Molecular and functional characterization of peptidoglycan-recognition protein SC2 (PGRP-SC2) from Nile tilapia (Oreochromis niloticus) involved in the immune response to Streptococcus agalactiae

Gan, Zhen; Chen, Shannan; Hou, Jing; Huo, Huijun; Zhang, Xiaolin; Ruan, Baiye; Laghari, Zubair Ahmed; Li, Li; Lu, Yue; Nie, Pin

doi:10.1016/j.fsi.2016.03.158

Cited by 30 publications

(6 citation statements)

References 40 publications

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“…For instance, PGRP from red drum is bactericidal against Gram-positive species and shows slight bactericidal activity against Gram-negative bacteria, and it blocks bacterial infection of host cells [25]. Similarly, Nile tilapia PGRP significantly reduces bacterial load in target organs attacked by pathogens [46]. Consistent with these results, rSgPGRP-S1 exhibited significant in vitro bactericidal activity against Gram-negative E. coli and Gram-positive S. aureus in our current study.…”

Section: Discussionsupporting

confidence: 88%

Peptidoglycan recognition protein of Solen grandis (SgPGRP-S1) mediates immune recognition and bacteria clearance

Wei

Yang

et al. 2018

Fish & Shellfish Immunology

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Peptidoglycan recognition proteins (PGRPs) are indispensable molecules in innate immunity due to their prominent function in sensing and eliminating invading microorganisms. In the present study, a short type PGRP from razor clam Solen grandis (SgPGRP-S1) was recombinantly expressed and purified to investigate its potential function in innate immunity. As a pattern recognition receptor, recombinant SgPGRP-S1 (rSgPGRP-S1) specifically bind Lys-type and Dap-type peptidoglycan in vitro, but not lipopolysaccharide or β-glucan. The peptidoglycan binding ability of rSgPGRP-S1 resulted in significant agglutination activity against Gram-negative Escherichia coli and Listonella anguillarum, as well as Gram-positive Micrococcus luteus. Furthermore, rSgPGRP-S1 was bactericidal, significantly suppressing the growth of both E. coli and Gram-positive Staphylococcus aureus. The protein also exhibited strong amidase activity and degraded bacterial peptidoglycan in the presence of Zn, suggesting amidase activity might contribute to SgPGRP-S1 antibacterial activity. These results indicate SgPGRP-S1 is multifunctional in innate immunity, mediating both immune recognition and bacteria elimination.

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Section: Discussionsupporting

confidence: 88%

Peptidoglycan recognition protein of Solen grandis (SgPGRP-S1) mediates immune recognition and bacteria clearance

Wei

Yang

et al. 2018

Fish & Shellfish Immunology

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“…The high expression of MMP-9 was observed in spleen ( Figure 5), where necrotic lymphocytes and the breakage of cells appeared in spleen after the S. agalactiae challenge [23]. This finding coincides with those of other fish [13,38]. The damage to the tilapia brain was identified with macrophages and cavities in cytoplasm at 72 h [16], suggesting that the brain is a susceptible organ; and its pathological changes may be used to reasonably explain the expression pattern of NtMMP-9 against the S. agalactiae challenge.…”

Section: Transcriptional Expression Of Ntmmp-9supporting

confidence: 85%

“…These results indicate that NtMMP-9 has a positive role in the immunological regulation of Nile tilapia. The liver, brain, and spleen of Nile tilapia proved to be more susceptive to the S. agalactiae challenge due to the rapid response of NtMMP-9 ( Figure 5), which is consistent with the damage of immune organs (i.e., spleen and head kidney) of tilapia after the S. agalactiae challenge [38]. In histopathology, several pathological changes such as encephalitis, lymphocyte necrosis, and atrophied neuronal cells have been found in fish [39].…”

Section: Transcriptional Expression Of Ntmmp-9supporting

confidence: 61%

Characterization of Matrix Metalloprotease-9 Gene from Nile tilapia (Oreochromis niloticus) and Its High-Level Expression Induced by the Streptococcus agalactiae Challenge

et al. 2020

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The bacterial diseases of tilapia caused by Streptococcus agalactiae have resulted in the high mortality and huge economic loss in the tilapia industry. Matrix metalloproteinase-9 (MMP-9) may play an important role in fighting infection. However, the role of MMP-9 in Nile tilapia against S. agalactiae is still unclear. In this work, MMP-9 cDNA of Nile tilapia (NtMMP-9) has been cloned and characterized. NtMMP-9 has 2043 bp and encodes a putative protein of 680 amino acids. NtMMP-9 contains the conserved domains interacting with decorin and inhibitors via binding forces compared to those in other teleosts. Quantitative real-time-polymerase chain reaction (qPCR) analysis reveals that NtMMP-9 distinctly upregulated following S. agalactiae infection in a tissue- and time-dependent response pattern, and the tissues, including liver, spleen, and intestines, are the major organs against a S. agalactiae infection. Besides, the proteolytic activity of NtMMP-9 is also confirmed by heterologous expression and zymography, which proves the active function of NtMMP-9 interacting with other factors. The findings indicate that NtMMP-9 was involved in immune responses against the bacterial challenge at the transcriptional level. Further work will focus on the molecular mechanisms of NtMMP-9 to respond and modulate the signaling pathways in Nile tilapia against S. agalactiae invasion and the development of NtMMP-9-related predictive biomarkers or vaccines for preventing bacterial infection in the tilapia industry.

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“…Compared with those in insects and mammals, studies on marine organisms PGRPs were also carried out. In fish, researchers have shown that PGRPs from Pseudosciaena crocea , Sciaenops ocellatus , Branchiostoma japonicum , Ctenopharyngodon idella , Ictalurus punctatus , Cynoglossus semilaevis , Oreochromis niloticus , and Scophthalmus maximus L. were all constitutively expressed or up-regulated in response to pathogen or PAMP challenge ( Yong et al, 2010 ; Li et al, 2012 , 2014a , b ; Yao et al, 2012 ; Sun et al, 2014 ; Sun and Sun, 2015 ; Gan et al, 2016 ; Zhang et al, 2016 ). In Echinodermata, PGRP-S2a from European sea star Asterias rubens breaks down peptidoglycan and stimulates phagocytosis of Micrococcus luteus through sea star phagocytes ( Coteur et al, 2007 ).…”

Section: Introductionmentioning

confidence: 99%

Two Novel Short Peptidoglycan Recognition Proteins (PGRPs) From the Deep Sea Vesicomyidae Clam Archivesica packardana: Identification, Recombinant Expression and Bioactivity

Kong

Liu

et al. 2018

Front. Physiol.

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Vesicomyidae clams are common species living in cold seeps, which incorporates symbiotic bacteria into their body maintaining endosymbiosis relationship. As members of pattern recognition receptor (PRR) family, peptidoglycan recognition proteins (PGRPs) recognize pathogen associated molecular patterns and play an important role in innate immunity. In present study, two short PGRPs (ApPGRP-1 and -2) were first identified from Vesicomyidae clam Archivesica packardana. Sequences analysis showed that they have both conserved Zn2+ binding sites (H-H-C) and amidase catalytic sites (H-Y-H-T-C), and phylogenetic tree indicated that they clustered with short PGRPs of other molluscs. PGN assay showed that ApPGRPs could bind Lys-type PGN from Staphylococcus aureus and Dap-type PGN from Bacillus subtilis, and revealed amidase activity with selective zinc ion dependence. rApPGRP-1 and -2 (recombinant ApPGRP-1 and -2) could bind six bacteria with a broad spectrum and had both zinc-dependent and -independent bactericidal activity. ApPGRPs had the complete functions of effectors and partial functions of receptors from PGRPs. Further analyses showed that ApPGRPs from A. packardana might be involved in the endosymbiosis relationship between the host clam and endosymbiotic bacteria as a regulator. The results of these experiments suggested that ApPGRPs were involved in cold seep clams’ immune response. This study provides basic information for further research on the immune mechanisms of deep sea organisms.

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Molecular and functional characterization of peptidoglycan-recognition protein SC2 (PGRP-SC2) from Nile tilapia (Oreochromis niloticus) involved in the immune response to Streptococcus agalactiae

Cited by 30 publications

References 40 publications

Peptidoglycan recognition protein of Solen grandis (SgPGRP-S1) mediates immune recognition and bacteria clearance

Peptidoglycan recognition protein of Solen grandis (SgPGRP-S1) mediates immune recognition and bacteria clearance

Characterization of Matrix Metalloprotease-9 Gene from Nile tilapia (Oreochromis niloticus) and Its High-Level Expression Induced by the Streptococcus agalactiae Challenge

Two Novel Short Peptidoglycan Recognition Proteins (PGRPs) From the Deep Sea Vesicomyidae Clam Archivesica packardana: Identification, Recombinant Expression and Bioactivity

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