The Diverse Transformer (Trf) Protein Family in the Sea Urchin Paracentrotus lividus Acts through a Collaboration between Cellular and Humoral Immune Effector Arms.

Iryna Yakovenko,Matan Oren,Benyamin Rosental,Or Ioscovich,Asaf Donnyo

doi:10.3390/ijms22136639

Abstract

Sea urchins are long-living marine invertebrates with a complex innate immune system, which includes expanded families of immune receptors. A central immune gene family in sea urchins encodes the Transformer (Trf) proteins. The Trf family has been studied mainly in the purple sea urchin Strongylocentrotus purpuratus. Here, we explore this protein family in the Mediterranean Sea urchin Paracentrotus lividus. The PlTrf genes and predicted proteins are highly diverse and show a typical Trf size range and structure. Coelomocytes and cell-free coelomic fluid from P. lividus contain different PlTrf protein repertoires with a shared subset, that bind specifically to E. coli. Using FACS, we identified five different P. lividus coelomocyte sub-populations with cell surface PlTrf protein expression. The relative abundance of the PlTrf-positive cells increases sharply following immune challenge with E. coli, but not following challenge with LPS or the sea urchin pathogen, Vibrio penaeicida. Phagocytosis of E. coli by P. lividus phagocytes is mediated through the cell-free coelomic fluid and is inhibited by blocking PlTrf activity with anti-SpTrf antibodies. Together, our results suggest a collaboration between cellular and humoral PlTrf-mediated effector arms in the P. lividus specific immune response to pathogens.

Highlights

Sea urchins are long-living marine invertebrates that are constantly exposed in nature to pathogens in the marine environment through direct contact with marine substrates, seawater, and consumed food.For protection, they have evolved a very sophisticated and robust innate immune system with multiple effector arms and a wide genome representation of immune genes [2]
We show that a challenge with heat-killed E. coli is followed by a sharp increase in the ratios of Trfpositive coelomocytes and that the P. lividus response to E. coli challenge is likely mediated by a specific set of PlTrf proteins
No Trf sequences have been identified in non-echinoid echinoderm classes such as sea stars and sea cucumbers nor in basal sea urchins such as pencil sea urchin Eucidaris tribuloides of the cidaroid order (Figure 1A), suggesting the Trf family is unique to higher sea urchins [25]

Summary

Introduction

Sea urchins are long-living marine invertebrates (estimated life-span of ~15 years on average for P. lividus [1]) that are constantly exposed in nature to pathogens in the marine environment through direct contact with marine substrates, seawater, and consumed food. They have evolved a very sophisticated and robust innate immune system with multiple effector arms and a wide genome representation of immune genes [2]. The Trf protein family (formerly termed 185/333) was first identified in the California purple sea urchin Strongylocentrotus purpuratus [6]. In S. purpuratus, a robust Trf-mediated response was documented upon challenge with bacteria including Escherichia coli and Vibrio diazotrophicus [8,9]

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Results

Conclusion