The immunocytochemical detection of gamma-aminobutyric acid (GABA) in the pancreas of amphibian…
February 19, 2010
The immunocytochemical detection of gamma-aminobutyric acid (GABA) in the pancreas of amphibian…
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Title: | The immunocytochemical detection of gamma-aminobutyric acid (GABA) in the pancreas of amphibian… |
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Article_Title: | The immunocytochemical detection of gamma-aminobutyric acid (GABA) in the pancreas of amphibian Rana esculenta; light- and electron-microscopic observations |
Authors: | Ioana TRANDABURU1, Wolfgang KUMMER2, Tiberiu TRANDABURU3 |
Affiliation: | 1 Center of Cytobiology, Institute of Biology, Bucharest, Romania 2 Institute of Anatomy and Cell Biology, Giessen, Germany 3 Laboratory of Histology and Embryology, Faculty of Sciences, University of Piteşti, Romania |
Abstract: | The immunolabelled structures for gamma-aminobutyric acid (GABA) and their topographic distributions in the pancreas of the frog Rana esculenta are described for the first time in light and electron microscopy. At light microscopic level, the immunoreaction was detected both in the islets of Langerhans and the nerve fibbers supplying the exocrine tissue. At submicroscopic level, this multifunctional amino acid was identified in cytosol, secretory granules matrix and nuclear chromatin of insulin (INS)-, stomatostatin (SOM)-, glucagon (GLUC)- and pancreatic polypeptide (PP)- producing cells. Other reactive sites for this amino acid included the zymogen granules, mitochondria and nuclei of acinar cells. The above results and their functional significances entirely supporting the concept of a good conservation of this amino acid during phylogeny are discussed in connection with the findings previously reported in human and mammalian organs. |
Keywords: | gamma-aminobutyric acid, GABA, Rana esculenta, pancreas, immunocytochemistry |
References: | Awapara J, Landau AJ, Fuerst R, Seale B. Free aminobutyric acid in brain. J. Biol. Chem.1950; 187: 35-39. Roberts E, Frankel S. γ- aminobutyric acid in brain. Its formation from glutamic acid. J. Biol. Chem. 1950; 187: 55-63. Roberts E, Hammerschlag RS. Gamma-aminobutyric acid (GABA). In Albers RW, Siegel GL, Katzman R, Agranoff BW (eds) Basic neurochemistry, 1972; pp. 131-165. Krnjevic K: Inhibitory action of GABA and GABA-mimetics on vertebrate neurons. In: GABA in Nervous System Function, Roberts, E.: Chase, T.N.; Tower, D.B., editors, Raven Press, New York 1976; pp.269-281. Fekete C, Wittmann G, Liposits Z, Lechan RM. GABA-ergic innervation of thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus of the rat. Brain Res. 2002; 957: 251-8. Kalsbeek A, Foppen E, Schalij I, Van Heijningen C, van der Vliet J, Fliers E, Buijs RM. Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate. PLoS One. 2008; 3: e3194. Iwasa K, Oomori Y, Tanaka H. Gamma aminobutyric acid immunoreactivity in the mouse adrenal gland during postnatal development. Arch Histol Cytol. 1998; 61: 373-82. Iwasa K, Oomori Y, Tanaka H. Colocalization of gamma-aminobutyric acid immunoreactivity and acetylcholinesterase activity in nerve fibers of the mouse adrenal gland. J Vet Med Sci. 1999; 61: 631-5. Gladkevich A, Korf J, Hakobyan VP, Melkonyan KV. The peripheral GABAergic system as a target in endocrine disorders. Auton Neurosci. 2006; 124: 1-8. Wiens SC, Trudeau VL. Thyroid hormone and gamma-aminobutyric acid (GABA) interactions in neuroendocrine systems. Comp Biochem Physiol A Mol Integr Physiol. 2006; 144: 332-44. Schaeffer JM, Hsueh AJ. Identification of gamma-aminobutyric acid and its binding sites in the rat ovary. Life Sci. 1982; 30: 1599-1604. László A, Villányi P, Zsolnai B, Erdö SL. Gamma-aminobutyric acid, its related enzymes and receptor-binding sites in the human ovary and fallopian tube. Gynecol Obstet Invest. 1989; 28: 94-7. Erdö SL, Joo F, Wolff JR. Immunohistochemical localization of glutamate decarboxylase in the rat oviduct and ovary: further evidence for non-neural GABA systems. Cell Tissue Res. 1989; 255: 431-4. Hu JH, Yan YC. Identification of gamma 1 subunit of GABA(A) receptor in rat testis. Cell Res. 2002; 12: 33-7. Geigerseder C, Doepner R, Thalhammer A, Frungieri MB, Gamel-Didelon K, Calandra RS, Köhn FM, Mayerhofer A. Evidence for a GABAergic system in rodent and human testis: local GABA production and GABA receptors. Neuroendocrinology. 2003; 77: 314-23. Akinci MK, Schofield PR. Widespread expression of GABA(A) receptor subunits in peripheral tissues. Neurosci Res. 1999; 35: 145-53. Metzeler K, Agoston A, Gratzl M. An Intrinsic gamma-aminobutyric acid (GABA)ergic system in the adrenal cortex: findings from human and rat adrenal glands and the NCI-H295R cell line. Endocrinology. 2004; 145: 2402-11. Garry DJ, Sorenson RL, Coulter HD. Ultrastructural localization of gamma amino butyric acid immunoreactivity in B cells of the rat pancreas. Diabetologia. 1987b; 30: 115-9. Adeghate E, Ponery AS. GABA in the endocrine pancreas: cellular localization and function in normal and diabetic rats.Tissue Cell. 2002; 34: 1-6. Gammelsaeter R, Frøyland M, Aragón C, Danbolt NC, Fortin D, Storm-Mathisen J, Davanger S, Gundersen V. Glycine, GABA and their transporters in pancreatic islets of Langerhans: evidence for a paracrine transmitter interplay. J Cell Sci. 2004; 117: 3749-58. Garry DJ, Garry MG, Sorenson RL. Ultrastructural immunocytochemical localization of L-glutamate decarboxylase and GABA in rat pancreatic zymogen granules. Cell Tissue Res. 1988; 252: 191-7. Park YD, Cui ZY, Wu G, Park HS, Park HJ. Gamma-aminobutyric acid secreted from islet beta-cells modulates exocrine secretion in rat pancreas. World. J.Gastroenterol. 2006; 12: 3026-30. End K, Gamel-Didelon K, Jung H, Tolnay M, Lüdecke D, Gratzl M, Mayerhofer A. Receptors and sites of synthesis and storage of gamma-aminobutyric acid in human pituitary glands and in growth hormone adenomas. Am J Clin Pathol. 2005; 124: 550-8. Hardt J, Larsson LI, Hougaard DM. Immunocytochemical evidence suggesting that diamine oxidase catalyzes biosynthesis of gamma-aminobutyric acid in antropyloric gastrin cells. J Histochem Cytochem. 2000; 48: 839-46. Kosuge Y, Kawaguchi M, Sawaki K, Okubo M, Shinomiya T, Sakai T. Immunohistochemical study on GABAergic system in salivary glands. Eur J Pharmacol. 2009; 610: 18-22. Taniguchi H, Okada Y, Seguchi H, Shimada C, Seki M, Tsutou A, Baba S. High concentration of gamma-aminobutyric acid in pancreatic beta cells. Diabetes. 1979; 28: 629-33. Michalik M, Erecińska M. GABA in pancreatic islets: metabolism and function. Biochem Pharmacol. 1992; 44: 1-9. Roberts E, Kuriyama K. Biochemical-physiological correlations in studies of the gamma-aminobutyric acid system. Brain Res. 1968; 8: 1-35. Zamboni L, De Martino C. Buffered picric acid-formaldehyde: a new rapid fixative for electron microscopy. J Cell Biol. 1967; 35:148A. Mőller W. Paraffinum liquidum in einer Intermedienkombination fǖr die Paraffineinbettung. Mikroskopie. 1976; 32:100-104. Sternberger LA. Immunocytochemistry. Prentice Hall, Englewood Cliffs. 1974. Carlemalm E, Garavito RM, Williger W. Resin devolepement for electron microscopy and an analysis of embedding at low temperature. J Microsc. 1982; 126:123-143. Roth J. The protein A-gold technique – a quantitative approach for antigen localization on thin sections. In: Bullock GR, Petrusz P (eds). Techiques in immunocytochemistry. Academic Press, London, New York. 1982; pp 107-132. Bendayan M. Protein A-gold electron microscopic immunocytochemistry: methods, applications, and limitations. J Electron Microsc techn. 1984; 1: 243-270. Reynolds ES. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol. 1963; 17: 208-212. Okada Y, Taniguchi H, Schimada C. High concentration of GABA and high glutamate decarboxylase activity in rat pancreatic islets and human insulinoma. Science. 1976 ; 194: 620-2. Taniguchi H, Murakomi K, Yoshioka M, Ejiri K, Ishihara K, Baba S, Okada Y. GABA and insulin in pancreatic islets. In: Problems in GABA Research from Brain to Bacteria, Okada Y, Roberts E. Editors, Excerpta Medica, Amsterdam, 1982a; pp.382-405. Taniguchi H, Yoshioka M, Ejiri K, Ishikara K, Tamagawa M, Hirose Y, Utsumi M, Baba S, Okada Y. Suppression of somatostatin release and increase of somatostatin content in pancreatic islets by GABA. In: In: Problems in GABA Research from Brain to Bacteria, Okada Y, Roberts E. Editors, Excerpta Medica, Amsterdam, 1982b; pp.406-412. Tanaka C. gamma-Aminobutyric acid in peripheral tissues. Life Sci. 1985; 37: 2221-35. Garry DJ, Sorenson RL, Elde RP, Maley BE, Madsen A. Immunohistochemical colocalization of GABA and insulin in beta-cells of rat islet. Diabetes. 1986; 35: 1090-5. Garry DJ, Coulter HD, McIntee TJ, Wu JY, Sorenson RL. Immunoreactive GABA transaminase within the pancreatic islet is localized in mitochondria of the B-cell. J Histochem Cytochem. 1987a; 35: 831-6. McIntire SL, Jorgensen E, Kaplan J, Horvitz HR. The GABAergic nervous system of Caenorhabditis elegans. Nature. 1993; 364: 337-41. Ukena K, Oumi T, Matsushima O, Ikeda T, Fujita T, Minakata H, Nomoto K. Effects of annetocin, an oxytocin-related peptide isolated from the earthworm Eisenia foetida, and some putative neurotransmitters on gut motility of the earthworm. J Exp Zool. 1995; 272: 184-93. Telkes I, Csoknya M, Buzas P, Gabriel R, Hamori J, Elekes K. GABA-immunoreactive neurons in the central and peripheral nervous system of the earthworm, Lumbricus terrestris (Oligochaeta, Annelida). Cell Tissue Res. 1996; 285: 463-475. Sakaue M, Saito N, Tanaka C. Immunohistochemical localization of gamma-aminobutyric acid (GABA) in the rat pancreas. Histochemistry. 1987; 86: 365-9. Gerber JC, Hare TA. GABA in peripheral tissues: Presence and action in pancreatic function. Brain Res 1980; 5: 341-346. Smismans A, Schuit E, Pipeleers D. Nutrient regulation of gamma-aminobutyric acid release. 1997; 40: 1411-1415. Ligon B, Yang J, Morin SB, Ruberti MF, Steer ML. Regulation of pancreatic islet cell survival and replication by gamma-aminobutyric acid. Diabetologia. 2007; 50: 764-73. Dong H, Kumar M, Zhang Y, Gyulkhandanyan A, Xiang YY, Ye B, Perrella J, Hyder A, Zhang N, Wheeler M, Lu WY, Wang Q. Gamma-aminobutyric acid up- and downregulates insulin secretion from beta cells in concert with changes in glucose concentration. Diabetologia. 2006; 49: 697-705. Gilon P, Tappaz M, Remacle C. Localization of GAD-like immunoreactivity in the pancreas and stomach of the rat and mouse. Histochemistry. 1991; 96: 355-65. Gilon P, Remacle C. High-affinity GABA uptake in a subpopulation of somatostatin cells in rat pancreas. J Histochem Cytochem. 1989; 37: 1133-9. |
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Correspondence: | Ioana Trandaburu, Institute of Biology, Spl. Independenţei 296, 060031, Bucharest, Romania, e-mail: itrandaburu@yahoo.com; ioana.trandaburu@ibiol.ro |
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Article Title: | The immunocytochemical detection of gamma-aminobutyric acid (GABA) in the pancreas of amphibian Rana esculenta; light- and electron-microscopic observations |
Authors: | Ioana TRANDABURU1, Wolfgang KUMMER2, Tiberiu TRANDABURU3 |
Affiliation: | 1 Center of Cytobiology, Institute of Biology, Bucharest, Romania 2 Institute of Anatomy and Cell Biology, Giessen, Germany 3 Laboratory of Histology and Embryology, Faculty of Sciences, University of Piteşti, Romania |
Abstract: | The immunolabelled structures for gamma-aminobutyric acid (GABA) and their topographic distributions in the pancreas of the frog Rana esculenta are described for the first time in light and electron microscopy. At light microscopic level, the immunoreaction was detected both in the islets of Langerhans and the nerve fibbers supplying the exocrine tissue. At submicroscopic level, this multifunctional amino acid was identified in cytosol, secretory granules matrix and nuclear chromatin of insulin (INS)-, stomatostatin (SOM)-, glucagon (GLUC)- and pancreatic polypeptide (PP)- producing cells. Other reactive sites for this amino acid included the zymogen granules, mitochondria and nuclei of acinar cells. The above results and their functional significances entirely supporting the concept of a good conservation of this amino acid during phylogeny are discussed in connection with the findings previously reported in human and mammalian organs. |
Keywords: | gamma-aminobutyric acid, GABA, Rana esculenta, pancreas, immunocytochemistry |
References: | Awapara J, Landau AJ, Fuerst R, Seale B. Free aminobutyric acid in brain. J. Biol. Chem.1950; 187: 35-39. Roberts E, Frankel S. γ- aminobutyric acid in brain. Its formation from glutamic acid. J. Biol. Chem. 1950; 187: 55-63. Roberts E, Hammerschlag RS. Gamma-aminobutyric acid (GABA). In Albers RW, Siegel GL, Katzman R, Agranoff BW (eds) Basic neurochemistry, 1972; pp. 131-165. Krnjevic K: Inhibitory action of GABA and GABA-mimetics on vertebrate neurons. In: GABA in Nervous System Function, Roberts, E.: Chase, T.N.; Tower, D.B., editors, Raven Press, New York 1976; pp.269-281. Fekete C, Wittmann G, Liposits Z, Lechan RM. GABA-ergic innervation of thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus of the rat. Brain Res. 2002; 957: 251-8. Kalsbeek A, Foppen E, Schalij I, Van Heijningen C, van der Vliet J, Fliers E, Buijs RM. Circadian control of the daily plasma glucose rhythm: an interplay of GABA and glutamate. PLoS One. 2008; 3: e3194. Iwasa K, Oomori Y, Tanaka H. Gamma aminobutyric acid immunoreactivity in the mouse adrenal gland during postnatal development. Arch Histol Cytol. 1998; 61: 373-82. Iwasa K, Oomori Y, Tanaka H. Colocalization of gamma-aminobutyric acid immunoreactivity and acetylcholinesterase activity in nerve fibers of the mouse adrenal gland. J Vet Med Sci. 1999; 61: 631-5. Gladkevich A, Korf J, Hakobyan VP, Melkonyan KV. The peripheral GABAergic system as a target in endocrine disorders. Auton Neurosci. 2006; 124: 1-8. Wiens SC, Trudeau VL. Thyroid hormone and gamma-aminobutyric acid (GABA) interactions in neuroendocrine systems. Comp Biochem Physiol A Mol Integr Physiol. 2006; 144: 332-44. Schaeffer JM, Hsueh AJ. Identification of gamma-aminobutyric acid and its binding sites in the rat ovary. Life Sci. 1982; 30: 1599-1604. László A, Villányi P, Zsolnai B, Erdö SL. Gamma-aminobutyric acid, its related enzymes and receptor-binding sites in the human ovary and fallopian tube. Gynecol Obstet Invest. 1989; 28: 94-7. Erdö SL, Joo F, Wolff JR. Immunohistochemical localization of glutamate decarboxylase in the rat oviduct and ovary: further evidence for non-neural GABA systems. Cell Tissue Res. 1989; 255: 431-4. Hu JH, Yan YC. Identification of gamma 1 subunit of GABA(A) receptor in rat testis. Cell Res. 2002; 12: 33-7. Geigerseder C, Doepner R, Thalhammer A, Frungieri MB, Gamel-Didelon K, Calandra RS, Köhn FM, Mayerhofer A. Evidence for a GABAergic system in rodent and human testis: local GABA production and GABA receptors. Neuroendocrinology. 2003; 77: 314-23. Akinci MK, Schofield PR. Widespread expression of GABA(A) receptor subunits in peripheral tissues. Neurosci Res. 1999; 35: 145-53. Metzeler K, Agoston A, Gratzl M. An Intrinsic gamma-aminobutyric acid (GABA)ergic system in the adrenal cortex: findings from human and rat adrenal glands and the NCI-H295R cell line. Endocrinology. 2004; 145: 2402-11. Garry DJ, Sorenson RL, Coulter HD. Ultrastructural localization of gamma amino butyric acid immunoreactivity in B cells of the rat pancreas. Diabetologia. 1987b; 30: 115-9. Adeghate E, Ponery AS. GABA in the endocrine pancreas: cellular localization and function in normal and diabetic rats.Tissue Cell. 2002; 34: 1-6. Gammelsaeter R, Frøyland M, Aragón C, Danbolt NC, Fortin D, Storm-Mathisen J, Davanger S, Gundersen V. Glycine, GABA and their transporters in pancreatic islets of Langerhans: evidence for a paracrine transmitter interplay. J Cell Sci. 2004; 117: 3749-58. Garry DJ, Garry MG, Sorenson RL. Ultrastructural immunocytochemical localization of L-glutamate decarboxylase and GABA in rat pancreatic zymogen granules. Cell Tissue Res. 1988; 252: 191-7. Park YD, Cui ZY, Wu G, Park HS, Park HJ. Gamma-aminobutyric acid secreted from islet beta-cells modulates exocrine secretion in rat pancreas. World. J.Gastroenterol. 2006; 12: 3026-30. End K, Gamel-Didelon K, Jung H, Tolnay M, Lüdecke D, Gratzl M, Mayerhofer A. Receptors and sites of synthesis and storage of gamma-aminobutyric acid in human pituitary glands and in growth hormone adenomas. Am J Clin Pathol. 2005; 124: 550-8. Hardt J, Larsson LI, Hougaard DM. Immunocytochemical evidence suggesting that diamine oxidase catalyzes biosynthesis of gamma-aminobutyric acid in antropyloric gastrin cells. J Histochem Cytochem. 2000; 48: 839-46. Kosuge Y, Kawaguchi M, Sawaki K, Okubo M, Shinomiya T, Sakai T. Immunohistochemical study on GABAergic system in salivary glands. Eur J Pharmacol. 2009; 610: 18-22. Taniguchi H, Okada Y, Seguchi H, Shimada C, Seki M, Tsutou A, Baba S. High concentration of gamma-aminobutyric acid in pancreatic beta cells. Diabetes. 1979; 28: 629-33. Michalik M, Erecińska M. GABA in pancreatic islets: metabolism and function. Biochem Pharmacol. 1992; 44: 1-9. Roberts E, Kuriyama K. Biochemical-physiological correlations in studies of the gamma-aminobutyric acid system. Brain Res. 1968; 8: 1-35. Zamboni L, De Martino C. Buffered picric acid-formaldehyde: a new rapid fixative for electron microscopy. J Cell Biol. 1967; 35:148A. Mőller W. Paraffinum liquidum in einer Intermedienkombination fǖr die Paraffineinbettung. Mikroskopie. 1976; 32:100-104. Sternberger LA. Immunocytochemistry. Prentice Hall, Englewood Cliffs. 1974. Carlemalm E, Garavito RM, Williger W. Resin devolepement for electron microscopy and an analysis of embedding at low temperature. J Microsc. 1982; 126:123-143. Roth J. The protein A-gold technique – a quantitative approach for antigen localization on thin sections. In: Bullock GR, Petrusz P (eds). Techiques in immunocytochemistry. Academic Press, London, New York. 1982; pp 107-132. Bendayan M. Protein A-gold electron microscopic immunocytochemistry: methods, applications, and limitations. J Electron Microsc techn. 1984; 1: 243-270. Reynolds ES. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol. 1963; 17: 208-212. Okada Y, Taniguchi H, Schimada C. High concentration of GABA and high glutamate decarboxylase activity in rat pancreatic islets and human insulinoma. Science. 1976 ; 194: 620-2. Taniguchi H, Murakomi K, Yoshioka M, Ejiri K, Ishihara K, Baba S, Okada Y. GABA and insulin in pancreatic islets. In: Problems in GABA Research from Brain to Bacteria, Okada Y, Roberts E. Editors, Excerpta Medica, Amsterdam, 1982a; pp.382-405. Taniguchi H, Yoshioka M, Ejiri K, Ishikara K, Tamagawa M, Hirose Y, Utsumi M, Baba S, Okada Y. Suppression of somatostatin release and increase of somatostatin content in pancreatic islets by GABA. In: In: Problems in GABA Research from Brain to Bacteria, Okada Y, Roberts E. Editors, Excerpta Medica, Amsterdam, 1982b; pp.406-412. Tanaka C. gamma-Aminobutyric acid in peripheral tissues. Life Sci. 1985; 37: 2221-35. Garry DJ, Sorenson RL, Elde RP, Maley BE, Madsen A. Immunohistochemical colocalization of GABA and insulin in beta-cells of rat islet. Diabetes. 1986; 35: 1090-5. Garry DJ, Coulter HD, McIntee TJ, Wu JY, Sorenson RL. Immunoreactive GABA transaminase within the pancreatic islet is localized in mitochondria of the B-cell. J Histochem Cytochem. 1987a; 35: 831-6. McIntire SL, Jorgensen E, Kaplan J, Horvitz HR. The GABAergic nervous system of Caenorhabditis elegans. Nature. 1993; 364: 337-41. Ukena K, Oumi T, Matsushima O, Ikeda T, Fujita T, Minakata H, Nomoto K. Effects of annetocin, an oxytocin-related peptide isolated from the earthworm Eisenia foetida, and some putative neurotransmitters on gut motility of the earthworm. J Exp Zool. 1995; 272: 184-93. Telkes I, Csoknya M, Buzas P, Gabriel R, Hamori J, Elekes K. GABA-immunoreactive neurons in the central and peripheral nervous system of the earthworm, Lumbricus terrestris (Oligochaeta, Annelida). Cell Tissue Res. 1996; 285: 463-475. Sakaue M, Saito N, Tanaka C. Immunohistochemical localization of gamma-aminobutyric acid (GABA) in the rat pancreas. Histochemistry. 1987; 86: 365-9. Gerber JC, Hare TA. GABA in peripheral tissues: Presence and action in pancreatic function. Brain Res 1980; 5: 341-346. Smismans A, Schuit E, Pipeleers D. Nutrient regulation of gamma-aminobutyric acid release. 1997; 40: 1411-1415. Ligon B, Yang J, Morin SB, Ruberti MF, Steer ML. Regulation of pancreatic islet cell survival and replication by gamma-aminobutyric acid. Diabetologia. 2007; 50: 764-73. Dong H, Kumar M, Zhang Y, Gyulkhandanyan A, Xiang YY, Ye B, Perrella J, Hyder A, Zhang N, Wheeler M, Lu WY, Wang Q. Gamma-aminobutyric acid up- and downregulates insulin secretion from beta cells in concert with changes in glucose concentration. Diabetologia. 2006; 49: 697-705. Gilon P, Tappaz M, Remacle C. Localization of GAD-like immunoreactivity in the pancreas and stomach of the rat and mouse. Histochemistry. 1991; 96: 355-65. Gilon P, Remacle C. High-affinity GABA uptake in a subpopulation of somatostatin cells in rat pancreas. J Histochem Cytochem. 1989; 37: 1133-9. |
*Correspondence: | Ioana Trandaburu, Institute of Biology, Spl. Independenţei 296, 060031, Bucharest, Romania, e-mail: itrandaburu@yahoo.com; ioana.trandaburu@ibiol.ro |