Cytotoxic Activity of Tunicate Hemocytes

  • N. Parrinello
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 15)


Tunicates (protochordates) are filter-feeding marine invertebrates with a worldwide distribution. In their larval form, they exhibit many of the features characteristic of the vertebrates. The larva, with a tail, notochord, and dorsal neural tube, upon settlement undergoes a remarkable metamorphosis in which it loses most of its chordate characteristics and becomes a sessile invertebrate adult. Thus, due to these characteristics, tunicates are considered to be the most primitive members of the phylum Chordata. Owing to their position in the phylogenetic line leading to the vertebrates, they have attained importance as experimental organisms and have been examined by researchers from a variety of disciplines (developmental biology, ecology, physiology, and immunology).


Contact Reaction Cytotoxic Reaction Solitary Ascidian Morula Cell Tunic Reaction 
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  1. Anderson RS (1971) Cellular responses to foreign bodies in the tunicate Molgula manhattensis (De Kay). Biol Bull 141: 91–98Google Scholar
  2. Arizza V, Parrinello N, Cammarata M (1993) Immunocytochemical localization of cellular lectins in Phallusia mamillata hemocytes. Anim Biol 2: 15–22Google Scholar
  3. Arizza V, Parrinello N, Schimmenti S (1991) In vitro release of lectins by Phallusia mamillata hemocytes. Dev Comp Immunol 15: 219–226PubMedGoogle Scholar
  4. Arizza V, Cammarata M, Tomasino MC, Parrinello N (1995) Phenoloxidase characterisation in vacuolar hemocytes from the solitary ascidian Styela plicata. J Invertebr Path, in pressGoogle Scholar
  5. Ballarin L, Cima F, Sabbadin A (1993) Histoenzymatic staining and characterization of the colonial ascidian Botryllus schlössen hemocytes. Boll Zool 60: 19–24Google Scholar
  6. Ballarin L, Cima F, Sabbadin A (1994) Phenoloxidase in the colonial ascidian Botryllus schlössen (Urochordata: Ascidiacea). Anim Biol 3: 41–48Google Scholar
  7. Barrington EJW (1975) Problems of iodine binding in ascidians. In: Barrington EJW, Jefferies RPS (eds) Protochordates. Academic Press, London, pp 129–158Google Scholar
  8. Beck G, Vasta GR, Marchlonis J J (1989) Characterization of interleukin-1 activity in tunicates. Comp Biochem Physiol 92B: 93–98Google Scholar
  9. Boyd HC, Weissman IL, Saito Y (1990) Morphologic and genetic verification that Monterey Botryllus and Woods HoleBotryllus are the same species. Biol Bull 178: 239–250Google Scholar
  10. Brancoft FW (1903) Variation and fusion of colonies in compound ascidians. Proc Calif Acad Sci 8: 137–186Google Scholar
  11. Cammarata M, Parrinello N, Arizza V (1993) Lectin release by density gradient separated and in vitro cultured hemocytes from Phallusia mamillata. J Exp Zool 266: 319–327Google Scholar
  12. Canicatti C (1989) Evolution of lytic system in echinoderms. II Naturally occurring hemolytic activity inMarthasterias glacialis (Asteroida). Comp Biochem Physiol 93A: 587–591Google Scholar
  13. Canicatti C (1991) Binding properties of Paracentrotus lividus (Echinoidea) hemolysin. Comp Biochem Physiol 98A: 463–468Google Scholar
  14. Canicatti C, Parrinello N, Arizza V (1987) Inhibitory activity of sphingomyelin of hemolytic activity of coelomic fluid of Holothuria polii (Echinodermata). Dev Comp Immunol 11: 29–35PubMedGoogle Scholar
  15. Cooper EL (1980) Phylogeny of cytotoxicity. Endeavour 4: 160–165PubMedGoogle Scholar
  16. Davis AR (1987) Variation in recruitment of the subtidal colonial ascidian Podoclavella cylindrica (Quoy & Gaimard): the role of substratum choice and early survival. J Exp Mar Biol Ecol 106: 57–71Google Scholar
  17. De Leo G (1992) Ascidian hemocytes and their involvement in defence reactions. Boll Zool 59:195–213Google Scholar
  18. De Leo G, Patricolo E, Frittitta G (1981) Fine structure of the tunic of dona intestinalis L. II. Tunic morphology, cell distribution and their functinal importance. Acta Zool 62: 259–271Google Scholar
  19. Du Pasquier L, Blomber B, Bernard CCA (1979) Ontogeny of immunity in amphibians: changes in antibody repertoires and appearance of adult major histocompatibility antigens in Xenopus. Eur J Immunol 9: 900–906PubMedGoogle Scholar
  20. Ermak TH (1975) An autoradiographic demonstration of blood cell renewal in Styela clava (Urochordata: Ascidiacea). Experientia 31: 837–838Google Scholar
  21. Ermak TH (1976) The hematogenic tissues of tunicates. In: Wright RK, Cooper EL (eds) Phylogeny of thymus and bone marrow-bursa cells. Elsevier, Amsterdam, pp 45–55Google Scholar
  22. Ermak TH (1982) The renewing cell populations of ascidians. Am Zool 22: 795–805Google Scholar
  23. Evans DL, McKinney EC (1991) Phylogeny of cytotoxic cells. In: Warr GW, Cohen N (eds) Phylogenesis of immune functions. CRC Press, Boca Raton, pp 215–239Google Scholar
  24. Fuke MT (1979) Studies on coelomic cells of some Japanese ascidians. Bull Mar Biol Stn Asamushi Tohoku Univ 16: 142–159Google Scholar
  25. Fuke MT (1980) “Contact reaction” between xenogeneic or allogeneic celomic cells of solitary ascidians. Biol Bull 158: 304–315Google Scholar
  26. Fuke MT (1990) Self and nonself recognition in the solitary ascidian Halocynthia roretzi. In: Marchalonis J, Reinish C (eds) Defense molecules. Alan R Liss, New York, pp 107–117Google Scholar
  27. Fuke MT, Fukumoto M (1993) Correlative fine structural behavioral, and histochemical analysis of ascidian blood cells. Acta Zool 74: 61–71Google Scholar
  28. Fuke MT, Nakamura I (1985) Patterns of cellular alloreactivity of the solitary ascidian, Halocynthia roretzi, in relation to genetic control. Biol Bull 178: 239–250Google Scholar
  29. Fuke MT, Numakunai T (1982) Allogeneic cellular reactions between intraspecific types of a solitary ascidian, Halocynthia roretzi. Dev Comp Immunol 6: 253–261PubMedGoogle Scholar
  30. Gleisner JM (1979) Lysosmal factors in inflammation. In: Houck JC (ed) Chemical messangers of the inflammatory process. Elsevier, Amsterdam, pp 229–260Google Scholar
  31. Grosberg RK, Quinn JF (1986) The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate. Nature 322: 456–459Google Scholar
  32. Hirsoehhron R (1974) Lysosomal mechanisms in the inflammatory process. In: Zweifach BW, Grant L, Mc Cluskey RT (eds) The inflammatory process, vol 1. Academic Press, New York, pp 259–285Google Scholar
  33. Hirose E, Saito Y, Watanabe H (1988) A new type of the manifestation of colony specificity in the compound ascidian, Botrylloides violaceus Oka. Biol Bull 175: 240–245Google Scholar
  34. Hirose E, Saito Y, Watanabe H (1990) Allogeneic rejection induced by cut surface contact in the compound scidian, Botrylloides simodensis. Invertebr Reprod Dev 17: 159–164Google Scholar
  35. Jackson AD, Smith VJ, Peddie CM (1993) In vitro phenoloxidase activity in the blood of Ciona intestinalis and other ascidians. Dev Comp Immunol 17: 97–108PubMedGoogle Scholar
  36. Johansson MW, Söderhäll K (1992) Cellular defence and cellular adhesion in crustacean. Parasitol Today 5: 171–176Google Scholar
  37. Karre K, Ljunggren HG, Piontek G, Kiessling R (1986) Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319: 675–678PubMedGoogle Scholar
  38. Kelly KL, Cooper EL, Raftos DA (1992) In vitro allogenic cytotoxicity in the solitary urochordate Styela clava. J Exp Zool 262: 202–208PubMedGoogle Scholar
  39. Klebanoff SJ (1982) The iron-H202-iodide cytotoxic system. J Exp Med 256: 1262–1267Google Scholar
  40. Klein E, Mantovani A (1993) Action of natural killer cells and macrophages in cancer. Curr Opin Immunol 5: 714–718PubMedGoogle Scholar
  41. Koyama H, Watanabe H (1982) Colony specificity in the ascidian Perophora sagamiensis. Biol Bull 162: 171–186Google Scholar
  42. Michibata H, Tareda T, Anada N, Yamakawa K, Numakunai T (1986) The accumulation and distribution of vanadium, iron, and manganese in some solitary ascidians. Biol Bull 171: 672–681Google Scholar
  43. Michibata H, Hirata J, Uesaka M, Numakunai T, Sakurai H (1987) Separation of vanadocytes: determination and characterization of vanadium ion in the separated blood cells of ascidian, Ascidia ahodori. J Exp Zool 244: 33–38Google Scholar
  44. Milanesi C, Burighel P (1978) Blood cell ultrastructure of the ascidian Botryllus schlössen I. Hemo-blast, granulocytes, macrophage, morula cell and nephrocyte. Acta Zool 59: 135–147Google Scholar
  45. Mukai H, Watanabe H (1974) On the occurrence of colony specificity in some compound ascidians. Biol Bull 147:411–421PubMedGoogle Scholar
  46. Mukai H, Watanabe H (1975) Fusibility of colonies in natural populations of the compound ascidian Botrylloides violamus. Proc Jpn Acad 51: 48–50Google Scholar
  47. Neigel JE (1988) Recognition of self or nonself? Theoretical implications and an empirical test. In: Grossberg RK, Hedgecock D, Nelson K (eds) Invertebrate historecognition. Plenum Press, New York, pp 127–142Google Scholar
  48. Ojcius DM, Young JDE (1990) Characterization of the inhibitory effect of lysolipds on perforin-mediated hemolysis. Mol Immunol 27: 257–261PubMedGoogle Scholar
  49. Oka H, Watanabe H (1957) Colony specificity in compound ascidians as tested by fusion experiments. Proc Jpn Acad 33: 657–659Google Scholar
  50. Parrinello N (1981) The reaction of Ciona intestinalis L. (Tunicata) to subcuticular erythrocyte and protein injection. Dev Comp Immunol 5 (Suppl) 1: 105–110Google Scholar
  51. Parrinello N, Arizza V (1992) Cytotoxic activity of the invertebrate hemocytes with preliminary findings on the tunicate Ciona intestinalis. Boll Zool 59: 183–189Google Scholar
  52. Parinello N, Patricolo E (1984) Inflammatory-like reaction in the tunic of Ciona intestinalis (Tunicata). II. Capsule components Bio Bull 167: 238–250Google Scholar
  53. Parrinello N, Cammarata M, Arizza V (1995) Univacuolar hemocytes from the tunicate Ciona intestinalis are cytotoxic for mammalian erythrocytes in vitro. Biol Bull, submittedGoogle Scholar
  54. Parrinello N, Patricolo E, Canicatti C (1977) Tunicate immunobiology. Tunic reaction of Ciona intestinalis L. to erythrocyte injection. Boll Zool 44: 373–381Google Scholar
  55. Parrinello N, Patricolo E, Canicatti C (1984) Inflammatory-like reaction in the tunic of Ciona intestinalis (Tunicata). I. Encapsulation and tissue injury. Biol Bull 167: 229–237Google Scholar
  56. Parrinello N, De Leo G, Di Bella MA (1990) Fine structural observation of the granuldcytes involved in the tunic inflammatory-like reaction of Ciona intestinalis (Tunicata). J Invertebr Pathol 56: 181–189PubMedGoogle Scholar
  57. Parrinello N, Arizza V, Cammarata M, Parrinello DM (1993) Cytotoxic activity of the Ciona intestinalis (Tunicata) hemocytes: properties of the in vitro reaction against erythrocyte targets. Dev Comp Immunol 17: 19–27PubMedGoogle Scholar
  58. Parrinello N, Cammarata M, Lipari L, Arizza V (1995) Sphingomyelin inhibition of Ciona intestinalis (Tunicata) cytotoxic hemocytes assayed against sheep erythrocytes. Dev Comp Immunol 19: 31–42PubMedGoogle Scholar
  59. Peddie CM, Smith VJ (1993) In vitro spontaneous cytotoxic activity against mammalian target cells by the hemocytes of the solitary ascidian, Ciona intestinalis. J Exp Zool 267: 616–623PubMedGoogle Scholar
  60. Peddie CM, Smith VJ (1994) Mechanism of cytotoxic activity by hemocytes of solitary ascidian, Ciona intestinalis. J Exp Zool 270: 335–342Google Scholar
  61. Raftos DA (1990) The morphology of allograft rejection in Styela plicata (Urochordate: Ascidiacea). Cell Tissue Res 261: 389–396Google Scholar
  62. Raftos DA (1991) Cellular restriction of histocompatibility responses in the solitary urochordate, Styela plicata. Dev Comp Immunol 15: 93–98PubMedGoogle Scholar
  63. Raftos DA, Briscoe DA (1990) Genetic basis of histocompatibility the solitary urochordate Styela plicata. J Hered 81: 96–100Google Scholar
  64. Raftos DA, Cooper EL (1991) Proliferation of lymphocyte-like cells from the solitary tunicate, Styela clava, in response to allogeneic stimuli. J Exp Zool 260: 391–400PubMedGoogle Scholar
  65. Raftos DA, Tait NN, Briscoe DA (1987a) Allograft rejection and alloimmune memory in the solitary urochordate, Styela plicata. Dev Comp Immunol 11: 343–351PubMedGoogle Scholar
  66. Raftos DA, Tait NN, Briscoe DA (1987b) Cellular basis of allograft rejection in the solitary urochoradate, Styela plicata. Dev Comp Immunol 11: 713–725PubMedGoogle Scholar
  67. Raftos DA, Briscoe DA, Tait NN (1988) The mode of recognition of allogeneic tissue in the solitary urochordate Styela plicata. Transplantation 45: 1123–1126PubMedGoogle Scholar
  68. Raftos DA, Stillmann DL, Cooper EL (1990) In vitro culture of tissue from the tunicateStyela clava. In Vitro Cell Dev Biol 26: 962–970Google Scholar
  69. Raftos DA, Cooper EL, Habicht GS, Beck G (1991) Invertebrate cytokines: tunicate cell proliferation stimulated by an interleukin 1-like molecule. Proc Natl Acad Sci USA 88: 9518–9522PubMedGoogle Scholar
  70. Reddey AL, Bryan B, Hidelmann WH (1975) Integumentary allograft versus autograft reactions in Ciona intestinalis: a protochordate species of solitary tunicate. Immunogenetics 1: 584–590Google Scholar
  71. Rinkevich B (1992) Aspects of the incompatibility nature in botryllid ascidians. Anim Biol 1: 17–28Google Scholar
  72. Rinkevich B, Rabinowitz C (1993) In vitro culture of blood cells from the colonial protochordate Botryllus schlössen. In Vitro Cell Dev Biol 29A: 79–85Google Scholar
  73. Rinkevich B, Weissman IL (1988) Retreat growth in the ascidian Botryllus schlössen: a consequence of nonself recognition. In: Grosberg RK, Hedgecock D, Nelson K (eds) Invertebrate historecognition. Plenum Press, New York, pp 93–109Google Scholar
  74. Rinkevich B, Weissman IL (1991) Interpopulational allogeneic reactions in the colonial protochordate Botryllus schlössen. Inter Immun 3: 1265–1272Google Scholar
  75. Rinkevich B, Weissman IL (1992) Chimeras vs genetically homogeneous individuals: potential fitness costs and benefits. OIKOS 63: 119–124Google Scholar
  76. Roder JC, Helfand SJ, Werkemeister J, McGarry R, Beaumont TJ, Duwe A (1982) Oxygen intermediates are triggered early in the cytolytic pathway of human NK cells. Nature 298: 569–572PubMedGoogle Scholar
  77. Rowley AF (1982) Ultrastructural and cytochemical studies on the blood cells of the sea squirt, Ciona intestinalis I. Stem cells and amoebocytes. Cell Tissue Res 223: 403–414PubMedGoogle Scholar
  78. Sabbadin A (1962) le basi genetiche della capacita’ di fusione fra colonie in Botryllus schlössen (Ascidiacea). Rend Accad Naz Lincei 32: 1031–1035Google Scholar
  79. Sabbadin A, Zaniolo G, Ballarin L (1992) Genetic and cytological aspects of histocompatibility in ascidians. Boll Zool 59: 167–173Google Scholar
  80. Saito Y, Watanabe H (1984) Partial biochemical characterization of humoral factors involved in the nonfusion reaction of the botryllid ascidian Botrylloides simodensis. Zool Sci 1: 229–235Google Scholar
  81. Sawada T, Fujikura Y, Tomonaga S, Fukumoto T (1991) Classification and characterization of ten types of hemocytes in tunicate Halocynthia roretzi. Zool Sci 8: 939–950Google Scholar
  82. Sawada T, Zhang J, Cooper E (1993) Classification and characterization of hemocytes in Stye la clava. Biol Bull 184: 87–96Google Scholar
  83. Schmidt CH (1982) Aggregation and fusion between conspecifies of a solitary ascidian. Biol Bull 162: 195–201Google Scholar
  84. Scofield VL, Nagashima LS (1983) Morphology and genetics of rejection reactions between oozoids from the tunicate Botryllus schlössen. Biol Bull 165: 733–744Google Scholar
  85. Scofield VL, Schlumpberger JM, Weissman IL (1982a) Colony specificity in the colonial tunicate Botryllus and the origin of vertebrate immunity. Am Zool 22: 783–794Google Scholar
  86. Scofield VL, Schlumpberger JM, West LA, Weissman IL (1982b) Protochordate allorecognition is controlled by an MHC-like gene system. Nature 295: 499–502PubMedGoogle Scholar
  87. Smith MJ (1970) The blood cells and tunic of the ascidian Halocynthia aurantum (Pallas). I. Hematology, tunic morphology, and partition of cells between blood and tunic. Biol Bull 138: 345–378Google Scholar
  88. Smith MJ, Peddie CM (1992) Cell cooperation during host defence in the solitary turnicate Ciona intestinalis (L). Biol Bull 183: 211–219Google Scholar
  89. Smith VJ, Söderhäll K (1983) Induction of degranulation and lysis of haematocytes in the freshwater crayfish, Asctacus astacus by components of the prophenoloxidase activating system in vitro. Cell Tissue Res 233: 295–303PubMedGoogle Scholar
  90. Smith MJ, Söderhäll K (1991) A comparison of phenoloxidase activity in the blood of marine invertebrates. Dev Comp Immunol 15: 251–262PubMedGoogle Scholar
  91. Söderhäll K, Wingren A, Johansson MW, Bertheussen K (1985) The cytotoxic reaction of hemocytes from the freshwater crayfish, Asatacus astacus. Cell Immunol 94: 326–332PubMedGoogle Scholar
  92. Tanaka K (1973) Allogeneic inhibition in a compound ascidian, Botryllusprimigenus Oka. II Cellular and humoral responses in “nonfusion” reaction. Cell Immunol 7: 427–443PubMedGoogle Scholar
  93. Tanaka K, Watanabe H (1973) Allogeneic inhibition in a compound ascidian Botryllus primigenus Oka. I. Processes and features of “nonfusion” reaction. Cell Immunol 7: 410–426PubMedGoogle Scholar
  94. Taneda Y, Watanabe H (1982a) Studies in colony specificity in the compound ascidian Botryllus primigenus Oka. I. Initiation of “nonfusion” reaction with special reference to blood cells infiltration. Dev Comp Immunol 6: 43–52PubMedGoogle Scholar
  95. Taneda Y, Watanabe H (1982b) Studies in colony specificity in the compound ascidian Botryllus primigenus Oka. II. In vivo bioassay for analyzing the mechanism of “nonfusion” reaction. Dev Comp Immunol 6: 243–252Google Scholar
  96. Taneda Y, Watanabe H (1982c) Effect of X-irradiation on colony specificity in the compound ascidian Botryllus primigenus Oka. Dev Comp Immunol 6: 665–673PubMedGoogle Scholar
  97. Taneda Y, Saito Y, Watanabe H (1985) Self or nonself discrimination in ascidians. Zool Sci 2:433–442Google Scholar
  98. Tschopp J, Schafer S, Masson D, Peitsch M, Heusser C (1989) Phosphorylcholine acts as a Ca-Dependent receptor molecule for lymphocyte perforin. Nature 337: 272–274PubMedGoogle Scholar
  99. Van Deenen LLM (1981) Topology and dynamics of phospholipids in membranes. FEBS Lett 123: 3–15PubMedGoogle Scholar
  100. Van Duyl FC, Bäk RPM, Sybesma J (1981) The ecology of the tropical compound ascidian Trididemnum solidum. I. Reproductive strategy and larval behaviour. Mar Ecol Prog Ser 6: 35–42Google Scholar
  101. Warr GW, Decker JM, Mandel TE, De LucaD, Hudson R, Marchalonis J J (1977) Lymphocyte-like cells of the tunicate, Pyura stolonifera: binding of lectins, morphological and functional studies. Aust J Exp Biol Med Sci 55: 151–164PubMedGoogle Scholar
  102. Watanabe H, Taneda Y (1982) Self or nonself recognition in compound ascidians. Am Zool 22: 775–782Google Scholar
  103. Weissman IL (1988) Was the MHC made for the immune system or did immunity take advantage of an ancient polymorphic gene family encoding cell surface interaction molecules? A speculative essay. Int Rev Immunol 3: 397–416PubMedGoogle Scholar
  104. Weissman IL, Scofield V, Saito Y, Boyd H, Rinkevich B (1988) Speculations on the relationships of two Botryllus allorecognition reactions-colony specificity and resorption-to vertebrate histocompatibility. In: Grosberg RK, Hedgecock D, Nelson K (eds) Invertebrate hitorecognition. Plenum Press, New York, pp 67–78Google Scholar
  105. Weissman IL, Saito Y, Rinkevich B (1990) Allorecognition histocompatibility in a protochordate species: Is the relationship to MHC semantic or structural? Immunol Rev 113: 227–241PubMedGoogle Scholar
  106. Wright RK (1981) Unrochordates. In: Ratcliff NA, Rowley AF (eds) Invertebrate blood cells, vol 2. Academic Press, New York, pp 565–626Google Scholar
  107. Young CM, Braithwaite LF (1980) Larval behavior and post-setting morphology in the ascidian, Chelyosoma productum Stimpson. J Exp Mar Biol Ecol 42: 157–169Google Scholar
  108. Yue CC, Reynolds CW, Henkart PA (1987) Inhibition of cytolysin activity in large granular lymphocyte granules by lipids: evidence for a membrane insertion mechanism of lysis. Mol Immunol 24: 647–653PubMedGoogle Scholar
  109. Zaniolo G (1981) Histology of the ascidian Botryllus schlosseri tunic: in particular, the test cells. Boll Zool 48: 169–178Google Scholar

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© Springer-Verlag Berlin Heidelberg 1996

Authors and Affiliations

  • N. Parrinello
    • 1
  1. 1.Institute of Zoology, Laboratory of Marine ImmunobiologyUniversity of PalermoPalermoItaly

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