Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-30T16:15:13.009Z Has data issue: false hasContentIssue false
  • English
  • Français

High potassium seawater inhibits ascidian sperm chemotaxis, but does not affect the male gamete chemotaxis of a brown alga

Published online by Cambridge University Press:  18 July 2019

Nana Kinoshita-Terauchi ,
Kogiku Shiba ,
Makoto Terauchi ,
Francisco Romero ,
Héctor Vincente Ramírez-Gómez ,
Manabu Yoshida ,
Taizo Motomura ,
Hiroshi Kawai  and
Takuya Nishigaki Open the ORCID record for Takuya Nishigaki [Opens in a new window]
Nana Kinoshita-Terauchi
Affiliation:
Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan Shimoda Marine Research Center, University of Tsukuba, 5-10-1 Shimoda City, Shizuoka 415-0025, Japan
Kogiku Shiba
Affiliation:
Shimoda Marine Research Center, University of Tsukuba, 5-10-1 Shimoda City, Shizuoka 415-0025, Japan Misaki Marine Biological Station, Graduate School of Science, University of Tokyo, Miura, Kanagawa 238-0225, Japan
Makoto Terauchi
Affiliation:
Kobe University Research Center for Inland Seas, Rokkodai, Kobe 657-8501, Japan Center for Genome Informatics, Joint Support-Center for Data Science Research, Research Organization of Information and Systems, Mishima, Shizuoka 411-8540, Japan
Francisco Romero
Affiliation:
Institute of Biotechnology, National Autonomous University of Mexico (IBT-UNAM), Av. Universidad 2001, Col. Chamilpa, Cuernavaca, Mor. 62210, Mexico
Héctor Vincente Ramírez-Gómez
Affiliation:
Institute of Biotechnology, National Autonomous University of Mexico (IBT-UNAM), Av. Universidad 2001, Col. Chamilpa, Cuernavaca, Mor. 62210, Mexico
Manabu Yoshida
Affiliation:
Misaki Marine Biological Station, Graduate School of Science, University of Tokyo, Miura, Kanagawa 238-0225, Japan
Taizo Motomura
Affiliation:
Muroran Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Muroran 051-0013, Hokkaido, Japan
Hiroshi Kawai
Affiliation:
Kobe University Research Center for Inland Seas, Rokkodai, Kobe 657-8501, Japan
Takuya Nishigaki*
Affiliation:
Institute of Biotechnology, National Autonomous University of Mexico (IBT-UNAM), Av. Universidad 2001, Col. Chamilpa, Cuernavaca, Mor. 62210, Mexico
*
*Address for correspondence: Takuya Nishigaki. Institute of Biotechnology, National Autonomous University of Mexico (IBT-UNAM), Av. Universidad 2001, Col. Chamilpa, Cuernavaca, Mor. 62210, Mexico. Tel: +52 777 3291709. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Male gamete chemotaxis towards the female gamete is a general strategy to facilitate the sexual reproduction in many marine eukaryotes. Biochemical studies of chemoattractants for male gametes of brown algae have advanced in the 1970s and 1980s, but the molecular mechanism of male gamete responses to the attractants remains elusive. In sea urchin, a K+ channel called the tetraKCNG channel plays a fundamental role in sperm chemotaxis and inhibition of K+ efflux through this channel by high K+ seawater blocks almost all cell responses to the chemoattractant. This signalling mechanism could be conserved in marine invertebrates as tetraKCNG channels are conserved in the marine invertebrates that exhibit sperm chemotaxis. We confirmed that high K+ seawater also inhibited sperm chemotaxis in ascidian, Ciona intestinalis (robusta), in this study. Conversely, the male gamete chemotaxis towards the female gamete of a brown alga, Mutimo cylindricus, was preserved even in high K+ seawater. This result indicates that none of the K+ channels is essential for male gamete chemotaxis in the brown alga, suggesting that the signalling mechanism for chemotaxis in this brown alga is quite different from that of marine invertebrates. Correlated to this result, we revealed that the channels previously proposed as homologues of tetraKCNG in brown algae have a distinct domain composition from that of the tetraKCNG. Namely, one of them possesses two repeats of the six transmembrane segments (diKCNG) instead of four. The structural analysis suggests that diKCNG is a cyclic nucleotide-modulated and/or voltage-gated K+ channel.

Keywords

ChemotaxisCNGK channelHyperpolarizationMembrane potentialTetraKCNG channel
Type
Research Article
Information
Zygote , Volume 27 , Issue 4 , August 2019 , pp. 225 - 231
Copyright
© Cambridge University Press 2019 

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.)

References

Beltrán, C, Zapata, O and Darszon, A (1996) Membrane potential regulates sea urchin sperm adenylylcyclase. Biochemistry 35, 7591–7598.CrossRefGoogle ScholarPubMed
Böhmer, M, Van, Q, Weyand, I, Hagen, V, Beyermann, M, Matsumoto, M, Hoshi, M, Hildebrand, E and Kaupp, UB (2005) Ca2+ spikes in the flagellum control chemotactic behavior of sperm. EMBO J 24, 2741–2752.CrossRefGoogle Scholar
Bonigk, W, Loogen, A, Seifert, R, Kashikar, N, Klemm, C, Krause, E, Hagen, V, Kremmer, E, Strunker, T and Kaupp, UB (2009) An atypical CNG channel activated by a single cGMP molecule controls sperm chemotaxis. Sci Signal 2, ra68.CrossRefGoogle ScholarPubMed
Brams, M, Kusch, J, Spurny, R, Benndorf, K and Ulens, C (2014) Family of prokaryote cyclic nucleotide-modulated ion channels. Proc Natl Acad Sci USA 111, 7855–7860.CrossRefGoogle ScholarPubMed
Brelidze, TI, Carlson, AE and Zagotta, WN (2009) Absence of direct cyclic nucleotide modulation of mEAG1 and hERG1 channels revealed with fluorescence and electrophysiological methods. J Biol Chem 284, 27989–27997.CrossRefGoogle ScholarPubMed
Brelidze, TI, Carlson, AE, Sankaran, B and Zagotta, WN (2012) Structure of the carboxy-terminal region of a KCNH channel. Nature 481, 530–533.CrossRefGoogle ScholarPubMed
Cock, JM, Sterck, L, Rouzé, P, Scornet, D, Allen, AE, Amoutzias, G, Anthouard, V, Artiguenave, F, Aury, JM, Badger, JH, et al. (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465, 617–6121.CrossRefGoogle ScholarPubMed
Darszon, A, Nishigaki, T, Beltran, C and Trevino, CL (2011) Calcium channels in the development, maturation, and function of spermatozoa. Physiol Rev 91, 1305–1355.CrossRefGoogle ScholarPubMed
Espinal-Enríquez, J, Priego-Espinosa, DA, Darszon, A, Espinal-Enríquez, J, Priego-Espinosa, DA, Darszon, A, Beltrán, C and Martínez-Mekler, G (2017) Network model predicts that CatSper is the main Ca2+ channel in the regulation of sea urchin sperm motility. Sci Rep 7, 4236.CrossRefGoogle ScholarPubMed
Fechner, S, Alvarez, L, Bönigk, W, Müller, A, Berger, TK, Pascal, R, Trötschel, C, Poetsch, A, Stölting, G, Siegfried, KR, Kremmer, E, Seifert, R, and Kaupp, UB (2015) A K+-selective CNG channel orchestrates Ca2+ signalling in zebrafish sperm. eLife 4, 1–25.CrossRefGoogle Scholar
Froese, A, Breher, SS, Waldeyer, C, Schindler, RF, Nikolaev, VO, Rinné, S, Wischmeyer, E, Schlueter, J, Becher, J, Simrick, S, Vauti, F, Kuhtz, J, Meister, P, Kreissl, S, Torlopp, A, Liebig, SK, Laakmann, S, Müller, TD, Neumann, J, Stieber, J, Ludwig, A, Maier, SK, Decher, N, Arnold, HH, Kirchhof, P, Fabritz, L, and Brand, T (2012) Popeye domain containing proteins are essential for stress-mediated modulation of cardiac pacemaking in mice. J Clin Invest 122, 1119–1130.Google Scholar
Fu, G, Nagasato, C, Oka, S, Fu, G, Nagasato, C, Oka, S, Cock, JM and Motomura, T (2014) Proteomics analysis of heterogeneous flagella in brown algae (Stramenopiles). Protist 165, 662–675.CrossRefGoogle ScholarPubMed
Galindo, BE, de la Vega-Beltrán, JL, Labarca, P, Vacquier, VD and Darszon, A (2007) Sp-tetraKCNG: A novel cyclic nucleotide gated K+ channel. Biochem Biophys Res Commun 354, 668–675.CrossRefGoogle Scholar
Gauss, R, Seifert, R and Kaupp, UB (1998) Molecular identification of a hyperpolarization-activated channel in sea urchin sperm. Nature 393, 583–587.CrossRefGoogle ScholarPubMed
Geller, A and Müller, DG (1981) Anaysis of the flagellar beat pattern of male Ectocarpus siliculosus gametes (Phaeophyta) in relation to chemotactic stimulation by female cells. J Exp Biol 92, 53–66.CrossRefGoogle ScholarPubMed
González-Cota, AL, Silva, PÂ, Carneiro, J and Darszon, A (2015) Single cell imaging reveals that the motility regulator speract induces a flagellar alkalinization that precedes and is independent of Ca2+ influx in sea urchin spermatozoa. FEBS Lett 589, 2146–2154.Google Scholar
Gough, J, Karplus, K, Hughey, R and Chothia, C (2001) Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 313, 903–919.CrossRefGoogle Scholar
Haitin, Y, Carlson, AE and Zagotta, WN (2013) The structural mechanism of KCNH-channel regulation by the eag domain. Nature 501, 444–448.CrossRefGoogle ScholarPubMed
Harumi, T, Hoshino, K and Suzuki, N (1992) Effects of sperm-activating peptide I on Hemicentrotus pulcherrimus spermatozoa in high potassium sea water. Dev Growth Differ 34, 163–172.CrossRefGoogle ScholarPubMed
Heffernan, R, Dehzangi, A, Lyons, J, Paliwal, K, Sharma, A, Wang, J, Sattar, A, Zhou, Y and Yang, Y (2015a) Highly accurate sequence-based prediction of half-sphere exposures of amino acid residues in proteins. Bioinformatics 32, 843–849.CrossRefGoogle Scholar
Heffernan, R, Paliwal, K, Lyons, J, Dehzangi, A, Sharma, A, Wang, J, Sattar, A, Yang, Y and Zhou, Y (2015b) Improving prediction of secondary structure, local backbone angles, and solvent accessible surface area of proteins by iterative deep learning. Sci Rep 5, 1–11.CrossRefGoogle Scholar
Izumi, H, Marian, T, Inaba, K, Oka, Y and Morisawa, M (1999) Membrane hyperpolarization by sperm-activating and -attracting factor increases cAMP level and activates sperm motility in the ascidian Ciona intestinalis. Dev Biol 213, 246–256.CrossRefGoogle Scholar
Jiang, SZ, Xu, W, Emery, AC, Gerfen, CR, Eiden, MV and Eiden, LE (2017) NCS-Rapgef2, the protein product of the neuronal Rapgef2 gene, is a specific activator of D1 dopamine receptor-dependent ERK phosphorylation in mouse brain. eNeuro 4, 1–17.CrossRefGoogle ScholarPubMed
Kawai, H, Müller, DG, Fölster, E and Häder, DP (1990) Phototactic responses in the gametes of the brown alga, Ectocarpus siliculosus . Planta 182, 292–297.CrossRefGoogle ScholarPubMed
Kinoshita, N, Nagasato, C, Tanaka, A and Motomura, T (2016a) Chemotaxis in the anisogamous brown alga Mutimo cylindricus (Cutleriaceae, Tilopteridales). Phycologia 55, 359–364.CrossRefGoogle ScholarPubMed
Kinoshita, N, Shiba, K, Inaba, K, Fu, G, Nagasato, C and Motomura, T (2016b) Flagellar waveforms of gametes in the brown alga Ectocarpus siliculosus . Eur J Phycol 51, 139–148.CrossRefGoogle Scholar
Kinoshita, N, Nagasato, C and Motomura, T (2017a) Phototaxis and chemotaxis of brown algal swarmers. J Plant Res, 1–11.CrossRefGoogle Scholar
Kinoshita, N, Nagasato, C and Motomura, T (2017b) Chemotactic movement in sperm of the oogamous brown algae, Saccharina japonica and Fucus distichus . Protoplasma 254, 547–555.Google Scholar
Kirichok, Y, Navarro, B and Clapham, DE (2006) Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel. Nature 439, 737–740.CrossRefGoogle Scholar
Lipinska, AP, D’Hondt, S, Van Damme, EJM and De Clerck, O (2013) Uncovering the genetic basis for early isogamete differentiation: a case study of Ectocarpus siliculosus . BMC Genomics 14, 909.CrossRefGoogle ScholarPubMed
Lishko, PV, Botchkina, IL, Fedorenko, A and Kirichok, Y (2010) Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel. Cell 140, 327–337.CrossRefGoogle ScholarPubMed
Maier, I and Müller, DG (1986) Sexual pheromones in algae. Biol Bull 170, 145–175.CrossRefGoogle ScholarPubMed
Maler, I and Calenberg, M (1994) Movement and chemoorientation of male gametes of Ectocarpus siliculosus (Phaeophyceae). Plant Biol 107, 451–460.CrossRefGoogle Scholar
Meijering, E, Dzyubachyk, O and Smal, I (2012) Chapter 9 − Methods for cell and particle tracking. Imaging and Spectroscopic Analysis of Living Cells. Methods Enzymol 504, 183–200.Google Scholar
Miller, RL (1985) Sperm chemo-orientation in the metazoa. In: Biology of Fertilization V2. pp. 275–337.CrossRefGoogle Scholar
Müller, DG, Jaenicke, L, Donike, M and Akintobi, T (1971) Sex attractant in a brown alga: chemical structure. Science 171, 1132.Google Scholar
Nishigaki, T, Zamudio, FZ, Possani, LD and Darszon, A (2001) Time-resolved sperm responses to an egg peptide measured by stopped-flow fluorometry. Biochem Biophys Res Commun 284, 531–535.CrossRefGoogle Scholar
Nishigaki, T, Wood, CD, Tatsu, Y, Nishigaki, T, Wood, CD, Tatsu, Y, Yumoto, N, Furuta, T, Elias, D, Shiba, K, Baba, SA and Darszon, A (2004) A sea urchin egg jelly peptide induces a cGMP-mediated decrease in sperm intracellular Ca2+ before its increase. Dev Biol 272, 376–388.CrossRefGoogle Scholar
Nomura, M and Vacquier, VD (2006) Proteins associated with soluble adenylyl cyclase in sea urchin sperm flagella. Cell Motil Cytoskeleton 63, 582–590.CrossRefGoogle Scholar
Nomura, M, Beltrán, C, Darszon, A and Vacquier, VD (2005) A soluble adenylyl cyclase from sea urchin spermatozoa. Gene 353, 231–238.CrossRefGoogle ScholarPubMed
Nutting, WH, Rapoport, H and Machlis, L (1968) The structure of sirenin. J Am Chem Soc 90, 6434–6438.CrossRefGoogle ScholarPubMed
Oishi, T, Tsuchikawa, H, Murata, M, Oishi, T, Tsuchikawa, H, Murata, M, Yoshida, M and Morisawa, M (2003) Synthesis of endogenous sperm-activating and attracting factor isolated from ascidian Ciona intestinalis . Tetrahedron Lett 44, 6387–6389.CrossRefGoogle Scholar
Oishi, T, Tsuchikawa, H, Murata, M, Yoshida, M and Morisawa, M (2004) Synthesis and identification of an endogenous sperm activating and attracting factor isolated from eggs of the ascidian Ciona intestinalis. An example of nanomolar-level structure elucidation of novel natural compound. Tetrahedron 60, 6971–6980.CrossRefGoogle Scholar
Orta, G, Ferreira, G, José, O, Treviño, CL, Beltrán, C and Darszon, A (2012) Human spermatozoa possess a calcium-dependent chloride channel that may participate in the acrosomal reaction. J Physiol 590, 2659–2675.CrossRefGoogle Scholar
Provasoli, L (1968) Media and prospects for the cultivation of marine algae. In Culture and Collection of Algae US Japan Conference 1966, Hakone, eds. Watanabe A, Hattori A, pp. 63–75.CrossRefGoogle ScholarPubMed
Romero, F, Santana-Calvo, C and Sánchez-Guevara, Y, Nishigaki, T (2017) FRET-based binding assay between a fluorescent cAMP analogue and a cyclic nucleotide-binding domain tagged with a CFP. FEBS Lett 591, 2869–2878.Google Scholar
Seifert, R, Flick, M, Bönigk, W, Alvarez, L, Trötschel, C, Poetsch, A, Müller, A, Goodwin, N, Pelzer, P, Kashikar, ND, Kremmer, E, Jikeli, J, Timmermann, B, Kuhl, H, Fridman, D, Windler, F, Kaupp, UB, and Strünker, T (2015) The CatSper channel controls chemosensation in sea urchin sperm. EMBO J 34, 379–392.CrossRefGoogle Scholar
Shiba, K, Baba, SA, Inoue, T and Yoshida, M (2008) Ca2+ bursts occur around a local minimal concentration of attractant and trigger sperm chemotactic response. Proc Natl Acad Sci USA 105, 19312–193127.CrossRefGoogle ScholarPubMed
Strünker, T, Weyand, I, Bönigk, W, Van, Q, Loogen, A, Brown, JE, Kashikar, N, Hagen, V, Krause, E and Kaupp, UB (2006) A K+-selective cGMP-gated ion channel controls chemosensation of sperm. Nat Cell Biol 8, 1149–1154.CrossRefGoogle ScholarPubMed
Suzuki, N, Nomura, K, Ohtake, H and Isaka, S (1981) Purification and the primary structure of sperm-activity peptides from the jelly coat of sea urchin eggs. Biochem Biophys Res Commun 99, 1238–1244.CrossRefGoogle Scholar
Wang, D, King, SM, Quill, TA, Doolittle, LK and Garbers, DL (2003) A new sperm-specific Na+/H+ Exchanger required for sperm motility and fertility. Nat Cell Biol 5, 1117–1122.CrossRefGoogle ScholarPubMed
Wood, CD, Nisihigaki, T, Furuta, T, Baba, SA and Darszon, A (2005) Real-time analysis of the role of Ca2+ in flagellar movement and motility in single sea urchin sperm. J Cell Biol 169, 725–731.CrossRefGoogle ScholarPubMed
Yoshida, K, Shiba, K, Sakamoto, A, Ikenaga, J, Matsunaga, S, Inaba, K, and Yoshida, M (2018) Ca2+ efflux via plasma membrane Ca2+-ATPase mediates chemotaxis in ascidian sperm. Sci Rep 8, 16622.CrossRefGoogle Scholar
Yoshida, M and Yoshida, K (2011) Sperm chemotaxis and regulation of flagellar movement by Ca2 +. Mol Hum Reprod 17, 457–465.CrossRefGoogle ScholarPubMed
Yoshida, M, Inaba, K, Ishida, K and Morisawa, M (1994) Calcium and cyclic-amp mediate sperm activation, but Ca2+ alone contributes sperm chemotaxis in the ascidian, Ciona savignyi . Dev Growth Differ 36, 589–595.CrossRefGoogle ScholarPubMed
Yoshida, M, Murata, M, Inaba, K and Morisawa, M (2002) A chemoattractant for ascidian spermatozoa is a sulfated steroid. Proc Natl Acad Sci USA 99, 14831–14836.CrossRefGoogle Scholar
Supplementary material: PDF

Kinoshita-Terauchi et al. supplementary material

Figures S1-S5

Download Kinoshita-Terauchi et al. supplementary material(PDF)
PDF 2.7 MB