfo Erik Vilchis-Rangel
    • 1
  • María del Rosario Espinoza-Mellado
    • 2
    Email author
  • Irving Jesús Salinas-Jaramillo
    • 3
  • Marcos Daniel Martinez-Peña
    • 4
  • Oscar Rodolfo Rodas-Suárez
    • 3
  1. 1.Laboratorio de Bacteriología Médica, Depto. MicrobiologíaEscuela Nacional de Ciencias Biológicas-Instituto Politécnico Nacional (ENCB-IPN)Mexico CityMexico
  2. 2.Depto. InvestigaciónCentral de Instrumentación de Microscopia, ENCB-IPNMexico CityMexico
  3. 3.Laboratorio de Microbiología General, Depto. MicrobiologíaENCB-IPNMexico CityMexico
  4. 4.Laboratorio de Recursos Genéticos MicrobianosCentro Nacional de Recursos Genéticos (CNRG), Instituto Nacional de Investigaciones ForestalesTepatitlán de MorelosMexico

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