Abstract
Macrophages are critical components of the antimicrobial response. The recent explosion of knowledge on the evolutionary, genetic, and biochemical aspects of the interaction between macrophages and microbes has renewed scientific interest in macrophages. The conservation of immune components or mechanisms between organisms during the evolutionary process allows us to elucidate antimicrobial mechanisms or discover new immune functions through the study of basal-branching organisms, such as invertebrates. As a result, immunity in non-vertebrates has attracted the attention of researchers in the last few decades. In this review, we summarize what is presently known about macrophage-like cells in various invertebrate species.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsAbbreviations
- PAMPs:
-
Pathogen-associated molecular patterns
- PGRP:
-
Peptidoglycan recognition protein
- PRR:
-
Pattern recognition receptor
- RNS:
-
Reactive nitrogen species
- ROS:
-
Reactive oxygen species
- TEP:
-
Thioester-containing protein
References
Abnave P, Mottola G, Gimenez G, Boucherit N, Trouplin V, Torre C, Conti F, Ben Amara A, Lepolard C, Djian B, Hamaoui D, Mettouchi A, Kumar A, Pagnotta S, Bonatti S, Lepidi H, Salvetti A, Abi-Rached L, Lemichez E, Mege JL, Ghigo E (2014) Screening in planarians identifies MORN2 as a key component in LC3-associated phagocytosis and resistance to bacterial infection. Cell Host Microbe 16(3):338–350
Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124(4):783–801
Bachere E, Rosa RD, Schmitt P, Poirier AC, Merou N, Charriere GM, Destoumieux-Garzon D (2015) The new insights into the oyster antimicrobial defense: cellular, molecular and genetic view. Fish Shellfish Immunol 46(1):50–64
Beaven AE, Paynter KT (1999) Acidification of the phagosome in Crassostrea virginica hemocytes following engulfment of zymosan. Biol Bull 196(1):26–33
Blaise C, Trottier S, Gagne F, Lallement C, Hansen PD (2002) Immunocompetence of bivalve hemocytes as evaluated by a miniaturized phagocytosis assay. Environ Toxicol 17(3):160–169
Blandin S, Levashina EA (2004) Thioester-containing proteins and insect immunity. Mol Immunol 40(12):903–908
Bosco-Drayon V, Poidevin M, Boneca IG, Narbonne-Reveau K, Royet J, Charroux B (2012) Peptidoglycan sensing by the receptor PGRP-LE in the Drosophila gut induces immune responses to infectious bacteria and tolerance to microbiota. Cell Host Microbe 12(2):153–165
Browne N, Heelan M, Kavanagh K (2013) An analysis of the structural and functional similarities of insect hemocytes and mammalian phagocytes. Virulence 4(7):597–603
Buchmann K (2014) Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol 5:459
Butt TM, Shields KS (1996) The structure and behavior of gypsy moth (Lymantria dispar) hemocytes. J Invertebr Pathol 68(1):1–14
Canesi L, Betti M, Ciacci C, Citterio B, Pruzzo C, Gallo G (2003) Tyrosine kinase-mediated cell signalling in the activation of Mytilus hemocytes: possible role of STAT-like proteins. Biol Cell 95(9):603–613
Canesi L, Gallo G, Gavioli M, Pruzzo C (2002) Bacteria-hemocyte interactions and phagocytosis in marine bivalves. Microsc Res Tech 57(6):469–476
Cheng TC (1975) Functional morphology and biochemistry of molluscan phagocytes. Ann N Y Acad Sci 266:343–379
Ciacci C, Betti M, Canonico B, Citterio B, Roch P, Canesi L (2010) Specificity of anti-Vibrio immune response through p38 MAPK and PKC activation in the hemocytes of the mussel Mytilus galloprovincialis. J Invertebr Pathol 105(1):49–55
Coulaud PJ, Lepolard C, Bechah Y, Berenger JM, Raoult D, Ghigo E (2015) Hemocytes from Pediculus humanus humanus are hosts for human bacterial pathogens. Front Cell Infect Microbiol 4:183
da Silva C, Dunphy GB, Rau ME (2000) Interaction of hemocytes and prophenoloxidase system of fifth instar nymphs of Acheta domesticus with bacteria. Dev Comp Immunol 24(4):367–379
de Azambuja P, Garcia ES, Ratcliffe NA (1991) Aspects of classification of Hemiptera hemocytes from six triatomine species. Mem Inst Oswaldo Cruz 86(1):1–10
Destoumieux D, Bulet P, Loew D, Van Dorsselaer A, Rodriguez J, Bachere E (1997) Penaeidins, a new family of antimicrobial peptides isolated from the shrimp Penaeus vannamei (Decapoda). J Biol Chem 272(45):28398–28406
Dodd RB, Drickamer K (2001) Lectin-like proteins in model organisms: implications for evolution of carbohydrate-binding activity. Glycobiology 11(5):71R–79R
Dziarski R, Gupta D (2006) The peptidoglycan recognition proteins (PGRPs). Genome Biol 7(8):232
Elrod-Erickson M, Mishra S, Schneider D (2000) Interactions between the cellular and humoral immune responses in Drosophila. Curr Biol 10(13):781–784
Epelman S, Lavine KJ, Randolph GJ (2014) Origin and functions of tissue macrophages. Immunity 41(1):21–35
Foukas LC, Katsoulas HL, Paraskevopoulou N, Metheniti A, Lambropoulou M, Marmaras VJ (1998) Phagocytosis of Escherichia coli by insect hemocytes requires both activation of the Ras/mitogen-activated protein kinase signal transduction pathway for attachment and beta3 integrin for internalization. J Biol Chem 273(24):14813–14818
Gaitanaki C, Kefaloyianni E, Marmari A, Beis I (2004) Various stressors rapidly activate the p38-MAPK signaling pathway in Mytilus galloprovincialis (Lam.). Mol Cell Biochem 260 (1–2):119–127
Gelinas M, Fortier M, Lajeunesse A, Fournier M, Gagnon C, Barnabe S, Gagne F (2014) Responses of freshwater mussel (Elliptio complanata) hemocytes exposed in vitro to crude extracts of Microcystis aeruginosa and Lyngbya wollei. Ecotoxicology (London, England) 23(2):260–266
Giulianini PG, Bierti M, Lorenzon S, Battistella S, Ferrero EA (2007) Ultrastructural and functional characterization of circulating hemocytes from the freshwater crayfish Astacus leptodactylus: cell types and their role after in vivo artificial non-self challenge. Micron 38(1):49–57
Gordon S (2008) Elie Metchnikoff: father of natural immunity. Eur J Immunol 38(12):3257–3264
Gordon S (2016) Phagocytosis: an immunobiologic process. Immunity 44(3):463–475
Hernandez S, Lanz H, Rodriguez MH, Torres JA, Martinez-Palomo A, Tsutsumi V (1999) Morphological and cytochemical characterization of female Anopheles albimanus (Diptera: Culicidae) hemocytes. J Med Entomol 36(4):426–434
Hillyer JF, Strand MR (2014) Mosquito hemocyte-mediated immune responses. Curr Opin Insect Sci 3:14–21
Imler JL (2014) Overview of Drosophila immunity: a historical perspective. Dev Comp Immunol 42(1):3–15
Jauzein C, Donaghy L, Volety AK (2013) Flow cytometric characterization of hemocytes of the sunray venus clam Macrocallista nimbosa and influence of salinity variation. Fish Shellfish Immunol 35(3):716–724
Jiang Q, Zhou Z, Wang L, Wang L, Yue F, Wang J, Song L (2013) A scallop nitric oxide synthase (NOS) with structure similar to neuronal NOS and its involvement in the immune defense. PloS One 8(7):e69158
Kaufmann SH, Dorhoi A (2016) Molecular determinants in phagocyte-bacteria interactions. Immunity 44(3):476–491
Khoo L, Robinette DW, Noga EJ (1999) Callinectin, an antibacterial peptide from blue crab, Callinectes sapidus, hemocytes. Mar Biotechnol (New York, NY) 1(1):44–51
Kinchen JM, Ravichandran KS (2008) Phagosome maturation: going through the acid test. Nat Rev 9(10):781–795
Koizumi N, Imai Y, Morozumi A, Imamura M, Kadotani T, Yaoi K, Iwahana H, Sato R (1999) Lipopolysaccharide-binding protein of Bombyx mori participates in a hemocyte-mediated defense reaction against gram-negative bacteria. J Insect Physiol 45(9):853–859
Kounatidis I, Ligoxygakis P (2012) Drosophila as a model system to unravel the layers of innate immunity to infection. Open Biol 2(5):120075
Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32(10):1295–1309
Lee SY, Lee BL, Soderhall K (2003) Processing of an antibacterial peptide from hemocyanin of the freshwater crayfish Pacifastacus leniusculus. J Biol Chem 278(10):7927–7933
Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, Kafatos FC (2001) Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104(5):709–718
Luckhart S, Cupp MS, Cupp EW (1992) Morphological and functional classification of the hemocytes of adult female Simulium vittatum (Diptera: Simuliidae). J Med Entomol 29(3):457–466
Matozzo V, Bailo L (2015) A first insight into haemocytes of the smooth venus clam Callista chione. Fish Shellfish Immunol 42(2):494–502
Mechnikov II (1905) Immunity in infective diseases. By Il’ia Il’ich Mechnikov, 1905. Rev Infect Dis 10(1):617
Medzhitov R, Preston-Hurlburt P, Janeway CA Jr (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388(6640):394–397
Molina-Cruz A, DeJong RJ, Charles B, Gupta L, Kumar S, Jaramillo-Gutierrez G, Barillas-Mury C (2008) Reactive oxygen species modulate Anopheles gambiae immunity against bacteria and Plasmodium. J Biol Chem 283(6):3217–3223
Myllymaki H, Valanne S, Ramet M (2014) The Drosophila imd signaling pathway. J Immunol 192(8):3455–3462
Nandety RS, Kuo YW, Nouri S, Falk BW (2015) Emerging strategies for RNA interference (RNAi) applications in insects. Bioengineered 6(1):8–19
Nappi AJ, Vass E, Frey F, Carton Y (2000) Nitric oxide involvement in Drosophila immunity. Nitric Oxide 4(4):423–430
Nonaka S, Nagaosa K, Mori T, Shiratsuchi A, Nakanishi Y (2013) Integrin alphaPS3/betanu-mediated phagocytosis of apoptotic cells and bacteria in Drosophila. J Biol Chem 288(15):10374–10380
O’Neill LA, Golenbock D, Bowie AG (2013) The history of Toll-like receptors—redefining innate immunity. Nat Rev Immunol 13(6):453–460
Pauletto M, Milan M, Moreira R, Novoa B, Figueras A, Babbucci M, Patarnello T, Bargelloni L (2014) Deep transcriptome sequencing of Pecten maximus hemocytes: a genomic resource for bivalve immunology. Fish Shellfish Immunol 37(1):154–165
Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS (2007) A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 3(3):e26
Pons J, Bauza-Ribot MM, Jaume D, Juan C (2014) Next-generation sequencing, phylogenetic signal and comparative mitogenomic analyses in Metacrangonyctidae (Amphipoda: Crustacea). BMC Genomics 15:566
Ramet M (2012) The fruit fly Drosophila melanogaster unfolds the secrets of innate immunity. Acta Paediatr 101(9):900–905
Rauta PR, Samanta M, Dash HR, Nayak B, Das S (2014) Toll-like receptors (TLRs) in aquatic animals: signaling pathways, expressions and immune responses. Immunol Lett 158(1–2):14–24
Royet J, Gupta D, Dziarski R (2011) Peptidoglycan recognition proteins: modulators of the microbiome and inflammation. Nat Rev Immunol 11(12):837–851
Sagi A, Manor R, Ventura T (2013) Gene silencing in crustaceans: from basic research to biotechnologies. Genes 4(4):620–645
Satake H, Sekiguchi T (2012) Toll-like receptors of deuterostome invertebrates. Front Immunol 3:34
Sellge G, Kufer TA (2015) PRR-signaling pathways: learning from microbial tactics. Semin Immunol 27(2):75–84
Shi XZ, Zhao XF, Wang JX (2014) A new type antimicrobial peptide astacidin functions in antibacterial immune response in red swamp crayfish Procambarus clarkii. Dev Comp Immunol 43(1):121–128
Su GL, Simmons RL, Wang SC (1995) Lipopolysaccharide binding protein participation in cellular activation by LPS. Crit Rev Immunol 15(3–4):201–214
Tzou P, Ohresser S, Ferrandon D, Capovilla M, Reichhart JM, Lemaitre B, Hoffmann JA, Imler JL (2000) Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13(5):737–748
Valanne S, Wang JH, Ramet M (2014) The Drosophila Toll signaling pathway. J Immunol 186(2):649–656
Valenzuela-Munoz V, Gallardo-Escarate C (2014) TLR and IMD signaling pathways from Caligus rogercresseyi (Crustacea: Copepoda): in silico gene expression and SNPs discovery. Fish Shellfish Immunol 36(2):428–434
Vasta GR, Cheng TC, Marchalonis JJ (1984) A lectin on the hemocyte membrane of the oyster (Crassostrea virginica). Cell Immunol 88(2):475–488
Vazquez L, Alpuche J, Maldonado G, Agundis C, Pereyra-Morales A, Zenteno E (2009) Review: immunity mechanisms in crustaceans. Innate Immun 15(3):179–188
Wang W, Li M, Wang L, Chen H, Liu Z, Jia Z, Qiu L, Song L (2016) The granulocytes are the main immunocompetent hemocytes in Crassostrea gigas. Dev Comp Immunol 67:221–228
Weber AN, Tauszig-Delamasure S, Hoffmann JA, Lelievre E, Gascan H, Ray KP, Morse MA, Imler JL, Gay NJ (2003) Binding of the Drosophila cytokine Spatzle to Toll is direct and establishes signaling. Nat Immunol 4(8):794–800
Weiss G, Schaible UE (2015) Macrophage defense mechanisms against intracellular bacteria. Immunol Rev 264(1):182–203
Wynn TA, Vannella KM (2016) Macrophages in tissue repair, regeneration, and fibrosis. Immunity 44(3):450–462
Ye T, Tang W, Zhang X (2012) Involvement of Rab6 in the regulation of phagocytosis against virus infection in invertebrates. J Proteome Res 11(10):4834–4846
Yi HY, Chowdhury M, Huang YD, Yu XQ (2014) Insect antimicrobial peptides and their applications. Appl Microbiol Biotechnol 98(13):5807–5822
You Y, Huan P, Liu B (2012) RNAi assay in primary cells: a new method for gene function analysis in marine bivalve. Mol Biol Rep 39(8):8209–8216
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Abnave, P., Muracciole, X., Ghigo, E. (2017). Macrophages in Invertebrates: From Insects and Crustaceans to Marine Bivalves. In: Kloc, M. (eds) Macrophages. Results and Problems in Cell Differentiation, vol 62. Springer, Cham. https://doi.org/10.1007/978-3-319-54090-0_6
Download citation
DOI: https://doi.org/10.1007/978-3-319-54090-0_6
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-54089-4
Online ISBN: 978-3-319-54090-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)