Detection of virulence-associated genes and epidemic clone markers in Listeria monocytogenes isolates from PDO Gorgonzola cheese

International Journal of Food Microbiology

Volumn 160, Issue 1, 2012, Pages 76-79

  Lomonaco, Sara ^a   Patti, Rossella ^a   Knabel, Stephen J ^b   Civera, Tiziana ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Epidemic clones; Gorgonzola; Listeria monocytogenes; Pathogenic potential; Virulence genes

Indexed keywords

RNA 16S;

ACTA GENE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CHEESE; CLONE; DAIRY PRODUCT; GENE AMPLIFICATION; GENE SEQUENCE; GORGONZOLA CHEESE; HEALTH HAZARD; HLYA GENE; IAP GENE; INLC GENE; INLJ GENE; LISTERIA MONOCYTOGENES; LISTERIOSIS; MARKER GENE; MULTIPLEX POLYMERASE CHAIN REACTION; NONHUMAN; PHENOTYPE; PLCA GENE; POLYMERASE CHAIN REACTION; PRFA GENE;

CHEESE; CONSUMER PRODUCT SAFETY; ELECTROPHORESIS, GEL, PULSED-FIELD; FOOD CONTAMINATION; FOOD MICROBIOLOGY; HUMANS; LISTERIA MONOCYTOGENES; POLYMERASE CHAIN REACTION; SEROTYPING; VIRULENCE FACTORS;

LISTERIA INNOCUA; LISTERIA MONOCYTOGENES;

EID: 84868672811     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2012.09.011     Document Type: Article

References (40)

1. Bierne H., Sabet C., Personnic N., Cossart P. Internalins: a complex family of leucine-rich repeat-containing proteins in Listeria monocytogenes. Microbes and Infection / Institut Pasteur 2007, 9:1156-1166.
2. Bubert A., Sokolovic Z., Chun S.K., Papatheodorou L., Simm A., Goebel W. Differential expression of Listeria monocytogenes virulence genes in mammalian host cells. Molecular & General Genetics: MGG 1999, 261:323-336.
3. Carminati D., Mucchetti G., Neviani E., Fontana S. Il formaggio Gorgonzola e il problema Listeria monocytogenes (GOLIS) 2004, Regione Lombardia, Available in Italian at: http://www.agricoltura.regione.lombardia.it/shared/ccurl/57/695/QdR%2028%20GOLIS.pdf (Accessed on September 10, 2012).
4. Chen Y., Knabel S.J. Multiplex PCR for simultaneous detection of bacteria of the genus Listeria, Listeria monocytogenes, and major serotypes and epidemic clones of L. monocytogenes. Applied and Environmental Microbiology 2007, 73:6299-6304.
5. Chen Y., Zhang W., Knabel S.J. Multi-virulence-locus sequence typing identifies single nucleotide polymorphisms which differentiate epidemic clones and outbreak strains of Listeria monocytogenes. Journal of Clinical Microbiology 2007, 45:835-846.
6. Cheng Y., Siletzky R., Kathariou S. Genomic divisions/lineages, epidemic clones, and population structure. Handbook of Listeria monocytogenes 2008, 337-357. CRC Press. D. Liu (Ed.).
7. Conter M., Di Ciccio P., Zanardi E., D'Orio V., Ghidini S., Vergara A., Ianieri A. Caratterizzazione genotipica e sierologica di Listeria monocytogenes isolata da alimenti e ambienti di lavorazione. XVII Convegno Nazionale Associazione Italiana Veterinari Igienisti 2007, 313-317. (In Italian), Cesenatico.
8. CPGC Consortium for the protection of Gorgonzola Cheese Available at:, (Accessed on September 10, 2012). http://www.gorgonzola.com/Default.asp?selopt=1.
9. EU Regulation Regulation (EC) No 1107/96 of 12 June 1996 on the registration of geographical indications and designations of origin under the procedure laid down in Article 17 of Council Regulation (EEC) No 2081/92. Official Journal of the European Communities 1996, (L,148).
10. EU Regulation Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. Official Journal of the European Communities 2002, (L,31).
11. Farber J.M., Carter A.O., Varughese P.V., Ashton F.E., Ewan E.P. Listeriosis traced to the consumption of alfalfa tablets and soft cheese. The New England Journal of Medicine 1990, 322:338.
12. Franciosa G., Scalfaro C., Maugliani A., Floridi F., Gattuso A., Hodzic S., Aureli P. Distribution of epidemic clonal genetic markers among Listeria monocytogenes 4b isolates. Journal of Food Protection 2007, 70:574-581.
13. Fugett E., Fortes E., Nnoka C., Wiedmann M. International Life Sciences Institute North America Listeria monocytogenes strain collection: development of standard Listeria monocytogenes strain sets for research and validation studies. Journal of Food Protection 2006, 69:2929-2938.
14. Gaulin C., Ramsay D., Ringuette L., Ismaïl J. First documented outbreak of Listeria monocytogenes in Quebec, 2002. Canada Communicable Disease Report 2003, 29:181-186.
15. Gianfranceschi M., D'Ottavio M.C., Gattuso A., Pourshaban M., Bertoletti I., Bignazzi R., Manzoni P., Marchetti M., Aureli P. Listeriosis associated with gorgonzola (Italian blue-veined cheese). Foodborne Pathogens and Disease 2006, 3:190-195.
16. Gilmour M.W., Graham M., Van Domselaar G., Tyler S., Kent H., Trout-Yakel K.M., Larios O., Allen V., Lee B., Nadon C. High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genomics 2010, 11:120.
17. Jacquet C., Doumith M., Gordon J.I., Martin P.M.V., Cossart P., Lecuit M. A molecular marker for evaluating the pathogenic potential of foodborne Listeria monocytogenes. The Journal of Infectious Diseases 2004, 189:2094-2100.
18. Jiang L.L., Xu J.J., Chen N., Shuai J.B., Fang W.H. Virulence phenotyping and molecular characterization of a low-pathogenicity isolate of Listeria monocytogenes from cow's milk. Acta Biochimica et Biophysica Sinica 2006, 38:262-270.
19. Johnson J., Jinneman K., Stelma G., Smith B.G., Lye D., Messer J., Ulaszek J., Evsen L., Gendel S., Bennett R.W., Swaminathan B., Pruckler J., Steigerwalt A., Kathariou S., Yildirim S., Volokhov D., Rasooly A., Chizhikov V., Wiedmann M., Fortes E., Duvall R.E., Hitchins A.D. Natural atypical Listeria innocua strains with Listeria monocytogenes pathogenicity island 1 genes. Applied and Environmental Microbiology 2004, 70:4256-4266.
20. Kathariou S. Listeria monocytogenes virulence and pathogenicity, a food safety perspective. Journal of Food Protection 2002, 65:1811-1829.
21. Kaur S., Malik S.V.S., Vaidya V.M., Barbuddhe S.B. Listeria monocytogenes in spontaneous abortions in humans and its detection by multiplex PCR. Journal of Applied Microbiology 2007, 103:1889-1896.
22. Knabel S., Reimer A., Verghese B., Lok M., Ziegler J., Farber J., Pagotto F., Graham M., Nadon C., Gilmour M. Sequence typing confirms that a predominant Listeria monocytogenes clone caused human listeriosis cases and outbreaks in Canada from 1988-2010. Journal of Clinical Microbiology 2012, 50:1748-1751.
23. Linnan M.J., Mascola L., Lou X.D., Goulet V., May S., Salminen C., Hird D.W., Yonekura M.L., Hayes P., Weaver R. Epidemic listeriosis associated with Mexican-style cheese. The New England Journal of Medicine 1988, 319:823-828.
24. Liu D., Lawrence M.L., Austin F.W., Ainsworth A.J. A multiplex PCR for species- and virulence-specific determination of Listeria monocytogenes. Journal of Microbiological Methods 2007, 71:133-140.
25. Lomonaco S., Decastelli L., Nucera D., Gallina S., Manila Bianchi D., Civera T. Listeria monocytogenes in Gorgonzola: subtypes, diversity and persistence over time. International Journal of Food Microbiology 2009, 128:516-520.
26. Lomonaco S., Knabel S.J., Dalmasso A., Civera T., Bottero M.T. Novel multiplex single nucleotide polymorphism-based method for identifying epidemic clones of Listeria monocytogenes. Applied and Environmental Microbiology 2011, 77:6290-6294.
27. Lundén J., Tolvanen R., Korkeala H. Human listeriosis outbreaks linked to dairy products in Europe. Journal of Dairy Science 2004, 87:E6-E11.
28. Mammina C., Aleo A., Romani C., Pellissier N., Nicoletti P., Pecile P., Nastasi A., Pontello M.M. Characterization of Listeria monocytogenes isolates from human listeriosis cases in Italy. Journal of Clinical Microbiology 2009, 47:2925-2930.
29. Mazzette R., Meloni D., Conter M., Mureddu A., Piras F., Colleo M. Indagine epidemiologica e profilo di patogenicità di ceppi di Listeria monocytogenes isolati da prodotti della pesca Ready-To-Eat. XVII Convegno Nazionale Associazione Italiana Veterinari Igienisti 2007, 229-233. (In Italian), Cesenatico.
30. Moreno L.Z., Paixão R., Gobbi D.D., Raimundo D.C., Ferreira T.P., Hofer E., Matte M.H., Moreno A.M. Characterization of atypical Listeria innocua isolated from swine slaughterhouses and meat markets. Research in Microbiology 2012, 163:268-271.
31. Neves E., Lourenço A., Silva A.C., Coutinho R., Brito L. Pulsed-field gel electrophoresis (PFGE) analysis of Listeria monocytogenes isolates from different sources and geographical origins and representative of the twelve serovars. Systematic and Applied Microbiology 2008, 31:387-392.
32. Nightingale K.K., Milillo S.R., Ivy R.A., Ho A.J., Oliver H.F., Wiedmann M. Listeria monocytogenes F2365 carries several authentic mutations potentially leading to truncated gene products, including inlB, and demonstrates atypical phenotypic characteristics. Journal of Food Protection 2007, 70:482-488.
33. Nightingale K.K., Ivy R.A., Ho A.J., Fortes E.D., Njaa B.L., Peters R.M., Wiedmann M. inlA premature stop codons are common among Listeria monocytogenes isolates from foods and yield virulence-attenuated strains that confer protection against fully virulent strains. Applied and Environmental Microbiology 2008, 74:6570-6583.
34. Pagotto F., Ng L.-K., Clark C., Farber J. Canadian listeriosis reference service. Foodborne Pathogens and Disease 2006, 3:132-137.
35. Roberts A.J., Williams S.K., Wiedmann M., Nightingale K.K. Some Listeria monocytogenes outbreak strains demonstrate significantly reduced invasion, inlA transcript levels, and swarming motility in vitro. Applied and Environmental Microbiology 2009, 75:5647-5658.
36. Roche S.M., Grépinet O., Corde Y., Teixeira A.P., Kerouanton A., Témoin S., Mereghetti L., Brisabois A., Velge P. A Listeria monocytogenes strain is still virulent despite nonfunctional major virulence genes. The Journal of Infectious Diseases 2009, 200:1944-1948.
37. Swaminathan B., Gerner-Smidt P. The epidemiology of human listeriosis. Microbes and Infection / Institut Pasteur 2007, 9:1236-1243.
38. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 2011, 28:2731-2739.
39. Van Stelten A., Simpson J.M., Ward T.J., Nightingale K.K. Revelation by single-nucleotide polymorphism genotyping that mutations leading to a premature stop codon in inlA are common among Listeria monocytogenes isolates from ready-to-eat foods but not human listeriosis cases. Applied and Environmental Microbiology 2010, 76:2783-2790.
40. Vázquez-Boland J.A., Kuhn M., Berche P., Chakraborty T., Domínguez-Bernal G., Goebel W., González-Zorn B., Wehland J., Kreft J. Listeria pathogenesis and molecular virulence determinants. Clinical Microbiology Reviews 2001, 14:584-640.