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Interplay between proinflammatory cytokines, miRNA, and tissue lesions in Anisakis-infected Sprague-Dawley rats.
PLoS Negl Trop Dis 2019; 13(5):e0007397PN

Abstract

BACKGROUND

Anisakiasis is an emerging public health problem, caused by Anisakis spp. nematode larvae. Anisakiasis presents as variable and unspecific gastrointestinal and/or allergic clinical symptoms, which accounts for the high rate of misdiagnosed cases.

METHODOLOGY/PRINCIPAL FINDINGS

The aim of this study was to characterize the early cellular (6-72 h p.i.) and molecular (6 h p.i.) immune response and general underlying regulatory mechanism in Anisakis infected rats. Each Sprague-Dawley rat was infected with 10 Anisakis spp. larvae by gastric intubation. Tissues with visible lesions were processed for: i) classic histopathology (HE), immunofluorescence (CD3, iNOS, S100A8/A9), and transmission electron microscopy (TEM); ii) target genes (Il1b, Il6, Il18, Ccl3, Icam1, Mmp9) and microRNA (Rat Immunopathology MIRN-104ZF plate, Quiagen) expression analysis; and iii) global DNA methylation. Histopathology revealed that Anisakis larval migration caused moderate to extensive hemorrhages in submucosal and epimysial/perimysial connective tissue. In stomach and muscle, moderate to abundant mixed inflammatory infiltrate was present, dominated by neutrophils and macrophages, while only mild infiltration was seen in intestine. Lesions were characterized by the presence of CD3+, iNOS+, and S100A8/A9+ cells. The greatest number of iNOS+ and S100A8/A9+ cells was seen in muscle. Il6, Il1b, and Ccl3 showed particularly strong expression in stomach and visceral adipose tissues, but the order of expression differed between tissues. In total, three miRNAs were differentially expressed, two in stomach (miRNA-451 and miRNA-223) and two in intestine (miRNA-451 and miRNA-672). No changes in global DNA methylation were observed in infected tissues relative to controls.

CONCLUSIONS/SIGNIFICANCE

Anisakis infection induces strong immune responses in infected rats with marked induction of specific proinflammatory cytokines and miRNA expression. Deciphering the functional role of these cytokines and miRNAs will help in understanding the anisakiasis pathology and controversies surrounding Anisakis infection in humans.

Authors+Show Affiliations

Laboratory of Aquaculture, Institute of Oceanography and Fisheries, Split, Croatia.Department of Marine Studies, University of Split, Split, Croatia.Faculty of Science, University of Split, Split, Croatia.Laboratory of Aquaculture, Institute of Oceanography and Fisheries, Split, Croatia.Laboratory of Aquaculture, Institute of Oceanography and Fisheries, Split, Croatia.Laboratory of Aquaculture, Institute of Oceanography and Fisheries, Split, Croatia.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

31091271

Citation

Hrabar, Jerko, et al. "Interplay Between Proinflammatory Cytokines, miRNA, and Tissue Lesions in Anisakis-infected Sprague-Dawley Rats." PLoS Neglected Tropical Diseases, vol. 13, no. 5, 2019, pp. e0007397.
Hrabar J, Trumbić Ž, Bočina I, et al. Interplay between proinflammatory cytokines, miRNA, and tissue lesions in Anisakis-infected Sprague-Dawley rats. PLoS Negl Trop Dis. 2019;13(5):e0007397.
Hrabar, J., Trumbić, Ž., Bočina, I., Bušelić, I., Vrbatović, A., & Mladineo, I. (2019). Interplay between proinflammatory cytokines, miRNA, and tissue lesions in Anisakis-infected Sprague-Dawley rats. PLoS Neglected Tropical Diseases, 13(5), pp. e0007397. doi:10.1371/journal.pntd.0007397.
Hrabar J, et al. Interplay Between Proinflammatory Cytokines, miRNA, and Tissue Lesions in Anisakis-infected Sprague-Dawley Rats. PLoS Negl Trop Dis. 2019;13(5):e0007397. PubMed PMID: 31091271.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Interplay between proinflammatory cytokines, miRNA, and tissue lesions in Anisakis-infected Sprague-Dawley rats. AU - Hrabar,Jerko, AU - Trumbić,Željka, AU - Bočina,Ivana, AU - Bušelić,Ivana, AU - Vrbatović,Anamarija, AU - Mladineo,Ivona, Y1 - 2019/05/15/ PY - 2019/01/28/received PY - 2019/04/16/accepted PY - 2019/05/28/revised PY - 2019/5/16/pubmed PY - 2019/5/16/medline PY - 2019/5/16/entrez SP - e0007397 EP - e0007397 JF - PLoS neglected tropical diseases JO - PLoS Negl Trop Dis VL - 13 IS - 5 N2 - BACKGROUND: Anisakiasis is an emerging public health problem, caused by Anisakis spp. nematode larvae. Anisakiasis presents as variable and unspecific gastrointestinal and/or allergic clinical symptoms, which accounts for the high rate of misdiagnosed cases. METHODOLOGY/PRINCIPAL FINDINGS: The aim of this study was to characterize the early cellular (6-72 h p.i.) and molecular (6 h p.i.) immune response and general underlying regulatory mechanism in Anisakis infected rats. Each Sprague-Dawley rat was infected with 10 Anisakis spp. larvae by gastric intubation. Tissues with visible lesions were processed for: i) classic histopathology (HE), immunofluorescence (CD3, iNOS, S100A8/A9), and transmission electron microscopy (TEM); ii) target genes (Il1b, Il6, Il18, Ccl3, Icam1, Mmp9) and microRNA (Rat Immunopathology MIRN-104ZF plate, Quiagen) expression analysis; and iii) global DNA methylation. Histopathology revealed that Anisakis larval migration caused moderate to extensive hemorrhages in submucosal and epimysial/perimysial connective tissue. In stomach and muscle, moderate to abundant mixed inflammatory infiltrate was present, dominated by neutrophils and macrophages, while only mild infiltration was seen in intestine. Lesions were characterized by the presence of CD3+, iNOS+, and S100A8/A9+ cells. The greatest number of iNOS+ and S100A8/A9+ cells was seen in muscle. Il6, Il1b, and Ccl3 showed particularly strong expression in stomach and visceral adipose tissues, but the order of expression differed between tissues. In total, three miRNAs were differentially expressed, two in stomach (miRNA-451 and miRNA-223) and two in intestine (miRNA-451 and miRNA-672). No changes in global DNA methylation were observed in infected tissues relative to controls. CONCLUSIONS/SIGNIFICANCE: Anisakis infection induces strong immune responses in infected rats with marked induction of specific proinflammatory cytokines and miRNA expression. Deciphering the functional role of these cytokines and miRNAs will help in understanding the anisakiasis pathology and controversies surrounding Anisakis infection in humans. SN - 1935-2735 UR - https://www.unboundmedicine.com/medline/citation/31091271/Interplay_between_proinflammatory_cytokines,_miRNA,_and_tissue_lesions_in_Anisakis-infected_Sprague-Dawley_rats L2 - http://dx.plos.org/10.1371/journal.pntd.0007397 DB - PRIME DP - Unbound Medicine ER -