Discovery of J chain in African lungfish (Protopterus dolloi, Sarcopterygii) using high throughput transcriptome sequencing: implications in mucosal immunity.

Luca Tacchi,Irene Salinas,Erin Larragoite,Pierre Boudinot

doi:10.1371/journal.pone.0070650

Abstract

J chain is a small polypeptide responsible for immunoglobulin (Ig) polymerization and transport of Igs across mucosal surfaces in higher vertebrates. We identified a J chain in dipnoid fish, the African lungfish (Protopterus dolloi) by high throughput sequencing of the transcriptome. P. dolloi J chain is 161 aa long and contains six of the eight Cys residues present in mammalian J chain. Phylogenetic studies place the lungfish J chain closer to tetrapod J chain than to the coelacanth or nurse shark sequences. J chain expression occurs in all P. dolloi immune tissues examined and it increases in the gut and kidney in response to an experimental bacterial infection. Double fluorescent in-situ hybridization shows that 88.5% of IgM+ cells in the gut co-express J chain, a significantly higher percentage than in the pre-pyloric spleen. Importantly, J chain expression is not restricted to the B-cell compartment since gut epithelial cells also express J chain. These results improve our current view of J chain from a phylogenetic perspective.

Highlights

Jchain is a unique 15 KDa polypeptide that is incorporated in the polymeric immunoglobulins such as IgM and IgA
Lungfish J chain has had both Cys 2 and Cys 3 conserved indicating that double disulphide bonds may link the J chain to form polymeric IgM or IgW
Cys 6 is not conserved in the nurse shark but it is present in P. dolloi

Summary

Introduction

Jchain is a unique 15 KDa polypeptide that is incorporated in the polymeric immunoglobulins such as IgM and IgA. Comparative studies on J chain suggest a possible enigmatic function for this molecule other than the Ig polymerization and mucosal transport roles first described in mammals [17]. Dipnoi fish, such as the African lungfishes, are sarcopterygian or lobed-fin fishes with a very interesting phylogenetic position. We provide amino acid sequence comparisons with other vertebrate J chains and give insights into the function of J chain in lungfish by investigating its expression in central and mucosal tissues in an infection model as well as the cellular co-expression of J chain with IgM and IgW. We show that J chain is not confined to the B-cell compartment but is expressed in non-lymphoid cells like the gut epithelial cells

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Results

Discussion