Infection of human enterocyte-like cells with rotavirus enhances invasiveness of Yersinia enterocolitica and Y. pseudotuberculosis

Biase, Assunta Maria Di; Petrone, G; Conte, Maria Pia; Seganti, L; Ammendolia, Maria Grazia; Tinari, Antonella; Iosi, Francesca; Marchetti, Magda; Superti, Fabiana

doi:10.1099/0022-1317-49-10-897

Cited by 31 publications

(21 citation statements)

References 13 publications

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“…The unchanged ␣5 expression at 8 h p.i. observed in this study confirms the previous report that ␣5 is unaltered at this time (21). The kinetics of integrin regulation in Caco-2 cells infected with CRW-8 or RRV were indistinguishable (data not shown).…”

Section: Rotavirus Replication In Intestinal Cells Led To Differentiasupporting

confidence: 82%

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Rotavirus Replication in Intestinal Cells Differentially Regulates Integrin Expression by a Phosphatidylinositol 3-Kinase-Dependent Pathway, Resulting in Increased Cell Adhesion and Virus Yield

Halász

Holloway

Turner

et al. 2008

J Virol

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Changes in the interactions between intestinal cells and their surrounding environment during virus infection have not been well documented. The growth and survival of intestinal epithelial cells, the main targets of rotavirus infection, are largely dependent on the interaction of cell surface integrins with the extracellular matrix. In this study, we detected alterations in cellular integrin expression following rotavirus infection, identified the signaling components required, and analyzed the subsequent effects on cell binding to the matrix component collagen. After rotavirus infection of intestinal cells, expression of ␣2␤1 and ␤2 integrins was up-regulated, whereas that of ␣V␤3, ␣V␤5, and ␣5␤1 integrins, if present, was down-regulated. This differential regulation of integrins was reflected at the transcriptional level. It was unrelated to the use of integrins as rotavirus receptors, as both integrin-using and integrin-independent viruses induced integrin regulation. Using pharmacological agents that inhibit kinase activity, integrin regulation was shown to be dependent on phosphatidylinositol 3-kinase (PI3K) but independent of the activities of the mitogen-activated protein kinases p38 and ERK1/2, and cyclooxygenase-2. Replication-dependent activation of the PI3K/Akt pathway was observed following infection of intestinal and nonintestinal cell lines. Rotavirus activation of PI3K was important for regulation of ␣2␤1 expression. Blockade of integrin regulation by PI3K inhibition led to decreased adherence of infected intestinal cells to collagen and a concomitant decrease in virus titer. These findings indicate that rotavirus-induced PI3K activation causes regulation of integrin expression in intestinal cells, leading to prolonged adherence of infected cells to collagen and increased virus production.Rotavirus is a major cause of dehydrating gastroenteritis in infant humans and animals throughout the world. Differentiated epithelial cells on villi in the small intestine (enterocytes) are the main targets of infection, leading to cell death, a reduction in villus epithelium area, loss of absorptive capacity, and osmotic dysregulation (3,7,48,53). Enterocytes are attached to the basement membrane through interactions between the basement matrix and cell-surface adhesion molecules, mainly members of the integrin family (4,6,49,64). Increased enterocyte loss is a feature of rotavirus disease, suggesting that reduced enterocyte adhesion occurs (9). However, the molecules involved in changes in attachment of enterocytes to the matrix during rotavirus infection and how this process relates to viral replication and pathogenesis have not been analyzed.Integrins provide a means for cells to respond to their environment through intracellular signaling networks controlling crucial cellular processes such as adhesion, proliferation, migration, differentiation, and survival (1,20,38,55,69). These ␣␤ heterodimeric glycoproteins have been identified as cellular receptors or entry cofactors for many viruses, including rotavi...

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Section: Rotavirus Replication In Intestinal Cells Led To Differentiasupporting

confidence: 82%

“…(21). Microarray analysis showed that levels of ␣2, ␣6, and ␤1 integrin subunit mRNA increased 3.1-, 2.7-, and 2.8-fold, respectively, in rhesus monkey rotavirus (RRV)-infected Caco-2 cell cultures at 16 h p.i., compared with levels in mock-infected cells (19).…”

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confidence: 99%

Rotavirus Replication in Intestinal Cells Differentially Regulates Integrin Expression by a Phosphatidylinositol 3-Kinase-Dependent Pathway, Resulting in Increased Cell Adhesion and Virus Yield

Halász

Holloway

Turner

et al. 2008

J Virol

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“…Viral and bacterial intestinal pathogens could affect either the same or different regions of the gut, and their effects would be enhanced (11). Mixed infections have been described previously in children with acute gastroenteritis, but few data on the role of noroviruses in dual infections are available.…”

Section: Discussionmentioning

confidence: 99%

Etiology of Sporadic Cases of Pediatric Acute Gastroenteritis in Asturias, Spain, and Genotyping and Characterization of Norovirus Strains Involved

et al. 2004

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a reverse transcription-PCR using primers directed to the norovirus RNA polymerase coding region was included in a viral and bacterial routine screening to diagnose sporadic cases of acute gastroenteritis among children in Asturias, Spain. The role of noroviruses (8.6% of the positively diagnosed cases) as the cause of sporadic pediatric gastroenteritis was evaluated with respect to the detection rates of other gastroenteritis-associated viruses and bacteria. The results indicated that noroviruses were less common than rotaviruses (36.9%), Campylobacter spp. (28.8%), and Salmonella spp. (18.4%) but more frequent than astroviruses (4.3%), adenoviruses (3.8%), and Yersinia spp. (2.2%). Mixed infections involving noroviruses were rarely observed (0.5%). The presence of a norovirus-associated pediatric gastroenteritis peak in summer, as well as the complete absence of norovirus-associated cases in colder months, challenges the view that norovirus infections exclusively have wintertime seasonality. On the other hand, phylogenetic analysis of the amplified fragments showed that the norovirus strains responsible were closely related. A further study using the full-length capsid region showed that these strains could be included into genogroup II, Bristol/Lorsdale cluster, and were closely related to the 1995 and 1996 U.S. subset of strains associated with outbreaks recorded worldwide between 1995 and 1996.Gastroenteritis remains a major public health problem worldwide, especially among children. More than 700 million cases of acute gastroenteritis are estimated to occur annually in children less than 5 years old. The mortality associated with gastroenteritis has been estimated to be 3.5 to 5 million per year (14, 33).Many different pathogens have been found in the stools of children with gastroenteritis. From them, bacteria, such as Salmonella spp., Shigella spp., Campylobacter spp., and Yersinia spp. among others and viruses, such as rotaviruses, adenoviruses, and astroviruses, have been clearly established as etiologic agents of gastroenteritis in children (8,21,28).Recently, noroviruses (formerly known as "Norwalk-like viruses") have been included as a common cause of outbreaks and sporadic cases of gastroenteritis worldwide in individuals of all ages. Their role as the major cause of viral gastroenteritis outbreaks has been recently reported (6,18,39). Nevertheless, few studies have been carried out to evaluate the relative contribution of noroviruses to pediatric sporadic gastroenteritis with respect to other classic gastroenteritis-associated viruses and bacteria.The Norovirus genus within the family Caliciviridae includes single-stranded positive-sense RNA viruses. They have been divided into two distinct genogroups, GGI and GGII, and further subdivided into several clusters or genotypes based on genetic divergence in regions of the RNA-dependent RNA polymerase and the major viral capsid protein (VP60) (38). Thus, GGI includes Norwalk, Southampton, Chiba, and Desert Shield viruses, whereas GGII includes Hawaii, ...

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“…Finally, viral and bacterial intestinal pathogens could affect either the same or different regions of the gut, and their effects would be enhanced (Di Biase et al, 2000). Currently, we still know little about the exact pathology of human gut infections, and it is useful to report studies which examine both viruses and bacteria.…”

Section: E Romá N and Others 438mentioning

confidence: 99%

Acute viral gastroenteritis: proportion and clinical relevance of multiple infections in Spanish children

Román

Wilhelmi

Colomina

et al. 2003

Journal of Medical Microbiology

100

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Dual infections associated with acute infectious diarrhoea and its microbiological, epidemiological and clinical findings have been evaluated in patients selected from a comprehensive survey of children under 4 years old, admitted to hospital emergency rooms from October 1996 to November 1997. A total of 820 children (433 males and 387 females) were enrolled. Stools were tested for rotavirus, adenovirus, astrovirus and bacterial enteropathogens. Patients were grouped according to age, and the seasonality of mixed infections was evaluated. Clinical trends and severity of gastrointestinal disease by Ruuska's score were also analysed. Mixed infections were identified in 39 cases (5 %), of which 23 were males and 16 were females. The majority of cases were in the 7-18-month age group (26 cases) and occurred in autumn (67 %). Virus-virus co-infections were more frequent (26/39) than virus-bacteria co-infections (13/39). More than two infectious agents were detected in only four cases. The most common viral co-infections were rotavirus-astrovirus (13/26) and rotavirus-adenovirus (10/26). The present report is the first prospective analysis of clinical-epidemiological trends of dual infections in young Spanish children with acute viral gastroenteritis. Our results emphasize the clinical importance of mixed infections as a cause of severe diarrhoea in children.

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Infection of human enterocyte-like cells with rotavirus enhances invasiveness of Yersinia enterocolitica and Y. pseudotuberculosis

Cited by 31 publications

References 13 publications

Rotavirus Replication in Intestinal Cells Differentially Regulates Integrin Expression by a Phosphatidylinositol 3-Kinase-Dependent Pathway, Resulting in Increased Cell Adhesion and Virus Yield

Rotavirus Replication in Intestinal Cells Differentially Regulates Integrin Expression by a Phosphatidylinositol 3-Kinase-Dependent Pathway, Resulting in Increased Cell Adhesion and Virus Yield

Etiology of Sporadic Cases of Pediatric Acute Gastroenteritis in Asturias, Spain, and Genotyping and Characterization of Norovirus Strains Involved

Acute viral gastroenteritis: proportion and clinical relevance of multiple infections in Spanish children

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