Abstract
Adrenomedullin (AMD), proadrenomedullin N-terminal 20 peptide (PAMP) and calcitonin gene-related peptide (CGRP) were studied for chemotaxis, chemotactic selection and G-actin/F-actin transition in Tetrahymena. The aim of the experiments was to study the effects of two different peptides encoded by the same gene compared to a peptide related to one of the two, but encoded by a different gene, at a low level of phylogeny. The positive, chemotactic effect of ADM and the strong negative, chemorepellent effect of PAMP suggest that in Tetrahymena, the two peptides elicit their chemotactic effects via different signalling mechanisms. The complexity of swimming behaviour modulated by the three peptides underlines that chemotaxis, chemokinesis and some characteristics of migratory behaviour (velocity, tortuosity) are working as a sub-population level complex functional unit. Chemotactic responsiveness to ADM and CGRP is short-term, in contrast to PAMP, which as a chemorepellent ligand, has the ability to select sub-populations with negative chemotactic responsiveness. The different effects of ADM and PAMP on the polymerization of actin networks show that the microtubular structure of cilia is more essential to chemotactic response than are transitions of the actin network. The results draw attention to the characteristic effects of vasoactive peptides at this low level of phylogeny.
Similar content being viewed by others
References
LeRoith D, Schiloach J, Roth J, Lesniak MA (1980) Evolutionary origins of vertebrate hormones: substances similar to mammalian insulin are native to unicellular eukaryotes. Proc Natl Acad Sci USA 77:6184–6186
LeRoith D, Schiloach J, Berelowitz M, Frohman LA, Krieger BT, Roth J (1983) Are messenger molecules in microbes the ancestors of the vertebrate hormones and tissue factors? Fed Proc 42:2602–2607
Csaba G (1980) Phylogeny and ontogeny of hormone receptors: the selection theory of receptor formation and hormonal imprinting. Biol Rev 55:47–63
Csaba G (2000) Hormonal imprinting: its role during the evolution and development of hormone receptors. Cell Biol Int 24:407–414
Kovács P, Csaba G (1990) Influence of phosphoinositol (PI) system in the mechanism of hormonal imprinting. Biochem Biophys Res Commun 170:119–126
Lenhoff HM (1968) Behavior, hormones and hydra. Science 161:434–442
Kőhidai L, Soós P, Csaba G (1997) Effects of dipeptides containing the amino acid, proline on the chemotaxis of Tetrahymena pyriformis. - Evolutionary conclusions on the formation of hormone receptors and hormones. Cell Biol Int 21:341–345
Kőhidai L, Tóth K, Ruskoaho H, Csaba G (2001) Effect of vasoactive peptides on Tetrahymena. chemotactic properties of endothelins (ET-1, ET-2, ET-3, fragment 11-21 of ET-1 and big endothelin-1): a short-term inducible signalling mechanism of chemotaxis. Cell Biol Int 25:1173–1177
Kitamura K, Kangawa K, Kawamoto M, Ichiki Y, Nakamura S, Matsuo H, Eto T (1993) Adrenomedullin. A novel hypotensive peptide isolated from human pheochromocytoma. Biochem Biophys Res Commun 192:553–560
Kuwasako K, Kitamura K, Ichiki Y, Kato J, Kangawa K, Matsuo H, Eto T (1995) Human proadrenomedullin N-terminal 20 peptide in pheochromocytoma and normal adrenal medulla. Biochem Biophys Res Commun 211:694–699
Kitamura K, Sakata J, Kangawa K, Kojima M, Matsuo H, Eto T (1993) Cloning and characterization of cDNA encoding a precursor for human adrenomedullin. Biochem Biophys Res Commun 194:720–725
Sakata J, Shimokubo T, Kitamura K, Nakamura S, Kangawa K, Matsuo H, Eto T (1993) Molecular cloning and biological activities of rat adrenomedullin, a hypotensive peptide. Biochem Biophys Res Commun 195:921–927
Iwasaki H, Hirata Y, Iwashina M, Sato K, Marumo F (1996) Specific binding sites for proadrenomedullin N-terminal peptide (PAMP) in rat. Endocrinology 137:3045–3050
Kitamura K, Kangawa K, Kojima M, Ichiki Y, Matsuo H, Eto T (1994) Complete amino acid sequence of porcine adrenomedullin and cloning of cDNA encoding its precursor. FEBS Lett 338:306–310
Yousufzai SY, Ali N, Abdel-Latif AA (1999) Effects of adrenomedullin on cyclic AMP formation and on relaxation in iris sphincter smooth muscle. Invest Ophthalmol Vis Sci 40:3245–3253
McLatchle LM, Fraser NJ, Main MJ, Wise A, Brown J, Thompson N, Solari R, Lee MG, Foord SM (1998) RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393:333–339
Owji AA, Smith DM, Coppock HA, Morgan DG, Bhogal R, Ghatei MA, Bloom SR (1995) An abundant and specific binding site for the novel vasodilator adrenomedullin in the rat. Endocrinology 136:2127–2134
Takano K, Yamashita N, Fujita T (1996) Proadrenomedullin NH2-terminal 20 peptide inhibits the voltage-gated Ca2+ channel current through a pertussis toxin-sensitive G protein in rat pheochromocytoma-derived PC 12 cells. J Clin Invest 98:14–17
Shimosawa T, Ito Y, Ando K, Kitamura K, Kangawa K, Fujita T (1995) Proadrenomedullin NH2-terminal 20 peptide, a new product of the adrenomedullin gene, inhibits norepinephrine overflow from nerve endings. J Clin Invest 96:1672–1676
Feng CJ, Kang B, Kaye AD, Kadowitz PJ, Nossmman BD (1994) L-NAME modulates responses to adrenomedullin in the hindquarters vascular bed of the rat. Life Sci 55:433–438
Szokodi I, Kinnunen P, Tavi P, Weckström M, Tóth M, Ruskoaho H (1998) Evidence for cAMP-independent mechanisms mediating the effects of adrenomedullin, a new inotropic peptide. Circulation 97:1062–1070
Isumi Y, Minamino N, Kubo A, Nishimoto N, Yoshizaki K, Yoshioka M, Kangawa K, Matsuo H (1998) Adrenomedullin stimulates interleukin-6 production in Swiss 3T3 cells. Biochem Biophys Res Commun 244:325–331
Kamoi H, Kanzawa H, Hirata K, Kurihara N, Yano Y, Otani S (1995) Adrenomedullin inhibits the secretion of cytokine-induced neutrophil chemoattractant, a member of the interleukin-8 family, from rat alveolar macrophages. Biochem Biophys Res Commun 211:1031–1035
Horio T, Kohno M, Kano H, Ikeda M, Yasunari K, Yokokawa K, Minami M, Takeda T (1995) Adrenomedullin as a novel antimigration factor of vascular smooth muscle cells. Circ Res 77:660–664
Masakazu K, Koji Y, Hiroaki K, Kenichi Y, Mieko M, Hanehira T, Junichi Y (1997) Adrenomedullin is a potent inhibitor of angiotensin II induced migration of human coronary artery smooth muscle cells. Hypertension 29:1309–1313
Csaba G (1985) The unicellular Tetrahymena as a model cell for receptor research. Int Rev Cytol 95:327–377
Kőhidai L (1999) Chemotaxis: the proper physiological response to evaluate phylogeny of signal molecules. Acta Biol Hung 50:375–394
Levandowsky M, Cheng T, Kehr A, Kim J, Gardner L, Silvern L, Tsang L, Lai G, Chung C, Prakash E (1984) Chemosensory responses to amino acids and certain amines by the ciliate Tetrahymena: a flat capillary assay. Biol Bull 167:322–330
Kőhidai L, Karsa J, Csaba G (1994) Effects of hormones on chemotaxis in Tetrahymena: investigations on receptor memory. Microbios 77:75–85
Csaba G, Kovács P, Kőhidai L (1994) Tetrahymena cells distinguish insulin preparations according to their amorphous and crystalline form or their bovine and porcine origin. Aspects of hormone binding and chemotaxis in relation to imprinting. Microbios 80:215–221
Kőhidai L, Csaba G (1995) Effects of mammalian vasoconstrictor peptide endothelin-1 on Tetrahymena pyriformis GL and immunocytochemical detection of endogenous endothelin-like activity. Comp Biochem Physiol 111C:311–316
Kőhidai L, Csaba G, Karsa J (1994) Effects of atrial natriuretic peptide on the unicellular Tetrahymena pyriformis model. Microbios 82:27–40
Kőhidai L, Csaba G (1998) Chemotaxis and chemotactic selection induced with cytokines (IL-8, RANTES and TNF-a) in the unicellular Tetrahymena pyriformis. Cytokine 10:481–486
Kőhidai L, Láng O, Csaba G (2003) Chemotactic-range-fitting of amino acids and its correlations to physicochemical parameters in Tetrahymena pyriformis-evolutionary consequences. Cell Mol Biol (Noisy-le-grand) 49 Online Pub:OL487–495
Kőhidai L, Lemberkovits É, Csaba G (1995) Molecule dependent chemotactic responses of Tetrahymena pyriformis elicited by volatile oils. Acta Protozool 34:181–185
Huang ZJ, Haugland RP, You WM, Haugland RP (1992) Phallotoxin and actin binding assay by fluorescence enhancement. Anal Biochem 200:199–204
Hirono M, Kumagai Y, Numata O, Watanabe Y (1989) Purification of Tetrahymena actin reveals some unusual properties. Proc Natl Acad Sci USA 86:75–79
Hoey JG, Gavin RH (1992) Localization of actin in the Tetrahymena basal body-cage complex. J Cell Sci 103:629–641
Kőhidai L, Schiess N, Csaba G (2000) Chemotactic selection of Tetrahymena pyriformis GL induced with histamine, di-iodotyrosine or insulin. Comp Biochem Physiol 126C:1–9
Fry RC, Champion HC, Lawrence TC, Murphy WA, Coy DH, Kadowitz PJ (1997) Proadrenomedullin NH2-terminal peptide (PAMP)(12–20) has vasodepressor activity in the rat and cat. Life Sci 60:161–167
Kőhidai L, Kovács K, Csaba G (2002) Direct chemotactic effect of bradykinin and related peptides-significance of amino- and carboxyterminal character of oligopeptides in chemotaxis of tetrahymena pyriformis. Cell Biol Int 26:55–62
Kőhidai L, Bősze S, Soós P, Illyés E, Láng O, Mák M, Sebestyen F, Hudecz F (2003) Chemotactic activity of oligopeptides containing an EWS motif on Tetrahymena pyriformis: the effect of amidation of the C-terminal residue. Cell Biochem Funct 21:113–120
Kim JY, Borleis JA, Devreotes PN (1998) Switching of chemoattractant receptors programs development and morphogenesis in Dictyostelium: receptor subtypes activate common responses at different agonist concentrations. Dev Biol 197:117–128
Csaba G (2012) The hormonal system of the unicellular Tetrahymena: a review with evolutionary aspects. Acta Microbiol Immunol Hung 59:131–156
Csaba G (2012) Hormonal imprinting in the unicellular Tetrahymena: the proto-model of epigenetics. Acta Microbiol Immunol Hung 59:291–310
Acknowledgments
This study was funded by a research grant from the Hungarian Scientific Research Fund – OTKA (T17773).
Author information
Authors and Affiliations
Corresponding author
Additional information
László Kőhidai and Katalin Tóth have contributed equally to this work.
Rights and permissions
About this article
Cite this article
Kőhidai, L., Tóth, K., Samotik, P. et al. Effect of vasoactive peptides in Tetrahymena: chemotactic activities of adrenomedullin, proadrenomedullin N-terminal 20 peptide (PAMP) and calcitonin gene-related peptide (CGRP). Mol Cell Biochem 411, 271–280 (2016). https://doi.org/10.1007/s11010-015-2589-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11010-015-2589-6