Photosensory transduction in unicellular eukaryotes: A comparison between related ciliates Blepharisma japonicum and Stentor coeruleus and photoreceptor cells of higher organisms

Journal of Photochemistry and Photobiology B: Biology 83 (2006) 163–171 www.elsevier.com/locate/jphotobiol

Invited review

Photosensory transduction in unicellular eukaryotes: A comparison between related ciliates Blepharisma japonicum and Stentor coeruleus and photoreceptor cells of higher organisms Katarzyna Sobierajska, Hanna Fabczak, Stanisław Fabczak

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Department of Cell Biology, Nencki Institute of Experimental Biology, Polish Academy of Sciences, 3, Pasteur Street, PL 02 093 Warsaw, Poland Received 8 November 2005; received in revised form 29 December 2005; accepted 7 January 2006 Available online 20 February 2006

Abstract Blepharisma japonicum and Stentor coeruleus are related ciliates, conspicuous by their photosensitivity. They are capable of avoiding illuminated areas in the surrounding medium, gathering exclusively in most shaded places (photodispersal). Such behaviour results mainly from motile photophobic response occurring in ciliates. This light-avoiding response is observed during a relatively rapid increase in illumination intensity (light stimulus) and consists of cessation of cell movement, a period of backward movement (ciliary reversal), followed by a forward swimming, usually in a new direction. The photosensitivity of ciliates is ascribed to their photoreceptor system, composed of pigment granules, containing the endogenous photoreceptor – blepharismin in Blepharisma japonicum, and stentorin in Stentor coeruleus. A light stimulus, applied to both ciliates activates specific stimulus transduction processes leading to the electrical changes at the plasma membrane, correlated with a ciliary reversal during photophobic response. These data indicate that both ciliates Blepharisma japonicum and Stentor coeruleus, the lower eukaryotes, are capable of transducing the perceived light stimuli in a manner taking place in some photoreceptor cells of higher eukaryotes. Similarities and differences concerning particular stages of light transduction in eukaryotes at different evolutional levels are discussed in this article. Ó 2006 Elsevier B.V. All rights reserved. Keywords: Ciliates Blepharisma and Stentor; Cyclic nucleotide-activated channels; G-proteins; Phosducin; Photophobic response; Photoreceptor cells; Photosensory transduction; Protein phosphorylation; Second messengers

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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Photoreceptor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phototransduction cascade . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. G-proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Phosducins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Second messengers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.1. Cyclic nucleotides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.2. Inositol trisphosphate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Effector. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Cyclic nucleotide-activated ion channels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Photoreceptor and action potentials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Corresponding author. Tel.: + 48 22 822 2343; fax: + 48 22 822 5342. E-mail address: [email protected] (S. Fabczak).

1011-1344/$ - see front matter Ó 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.jphotobiol.2006.01.005

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Function . . . . . . . . Abbreviations . . . . Acknowledgements References . . . . . .

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1. Introduction Light is a stimulus, which can be perceived by organisms at nearly all stages of evolution. The process of perception begins with the absorption of light by the specific receptors, which in higher organisms are located in photoreceptor cells of some organs, while in eukaryotic microorganisms, in specialized organelles. In almost all eukaryotic organisms studied so far, the photoactivation of receptors triggers a specific transduction pathway, leading to the generation of photoreceptor potential at the plasma membrane. Thus a light stimulus can be either transduced into electrical signals, transmitted through the system of neurones to the central nervous system (as in the visual system of higher eukaryotes), or cause alterations in the motile behaviour of cells (as it happens in some protists) [1–3]. To protozoans, which possess a peculiar ‘‘visual’’ system, belong related light-pink Blepharisma japonicum and blue-green Stentor coreuleus. Both of them are capable of detecting illumination changes in the surrounding medium, which is manifested in avoidance of more intensely illuminated areas [4–10]. This photodispersion is the consequence of different motile photophobic behaviours: photokinesis, phototactic and photophobic responses. The phototactic response has so far been observed in Stentor coeruleus where it can appear when a moving ciliate is accidentally been exposed to a focused light beam and continues to move away from the light source, along the direction of light propagation [11–13]. Another form of movement alteration, observed in both ciliates, is the positive photokinesis, when in areas of continuous illumination of higher intensity, a cell moves faster than in more shaded places [8,9,14,15]. The crucial role in evoking photodispersion effect seems to be played by the motile photophobic response and its progress take place almost in the same manner in both ciliates. It occurs when a cell leaves a shaded surrounding and enters an illuminated area, i.e., in the case of a relatively rapid increase in light intensity (light stimulus) [8,16–19]. Photophobic response begins, after some time-lag from the stimulus onset, with cessation of cell movement as a result of ciliary beating being stopped. Subsequently, due to a transient ciliary reversion, the cell swims backward for some time and stops again to resume its forward movement, but usually in a direction changed as compared with that before the response. A delay of the photophobic response and the period of cellular backward movement depends on the intensity of the

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stimulus received, i.e., the higher the light intensity, the shorter time-lag and the longer period of backward movement. The photosensitivity of Blepharisma japonicum and Stentor coeruleus is ascribed to the endogenous photoreceptor system, which is present in these cells. Photoexcitation of the receptor system triggers a specific molecular mechanism, transducing perceived stimulus into bioelectrical changes at the plasma membrane, correlated with the photophobic response of the ciliate. In this review, we summarize our current understanding of the phototransduction processes in the ciliates Blepharisma japonicum and Stentor coeruleus, the earliest eukaryotes, evolved about two billion years ago, and compare it with well-known light transduction pathways in vertebrate or invertebrate photoreceptor cells. Some stages of the photosignal transduction in these protists are also compared to that of other lower eukaryotes. 2. Photoreceptor Studies on the cellular photopigment in Stentor coeruleus began in the late 19th century [20], and a few dozen years later, similar research was performed on the related ciliate Blepharisma japonicum [21]. In both protists the cellular photopigment is located in specific granules in the form of the multilayered lamella [22–25]. These organella contain a primary photoreceptor, a hypericin derivative – blepharismin in Blepharisma japonicum and stentorin in Stentor coeruleus [22,26] and are arranged longitudinally along the cell body between the ciliary rows [7,26–32]. Spectroscopic analysis of pigments showed that the blepharismin in Blepharisma japonicum and stentorin in Stentor coeruleus, constitutes a new class of photopigments. Their structure considerably differs from well-known photoreceptors, such as rhodopsin, bacteriorhodopsin, chlorophyll, phytochrome or flavins. Both pigments contain as a chromophore, the hypericin derivatives classified as meso-naphthodianthrones [23,33,34]. In Stentor coeruleus two groups of pigments are present, stentorin-1 and stentorin-2 [23,35]. The stentorin-1, characterized by a strong fluorescence, is a small protein complex, composed of at least two subunits (molecular weights 46 and 52 kDa). Unlike stentorin-1, stentorin-2, showing very faint fluorescence, is a large protein complex, composed of stentorin-2B, containing a chromophore, covalently bound to apoprotein of molecular weight approx. 50 kDa. Initial studies on the pigment detected in the granules of Blepharisma japonicum demon-

K. Sobierajska et al. / Journal of Photochemistry and Photobiology B: Biology 83 (2006) 163–171

strated that blepharismin, as a chromophore, is connected to a protein of molecular weight between 38 and 50 kDa [26,36]. Further studies showed, however, that blepharismin forms in this ciliate a complex with a protein of molecular weight approx. 200 kDa [25,26,37]. Photoreceptor, containing a hypericin-like chromophore, has been found also in Fabrea salina, another photosensitive ciliate [38,39]. However, using molecular biology techniques it also was possible to find out the presence of opsin coding gene in these cells. Opsin together with retinal forms rhodopsin, a photoreceptor, playing an essential role in the photoreceptor cells of invertebrates and vertebrates. Moreover, rhodopsin immunoanalogue has been shown to be present as well in Paramecium bursaria, the ciliate also susceptible to light [40]. At the present state of knowledge it becomes evident that further studies on the light perception in protists are required in order to determine the type of photoreceptor involved in light detection and related phenomena. 3. Phototransduction cascade 3.1. G-proteins Heterotrimeric G-proteins constitute an important link in signal transduction pathway in the receptor cells of all eukaryotes, including unicellular organisms [41]. Among the best recognized mechanisms of signalling pathways are those of photosensory transduction in vertebrates, where a stimulated photoreceptor, rhodopsin, activates a G-protein (transducin), thus catalysing the exchange of GDP for GTP, accompanied by a concomitant release of the Gbc complex. As a result of this process, two signal molecules are formed, Ga-GTP, which activates phosphodiesterase cGMP (PDE) and the Gbc dimer, responsible for proper interaction between the G-protein and the receptor, following activation of the latter, and initiation of the exchange of GDP for GTP. Moreover, the Gbc dimer has the capacity for making a complex with phosducin, expressing regulatory properties for G-protein activity [42,43]. The studies on the motile photobehaviour in lower eukaryotes, ciliates Blepharisma japonicum and Stentor coeruleus, also indicate the presence of G-proteins in these cells, and suggest that these proteins can, similarly as in cells of higher organisms, be involved in the mechanism of light transduction. This stems from experiments using antibodies against the a-subunit of transducin from the bovine retina that permitted to detect a protein of molecular weight 39 kDa in Stentor coeruleus [44]. This protein exhibits approximately 35% homology with the a-subunit of various heterotrimeric G-proteins of other eukaryotic organisms. Similar studies showed that also related Blepharisma japonicum possesses immunoanalogue of a-subunit of G-proteins of about 55 kDa [3]. Among other ciliates studied, the presence of proteins of molecular weight 57 kDa, binding GTP and involved in transduction of light

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stimuli, has also been demonstrated in the above-mentioned photosensitive ciliate Paramecium bursaria [45]. The possible role of G-proteins in phototransduction pathway in Blepharisma japonicum and Stentor coeruleus, was elucidated using selectively acting modulators of G-protein activity, such as cholera and pertussis toxins, fluoroaluminate and mastoparan [3]. Cholera and pertussis toxins are known to cause catalytic ADP-ribosylation of transducin involved in signal transduction by vertebrate photoreceptor cells [46]. Cholera toxin-catalyzed ribosylation of transducin was shown to prolong the action of the G-protein on its effector, the retinal cyclic nucleotide PDE. In the case of pertussis toxin, the transducin ADP-ribosylation can uncouple the G-protein from its receptor, photoactivated rhodopsin. As a consequence, the GTP-dependent action of transducin on the PDE appears as quenched by pertussis toxin. Fluoroaluminate is the factor, which can directly activate G-proteins by binding with them, in a manner similar to GTP [47]. Mastoparan has also been found to directly increase the activity of G-proteins, thus mimicking the role of the stimulus itself [48]. The most significant effect on the photoreaction in both Blepharisma japonicum and Stentor coeruleus has been observed while using pertussis and fluoroaluminate [44,49]. Though mastoparan also markedly changed kinetic parameters of photophobic response in Blepharisma japonicum [3]. These behavioural results indirectly confirm the presence of functional G-proteins and their involvement in the process of light transduction in these ciliates. 3.2. Phosducins Eukaryotic cells have developed mechanisms, allowing them to control very precisely different stages of the stimuli transduction pathways. The most important stages of this pathway comprise the regulation of G-proteins activity. One of G-protein regulators is a highly conserved phosphoprotein, phosducin. Although phosducin probably plays a role in signal transduction in variety of cell types, it is expressed at especially high levels in retinal rod cells, where it has been proposed to play an important role in light adaptation [50]. In photoreceptor cells of dark-adapted rods phosducin exists in the phosphorylated form and is a substrate of the protein kinase A, calmodulin-dependent kinase type II and G-protein coupled receptor kinase 2 [50– 54]. Illumination of the cells leads to a rapid dephosphorylation of this protein, resulting from activation of protein phosphatases, type 1 or 2A [51,55]. Unphosphorylated phosducin forms a complex with transducin bc dimer, thereby sequestering dimer in the cytosol and thus inhibiting bc association with a subunits, effectors or membranes [42,56–58]. Phosducin has been first identified in the photoreceptor cells and pineal gland of mammals [59–61]. However, further studies revealed that it also can be present in various tissues of higher organisms [42,62] as well as in some lower eukaryotes, like yeast [63], fungus [64] and Dictyostelium

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discoideum [65]. More recently, in Blepharisma japonicum a protein of molecular weight 28 kDa has been found, undergoing a specific, reversible dephosphorylation in light [66] and exhibiting a considerably high homology to phosducin of other organisms [67–69]. Phosducin of ciliates is a substrate of protein kinases A and G, and the level of its phosphorylation also depends on the Ca2+ and calmodulin. Illumination of Blepharisma japonicum cells activates protein phosphatases, whose functions are inhibited in the presence of okadaic acid and calyculin A, well-known phosphatase inhibitors, which can be attributed to the presence of protein phosphatases, type 1 and 2A, in this lightrelated process [69]. In vivo studies demonstrated that in a cell stimulated with light the dephosphorylated phosducin undergoes translocation towards the plasma membrane, where it has been proven to build a complex with Gbc [67,68]. A similar translocation has been observed in the photoreceptor cells of vertebrates where, following photoreceptor activation by light, dephosphorylated phosducin, coupled with Gbc, relocated from membrane discs to cytosol and next from outer to inner segment of the rod [51,70]. This phenomenon is of crucial importance for the process of photoreceptor adaptation in vision systems to various levels of background light [71]. 3.3. Second messengers 3.3.1. Cyclic nucleotides Vision in animals has evolved differently in vertebrates and invertebrates. Both groups use the rhodopsin, a seven transmembrane helix protein with covalently linked retinal, as the primary photoreceptor. In vertebrate photoreceptor cells (rods and cones), after light excitation, photoreceptor activates a transducin and a subsequent cyclic nucleotide PDE, resulting in the hydrolysis of cGMP and closure of the cGMP-activated cation channels. The Na+ and Ca2+ influx into the photoreceptor cells is inhibited, which leads to hyperpolarization of the plasma membrane. In photoreceptor cells of invertebrates the rhodopsins also activate Gprotein, which in this case however, activates phospholipase C (PLC). The activated PLC hydrolyses phosphatidylinositol-4,5-biphosphate (PInsP2) to inositol 1,4,5-trisphosphate (InsP3) and diacylglycerol (DAG). Subsequent steps differ among different photoreceptor cells. In Drosophila, DAG may activate TRP channels, thus Na+ and Ca2+ influx is enhanced and plasma membrane is depolarized [71]. In the photoreceptor cells of the Limulus ventral eye, the cascade of stimuli transduction involves InsP3 and Ca2+ and ends with stimulation of cGMP synthesis what results with opening of the cGMP-dependent channels and generation of the depolarizing receptor potential [72]. The first suggestions that second messengers participate in the light transduction process of ciliates originate from the studies on the cells elongation in Blepharisma japonicum during a long-term exposure to increased light intensity [73]. These studies have proven that the effect of light

may be considerably reduced in the result of increase of cytoplasmatic cGMP or cAMP levels. The involvement of cGMP in the photophobic response is indicated by a decrease in photosensitivity of Blepharisma japonicum and Stentor coeruleus in presence of factors increasing cytoplasmic cGMP level [44,49]. An opposite effect has been observed while using inhibitors of enzymatic activity, responsible for the synthesis of the cyclic nucleotide [44,49,74,75]. The above suggestion was confirmed by demonstration that illumination of Stentor coeruleus causes a rapid decrease in the concentration of cGMP and the presence of cGMP hydrolysis inhibitors decreases the photoinduced changes in the cGMP level. Therefore, it can be assumed that in Stentor coeruleus, similarly as in vertebrate photoreceptor cells, light can induce an activation of the PDE [75]. It should be pointed out that the period in which changes in cGMP level of the photostimulated Stentor coeruleus occur is similar to processes in the photoreceptor cells of the visual system in higher organisms [76]. 3.3.2. Inositol trisphosphate However, earlier behavioural studies, performed with the use of factors known to markedly disturb the inositol transduction pathway in the higher organism’s cells, suggest that in the course of the photophobic response in Blepharisma japonicum, InsP3 as second messenger can also be involved. This conclusion comes from the observation that neomycin, an inhibitor of the PInsP2 hydrolysis to InsP3 and DAG [77,78], causes a significant decrease in ciliate photosensitivity [79,80]. Similar changes in the cell photoresponses also occur under the influence of heparin, a well-known blocker of InsP3 receptor activity [81] as well as lithium ions, well-known for the property of reducing the monophosphoinositol phosphatase activity and decreasing the level of InsP3 in various cells [82–84]. As revealed by an in vivo analysis of the InsP3 level in this ciliate, in light-treated cells a fairly rapid increase in the cytoplasmatic level of this phosphoinositol can be observed, which is likely to result from the stimulation of PLC and PInsP2 hydrolysis [85]. Such changes in the cellular content of InsP3 are significantly reduced in ciliates, preincubated with lithium ions or neomycin. Protein analysis of the ciliate cortex fraction revealed in these preparations the occurrence of a protein of molecular weight approx. 200 kDa [86], showing similarity to the receptor protein for InsP3, (InsP3R). The evidence for the involvement of the identified receptor in transducing the photosignal and photophobic response in Blepharisma japonicum have also been provided by subsequent in vivo studies, in which an introduction of antibodies against InsP3R or antisense nucleotides blocked the photophobic reaction and reduced the expression level of InsP3R in these ciliates [87]. In view of the above presented experimental data, it seems likely that there exist two pathways of light stimulus transduction in the ciliate Blepharisma japonicum, similarly as in the photoreceptor cells of some invertebrates [72,88].

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4. Effector 4.1. Cyclic nucleotide-activated ion channels The final stage of the light transduction pathway in photoreceptor cells, both in invertebrates and vertebrates, modify the activity of the ion channels, located in the plasma membrane. As mentioned above, photostimulation of photoreceptor cells in vertebrates causes a reduction of the intracellular level of cGMP, and closure of cGMP-activated ion channel, followed by a membrane hyperpolarization [43]. Contrary to vertebrates, in most photoreceptor cells of invertebrates, light stimuli cause a plasma membrane depolarization and changes activity of different types of ion channels, depending on the type of photoreceptor cell [71,72]. Evidently, also in the plasma membrane of Stentor coeruleus, there can be observed functional, cGMP-activated channels [75,89,90], whose changed activity in photostimulated cells results, as in invertebrates, in a plasma membrane depolarization [18,19]. These channels are possibly composed of a protein of molecular weight 63 kDa found in the ciliate, which reveals immunoanalogy to the a-subunit of the cGMP-activated channel from the photoreceptor cells of vertebrates [90]. The identified channels in Stentor coeruleus exhibit similar properties to those observed in the photoreceptor cells of higher organisms [91–94]. Also the pattern of blocking the cGMP-activated channel conductance in Stentor coeruleus by l-cis-diltiazem, a well-known blocker of these types of channels, is similar to that observed in higher organisms [94–97]. Unsurprisingly, significant changes, both in occurrence and the pattern of the photophobic response, have been observed in Stentor coeruleus incubated with the above-mentioned agent. All the above indirect and direct data confirm an involvement of the cyclic nucleotide-activated channels in the process of light transduction in the ciliates [75,98]. 4.2. Photoreceptor and action potentials The consequence of the ion channels activity modulation by step increase in light intensity in Stentor coeruleus and Blepharisma japonicum, is the generation of a gradual, depolarizing photoreceptor potential, the amplitude of which increases with an increase in stimulus intensity up to certain maximal value [18,19,99]. These receptor potentials usually appear with some response delay to the onset of light stimulus applied. The stimulus of higher intensity elicits in the ciliates the photoreceptor potential of higher amplitude that in turn leads to the generation of a Ca2+-dependent action potential [16,18,19,100]. The induced action potential in both ciliates is associated with the ciliary reversal during photophobic response, whereas the receptor potential alone correlates with the photokinesis, i.e., acceleration of forward cell swimming. Cell stimulation by a prolonged

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light stimulus results in a long-lasting receptor potential in these microorganisms, its amplitude decreasing in time regardless continuous stimulation [18,19]. This event is probably linked to the process of cell adaptation to light. Similar photoadaptation is observed in vertebrates and invertebrates photoreceptor cells [1]. Due to these processes, organisms possessing a visual system have ensured an optimal vision within a wide range of light intensity in their environment. Photostimulation of these ciliates, preadapted to intensive illumination, leads to the release of photoreceptor potentials with lowered amplitude, so that no action potential and thus no photophobic response occur. Within the photosensitive ciliate already studied, membrane depolarization to a step-increase to low light intensity has been found only in the ciliate Paramecium bursaria. The light-induced membrane depolarization in this ciliate also triggers an action potential, accompanied by light-avoiding reaction. However, the cells of Paramecium bursaria when exposed to step-increase to light of high intensity exhibit membrane hyperpolarization, followed by an increase in swimming speed (photokinesis) [101]. 5. Function The ciliates Blepharisma japonicum and Stentor coeruleus have developed different strategies of motile response to light. A relatively large number of studies on these behaviours in both ciliates have so far been devoted to the photophobic response of cells to increased illumination in the medium. The results of these studies point to the presence of an endogenous enzymatic pathway for cGMP metabolism in Stentor coeruleus, and provide evidence for a G-protein-cGMP-mediated photosensory transduction pathway, resulting in cell photobehaviour (Fig. 1). This signalling mechanism seems to comprise a continuous production of intracellular cGMP by the cellular guanylate cyclase and transient degradation of the cGMP due to the increased activity of cyclic nucleotide-dependent PDE, resulting from photoexcitation of the stentorin-based photoreceptor system. The ensuing drop in the cyclic nucleotide content may lead to the closure of membrane cyclic nucleotide-activated channels that are open in darkness (as in molluscan extra-ocular photoreceptor cells [102–104]), and to the generation of a graded, depolarizing receptor potential. This receptor potential may in turn, trigger an action potential and inflow of Ca2+ into the cilia from the medium, as it takes place in other ciliates. This may initiate the ciliary reversal and simultaneous activation of the calmodulin-dependent GC in the ciliary membrane what results in an increase in the cGMP level and subsequent recovery of cilia from their reversed state [105,106]. As indicated by behavioural studies, a similar mechanism of light transduction is likely to exist in the related

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Light stimulus

6. Abbreviations

⇓

cAMP adenosine 3 0 ,5 0 -cyclic monophosphate cGMP guanosine 3 0 ,5 0 -cyclic monophosphate DAG diacylglycerol G-protein GTP-binding regulatory protein Gbc bc-subunit of G-proteins Ga a-subunit of G-proteins GC guanylate cyclase InsP3 inositol 1,4,5-trisphosphate InsP3R receptor protein for InsP3 PDE cyclic nucleotide phosphodiesterase PInsP2 phosphatidylinositol-4,5-biphosphate PLC phospholipase C TRP transient receptor potential

Stentorin excitation ↓ G-protein activation of PDE(s) (decrease in cellular cGMP) ↓ Inactivation of cGMP-dependent ion channels (generation of photoreceptor potential) ↓ 2+

Activation of ciliary Ca channels

Acknowledgements (generation of action potential) ↓ 2+

Increase in ciliary [Ca ]i⇒ Ciliary reversal

This study was supported by Grant 2P04C 014 27 from the Committee for Scientific Research and by statutory funding for the Nencki Institute of Experimental Biology in Warsaw (Poland).

(backward swimming)

References

↓ Activation of calmodulin-dependent ciliary GC ↓ Increase in ciliary cGMP ⇒ Recovery from ciliary reversal (forward swimming) Fig. 1. Schematic presentation of the physiological role of the possible cGMP-mediated light transduction pathway in the control of cell movement during photophobic response by Stentor coeruleus [75].

Blepharisma japonicum, where it leads to similar electrical changes at the plasma membrane and to the photophobic response. At the same time, some observations point to the contribution of phosphoinositide-dependent signalling to photomotility in this ciliate. A light-stimulated changes in the internal inositol trisphosphate level, possibly elicited by G-protein/phosducin-coupled PLC, may lead to changes in the activity of receptors for inositol trisphosphate, thus causing, via cGMP channels (as in ventral eye of Limulus [72]), the generation of photoreceptor potential followed by action potential correlated with the ciliary reversal. As indicated by the data presented in this article, our knowledge on photosensitivity in the unicellular organisms still remains limited. In order to clarify in more detail the process of photosignal transduction in these ciliates, further studies are required. These would allow us to recognize with utmost accuracy either the general principles, common for all organisms, as well as the differences, existing between highly specialized systems.

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