Was the evolutionary road towards adaptive immunity paved with endothelium?

Biology Direct

Gustav van Niekerk¹  Tanja Davis¹  Anna-Mart Engelbrecht¹ 

[1] Department of Physiological Sciences, Stellenbosch University, Matieland, Stellenbosch 7600, South Africa

关键词: Invertebrate;    Vertebrate;    Inflammation;    Endothelium;    Evolutionary constraint;    Adaptive immune system;   

Others  :  1225786
DOI  :  10.1186/s13062-015-0079-0

 received in 2015-06-11, accepted in 2015-09-02,  发布年份 2015

【 摘 要 】

Background

The characterization of a completely novel adaptive immune system (AIS) in jawless vertebrates (hagfish and lampreys) presents an excellent opportunity for exploring similarities and differences in design principles. It also highlights a somewhat neglected question Why did vertebrates, representing only 5 % of all animals, evolve a system as complex as an AIS twice, whereas invertebrates failed to do so? A number of theories have been presented in answer to this question. However, these theories either fail to explain why invertebrates would not similarly develop an AIS and are confounded by issues of causality, or have been challenged by more recent findings.

Presentation of the hypothesis

Instead of identifying a selective pressure that would drive the development of an AIS, we hypothesise that invertebrates failed to develop an AIS because of the evolutionary constraints imposed by these animals’ physiological context. In particular, we argue that a number of vascular innovations in vertebrates allowed the effective implementation of an AIS. A lower blood volume allowed for a higher antibody titer (i.e., less ‘diluted’ antibody concentration), rendering these immune effectors more cost-effective. In addition, both a high circulatory velocity and the ability of endothelium to coordinate immune cell trafficking promote ‘epitope sampling’. Collectively, these innovations allowed the effective implementation of AIS in vertebrates.

Testing the hypothesis

The hypothesis posits that a number of innovations to the vascular system provided the release from constraints which allowed the implementation of an AIS. However, this hypothesis would be refuted by phylogenetic analysis demonstrating that the AIS preceded these vascular innovations. The hypothesis also suggests that vascular performance would have an impact on the efficacy of an AIS, thus predicting a correlation between the vascular parameters of a species and its relative investment in AIS. The contribution of certain vascular innovations in augmenting immune functionality of an AIS can be tested by modelling the effect of different vascular parameters on AIS efficacy.

Implications of the hypothesis

The hypothesis not only explains the immunological dimorphism between vertebrates and invertebrates but also brings to attention the fact that immunity is dependent on more than just an immune system.

Reviewers

This article was reviewed by Dr. Jun Yu and Prof. Neil Greenspan.

【 授权许可】

   
2015 van Niekerk et al.

【 图 表 】

Fig. 1.

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