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The Melanin of the Myxomycete Stemonitis Herbatica NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY VOLUME 38 NUMBER 2 http://rcin.org.pl WARSAW, POLAND 1999 ISSN 0065-1583 Polish Academy of Sciences Nencki Institute of Experimental Biology and Polish Society of Cell Biology ACTA PROTOZOOLOGICA International Journal on Protistology Editor in Chief Jerzy SIKORA Editors Hanna FABCZAK and Anna WASIK Managing Editor Małgorzata WORONOWICZ Editorial Board Andre ADOUTTE, Paris J. I. Ronny LARSSON, Lund Christian F. BARDELE, Tübingen John J. LEE, New York Magdolna Cs. BERECZKY, Göd Jiri LOM, Ćeske Budejovice Jean COHEN, Gif-Sur-Yvette Pierangelo LUPORINI, Camerino John O. CORLISS, Albuquerque Hans MACHEMER, Bochum Gyorgy CSABA, Budapest Jean-Pierre MIGNOT, Aubiere Isabelle DESPORTES-LIVAGE, Paris Yutaka NAITOH, Tsukuba Tom FENCHEL, Helsing0r Jytte R. NILSSON, Copenhagen Wilhelm FOISSNER, Salsburg Eduardo ORIAS, Santa Barbara Vassil GOLEMANSKY, Sofia Dimitrii V. OSSIPOV, St. Petersburg Andrzej GRĘBECKI, Warszawa, Vice-Chairman Leif RASMUSSEN, Odense Lucyna GRĘBECKA, Warszawa Sergei O. SKARLATO, St. Petersburg Donat-Peter HÄDER, Erlangen Michael SLEIGH, Southampton Janina KACZANOWSKA, Warszawa JifiVÄVRA, Praha Stanisław L. KAZUBSKI, Warszawa Patricia L. WALNE, Knoxville Leszek KUŹNICKI, Warszawa, Chairman ACTA PROTOZOOLOGICA appears quarterly. The price (including Air Mail postage) of subscription to ACTA PROTOZOOLOGICA at 1999 is: US $ 180,- by institutions and US $ 120,- by individual subscribers. Limited numbers of back volumes at reduced rate are available. TERMS OF PAYMENT: check, money oder or payment to be made to the Nencki Institute of Experimental Biology account: 11101053-3522-2700-1-34 at Państwowy Bank Kredytowy XIII Oddz. Warszawa, Poland. For matters regarding ACTA PROTOZOOLOGICA, contact Editor, Nencki Institute of Experimental Biology, ul. Pasteura 3, 02-093 Warszawa, Poland; Fax: (4822) 822 53 42; E-mail: [email protected] For more information see Web page http://www.nencki.gov.pl/public.htm), Front cover: Trichomonas aotus sp. n. In: F. F. Pindak and M. Mora de Pindak (1998) Diagnostic characteristics of owl monkey (AoTus trivignatus) intestinal trichomonads. Acta Protozool. 37: 159-172 ©Nencki Institute of Experimental Biology, Desktop processing: Justyna Osmulska, Data Processing Polish Academy of Sciences Laboratory of the Nencki Institute This publication is supported by the State Committee for Printed at the MARBIS, ul. Kombatantów 60, Scientific Research 05-070 Sulejówek, Poland http://rcin.org.pl ACTA Acta Protozool. (1999) 38: 87 - 96 PROTOZOOLOGICA Review Article Ciliary and Flagellar Activity Control in Eukaryotic Cells by Second Messengers: Calcium Ions and Cyclic Nucleotides Hanna FABCZAK, Mirosława WALERCZYK, Jerzy SIKORA and Stanisław FABCZAK Department of Cell Biology, Nencki Institute of Experimental Biology, Warsaw, Poland Key words: axoneme, Ca:+, calmodulin, cAMP, cGMP, cilium, flagellum, ion channels, protein kinases. Summary. Extracellular stimuli are converted in eukaryotic cells through signal transduction mechanisms to generate intracellular second messengers such as cyclic nucleotides and Ca2+. These molecular signals, amongst other, may control the ciliary and flagellar locomotor systems by modulating the activity of axonemes, changing the direction and frequency of effective ciliary beating or changing the pattern of flagellar motion. The primary role in regulating the mechanisms of axonemal motility by second messengers is played by processes of phosphorylation and dephosphorylation of axoneme proteins. Ca2+ may also regulate the levels of cAMP and cGMP by controlling the activity of cAMP and cGMP cyclases. In addition, Ca:+ and cyclic nucleotides may regulate ion channel conductance, thus affecting the cell membrane potential in these cells. INTRODUCTION invertebrates and spermatozoa. They are also essential for the movement of eggs along oviducts and mucus in the The forces that make the movement of eukaryotic tracts of respiratory systems. The microtubules within an cells possible by means of flagella and cilia are generated axoneme are arranged in a way that a central pair of by cytoskeletal microtubular systems. The essential ele- microtubules is surrounded by a ring of peripheral nine ment of these structures consists of microtubules which, microtubular doublets (9 + 2 scheme) (Fig. 1). Each together with numerous accompanying proteins, form the microtubule consists of tubulin heterodimers, known as axoneme - the skeleton of flagella and cilia covered by the a- and (3-tubulins. The tubulin dimers in central doublets ciliary or flagellar membrane. These organelles constitute are organized into a complete tubule containing 13 the motile systems of protozoa, algae, the larvae of some protofilaments per one tubule. The nine peripheral dou- blets are formed by one complete tubule A and an attached one incomplete tubule B. Each tubule A of these doublets Address for correspondence: Hanna Fabczak, Nencki Institute of is joined to the central sheath of the axoneme by radial Experimental Biology, Polish Academy of Sciences, Department of spokes and bears also two dynein arms pointed toward the Cell Biology, ul. Pasteura 3, 02-093 Warszawa, Poland; Fax: (4822) 822 53 42; E-mail: [email protected] tubule B of the next doublet. Microtubule doublets are also http://rcin.org.pl 88 H. Fabczak et al. Ciliary/ external stimuli and leads over a series of intracellular flagellar events to axoneme activity changes. membrane Tubule A Tubule B IMPORTANCE OF Ca2+ AND CALMODULIN FOR THE AXONEME FUNCTION Outer dynein External stimuli recognized by receptors located within arm the cell membrane affect the pattern of axoneme move- ment and of cell motile behavior through the action of secondary transmitters like Ca2+ and cyclic nucleotides. Nexin link Studies on the regulation of ciliary movement have been carried out for a long time on ciliate cells and recently on Central the ciliated respiratory epithelium of higher organisms Inner singlet (Schultz et al. 1990; Bonini et al. 1991; Salathe et al dynein microtubule arm 1993; Geary et al. 1995; Salathe and Bookman 1995). The mechanism of flagellar movement is most often Outer studied in Chlamydomonas (Tash 1989; Walczak and doublet Nelson 1994; Habermacher and Sale 1995, 1997) and in microtubule spermatozoa (Cook and Babcocks 1993 a, b; Cook et al. 1994). Ciliates Fig. 1. Schematic illustration of the microtubule arrangement of ciliary or flagellar axoneme The phenomenon of ciliary reversal has long been known to occur in freshwater ciliates in response to different stimuli such as light, temperature, and chemical or mechanical stimulations (Fabczak and Wood 1980; held together by nexin protein links (Stephens 1974, Ogura and Machemer 1980, Machemer and Deitmer Warner 1974, Omoto 1995). The protein of which the 1985; Nakaoka et al. 1987; Van Houten 1988; Fabczak dynein arms consist exhibits Mg2+-dependent ATPase etal. 1993 a, b; Kuriu etal. 1996). It consists of a transient activity. The longitudinal sliding of the outer doublets of change in the direction of power stroke of cilia to an microtubules coupled to the hydrolysis of ATP by dynein opposite one and an increased beat frequency, which (Satir 1985, Gibbons 1989), is converted to a bending results in backward swimming (Eckert 1972, Eckert and motion, characteristic for ciliary and flagellar beating, by Brehm 1979, Preston and Saimi 1990). In natural condi- shear resistance due to some structures such as nexin tions this phenomenon, for example, occurs when a links, radial spokes and basal bodies. This is an essential forward swimming ciliate encounters a stable obstacle. It feature of the motile behavior of cilium and flagellum briefly backs away, tumbles momentarily and changes its (Satir 1985). Movement of flagella can be approximately swimming direction. Reversal of the ciliary beat in these characterized as oscillation in two dimensions. The motion cells is strictly correlated with the generation of depolar- of cilium is more complex, occurring in two phases, a rapid izing receptor potential, which in turn evokes an action one-dimensional power stroke affecting the forward move- potential. The action potential is generated due to the ment of the cell and a slower three-dimensional return of activation of voltage-dependent Ca2+ channels located in the cilium to the initial position. The frequency of ciliary the ciliary membrane and an influx of Ca2+ into the cilium beatings and the direction of effective power stroke of the (Dunlap 1977, Tamm 1994). Restoration of the mem- cilium, as well as flagellar waveform, are modulated when brane potential (repolarization) following stimulation oc- the cell responds behaviorally to environmental stimuli curs due to activation of K+ channels in the plasma (Sleigh 1974). Thus, both the cilium and flagellum serve membrane (Eckert and Brehm 1979, Bonini et. al. 1991), as the effector in the complex process of signal transduc- whereas the resting Ca2+ level within cell is restored by tion. This process starts with the receptor perception of Ca2+-ATPase existing in the plasma, ciliary and alveolar http://rcin.org.pl Cilia and flagella motility 89 Depolarization Hyperpolarization ciliary reversal fast forward swimming Fig. 2. Diagrams showing cilium responses to the membrane depolarization (A) or its hyperpolarization (B). A - depolarizing stimulus causes an opening of voltage-dependent Ca2+ channels in ciliary membrane and influx of extracellular Ca2+ into the cilium. The transient increase in ciliary free
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