Abstract
C-type lectins (CTLs) are a family of carbohydrate-recognition domain (CRD)-containing proteins that bind to ligands in a calcium-dependent manner. CTLs act as important components of insect innate immune responses, such as pattern recognition, agglutination, encapsulation, melanization, phagocytosis and prophenoloxidase activation, as well as gut microbiome homeostasis maintenance, to defend against pathogens. Besides, some insect CTLs can facilitate pathogen infection and colonization. In this review, we describe the properties of insect CTLs and focus on explaining their role in viral, bacterial, parasitic and fungal infections.
Y Zhu and X Yu are equally contributed to this work.
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5.1 Introduction
Insects are the most diverse group of organisms on Earth, occupying an extremely important position in the ecosystem. Over long-term evolution in an adverse environment with various pathogens, insects have developed a unique innate immune system involving cellular immunity and humoral immunity (Sadd and Siva-Jothy 2006). Cellular immunity depends mainly on blood cells that engulf foreign antigens by phagocytosis. The humoral immune system is an open and complete defence system consisting of lectins, antimicrobial peptides (AMPs), antiviral factors, lysozyme and protease inhibitors, and multifunctional blood cells (Hillyer 2015). Because of their inability to synthesize specific antibodies, invertebrates rely solely on non-specific immune responses to defend against pathogens. Upon pathogen invasion, insect immunity utilizes pattern-recognition proteins (PRPs) to help recognize pathogen-associated molecular patterns (PAMPs). There are many types of PRPs in insects, including peptidoglycan-recognition proteins (PGRPs), beta-1,3-glucan recognition proteins (bGRPs), scavenger receptors (SCRs), and C-type lectins (CTLs). Within the PRPs, CTLs play one of the most important roles and form the most diverse family (Zhang et al. 2015).
CTLs are a superfamily of carbohydrate-binding proteins and have a characteristic carbohydrate-recognition domain (CRD) (Dodd and Drickamer 2001) that binds to carbohydrates in a calcium-dependent manner (Drickamer 1993; Weis et al. 1998; Drickamer 1999). Some CRD-containing proteins are referred to as C-type lectin-like domain (CTLD) proteins, and with the continuous growth of the family, a few have been found that do not depend on calcium for binding activity (Zelensky and Gready 2005; Pees et al. 2016). Insect C-type lectins have various functional domains, including single CRDs, double CRDs (the immulectin group) and other functional domains (the CTL-X group). In the CTL-X group, functional domains containing complement control protein (CCP), immunoglobulin modules (Ig), an extracellular domain (CUB), epidermal growth factor-like domain (EGFL) and chitin binding domain (CBM) have been identified (Rao et al., 2015a, b; Waterhouse et al. 2007; Xia et al. 2015). Most insect CTLs have signal peptides, indicating that they are secreted proteins, while some CTLs contain transmembrane domains.
Recently, many works have reported the important position of CTLs in insect innate immune defence against microorganisms. Some insect CTLs play important roles as pattern-recognition receptors by binding invading pathogens and mediating immune responses, such as agglutination, encapsulation, melanization, phagocytosis and prophenoloxidase activation, to clear the pathogens. Certain other CTLs, however, have the opposite function; they facilitate pathogen infection. Thus, we will mainly focus on explaining the role of insect C-type lectins in viral, bacterial, parasitic and fungal infections.
5.2 Insect C-Type Lectin and Viral Infections
Multiple C-type lectins have been identified as susceptibility factors for viral infection in mosquitoes. Arthropod-borne viruses (arboviruses) are named for their unique method of transmission, via the bite of an arthropod vector, among which dengue virus (DENV), Zika virus (ZIKV), yellow fever virus (YFV), West Nile virus (WNV), Japanese encephalitis virus (JEV) and chikungunya virus (CHIKV) are transmitted by mosquito vectors and pose a major threat to human health (Zhu et al. 2017). These viruses enter the mosquito by an infectious blood meal and infect the vector in a sequential manner; first, the midgut epithelium is infected, and then the surrounding tissues become infected before the virus disseminates to the salivary gland (Guzman et al. 2016). During this process, viruses are able to utilize mosquito C-type lectins to facilitate infection. A previous study identified an Aedes aegypti C-type lectin, mosGCTL-1, which facilitates WNV infection in vitro and in vivo. The expression of mosGCTL-1 is upregulated by WNV, and it interacts with WNV in a calcium-dependent manner. mosGCTL-1 also plays an important role in WNV infection by interacting with a mosquito homologue of human CD45 (mosPTP-1), which enables viral attachment to cells and facilitates viral entry (Cheng et al. 2010). In addition, Liu and colleagues first identified 9 Aedes aegypti mosGCTL genes as key susceptibility factors for DENV-2 infection, among which mosGCTL-3 was found to most significantly enhance viral infectivity by interacting with the DENV-2 envelope protein in vitro and in vivo. In contrast, antisera against multiple lectins efficiently reduced DENV-2 infection during a mosquito blood meal (Liu et al. 2014). Other studies have also shown that mosGCTL-7 can bind to the JEV envelope protein via an N-glycan at N154 in a calcium-dependent manner. After binding, cell surface mosPTP-1 interacts with the mosGCTL-7-JEV complex and facilitates viral infection in vitro and in vivo (Liu et al. 2017).
In contrast to these viral infection facilitating roles in insects, C-type lectins can also induce protective responses during viral infections of insects. Spodoptera exigua C-type lectins (bracovirus-like lectins, Se-BLLs) are acquired by horizontal gene transfer and confer an adaptive advantage against baculovirus, a natural viral pathogen of S. exigua. Specifically, Se-BLL2 can reduce the pathogenicity of baculovirus, indicating that lectins can increase the resistance of S. exigua larvae to baculoviral infection (Gasmi et al. 2015). In addition, another lectin derived from Spodoptera, Se-BLL3, is able to reduce the mortality of Spodoptera frugiperda larvae during Junonia coenia densovirus (JcDV) infection, but no such effect is found in S. exigua larvae (Gasmi et al. 2018). Recently, two novel C-type lectins (MdCTLs) have been obtained from Musca domestica and show agglutination and antiviral properties in the laboratory. Interestingly, MdCTL-2 protein can inhibit the replication of influenza H1N1 virus, resembling the effect of ribavirin (Zhou et al. 2018).
Taken together, these studies show that insect C-type lectins play various roles in immune responses upon viral infection. Investigating the effect of C-type lectins during arbovirus infection may provide a better understanding of the replication of the virus in insects and shed light on new strategies for arbovirus transmission control. For instance, a transmission-blocking strategy may be feasible by blocking the C-type lectins that facilitate viral infection. Additionally, identifying novel insect C-type lectins may also lead to the discovery of new antiviral proteins.
5.3 Insect C-Type Lectins and Bacterial Infection
Insects utilize multiple immune systems to control bacterial overgrowth and maintain gut microbiome homeostasis. Specifically, C-type lectins are a large group of proteins in insects known for their ability to regulate bacterial survival and colonization. The role of insect C-type lectin in antibacterial immunity has been identified for Manduca sexta (Yu et al. 1999a, b). The M. sexta genome encodes 34 C-type lectins, among which is M. sexta immulectin-1 (MsIML-1), which was first cloned from the larval fat body. MsIML-1 expression is induced by the injection of inactivated gram-positive and gram-negative bacteria or yeast, and it is highly expressed in insect immune tissues, such as fat body and haemolymph, after bacterial infection. Recombinant MsIML-1 protein impairs bacterial growth by agglutinating bacteria and stimulating the activation of prophenoloxidase (PPO) (Yu et al. 1999a). Immulectin-2 from M. sexta (MsIML-2) was also isolated from the larval fat body and is induced by Escherichia coli and Saccharomyces cerevisiae. However, MsIML-2 has not been measured in haemocytes after bacterial stimulation. MsIML-2 can agglutinate E. coli in a calcium-dependent manner but has no effect on the agglutination of S. cerevisiae (Yu and Kanost 2000). M. sexta immulectin-3 (MsIML-3) and immulectin-4 (MsIML-4) cDNA has also been cloned from the larval fat body. By coating the proteins onto agarose beads, it has been shown that MsIML-4 can facilitate encapsulation and melanization by haemocytes in vitro, while MsIML-3 only enhances encapsulation in vitro (Yu et al. 2005, 2006). The silkworm Bombyx mori genome encodes 23 CTL genes (Rao et al. 2015b). A recent study revealed that C-type lectin-S3 from silkworm B. mori (BmCTL-S3) is expressed in various tissues, including the fat body, haemocytes, midgut, Malpighian tubule, ovary and embryo. The BmCTL-S3 protein facilitates the rapid clearance of E. coli, S. aureus, Serratia marcescens and Bacillus subtilis by binding to bacterial cell wall components (Zhan et al. 2016). Shahzad and colleagues also cloned a C-type lectin-S2 (BmCTL-S2) from the silkworm B. mori and performed functional analyses, which suggested that BmCTL-S2 is a pattern-recognition receptor with antibacterial activity (Shahzad et al. 2017). In the mosquito field, Schnitger and colleagues identified two CTLs from Anopheles gambiae, which are required for the clearance of E. coli but not S. aureus (Schnitger et al. 2009). These results reveal that multifunctional CTLs in insects can promote the interaction between host and bacteria. A better understanding of the molecular mechanism of the antibacterial activity of CTLs may provide novel strategies for bacterial defence.
In addition, CTLs function as pattern-recognition receptors and exhibit antimicrobial activity in invertebrates other than insects. A recent study identified a novel soluble and bacteria-inducible PRR, Leulectin, containing a CTLD from the hepatopancreas of kuruma shrimp Marsupenaeus japonicus. This CTLD can agglutinate bacteria and promote haemocytic phagocytosis by recognizing LPS (Wang et al. 2017a, b). Another CTL, PmCLec, from the black tiger shrimp Penaeus monodon, was characterized. Purified recombinant PmCLec protein binds and agglutinates gram-positive bacteria, Staphylococcus aureus and S. haemolyticus, in the presence of calcium (Wongpanya et al. 2017). A mannose-binding CTL called FmLC3 was isolated from Fenneropenaeus merguiensis and exhibits agglutination activity against various microbial strains in a calcium-dependent manner (Runsaeng et al. 2017). Moreover, a CTL named MjCC-CL in the kuruma shrimp (Marsupenaeus japonicus) contains both a CTLD and a coiled-coil domain (CCD). In an antibacterial response, the CTLD recognizes bacterial glycans leading to the interaction of the CCD with the surface receptor Domeless and subsequent activation of the JAK/STAT pathway and upregulation of AMP expression (Sun et al. 2017).
Most CTLs serve as immune factors suppressing bacterial growth in insects. However, some mosquito C-type lectins function as immune factors facilitating bacterial growth. Pang and colleagues revealed that blockade of mosGCTLs suppresses the growth of gut bacteria in Aedes aegypti and Culex pipiens pallens. It has been demonstrated that mosGCTLs function by directly coating bacterial cells and neutralizing antimicrobial peptide (AMP)-mediated elimination (Pang et al. 2016). In summary, insect C-type lectins mediate the regulation of insect microbiome homeostasis via various mechanisms and show pleiotropic effects in insect–microbial interactions.
5.4 Insect C-Type Lectins and Parasite Infections
Malaria parasites must go through a complex life cycle in an Anopheles mosquito to establish an infection before being transmitted to a new host. Osta and colleagues conducted a large-scale functional screen of mosquito genes and identified two C-type lectins (CTL4 and CTLMA2), which act as protective agonists for the development of Plasmodium ookinetes to oocysts and facilitate parasite susceptibility by inhibiting parasite melanization (Osta et al. 2004). Recently, Simoes and colleagues found that protection against parasite melanization by CTL4 and CTLMA2 in A. gambiae mosquitoes is dependent on infection intensity. Interestingly, CTL4 and CLTMA2 exert agonistic and antagonistic parasite regulation effects in different Anopheles species. (Simoes et al. 2017). However, silencing of CTL4 and CTLMA2 has no effect on Plasmodium falciparum development in humans (Cohuet et al. 2006). Additionally, Shin and colleagues identified a novel gene, CLSP2, encoding C-type lectin domains. Knockdown of CLSP2 activates prophenoloxidase and thus inhibits parasite growth, suggesting that CLSP2 is an antagonist of Plasmodium parasite infection in mosquitoes (Shin et al. 2011).
Recently, another CTL was found in the cotton bollworm Helicoverpa armigera (HaCTL3), which is involved in defence against parasites. HaCTL3 enhances haemocytic encapsulation and melanization by interacting with β-integrin. The expression of HaCTL3 is induced by 20-hydroxyecdysone (20E) treatment while silencing of the 20E receptor can abolish this response (Wang et al. 2017a, b).
Indeed, C-type lectins play various roles in host–parasite interactions. Investigating and understanding these dramatically different CTL mechanisms during the parasite defence process may lead to novel strategies to inhibit parasite transmission. Notably, Yoshida and colleagues generated transgenic mosquitoes expressing the C-type lectin from sea cucumber Cucumaria echinata, which impairs Plasmodium berghei oocyst formation. It is the first established Anopheles mosquito engineered to block parasite transmission (Yoshida et al. 2007).
5.5 Insect C-Type Lectins and Fungal Infection
Upon fungal infection, the innate immune system of insects must perform all defence functions because of the lack of adaptive immunity. Therefore, C-type lectins act as an important component in the defence against fungal infections in insects. Tian and colleagues identified a C-type lectin from Helicoverpa armigera (Halectin), which promotes haemocyte phagocytosis of pathogens and protects the insect from fungal infection (Tian et al. 2009). In addition, C-type lectin 14 (CTL14) from H. armigera is induced in the fifth larval stage by entomopathogen Beauveria bassiana infection specifically. Recombinant CTL14 protein can aggregate B. bassiana in vitro while silencing of CTL14 decreases the resistance to fungal infection in H. armigera (Cheng et al. 2018). Recently, to investigate the role of the JAK/STAT signalling pathway in the antifungal immune response of silkworm Bombyx mori, Geng and colleagues revealed that B. mori C-type lectin 5 (BmCTL5) is induced by Beauveria bassiana infection and showed that BmCTL5 might be a pattern-recognition receptor for the JAK/STAT signalling pathway in silkworms (Geng et al. 2016).
5.6 Conclusion
Insects utilize lectins to recognize pathogens, gain access to invaders through in vivo interactions, and eliminate exogenous invaders. Understanding the role of insect lectins in the insect immune system may provide insight into the interactions between pathogens and their hosts. Insect CTL genes regulate various innate immune responses, including pattern recognition, agglutination, encapsulation, melanization, phagocytosis and prophenoloxidase activation, as well as the maintenance of gut microbiome homeostasis. Some CTLs have specialized functions, such as stimulating cell proliferation (Table 5.1).
Mosquitoes are one of the major insect vectors of several human diseases in the world. The mosquito immune response regulates pathogen infection and transmission via multiple pathways. Specifically, different C-type lectins from A. aegypti have been found to facilitate the infection of mosquitoes by various arboviruses, including WNV, DENV and JEV (Cheng et al. 2010; Liu et al. 2014, 2017). Furthermore, other CTLs that regulate flavivirus infection in mosquitoes may be identified by using bioinformatics methods to analyse homologous functional domains of the CLTs in mosquitoes. The development of strategies to inhibit certain C-type lectins in the flavivirus life cycle may be a promising strategy for flavivirus transmission control. A better understanding of the role of C-type lectins in insect gut ecology, maintaining gut microbiome homeostasis or dysregulating the gut microbiota, may offer a novel target for vector-borne disease control in nature (Pang et al. 2016).
Unfortunately, research on insect lectins is still extremely limited. While a few studies have focused on certain lectins from a specific species of insect, the molecular mechanisms underlying the interactions between pathogens and most lectins are poorly understood. Current knowledge of CTLs suggests that, in addition to mediating innate immune responses, some insect CTLs have unique functions, such as antimicrobial activity and stimulating cell proliferation, while other CTLs have multiple functions. Current research on CTLs mainly focuses on the functional analysis of individual CTLs, while a general and extensive CTL functional investigation in insects should be considered. A better understanding of insect CTLs may promote the development of novel antibacterial or viral transmission-blocking strategies. Further investigation into the functions and mechanisms of insect CTLs in innate immunity is expected because it may contribute to the protection of beneficial insects as well as the biological control of pests and disease vectors.
References
Cheng G, Cox J, Wang P, Krishnan MN, Dai J, Qian F, Anderson JF, Fikrig E (2010) A C-type lectin collaborates with a CD45 phosphatase homolog to facilitate West Nile virus infection of mosquitoes. Cell 142(5):714–725. https://doi.org/10.1016/j.cell.2010.07.038
Cheng Y, Lin Z, Wang JM, Xing LS, Xiong GH, Zou Z (2018) CTL14, a recognition receptor induced in late stage larvae, modulates anti-fungal immunity in cotton bollworm Helicoverpa armigera. Dev Comp Immunol 84:142–152. https://doi.org/10.1016/j.dci.2018.02.010
Cohuet A, Osta MA, Morlais I, Awono-Ambene PH, Michel K, Simard F, Christophides GK, Fontenille D, Kafatos FC (2006) Anopheles and Plasmodium: from laboratory models to natural systems in the field. EMBO Rep 7(12):1285–1289. https://doi.org/10.1038/sj.embor.7400831
Dodd RB, Drickamer K (2001) Lectin-like proteins in model organisms: implications for evolution of carbohydrate-binding activity. Glycobiology 11(5):71R–79R
Drickamer K (1993) Evolution of Ca(2+)-dependent animal lectins. Prog Nucleic Acid Res Mol Biol 45:207–232
Drickamer K (1999) C-type lectin-like domains. Curr Opin Struct Biol 9(5):585–590
Gasmi L, Boulain H, Gauthier J, Hua-Van A, Musset K, Jakubowska AK, Aury JM, Volkoff AN, Huguet E, Herrero S et al (2015) Recurrent domestication by lepidoptera of genes from their parasites mediated by bracoviruses. PLoS Genet 11:e1005470
Gasmi L, Jakubowska AK, Ferre J, Ogliastro M, Herrero S (2018) Characterization of two groups of Spodoptera exigua Hubner (Lepidoptera: Noctuidae) C-type lectins and insights into their role in defense against the densovirus JcDV. Arch Insect Biochem Physiol 97(1). https://doi.org/10.1002/arch.21432
Geng T, Lv DD, Huang YX, Hou CX, Qin GX, Guo XJ (2016) JAK/STAT signaling pathway-mediated immune response in silkworm (Bombyx mori) challenged by Beauveria bassiana. Gene 595(1):69–76. https://doi.org/10.1016/j.gene.2016.09.043
Guzman MG, Gubler DJ, Izquierdo A, Martinez E, Halstead SB (2016) Dengue infection. Nat Rev Dis Primers 2(1)
Hillyer JF (2015) Integrated immune and cardiovascular function in pancrustacea: lessons from the insects. Integr Comp Biol 55(5):843–855. https://doi.org/10.1093/icb/icv021
Liu Y, Zhang F, Liu J, Xiao X, Zhang S, Qin C, Xiang Y, Wang P, Cheng G (2014) Transmission-blocking antibodies against mosquito C-type lectins for dengue prevention. PLoS Pathog 10(2):e1003931. https://doi.org/10.1371/journal.ppat.1003931
Liu K, Qian Y, Jung YS, Zhou B, Cao R, Shen T, Shao D, Wei J, Ma Z, Chen P, Zhu H, Qiu Y (2017) mosGCTL-7, a C-type lectin protein, mediates Japanese encephalitis virus infection in mosquitoes. J Virol 91(10). https://doi.org/10.1128/jvi.01348-16
Osta MA, Christophides GK, Kafatos FC (2004) Effects of mosquito genes on Plasmodium development. Science 303(5666):2030–2032. https://doi.org/10.1126/science.1091789
Pang X, Xiao X, Liu Y, Zhang R, Liu J, Liu Q, Wang P, Cheng G (2016) Mosquito C-type lectins maintain gut microbiome homeostasis. Nat Microbiol 1:16023. https://doi.org/10.1038/nmicrobiol.2016.23
Pees B, Yang W, Zarate-Potes A, Schulenburg H, Dierking K (2016) High innate immune specificity through diversified C-type lectin-like domain proteins in invertebrates. J Innate Immun 8(2):129–142. https://doi.org/10.1159/000441475
Rao XJ, Cao X, He Y, Hu Y, Zhang X, Chen YR, Blissard G, Kanost MR, Yu XQ, Jiang H (2015a) Structural features, evolutionary relationships, and transcriptional regulation of C-type lectin-domain proteins in Manduca sexta. Insect Biochem Mol Biol 62:75–85. https://doi.org/10.1016/j.ibmb.2014.12.006
Rao XJ, Shahzad T, Liu S, Wu P, He YT, Sun WJ, Fan XY, Yang YF, Shi Q, Yu XQ (2015b) Identification of C-type lectin-domain proteins (CTLDPs) in silkworm Bombyx mori. Dev Comp Immunol 53(2):328–338. https://doi.org/10.1016/j.dci.2015.07.005
Runsaeng P, Puengyam P, Utarabhand P (2017) A mannose-specific C-type lectin from Fenneropenaeus merguiensis exhibited antimicrobial activity to mediate shrimp innate immunity. Mol Immunol 92:87–98. https://doi.org/10.1016/j.molimm.2017.10.005
Sadd BM, Siva-Jothy MT (2006) Self-harm caused by an insect’s innate immunity. Proc Biol Sci 273(1600):2571–2574. https://doi.org/10.1098/rspb.2006.3574
Schnitger AK, Yassine H, Kafatos FC, Osta MA (2009) Two C-type lectins cooperate to defend Anopheles gambiae against gram-negative bacteria. J Biol Chem 284(26):17616–17624. https://doi.org/10.1074/jbc.M808298200
Shahzad T, Zhan MY, Yang PJ, Yu XQ, Rao XJ (2017) Molecular cloning and analysis of a C-type lectin from silkworm Bombyx mori. Arch Insect Biochem Physiol 95(3). https://doi.org/10.1002/arch.21391
Shin SW, Zou Z, Raikhel AS (2011) A new factor in the Aedes aegypti immune response: CLSP2 modulates melanization. EMBO Rep 12(9):938–943. https://doi.org/10.1038/embor.2011.130
Simoes ML, Mlambo G, Tripathi A, Dong Y, Dimopoulos G (2017) Immune regulation of plasmodium is anopheles species specific and infection intensity dependent. MBio 8(5). https://doi.org/10.1128/mbio.01631-17
Sun JJ, Lan JF, Zhao XF, Vasta GR, Wang JX (2017) Binding of a C-type lectin’s coiled-coil domain to the Domeless receptor directly activates the JAK/STAT pathway in the shrimp immune response to bacterial infection. PLoS Pathog 13(9):e1006626. https://doi.org/10.1371/journal.ppat.1006626
Tian YY, Liu Y, Zhao XF, Wang JX (2009) Characterization of a C-type lectin from the cotton bollworm, Helicoverpa armigera. Dev Comp Immunol 33(6):772–779. https://doi.org/10.1016/j.dci.2009.01.002
Wang P, Zhuo XR, Tang L, Liu XS, Wang YF, Wang GX, Yu XQ, Wang JL (2017a) C-type lectin interacting with beta-integrin enhances hemocytic encapsulation in the cotton bollworm, Helicoverpa armigera. Insect Biochem Mol Biol 86:29–40. https://doi.org/10.1016/j.ibmb.2017.05.005
Wang XW, Gao J, Xu YH, Xu JD, Fan ZX, Zhao XF, Wang JX (2017b) novel pattern recognition receptor protects shrimp by preventing bacterial colonization and promoting phagocytosis. J Immunol 198(8):3045–3057. https://doi.org/10.4049/jimmunol.1602002
Waterhouse RM, Kriventseva EV, Meister S, Xi Z, Alvarez KS, Bartholomay LC, Barillas-Mury C, Bian G, Blandin S, Christensen BM, Dong Y, Jiang H, Kanost MR, Koutsos AC, Levashina EA, Li J, Ligoxygakis P, Maccallum RM, Mayhew GF, Mendes A, Michel K, Osta MA, Paskewitz S, Shin SW, Vlachou D, Wang L, Wei W, Zheng L, Zou Z, Severson DW, Raikhel AS, Kafatos FC, Dimopoulos G, Zdobnov EM, Christophides GK (2007) Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316(5832):1738–1743. https://doi.org/10.1126/science.1139862
Weis WI, Taylor ME, Drickamer K (1998) The C-type lectin superfamily in the immune system. Immunol Rev 163:19–34
Wongpanya R, Sengprasert P, Amparyup P, Tassanakajon A (2017) A novel C-type lectin in the black tiger shrimp Penaeus monodon functions as a pattern recognition receptor by binding and causing bacterial agglutination. Fish Shellfish Immunol 60:103–113. https://doi.org/10.1016/j.fsi.2016.11.042
Xia X, Yu L, Xue M, Yu X, Vasseur L, Gurr GM, Baxter SW, Lin H, Lin J, You M (2015) Genome-wide characterization and expression profiling of immune genes in the diamondback moth, Plutella xylostella (L.). Sci Rep 5:9877. https://doi.org/10.1038/srep09877
Yoshida S, Shimada Y, Kondoh D, Kouzuma Y, Ghosh AK, Jacobs-Lorena M, Sinden RE (2007) Hemolytic C-type lectin CEL-III from sea cucumber expressed in transgenic mosquitoes impairs malaria parasite development. PLoS Pathog 3(12):e192. https://doi.org/10.1371/journal.ppat.0030192
Yu XQ, Kanost MR (2000) Immulectin-2, a lipopolysaccharide-specific lectin from an insect, Manduca sexta, is induced in response to gram-negative bacteria. J Biol Chem 275(48):37373–37381. https://doi.org/10.1074/jbc.M003021200
Yu XQ, Gan H, Kanost MR (1999a) Immulectin, an inducible C-type lectin from an insect, Manduca sexta, stimulates activation of plasma prophenol oxidase. Insect Biochem Mol Biol 29(7):585–597
Yu XQ, Prakash O, Kanost MR (1999b) Structure of a paralytic peptide from an insect, Manduca sexta. J Peptide Res Off J Am Peptide Soc 54(3):256–261
Yu XQ, Tracy ME, Ling E, Scholz FR, Trenczek T (2005) A novel C-type immulectin-3 from Manduca sexta is translocated from hemolymph into the cytoplasm of hemocytes. Insect Biochem Mol Biol 35(4):285–295. https://doi.org/10.1016/j.ibmb.2005.01.004
Yu XQ, Ling E, Tracy ME, Zhu Y (2006) Immulectin-4 from the tobacco hornworm Manduca sexta binds to lipopolysaccharide and lipoteichoic acid. Insect Mol Biol 15(2):119–128. https://doi.org/10.1111/j.1365-2583.2006.00618.x
Zelensky AN, Gready JE (2005) The C-type lectin-like domain superfamily. FEBS J 272(24):6179–6217. https://doi.org/10.1111/j.1742-4658.2005.05031.x
Zhan MY, Shahzad T, Yang PJ, Liu S, Yu XQ, Rao XJ (2016) A single-CRD C-type lectin is important for bacterial clearance in the silkworm. Dev Comp Immunol 65:330–339. https://doi.org/10.1016/j.dci.2016.08.004
Zhang X, He Y, Cao X, Gunaratna RT, Chen YR, Blissard G, Kanost MR, Jiang H (2015) Phylogenetic analysis and expression profiling of the pattern recognition receptors: Insights into molecular recognition of invading pathogens in Manduca sexta. Insect Biochem Mol Biol 62:38–50. https://doi.org/10.1016/j.ibmb.2015.02.001
Zhou J, Fang NN, Zheng Y, Liu KY, Mao B, Kong LN, Chen Y, Ai H (2018) Identification and characterization of two novel C-type lectins from the larvae of housefly, Musca domestica L. Arch Insect Biochem Physiol 98(3):e21467. https://doi.org/10.1002/arch.21467
Zhu Y, Zhang R, Zhang B, Zhao T, Wang P, Liang G, Cheng G (2017) Blood meal acquisition enhances arbovirus replication in mosquitoes through activation of the GABAergic system. Nat Commun 8(1):1262. https://doi.org/10.1038/s41467-017-01244-6
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This work was funded by grants from the National Key Research and Development Plan of China (2018ZX09711003-004-003 and 2018YFA0507202), the Natural Science Foundation of China (81730063 and 31825001), the Shenzhen San-Ming Project for prevention and research on vector-borne diseases (SZSM201611064).
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Zhu, Y., Yu, X., Cheng, G. (2020). Insect C-Type Lectins in Microbial Infections. In: Hsieh, SL. (eds) Lectin in Host Defense Against Microbial Infections. Advances in Experimental Medicine and Biology, vol 1204. Springer, Singapore. https://doi.org/10.1007/978-981-15-1580-4_5
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