Abstract
The ultrastructure of the resting thrombocytes of the snake Waglerophis merremii and the process of ADP aggregation are studied. These thrombocytes are nucleate, ellipsoidal, and contain a marginal band. Endoplasmic reticulum and ribosomes are few. An open canalicular system, Golgi complex, granules resembling the alpha-granules in human platelets, and structures similar to secondary lysosomes are also present. The activation response of W. merremii thrombocytes to ADP is examined and compared to the morphological alterations in human platelets. The thrombocytes, normally ellipitical in shape, become spheroid with cytoplasmic protrusions, and adhere to one another. The open canalicular system undergoes dilation and the granules cluster at the centre of the thrombocytes. The release reaction of these granules occurs after stimulation by ADP, similar to what happens in human platelets. This similarity may suggest a process of evolutional specialization since thrombocytes in the majority of non-mammal vertebrates are not aggregated by ADP.
Similar content being viewed by others
References
Archer RK (1970) Blood coagulation in non-human vertebrates. Symp Zool Soc Lond 27:121–132
Arocha-Piñango CL, Gorzula S (1975) A naturally-occurring inhibitor in the blood-clotting mechanism of Caiman crocodilus. Herpetologica 31:419–420
Arocha-Piñango CL, Gorzula SJ, Ojeda A (1982) The blood clotting mechanism of spectacled Caiman caiman crocodilus. Mol Physiol 2:161–170
Behnke O (1967) Electron microscopic observations on the membrane systems of the rat blood platelet. Anat Rec 158:121–138
Belamarich FA, Fusari MH, Shepro D, Kien M (1966) In vitro studies of aggregation of non mammalian thrombocytes. Nature (Lond.) 212:1579–1580
Belamarich FA, Shepro D, Kien M (1968) ADP is not involved in thrombin-induced aggregation of thrombocytes of a non mammalian vertebrate. Nature (Lond.) 217:509–511
Belamarich FA, Simoneit LW (1973) Aggregation of duck thrombocytes by 5-hydroxytryptamine. Microvasc Res 6:229–234
Biggs R (1976) The preparation of general reagents and coagulation factors. In: Biggs R (ed) Human blood coagulation, haemostasis and thrombosis. Blackwell Scientific Publications, Oxford
Bigland CH, Triantophyllopoulos DC (1960) A re-evaluation of the clotting time of chicken blood. Nature 186:644
Born GVR (1962) Aggregation of blood platelets by adrenosine diphosphate and its reversal. Nature 194:927–929
Carlson HC, Sweeny PR, Tokaryk JM (1968) Demonstration of phagocytic and trephocytic activities of chicken thrombocytes by microscopic and vital staining techniques. Avian Dis 12:700–715
Chao-Fu C, Hamilton PB (1979) The thombocyte as the primary circulating phagocyte in chickens. J Reticuloendothelial Soc 25:585–590
Charo IF, Feinman RD, Detwiler TC (1977) Interrelations of platelets aggregation and secretion. J Clin Invest 60:866–873
Coiro JRR, Brunner A Jr (1972) Polylite 8001, a new embedding medium for electron microscopy. Rev Microsc Electr 1:12
Daimon T, Uchida K (1978) Electron microscopic and cytochemical observations on the membrane systems of the chicken thrombocyte. J Anat 125:11–21
Daimon T, Uchida K (1982) Cytochemical demonstration of aminestoring vacuoles and lysosomes in the chicken thrombocytes. Histochemistry 75:309–317
Daimon T, Uchida K (1985) Ultrastructural evidence of the existence of the surface connected canalicular system in the thrombocyte of the shark (Triakes scylla). J Anat 141:193–200
Daimon T, Mizuhira V, Takahashi I, Uchida K (1979a) The surface connected canalicular system of carp (Cyprinus carpio) thrombocytes. Its fine structure and three-dimensional architecture. Cell Tissue Res 203:355–365
Daimon T, Mizuhira V, Uchida K (1979b) Fine structural distribution of the surface connected canalicular system in frog thrombocytes. Cell Tissue Res 201:431–439
Daimon T, Gotoh Y, Kawai K, Uchida K (1985) Ultrastructural distribution of peroxidase in thrombocytes of mammals and submammals. Histochemistry 82:345–350
Desser SS, Weller I (1979) Ultrastructural observations on the erythrocytes and thrombocytes of the tuatara, Sphenodon punctatus (Gray). Tissue Cell 11:717–726
Dhingra LD, Parrish WB, Venzke WG (1969) Electron microscopy of non-granular leukocytes and thrombocytes of chicken. Am J Vet Res 30:1837–1842
Fantl P (1961) A comparative study of blood coagulation in vertebrates. Aust J Exp Biol Med Sci 39:402–412
Grouse LH, Rao GHR, Weiss DJ, Perman V, White JG (1990) Surface-activated bovine platelets do not spread, they unfold. Am J Path 13:399–408
Hackett E, Hann C (1967) Slow clotting of reptile blood. J Comp Path 77:175–180
Hattori A, Ito S, Tsukada T, Koike K, Matsuoka M (1974) Ultrastructure of platelets aggregation at an early stage. Thrombos Diathes haemorrh (Stuttg.) 60:147–158
Kunicki TJ, Newman PJ (1985) Synthesis of analogs of human platelet membrane glycoprotein IIb–IIIa complex by chicken peripheral blood thrombocytes. Proc Natl Acad Sci 82:7319–7323
Kuruma I, Okada T, Kataoka K, Sorimachi M (1970) Ultrastructural observations of 5-hydroxytryptamine-storing granules in the domestic fowl thrombocytes. Z Zellforsch 108:268–281
Lucas AM, Jamroz C (1961) Atlas of avian hematology. Agriculture Monograph Washington, US Dept Agriculture
Luft JH (1971) Ruthenium Red and Violet II. Fine structural localization in animal tissue. Anat Rec 171:369–416
Maxwell MH (1974) An ultrastructural comparison of the mononuclear leucocytes and thrombocytes in six species of domestic bird. J Anat 117:69–80
Maxwell MH, Trejo F (1970) The ultrastructure of white blood cells and thrombocytes of the domestic fowl. Br Vet J 126:576–592
Mills DCB (1970) Platelet aggregation and platelet nucleotide concentration in different species. Symp Zool Soc Lond 27:99–107. In: Macfarlane RG (ed) The haemostatic mechanism in man and other animals. Academic Press, London
Nahas L, Kamiguti AS, Sano-Martins IS, Betti F, Rodrigues MI (1981) Blood coagulation mechanism in the snake Waglerophis merremii and Bothrops jararaca. Comp Biochem Physiol 69A:739–743
Ollgard E (1961) Macroscopic studies of platelet aggregation; Nature of an aggregating factor in red blood cells and platelets. Thrombus Diathes haemorrh (Stuttg.) 6:86–97
Romano SALW, Hoge AR (1972) Nota sobre Xenodon e Ophis, Serpentes Colubridae. Mem Inst Butantan 36:209–214
Saint-Girons MC (1960) Dimorphisme sexual du leucogramme chez Vipera berus adulte. C R Soc Biol (Paris) 154:342–344
Saint-Girons MC (1970) Morphology of the circulating blood Cells. In Gans C, Parsons TS (eds) Biology of the Reptilia 3. Academic Press, New York, pp 73–91
Saint-Girons MC, Duguy R (1963) Notes de cytologie sanguine comparée sur les reptiles de France. Bull Soc Zool Fr 88:613–624
Saint-Girons MC, Saint-Girons H (1969) Contribution à la morphologie comparée des erythrocytes chez les reptiles. Brit J Herpet 4:67–82
Sano-Martins IS (1978) Hematologia comparada de serpentes Bothrops jararaca e Waglerophis merremii. Master's Dissertation, Universidade de São Paulo, Brazil
Shepro D, Belamarich FA, Merck FB, Chao-Fu C (1969) Changes in thrombocyte ultrastructure during clot retraction. J Cell Sci 4:763–779
Shirisawa K, Chandler AB (1969) Fine structure of the bond between platelets in artificial thrombi and in platelet aggregates induced by adenosine diphosphate. Am J Path 57:127–152
Sixma JJ, Geuze JJ (1968) Degranulation of human platelets during ADP-induced aggregation. Vox Sang 15:309–314
Sorimachi M, Takaoka K, Inoue A (1970) Release in vitro of 5-hydroxytryptamine from spindle cells of the domestic fowl. Europ J Pharmacol 10:243–248
Stiller RA, Belamarich FA, Shepro D (1974) Frog thrombocytes aggregation and the release reaction. Thrombos Diathes haemarrh (Stuttg.) 32:685–693
Stokes EE, Firkin BG (1971) Studies of the peripheral blood of the port jackson shark (Heterodontus portusjacksoni) with particular reference to the thrombocyte. British J Haematol 20:427–435
Stopforth A (1970) A study of coagulation mechanisms in domestic chickens. J Comp Path 80:525–533
Wachowicz B (1982) Binding of adenosine diphosphate to turkey thrombocytes. Haemostasis 11:139–148
Wachowicz B, Krajewski T (1979) The released proteins from avian thrombocytes. Thrombos and haemostas (Stuttg.) 42:1289–1295
Wachowicz B, Krajewski T, Stefanczyk B (1981) Isolation and partial characterization of anti-heparin proteins from avian thrombocytes. I.R.C.S. Medical Science: Biochemistry, Cardiovascular System, Cell and Membrane Biology, Experimental Animals, Hematology, Physiology, 9:331–332
Weinreb, EL (1963) Studies on the fine structure of teleost blood cells. I. Peripheral blood. Anat Rec 147:219–225
White JG (1968a) Fine structural alterations induced in platelets by adenosine diphosphate. Blood 31:604–622
White JG (1968b) Effects of colchicine and vinca alkaloids on human platelets. I. Influence on platelet microtubules and contractile function. Am J Pathol 53:281–291
White JG (1987a) Anatomy and structural organization of the platelet. In: Colman RW, Hirsh J, Marder VJ, Salzman EW (eds) Hemostasis and Thrombosis. J. B. Lippencott Co, Philadelphia, pp 537–554
White JG (1987b) The secretory pathway of bovine platelets. Blood 69:878–885
White JG, Krivit W (1966) The ultrastructural localization and release of platelet lipids. Blood 27:167–186
White JG, Krivit W (1967) An ultrastructural basis for the shape changes induced by chilling. Blood 30:625–635
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Sano-Martins, I.S., Jared, C. & Brunner, A. Ultrastructural alterations in thrombocytes of the snake Waglerophis merremii after Activation by ADP. Comp Haematol Int 4, 226–231 (1994). https://doi.org/10.1007/BF00185178
Issue date:
DOI: https://doi.org/10.1007/BF00185178


