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Chitin Metabolism in Insects

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Chitin Metabolism in Insects 7 Chitin Metabolism in Insects Subbaratnam Muthukrishnan Kansas State University, Manhattan, KS, USA Hans Merzendorfer University of Osnabrueck, Osnabrueck, Germany Yasuyuki Arakane Chonnam National University, Gwangju, South Korea Karl J Kramer Kansas State University, and USDA-ARS, Manhattan, KS, USA © 2012 Elsevier B.V. All Rights Reserved 7.1. Introduction 193 7.2. Chitin Structure and Occurrence 193 7.3. Chitin Synthesis 194 7.3.1. Sites of Chitin Biosynthesis 195 7.3.2. Chitin Biosynthetic Pathway 197 7.3.3. Chitin Synthases: Organization of Genes and Biochemical Properties 199 7.3.4. Chitin Synthases: Regulation and Function 203 7.4. Chitin Degradation and Modification 205 7.4.1. Insect Chitinases 207 7.4.2. Insect N-Acetylglucosaminidases 211 7.4.3. Insect Chitin Deacetylases 214 7.5. Chitin-Binding Proteins 216 7.5.1. Chitin-Binding Proteins with the R&R Consensus 217 7.5.2. Peritrophic Matrix Proteins 217 7.5.3. Cuticular Proteins Analogous to Peritrophins (CPAPs) 218 7.5.4. Enzymes of Chitin Metabolism 219 7.5.5. Role of Secondary Structure of ChtBD2 Motif in Binding to Chitin 219 7.6. Chitin-Organizing Proteins 219 7.7. Hormonal Regulation of Chitin Metabolism 220 7.8. Chitin Metabolism and Insect Control 221 7.8.1. Inhibition of Chitin Synthesis 221 7.8.2. Exploiting Chitinases for Insect Control 223 7.9. Future Studies and Concluding Remarks 225 7.1. Introduction significantly. In this chapter we will highlight some of the “Chitin Metabolism in Insects” was the title of chapters more recent and important findings, with emphasis on in both the original edition of the Comprehensive Insect results obtained from studies conducted on the synthesis, Physiology, Biochemistry and Pharmacology series published structure, physical state, modification, organization, and in 1985 and the follow-up Comprehensive Molecular Insect degradation of chitin in insect tissues, as well as the inter- Science series in 2005 (Kramer et al., 1985; Kramer and play of chitin with chitin-binding proteins, the regulation Muthukrishnan, 2005). Since 2005 substantial progress of genes responsible for chitin metabolism, and, finally, the in gaining additional understanding of this topic has con- targeting of chitin metabolism for insect-control purposes. tinued to take place, primarily through the application of the techniques of molecular genetics, functional genom- 7.2. Chitin Structure and Occurrence ics, proteomics, transcriptomics, metabolomics, and bio- technology to an assortment of studies focused on insect Chitin is the major polysaccharide present in insects and chitin metabolism. Several other reviews have also been many other invertebrates as well as in several microbes, published that have reported on some of the advances that including fungi. Structurally, it is the simplest of the glycos- have taken place (Dahiya et al., 2006; Merzendorfer, 2006, aminoglycans, being a β(1→4) linked linear homopolymer 2009; Arakane and Muthukrishnan, 2010). Most inter- of N-acetylglucosamine (GlcNAc, [C8H13O5N]n, where estingly, the list of genes and gene products found to be n> > 1). It serves as the skeletal polysaccharide of several involved in insect chitin metabolism has been lengthened animal phyla, such as the Arthropoda, Annelida, Molluska, DOI:10.1016/B978-0-12-384747-8.10007-8 194 7: Chitin Metabolism in Insects and Coelenterata. In several groups of fungi, chitin replaces Alpha-chitin fibers, because of their hydrophilic nature, cellulose as the structural polysaccharide. In insects, it is are generally highly hydrated. Chitin dehydration via found in the body wall or cuticle, gut lining or peritrophic impregnation of hydrophobic proteins probably contributes matrix (PM), salivary gland, trachea, eggshells, and muscle to tissue stiffening and deplasticization (Vincent, 2009). In attachment points. In the course of evolution, insects have addition, the formation of a cross-linked and interpenetrat- made excellent use of the rigidity and chemical stability of ing protein network in the dehydrated composite leads to the polymeric chitin to assemble both hard and soft extra- additional hardening (Andersen, 2010); thus, chemical cellular structures such as the cuticle (exoskeleton) and PM bonds surely play a crucial role in cuticle mechanics by respectively, both of which enable insects to be protected increasing the load carried by the proteins and by provid- from the environment while allowing for growth, mobil- ing a hydrophobic “coating” around the chitin nanofibers, ity, respiration, and communication. All of these structures thus preventing softening of the latter by water adsorption. are primarily composites of chitin fibers and proteins with Chitin nanofibrils probably form the initial template, simi- varying degrees of hydration and trace materials distrib- lar to glass or carbon fiber mats in composite processing. uted along the structures. The insolubility and structural Filler proteins and catechols are then secreted through the complexity of the cuticle has limited its study. However, chitinous procuticle. Once oxidation of catechols to qui- sclerotized cuticle can be modeled as an interpenetrat- nones and quinone methides has occurred, cross-linking ing network of chitin fibers with embedded cross-linked and hardening of the extracellular matrix ensues. As sclero- protein and pigments. Both synthesis and degradation of tization proceeds, water is progressively expelled. The pre- chitin take place at multiple developmental stages in the cise role of water removal on the structural properties of the cuticle and the PM. It is usually synthesized as portions cuticle is not fully understood, in part because the effect of of the old endocuticle and PM and trachaea are resorbed, water on individual components of the composite is poorly and the digested materials are recycled. Although primar- understood, but some progress is starting to take place. ily composed of poly-GlcNAc, chitin also can contain a Also, the individual contributions of chitin and protein to small percentage of unsubstituted (or N-deacetylated) glu- the mechanical properties are unknown. In the hydrated cosamine (GlcNAc) residues, making it a GlcNAc-GlcN state, there is considerable variation in moduli reported for heteropolymer (Muzzarelli, 1973; Fukamizo et al., 1986). chitosan/chitin scaffolds (Wuet al., 2006). There is a dif- When the epidermal and gut cells synthesize and secrete a ference of several orders of magnitude in the stiffness of particular form of chitin consisting of antiparallel chains or chitin/chitosan between the fully hydrated state, where it alpha-chitin, the chains are assembled into microfibrils and is present as a porous, water-saturated scaffold, and the dry then into sheets. As layers of chitin are added, the sheets state. To mimic the action of catechols to stiffen chitosan are cross-oriented relative to one another at a constant scaffolds, Wuet al. (2005) achieved a two-fold increase in angle to form a helicoidal bundle (known as the Bouligand stiffness after treatment of chitosan films with oxidized cat- structure), which can contribute to the formation of an echols. Although there was a significant increase in stiff- extremely strong, plywood-like material. ness, it was less than the increase observed from insect Although there is no doubt that there are strong non- cuticle tanning. Recently, dynamic mechanical analysis of covalent interactions between chitin and chitin-binding insect cuticle during maturation revealed that while the proteins, there is only weak indirect evidence that there water content has an important role in determining cuticle are covalent interactions between them. The evidence so mechanical properties, the tanning reactions themselves far for direct involvement of chitin in cross-links to pro- contribute substantially to these properties beyond sim- teins has been inconclusive. Results of solid state NMR ply inducing dehydration (Lomakin et al., 2011). Cuticle, and chemical analyses have indicated the presence of trace whether tanned or untanned, increases in hardness while levels of aromatic amino acids in chitin preparations, drying, but the increase is generally less than that observed suggesting that those amino acids were there because from tanning alone. they were involved in protein cross-links with chitin (Schaefer et al., 1987). Additional spectroscopic evidence 7.3. Chitin Synthesis for glucosamine–catecholamine adducts derived from chi- tin–protein cross-links in cuticle was obtained using elec- Although extensive knowledge on the precise molecular trospray mass spectrometry and tandem mass spectrometry mechanism of chitin synthesis is lacking, substantial prog- (Kerwin et al., 1999). However, those observations have ress has been made regarding the function and regulation not been investigated further. More direct evidence for of several genes involved in the chitin biosynthetic pathway. chitin–protein cross-links from studies of intact cuticle In the past 10 years, many genes coding for key enzymes of instead of degraded or digested samples is needed before this pathway have been isolated and sequenced from various the precise nature of the covalent interactions of cuticu- insect species. Analyses of their expression in different tis- lar proteins with chitin fibers can be resolved (Demolliens sues during development have provided the first clues about et al., 2008). their function. The availability of Drosophila melanogaster 7: Chitin Metabolism in Insects 195 (fruit fly) mutants defective
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