Molecular Characterization and Expression Analysis of Intercellular Adhesion Molecule-1 (ICAM-1) Genes in Rainbow Trout (Oncorhynchus mykiss) in Response to Viral, Bacterial and Parasitic Challenge.

Xue Zhai,Yan-Ling Song,Chuan-Jie Qin,Wei-Guang Kong,Jia-Feng Cao,Fen Dong,Gao-Feng Cheng,Guang-Kun Han,Zhen Xu

doi:10.3389/fimmu.2021.704224

Abstract

The intercellular adhesion molecule-1 (ICAM-1), known as CD54, is a transmembrane cell surface glycoprotein that interacts with two integrins (i.e., LFA-1 and Mac-l) important for trans-endothelial migration of leukocytes. The level of ICAM-1 expression is upregulated in response to some inflammatory stimulations, including pathogen infection and proinflammatory cytokines. Yet, to date, our knowledge regarding the functional role of ICAM-1 in teleost fish remains largely unknown. In this study, we cloned and characterized the sequence of ICAM-1 in rainbow trout (Oncorhynchus mykiss) for the first time, which exhibited that the molecular features of ICAM-1 in fishes were relatively conserved compared with human ICAM-1. The transcriptional level of ICAM-1 was detected in 12 different tissues, and we found high expression of this gene in the head kidney, spleen, gills, skin, nose, and pharynx. Moreover, upon stimulation with infectious hematopoietic necrosis virus (IHNV), Flavobacterium columnare G4 (F. columnare), and Ichthyophthirius multifiliis (Ich) in rainbow trout, the morphological changes were observed in the skin and gills, and enhanced expression of ICAM-1 mRNA was detected both in the systemic and mucosal tissues. These results indicate that ICAM-1 may be implicated in the mucosal immune responses to viral, bacterial, and parasitic infections in teleost fish, meaning that ICAM-1 emerges as a master regulator of mucosal immune responses against pathogen infections in teleost fish.

Highlights

Intercellular adhesion molecule-1 (ICAM-1), an inducible transmembrane glycoprotein, belongs to the immunoglobulin superfamily
Trout ICAM-1 represented the highest similarity with Oncorhynchus tshawytscha (89%), followed by Salvelinus alpinus (85%), but low identities to ICAM-1 of Ctenopharyngodon idella (49%) (Figure 2)
The exon and intron organization of ICAM-1 was analyzed in four teleost fishes and human, which showed that rainbow trout existing 12 exons and 11 introns shared more similar with Oncorhynchus tshawytscha and Salvelinus alpinus (Supplementary Figure 1)

Summary

Introduction

Intercellular adhesion molecule-1 (ICAM-1), an inducible transmembrane glycoprotein, belongs to the immunoglobulin superfamily. Previous studies have demonstrated that ICAM-1 mainly binds to lymphocyte function-associated antigen 1 (LFA-1, CDlla/CD18) [5] and macrophage antigen 1 (Mac-l, CDllb/CD18) [6, 7] (i.e., two integrins belonging to the b2 subfamily) as receptors that are essential for cell–cell and cell–matrix adhesive interactions and activation of signal-transduction into the cell pathways [8]. CD43, known as sialophorin, a lesser-known membrane receptor for ICAM-1, facilitates the adhesion of Th17 cells to ICAM-1 and modulates apical and trans-endothelial migration [10]. The interaction between ICAM-1 and CD43 plays an important role in the adhesion and invasion of tumor cells to peritoneum [11]. ICAM-1 serves as pathogen receptors, such as a sequestration receptor for malarial parasite Plasmodium falciparum [12], human rhinovirus [13], and Coxsackievirus A21 [14, 15] and as a coreceptor for human immunodeficiency virus-1 (HIV-1) [16]

Methods

Results

Conclusion