Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-23T03:27:58.409Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects on larval metamorphosis in the mussel Mytilus coruscus of compounds that act on downstream effectors of G-protein-coupled receptors

Published online by Cambridge University Press:  11 October 2016

Xiao Liang ,
Yu-Ru Chen ,
Wei Gao ,
Xing-Pan Guo ,
De-Wen Ding ,
Asami Yoshida ,
Kiyoshi Osatomi  and
Jin-Long Yang
Xiao Liang
Affiliation:
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China
Yu-Ru Chen
Affiliation:
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China
Wei Gao
Affiliation:
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China
Xing-Pan Guo
Affiliation:
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China
De-Wen Ding
Affiliation:
Marine Ecology Research Center, The First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China
Asami Yoshida
Affiliation:
Graduate School of Fisheries and Environmental Sciences, Nagasaki University, Nagasaki 852-8521, Japan
Kiyoshi Osatomi
Affiliation:
Graduate School of Fisheries and Environmental Sciences, Nagasaki University, Nagasaki 852-8521, Japan
Jin-Long Yang*
Affiliation:
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China Marine Ecology Research Center, The First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China
*
Correspondence should be addressed to: J.L. Yang, Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The metamorphic responses of mussel (Mytilus coruscus) larvae to pharmacological agents affecting G proteins and the adenylate cyclase/cyclic AMP (AC/cAMP) pathway were examined in the laboratory. The G protein activators guanosine 5′-[β,γ-imido]triphosphate trisodium salt hydrate and guanosine 5′-[γ-thio]triphosphate tetralithium salt only induced larval metamorphosis in continuous exposure assays, and the G protein inhibitor guanosine 5′-[β-thio]diphosphate trilithium salt did not exhibit inducing activity. The non-specific phosphodiesterase inhibitor theophylline and the cAMP-specific phosphodiesterase IV inhibitor 4-(3-Butoxy-4-methoxybenzyl)imidazolidin-2-one exhibited inducing activity, while the non-specific phosphodiesterase inhibitor 3-Isobutyl-1-methylxanthine only showed inducing activity at 10−4 M in continuous exposure assays. The cyclic nucleotide analogue N6,2′-O-Dibutyryladenosine 3′,5′-cyclic monophosphate sodium salt did not exhibit significant inducing activity. Both the adenylate cyclase activator forskolin and the adenylate cyclase inhibitor nitroimidazole exhibited inducing activity at 10−4 to 10−3 M concentrations in continuous exposure assays. Among these tested agents, the adenylate cyclase inhibitor (±)-miconazole nitrate salt showed the most promising inducing effect. The present results indicate that G protein-coupled receptors and signal transduction by AC/cAMP pathway could mediate metamorphosis of larvae in this species.

Keywords

Mytilus coruscuslarval metamorphosispharmacological compoundsG protein-coupled receptor
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 2 , March 2018 , pp. 333 - 339
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally.

References

REFERENCES

Alfaro, A.C., Young, T. and Ganesan, A.M. (2011) Regulatory effects of mussel (Aulacomya maoriana Iredale 1915) larval settlement by neuroactive compounds, amino acids and bacterial biofilms. Aquaculture 322–323, 158–168.Google Scholar
Amador-Cano, G., Carpizo-Ituarte, E. and Cristino-Jorge, D. (2006) Role of protein Kinase C, G-Protein coupled receptors, and calcium flux during metamorphosis of the sea urchin Strongylocentrotus purpuratus . Biological Bulletin 210, 121–131.CrossRefGoogle ScholarPubMed
Bao, W.Y., Yang, J.L., Satuito, C.G. and Kitamura, H. (2007) Larval metamorphosis of the mussel Mytilus galloprovincialis in response to Alteromonas sp. 1: evidence for two chemical cues? Marine Biology 152, 657–666.Google Scholar
Baxter, G. and Morse, D.E. (1987) G protein and diacylglycerol regulate metamorphosis of planktonic molluscan larvae. Proceedings of the National Academy of Sciences USA 84, 1867–1870.CrossRefGoogle ScholarPubMed
Biggers, W.J. and Laufer, H. (1999) Settlement and metamorphosis of Capitella larvae induced by juvenile hormone-active compounds is mediated by protein Kinase C and ion channels. Biological Bulletin 196, 187–198.Google Scholar
Cai, R.X., Chen, S.Q., Xue, J.Z. and Lu, J.P. (1994) The ecology of fouling organism in Gouqi waters, Zhoushan. Donghai Marine Science 12, 44–56. [In Chinese with English Abstract]Google Scholar
Chang, K.M., Liu, H.H., Li, J.L. and Shen, Y.B. (2008) A primary study on hybridization of Mytilus galloprovincialis, Mytilus coruscus, heterosis of F1 generation. Journal of Fisheries of China 32, 552–557. [in Chinese with English Abstract]Google Scholar
Clare, A.S. (2011) Toward a characterization of the chemical cue to barnacle gregariousness. In Breithaupt, T. and Thiel, M. (eds) Chemical communication in crustaceans. New York, NY: Springer, pp. 431–450.Google Scholar
Clare, A.S., Thomas, R.F. and Rittschof, D. (1995) Evidence for the involvement of cyclic AMP in the pheromonal modulation of barnacle settlement. Journal of Experimental Biology 198, 655–664.Google Scholar
Conzelmann, M., Williams, E.A., Tunaru, S., Randel, N., Shahidi, R., Asadulina, A., Berger, J., Offermanns, S. and Jékely, G. (2013) Conserved MIP receptor–ligand pair regulates Platynereis larval settlement. Proceedings of the National Academy of Sciences USA 110, 8224–8229.CrossRefGoogle ScholarPubMed
Coon, S.L. and Bonar, D.B. (1987) Pharmacological evidence that alphal-adrenoceptors mediate metamorphosis of the Pacific oyster, Crassostrea gigas . Neuroscience 23, 1169–1174.Google Scholar
Crisp, D.J. (1974) Factors influencing the settlement of marine invertebrate larvae. In Mackie, P.G. (ed.) Chemoreception in marine organisms. London: Academic Press, pp. 177–265.Google Scholar
Dobretsov, S.V. and Qian, P.Y. (2003) Pharmacological induction of larval settlement and metamorphosis in the blue mussel Mytilus edulis L . Biofouling 19, 57–63.CrossRefGoogle ScholarPubMed
Dreanno, C., Matsumura, K., Dohmae, N., Takio, K., Hirota, H., Kirby, R.R. and Clare, A.S. (2006) An α2-macroglobulin-like protein is the cue to gregarious settlement of the barnacle Balanus amphitrite . Proceedings of the National Academy of Sciences USA 103, 14396–14401.Google Scholar
Ganesan, A.M., Alfaro, A.C., Brooks, J.D. and Higgins, C.M. (2010) The role of bacterial biofilms and exudates on the settlement of mussel (Perna canaliculus) larvae. Aquaculture 306, 388–392.Google Scholar
Hadfield, M.G. (2011) Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Annual Review of Marine Science 3, 453–470.Google Scholar
Hadfield, M.G. and Paul, V.G. (2001) Natural chemical cues for settlement and metamorphosis of marine-invertebrate larvae. In McClintock, J.B. and Baker, J.B. (eds) Marine chemical ecology. Boca Raton, FL: CRC Press, pp. 431–460.Google Scholar
Hay, M.E. (2009) Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. Annual Review of Marine Science 1, 193–212.CrossRefGoogle ScholarPubMed
Holm, E.R., Nedved, B.T., Carpizo-Ituarte, E. and Hadfield, M.G. (1998) Metamorphic-signal transduction in Hydroides elegans (Polychaeta: Serpulidae) is not mediated by a G protein. Biological Bulletin 195, 21–29.Google Scholar
Huggett, M.J., de Nys, R., Williamson, J.E., Heasman, M. and Steinberg, P.D. (2005) Settlement of larval blacklip abalone, Haliotis rubra, in response to green and red macroalgae. Marine Biology 147, 1155–1163.Google Scholar
Jensen, R.A. and Morse, D.E. (1990) Chemically induced metamorphosis of polychaete larvae in both the laboratory and ocean environment. Journal of Chemical Ecology 16, 911–930.Google Scholar
Leitz, T. (1997) Induction of settlement and metamorphosis of Cnidarian larvae: signals and signal transduction. Invertebrate Reproduction and Development 31, 109–122.Google Scholar
Leitz, T. and Müller, W.A. (1987) Evidence for the involvement of PI-signaling and diacylglycerol second messengers in the initiation of metamorphosis in the hydroid Hydractinia echinata Fleming. Developmental Biology 121, 82–89.Google Scholar
Morse, D.E. (1990) Recent progress in larval settlement and metamorphosis: closing the gaps between molecular biology and ecology. Bulletin of Marine Science 46, 465–483.Google Scholar
Müller, W.A. (1985) Tumor-promoting phorbol esters induce metamorphosis and multiple head formation in the hydroid Hydractinia . Differentiation 29, 216–222.Google Scholar
Paul, V.J., Ritson-Williams, R. and Sharp, K. (2011) Marine chemical ecology in benthic environments. Natural Product Reports 28, 345–387.CrossRefGoogle ScholarPubMed
Pawlik, J.R. (1986) Chemical induction of larval settlement and metamorphosis in the reef-building tube worm Phragmatopoma californica (Sabellariidae: Polychaeta). Marine Biology 91, 59–68.Google Scholar
Pawlik, J.R. (1990) Natural and artificial induction of metamorphosis of Phragmatopoma lapidosa californica (Polychaeta: Sabellariidae), with a critical look at the effects of bioactive compounds on marine invertebrate larvae. Bulletin of Marine Science 46, 512–536.Google Scholar
Pawlik, J.R. (1992) Chemical ecology of the settlement benthic marine invertebrates. Oceanography and Marine Biology: An Annual Review 30, 273–335.Google Scholar
Rittschof, D., Maki, J., Mitchell, R. and Costlow, J.D. (1986) Ion and neuropharmacological studies of barnacle settlement. Netherlands Journal of Sea Research 20, 269–275.Google Scholar
Rittschof, D., Lai, C.H., Kok, L.M. and Teo, S.L.M. (2003) Pharmaceuticals as antifoulants: concept and principles. Biofouling 19, 207–212.Google Scholar
Sánchez-Lazo, C., Martínez-Pita, I., Young, T. and Alfaro, A.C. (2012) Induction of settlement in larvae of the mussel Mytilus galloprovincialis using neuroactive compounds. Aquaculture 344–349, 210–215.Google Scholar
Satuito, C.G., Natoyama, K., Yamazaki, M., Shimizu, K. and Fusetani, N. (1999) Induction of metamorphosis in the pediveliger larvae of the mussel Mytilus galloprovincialis by neuroactive compounds. Fisheries Science 65, 384–389.Google Scholar
Schneider, T. and Leitz, T. (1994) Protein kinase C in hydrozoans: involvement in metamorphosis of Hydractinia and in pattern formation of Hydra . Roux's Archives of Developmental Biology 203, 422–428.Google Scholar
Tebben, J., Tapiolas, D.M., Motti, C.A., Abrego, D., Negri, A.P., Blackall, L.L., Steinberg, P.D. and Harder, T. (2011) Induction of larval metamorphosis of the coral Acropora millepora by tetrabromopyrrole isolated from a Pseudoalteromonas bacterium. PLoS ONE 6, e19082. Available at http://dx.doi.org/10.1371/journal.pone.0019082.CrossRefGoogle ScholarPubMed
Tran, C. and Hadfield, M.G. (2012) Are G-protein-coupled receptors involved in mediating larval settlement and metamorphosis of coral planulae? Biological Bulletin 222, 128–136.Google Scholar
Walters, L.J., Hadfield, M.G. and Smith, C.M. (1996) Waterborne chemical compounds in tropical macroalgae: positive and negative cues for larval settlement. Marine Biology 126, 383–393.Google Scholar
Wang, C., Bao, W.Y., Gu, Z.Q., Li, Y.F., Liang, X., Ling, Y., Cai, S.L., Shen, H.D. and Yang, J.L. (2012) Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to natural biofilms. Biofouling 28, 249–256.Google Scholar
Yamamoto, H., Tachibana, A., Kawaii, S., Matsumura, K. and Fusetani, N. (1996) Serotonin involvement in larval settlement of the barnacle, Balanus amphitrite . Journal of Experimental Zoology 275, 339–345.Google Scholar
Yamamoto, H., Tachibana, A., Matsumura, K. and Fusetani, N. (1995) Protein kinase C (PKC) signal transduction system involved in larval metamorphosis of the barnacle, Balanus amphitrite . Zoological Science 12, 391–396.Google Scholar
Yang, J.L., Satuito, C.G., Bao, W.Y. and Kitamura, H. (2007) Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis on different macroalgae. Marine Biology 152, 1121–1132.Google Scholar
Yang, J.L., Satuito, C.G., Bao, W.Y. and Kitamura, H. (2008) Induction of metamorphosis of pediveliger larvae of the mussel Mytilus galloprovincialis Lamarck, 1819 using neuroactive compounds, KCl, NH4Cl and organic solvents. Biofouling 24, 461–470.CrossRefGoogle ScholarPubMed
Yang, J.L., Shen, P.J., Liang, X., Li, Y.F., Bao, W.Y. and Li, J.L. (2013a) Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to monospecific bacterial biofilms. Biofouling 29, 247–259.Google Scholar
Yang, J.L., Li, S.H., Li, Y.F., Liu, Z.W., Liang, X., Bao, W.Y. and Li, J.L. (2013b) Effects of neuroactive compounds, ions and organic solvents on larval metamorphosis of the mussel Mytilus coruscus . Aquaculture 396–399, 106–112.Google Scholar
Yang, J.L., Li, Y.F., Satuito, C.G., Bao, W.Y. and Kitamura, H. (2011) Larval metamorphosis of the mussel Mytilus galloprovincialis Lamarck, 1819 in response to neurotransmitter blockers and tetraethylammonium. Biofouling 27, 193–199.Google Scholar
Yang, J.L., Li, W.S., Liang, X., Li, Y.F., Chen, Y.R., Bao, W.Y. and Li, J.L. (2014) Effects of adrenoceptor compounds on larval metamorphosis of the mussel Mytilus coruscus . Aquaculture 426–427, 282–287.Google Scholar
Yang, J.L., Li, S.H., Bao, W.Y., Yamada, H. and Kitamura, H. (2015) Effect of different ions on larval metamorphosis of the mussel Mytilus galloprovincialis . Aquaculture Research 46, 155–162.Google Scholar
Young, T., Alfaro, A.C. and Robertson, J. (2011) Effect of neuroactive compounds on the settlement of mussel (Perna canaliculus). Aquaculture 319, 277–283.Google Scholar
Young, T., Alfaro, A.C., Sánchez-Lazo, C. and Robertson, J. (2015) Putative involvement of adrenergic receptors in regulation of mussel (Perna canaliculus) larval settlement. Marine Biology Research 11, 655–665.Google Scholar
Yvin, J.C., Chevolot, L., Chevolot-Magueur, A.M. and Cochard, J.C. (1985) First isolation of jacaraone from an alga, Delesseria sanguinea. A metamorphosis inducer of pectin larvae. Journal of Natural Products 48, 814–816.Google Scholar