Abstract
Like other cnidarians, the freshwater organism Hydra is characterized by the possession of cnidocytes (stinging cells). Most cnidocytes are located on hydra tentacles, where they are organized along with sensory cells and ganglion cells into battery complexes. The function of the battery complexes is to integrate multiple types of stimuli for the regulation of cnidocyte discharge. The molecular mechanisms controlling the discharge of cnidocytes are not yet fully understood, but it is known that discharge depends on extracellular Ca2+ and that mechanically induced cnidocyte discharge can be enhanced by the presence of prey extracts and other chemicals. Experiments in this paper show that a PKD2 (polycystin 2) transient receptor potential (TRP) channel is expressed in hydra tentacles and bases. PKD2 (TRPP) channels belong to the TRP channel superfamily and are non-selective Ca2+ channels involved in the transduction of both mechanical and chemical stimuli in other organisms. Non-specific PKD2 channel inhibitors Neo (neomycin) and Gd3+ (gadolinium) inhibit both prey capture and cnidocyte discharge in hydra. The PKD2 activator Trip (triptolide) enhances cnidocyte discharge in both starved and satiated hydra and reduces the inhibition of cnidocyte discharge caused by Neo. PKD1 and 2 proteins are known to act together to transduce mechanical and chemical stimuli; in situ hybridization experiments show that a PKD1 gene is expressed in hydra tentacles and bases, suggesting that polycystins play a direct or indirect role in cnidocyte discharge.
Similar content being viewed by others
References
Babich V, Zeng WZ, Yeh BI, Ibraghimov-Beskrovnaya O, Cai Y, Somo S et al (2004) The N-terminal extracellular domain is required for polycystin-1-dependent channel activity. J Biol Chem 279:25582–25589
Barr MM, Sternberg PW (1999) A polycystic kidney-disease gene homologue required for male mating behavior in C. elegans. Nature 401:386–389
Beckmann A (2013) Molecular factors of nematocyst morphogenesis and discharge in the freshwater polyp hydra. http://www.ub.uni-heidelberg.de/archiv/15956
Bellis SL, Laux DC, Rhoads DE (1994) Affinity purification of Hydra glutathione binding proteins. FEBS Lett 354:320–324
Besschetnova TY, Kolpakova-Hart E, Guan Y, Zhou J, Olsen BR, Shah JV (2010) Identification of signaling pathways regulating primary cilium length and flow-mediated adaptation. Curr Biol 20:182–187
Burnett AL, Davidson R, Wiernik P (1963) On the presence of a feeding hormone in the nematocyst of Hydra pirardi. Biol Bull 125(2):226–233
Chasnov JR, So WK, Chan CM, Chow KL (2007) The species, sex, and stage specificity of a Caenorhabditis sex pheromone. Proc Natl Acad Sci USA 104:6730–6735
Chen X-Z, Li Q, Wu Y, Liang G, Lara CJ, Cantiell HF (2008) Submembranous microtubule cytoskeleton: interaction of TRPP2 with the cell cytoskeleton. FEBS J 275:4675–4683
Field S, Riley K-L, Grimes DT, Hilton H, Simon M, Powles-Glover N, Siggers P, Bogani D, Greenfield A, Norris DP (2011) Pkd1l1 establishes left-right asymmetry and physically interacts with Pkd2. Development 138:1131–1142
Gale JE, Marcotti W, Kennedy HJ, Kros CJ, Richardson GP (2001) FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J Neurosci 21:7013–7025
Geng L, Okuhara D, Yu Z, Tian X, Cai Y, Shibazaki S, Somio S (2006) Polycystin-2 traffics to cilia indepently of polycystin-1 by using an N-terminal RVxP motif. J Cell Sci 119(Pt 7):1383–1395
Gitter AH, Oliver D, Thurm U (1993) Streptomycin inhibits nematocyte discharge in Hydra vulgaris by blockage of mechanosensitivity. Naturvissenschaften 80:273–276
Gitter AH, Oliver D, Thurm U (1994) Calcium- and voltage-dependence of nematocyst discharge in Hydra vulgaris. J Comp Physiol A 175:115–222
Grosvenor W, Kass-Simon G (1987) Feeding behavior in Hydra. I. Effects of Artemia homogenate on nematocyst discharge. Biol Bull 173:527–538
Grosvenor W, Rhoads DE, Kass-Simon G (1996) Chemoreceptive control of feeding processes in Hydra. Chem Senses 21:313–321
Gunaratne HJ, Moy GW, Kinukawa M, Miyata S, Mah SA, Bacquier FD (2007) The 10 sea urchin receptor for egg jelly proteins (SpREF) are members of the polycystic kidney disease-1 (PKD1) family. BMC Genom 8:235
Hamill OP, McBride DW (1996) The pharmacology of mechanogated membrane ion channels. Pharm Rev 48(2):231–252
Hanaoka K, Qian F, Boletta A, Bhunia AK, Piontek K, Tsiokas L, Sukhatme VP, Guggino WB, Germino GG (2000) Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature 408:990–994
Hansen GN, Cornelis MW, Grimmelikhuijzen JP (2000) Two-color double-labeling in situ hybridization of whole-mount Hydra using RNA probes for five different Hydra neurpeptide preprohormones: evidence for colocalization. Cell Tissue Res 301:245–253
Huang K, Diener DR, Mitchell A, Pazour GJ, Witman GB, Rosenbaum JL (2007) Function and dynamics of PKD2 in Chlamydomonas reinhardtii flagella. J Cell Biol 179:501–514
Ishimaru Y, Inada H, Kubota M, Zhuang H, Tominaga M, Matsunami H (2006) Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc Natl Acad Sci USA 103:12569–12574
Jeziorski MC, Greenberg RB, Clark KS, Anderson PAV (1998) Cloning and functional expression of a voltage-gated calcium channel α1 subunit from jellyfish. J Biol Chem 273(35):22792–22799
Jiang XH, Wong BC, Lin MC, Zhu GH, Kung HF, Jiang SH et al (2001) Functional p53 is required for triptolide-induced apoptosis and AP-1 and nuclear factor-kappaB activation in gastric cancer cells. Oncogene 20:8009–8018
Johnson BD, Hockerman GH, Scheuer T, Catterall WA (1996) Distinct effects of mutations in transmembrane segment IVS6 on block of L-type calcium channels by structurally similar phenylalkylamines. Mol Pharmocol 50(5):1388–1400
Kamura K, Kobayashi D, Uehara Y, Koshida S, Iijima N, Kudo A, Yokoyama T, Takeda H (2011) Pkd1l1 complexes with Pkd2 on motile cilia and functions to establish the left-right axis. Development 138:1121–1129
Kang L, Gao J, Schafer WR, Xie Z, Xu XZ (2010) C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel. Neuron 67(3):381–391
Kass-Simon G, Hufnagel LA (1992) Suspected chemoreceptors in coelenterates and ctenophores. Microsc Res Tech 22:265–284
Kass-Simon G, Scapaticci AA Jr (2002) The behavioral and developmental physiology of nematocysts. Can J Zool 80:1772–1794
Kim S, Nie H, Nesin V, Tran U, Outeda Pl, Bai C-X, Keeling J, Maskey D, Watnick T, Wessely O, Tsiokas L (2016) The polycystin coplex mediates Wnt/Ca2+ signaling. Nat Cell Biol 18(7):752–774
Kottgen M, Bucholz B, Garcia-Gonzalez MA, Kotsis F, Fu X, Doerken M, Boehlke C, Steffl D, Tauber R, Wegierski T et al (2008) TRPP2 and TRPV4 form a polymodal sensory channel complex. J Cell Biol 182(3):437–447
Kuehn EW, Hirt MN, John A-K, Muehlenhardt P, Boehlke C, Putz M, Kramer-Zucker AG, Bashkurov M, van de Weyer PS, Kotsis F et al (2007) Kidney injury molecule 1 (Kim1) is a novel ciliary molecule and interactor of polycystin 2. Biochem Biophys Res Commun 364:861–866
Lawonn P, Thurm U (1992) The chemical sensitivity of nematocytes of Hydra vulgaris. In: Elsner N, Richter D (eds) Rhythmogenese in Neuronen and Netzwerken, Proceedings of the 20th Gottingen neuerobiology conference. G. Thieme, Leipzig
Lenhoff HM, Bovaird J (1959) Requirement for bound Ca2+ for the action of surface chemoreceptors. Science 130:1474–1476
Leuenroth SJ, Okuhara D, Shotwell JD, Markowtiz GS, Yu Z, Somlo S, Crews CM (2007) Triptolide is a traditional Chinese medicine-derived inhibitor of polycystic kidney disease. Proc Natl Acad Sci 104(11):4389–4394
Li A, Tian X, Sung SW, Somlo S (2003) Identification of two novel polycystic kidney diseae-1-like genes in human and mouse genomes. Genomics 81(6):596–608
Loomis WF (1955) Glutathione control of the specific feeding reactions of hydra. Ann NY Acad Sci 62:211–227
Mahoney JL, Graugard EM, Mire P, Watson GM (2011) Evidence for involvement of TRPA1 in the detection of vibrations by hair bundle mechanoreceptors in sea anemones. J Comp Physiol 197:729–742
Martinez DE, Dirksen ML, Bode PM, Jamrich M, Steele RE, Bode HR (1997) Budhead, a fork head/NNF-3 homologue, is expressed during axis formation and head specification in hydra. Dev Biol 192(2):523–536
Mire-Thibodeaux P, Watson G (1994) Morphodynamic hair bundles arising fromsensory cell/supporting cell complexes frequency-tune nematocyst discharge in sea anemones. J Exp Zool 268:282–292
Murakami M, Ohba T, Xu F, Shida S, Satoh E, Ono K, Miyoshi I, Watanabe H, Ito H, Iijima T (2005) Genomic organization and functional analysis of murine PKD2L1. J Biol Chem 280(7):5626–5635
Nawrath H, Wegener JW (1997) Kinetics and state-dependent effects of verapamil on cardiac L-type calcium channels. Naunyn Schmiedebergs Arch Pharmacol 355(1):79–86
Newby LJ, Streets AJ, Zhao Y, Harris PC, Ward CJ, Ong ACM (2002) Identification, characterization and localization of a novel kidney polycystin-1-polycystin-2 complex. J Biol Chem 27(23):20763–20773
Nuali SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AEH, Lu W, Brown EM, Quinn SJ, Ingber D, Zhou J (2003) Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33:129–137
Ohta K, Hanai K, Morita H (1992) Glutathione-binding proteins identified by monoclonal antibodies which depress the behavioral response evoked by glutathione in Hydra. Biochim Biophys Acta 1117:136–142
Ozbek S, Balasubramaniam PG, Holstein TW (2009) Cnidocyst structure and the biomechanics of discharge. Toxicon 54:1038–1045
Peng G, Shi X, Kadowaki T (2014) Evolution of TRP channels inferred by their claissification in diverse animal species. Mol Phylogenet Evol 84:145–157
Plachetzki DC, Fong CR, Oakley TH (2012) Cnidocyte discharge is regulated by light and opsin-mediated phototransduction. BMC Biol 10:17
Retailleau K, Duprat F (2014) Polycystins and partners: proposed role in mechanosensitivity. J Physiol 592(Pt. 12):2453–2471
Scappaticci AA Jr, Kahn F, Kass-Simon G (2010) Nematocyst discharge in Hydra vulgaris: differential responses of desmonemes and stenoteles to mechanical and chemical stimulation. Comp Biochem Physiol 157:184–191
Schuler A, Schmitz G, Reft A, Ozbek S, Thurm U, Bornbgerg-Bauer E (2015) The rise and fall of TRP-N, an ancient family of mechanogated ion channels, in Metazoa. Genome Biol Evol 7(6):1713–1727
Semmo M, Kottgen M, Hofherr A (2014) The TRPP subfamily and polycystin-1 proteins. In: Nilius B, Flockerazi V (eds) Mammalian transient receptor potential (TRP) cation channels. Handbook of experimental pharmacology, vol 222. Springer, pp 675–711
Sharif-Naeini R, Folgering JHA, Bichet D, Duprat F, Lauritzen I, Arhatte M, Jodar M, Dedman A, Chatelain FC, Schulte U et al (2009) Polycystin-1 and -2 dosage regulates pressure sensing. Cell 139:587–596
Sidi S, Friedrich RW, Nicolson T (2003) NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96–99
So EC, Lo Y-C, Chen L-T, Kao C-A, Wu S-N (2014) High effectiveness of triptolide, an active diterpenoid triepoxide, in suppressing Kir-channel currents from human glioma cells. Mol Cell Pharmacol 738:332–341
Susankova K, Tousova K, Vyklicky L, Teisinger J, Vlachova V (2006) Reducing and oxidizing agents sensitize heat-activated vanilloid receptor (TRPV1) current. Mol Pharmacol 70:383–394
Thorington GU, Hessinger DA (1988) Control of discharge: factors affecting discharge of cnidae. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, San Diego, pp 233–254
Titov DV, Gilman B, He Q-L, Bhat S, Low W-K, Dang Y, Smeaton M, Demain AL, Miller PS, Kugel JF, Goodrich JA, Liu JO (2011) XPB, a subunit of TFIIH, is a target of the natural product triptolide. Nat Chem Biol 7:182–188
Tsiokas L, Arnould T, Zhu C, Kim E, Walz G, Sukhatme P (1999) Specific association of the gene product of PKD2 with the TRPC1 channel. Proc Natl Acad Sci USA 96(7):3934–3939
Van Den Wijngaard R, Welting O, Bulmer DC, Wouters MM, Lee K, De Jonge WJ, Boeckxstaens GE (2009) Possible role for TRPV1 in neomycin-induced inhibition of visceral hypersensitivity in rat. Neurogastroenterol Motil 21:863–870
Venkatachalm K, Montell C (2007) TRP channels. Ann Rev Biochem 76:387–417
Venturini G (1987) The hydra GSH receptor. Pharmacological and radioligand binding studies. Comp Biochem Physiol 87C:321–324
Walker RG, Willingham AT, Zucker CS (2000) A Drosophila mechanosensory transduction channel. Science 287:2229–2234
Watson GM, Hessinger DA (1989) Cnidocyte mechanoreceptors are tuned to the movements of swimming prey by chemoreceptors. Science 243:1589–1591
Watson GM, Hessinger DA (1991) Chemoreceptor-mediated elongation of stereocilium bundles tunes vibration-sensitive mechanoreceptors on cnidocyte-supporting cell complexes to lower frequences. J Cell Sci 99:307–316
Watson GM, Hessinger DA (1994) Evidence for calcium channels involved in regulating nematocyst discharge. Comp Biochem Physiol Part A Physiol 107(3):473–481
Westerheide SD, Kawahara TL, Orton K, Morimoto RI (2006) Triptolide, an inhibitor of the human heat shock response that enhances stress-induced cell death. J Biol Chem 281:9616–9622
Wilby OK (1976) Nematocyst discharge and the effects of antibiotics in feeding in hydra. Nature 262:387–388
Wu L-J, Sweet T-B, Clapham DE (2010) Current progress in the mammalian TRP ion channel family. Pharmacol Rev 62:381–404
Yuan S, Zhao L, Brueckner M, Sun Z (2015) Intraciliary calcium oscillations initiate vertebrate left–right asymmetry. Curr Biol 25:556–567
Yinjun L, Jie J, Yungui W (2005) Triptolide inhibits transcription factor NF-kappaB and induces apoptosis of multiple myeloma cells. Leuk Res 29:99–105
Acknowledgements
Hydra magnipapillata strain 105 was the kind gift of Dr. Robert Steele. Maria Villa, an undergraduate student in the lab, performed many of the cnidocyte capture assays. This work was supported by a National Science Foundation Grant (1243855) and a PSC-CUNY Grant (67524-00 45).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that she has no conflict of interest.
Rights and permissions
About this article
Cite this article
McLaughlin, S. Evidence that polycystins are involved in Hydra cnidocyte discharge. Invert Neurosci 17, 1 (2017). https://doi.org/10.1007/s10158-016-0194-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10158-016-0194-3