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Cellular immunity in an annelid (Nereis diversicolor, Polychaeta): production of melanin by a subpopulation of granulocytes

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Summary

We attempted to identify the nature and origin of the pigment produced by the marine worm Nereis diversicolor in order to isolate, in inert brown capsules, foreign objects introduced into its body cavity. This brown pigment, characterized by cytochemical techniques, could be a melanin. The activity of the enzyme phenoloxidase responsible for melanin biosynthesis was detected by enzyme cytochemistry techniques in vacuoles and the Golgi apparatus of coelomocytes activated by the presence of foreign bodies. Morphological techniques combined with a monoclonal immunological probe enabled us to establish that the “G2” granulocytes contain both the precursor of the pigment in dense bodies and the capacity for phenoloxidase synthesis when activated to encapsulate foreign bodies. The “G2” granulocyte may therefore be compared to a melanocyte in which melanin is not stored as in mammals, but immediately extruded following synthesis in the form of a thick fluid.

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Abbreviations

ACTH :

adrenocorticotropic hormone

Dopa L-3,4:

dihydroxyphenylalanine

FITC :

fluorescein isothiocyanate

G 1, G 2, G 3 :

granulocyte of types 1, 2, 3

MSH :

melanocyte-stimulating hormone

proPo :

prophenoloxidase

References

  • Boissy RE (1988) The melanocyte. Its structure, function and subpopulation in skin, eyes and hair. In: Nordlund JJ (ed) Dermatologic clinics, vol 6. Saunders, Philadelphia, pp 161–174

    Google Scholar 

  • Boissy RE, Moellmann GE, Halaban RH (1987) Tyrosinase and acid phosphatase activities in melanocytes from avian albinos. J Invest Dermatol 88:292–300

    Article  PubMed  Google Scholar 

  • Boulton M, Docchio F, Dayhaw-Barker P, Ramponi R, Cubeddu R (1990) Age-related changes in the morphology, absorption and fluorescence of melanosomes and lipofuscin granules of the retinal pigment epithelium. Vision Res 30:1291–1303

    Article  PubMed  Google Scholar 

  • Dales RP (1983) Observations on granulomata in the polychaetous annelid Nereis diversicolor. J Invertebr Pathol 42:288–291

    Google Scholar 

  • Della-Cioppa G, Garger SJ, Sverlov GG, Turpen TH, Grill LK (1990) Melanin production in Escherichia coli from a cloned tyrosinase gene. Bio/Technology 8:634–638

    Article  PubMed  Google Scholar 

  • Dhainaut-Courtois N, Dubois MP, Tramu G, Masson M (1985) Occurrence and coexistence in Nereis diversicolor (Annelida, Polychaeta) of substances immunologically related to vertebrate neuropeptides. Cell Tissue Res 242: 97–108

    PubMed  Google Scholar 

  • Ganter P, Jolles G (1969) Histochimie normale et pathologique. Gauthier-Villars, Paris

    Google Scholar 

  • Götz P (1986) Encapsulation in arthropods. In: Brehelin M (ed) Immunity in invertebrates. Springer, Berlin Heidelberg New York, pp 153–170

    Google Scholar 

  • Iwama R, Ashida M (1986) Biosynthesis of prophenol oxidase in hemocytes of larval hemolymph of the silkworm, Bombyx mori. Insect Biochem 16:547–555

    Article  Google Scholar 

  • Johansson MW, Söderhäll K (1989) Cellular immunity in crustaceans and the propo system. Parasitology Today 5:171–176

    Article  PubMed  Google Scholar 

  • Krutzay M (1971) Identifizierung von Pigmenten in Paraffinschnitten. Zbl Allg Pathol 114:374–376

    Google Scholar 

  • Lison L (1953) Histochimie et cytochimie animales. Gauthier-Villars, Paris

    Google Scholar 

  • Matsumoto S, Kitamura A, Nagasawa H, Katoka H, Osikasa C, Mitsui T, Susuki A (1990) Functional diversity of a neurohormone produced by the suboesophageal ganglion: molecular identity of melanization and reddish colouration hormone and pheromone biosynthesis activating neuropeptide. J Insect Physiol 36:427–432

    Article  Google Scholar 

  • Monpeyssin M, Beaulaton J (1977) Données sur la localisation ultrastructurale d'une activité phenoloxydasique dans les hémocytes circulants d'Antherea pernyi au dernier âge larvaire. J Insect Physiol 23:939–943

    Article  Google Scholar 

  • Nappi AJ, Christensen BM (1987) Insect immunity and mechanisms of resistance by nematodes. In: Veech JA, Dickson DW (eds) Vistas on nematology. Society of Nematologists, Inc Hyattsville, Maryland, pp 285–291

    Google Scholar 

  • Nordlund JJ, Abdel-Malek ZA, Boissy RE, Rheins LA (1989) Pigment cell biology: a historical review. J Invest Dermatol 92:539–605

    Article  Google Scholar 

  • Ottaviani E, Caselgrandi E, Bondi M, Cossarizza A, Monti D, Franceschi C (1991) The “immune-mobile brain”: evolutionary evidence. Adv Neuroimmunol: 27–39

  • Pearse AGE (1961) Histochemistry theoretical and applied. Churchill, London

    Google Scholar 

  • Poinar GO Jr, Hess RT (1977) Immune response in the earthworm Aporrectodea trapezoides (Annelida), against Rhabditis pellio (Nematoda). In: Bulla LA, Cheng TC (eds) Comparative pathobiology, vol 3. Plenum Press, New York, pp 69–84

    Google Scholar 

  • Porchet-Henneré E (1990) Cooperation between different coelomocyte populations during the encapsulation response of Nereis diversicolor, demonstrated using monoclonal antibodies. J Invert Pathol 56:353–361

    Google Scholar 

  • Porchet-Henneré E, M'Berri M (1987) Cellular reactions of the polychaete annelid Nereis diversicolor against coelomic parasites. J Invert Pathol 50:58–66

    Google Scholar 

  • Porchet-Henneré E, M'Berri M, Dhainaut A, Porchet M (1987) Ultrastructural study of the encapsulation response of the polychaete annelid Nereis diversicolor. Cell Tissue Res 248:463–471

    Article  Google Scholar 

  • Ratcliffe NA, Rowley AF, Fitzgerald SW, Rhodes CP (1985) Invertebrate immunity: basic concepts and recent advances. Int Rev Cytol 97:183–350

    Google Scholar 

  • Söderhäll K, Smith VJ (1986) The prophenoloxidase activating system: the biochemistry of its activation and role in arthropod cellular immunity, with special reference to crustaceans. In: Brehelin M (ed) Immunity in invertebrates. Springer, Berlin Heidelberg New York, pp 208–223

    Google Scholar 

  • Stefano GB, Zhao X, Bailey D, Metlay M, Leung MK (1989) High affinity dopamine binding to mouse thymocytes and Mytilus edulis (Bivalvia) hemocytes. J Neuroimmunol 21:67–74

    PubMed  Google Scholar 

  • Tsing A, Arcier JM, Brehelin M (1989) Hemocytes of peneid and palaemonid shrimps: morphology, cytochemistry and hemograms. J Invert Pathol 53:64–77

    Google Scholar 

  • Vuillaume M (1969) Les pigments des invertébrés. Biochimie et biologie des colorations. Masson et Cie, Paris

    Google Scholar 

  • Waite JH (1990) The phylogeny and chemical diversity of quinonetanned glues and varnishes. Comp Biochem Physiol 97B:19–29

    Google Scholar 

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Porchet-Henneré, E., Vernet, G. Cellular immunity in an annelid (Nereis diversicolor, Polychaeta): production of melanin by a subpopulation of granulocytes. Cell Tissue Res 269, 167–174 (1992). https://doi.org/10.1007/BF00384737

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  • DOI: https://doi.org/10.1007/BF00384737

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