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Review
. 2016 May;58:102-18.
doi: 10.1016/j.dci.2015.12.006. Epub 2015 Dec 13.

Insect Immunology and Hematopoiesis

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Free PMC article
Review

Insect Immunology and Hematopoiesis

Julián F Hillyer. Dev Comp Immunol. .
Free PMC article

Abstract

Insects combat infection by mounting powerful immune responses that are mediated by hemocytes, the fat body, the midgut, the salivary glands and other tissues. Foreign organisms that have entered the body of an insect are recognized by the immune system when pathogen-associated molecular patterns bind host-derived pattern recognition receptors. This, in turn, activates immune signaling pathways that amplify the immune response, induce the production of factors with antimicrobial activity, and activate effector pathways. Among the immune signaling pathways are the Toll, Imd, Jak/Stat, JNK, and insulin pathways. Activation of these and other pathways leads to pathogen killing via phagocytosis, melanization, cellular encapsulation, nodulation, lysis, RNAi-mediated virus destruction, autophagy and apoptosis. This review details these and other aspects of immunity in insects, and discusses how the immune and circulatory systems have co-adapted to combat infection, how hemocyte replication and differentiation takes place (hematopoiesis), how an infection prepares an insect for a subsequent infection (immune priming), how environmental factors such as temperature and the age of the insect impact the immune response, and how social immunity protects entire groups. Finally, this review highlights some underexplored areas in the field of insect immunobiology.

Keywords: Hemocyte; Immune signaling; Immunity; Insecta; Pathogen; Pattern recognition receptor.

Figures

Figure 1
Figure 1
Anatomy of the insect immune system. The insect body cavity, called the hemocoel, is a fluid and dynamic space that houses tissues with immune activity. The primary immune cells are the hemocytes. Hemocytes are found in circulation (circulating hemocytes) and attached to tissues (sessile hemocytes), where they phagocytose, encapsulate and nodulate pathogens, and produce humoral immune factors. The fat body, the midgut, the salivary glands, and other tissues produce numerous humoral immune factors with, among other things, lytic and melanizing activity. For a description of how hemolymph circulation impacts immune responses, and the activity of periostial hemocytes, see figure 7.
Figure 2
Figure 2
Gene counts for select genes and gene families in Anopheles gambiae (Order: Diptera), Aedes aegypti (Diptera), Drosophila melanogaster (Diptera), Pediculus humanus humanus (Siphonaptera), Manduca sexta (Lepidoptera), Tribolium castaneum (Coleoptera), Apis mellifera (Hymenoptera), and Acyrthosiphon pisum (Hemiptera). The gene number data was collected from (Cao et al., 2015; Chevignon et al., 2015; Evans et al., 2006; Gerardo et al., 2010; He et al., 2015; Kim et al., 2011; Sackton et al., 2007; Waterhouse et al., 2007; Zhang et al., 2015; Zou et al., 2007), with additional searches in https://www.vectorbase.org and http://metazoa.ensembl.org. The evolutionary relationships between the species, depicted at the top of the figure, are based on (Trautwein et al., 2012). Gene numbers can vary slightly depending on the analysis. Abbreviations: PRR, pattern recognition receptor; Toll (vertical orientation), Toll pathway; Imd (vertical orientation), Imd pathway; Effector, effector peptides and proteins; PGRP, peptidoglycan recognition protein; FREP, fibrinogen-related protein; βGRP, β-1,3 glucan recognition protein; GNBP, Gram(−) binding protein; CTL, C-type lectin; PPO, pro-phenoloxidase.
Figure 3
Figure 3
Simplified diagram illustrating key players in the Toll, Imd, and Jak/Stat pathways, using mosquitoes as the example. For a description of the pathways, see section 4.
Figure 4
Figure 4
Immune effector mechanisms of insects. Insects kill pathogens via phagocytosis (section 5.1), melanization (section 5.2), cellular encapsulation (section 5.3), nodulation (section 5.4), lysis (section 5.5), RNA interference (section 5.6), autophagy (section 5.7), and apoptosis (section 5.8).
Figure 5
Figure 5
Biochemical pathway of phenoloxidase-based melanization. For a description of the pathway, see section 5.2. Abbreviations: PRR, pattern recognition receptor; βGRP, β-1,3 glucan recognition protein; CTL, C-type lectin; GNBP, Gram(−) binding protein; PPAE, phenoloxidase activating enzyme; PAH, phenylalanine hydroxylase; PO, phenoloxidase; DDC, dopa decarboxylase; DCE, dopachrome conversion enzyme.
Figure 6
Figure 6
Small interfering RNA pathway. For a description of this RNAi pathway, see section 5.6.
Figure 7
Figure 7
Co-adaptation of the insect circulatory and immune systems, as exemplified in mosquitoes. Hemocytes exist in two states: in circulation and in sessile form. In naïve mosquitoes (top), some of the sessile hemocytes are aggregated around the ostia (valves) of the heart, and are called periostial hemocytes. Hemolymph flow is swift in the regions surrounding the ostia (the periostial regions), and the majority of hemolymph enters the heart through the ostia located in abdominal segments 4, 5, and 6. Upon infection (bottom), circulating hemocytes undergo mitosis and increase in number, and many hemocytes migrate to, and aggregate in, the periostial regions of the heart where they phagocytose pathogens. The periostial regions are the only location of the body where sessile hemocytes increase in number in response to infection. Infection does not significantly alter the proportion of hemolymph that flows through each periostial region, and periostial hemocytes – including their immune activity – preferentially aggregate around the ostia that experience the most hemolymph flow. Figure from Sigle and Hillyer (Sigle and Hillyer, 2016); reproduced with permission.

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