Host-pathogen Interaction at the Intestinal Mucosa Correlates With Zoonotic Potential of Streptococcus Suis

Overview

Journal J Infect Dis

Publisher Oxford University Press

Specialty Infectious Diseases

Date 2014 Dec 20

PMID 25525050

Citations 37

Authors

Maria Laura Ferrando

Astrid de Greeff

Willemien J M van Rooijen

Norbert Stockhofe-Zurwieden

Jens Nielsen

Paul J Wichgers Schreur

Yvonne Pannekoek

Annet Heuvelink

Arie van der Ende

Hilde Smith

Constance Schultsz

Affiliations

Soon will be listed here.

Abstract

Background: Streptococcus suis has emerged as an important cause of bacterial meningitis in adults. The ingestion of undercooked pork is a risk factor for human S. suis serotype 2 (SS2) infection. Here we provide experimental evidence indicating that the gastrointestinal tract is an entry site of SS2 infection.

Methods: We developed a noninvasive in vivo model to study oral SS2 infection in piglets. We compared in vitro interaction of S. suis with human and porcine intestinal epithelial cells (IEC).

Results: Two out of 15 piglets showed clinical symptoms compatible with S. suis infection 24-48 hours after ingestion of SS2. SS2 was detected in mesenteric lymph nodes of 40% of challenged piglets. SS2 strains isolated from patients showed significantly higher adhesion to human IEC compared to invasive strains isolated from pigs. In contrast, invasive SS9 strains showed significantly higher adhesion to porcine IEC. Translocation across human IEC, which occurred predominately via a paracellular route, was significantly associated with clonal complex 1, the predominant zoonotic genotype. Adhesion and translocation were dependent on capsular polysaccharide production.

Conclusions: SS2 should be considered a food-borne pathogen. S. suis interaction with human and pig IEC correlates with S. suis serotype and genotype, which can explain the zoonotic potential of SS2.

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References

Jacewicz M, Acheson D, Mobassaleh M, Donohue-Rolfe A, Balasubramanian K, Keusch G . Maturational regulation of globotriaosylceramide, the Shiga-like toxin 1 receptor, in cultured human gut epithelial cells. J Clin Invest. 1995; 96(3):1328-35. PMC: 185755. DOI: 10.1172/JCI118168. View

Swildens B, Stockhofe-Zurwieden N, van der Meulen J, Wisselink H, Nielen M, Niewold T . Intestinal translocation of Streptococcus suis type 2 EF+ in pigs. Vet Microbiol. 2004; 103(1-2):29-33. DOI: 10.1016/j.vetmic.2004.06.010. View

Feng Y, Zhang H, Wu Z, Wang S, Cao M, Hu D . Streptococcus suis infection: an emerging/reemerging challenge of bacterial infectious diseases?. Virulence. 2014; 5(4):477-97. PMC: 4063810. DOI: 10.4161/viru.28595. View

Liu B, Yin X, Feng Y, Chambers J, Guo A, Gong J . Verotoxin 2 enhances adherence of enterohemorrhagic Escherichia coli O157:H7 to intestinal epithelial cells and expression of {beta}1-integrin by IPEC-J2 cells. Appl Environ Microbiol. 2010; 76(13):4461-8. PMC: 2897442. DOI: 10.1128/AEM.00182-10. View

Kim H, Bhunia A . Secreted Listeria adhesion protein (Lap) influences Lap-mediated Listeria monocytogenes paracellular translocation through epithelial barrier. Gut Pathog. 2013; 5(1):16. PMC: 3716925. DOI: 10.1186/1757-4749-5-16. View

Brosnahan A, Brown D . Porcine IPEC-J2 intestinal epithelial cells in microbiological investigations. Vet Microbiol. 2011; 156(3-4):229-37. PMC: 3289732. DOI: 10.1016/j.vetmic.2011.10.017. View

Kouki A, Haataja S, Loimaranta V, Pulliainen A, Nilsson U, Finne J . Identification of a novel streptococcal adhesin P (SadP) protein recognizing galactosyl-α1-4-galactose-containing glycoconjugates: convergent evolution of bacterial pathogens to binding of the same host receptor. J Biol Chem. 2011; 286(45):38854-64. PMC: 3234710. DOI: 10.1074/jbc.M111.260992. View

Darzynkiewicz Z, Li X, Gong J . Assays of cell viability: discrimination of cells dying by apoptosis. Methods Cell Biol. 1994; 41:15-38. DOI: 10.1016/s0091-679x(08)61707-0. View

Pezzicoli A, Santi I, Lauer P, Rosini R, Rinaudo D, Grandi G . Pilus backbone contributes to group B Streptococcus paracellular translocation through epithelial cells. J Infect Dis. 2008; 198(6):890-8. DOI: 10.1086/591182. View

10.

Williams D, Lawson G, Rowland A . Streptococcal infection in piglets: the palatine tonsils as portals of entry for Streptococcus suis. Res Vet Sci. 1973; 15(3):352-62. View

11.

Schultsz C, Jansen E, Keijzers W, Rothkamp A, Duim B, Wagenaar J . Differences in the population structure of invasive Streptococcus suis strains isolated from pigs and from humans in The Netherlands. PLoS One. 2012; 7(5):e33854. PMC: 3341392. DOI: 10.1371/journal.pone.0033854. View

12.

Peterson L, Artis D . Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol. 2014; 14(3):141-53. DOI: 10.1038/nri3608. View

13.

Deer D, Lampel K, Gonzalez-Escalona N . A versatile internal control for use as DNA in real-time PCR and as RNA in real-time reverse transcription PCR assays. Lett Appl Microbiol. 2010; 50(4):366-72. DOI: 10.1111/j.1472-765X.2010.02804.x. View

14.

King S, Leigh J, Heath P, Luque I, Tarradas C, Dowson C . Development of a multilocus sequence typing scheme for the pig pathogen Streptococcus suis: identification of virulent clones and potential capsular serotype exchange. J Clin Microbiol. 2002; 40(10):3671-80. PMC: 130843. DOI: 10.1128/JCM.40.10.3671-3680.2002. View

15.

Thieu Nga T, Nghia H, Tu L, Song Diep T, Mai N, Chau T . Real-time PCR for detection of Streptococcus suis serotype 2 in cerebrospinal fluid of human patients with meningitis. Diagn Microbiol Infect Dis. 2011; 70(4):461-7. PMC: 3146703. DOI: 10.1016/j.diagmicrobio.2010.12.015. View

16.

Huong V, Ha N, Huy N, Horby P, Nghia H, Thiem V . Epidemiology, clinical manifestations, and outcomes of Streptococcus suis infection in humans. Emerg Infect Dis. 2014; 20(7):1105-14. PMC: 4073838. DOI: 10.3201/eid2007.131594. View

17.

Su Y, Yao W, Perez-Gutierrez O, Smidt H, Zhu W . Changes in abundance of Lactobacillus spp. and Streptococcus suis in the stomach, jejunum and ileum of piglets after weaning. FEMS Microbiol Ecol. 2008; 66(3):546-55. DOI: 10.1111/j.1574-6941.2008.00529.x. View

18.

Takamatsu D, Osaki M, Sekizaki T . Thermosensitive suicide vectors for gene replacement in Streptococcus suis. Plasmid. 2001; 46(2):140-8. DOI: 10.1006/plas.2001.1532. View

19.

Nielsen J, Vincent I, Botner A, Ladekaer-Mikkelsen A, Allan G, Summerfield A . Association of lymphopenia with porcine circovirus type 2 induced postweaning multisystemic wasting syndrome (PMWS). Vet Immunol Immunopathol. 2003; 92(3-4):97-111. DOI: 10.1016/s0165-2427(03)00031-x. View

20.

Nabuurs M, van Essen G, Nabuurs P, Niewold T, van der Meulen J . Thirty minutes transport causes small intestinal acidosis in pigs. Res Vet Sci. 2001; 70(2):123-7. DOI: 10.1053/rvsc.2001.0448. View