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• W2076869822 abstract "Although several second messengers are known to be involved in invertebrate photoresponses, the mechanism underlying invertebrate phototransduction remains unclear. In the present study, brief injection of inositol trisphosphate into Hermissendaphotoreceptors induced a transient Na+ current followed by burst activity, which accurately reproduced the native photoresponse. Injection of Ca2+ did not induce a significant change in the membrane potential but potentiated the native photoresponse. Injection of a Ca2+ chelator decreased the response amplitude and increased the response latency. Injection of cGMP induced a Ca2+-dependent, transient depolarization with a short latency. cAMP injection evoked Na+-dependent action potentials without a rise in membrane potential. Taken together, these results suggest that phototransduction in Hermissenda is mediated by Na+ channels that are directly activated by inositol trisphosphate without mobilization of cytosolic Ca2+. Although several second messengers are known to be involved in invertebrate photoresponses, the mechanism underlying invertebrate phototransduction remains unclear. In the present study, brief injection of inositol trisphosphate into Hermissendaphotoreceptors induced a transient Na+ current followed by burst activity, which accurately reproduced the native photoresponse. Injection of Ca2+ did not induce a significant change in the membrane potential but potentiated the native photoresponse. Injection of a Ca2+ chelator decreased the response amplitude and increased the response latency. Injection of cGMP induced a Ca2+-dependent, transient depolarization with a short latency. cAMP injection evoked Na+-dependent action potentials without a rise in membrane potential. Taken together, these results suggest that phototransduction in Hermissenda is mediated by Na+ channels that are directly activated by inositol trisphosphate without mobilization of cytosolic Ca2+. There is abundant evidence that the phosphoinositide cascade is involved in invertebrate phototransduction; however, the specific roles of inositol trisphosphate (IP3) 1The abbreviations used are: IP3inositol trisphosphatePIP2phosphatidylinositol 4,5-bisphosphatePLCphospholipase CBAPTAbis(0-aminophenoxy) ethane-N,N,N′,N′-tetraacetic acidASWartificial sea waterIBMXIsobutylmethylxanthineTTXtetrodotoxin.1The abbreviations used are: IP3inositol trisphosphatePIP2phosphatidylinositol 4,5-bisphosphatePLCphospholipase CBAPTAbis(0-aminophenoxy) ethane-N,N,N′,N′-tetraacetic acidASWartificial sea waterIBMXIsobutylmethylxanthineTTXtetrodotoxin. and/or Ca2+ in visual excitation have not yet been established (1Hardie R.C. Nature. 1993; 366: 113-114Crossref PubMed Scopus (8) Google Scholar, 2Nagy K. Q. Rev. Biophys. 1991; 24: 165-226Crossref PubMed Scopus (68) Google Scholar, 3Pak W.L. Shortridge R.D. Photochem. Photobiol. 1991; 53: 871-875Crossref Scopus (17) Google Scholar). The involvement of phosphatidylinositol 4,5-bisphosphate (PIP2) hydrolysis by phospholipase C (PLC) in the generation of IP3 in photoreceptors of Limulus (4Brown J.E. Rubin L.J. Ghalayni A.J. Tarver A.P. Irvine R.F. Berridge M.J. Anderson R.E. Nature. 1984; 311: 160-163Crossref PubMed Scopus (217) Google Scholar, 5Fein A. Payne R. Corson D.W. Berridge M.J. Irvine R.F. Nature. 1984; 311: 157-160Crossref PubMed Scopus (226) Google Scholar), squid (6Szuts E.T. Woods S.F. Reid M.S. Fein A. Biochem. J. 1986; 240: 929-932Crossref PubMed Scopus (49) Google Scholar, 7Brown J.E. Watkins D.C. Malbon C.C. Biochem. J. 1987; 247: 293-297Crossref PubMed Scopus (27) Google Scholar, 8Wood S.F. Szuts E.Z. Fein A. J. Biol. Chem. 1989; 264: 12970-12976Abstract Full Text PDF PubMed Google Scholar), Drosophila (9Yoshioka T. Inoue H. Hotta Y. Biochem. Biophys. Res. Commun. 1983; 111: 567-573Crossref PubMed Scopus (39) Google Scholar, 10Inoue H. Yoshioka T. Hotta Y. Biochem. Biophys. Res. Commun. 1985; 132: 513-519Crossref PubMed Scopus (58) Google Scholar, 11Bloomquist B.T. Shortridge R.D. Schneuwly S. Perdew M. Montell C. Steller H. Rubin G. Pak W.L. Cell. 1988; 54: 723-733Abstract Full Text PDF PubMed Scopus (513) Google Scholar, 12McKay R.R. Chen D.M. Miller K. Kim S. Stark W.S. Shortridge R.D. J. Biol. Chem. 1995; 270: 13271-13276Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar), andHermissenda (13Sakakibara M. Alkon D.L. Kouchi T. Inoue H. Yoshioka T. Biochem. Biophys. Res. Commun. 1994; 202: 299-306Crossref PubMed Scopus (27) Google Scholar) is supported by several lines of biochemical and biophysical evidence. In particular, the photoresponse in Drosophila was found to be absolutely dependent on PLC activity. Until recently, it was thought that IP3 is the second messenger involved in the photoresponse in invertebrates because a brief injection of IP3 mimicked the quantal response to light (4Brown J.E. Rubin L.J. Ghalayni A.J. Tarver A.P. Irvine R.F. Berridge M.J. Anderson R.E. Nature. 1984; 311: 160-163Crossref PubMed Scopus (217) Google Scholar, 5Fein A. Payne R. Corson D.W. Berridge M.J. Irvine R.F. Nature. 1984; 311: 157-160Crossref PubMed Scopus (226) Google Scholar) and IP3-induced Ca2+ release resulted in membrane depolarization in the Limulus ventral photoreceptor (14Frank T.M. Fein A. J. Gen. Physiol. 1991; 97: 697-723Crossref PubMed Scopus (81) Google Scholar) by activating Ca2+/Na+exchange (15Bolsover S.R. Brown J.E. J. Physiol. ( Lond. ). 1985; 364: 381-393Crossref PubMed Scopus (79) Google Scholar, 16O'Day P.M. Gray-Keller M.P. J. Gen. Physiol. 1989; 93: 473-492Crossref PubMed Scopus (57) Google Scholar). inositol trisphosphate phosphatidylinositol 4,5-bisphosphate phospholipase C bis(0-aminophenoxy) ethane-N,N,N′,N′-tetraacetic acid artificial sea water Isobutylmethylxanthine tetrodotoxin. inositol trisphosphate phosphatidylinositol 4,5-bisphosphate phospholipase C bis(0-aminophenoxy) ethane-N,N,N′,N′-tetraacetic acid artificial sea water Isobutylmethylxanthine tetrodotoxin. More recent evidence, however, indicates that the mechanism is more complex. For example, many contradictions arise if Ca2+/Na+ exchange is assumed to be the only mechanism involved in phototransduction: 1) the light response precedes the rise in Ca2+ (1Hardie R.C. Nature. 1993; 366: 113-114Crossref PubMed Scopus (8) Google Scholar), 2) excitation occurs in the absence of an IP3-induced increase in intracellular Ca2+ in Limulus (17Faddis M.N. Brown J.E. J. Gen. Physiol. 1993; 101: 909-931Crossref PubMed Scopus (34) Google Scholar), 3) abrupt Ca2+elevation using caged Ca2+ fails to activate any channels in Drosophila photoreceptor membrane (18Hardie R.C. J. Neurosci. 1995; 15: 889-902Crossref PubMed Google Scholar), and 4) theDrosophila mutant deficient in IP3 receptors still produces the native photoresponse (19Acharya J.K. Jalink K. Hardy R.W. Hartenstein V. Zucker C.S. Neuron. 1997; 18: 881-887Abstract Full Text Full Text PDF PubMed Scopus (200) Google Scholar). Furthermore, cGMP induces an inward current in photoreceptor cells in Limulus (20Johnson E.C. Robinson P.R. Lisman J.E. Nature. 1986; 324: 468-470Crossref PubMed Scopus (108) Google Scholar) andDrosophila (21Bacigalupo J. Bautista D.M. Brink D.L. Hetzer J.F. O'Day P.M. J. Neurosci. 1995; 15: 7196-7200Crossref PubMed Google Scholar) and activates channels directly in excised patches of molluscan microvilli membrane (1Hardie R.C. Nature. 1993; 366: 113-114Crossref PubMed Scopus (8) Google Scholar, 22Bacigalupo J. Johnson E.C. Vergara C. Lisman J.E. Proc. Natl. Acad. Sci. U. S. A. 1991; 88: 7938-7942Crossref PubMed Scopus (82) Google Scholar). It is still uncertain, however, whether intracellular cGMP concentration is altered by light (23Brown J.E. Kaupp U.B. Malbon C.C. J. Physiol. ( Lond. ). 1984; 353: 523-539Crossref PubMed Scopus (20) Google Scholar, 24Saibil H.R. FEBS Lett. 1984; 168: 213-216Crossref PubMed Scopus (34) Google Scholar, 25Brown J.E. Faddis M. Combs A. Exp. Eye Res. 1992; 54: 403-410Crossref PubMed Scopus (20) Google Scholar). Adding to the complexity of the system is the possibility of second messenger cross-talk between IP3, Ca2+, and cyclic nucleotides to activate intracellular chemical cascades (26Gomez M.P. Nasi E. Neuron. 1995; 15: 607-618Abstract Full Text PDF PubMed Scopus (58) Google Scholar). Hermissenda provide an ideal animal model in which to examine invertebrate visual transduction mechanisms. The photoreceptors are relatively large (50 μm in diameter) and are well characterized electrophysiologically (27Dennis M. J. Neurophysiol. 1967; 30: 1439-1465Crossref PubMed Scopus (49) Google Scholar, 28Alkon D.L. J. Gen. Physiol. 1973; 61: 444-461Crossref PubMed Scopus (44) Google Scholar, 29Alkon D.L. J. Gen Physiol. 1976; 67: 197-211Crossref PubMed Scopus (13) Google Scholar, 30Alkon D.L. Fuortes M.G.F. J. Gen. Physiol. 1972; 60: 631-649Crossref PubMed Scopus (89) Google Scholar, 31Alkon D.L. Grossman Y. J. Neurophysiol. 1978; 41: 1328-1342Crossref PubMed Scopus (29) Google Scholar, 32Detweiler P.B. J. Physiol. 1976; 256: 691-708Crossref PubMed Scopus (19) Google Scholar, 33Grossman Y. Schmidt J.A. Alkon D.L. Comp. Biochem. Physiol. 1981; 68A: 487-494Crossref Scopus (12) Google Scholar, 34Takeda T. Vision Res. 1982; 22: 303-309Crossref PubMed Scopus (7) Google Scholar, 35Etcheberrigaray R. Huddie P.L. Alkon D.L. J. Exp. Biol. 1991; 156: 619-623PubMed Google Scholar). They possess two types of photoreceptors: A and B (28Alkon D.L. J. Gen. Physiol. 1973; 61: 444-461Crossref PubMed Scopus (44) Google Scholar, 29Alkon D.L. J. Gen Physiol. 1976; 67: 197-211Crossref PubMed Scopus (13) Google Scholar). Photoreceptor B responds to a bright flash with a complex potential change involving an initial depolarization, a hyperpolarization, and a depolarizing tail, corresponding to a rapid and transient Na+ conductance increase, a slower increase in K+ permeability, and a delayed decrease in K+ permeability, respectively (32Detweiler P.B. J. Physiol. 1976; 256: 691-708Crossref PubMed Scopus (19) Google Scholar). The initial Na+ current appears to be the primary phototransduction event because 1) following light adaptation, light flashes produce only the hyperpolarization component (32Detweiler P.B. J. Physiol. 1976; 256: 691-708Crossref PubMed Scopus (19) Google Scholar) and 2) the hyperpolarization is Ca2+-dependent (33Grossman Y. Schmidt J.A. Alkon D.L. Comp. Biochem. Physiol. 1981; 68A: 487-494Crossref Scopus (12) Google Scholar) andHermissenda photoreceptors respond to single photons even in TTX containing, low Ca2+ high Mg2+ solution (34Takeda T. Vision Res. 1982; 22: 303-309Crossref PubMed Scopus (7) Google Scholar). Our previous work also indicates that the photoresponse may be generated through a TTX-resistant Na+ channel (36Alkon D.L. Sakakibara M. Biophys. J. 1985; 48: 983-995Abstract Full Text PDF PubMed Scopus (33) Google Scholar). The present study focuses on investigating the second messengers underlying the initial Na+ current component of the photoresponse. Recently, channels directly gated by IP3have been described in other cell lines (37Hatt H. Ache B.W. Proc. Natl. Acad. Sci. U. S. A. 1994; 91: 6264-6268Crossref PubMed Scopus (119) Google Scholar, 38Honda E. Teeter J.H. Restrepo D. Brain Res. 1995; 703: 79-85Crossref PubMed Scopus (19) Google Scholar), including Na+ channels in rat megakaryocytes (39Somasundaram B. Mahaut-Smith M.P. J. Biol. Chem. 1995; 270: 16638-16644Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar). This raises the possibility that the native photoresponse in Hermissenda is generated by an IP3-gated Na+ channel. To further characterize the role of IP3 and the possible role of cGMP, cAMP, and Ca2+ in invertebrate phototransduction, the effects of injection of these second messengers were examined electrophysiologically in Type B photoreceptors ofHermissenda. Hermissenda crassicornis obtained from the Sea Life Supply (Sand City, CA) were maintained in artificial sea water (ASW) at 14 °C. Type B photoreceptors were dissected in ASW (430 mm NaCl, 10 mm KCl, 50 mm MgCl2, 10 mm CaCl2, and 10 mm Tris-HCl, pH 7.4). Dissection and intracellular recording were performed as described previously (13Sakakibara M. Alkon D.L. Kouchi T. Inoue H. Yoshioka T. Biochem. Biophys. Res. Commun. 1994; 202: 299-306Crossref PubMed Scopus (27) Google Scholar). cGMP, cAMP, and IP3 (Sigma) were dissolved in intracellular solution (67 mm sodium acetate, 400 mm potassium gluconate, 10 mmMgCl2, 10 mm HEPES, 1.5 mmCaCl2, 1.5 mm EGTA, pH 7.4) at a concentration of 1 mm. Isobutylmethylxanthine (IBMX) was dissolved in Me2SO and diluted with intracellular solution to 1 mm. The intracellular solution alone or with Me2SO had no effect on the photoresponse. A microelectrode containing the drug was inserted into the photoreceptor cell, and the drug was injected using a pressure injector (Medical System, Greenvale, NY) at 30.0 p.s.i. for 200 ms. In some experiments the drug was iontophoresed into the photoreceptor for at least 3 min with DC current of 2.5 nA, after 10 min of dark adaptation. A photoresponse was elicited every 90 s during the entire experimental period to keep the adaptation level constant. Unattenuated light of 34.0 μW/cm2 at 550 nm delivered from a halogen lamp source was administered to the underside of the preparation. Isolated Hermissenda eyes were incubated in 10 μl of ASW containing 10 μCi of [3H]inositol (Amersham International) in darkness at 23 °C for 16 h. Then one eye of each pair was exposed to light for 30 s. The incubation was stopped by adding chloroform/methanol/12 n HCl (200:100:0.75), and PIP2 standard was added as a carrier and to aid in the identification of the lipids. Phospholipids were extracted and separated by thin layer chromatography as described previously (9Yoshioka T. Inoue H. Hotta Y. Biochem. Biophys. Res. Commun. 1983; 111: 567-573Crossref PubMed Scopus (39) Google Scholar). Lipids were visualized with I2 vapor, and appropriate bands were scraped and counted. PIP2-PLC activity was assayed using the particulate fraction obtained from theHermissenda circumesophageal nervous system as described previously (13Sakakibara M. Alkon D.L. Kouchi T. Inoue H. Yoshioka T. Biochem. Biophys. Res. Commun. 1994; 202: 299-306Crossref PubMed Scopus (27) Google Scholar). The IP3-evoked response was highly dependent on the distance between the injection site and the rhabdomeric membrane, the light-sensitive region (Fig.1 a). Immediately after IP3 was injected into a microvilli of the Type B photoreceptor close to the rhabdomeric membrane, a large transient response was observed (Fig. 1 a). No response was observed after injection approximately 10 μm away from the photosensitive region. The latency of the photoresponse decreased with increasing light intensity (Fig. 1 b). With low light intensity, the rate of rise and the peak amplitude of the photoresponse were low. With increased light intensity, a more complex response was observed, consisting of an initial depolarization, a hyperpolarization, and a depolarizing tail, consistent with previous reports (32Detweiler P.B. J. Physiol. 1976; 256: 691-708Crossref PubMed Scopus (19) Google Scholar). The first component was because of a rapid and transient Na+conductance increase, the hyperpolarization was because of a slow increase in K+ permeability, and the depolarizing tail was because of a slow decrease in K+ permeability (33Grossman Y. Schmidt J.A. Alkon D.L. Comp. Biochem. Physiol. 1981; 68A: 487-494Crossref Scopus (12) Google Scholar). The Na+ current was a graded response, consistent with previous observations in Hermissenda (36Alkon D.L. Sakakibara M. Biophys. J. 1985; 48: 983-995Abstract Full Text PDF PubMed Scopus (33) Google Scholar) and photoreceptors of other species (40Payne R. Fein A. J. Gen. Physiol. 1986; 87: 243-269Crossref PubMed Scopus (49) Google Scholar, 41Weckstrom M. Kouvalainen E. Jarvilehto M. Acta Physiol. Scand. 1988; 132: 103-113Crossref PubMed Scopus (13) Google Scholar). The spontaneous firing activity superimposed on the photoresponse is known to arise from the distal portion of the axon and is not involved in the visual transduction process (31Alkon D.L. Grossman Y. J. Neurophysiol. 1978; 41: 1328-1342Crossref PubMed Scopus (29) Google Scholar). Many characteristics of the response to IP3 injection were similar to the response to a relatively weak light flash, including the latency and the generation of action potentials (Fig. 1 c). Simultaneous light flash and IP3 injection were additive (Fig. 1 d). Furthermore, both responses were completely inhibited upon removal of extracellular Na+ (Fig.1 d). Similar to the native photoresponse, the IP3-evoked response was not dependent on the extracellular Ca2+ concentration (data not shown). Successive injection of IP3 resulted in a broadening and a decrease in the amplitude of the first peak and a higher frequency of spontaneous firing. This response mimicked the photoresponse to flickering light stimulation (Fig. 1 e). Flickering light stimulation elicited an increase in the Na+ conductance and a decrease in the hyperpolarization. To examine whether a transient increase in intracellular Ca2+activated the visual transduction channel, Ca2+ (1 mm) was injected into the photosensitive region of the Type B photoreceptor. In contrast to results obtained in Limulus (14Frank T.M. Fein A. J. Gen. Physiol. 1991; 97: 697-723Crossref PubMed Scopus (81) Google Scholar), injection of Ca2+ alone did not induce any significant response (Fig.2 a), but when a light flash was applied to the photoreceptor preinjected with Ca2+, the amplitude of the initial peak of the photoresponse and the hyperpolarization were potentiated (Fig. 2 b). This response was similar to the response to an intense light flash shown in Fig. lb. When BAPTA (a Ca2+ chelator; 1 mm) was injected intracellularly prior to a light flash, the latency of the photoresponse increased, and the amplitude decreased (Fig.2 c) and was eventually completely inhibited (data not shown). The decrease in the initial peak of the response may be because of a decline in PLC activity dependent on the levels of cytosolic Ca2+. Next we examined the involvement of PLC in the photoresponse by injecting PLC inhibitors such as aminoglycoside antibiotics and polyamines. Our previous data indicate that neomycin completely inhibits PLC activity in Hermissenda at concentrations higher than 0.1 mm and spermine inhibits PLC activity at concentrations higher than 0.5 mm (13Sakakibara M. Alkon D.L. Kouchi T. Inoue H. Yoshioka T. Biochem. Biophys. Res. Commun. 1994; 202: 299-306Crossref PubMed Scopus (27) Google Scholar). These suppressive effects are also carefully reconfirmed in this experiment (data not shown). Iontophoretic injection of 1 mm neomycin into Type B photoreceptors caused the response to light to be almost completely abolished 90 s after the injection without a change in the resting membrane potential (Fig. 3 a). The amplitude of the initial depolarization recovered gradually but incompletely. The amplitude of the depolarizing tail did not recover within 5 min after injection (data not shown) but recovered completely within 18 min. Gentamicin and higher concentrations of neomycin produced more prolonged inhibition of the photoresponse (data not shown). Injection of spermine (1 mm) produced a minor suppressive effect on the photoresponse without changing the resting membrane potential (Fig. 3 b). The amplitude of the initial depolarization was suppressed to 50% but recovered to 90% of the control response within 10 min after the injection (Fig.3 b). Injection of spermidine (1 mm), a weaker inhibitor of PLC, produced a smaller (less than 40%) inhibition of the photoresponse (data not shown). Inhibition of the hyperpolarization and the depolarizing tail of the photoresponse by spermine and spermidine is consistent with the fact that these compounds are Ca2+-activated K+ channel blockers (42Nomura K. Naruse K. Watanabe K. Sokabe M. J. Membr. Biol. 1990; 115: 241-251Crossref PubMed Scopus (41) Google Scholar). IBMX is a well characterized phosphodiesterase inhibitor and also a potent blocker of PIP2 synthesis (43Yoshioka T. Inoue H. Takagi M. Hayashi F. Amakawa T. Biochim. Biophys. Acta. 1983; 755: 50-55Crossref PubMed Scopus (15) Google Scholar). Iontophoretic injection of IBMX transiently suppressed the initial depolarization and the depolarizing tail and was completely reversible within 9 min (Fig.3 c). IBMX also reduced the light-induced Na+current in a similar manner (Fig. 3 d). These results resemble those obtained from the photoreceptor cells of octopus (43Yoshioka T. Inoue H. Takagi M. Hayashi F. Amakawa T. Biochim. Biophys. Acta. 1983; 755: 50-55Crossref PubMed Scopus (15) Google Scholar) and Limulus (23Brown J.E. Kaupp U.B. Malbon C.C. J. Physiol. ( Lond. ). 1984; 353: 523-539Crossref PubMed Scopus (20) Google Scholar). Other inhibitors of phosphoinositide metabolism, such as lithium and R59022, also decreased the initial depolarization (13Sakakibara M. Alkon D.L. Kouchi T. Inoue H. Yoshioka T. Biochem. Biophys. Res. Commun. 1994; 202: 299-306Crossref PubMed Scopus (27) Google Scholar). The order of potency of suppression of the initial depolarization is as follows: gentamicin > neomycin > LiCl > spermine > R59022 > spermidine. Although a significant change in the concentration of cyclic nucleotides in invertebrate photoreceptors during light irradiation has not been observed (25Brown J.E. Faddis M. Combs A. Exp. Eye Res. 1992; 54: 403-410Crossref PubMed Scopus (20) Google Scholar, 43Yoshioka T. Inoue H. Takagi M. Hayashi F. Amakawa T. Biochim. Biophys. Acta. 1983; 755: 50-55Crossref PubMed Scopus (15) Google Scholar), we tested the possibility that these cyclic nucleotides are involved in visual transduction (44Feng J.J. Frank T.M. Fein A. Brain Res. 1991; 552: 291-294Crossref PubMed Scopus (20) Google Scholar). Intracellular pressure injection of 1 mm cAMP generated a train of action potentials without a significant change in resting membrane potential (Fig. 4 a). Consistent bursts of action potentials were observed in response to successive injections of cAMP (Fig. 4 b). Successive bursts were not significantly different from the first burst, indicating that the effects of the injection were transient, unlike the effects of IP3, Ca2+, or BAPTA injection. The responses to cAMP injections were abolished in Na+-free ASW, similar to the response to IP3 injection (Fig. 4 b). The response to cAMP inHermissenda also differed from that in Limulus (44Feng J.J. Frank T.M. Fein A. Brain Res. 1991; 552: 291-294Crossref PubMed Scopus (20) Google Scholar), suggesting further that the phototransduction mechanism in Hermissenda is different from the ventral eye in Limulus. Injection of cGMP-induced transient depolarizing responses that were dependent on the distance between the photosensitive area and injection site (Fig. 5 a). Interestingly, only the amplitude of the response, not the latency, was dependent on this distance. In contrast to previous observations inLimulus (20Johnson E.C. Robinson P.R. Lisman J.E. Nature. 1986; 324: 468-470Crossref PubMed Scopus (108) Google Scholar) and Drosophila (21Bacigalupo J. Bautista D.M. Brink D.L. Hetzer J.F. O'Day P.M. J. Neurosci. 1995; 15: 7196-7200Crossref PubMed Google Scholar), the transient response to injection of cGMP occurred without any change in the resting potential. The time course of the cGMP-induced response was different from that of the native photoresponse; simultaneous stimulation with cGMP injection and light flash resulted in a double-peaked response (Fig. 5 b). We examined the effect of long term iontophoretic injection of cGMP on the photoresponse and found that the photoresponse observed after the injection of cGMP was dramatically reduced compared with the photoresponse before the injection. The initial depolarization was suppressed almost completely after a 3-min cGMP injection but then gradually recovered (Fig. 6 a). This response is consistent with responses recorded previously in light-adapted Type B photoreceptors (32Detweiler P.B. J. Physiol. 1976; 256: 691-708Crossref PubMed Scopus (19) Google Scholar). The effect of cGMP or phosphodiesterase inhibitors on the photoresponse has been reported to vary with the extracellular Ca2+concentration (45Johnson E.C. O'Day P.M. J. Neurosci. 1995; 15: 6586-6591Crossref PubMed Google Scholar). Consistent with previous reports (43Yoshioka T. Inoue H. Takagi M. Hayashi F. Amakawa T. Biochim. Biophys. Acta. 1983; 755: 50-55Crossref PubMed Scopus (15) Google Scholar), we also found that cumulative cGMP, by pretreatment with cGMP via iontophoretic injection, dramatically decreased the photoresponse of light-adapted photoreceptors maintained in normal ASW but enhanced the photoresponse of cells maintained in low Ca2+ ASW (1 mm; Fig.6 b). The inhibitory effect of cGMP recovered after returning to normal ASW (data not shown). The cGMP-induced response was found to be insensitive to changes in extracellular Na+concentration (Fig. 6 c), unlike native photoresponses (Fig.6 e). Moreover, the cGMP-induced response was abolished in Ca2+-free ASW (Fig. 6 d), unlike native photoresponses, which were independent of extracellular Ca2+ (Fig. 6 f). The results of the present study demonstrate for the first time that IP3 may mediate invertebrate visual transduction, particularly in Hermissenda. Although cAMP, cGMP, and Ca2+ have been proposed to activate several types of channels, injection of these second messenger candidates did not reproduce the native photoresponse. In contrast, injections of IP3 produced responses that were very similar to the native photoresponse, whereas Ca2+ acted as a modulator of the photoresponse (46Levy S. Fein A.J. J. Gen. Physiol. 1985; 85: 805-841Crossref PubMed Scopus (88) Google Scholar). The hypothesis that IP3 may be the second messenger involved in visual transduction in Hermissenda is supported by the results of the present study and by results obtained previously: 1) light flashes result in greater increases in intracellular IP3 than cyclic nucleotides (25Brown J.E. Faddis M. Combs A. Exp. Eye Res. 1992; 54: 403-410Crossref PubMed Scopus (20) Google Scholar) and 2) inhibition of PLC activity and reduction of phosphoinositide turnover result in a reduction in the amplitude of the native photoresponse (13Sakakibara M. Alkon D.L. Kouchi T. Inoue H. Yoshioka T. Biochem. Biophys. Res. Commun. 1994; 202: 299-306Crossref PubMed Scopus (27) Google Scholar). Although the primary role of IP3 has been considered to be the release of Ca2+ from intracellular stores, several IP3-gated ion channels have been recently characterized in olfactory cilia (37Hatt H. Ache B.W. Proc. Natl. Acad. Sci. U. S. A. 1994; 91: 6264-6268Crossref PubMed Scopus (119) Google Scholar, 38Honda E. Teeter J.H. Restrepo D. Brain Res. 1995; 703: 79-85Crossref PubMed Scopus (19) Google Scholar) and rat megakaryocytes (39Somasundaram B. Mahaut-Smith M.P. J. Biol. Chem. 1995; 270: 16638-16644Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar), raising the possibility that IP3 directly activates a transduction channel in Hermissenda. The possibility that IP3 may be a second messenger inDrosophila visual transduction is supported by observations by Inoue et al. (10Inoue H. Yoshioka T. Hotta Y. Biochem. Biophys. Res. Commun. 1985; 132: 513-519Crossref PubMed Scopus (58) Google Scholar) that a reduction of PIP2-PLC activity is closely correlated with electrophysiological abnormality in the Drosophilaphototransduction mutant norpA (no receptor potential A) eye. Furthermore, the norpA gene has been shown to encode PLC (11Bloomquist B.T. Shortridge R.D. Schneuwly S. Perdew M. Montell C. Steller H. Rubin G. Pak W.L. Cell. 1988; 54: 723-733Abstract Full Text PDF PubMed Scopus (513) Google Scholar, 47Toyoshima S. Matsumoto N. Wang P. Inoue H. Yoshioka T. Hotta Y. Osawa T. J. Biol. Chem. 1990; 265: 14842-14848Abstract Full Text PDF PubMed Google Scholar). Yoshioka et al. (43Yoshioka T. Inoue H. Takagi M. Hayashi F. Amakawa T. Biochim. Biophys. Acta. 1983; 755: 50-55Crossref PubMed Scopus (15) Google Scholar) have also reported previously that IBMX inhibits phosphoinositide turnover and that the photoresponse is dependent on PIP2 hydrolysis by PLC in squid photoreceptor. The photoresponse in Limulus has also been shown to be diminished by the injection of the PLC inhibitor neomycin without affecting the response to IP3 (14Frank T.M. Fein A. J. Gen. Physiol. 1991; 97: 697-723Crossref PubMed Scopus (81) Google Scholar) and by polyamine injection (17Faddis M.N. Brown J.E. J. Gen. Physiol. 1993; 101: 909-931Crossref PubMed Scopus (34) Google Scholar). Therefore, we propose that IP3produced from PIP2 hydrolysis via PLC activation is an essential component of invertebrate visual transduction. The question remains about whether IP3 acts directly or via Ca2+ in Hermissenda visual transduction. In the present study, injection of Ca2+ into the photoreceptor inHermissenda induced no response in darkness, suggesting that Ca2+ is not directly involved. Furthermore, excitation occurs even in the absence of an IP3-induced increase in intracellular Ca2+ in Limulus (17Faddis M.N. Brown J.E. J. Gen. Physiol. 1993; 101: 909-931Crossref PubMed Scopus (34) Google Scholar) and inDrosophila mutants lacking IP3 receptors in photoreceptor cells (19Acharya J.K. Jalink K. Hardy R.W. Hartenstein V. Zucker C.S. Neuron. 1997; 18: 881-887Abstract Full Text Full Text PDF PubMed Scopus (200) Google Scholar). It has also been reported that the photoresponse precedes the rise of intracellular Ca2+ inLimulus (48Steive H. Benner S. Vision Res. 1992; 32: 403-416Crossref PubMed Scopus (28) Google Scholar, 49Ukhanov K.Y. Flores T.M. Hsiao H.S. Mohapatra P. Pitts C.H. Payne R. J. Gen. Physiol. 1995; 105: 95-116Crossref PubMed Scopus (49) Google Scholar). Recently, Hardie (18Hardie R.C. J. Neurosci. 1995; 15: 889-902Crossref PubMed Google Scholar) reported that a transient elevation of Ca2+ using a caged Ca2+compound did not directly excite Drosophila photoreceptors. These results indicate that Ca2+ is unlikely to be directly involved in phototransduction in Drosophila,Hermissenda, and Limulus but may act as a modulator of the photoresponse. Several previous studies indicate that Ca2+ excites photoreceptors (50Payne R. Corson D.W. Fein A.J. J. Gen. Physiol. 1986; 88: 107-126Crossref PubMed Scopus (112) Google Scholar, 51Payne R. Corson D.W. Fein A.J. Berridge M.J. J. Gen Physiol. 1986; 88: 127-142Crossref PubMed Scopus (120) Google Scholar, 52Shin J. Richard E.A. Lisman J. Neuron. 1993; 11: 845-855Abstract Full Text PDF PubMed Scopus (62) Google Scholar) and that the injection of a Ca2+buffer reduced the photoresponse in Limulus (50Payne R. Corson D.W. Fein A.J. J. Gen. Physiol. 1986; 88: 107-126Crossref PubMed Scopus (112) Google Scholar). Also, in the present study, reduction of intracellular Ca2+ by a Ca2+ chelator resulted in a reduction of the photoresponse; however, the mechanism underlying this response is presently unclear. It may be because of reduced activation of PLC and a subsequent decrease in IP3; however, a decrease in protein kinase C activity cannot be ruled out. According to Thio and Sontheimer (53Thio C.L. Sontheimer H. J. Neurosci. 1993; 13: 4889-4897Crossref PubMed Google Scholar), phorbol esters reduced the peak of the TTX-sensitive Na+current by 25–60% and potentiated the TTX-resistant Na+current by 60–150%. In the present study, the Ca2+-induced increase in the photoresponse was 60–80% of control, which is consistent with the phorbol ester-induced increase in the TTX-resistant Na+ current. Involvement of cyclic nucleotides in visual transduction is also unlikely. The cAMP-evoked response was very different from the light-evoked response; injection of cAMP induced short bursts of Na+-dependent action potentials. Repeated injection evoked trains of similar bursts, indicating that these action potentials may be mediated by fast-inactivating cAMP-sensitive Na+ channels. Interestingly, cGMP-evoked responses were similar to light-evoked responses, but the following differences were observed: the amplitude of the cGMP-evoked responses depended on the distance from the rhabdomeric membrane, but the latency of the response was constant for all trials; the rising phase of the responses to cGMP was faster than that of responses to light; the cGMP-evoked response depended on external Ca2+, whereas the light-evoked response depended on external Na+; and the response induced by long term cGMP injection and the light-evoked response from light-adapted cells were very similar. Taken together, these findings indicate that neither cAMP nor cGMP act as second messengers in invertebrate visual transduction. Thus the results of the present study suggest that the transduction channels of Drosophila and Hermissenda eye may be IP3-gated Na+ channels. Cloning of IP3-gated Na+ channels may help clarify the mechanisms underlying invertebrate visual transduction." @default.
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• W2076869822 title "Evidence for the Involvement of Inositol Trisphosphate but Not Cyclic Nucleotides in Visual Transduction in HermissendaEye" @default.
• W2076869822 cites W1483885724 @default.
• W2076869822 cites W1602904527 @default.
• W2076869822 cites W163112216 @default.
• W2076869822 cites W1667251229 @default.
• W2076869822 cites W1727356853 @default.
• W2076869822 cites W184608556 @default.
• W2076869822 cites W1964723257 @default.
• W2076869822 cites W1971445812 @default.
• W2076869822 cites W1973961034 @default.
• W2076869822 cites W1974978517 @default.
• W2076869822 cites W1981140707 @default.
• W2076869822 cites W1983486478 @default.
• W2076869822 cites W1987150096 @default.
• W2076869822 cites W1987155732 @default.
• W2076869822 cites W1987718946 @default.
• W2076869822 cites W1993668198 @default.
• W2076869822 cites W2000754576 @default.
• W2076869822 cites W2005464410 @default.
• W2076869822 cites W2006103165 @default.
• W2076869822 cites W2009303641 @default.
• W2076869822 cites W2019920766 @default.
• W2076869822 cites W2026390924 @default.
• W2076869822 cites W2030157973 @default.
• W2076869822 cites W2034330001 @default.
• W2076869822 cites W2040718486 @default.
• W2076869822 cites W2048017515 @default.
• W2076869822 cites W2050811498 @default.
• W2076869822 cites W2053968420 @default.
• W2076869822 cites W2054297318 @default.
• W2076869822 cites W2060131144 @default.
• W2076869822 cites W2078910447 @default.
• W2076869822 cites W2083028636 @default.
• W2076869822 cites W2095064556 @default.
• W2076869822 cites W2107448183 @default.
• W2076869822 cites W2111629985 @default.
• W2076869822 cites W2114317808 @default.
• W2076869822 cites W2127325505 @default.
• W2076869822 cites W2127487700 @default.
• W2076869822 cites W2133687351 @default.
• W2076869822 cites W2136352989 @default.
• W2076869822 cites W2145204729 @default.
• W2076869822 cites W2145284767 @default.
• W2076869822 cites W2147914782 @default.
• W2076869822 cites W2149753834 @default.
• W2076869822 cites W2150691484 @default.
• W2076869822 cites W2151590637 @default.
• W2076869822 cites W2169564440 @default.
• W2076869822 cites W2272462970 @default.
• W2076869822 cites W2402078870 @default.
• W2076869822 cites W2409862333 @default.
• W2076869822 cites W35887203 @default.
• W2076869822 cites W88839315 @default.
• W2076869822 cites W1997347882 @default.
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