Yersiniosis is a food-borne illness that has become more prevalent in recent years due to human transmission via the fecal-oral route and prevalence in farm animals. Yersiniosis is primarily caused by Yersinia enterocolitica and less frequently by Yersinia pseudotuberculosis. Infection is usually characterized by a self-limiting acute infection beginning in the intestine and spreading to the mesenteric lymph nodes. However, more serious infections and chronic conditions can also occur, particularly in immunocompromised individuals. Y. enterocolitica and Y. pseudotuberculosis are both heterogeneous organisms that vary considerably in their degrees of pathogenicity, although some generalizations can be ascribed to pathogenic variants. Adhesion molecules and a type III secretion system are critical for the establishment and progression of infection. Additionally, host innate and adaptive immune responses are both required for yersiniae clearance. Despite the ubiquity of enteric Yersinia species and their association as important causes of food poisoning world-wide, few national enteric pathogen surveillance programs include the yersiniae as notifiable pathogens. Moreover, no standard exists whereby identification and reporting systems can be effectively compared and global trends developed. This review discusses yersinial virulence factors, mechanisms of infection, and host responses in addition to the current state of surveillance, detection, and prevention of yersiniosis. 1. Introduction Yersiniosis is typically a self-limiting, gastrointestinal disease of global concern. However, despite the known association of the causative agents (Y. enterocolitica, YE, and very rarely Y. pseudotuberculosis, YPT) with both gastroenteritis and extraintestinal infections, it remains a poorly understood disease. Sporadic cases are still reported in which food is not suspected as the source of infection, and isolation from contaminated food sources is often problematic. Because yersiniosis is considered relatively uncommon and YE and YPT are ubiquitous, food and water supplies are not regularly monitored for these bacterial pathogens. However, the ability of the yersiniae to persist in a nonculturable but viable state in natural samples [1] and to grow and thrive at refrigeration temperatures (~4°C) suggests that their contribution to disease might be underappreciated. 1.1. YE Infections The major causative agent of yersiniosis is the gram-negative, zoonotic bacterial pathogen, YE, which is typically transmitted via the fecal-oral route [2]. The closely related YPT can
References
[1]
M. Alexandrino, E. Grohmann, and U. Szewzyk, “Optimization of PCR-based methods for rapid detection of Campylobacter jejuni, Campylobacter coli and Yersinia enterocolitica serovar 0:3 in wastewater samples,” Water Research, vol. 38, no. 5, pp. 1340–1346, 2004.
[2]
N. R. H. El-Maraghi and N. S. Mair, “The histopathology of enteric infection with Yersinia pseudotuberculosis,” American Journal of Clinical Pathology, vol. 71, no. 6, pp. 631–639, 1979.
[3]
E. J. Bottone, “Yersinia enterocolitica: overview and epidemiologic correlates,” Microbes and Infection, vol. 1, no. 4, pp. 323–333, 1999.
[4]
K. Fr？lich, J. Wisser, H. Schmüser et al., “Epizootiologic and ecologic investigations of European brown hares (Lepus europaeus) in selected populations from Schleswig-Holstein, Germany,” Journal of Wildlife Diseases, vol. 39, no. 4, pp. 751–761, 2003.
[5]
E. V. Langford, “Pasteurella pseudotuberculosis infections in Western Canada,” Canadian Veterinary Journal, vol. 13, no. 4, pp. 85–87, 1972.
[6]
K. Mühldorfer, G. Wibbelt, J. Haensel, J. Riehm, and S. Speck, “Yersinia species isolated from Bats, Germany,” Emerging Infectious Diseases, vol. 16, no. 3, pp. 578–580, 2010.
[7]
M. Fredriksson-Ahomaa, A. Stolle, A. Siitonen, and H. Korkeala, “Sporadic human Yersinia enterocolitica infections caused by bioserotype 4/O:3 originate mainly from pigs,” Journal of Medical Microbiology, vol. 55, no. 6, pp. 747–749, 2006.
[8]
S. Bonardi, A. Paris, L. Bassi et al., “Detection, semiquantitative enumeration, and antimicrobial susceptibility of Yersinia enterocolitica in Pork and Chicken Meats in Italy,” Journal of Food Protection, vol. 73, no. 10, pp. 1785–1792, 2010.
[9]
T. F. Jones, S. C. Buckingham, C. A. Bopp, E. Ribot, and W. Schaffner, “From pig to pacifier: chitterling-associated Yersiniosis outbreak among black infants,” Emerging Infectious Diseases, vol. 9, no. 8, pp. 1007–1009, 2003.
[10]
X. Wang, Z. Cui, H. Wang et al., “Pathogenic strains of Yersinia enterocolitica isolated from domestic dogs (Canis familiaris) belonging to farmers are of the same subtype as pathogenic Y. enterocolitica strains isolated from humans and may be a source of human infection in Jiangsu Province, China,” Journal of Clinical Microbiology, vol. 48, no. 5, pp. 1604–1610, 2010.
[11]
A. Backhans, C. Fellstrom, and S. T. Lambertz, “Occurrence of pathogenic Yersinia enterocolitica and Yersinia pseudotuberculosis in small wild rodents,” Epidemiology and Infection, pp. 1–9, 2010.
[12]
H. Fukushima, Y. Ito, and K. Saito, “Role of the fly in the transport of Yersinia enterocolitica,” Applied and Environmental Microbiology, vol. 38, no. 5, pp. 1009–1010, 1979.
[13]
N. Rahuma, K. S. Ghenghesh, R. Ben Aissa, and A. Elamaari, “Carriage by the housefly (Musca domestica) of multiple-antibiotic-resistant bacteria that are potentially pathogenic to humans, in hospital and other urban environments in Misurata, Libya,” Annals of Tropical Medicine and Parasitology, vol. 99, no. 8, pp. 795–802, 2005.
[14]
M. Lynch, J. Painter, R. Woodruff, and C. Braden, “Surveillance for foodborne-disease outbreaks—United States, 1998–2002,” Morbidity and Mortality Weekly Report, vol. 55, no. 10, pp. 1–42, 2006.
[15]
E. J. Bottone, “Yersinia enterocolitica: the charisma continues,” Clinical Microbiology Reviews, vol. 10, no. 2, pp. 257–276, 1997.
[16]
A. Grutzkau, C. Hanski, H. Hahn, and E. O. Riecken, “Involvement of M cells in the bacterial invasion of Peyer's patches: a common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria,” Gut, vol. 31, no. 9, pp. 1011–1015, 1990.
[17]
J. C. Pepe and V. L. Miller, “The biological role of invasin during a Yersinia enterocolitica infection,” Infectious Agents and Disease, vol. 2, no. 4, pp. 236–241, 1993.
[18]
J. C. Pepe and V. L. Miller, “Yersinia enterocolitica invasin: a primary role in the initiation of infection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 14, pp. 6473–6477, 1993.
[19]
K. Trülzsch, M. F. Oellerich, and J. Heesemann, “Invasion and dissemination of Yersinia enterocolitica in the mouse infection model,” Advances in Experimental Medicine and Biology, vol. 603, pp. 279–285, 2007.
[20]
K. Donald, J. Woodson, H. Hudson, and J. O. Menzoian, “Multiple mycotic pseudoaneurysms due to Yersinia enterocolitica: report of a case and review of the literature,” Annals of Vascular Surgery, vol. 10, no. 6, pp. 573–577, 1996.
[21]
M. E. Hagensee, “Mycotic aortic aneurysm due to Yersinia enterocolitica,” Clinical Infectious Diseases, vol. 19, no. 4, pp. 801–802, 1994.
[22]
B. La Scola, D. Musso, A. Carta, P. Piquet, and J. P. Casalta, “Aortoabdominal aneurysm infected by Yersinia enterocolitica serotype O:9,” Journal of Infection, vol. 35, no. 3, pp. 314–315, 1997.
[23]
P. Mercié, P. Morlat, A. N'gako et al., “Aortic aneurysms due to Yersinia enterocolitica: three new cases and a review of the literature,” Journal des Maladies Vasculaires, vol. 21, no. 2, pp. 68–71, 1996.
[24]
G. R. Plotkin and J. N. O'Rourke, “Mycotic aneurysm due to Yersinia enterocolitica,” American Journal of the Medical Sciences, vol. 281, no. 1, pp. 35–42, 1981.
[25]
M. B. Prentice, N. Fortineau, T. Lambert, A. Voinnesson, and D. Cope, “Yersinia enterocolitica and mycotic aneurysm,” Lancet, vol. 341, no. 8859, pp. 1535–1536, 1993.
[26]
S. Tame, D. De Wit, and A. Meek, “Yersinia enterocolitica and mycotic aneurysm,” Australian and New Zealand Journal of Surgery, vol. 68, no. 11, pp. 813–814, 1998.
[27]
R. Van Noyen, P. Peeters, F. Van Dessel, and J. Vandepitte, “Mycotic aneurysm of the aorta due to Yersinia enterocolitica,” Contributions to Microbiology and Immunology, vol. 9, pp. 122–126, 1987.
[28]
J. Van Steen, J. Vercruysse, G. Wilms, and A. Nevelsteen, “Arteriosclerotic abdominal aortic aneurysm infected with Yersinia enterocolitica,” RoFo Fortschritte auf dem Gebiete der Rontgenstrahlen und der Neuen Bildgebenden Verfahren, vol. 151, no. 5, pp. 625–626, 1989.
[29]
M. Fredriksson-Ahomaa, A. Stolle, and H. Korkeala, “Molecular epidemiology of Yersinia enterocolitica infections,” FEMS Immunology and Medical Microbiology, vol. 47, no. 3, pp. 315–329, 2006.
[30]
T. L. Cover and R. C. Aber, “Yersinia enterocolitica,” New England Journal of Medicine, vol. 321, no. 1, pp. 16–24, 1989.
[31]
H. Fukushima, M. Gomyoda, S. Ishikura et al., “Cat-contaminated environmental substances lead to Yersinia pseudotuberculosis infection in children,” Journal of Clinical Microbiology, vol. 27, no. 12, pp. 2706–2709, 1989.
[32]
M. Tsubokura, K. Otsuki, K. Sato et al., “Special features of distribution of Yersinia pseudotuberculosis in Japan,” Journal of Clinical Microbiology, vol. 27, no. 4, pp. 790–791, 1989.
[33]
A. Gaulier and F. Poulton, “The place of anatomo-pathological study in the diagnosis of enterocolitis complicated by Yersinia pseudotuberculosis,” Annales de Pathologie, vol. 3, no. 4, pp. 301–305, 1983.
[34]
J. C. Delchier, D. Constantini, and J. C. Soule, “Presence of anti-Yersinia pseudotuberculosis agglutinins during a flare-up of ileal Crohn's disease. Apropos of 3 cases,” Gastroenterologie Clinique et Biologique, vol. 7, no. 6-7, pp. 580–584, 1983.
[35]
J. W. Koo, C. R. Cho, S. J. Cha, and C. Y. Chung, “Intussusception associated with Yersinia pseudotuberculosis infection,” Acta Paediatrica, International Journal of Paediatrics, vol. 85, no. 10, pp. 1253–1255, 1996.
[36]
J. W. Koo, S. N. Park, S. M. Choi et al., “Acute renal failure associated with Yersinia pseudotuberculosis infection in children,” Pediatric Nephrology, vol. 10, no. 5, pp. 582–586, 1996.
[37]
M. V. Tobin, R. E. Meigh, C. L. Smith, and I. T. Gilmore, “Yersinia pseudotuberculosis ileitis presenting with severe intestinal haemorrhage,” Journal of the Royal Society of Medicine, vol. 81, no. 7, pp. 423–424, 1988.
[38]
G. Kacerovsky-Bielesz, E. Hentschel, and M. Rotter, “Massive intestinal bleeding caused by Yersinia pseudotuberculosis,” Zeitschrift fur Gastroenterologie, vol. 18, no. 7, pp. 372–375, 1980.
[39]
E. Bülbülo？lu, H. ？iralik, B. Kantar？eken, A. ？etinkaya, M. Gül, and F. Ezberci, “Yersinia pseudotuberculosis colitis presented with severe gastrointestinal bleeding,” Turkish Journal of Gastroenterology, vol. 21, no. 2, pp. 179–182, 2010.
[40]
R. Tertti, R. Vuento, P. Mikkola, K. Granfors, A. L. Makela, and A. Toivanen, “Clinical manifestations of Yersinia pseudotuberculosis infection in children,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 8, no. 7, pp. 587–591, 1989.
[41]
H. Grant, H. Rode, and S. Cywes, “Yersinia pseudotuberculosis affecting the appendix,” Journal of Pediatric Surgery, vol. 29, no. 12, p. 1621, 1994.
[42]
A. I. Parfenov and M. D. Chizhikova, “Chronic and lingering Yersinia ileitis,” Terapevticheskii Arkhiv, vol. 74, no. 12, pp. 77–80, 2002.
[43]
L. K. Logsdon and J. Mecsas, “Requirement of the Yersinia pseudotuberculosis effectors YopH and YopE in colonization and persistence in intestinal and lymph tissues,” Infection and Immunity, vol. 71, no. 8, pp. 4595–4607, 2003.
[44]
N. S. Mair, E. Fox, and E. Thal, “Biochemical, pathogenicity and toxicity studies of type III strains of Yersinia pseudotuberculosis isolated from the cecal contents of pigs,” Contributions to Microbiology and Immunology, vol. 5, pp. 359–365, 1979.
[45]
A. G. Deacon, A. Hay, and J. Duncan, “Septicemia due to Yersinia pseudotuberculosis—a case report,” Clinical Microbiology and Infection, vol. 9, no. 11, pp. 1118–1119, 2003.
[46]
M. Nakamura, T. Shikano, and N. Ueno, “A case of Yersinia pseudotuberculosis septicemia accompanied by a large abdominal tumor,” Clinical Pediatrics, vol. 23, no. 2, pp. 121–123, 1984.
[47]
M. Macari, J. Hines, E. Balthazar, and A. Megibow, “Mesenteric adenitis: CT diagnosis of primary versus secondary causes, incidence, and clinical significance in pediatric and adult patients,” American Journal of Roentgenology, vol. 178, no. 4, pp. 853–858, 2002.
[48]
N. Konishi, K. Baba, J. Abe et al., “A case of Kawasaki disease with coronary artery aneurysms documenting Yersinia pseudotuberculosis infection,” Acta Paediatrica, International Journal of Paediatrics, vol. 86, no. 6, pp. 661–664, 1997.
[49]
B. M. Rosner, K. Stark, and D. Werber, “Epidemiology of reported Yersinia enterocolitica infections in Germany, 2001–2008,” BMC Public Health, vol. 10, article 337, 2010.
[50]
R. M. Robins-Browne, M. D. Miliotis, S. Cianciosi, V. L. Miller, S. Falkow, and J. G. Morris Jr., “Evaluation of DNA colony hybridization and other techniques for detection of virulence in Yersinia species,” Journal of Clinical Microbiology, vol. 27, no. 4, pp. 644–650, 1989.
[51]
X. Wang, Z. Cui, D. Jin et al., “Distribution of pathogenic Yersinia enterocolitica in China,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 28, no. 10, pp. 1237–1244, 2009.
[52]
A. McNally, T. Cheasty, C. Fearnley et al., “Comparison of the biotypes of Yersinia enterocolitica isolated from pigs, cattle and sheep at slaughter and from humans with yersiniosis in Great Britain during 1999-2000,” Letters in Applied Microbiology, vol. 39, no. 1, pp. 103–108, 2004.
[53]
N. R. Thomson, S. Howard, B. W. Wren et al., “The complete genome sequence and comparative genome analysis of the high pathogenicity Yersinia enterocolitica strain 8081.,” PLoS genetics, vol. 2, no. 12, article e206, 2006.
[54]
X. Wang, Y. Li, H. Jing et al., “Complete genome sequence of a Yersinia enterocolitica “old world” (3/o:9) strain and comparison with the “new world” (1B/O:8) strain,” Journal of Clinical Microbiology, vol. 49, no. 4, pp. 1251–1259, 2011.
[55]
C. Pelludat, A. Rakin, C. A. Jacobi, S. Schubert, and J. Heesemann, “The yersiniabactin biosynthetic gene cluster of Yersinia enterocolitica: organization and siderophore-dependent regulation,” Journal of Bacteriology, vol. 180, no. 3, pp. 538–546, 1998.
[56]
A. Iwobi, J. Heesemann, E. Garcia, E. Igwe, C. Noelting, and A. Rakin, “Novel virulence-associated type II secretion system unique to high-pathogenicity Yersinia enterocolitica,” Infection and Immunity, vol. 71, no. 4, pp. 1872–1879, 2003.
[57]
L. A. Lee, J. Taylor, G. P. Carter, B. Quinn, J. J. Farmer III., and R. V. Tauxe, “Yersinia enterocolitica O:3: an emerging cause of pediatric gastroenteritis in the United States,” Journal of Infectious Diseases, vol. 163, no. 3, pp. 660–663, 1991.
[58]
M. Tsubokura and S. Aleksi？, “A simplified antigenic scheme for serotyping of Yersinia pseudotuberculosis: phenotypic characterization of reference strains and preparation of O and H factor sera,” Contributions to Microbiology and Immunology, vol. 13, pp. 99–105, 1995.
[59]
H. Fukushima, M. Gomyoda, N. Hashimoto et al., “Putative origin of Yersinia pseudotuberculosis in Western and Eastern countries. A comparison of restriction endonuclease analysis of virulence plasmids,” Zentralblatt fur Bakteriologie, vol. 288, no. 1, pp. 93–102, 1998.
[60]
H. Fukushima, M. Gomyoda, and S. Kaneko, “Mice and moles inhabiting mountainous areas of Shimane Peninsula as sources of infection with Yersinia pseudotuberculosis,” Journal of Clinical Microbiology, vol. 28, no. 11, pp. 2448–2455, 1990.
[61]
H. Fukushima, M. Tsubokura, and K. Otsuki, “Epidemiological study of Yersinia enterocolitica and Yersinia pseudotuberculosis infections in Shimane Prefecture, Japan,” Zentralblatt fur Bakteriologie Mikrobiologie und Hygiene, vol. 180, no. 5-6, pp. 515–527, 1985.
[62]
T. M. Bogdanovich, E. Carniel, H. Fukushima, and M. Skurnik, “Genetic (sero) typing of Yersinia pseudotuberculosis,” Advances in Experimental Medicine and Biology, vol. 529, pp. 337–340, 2003.
[63]
H. Fukushima, Y. Matsuda, R. Seki et al., “Geographical heterogeneity between Far Eastern and western countries in prevalence of the virulence plasmid, the superantigen Yersinia pseudotuberculosis-derived mitogen, and the high-pathogenicity island among Yersinia pseudotuberculosis strains,” Journal of Clinical Microbiology, vol. 39, no. 10, pp. 3541–3547, 2001.
[64]
C. Buchrieser, R. Brosch, S. Bach, A. Guiyoule, and E. Carniel, “The high-pathogenicity island of Yersinia pseudotuberculosis can be inserted into any of the three chromosomal asn tRNA genes,” Molecular Microbiology, vol. 30, no. 5, pp. 965–978, 1998.
[65]
A. M. P. De Almeida, A. Guiyoule, I. Guilvout, I. Iteman, G. Baranton, and E. Carniel, “Chromosomal irp2 gene in Yersinia: distribution, expression, deletion and impact on virulence,” Microbial Pathogenesis, vol. 14, no. 1, pp. 9–21, 1993.
[66]
A. Rakin, P. Urbitsch, and J. Heesemann, “Evidence for two evolutionary lineages of highly pathogenic Yersinia species,” Journal of Bacteriology, vol. 177, no. 9, pp. 2292–2298, 1995.
[67]
G. R. Cornelis, T. Biot, C. Lambert de Rouvroit et al., “The Yersinia yop regulon,” Molecular Microbiology, vol. 3, no. 10, pp. 1455–1459, 1989.
[68]
C. Carnoy, C. Mullet, H. Müller-Alouf, E. Leteurtre, and M. Simonet, “Superantigen YPMa exacerbates the virulence of Yersinia pseudotuberculosis in mice,” Infection and Immunity, vol. 68, no. 5, pp. 2553–2559, 2000.
[69]
E. Carniel, “The Yersinia high-pathogenicity island,” International Microbiology, vol. 2, no. 3, pp. 161–167, 1999.
[70]
J. Abe and T. Takeda, “Characterization of a superantigen produced by Yersinia pseudotuberculosis,” Preparative Biochemistry and Biotechnology, vol. 27, no. 2-3, pp. 173–208, 1997.
[71]
H. Ueshiba, H. Kato, T. Miyoshi-Akiyama et al., “Analysis of the superantigen-producing ability of Yersinia pseudotuberculosis strains of various serotypes isolated from patients with systemic or gastroenteric infections, wildlife animals and natural environments,” Zentralblatt fur Bakteriologie, vol. 288, no. 2, pp. 277–291, 1998.
[72]
K. I. Yoshino, T. Ramamurthy, G. B. Nair et al., “Geographical heterogeneity between Far East and Europe in prevalence of ypm gene encoding the novel superantigen among Yersinia pseudotuberculosis strains,” Journal of Clinical Microbiology, vol. 33, no. 12, pp. 3356–3358, 1995.
[73]
T. Bergsbaken and B. T. Cookson, “Innate immune response during Yersinia infection: critical modulation of cell death mechanisms through phagocyte activation,” Journal of Leukocyte Biology, vol. 86, no. 5, pp. 1153–1158, 2009.
[74]
F. Sebbane, D. Gardner, D. Long, B. B. Gowen, and B. J. Hinnebusch, “Kinetics of disease progression and host response in a rat model of bubonic plague,” American Journal of Pathology, vol. 166, no. 5, pp. 1427–1439, 2005.
[75]
T. Bergsbaken and B. T. Cookson, “Macrophage activation redirects yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis,” PLoS Pathogens, vol. 3, no. 11, article e161, 2007.
[76]
F. Guinet, P. Avé, L. Jones, M. Huerre, and E. Carniel, “Defective innate cell response and lymph node infiltration specify Yersinia pestis infection,” PLoS ONE, vol. 3, no. 2, Article ID e1688, 2008.
[77]
R. R. Brubaker, “Factors promoting acute and chronic diseases caused by yersiniae,” Clinical Microbiology Reviews, vol. 4, no. 3, pp. 309–324, 1991.
[78]
P. Gemski, J. R. Lazere, T. Casey, and J. A. Wohlhieter, “Presence of a virulence-associated plasmid in Yersinia pseudotuberculosis,” Infection and Immunity, vol. 28, no. 3, pp. 1044–1047, 1980.
[79]
D. A. Portnoy and S. Falkow, “Virulence-associated plasmids from Yersinia enterocolitica and Yersinia pestis,” Journal of Bacteriology, vol. 148, no. 3, pp. 877–883, 1981.
[80]
A. M. Gehring, E. DeMoll, J. D. Fetherston et al., “Iron acquisition in plague: modular logic in enzymatic biogenesis of yersiniabactin by Yersinia pestis,” Chemistry and Biology, vol. 5, no. 10, pp. 573–586, 1998.
[81]
A. Rakin, C. Noelting, S. Schubert, and J. Heesemann, “Common and specific characteristics of the high-pathogenicity island of Yersinia enterocolitica,” Infection and Immunity, vol. 67, no. 10, pp. 5265–5274, 1999.
[82]
J. D. Fetherston, S. W. Bearden, and R. D. Perry, “YbtA, an AraC-type regulator of the Yersinia pestis pesticin/yersiniabactin receptor,” Molecular Microbiology, vol. 22, no. 2, pp. 315–325, 1996.
[83]
J. Heesemann, K. Hantke, T. Vocke a et al., “Virulence of Yersinia enterocolitica is closely associated with siderophore production, expression of an iron-repressible outer membrane polypeptide of 65,000 Da and pesticin sensitivity,” Molecular Microbiology, vol. 8, no. 2, pp. 397–408, 1993.
[84]
E. Carniel, “The Yersinia high-pathogenicity island: an iron-uptake island,” Microbes and Infection, vol. 3, no. 7, pp. 561–569, 2001.
[85]
E. Carniel, I. Guilvout, and M. Prentice, “Characterization of a large chromosomal “high-pathogenicity island“ in biotype 1B Yersinia enterocolitica,” Journal of Bacteriology, vol. 178, no. 23, pp. 6743–6751, 1996.
[86]
J. Abe, T. Takeda, Y. Watanabe et al., “Evidence for superantigen production by Yersinia pseudotuberculosis,” Journal of Immunology, vol. 151, no. 8, pp. 4183–4188, 1993.
[87]
T. Uchiyama, T. Miyoshi-Akiyama, H. Kato, W. Fujimaki, K. Imanishi, and X. J. Yan, “Superantigenic properties of a novel mitogenic substance produced by Yersinia pseudotuberculosis isolated from patients manifesting acute and systemic symptoms,” Journal of Immunology, vol. 151, no. 8, pp. 4407–4413, 1993.
[88]
T. Ramamurthy, K. I. Yoshino, J. Abe, N. Ikeda, and T. Takeda, “Purification, characterization and cloning of a novel variant of the superantigen Yersinia pseudoturberculosis-derived mitogen,” FEBS Letters, vol. 413, no. 1, pp. 174–176, 1997.
[89]
C. Carnoy, S. Floquet, M. Marceau et al., “The superantigen gene ypm is located in an unstable chromosomal locus of Yersinia pseudotuberculosis,” Journal of Bacteriology, vol. 184, no. 16, pp. 4489–4499, 2002.
[90]
C. A. Schiano, L. E. Bellows, and W. W. Lathem, “The small RNA chaperone Hfq is required for the virulence of Yersinia pseudotuberculosis,” Infection and Immunity, vol. 78, no. 5, pp. 2034–2044, 2010.
[91]
H. Nakao, H. Watanabe, S. I. Nakayama, and T. Takeda, “Yst gene expression in Yersinia enterocolitica is positively regulated by a chromosomal region that is highly homologous to Escherichia coli host factor 1 gene (hfq),” Molecular Microbiology, vol. 18, no. 5, pp. 859–865, 1995.
[92]
E. A. Groisman, “The pleiotropic two-component regulatory system PhoP-PhoQ,” Journal of Bacteriology, vol. 183, no. 6, pp. 1835–1842, 2001.
[93]
J. P. Grabenstein, M. Marceau, C. Pujol, M. Simonet, and J. B. Bliska, “The response regulator PhoP of Yersinia pseudotuberculosis is important for replication in macrophages and for virulence,” Infection and Immunity, vol. 72, no. 9, pp. 4973–4984, 2004.
[94]
P. C. F. Oyston, N. Dorrell, K. Williams et al., “The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis,” Infection and Immunity, vol. 68, no. 6, pp. 3419–3425, 2000.
[95]
R. Rebeil, R. K. Ernst, B. B. Gowen, S. I. Miller, and B. J. Hinnebusch, “Variation in lipid A structure in the pathogenic yersiniae,” Molecular Microbiology, vol. 52, no. 5, pp. 1363–1373, 2004.
[96]
O. L. Champion, A. V. Karlyshev, I. A. Cooper, et al., “Yersinia pseudotuberculosis mntH functions in intracellular manganese accumulation that is essential for virulence and survival in cells expressing functional Nramp1,” Microbiology, vol. 157, part 4, pp. 1115–1122, 2011.
[97]
H. Matsumoto and G. M. Young, “Translocated effectors of Yersinia,” Current Opinion in Microbiology, vol. 12, no. 1, pp. 94–100, 2009.
[98]
D. W. Ellison, M. B. Lawrenz, and V. L. Miller, “Invasin and beyond: regulation of Yersinia virulence by RovA,” Trends in Microbiology, vol. 12, no. 6, pp. 296–300, 2004.
[99]
D. W. Ellison, B. Young, K. Nelson, and V. L. Miller, “YmoA negatively regulates expression of invasin from Yersinia enterocolitica,” Journal of Bacteriology, vol. 185, no. 24, pp. 7153–7159, 2003.
[100]
D. W. Ellison and V. L. Miller, “H-NS represses inv transcription in Yersinia enterocolitica through competition with RovA and interaction with YmoA,” Journal of Bacteriology, vol. 188, no. 14, pp. 5101–5112, 2006.
[101]
D. W. Ellison and V. L. Miller, “Regulation of virulence by members of the MarR/SlyA family,” Current Opinion in Microbiology, vol. 9, no. 2, pp. 153–159, 2006.
[102]
G. Nagel, A. Lahrz, and P. Dersch, “Environmental control of invasin expression in Yersinia pseudotuberculosis is mediated by regulation of RovA, a transcriptional activator of the SlyA/Hor family,” Molecular Microbiology, vol. 41, no. 6, pp. 1249–1269, 2001.
[103]
P. A. Revell and V. L. Miller, “A chromosomally encoded regulator is required for expression of the Yersinia enterocolitica inv gene and for virulence,” Molecular Microbiology, vol. 35, no. 3, pp. 677–685, 2000.
[104]
G. Balligand, Y. Laroche, and G. Cornelis, “Genetic analysis of virulence plasmid from a serogroup 9 Yersinia enterocolitica strain: role of outer membrane protein P1 in resistance to human serum and autoagglutination,” Infection and Immunity, vol. 48, no. 3, pp. 782–786, 1985.
[105]
T. Heise and P. Dersch, “Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrix-specific cell adhesion and uptake,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 9, pp. 3375–3380, 2006.
[106]
R. J. Martinez, “Thermoregulation-dependent expression of Yersinia enterocolitica protein 1 imparts serum resistance to Escherichia coli K-12,” Journal of Bacteriology, vol. 171, no. 7, pp. 3732–3739, 1989.
[107]
G. R. Cornelis and H. Wolf-Watz, “The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells,” Molecular Microbiology, vol. 23, no. 5, pp. 861–867, 1997.
[108]
M. Skurnik and P. Toivanen, “LcrF is the temperature-regulated activator of the yadA gene of Yersinia enterocolitica and Yersinia pseudotuberculosis,” Journal of Bacteriology, vol. 174, no. 6, pp. 2047–2051, 1992.
[109]
J. C. Pepe, M. R. Wachtel, E. Wagar, and V. L. Miller, “Pathogenesis of defined invasion mutants of Yersinia enterocolitica in a BALB/c mouse model of infection,” Infection and Immunity, vol. 63, no. 12, pp. 4837–4848, 1995.
[110]
I. Bolin and H. Wolf Watz, “Molecular cloning of the temperature-inducible outer membrane protein 1 of Yersinia pseudotuberculosis,” Infection and Immunity, vol. 43, no. 1, pp. 72–78, 1984.
[111]
Y. W. Han and V. L. Miller, “Reevaluation of the virulence phenotype of the inv yada double mutants of Yersinia pseudotuberculosis,” Infection and Immunity, vol. 65, no. 1, pp. 327–330, 1997.
[112]
R. Rosqvist, M. Skurnik, and H. Wolf-Watz, “Increased virulence of Yersinia pseudotuberculosis by two independent mutations,” Nature, vol. 334, no. 6182, pp. 522–525, 1988.
[113]
J. Eitel, T. Heise, U. Thiesen, and P. Dersch, “Cell invasion and IL-8 production pathways initiated by YadA of Yersinia pseudotuberculosis require common signalling molecules (FAK, c-Src, Ras) and distinct cell factors,” Cellular Microbiology, vol. 7, no. 1, pp. 63–77, 2005.
[114]
Y. Schmid, G. A. Grassl, O. T. Bühler, M. Skurnik, I. B. Autenrieth, and E. Bohn, “Yersinia enterocolitica adhesin A induces production of interleukin-8 in epithelial cells,” Infection and Immunity, vol. 72, no. 12, pp. 6780–6789, 2004.
[115]
O. Laitenen, J. Tuuhea, and P. Ahvonen, “Polyarthritis associated with Yersinia enterocolitica infection. Clinical features and laboratory findings in nine cases with severe joint symptoms,” Annals of the Rheumatic Diseases, vol. 31, no. 1, pp. 34–39, 1972.
[116]
O. Laitinen, M. Leirisalo, and G. Skylv, “Relation between HLA-B27 and clinical features in patients with yersinia arthritis,” Arthritis and Rheumatism, vol. 20, no. 5, pp. 1121–1124, 1977.
[117]
R. Lahesmaa, E. Eerola, and A. Toivanen, “Does reduced erythrocyte C3b receptor (CR1) activity contribute to the pathogenesis of yersinia triggered reactive arthritis?” Annals of the Rheumatic Diseases, vol. 51, no. 1, pp. 97–100, 1992.
[118]
R. Lahesmaa, H. Yssel, S. Batsford et al., “Yersinia enterocolitica activates a T helper type 1-like T cell subset in reactive arthritis,” Journal of Immunology, vol. 148, no. 10, pp. 3079–3085, 1992.
[119]
M. Skurnik, “Role of YadA in Yersinia-enterocolitica-induced reactive arthritis: a hypothesis,” Trends in Microbiology, vol. 3, no. 8, pp. 318–319, 1995.
[120]
M. Biedzka-Sarek, H. Jarva, H. Hyyti？inen, S. Meri, and M. Skurnik, “Characterization of complement factor H binding to Yersinia enterocolitica serotype O:3,” Infection and Immunity, vol. 76, no. 9, pp. 4100–4109, 2008.
[121]
M. Biedzka-Sarek, S. Salmenlinna, M. Gruber, A. N. Lupas, S. Meri, and M. Skurnik, “Functional mapping of YadA- and Ail-mediated binding of human factor H to Yersinia enterocolitica serotype O:3,” Infection and Immunity, vol. 76, no. 11, pp. 5016–5027, 2008.
[122]
M. Biedzka-Sarek, R. Venho, and M. Skurnik, “Role of YadA, Ail, and lipopolysaccharide in serum resistance of Yersinia enterocolitica serotype O:3,” Infection and Immunity, vol. 73, no. 4, pp. 2232–2244, 2005.
[123]
V. Kirjavainen, H. Jarva, M. Biedzka-Sarek, A. M. Blom, M. Skurnik, and S. Meri, “Yersinia enterocoliticaserum resistance proteins YadA and ail bind the complement regulator C4b-binding protein,” PLoS Pathogens, vol. 4, no. 8, Article ID e1000140, 2008.
[124]
F. Pouillot, C. Fayolle, and E. Carniel, “A putative DNA adenine methyltransferase is involved in Yersinia pseudotuberculosis pathogenicity,” Microbiology, vol. 153, no. 8, pp. 2426–2434, 2007.
[125]
Y. Hu, P. Lu, Y. Zhang, L. Li, and S. Chen, “Characterization of an aspartate-dependent acid survival system in Yersinia pseudotuberculosis,” FEBS Letters, vol. 584, no. 11, pp. 2311–2314, 2010.
[126]
B. Riot, P. Berche, and M. Simonet, “Urease is not involved in the virulence of Yersinia pseudotuberculosis in mice,” Infection and Immunity, vol. 65, no. 5, pp. 1985–1990, 1997.
[127]
M. Lavander, S. K. Ericsson, J. E. Br？ms, and A. Forsberg, “The twin arginine translocation system is essential for virulence of Yersinia pseudotuberculosis,” Infection and Immunity, vol. 74, no. 3, pp. 1768–1776, 2006.
[128]
C. Flamez, I. Ricard, S. Arafah, M. Simonet, and M. Marceau, “Phenotypic analysis of Yersinia pseudotuberculosis 32777 response regulator mutants: new insights into two-component system regulon plasticity in bacteria,” International Journal of Medical Microbiology, vol. 298, no. 3-4, pp. 193–207, 2008.
[129]
Y. Hu, P. Lu, Y. Wang, L. Ding, S. Atkinson, and S. Chen, “OmpR positively regulates urease expression to enhance acid survival of Yersinia pseudotuberculosis,” Microbiology, vol. 155, no. 8, pp. 2522–2531, 2009.
[130]
Y. Hu, P. Lu, Y. Zhang et al., “Cra negatively regulates acid survival in Yersinia pseudotuberculosis,” FEMS Microbiology Letters, vol. 317, no. 2, pp. 190–195, 2011.
[131]
G. R. Cornelis, “The type III secretion injectisome,” Nature Reviews Microbiology, vol. 4, no. 11, pp. 811–825, 2006.
[132]
M. Quinaud, J. Chabert, E. Faudry et al., “The PscE-PscF-PscG complex controls type III secretion needle biogenesis in Pseudomonas aeruginosa,” Journal of Biological Chemistry, vol. 280, no. 43, pp. 36293–36300, 2005.
[133]
G. R. Cornelis, “Yersinia type III secretion: send in the effectors,” Journal of Cell Biology, vol. 158, no. 3, pp. 401–408, 2002.
[134]
J. E. Trosky, A. D. B. Liverman, and K. Orth, “Yersinia outer proteins: Yops,” Cellular Microbiology, vol. 10, no. 3, pp. 557–565, 2008.
[135]
J. Eitel and P. Dersch, “The YadA protein of Yersinia pseudotuberculosis mediates high-efficiency uptake into human cells under environmental conditions in which invasin is repressed,” Infection and Immunity, vol. 70, no. 9, pp. 4880–4891, 2002.
[136]
R. R. Isberg and J. M. Leong, “Multiple β1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells,” Cell, vol. 60, no. 5, pp. 861–871, 1990.
[137]
E. Mejía, J. B. Bliska, and G. I. Viboud, “Yersinia controls type III effector delivery into host cells by modulating Rho activity,” PLoS Pathogens, vol. 4, no. 1, article 3, 2008.
[138]
S. Mohammadi and R. R. Isberg, “Yersinia pseudotuberculosis virulence determinants invasin, YopE, and YopT modulate RhoG activity and localization,” Infection and Immunity, vol. 77, no. 11, pp. 4771–4782, 2009.
[139]
J. Pettersson, R. Nordfelth, E. Dubinina et al., “Modulation of virulence factor expression by pathogen target cell contact,” Science, vol. 273, no. 5279, pp. 1231–1233, 1996.
[140]
V. L. Motin, A. M. Georgescu, J. P. Fitch et al., “Temporal global changes in gene expression during temperature transition in Yersinia pestis,” Journal of Bacteriology, vol. 186, no. 18, pp. 6298–6305, 2004.
[141]
S. C. Straley and R. D. Perry, “Environmental modulation of gene expression and pathogenesis in Yersinia,” Trends in Microbiology, vol. 3, no. 8, pp. 310–317, 1995.
[142]
S. C. Straley, G. V. Plano, E. Skrzypek, P. L. Haddix, and K. A. Fields, “Regulation by Ca2+ in the Yersinia low-Ca2+ response,” Molecular Microbiology, vol. 8, no. 6, pp. 1005–1010, 1993.
[143]
G. R. Cornelis, A. Boland, A. P. Boyd et al., “The virulence plasmid of Yersinia, an antihost genome,” Microbiology and Molecular Biology Reviews, vol. 62, no. 4, pp. 1315–1352, 1998.
[144]
G. I. Viboud and J. B. Bliska, “Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis,” Annual Review of Microbiology, vol. 59, pp. 69–89, 2005.
[145]
H. Shin and G. R. Cornelis, “Type III secretion translocation pores of Yersinia enterocolitica trigger maturation and release of pro-inflammatory IL-1β,” Cellular Microbiology, vol. 9, no. 12, pp. 2893–2902, 2007.
[146]
V. Petrilli, S. Papin, and J. Tschopp, “The inflammasome,” Current Biology, vol. 15, no. 15, p. R581, 2005.
[147]
F. L. van de Veerdonk, M. G. Netea, C. A. Dinarello, and L. A. Joosten, “Inflammasome activation and IL-1beta and IL-18 processing during infection,” Trends in Immunology, vol. 32, no. 3, pp. 110–116, 2011.
[148]
E. A. Miao, I. A. Leaf, P. M. Treuting et al., “Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria,” Nature Immunology, vol. 11, no. 12, pp. 1136–1142, 2010.
[149]
K. Hoebe, X. Du, P. Georgel et al., “Identification of Lps2 as a key transducer of MyD88-independent TIR signalling,” Nature, vol. 424, no. 6950, pp. 743–748, 2003.
[150]
K. Ruckdeschel, G. Pfaffinger, R. Haase et al., “Signaling of apoptosis through TLRs critically involves toll/IL-1 receptor domain-containing adapter inducing IFN-β, but not MyD88, in bacteria-infected murine macrophages,” Journal of Immunology, vol. 173, no. 5, pp. 3320–3328, 2004.
[151]
M. Karin and A. Lin, “NF-κB at the crossroads of life and death,” Nature Immunology, vol. 3, no. 3, pp. 221–227, 2002.
[152]
J. M. Park, F. R. Greten, A. Wong et al., “Signaling pathways and genes that inhibit pathogen-induced macrophage apoptosis - CREB and NF-κB as key regulators,” Immunity, vol. 23, no. 3, pp. 319–329, 2005.
[153]
Y. Zhang, A. T. Ting, K. B. Marcu, and J. B. Bliska, “Inhibition of MAPK and NF-κB pathways is necessary for rapid apoptosis in macrophages infected with Yersinia,” Journal of Immunology, vol. 174, no. 12, pp. 7939–7949, 2005.
[154]
L. E. Palmer, S. Hobble, J. E. Galán, and J. B. Bliska, “YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF-α production and downregulation of the MAP kinases p38 and JNK,” Molecular Microbiology, vol. 27, no. 5, pp. 953–965, 1998.
[155]
K. Schesser, A. K. Spiik, J. M. Dukuzumuremyi, M. F. Neurath, S. Pettersson, and H. Wolf-Watz, “The yopJ locus is required for Yersinia-mediated inhibition of NF-κB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity,” Molecular Microbiology, vol. 28, no. 6, pp. 1067–1079, 1998.
[156]
G. Denecker, W. Declercq, C. A. W. Geuijen et al., “Yersinia enterocolitica YopP-induced apoptosis of macrophages involves the apoptotic signaling cascade upstream of bid,” Journal of Biological Chemistry, vol. 276, no. 23, pp. 19706–19714, 2001.
[157]
K. Orth, L. E. Palmer, Z. Q. Bao et al., “Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector,” Science, vol. 285, no. 5435, pp. 1920–1923, 1999.
[158]
A. Boland and G. R. Cornelis, “Role of YopP in suppression of tumor necrosis factor alpha release by macrophages during Yersinia infection,” Infection and Immunity, vol. 66, no. 5, pp. 1878–1884, 1998.
[159]
G. Denecker, S. T？temeyer, L. J. Mota et al., “Effect of low- and high-virulence Yersinia enterocolitica strains on the inflammatory response of human umbilical vein endothelial cells,” Infection and Immunity, vol. 70, no. 7, pp. 3510–3520, 2002.
[160]
S. Gr？bner, S. E. Autenrieth, I. Soldanova et al., “Yersinia YopP-induced apoptotic cell death in murine dendritic cells is partially independent from action of caspases and exhibits necrosis-like features,” Apoptosis, vol. 11, no. 11, pp. 1959–1968, 2006.
[161]
S. Gr？bner, I. Adkins, S. Schulz et al., “Catalytically active Yersinia outer protein P induces cleavage of RIP and caspase-8 at the level of the DISC independently of death receptors in dendritic cells,” Apoptosis, vol. 12, no. 10, pp. 1813–1825, 2007.
[162]
S. E. Erfurth, S. Gr？bner, U. Kramer et al., “Yersinia enterocolitica induces apoptosis and inhibits surface molecule expression and cytokine production in murine dendritic cells,” Infection and Immunity, vol. 72, no. 12, pp. 7045–7054, 2004.
[163]
S. Bedoui, A. Kupz, O. L. Wijburg, A. K. Walduck, M. Rescigno, and R. A. Strugnell, “Different bacterial pathogens, different strategies, yet the aim is the same: evasion of intestinal dendritic cell recognition,” Journal of Immunology, vol. 184, no. 5, pp. 2237–2242, 2010.
[164]
K. Trülzsch, G. Geginat, T. Sporleder et al., “Yersinia outer protein P inhibits CD8 T cell priming in the mouse infection model,” Journal of Immunology, vol. 174, no. 7, pp. 4244–4251, 2005.
[165]
S. E. Autenrieth, I. Soldanova, R. R？semann et al., “Yersinia enterocolitica YopP inhibits MAP kinase-mediated antigen uptake in dendritic cells,” Cellular Microbiology, vol. 9, no. 2, pp. 425–437, 2007.
[166]
A. Fahlgren, L. Westermark, K. Akopyan, and M. F？llman, “Cell type-specific effects of Yersinia pseudotuberculosis virulence effectors,” Cellular Microbiology, vol. 11, no. 12, pp. 1750–1767, 2009.
[167]
L. K. Garrity-Ryan, O. K. Kim, J. M. Balada-Llasat et al., “Small molecule inhibitors of LcrF, a Yersinia pseudotuberculosis transcription factor, attenuate virulence and limit infection in a murine pneumonia model,” Infection and Immunity, vol. 78, no. 11, pp. 4683–4690, 2010.
[168]
R. R. Brubaker, “Interleukin-10 and inhibition of innate immunity to Yersiniae: roles of Yops and LcrV (V antigen),” Infection and Immunity, vol. 71, no. 7, pp. 3673–3681, 2003.
[169]
R. Rosqvist, A. Forsberg, M. Rimpilainen, T. Bergman, and H. Wolf-Watz, “The cytotoxic protein YopE of Yersinia obstructs the primary host defence,” Molecular Microbiology, vol. 4, no. 4, pp. 657–667, 1990.
[170]
D. S. Black and J. B. Bliska, “The RhoGAP activity of the Yersinia pseudotuberculosis cytotoxin YopE is required for antiphagocytic function and virulence,” Molecular Microbiology, vol. 37, no. 3, pp. 515–527, 2000.
[171]
U. Von Pawel-Rammingen, M. V. Telepnev, G. Schmidt, K. Aktories, H. Wolf-Watz, and R. Rosqvist, “GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure,” Molecular Microbiology, vol. 36, no. 3, pp. 737–748, 2000.
[172]
M. Iriarte and G. R. Cornelis, “YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells,” Molecular Microbiology, vol. 29, no. 3, pp. 915–929, 1998.
[173]
F. Shao, P. M. Merritt, Z. Bao, R. W. Innes, and J. E. Dixon, “A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis,” Cell, vol. 109, no. 5, pp. 575–588, 2002.
[174]
E. E. Galyov, S. Hakansson, A. Forsberg, and H. Wolf-Watz, “A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant,” Nature, vol. 361, no. 6414, pp. 730–732, 1993.
[175]
J. M. Dukuzumuremyi, R. Rosqvist, B. Hallberg, B. ？kerstr？m, H. Wolf-Watz, and K. Schesser, “The Yersinia protein kinase A is a host factor inducible RhoA/Rac-binding virulence factor,” Journal of Biological Chemistry, vol. 275, no. 45, pp. 35281–35290, 2000.
[176]
S. J. Juris, A. E. Rudolph, D. Huddler, K. Orth, and J. E. Dixon, “A distinctive role for the Yersinia protein kinase: actin binding, kinase activation, and cytoskeleton disruption,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 17, pp. 9431–9436, 2000.
[177]
N. Sauvonnet, B. Pradet-Balade, J. A. Garcia-Sanz, and G. R. Cornelis, “Regulation of mRNA expression in macrophages after Yersinia enterocolitica infection,” Journal of Biological Chemistry, vol. 277, no. 28, pp. 25133–25142, 2002.
[178]
T. Yao, J. Mecsas, J. I. Healy, S. Falkow, and Y. H. Chien, “Suppression of T and B lymphocyte activation by a Yersinia pseudotuberculosis virulence factor, YopH,” Journal of Experimental Medicine, vol. 190, no. 9, pp. 1343–1350, 1999.
[179]
A. Alonso, N. Bottini, S. Bruckner et al., “Lck dephosphorylation at Tyr-394 and inhibition of T cell antigen receptor signaling by Yersinia Phosphatase YopH,” Journal of Biological Chemistry, vol. 279, no. 6, pp. 4922–4928, 2004.
[180]
K. Trülzsch, T. Sporleder, E. I. Igwe, H. Rüssmann, and J. Heesemann, “Contribution of the major secreted Yops of Yersinia enterocolitica O:8 to pathogenicity in the mouse infection model,” Infection and Immunity, vol. 72, no. 9, pp. 5227–5234, 2004.
[181]
A. Boland, M. P. Sory, M. Iriarte, C. Kerbourch, P. Wattiau, and G. R. Cornelis, “Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y. enterocolitica is internalized inside the cytosol of PU5-1.8 macrophages by the YopB, D, N delivery apparatus,” EMBO Journal, vol. 15, no. 19, pp. 5191–5201, 1996.
[182]
G. Heusipp, K. M. Nelson, M. A. Schmidt, and V. L. Miller, “Regulation of htrA expression in Yersinia enterocolitica,” FEMS Microbiology Letters, vol. 231, no. 2, pp. 227–235, 2004.
[183]
M. Hentschke, L. Berneking, C. B. Campos, F. Buck, K. Ruckdeschel, and M. Aepfelbacher, “Yersinia virulence factor YopM induces sustained RSK activation by interfering with dephosphorylation,” PLoS ONE, vol. 5, no. 10, Article ID e13165, 2010.
[184]
M. W. McCoy, M. L. Marré, C. F. Lesser, and J. Mecsas, “The C-terminal tail of Yersinia pseudotuberculosis YopM is critical for interacting with RSK1 and for virulence,” Infection and Immunity, vol. 78, no. 6, pp. 2584–2598, 2010.
[185]
J. B. McPhee, P. Mena, and J. B. Bliska, “Delineation of regions of the Yersinia YopM protein required for interaction with the RSK1 and PRK2 host kinases and their requirement for interleukin-10 production and virulence,” Infection and Immunity, vol. 78, no. 8, pp. 3529–3539, 2010.
[186]
J. C. Haller, S. Carlson, K. J. Pederson, and D. E. Pierson, “A chromosomally encoded type III secretion pathway in Yersinia enterocolitica is important in virulence,” Molecular Microbiology, vol. 36, no. 6, pp. 1436–1446, 2000.
[187]
G. M. Young, M. J. Smith, S. A. Minnich, and V. L. Miller, “The Yersinia enterocolitica motility master regulatory operon, flhDC, is required for flagellin production, swimming motility, and swarming motility,” Journal of Bacteriology, vol. 181, no. 9, pp. 2823–2833, 1999.
[188]
S. Mildiner-Earley, V. L. Miller, and K. A. Walker, “Environmental stimuli affecting expression of the Ysa type three secretion locus,” Advances in Experimental Medicine and Biology, vol. 603, pp. 211–216, 2007.
[189]
K. A. Walker and V. L. Miller, “Regulation of the Ysa type III secretion system of Yersinia enterocolitica by YsaE/SycB and YsrS/YsrR,” Journal of Bacteriology, vol. 186, no. 13, pp. 4056–4066, 2004.
[190]
K. Venecia and G. M. Young, “Environmental regulation and virulence attributes of the Ysa type III secretion system of Yersinia enterocolitica biovar 1B,” Infection and Immunity, vol. 73, no. 9, pp. 5961–5977, 2005.
[191]
H. Matsumoto and G. M. Young, “Proteomic and functional analysis of the suite of Ysp proteins exported by the Ysa type III secretion system of Yersinia enterocolitica Biovar 1B,” Molecular Microbiology, vol. 59, no. 2, pp. 689–706, 2006.
[192]
D. H. Schmiel, G. M. Young, and V. L. Miller, “The Yersinia enterocolitica phospholipase gene yplA is part of the flagellar regulon,” Journal of Bacteriology, vol. 182, no. 8, pp. 2314–2320, 2000.
[193]
W. Zhang, S. Xu, J. Li, X. Shen, Y. Wang, and Z. Yuan, “Modulation of a thermoregulated type VI secretion system by ahl-dependent quorum sensing in Yersinia pseudotuberculosis,” Archives of Microbiology, vol. 193, no. 5, pp. 351–363, 2011.
[194]
F. Collyn, M. A. Léty, S. Nair et al., “Yersinia pseudotuberculosis harbors a type IV pilus gene cluster that contributes to pathogenicity,” Infection and Immunity, vol. 70, no. 11, pp. 6196–6205, 2002.
[195]
J. M. Balada-Llasat and J. Mecsas, “Yersinia has a tropism for B and T cell zones of lymph nodes that is independent of the type III secretion system.,” PLoS Pathogens, vol. 2, no. 9, article e86, 2006.
[196]
I. B. Autenrieth, P. Hantschmann, B. Heymer, and J. Heesemann, “Immunohistological characterization of the cellular immune response against Yersinia enterocolitica in mice: evidence for the involvement of T lymphocytes,” Immunobiology, vol. 187, no. 1-2, pp. 1–16, 1993.
[197]
P. H. Dube, P. A. Revell, D. D. Chaplin, R. G. Lorenz, and V. L. Miller, “A role for IL-1α in inducing pathologic inflammation during bacterial infection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 19, pp. 10880–10885, 2001.
[198]
S. A. Handley, P. H. Dube, P. A. Revell, and V. L. Miller, “Characterization of Oral Yersinia enterocolitica infection in three different strains of inbred mice,” Infection and Immunity, vol. 72, no. 3, pp. 1645–1656, 2004.
[199]
W. W. Lathem, S. D. Crosby, V. L. Miller, and W. E. Goldman, “Progression of primary pneumonic plague: a mouse model of infection, pathology, and bacterial transcriptional activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 49, pp. 17786–17791, 2005.
[200]
J. M. Balada-Llasat, B. Panilaitis, D. Kaplan, and J. Mecsas, “Oral inoculation with Type III secretion mutants of Yersinia pseudotuberculosis provides protection from oral, intraperitoneal, or intranasal challenge with virulent Yersinia,” Vaccine, vol. 25, no. 8, pp. 1526–1533, 2007.
[201]
E. L. Hartland, A. M. Bordun, and R. M. Robins-Browne, “Contribution of YopB to virulence of Yersinia enterocolitica,” Infection and Immunity, vol. 64, no. 6, pp. 2308–2314, 1996.
[202]
T. Une and R. R. Brubaker, “In vivo comparison of avirulent Vwa- and Pgm- of Pst(r) phenotypes of Yersiniae,” Infection and Immunity, vol. 43, no. 3, pp. 895–900, 1984.
[203]
N. A. Okan, P. Mena, J. L. Benach, J. B. Bliska, and A. W. Karzai, “The smpB-ssrA mutant of Yersinia pestis functions as a live attenuated vaccine to protect mice against pulmonary plague infection,” Infection and Immunity, vol. 78, no. 3, pp. 1284–1293, 2010.
[204]
J. A. Rosenzweig, O. Jejelowo, J. Sha, et al., “Progress on plague vaccine development,” Applied Microbiology and Biotechnology, vol. 91, no. 2, pp. 265–286, 2011.
[205]
H. Rüssmann, K. Panthel, B. K？hn et al., “Alternative endogenous protein processing via an autophagy-dependent pathway compensates for Yersinia-mediated inhibition of endosomal major histocompatibility complex class II antigen presentation,” Infection and Immunity, vol. 78, no. 12, pp. 5138–5150, 2010.
[206]
A. Deuretzbacher, N. Czymmeck, R. Reimer et al., “β1 integrin-dependent engulfment of Yersinia enterocolitica by macrophages is coupled to the activation of autophagy and suppressed by type III protein secretion,” Journal of Immunology, vol. 183, no. 9, pp. 5847–5860, 2009.
[207]
K. Moreau, S. Lacas-Gervais, N. Fujita et al., “Autophagosomes can support Yersinia pseudotuberculosis replication in macrophages,” Cellular Microbiology, vol. 12, no. 8, pp. 1108–1123, 2010.
[208]
I. B. Autenrieth, A. Tingle, A. Reske-Kunz, and J. Heesemann, “T lymphocytes mediate protection against Yersinia enterocolitica in mice: characterization of murine T-cell clones specific for Y. enterocolitica,” Infection and Immunity, vol. 60, no. 3, pp. 1140–1149, 1992.
[209]
E. Bohn, E. Schmitt, C. Bielfeldt, A. Noll, R. Schulte, and I. B. Autenrieth, “Ambiguous role of interleukin-12 in Yersinia enterocolitica infection in susceptible and resistant mouse strains,” Infection and Immunity, vol. 66, no. 5, pp. 2213–2220, 1998.
[210]
E. Bohn, J. Heesemann, S. Ehlers, and I. B. Autenrieth, “Early gamma interferon mRNA expression is associated with resistance of mice against Yersinia enterocolitica,” Infection and Immunity, vol. 62, no. 7, pp. 3027–3032, 1994.
[211]
E. Bohn and I. B. Autenrieth, “IL-12 is essential for resistance against Yersinia enterocolitica by triggering IFN-γ production in NK cells and CD4+ T cells,” Journal of Immunology, vol. 156, no. 4, pp. 1458–1468, 1996.
[212]
I. B. Autenrieth and J. Heesemann, “In vivo neutralization of tumor necrosis factor-alpha and interferon-gamma abrogates resistance to Yersinia enterocolitica infection in mice,” Medical Microbiology and Immunology, vol. 181, no. 6, pp. 333–338, 1992.
[213]
S. E. Autenrieth, T.-R. Linzer, C. Hiller et al., “Immune evasion by Yersinia enterocolitica: differential targeting of dendritic cell subpopulations in vivo,” PLoS Pathogens, vol. 6, no. 11, Article ID e1001212, 2010.
[214]
E. M. Ribot, M. A. Fair, R. Gautom et al., “Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet,” Foodborne Pathogens and Disease, vol. 3, no. 1, pp. 59–67, 2006.
[215]
K. Asplund, T. Johansson, and A. Siitonen, “Evaluation of pulsed-field gel electrophoresis of genomic restriction fragments in the discrimination of Yersinia enterocolitica O:3,” Epidemiology and Infection, vol. 121, no. 3, pp. 579–586, 1998.
[216]
I. Iteman, A. Guiyoule, and E. Carniel, “Comparison of three molecular methods for typing and subtyping pathogenic Yersinia enterocolitica strains,” Journal of Medical Microbiology, vol. 45, no. 1, pp. 48–56, 1996.
[217]
H. Najdenski, I. Iteman, and E. Carniel, “Efficient subtyping of pathogenic Yersinia enterocolitica strains by pulsed-field gel electrophoresis,” Journal of Clinical Microbiology, vol. 32, no. 12, pp. 2913–2920, 1994.
[218]
P. Thoerner, C. I.B. Kingombe, K. B？gli-Stuber et al., “PCR detection of virulence genes in Yersinia enterocolitica and Yersinia pseudotuberculosis and investigation of virulence gene distribution,” Applied and Environmental Microbiology, vol. 69, no. 3, pp. 1810–1816, 2003.
[219]
L. M. Sihvonen, S. Hallanvuo, K. Haukka, M. Skurnik, and A. Siitonen, “The ail gene is present in some Yersinia enterocolitica biotype 1A strains,” Foodborne Pathogens and Disease, vol. 8, no. 3, pp. 455–457, 2011.
[220]
R. Gierczyński, A. Golubov, H. Neubauer, J. N. Pham, and A. Rakin, “Development of multiple-locus variable-number tandem-repeat analysis for Yersinia enterocolitica subsp. palearctica and its application to bioserogroup 4/O3 subtyping,” Journal of Clinical Microbiology, vol. 45, no. 8, pp. 2508–2515, 2007.
[221]
L. M. Sihvonen, S. Toivonen, K. Haukka, M. Kuusi, M. Skurnik, and A. Siitonen, “Multilocus variable-number tandem-repeat analysis, pulsed-field gel electrophoresis, and antimicrobial susceptibility patterns in discrimination of sporadic and outbreak-related strains of Yersinia enterocolitica,” BMC Microbiology, vol. 11, article 42, 2011.
[222]
E. Palonen, M. Lindstr？m, and H. Korkeala, “Adaptation of enteropathogenic Yersinia to low growth temperature,” Critical Reviews in Microbiology, vol. 36, no. 1, pp. 54–67, 2010.
[223]
A. Lawal, O. Jejelowo, A. K. Chopra, and J. A. Rosenzweig, “Ribonucleases and bacterial virulence,” Microbial Biotechnology, vol. 4, no. 5, pp. 558–571, 2011.
[224]
S. M. Tennant, N. A. Skinner, A. Joe, and R. M. Robins-Browne, “Homologues of insecticidal toxin complex genes in Yersinia enterocolitica biotype 1A and their contribution to virulence,” Infection and Immunity, vol. 73, no. 10, pp. 6860–6867, 2005.
[225]
R. H. ffrench-Constant, A. Dowling, and N. R. Waterfield, “Insecticidal toxins from Photorhabdus bacteria and their potential use in agriculture,” Toxicon, vol. 49, no. 4, pp. 436–451, 2007.
[226]
G. Bresolin, J. A. W. Morgan, D. Ilgen, S. Scherer, and T. M. Fuchs, “Low temperature-induced insecticidal activity of Yersinia enterocolitica,” Molecular Microbiology, vol. 59, no. 2, pp. 503–512, 2006.
[227]
M. C. Hares, S. J. Hinchliffe, P. C. R. Strong et al., “The Yersinia pseudotuberculosis and Yersinia pestis toxin complex is active against cultured mammalian cells,” Microbiology, vol. 154, no. 11, pp. 3503–3517, 2008.
[228]
G. Cornelis, “Distribution of beta-lactamases A and B in some groups of Yersinia enterocolitica and their role in resistance,” Journal of General Microbiology, vol. 91, no. 2, pp. 391–402, 1975.
[229]
G. Cornelis and E. P. Abraham, “Beta-lactamases from Yersinia enterocolitica,” Journal of General Microbiology, vol. 87, no. 2, pp. 273–284, 1975.
[230]
C. Long, T. F. Jones, D. J. Vugia et al., “Yersinia pseudotuberculosis and Y. enterocolitica infections, FoodNet, 1996–2007,” Emerging Infectious Diseases, vol. 16, no. 3, pp. 566–567, 2010.
[231]
W. Knapp, “Mesenteric adenitis due to Pasteurella pseudotuberculosis in young people,” The New England Journal of Medicine, vol. 259, no. 16, pp. 776–778, 1958.
[232]
J. R. Paff, D. A. Triplett, and T. N. Saari, “Clinical and laboratory aspects of Yersinia pseudotuberculosis infections, with a report of two cases,” American Journal of Clinical Pathology, vol. 66, no. 1, pp. 101–110, 1976.
