Physical Chemical Barriers and Evasion Behavior

Metazoans are endowed with an innate immune defense that provides protection against infection and consists of five interconnected components: (1) physical barriers to prevent microbial invasion (2) constitutive chemical shields to inhibit microbial growth; (3) recognition systems to identify the entry of foreign microorganisms; (4) inducible antimicrobial responses triggered by the recognition system; (5) cellular recruitment processes to amplify and enhance defense (Akira et al. 2006).

Currently, it seems that the innate immune response of nematodes relies on four of these components. Like all metazoans C. elegans is equipped with a panoply of defense mechanisms, both constitutive and inducible. However, an obvious cellular defense response consisting of phagocytosis and/or encapsulation of invading microorganisms remains to be demonstrated in the worm. Although the body cavity of the worm is filled with pseudocoelomic fluid that contains coelomocytes, which are candidate macrophages, a role in microorganism engulfment and disposal has not been established. Likewise, C. elegans lacks several characteristics of animal humoral immune systems such as a phenoloxidase pathway. In Drosophila this defense cascade is believed to target Gram-positive bacterial challenges and involves the release of cytotoxic reactive oxygen species.

Primary defense in nematodes is provided by the multi-layered cuticle, which offers a superb physical barrier against external aggressions. Secondly, they are equipped not only with a muscular grinder that breaks down bacteria but also with an intestine which generates an environment hostile to microbial colonization. A complete transcript inventory of the C. elegans intestine reveals an arsenal of secretory proteins with roles in bacterial digestion (lysozymes, saposins, lipases, lectins and proteases), detoxification and stress responses (thaumatin-like, ABC transporters) (McGhee et al. 2007). Furthermore, the worm has a sophisticated chemosensory system, which enables it to sense different bacteria and to learn how to discriminate between innocuous and pathogenic microbes (reviews by Schulenburg and Boehnisch 2008; Zhang 2008). For an organism that lives in decaying matter and feeds on microorganisms, an efficient pathogen avoidance behavior appears to be one of the best strategies to escape infectious diseases. In the case of S. marcescens Db10, for example the nematode avoids this pathogenic bacterium by detecting the natural secreted product serrawettin W2 (Pradel et al. 2007). Physical evasion of S. marcescens and serrawettin requires the function of the only C. elegans Toll-like receptor gene, tol-1 (Pradel et al. 2007; Pujol et al. 2001). This is substantiated by data showing that partial loss-of-function mutants are defective in avoiding the bacterial lawn of Db10. Another example comes from work with M. nematophilum, where it has been shown that C. elegans avoids the smell of this infectious bacterial pathogen through tax-4 and tax-2 cGMP-gated channels (Yook and Hodgkin 2007). Although these genes are required in the chemosensory neurons for pathogen and hyperoxia avoidance (Chang et al. 2006), they are also likely to play a role in coordinating the secretion of the components of the cuticle that mediate adhesion by M. nematophilum to the rectum of infected animals.

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