Macrophage Migration Inhibitory Factor in <i>Psoroptes ovis</i>: Molecular Characterization and Potential Role in Eosinophil Accumulation of Skin in Rabbit and Its Implication in the Host–Parasite Interaction

<i>Psoroptes ovis,</i> a common surface-living mite of domestic and wild animals worldwide, results in huge economic losses and serious welfare issues in the animal industry. <i>P. ovis</i> infestation rapidly causes massive eosinophil infiltration in skin lesions, and increa...

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Main Authors: Xiaobin Gu, You Ge, Ya Wang, Cuirui Huang, Guangyou Yang, Yue Xie, Jing Xu, Ran He, Zhijun Zhong, Deying Yang, Zhi He, Xuerong Peng
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/6/5985
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author Xiaobin Gu
You Ge
Ya Wang
Cuirui Huang
Guangyou Yang
Yue Xie
Jing Xu
Ran He
Zhijun Zhong
Deying Yang
Zhi He
Xuerong Peng
author_facet Xiaobin Gu
You Ge
Ya Wang
Cuirui Huang
Guangyou Yang
Yue Xie
Jing Xu
Ran He
Zhijun Zhong
Deying Yang
Zhi He
Xuerong Peng
author_sort Xiaobin Gu
collection DOAJ
description <i>Psoroptes ovis,</i> a common surface-living mite of domestic and wild animals worldwide, results in huge economic losses and serious welfare issues in the animal industry. <i>P. ovis</i> infestation rapidly causes massive eosinophil infiltration in skin lesions, and increasing research revealed that eosinophils might play an important role in the pathogenesis of <i>P. ovis</i> infestation. Intradermal injection of <i>P. ovis</i> antigen invoked massive eosinophil infiltration, suggesting that this mite should contain some relative molecules involved in eosinophil accumulation in the skin. However, these active molecules have not yet been identified. Herein, we identified macrophage migration inhibitor factor (MIF) in <i>P. ovis</i> (<i>Pso</i>MIF) using bioinformatics and molecular biology methods. Sequence analyses revealed that <i>Pso</i>MIF appeared with high similarity to the topology of monomer and trimer formation with host MIF (RMSD = 0.28 angstroms and 2.826 angstroms, respectively) but with differences in tautomerase and thiol-protein oxidoreductase active sites. Reverse transcription PCR analysis (qRT-PCR) results showed that <i>Pso</i>MIF was expressed throughout all the developmental stages of <i>P. ovis</i>, particularly with the highest expression in female mites. Immunolocalization revealed that MIF protein located in the ovary and oviduct of female mites and also localized throughout the stratum spinosum, stratum granulosum, and even basal layers of the epidermis in skin lesions caused by <i>P. ovis</i>. r<i>Pso</i>MIF significantly upregulated eosinophil-related gene expression both in vitro (PBMC: CCL5, CCL11; HaCaT: IL-3, IL-4, IL-5, CCL5, CCL11) and in vivo (rabbit: IL-5, CCL5, CCL11, P-selectin, ICAM-1). Moreover, r<i>Pso</i>MIF could induce cutaneous eosinophil accumulation in a rabbit model and increased the vascular permeability in a mouse model. Our findings indicated that <i>Pso</i>MIF served as one of the key molecules contributing to skin eosinophil accumulation in <i>P. ovis</i> infection of rabbits.
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spelling doaj.art-e1099ef33a2d48d7b3e59ab424dd65902023-11-17T11:41:53ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-03-01246598510.3390/ijms24065985Macrophage Migration Inhibitory Factor in <i>Psoroptes ovis</i>: Molecular Characterization and Potential Role in Eosinophil Accumulation of Skin in Rabbit and Its Implication in the Host–Parasite InteractionXiaobin Gu0You Ge1Ya Wang2Cuirui Huang3Guangyou Yang4Yue Xie5Jing Xu6Ran He7Zhijun Zhong8Deying Yang9Zhi He10Xuerong Peng11Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaInstitute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, ChinaInstitute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Chemistry, College of Life and Basic Science, Sichuan Agricultural University, Ya’an 625014, China<i>Psoroptes ovis,</i> a common surface-living mite of domestic and wild animals worldwide, results in huge economic losses and serious welfare issues in the animal industry. <i>P. ovis</i> infestation rapidly causes massive eosinophil infiltration in skin lesions, and increasing research revealed that eosinophils might play an important role in the pathogenesis of <i>P. ovis</i> infestation. Intradermal injection of <i>P. ovis</i> antigen invoked massive eosinophil infiltration, suggesting that this mite should contain some relative molecules involved in eosinophil accumulation in the skin. However, these active molecules have not yet been identified. Herein, we identified macrophage migration inhibitor factor (MIF) in <i>P. ovis</i> (<i>Pso</i>MIF) using bioinformatics and molecular biology methods. Sequence analyses revealed that <i>Pso</i>MIF appeared with high similarity to the topology of monomer and trimer formation with host MIF (RMSD = 0.28 angstroms and 2.826 angstroms, respectively) but with differences in tautomerase and thiol-protein oxidoreductase active sites. Reverse transcription PCR analysis (qRT-PCR) results showed that <i>Pso</i>MIF was expressed throughout all the developmental stages of <i>P. ovis</i>, particularly with the highest expression in female mites. Immunolocalization revealed that MIF protein located in the ovary and oviduct of female mites and also localized throughout the stratum spinosum, stratum granulosum, and even basal layers of the epidermis in skin lesions caused by <i>P. ovis</i>. r<i>Pso</i>MIF significantly upregulated eosinophil-related gene expression both in vitro (PBMC: CCL5, CCL11; HaCaT: IL-3, IL-4, IL-5, CCL5, CCL11) and in vivo (rabbit: IL-5, CCL5, CCL11, P-selectin, ICAM-1). Moreover, r<i>Pso</i>MIF could induce cutaneous eosinophil accumulation in a rabbit model and increased the vascular permeability in a mouse model. Our findings indicated that <i>Pso</i>MIF served as one of the key molecules contributing to skin eosinophil accumulation in <i>P. ovis</i> infection of rabbits.https://www.mdpi.com/1422-0067/24/6/5985<i>Psoroptes ovis</i>MIFsequence analysistranscriptional leveltissue localizationskin eosinophil recruitment
spellingShingle Xiaobin Gu
You Ge
Ya Wang
Cuirui Huang
Guangyou Yang
Yue Xie
Jing Xu
Ran He
Zhijun Zhong
Deying Yang
Zhi He
Xuerong Peng
Macrophage Migration Inhibitory Factor in <i>Psoroptes ovis</i>: Molecular Characterization and Potential Role in Eosinophil Accumulation of Skin in Rabbit and Its Implication in the Host–Parasite Interaction
International Journal of Molecular Sciences
<i>Psoroptes ovis</i>
MIF
sequence analysis
transcriptional level
tissue localization
skin eosinophil recruitment
title Macrophage Migration Inhibitory Factor in <i>Psoroptes ovis</i>: Molecular Characterization and Potential Role in Eosinophil Accumulation of Skin in Rabbit and Its Implication in the Host–Parasite Interaction
title_full Macrophage Migration Inhibitory Factor in <i>Psoroptes ovis</i>: Molecular Characterization and Potential Role in Eosinophil Accumulation of Skin in Rabbit and Its Implication in the Host–Parasite Interaction
title_fullStr Macrophage Migration Inhibitory Factor in <i>Psoroptes ovis</i>: Molecular Characterization and Potential Role in Eosinophil Accumulation of Skin in Rabbit and Its Implication in the Host–Parasite Interaction
title_full_unstemmed Macrophage Migration Inhibitory Factor in <i>Psoroptes ovis</i>: Molecular Characterization and Potential Role in Eosinophil Accumulation of Skin in Rabbit and Its Implication in the Host–Parasite Interaction
title_short Macrophage Migration Inhibitory Factor in <i>Psoroptes ovis</i>: Molecular Characterization and Potential Role in Eosinophil Accumulation of Skin in Rabbit and Its Implication in the Host–Parasite Interaction
title_sort macrophage migration inhibitory factor in i psoroptes ovis i molecular characterization and potential role in eosinophil accumulation of skin in rabbit and its implication in the host parasite interaction
topic <i>Psoroptes ovis</i>
MIF
sequence analysis
transcriptional level
tissue localization
skin eosinophil recruitment
url https://www.mdpi.com/1422-0067/24/6/5985
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