Skip to main content
Book cover

Macrophages pp 147–158Cite as

Macrophages in Invertebrates: From Insects and Crustaceans to Marine Bivalves

  • Chapter
  • First Online:

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 62))

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Abbreviations

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

    Article  CAS  PubMed  Google Scholar 

  • Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124(4):783–801

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Beaven AE, Paynter KT (1999) Acidification of the phagosome in Crassostrea virginica hemocytes following engulfment of zymosan. Biol Bull 196(1):26–33

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Blandin S, Levashina EA (2004) Thioester-containing proteins and insect immunity. Mol Immunol 40(12):903–908

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Buchmann K (2014) Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol 5:459

    Article  PubMed  PubMed Central  Google Scholar 

  • Butt TM, Shields KS (1996) The structure and behavior of gypsy moth (Lymantria dispar) hemocytes. J Invertebr Pathol 68(1):1–14

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Canesi L, Gallo G, Gavioli M, Pruzzo C (2002) Bacteria-hemocyte interactions and phagocytosis in marine bivalves. Microsc Res Tech 57(6):469–476

    Article  PubMed  Google Scholar 

  • Cheng TC (1975) Functional morphology and biochemistry of molluscan phagocytes. Ann N Y Acad Sci 266:343–379

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Dodd RB, Drickamer K (2001) Lectin-like proteins in model organisms: implications for evolution of carbohydrate-binding activity. Glycobiology 11(5):71R–79R

    Article  CAS  PubMed  Google Scholar 

  • Dziarski R, Gupta D (2006) The peptidoglycan recognition proteins (PGRPs). Genome Biol 7(8):232

    Article  PubMed  PubMed Central  Google Scholar 

  • Elrod-Erickson M, Mishra S, Schneider D (2000) Interactions between the cellular and humoral immune responses in Drosophila. Curr Biol 10(13):781–784

    Article  CAS  PubMed  Google Scholar 

  • Epelman S, Lavine KJ, Randolph GJ (2014) Origin and functions of tissue macrophages. Immunity 41(1):21–35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gordon S (2008) Elie Metchnikoff: father of natural immunity. Eur J Immunol 38(12):3257–3264

    Article  CAS  PubMed  Google Scholar 

  • Gordon S (2016) Phagocytosis: an immunobiologic process. Immunity 44(3):463–475

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hillyer JF, Strand MR (2014) Mosquito hemocyte-mediated immune responses. Curr Opin Insect Sci 3:14–21

    Article  PubMed  PubMed Central  Google Scholar 

  • Imler JL (2014) Overview of Drosophila immunity: a historical perspective. Dev Comp Immunol 42(1):3–15

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaufmann SH, Dorhoi A (2016) Molecular determinants in phagocyte-bacteria interactions. Immunity 44(3):476–491

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kinchen JM, Ravichandran KS (2008) Phagosome maturation: going through the acid test. Nat Rev 9(10):781–795

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kounatidis I, Ligoxygakis P (2012) Drosophila as a model system to unravel the layers of innate immunity to infection. Open Biol 2(5):120075

    Article  PubMed  PubMed Central  Google Scholar 

  • Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32(10):1295–1309

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Matozzo V, Bailo L (2015) A first insight into haemocytes of the smooth venus clam Callista chione. Fish Shellfish Immunol 42(2):494–502

    Article  PubMed  Google Scholar 

  • Mechnikov II (1905) Immunity in infective diseases. By Il’ia Il’ich Mechnikov, 1905. Rev Infect Dis 10(1):617

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Myllymaki H, Valanne S, Ramet M (2014) The Drosophila imd signaling pathway. J Immunol 192(8):3455–3462

    Article  PubMed  Google Scholar 

  • Nandety RS, Kuo YW, Nouri S, Falk BW (2015) Emerging strategies for RNA interference (RNAi) applications in insects. Bioengineered 6(1):8–19

    Article  CAS  PubMed  Google Scholar 

  • Nappi AJ, Vass E, Frey F, Carton Y (2000) Nitric oxide involvement in Drosophila immunity. Nitric Oxide 4(4):423–430

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Neill LA, Golenbock D, Bowie AG (2013) The history of Toll-like receptors—redefining innate immunity. Nat Rev Immunol 13(6):453–460

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramet M (2012) The fruit fly Drosophila melanogaster unfolds the secrets of innate immunity. Acta Paediatr 101(9):900–905

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Royet J, Gupta D, Dziarski R (2011) Peptidoglycan recognition proteins: modulators of the microbiome and inflammation. Nat Rev Immunol 11(12):837–851

    CAS  PubMed  Google Scholar 

  • Sagi A, Manor R, Ventura T (2013) Gene silencing in crustaceans: from basic research to biotechnologies. Genes 4(4):620–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satake H, Sekiguchi T (2012) Toll-like receptors of deuterostome invertebrates. Front Immunol 3:34

    Article  PubMed  PubMed Central  Google Scholar 

  • Sellge G, Kufer TA (2015) PRR-signaling pathways: learning from microbial tactics. Semin Immunol 27(2):75–84

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Su GL, Simmons RL, Wang SC (1995) Lipopolysaccharide binding protein participation in cellular activation by LPS. Crit Rev Immunol 15(3–4):201–214

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Valanne S, Wang JH, Ramet M (2014) The Drosophila Toll signaling pathway. J Immunol 186(2):649–656

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Vasta GR, Cheng TC, Marchalonis JJ (1984) A lectin on the hemocyte membrane of the oyster (Crassostrea virginica). Cell Immunol 88(2):475–488

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Weiss G, Schaible UE (2015) Macrophage defense mechanisms against intracellular bacteria. Immunol Rev 264(1):182–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wynn TA, Vannella KM (2016) Macrophages in tissue repair, regeneration, and fibrosis. Immunity 44(3):450–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Yi HY, Chowdhury M, Huang YD, Yu XQ (2014) Insect antimicrobial peptides and their applications. Appl Microbiol Biotechnol 98(13):5807–5822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eric Ghigo .

Editor information

Editors and Affiliations

Rights and permissions

Reprints 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

Publish with us

Policies and ethics