Response of swine spleen to Streptococcus suis infection revealed by transcription analysis

Li, Ran; Zhang, Anding; Chen, Bin; Teng, Liu; Wang, Ya; Chen, Huanchun; Jin, Meilin

doi:10.1186/1471-2164-11-556

Cited by 33 publications

(37 citation statements)

References 79 publications

(100 reference statements)

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“…suis infection-induced TREM-1 expression and high serum proinflammatory cytokine levels in a mouse model. Our previous transcription analysis indicated that TREM-1 expression was upregulated in the pig spleen and that some genes encoding proinflammatory cytokines were also upregulated during S. suis infection (41). The present mouse infection study also indicates that S. suis infection can induce trem-1 transcription (Fig.…”

Section: Resultssupporting

confidence: 54%

“…Our previous transcription analysis of the swine response to S. suis infection indicated that the gene encoding TREM-1 was upregulated and that a few inflammatory-response genes were also highly expressed (41). Given the role of TREM-1 signaling in the enhanced proinflammatory response associated with the pathogenesis of S. suis, we examined the effect of TREM-1 signaling on the outcome of S. suis infection.…”

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confidence: 99%

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TREM-1 Signaling Promotes Host Defense during the Early Stage of Infection with Highly Pathogenic Streptococcus suis

et al. 2015

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c Infection with highly pathogenic Streptococcus suis can cause septic shock, which is characterized by high levels of inflammatory cytokines and a high mortality rate. Our previous study indicated that TREM-1 (triggering receptor expressed on myeloid cells 1) was upregulated in swine spleen cells in response to S. suis infection. The role of TREM-1 signaling in enhancement of the proinflammatory response promoted us to examine its effect on the outcome of S. suis infection. In the present study, the recombinant extracellular domain of TREM-1 (rTREM-1) and an agonistic TREM-1 antibody were used to inhibit and activate TREM-1 signaling to evaluate its role in neutrophil activation, pathogen clearance, proinflammatory cytokine response, and the outcome of highly pathogenic S. suis infection in a mouse model. Blockage of TREM-1 signaling caused a more severe proinflammatory response to S. suis infection and increased the mortality rate, while its activation had the opposite effect. Blockage or activation of TREM-1 signaling lowered or raised the number of neutrophils in the blood, which correlated well with host clearance of S. suis. In conclusion, the TREM-1-mediated innate immune response played an essential role in the activation of neutrophils and S. suis clearance, which further reduced severe inflammation and finally benefited the outcome of the infection. Streptococcus suis is a major swine pathogen that is responsible for severe economic losses in the pork industry and also represents a significant threat to human health (1-3). Infection of humans could cause meningitis, sepsis, arthritis, endocarditis, and endophthalmitis, and the pooled case-fatality rate is 12.8% (4). The two large-scale human S. suis epidemics in China (the first was 25 cases with 14 deaths in Jiangsu in 1998, and the second was 204 cases with 38 deaths in Sichuan in 2005) have raised people's awareness of the public health threat (3, 5, 6). To date, more than 1,500 human infections have been reported worldwide (4). In addition, S. suis has also been identified as the third most common cause of community-acquired bacterial meningitis in Hong Kong and as the leading and second most common cause of adult meningitis in Vietnam and Thailand, respectively (3,7,8). S. suis is known to constitute a high risk of infection for occupationally exposed people (9-11), but it could also cause severe infection in people who lack contact with swine and pork-derived products (12, 13). Human S. suis isolates showed high adhesion to intestinal epithelial cells, suggesting that it should be considered a foodborne pathogen (14). Furthermore, S. suis infection is very dangerous for cancer patients (15), alcoholics (16), and splenectomy patients (17, 18). S. suis infection may also cause adverse clinical outcomes for people with influenza (19,20).A few comprehensive studies have been performed that yielded many advances in epidemiology, population genomics, serotyping, molecular diagnostics, the characterization of potential virulence factors, host-pathogen i...

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Section: Resultssupporting

confidence: 54%

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confidence: 99%

TREM-1 Signaling Promotes Host Defense during the Early Stage of Infection with Highly Pathogenic Streptococcus suis

et al. 2015

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“…S1) . In contrast to pathogenic SS2, Δ hp0197 infection did not induce high levels of cytokine expression [63], which could be provoked by highly pathogenic SS2 [55], [63], [64]. These data indicated that hp0197 significantly contributed to S. suis virulence.…”

Section: Discussionmentioning

confidence: 77%

HP0197 Contributes to CPS Synthesis and the Virulence of Streptococcus suis via CcpA

et al. 2012

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Streptococcus suis serotype 2 (SS2), a major swine pathogen and an emerging zoonotic agent, has greatly challenged global public health. The encoding proteins with unknown functions the bacterium encodes are an obstruction to studies of the pathogenesis. A novel surface protective antigen HP0197 is one of these proteins which have no sequence homology to any known protein. In the present study, the protein was determined to be involved in bacterial virulence through an evaluation of the isogenic mutant (Δhp0197) in both mice and pigs. The experimental infection also indicated that Δhp0197 could be cleared easily during infection, which could be attributed to the reduced thickness of the capsular polysaccharides (CPS) and the significantly reduced phagocytotic resistance. Microarrays-based comparative transcriptome analysis suggested that the suppressed expression of the operon responsible for CPS synthesis might be reversed by CcpA activity, which controlled global regulation of carbon catabolite through the binding of the CcpA and HPr-Ser-46-P to the catabolite-responsive elements (cre) of the target operons. The hypothesis was approved by the fact that the purified FLAG-tagged HPr from WT stain exhibited a higher binding activity to cre with CcpA compared to the Δhp0197 by the Electrophoretic Mobility Shift Assay, suggesting lower level of phosphorylation of the phosphocarrier protein HPr at residue Ser-46 (HPr-Ser-46P) in Δhp0197. These indicated that HP0197 could enhance CcpA activity to control the expression of genes involved in carbohydrate utilization and CPS synthesis, thus contributing to the virulence of S. suis.

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“…Within S. aureus abscesses, manganese and zinc levels are very low due to increased production of the metal binding host protein calprotectin (14). Interestingly, a recent transcriptome study of swine spleen showed a strong upregulation of calprotectin (also named S100A8/S100A9) after S. suis challenge (25). Our observations of reduced disease and mortality and of reduced bacterial recovery from organs of ⌬troA mutant-infected mice strongly suggest that TroA is an important virulence factor and contributes to overcome nutritional immunity of the host.…”

Section: Discussionmentioning

confidence: 99%

TroA of Streptococcus suis Is Required for Manganese Acquisition and Full Virulence

et al. 2011

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Streptococcus suis causes infections in pigs and occasionally in humans, resulting in manifestations as meningitis, sepsis, arthritis, and septic shock. For survival within the host, S. suis requires numerous nutrients including trace metals. Little is known about the specific proteins involved in metal scavenging in S. suis. In this study we evaluated the role of the putative high-affinity metal binding lipoprotein TroA in metal acquisition and virulence. A mutant strain deficient in the expression of TroA (⌬troA mutant) was constructed. Growth of the ⌬troA mutant in Todd-Hewitt broth was similar to wild-type growth; however, growth of the ⌬troA mutant in cation-deprived Todd-Hewitt broth and in porcine serum was strongly reduced compared to growth of wild-type bacteria. Supplementing the medium with extra manganese but not with magnesium, zinc, copper, nickel, or iron restored growth to wild-type levels, indicating that TroA is specifically required for growth in environments low in manganese. The ⌬troA mutant also showed increased susceptibility to H 2 O 2 , suggesting that TroA is involved in counteracting oxidative stress. Furthermore, the expression of the troA gene was subject to environmental regulation at the transcript level. In a murine S. suis infection model, the ⌬troA mutant displayed a nonvirulent phenotype. These data indicate that S. suis TroA is involved in manganese acquisition and is required for full virulence in mice.Streptococcus suis is an important pathogen of pigs and may cause meningitis, sepsis, arthritis, and septic shock. Occasionally, S. suis is able to infect humans. Infected humans may show symptoms similar to those in pigs (1,5,11,32). Although human infections are exceptional, a large outbreak in humans was reported in 2005 in China, with 215 cases and 39 deaths (52). Of the 33 known S. suis serotypes, serotype 2 is most frequently isolated from diseased pigs and humans. However, serotype 9 infections are emerging in pigs, especially in Europe (7,35,48). Current control measures are insufficient and mainly rely on antibiotic treatment and vaccination with homologous bacterins. Increased antibiotic resistance has been reported for S. suis (17, 49), and bacterin-based vaccines do not provide protection against multiple serotypes (6).For growth and function, bacteria have to acquire numerous nutrients from their surrounding environment. For pathogenic bacteria, an important group of essential nutrients are the trace metals. Metals such as iron, zinc, and manganese have been shown to be essential structural and catalytic cofactors for several bacterial proteins (2). However, the concentration of free available trace metals within an infected host is relatively low compared to the metal concentrations in medium usually applied for in vitro growth. Within the host, several trace metals are sequestered; for instance, iron binds to hemoglobin, and zinc and manganese bind to the S100 family of proteins produced by neutrophils (14,15). This recruitment of trace metals by host proteins ha...

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Response of swine spleen to Streptococcus suis infection revealed by transcription analysis

Cited by 33 publications

References 79 publications

TREM-1 Signaling Promotes Host Defense during the Early Stage of Infection with Highly Pathogenic Streptococcus suis

TREM-1 Signaling Promotes Host Defense during the Early Stage of Infection with Highly Pathogenic Streptococcus suis

HP0197 Contributes to CPS Synthesis and the Virulence of Streptococcus suis via CcpA

TroA of Streptococcus suis Is Required for Manganese Acquisition and Full Virulence

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