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Hemocitical responses to environmental stress in invertebrates: a review

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Abstract

Although invertebrates are recognized by the great facility to accumulate pollutants present in their environment and many of them are used as sentinel species in biomonitoring studies, little is known about the impact of toxicants on the immune system of these animals. In this regard, hemocytes play a fundamental role: these cells circulate freely through the hemolymph of invertebrates and act on the recognition of foreign material to the organism, mediating and effecting the cellular defense, such as phagocytosis, nodulation, and encapsulation. Different morphological types can be recognized but still there is controversy among the researchers about the exact classification of the hemocytes due to the diversity of techniques for the preservation and observation of these cells. In the present study, a review on the main hemocyte responses to environmental stress in different invertebrate organisms is presented, emphasizing the contamination by heavy metals. It is discussed parameters such as: alteration in the number of cells involved in the defense reaction, phagocytic activity, lysosomal responses, and production of reactive oxygen species.

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References

  • Ahearn, G. A., Mandal, P. K., & Mandal, A. (2004). Mechanisms of heavy-metal sequestration and detoxification in crustaceans: A review. Journal of Comparative Physiology B, 174, 439–452.

    Article  CAS  Google Scholar 

  • Andrade, F. G., Negreiro, M. C. C., & Falleiros, A. M. F. (2004). Aspectos dos mecanismos de defesa da lagarta da soja Anticarsia gemmatalis (Hübner 1818) relacionados ao controle biológico por Baculovirus anticarsia (AGMNPV). Arquivos do Instituto Biológico, 71(3), 391–398.

    Google Scholar 

  • Andrews, G. K. (2000). Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochemical Pharmacology, 59(1), 95–104.

    Article  CAS  Google Scholar 

  • Auffret, M., & Oubella, R. (1997). Hemocyte aggregation in the oyster Crassostrea gigas: In Vitro measurement and experimental modulation by xenobiotics. Comparative Biochemistry and Physiology, 118A(3), 705–712.

    CAS  Google Scholar 

  • Auffret, M., Mujdzic, N., Corporeau, C., & Moraga, D. (2002). Xenobiotic-induced immunomodulation in the European flat oyster, Ostrea edulis. Marine Environmental Research, 54, 585–589.

    Article  CAS  Google Scholar 

  • Barraco, M. A., & Amirante, G. A. (1992). Morphological and cytochemical studies of the hemocytes of Squilla mantis (Stomatopoda). Journal of Crustacean Biology, 12(3), 372–382.

    Article  Google Scholar 

  • Bogdan, C., Röllinghoff, M., & Diefenbach, A. (2000). Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Current Opinion in Immunology, 12, 64–76.

    Article  CAS  Google Scholar 

  • Bombonato, M. T., & Gregório, E. A. (1995). Estudo morfológico e quantitativo dos hemócitos em larvas de Diatraea sacharalis (Fabricius) (Lepidoptera, Pyralidae). Revista Brasileira de Zoologia, 12(4), 867–879.

    Article  Google Scholar 

  • Cajaraville, M. P., Olabarrieta, I., & Marigomez, I. (1996). In vitro activities in mussel hemocytes as biomarkers of environmental quality: A case study in the Abra Estuary (Biscay Bay). Ecotoxicology and Environmental Safety, 35, 253–260.

    Article  CAS  Google Scholar 

  • Carneiro, M. E., & Daemon, E. (1997). Caracterização dos tipos celulares presentes na hemolinfa de adultos de Rhipicephalus sanguineus (Latreille, 1806) (Ixodoidea: Ixodidae) em diferentes estados nutricionais. Revista Brasileira de Parasitologia Veterinária, 6(1), 1–9.

    Google Scholar 

  • Carneiro, M. E., & Daemon, E. (2001). Caracterização dos tipos celulares presentes na hemolinfa de adultos de Amblyomma cajennense (Fabricius) Koch, 1844 e de Haemaphysalis sp. Revista Brasileira de Zoociências, 3(2), 139–145.

    Google Scholar 

  • Coles, J. A., Farley, S. R., & Pipe, R. K. (1995). Alteration of the immune response of the common marine mussel Mytilus edulis resulting from exposure to cadmium. Diseases of Aquatic Organisms, 22, 59–65.

    Article  CAS  Google Scholar 

  • Correia, A. A. (2008). Histofisiologia do canal alimentar e hemócitos de Spodoptera frugiperda (J.E. Smith) (Lepdoptera: Noctuidae) tratadas com nim (Azadirachta indica A. Juss). Dissertation, Universidade Federal Rural de Pernambuco.

  • Correia, A. A., Ferreira, A. V. S., Wanderley-Teixeira, V., & Teixeira, A. A. C. (2005). Descrição morfológica dos hemócitos do gafanhoto Tropidacris collaris (Stoll, 1813) (Orthoptera: Romaleidae). Arquivos do Instituto Biológico, 72(1), 57–61.

    Google Scholar 

  • Coutinho, H. D., & Barbosa, A. R. (2007). Fitorremediação: Considerações gerais e características de utilização. Silva Lusitana, 15(1), 103–117.

    Google Scholar 

  • David, J. A. O., Salaroli, R. B., & Fontanetti, C. S. (2008). The significance of changes in Mytella falcata (Orbigny, 1842) gill filaments chronically exposed to polluted environments. Micron 39, 1293–1299.

    Article  CAS  Google Scholar 

  • Erold-Erickson, M., Mishra, S., & Schneider, D. (2000). Interactions between the cellular and humoral immune responses in Drosophila. Current Biology, 10, 781–784.

    Article  Google Scholar 

  • Falleiros, A. M. F. (1995). Células sanguíneas de Diatraea saccharalis (Lepidóptera: Pyralidae): Estudo citoquímico ultraestrutural e à microscopia de varredura. Thesis, Universidade Estadual Paulista Júlio de Mesquita Filho.

  • Falleiros, A. M. F., Bombonato, M. T. S., & Gregório, E. A. (2003). Ultrastructural and quantitative studies of hemocytes in sugarcane borer, Diatraea saccharalis (Lepidoptera: Pyralidae). Brazilian Archives of Biology and Technology, 46(2), 287–294.

    Article  Google Scholar 

  • Faraldo, A. C. (2000). Hemócitos de Diptera economicamente importantes: Análise qualitativa, quantitativa e funcional. Dissertation, Universidade Estadual Paulista Júlio de Mesquita Filho.

  • Fisher, W. S., Wishkovsky, A., & Chu, F.-L. E. (1990). Effects of tributyltin on defense-related activities of oyster hemocytes. Archives of Environmental Contamination and Toxicology, 19, 354–360.

    Article  CAS  Google Scholar 

  • Fisher, W. S., Oliver, L. M., Winstead, J. T., & Long, E. R. (2000). A survey of oysters Crassostrea virginica from Tampa Bay, Florida: Associations of internal defense measurements with contaminant burdens. Aquatic Toxicology, 51, 115–138.

    Article  CAS  Google Scholar 

  • Freire, M. M., Santos, V. G., Ginuino, I. S. F., & Arias, A. R. L. (2008). Biomarcadores na avaliação da saúde ambiental dos ecossistemas aquáticos. Oecologia Brasiliensis, 12(3), 347–354.

    Article  Google Scholar 

  • Giamberini, L., & Pihan, J. C. (1997). Lysosomal changes in the hemocytes of the freshwater mussel Dreissena polymorpha experimentally exposed to lead and zinc. Diseases of Aquatic Organisms, 28, 221–227.

    Article  CAS  Google Scholar 

  • Gillespie, J. P., Kanost, M. R., & Trenczek, T. (1997). Biological mediators of insect immunity. Annual Review of Entomology, 42, 611–643.

    Article  CAS  Google Scholar 

  • Gillespie, J. P., Burnett, C., & Charnley, A. K. (2000). The immune response of the desert locust Schistocerca gregaria during mycosis of the entomopathogenic fungus, Metarhizium anisopliae var acridum. Journal of Insect Physiology, 46(4), 429–437.

    Article  CAS  Google Scholar 

  • Godoy, J. A. P., & Fontanetti, C. S. (2009). Diplopods as bioindicators of soils: Analysis of midgut of individuals maintained in substract containing sewage sludge. Water, Air and Soil Pollution. doi:10.1007/s11270-009-0261-z.

    Google Scholar 

  • Greig, R. A., Sawyer, T. K., Lewis, E. J., & Galasso, M. E. (1982). A study of metal concentrations in relation to gill color and pathology in the rock crab. Archives of Environmental Contamination and Toxicology, 11, 539–545.

    Article  CAS  Google Scholar 

  • Gupta, A. P. (1979). Insect hemocytes: Development, forms, functions and techniques. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Gupta, A. P. (1985). Cellular elements in the hemolymph. In G. A. Kertutand & L. I. Gilbert (Eds.), Comprehensive insects physiology, biochemistry and pharmacology (pp. 402–444). Oxford: Pergamon Press.

    Google Scholar 

  • Hall, J. L. (2002). Cellular mechanisms for heavy metals detoxification and tolerance. Journal of Experimental Botany, 53(366), 1–11.

    Article  CAS  Google Scholar 

  • Jiravanichpaisal, P., Lee, B. L., & Söderhäll, K. (2006). Cell-mediated immunity en arthropods: Hematopoiesis, coagulation, melanization and opsonization. Immunobiology, 211, 213–236.

    Article  CAS  Google Scholar 

  • Johansson, M. W., Keyser, P., Sritunyalucksana, K., & Söderhäll, K. (2000). Crustacean haemocytes and haematopoiesis. Aquaculture, 191, 45–52.

    Article  CAS  Google Scholar 

  • Klaassen, C. D., Liu, J., & Choudhuri, S. (1999). Metallothionein: An intracellular protein to protect against cadmiun toxicity. Annual Review of Pharmacology and Toxicology, 39(1), 267–294.

    Article  CAS  Google Scholar 

  • Lavine, M. D., & Strand, M. R. (2002). Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology, 32, 1295–1309.

    Article  CAS  Google Scholar 

  • Lorenzon, S., Francese, M., Smith, V. J., & Ferrero, E. A. (2001). Heavy metals affect the circulating haemocyte number in the shrimp Palaemon elegans. Fish & Shellfish Immunology, 11, 459–472.

    Article  CAS  Google Scholar 

  • Lowe, D. M., & Pipe, R. K. (1994). Contaminant induced lysosomal membrane damage in marine mussel digestive cells: An in vitro study. Aquatic Toxicology, 30, 357–365.

    Article  CAS  Google Scholar 

  • Lowenberger, C. (2001). Innate immune response of Aedes aegypti. Insect Biochemistry and Molecular Biology, 31, 219–229.

    Article  CAS  Google Scholar 

  • Mandato, C. A. (1998). Modulators of the insect cellular immune response. Thesis, University of Waterloo.

  • Matozzo, V., Ballarin, L., Pampanin, D. M., & Marin, M. G. (2001). Effects of copper and cadmium exposure on functional responses of hemocytes in the clam, Tapes philippinarum. Archives of Environmental Contamination and Toxicology, 41, 163–170.

    Article  CAS  Google Scholar 

  • Mayrand, E., ST-Jean, S. D., & Courtenay, S. C. (2005). Haemocytes responses of blue mussels (Mytilus edulis L.) transferred from a contaminated site to a reference site: Can the immune system recuperate? Aquaculture Research, 36, 962–971.

    Article  Google Scholar 

  • Muta, T., & Iwanaga, S. (1996). The role of hemolymph coagulation in innate immunity. Current Opinion in Immunology, 8, 41–47.

    Article  CAS  Google Scholar 

  • Negreiro, M. C. C., Andrade, F. G., & Falleiros, A. M. F. (2004). Sistema imunológico de defesa em insetos: Uma abordagem em lagartas da soja, Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae), resistentes ao AgMNPV. Semina: Ciências Agrárias, 25(4), 293–308.

    Google Scholar 

  • Nogarol, L. R., & Fontanetti, C. S. (2010). Acute and subchronic exposure of diplopods to substrate containing sewage mud: Tissular responses of the midgut. Micron, 41(3), 239–246.

    Article  CAS  Google Scholar 

  • Olabarrieta, I., L’azou, B., Yuric, S., Cambar, J., & Cajaraville, M. P. (2001). In vitro effects of cadmium on two different animal cell models. Toxicology in Vitro, 15, 511–517.

    Article  CAS  Google Scholar 

  • Oliver, L. M., & Fisher, W. S. (1995). Comparative form and function of oyster Crassostrea virginica hemocytes from Chesapeake Bay (Virginia) and Apalachicola Bay (Florida). Diseases of Aquatic Organisms, 22, 217–225.

    Article  Google Scholar 

  • Oubella, R., Maes, P., Paillard, C., & Auffret, M. (1993). Experimentally induced variation in hemocyte density for Ruditapes philippinarum and R. decussatus (Mollusca, Bivalvia). Diseases of Aquatic Organisms, 15, 193–197.

    Article  Google Scholar 

  • Park, J. D., Liu, Y., & Klaassen, C. D. (2001). Protective effect of metallothionein against toxicity of cadmiun and other metals. Toxicology, 163(2–3), 93–100.

    Article  CAS  Google Scholar 

  • Pech, L. L., & Strand, M. R. (1996). Granular cells are required for encapsulation of foreign targets by insect haemocytes. Journal of Cell Science, 109, 2053–2060.

    CAS  Google Scholar 

  • Perez, D. G., & Fontanetti, C. S. (2008). Respostas tissulares do intestino médio do diplópodo Rhinocricus padbergi exposto a substrato contendo lodo de esgoto. Dissertation, Universidade Estadual Paulista.

  • Pipe, R. K. (1992). Generation of reactive oxygen metabolites by the haemocytes of the mussel Mytilus edulis. Developmental and Comparative Immunology, 16, 111–122.

    Article  CAS  Google Scholar 

  • Pipe, R. K., & Coles, J. A. (1995). Environmental contaminants influencing immune function in marine bivalve molluscs. Fish and Shellfish Immunology, 5, 581–595.

    Article  Google Scholar 

  • Pipe, R. K., Coles, J. A., Carissan, F. M. M., & Ramanathan, K. (1999). Copper induced immunomodulation in the marine mussel, Mytilus edulis. Aquatic Toxicology, 46, 43–54.

    Article  CAS  Google Scholar 

  • Pirie, B. J. S., George, S. G., Lytton, D. G., & Thomson, J. D. (1984). Metal-containing blood cells of oysters: Ultrastructure histochemistry X-ray microanalysis. Journal of the Marine Biological Association of the United Kingdom, 64, 115–123.

    Article  CAS  Google Scholar 

  • Radford, J. L., Hutchinson, A. E., Burandt, M., & Raftos, D. A. (2000). Effects of metal-based environmental pollutants on tunicate hemocytes. Journal of Invertebrate Pathology, 76, 242–248.

    Article  CAS  Google Scholar 

  • Ratcliffe, N. A., Rowley, A. F., Fitzgeald, S. W., & Rhodes, C. P. (1985). Invertebrate immunity: Basic concepts and recents advances. International Review of Cytology, 97, 183–350.

    Article  CAS  Google Scholar 

  • Ribeiro, C., & Brehélin, M. (2006). Insect haemocytes: What type of cell is that? Journal of Insect Physiology, 52, 417–429.

    Article  CAS  Google Scholar 

  • Robinson, W. E., & Ryan, D. K. (1988). Transport of cadmium and other metals in the blood of the bivalve mollusc Mercenaria mercenaria. Marine Biology, 97, 101–109.

    Article  CAS  Google Scholar 

  • Roesijadi, G., Brubacher, L. L., Unger, M. E., & Anderson, R. S. (1997). Metallothionein mRNA induction and generation of reactive oxygen species in molluscan hemocytes exposed to cadmiun in vitro. Comparative Biochemistry and Physiology, 118C(2), 171–176.

    CAS  Google Scholar 

  • Russo, J., Brehélin, M., & Carton, Y. (2001). Haemocyte changes in resistant and susceptible strains of D. melanogaster caused by virulent and avirulent strains of the parasitic wasp Leptopilina boulardi. Journal of Insect Physiology, 47, 167–172.

    Article  CAS  Google Scholar 

  • Sauvé, S., Brousseau, P., Pellerin, J., Morin, Y., Senécal, P., Goudreau, P., et al. (2002). Phagocytic activity of marine and freshwater bivalves: In vitro exposure of hemocytes to metals (Ag, Cd, Hg and Zn). Aquatic Toxicology, 58, 189–200.

    Article  Google Scholar 

  • Silva, J. E. B., Boleli, I. C., & Simões, Z. L. P. (2002). Hemocyte types and total and differential counts in unparasitized and parasitized Anastrepha obliqua (Diptera, Tephritidae) larvae. Brazilian Journal of Biology, 62(4a), 689–699.

    Article  CAS  Google Scholar 

  • Snyman, R. G., Reinecke, S. A., & Reinecke, A. J. (2000). Hemocytic lysosome response in the snail Helix aspersa after exposure to the fungicide cooper oxychloride. Archives of Environmental Contamination and Toxicology, 39, 480–485.

    Article  CAS  Google Scholar 

  • Sorvari, J., Rantala, L. M., Rantala, M. J., Hakkarainen, H., & Eeva, T. (2007). Heavy metal pollution disturbs immune response in wild ant populations. Environmental Pollution, 145, 324–328.

    Article  CAS  Google Scholar 

  • Truscott, R., & White, K. N. (1990). The influence of metal and temperature stress on the immune system of crabs. Functional Ecology, 4, 455–461.

    Article  Google Scholar 

  • Tzou, P., Gregorio, E., & Lemaitre, B. (2002). How Drosophila combats microbial infection: A model to study innate immunity and host–pathogen interactions. Current Opinion in Microbiology, 5, 102–110.

    Article  CAS  Google Scholar 

  • van de Braak, K. (2002). Haemocytic defence in black tiger shrimp (Penaeus monodon). Thesis, Wageningen University.

  • Vasak, M. (2005). Advances in metallothionein structure and functions. Journal of Trace Elements in Medicine and Biology, 19(1), 13–17.

    Article  CAS  Google Scholar 

  • Viarengo, A., Lowe, D., Bolognesi, C., Fabbri, E., & Koehler, A. (2007). The use of biomarkers in biomonitoring: A 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comparative Biochemistry and Physiology part C: Toxicology and Pharmacology, 146(3), 281–300.

    Article  CAS  Google Scholar 

  • Victor, B. (1993). Responses of hemocytes and gill tissues to sublethal cadmium chloride poisoning in the crab Paratelphusa hydrodromous (Herbst). Archives of Environmental Contamination and Toxicology, 24, 432–439.

    Article  CAS  Google Scholar 

  • Winston, G. W., Moore, M. N., Kirchin, M. A., & Soverchia, C. (1996). Production of reactive oxygen species by hemocytes from the marine mussel, Mytilus edulis: Lysosomal localization and effect of xenobiotics. Comparative Biochemistry and Physiology, 113C(2), 221–229.

    CAS  Google Scholar 

  • Wong, S., Fournier, M., Coderre, D., Banska, W., & Krzystyniak, K. (1992). Environmental immunotoxicology. In D. Peakall (Ed.), Animal biomarkers as pollution indicators (pp. 167–189). London: Chapman and Hall.

    Google Scholar 

  • Xylander, W. E. R. (2009). Hemocytes in Myriapoda (Arthropoda): A review. Invertebrate Survival Journal, 6, 114–124.

    Google Scholar 

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Perez, D.G., Fontanetti, C.S. Hemocitical responses to environmental stress in invertebrates: a review. Environ Monit Assess 177, 437–447 (2011). https://doi.org/10.1007/s10661-010-1645-7

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