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Evidence that polycystins are involved in Hydra cnidocyte discharge

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Invertebrate Neuroscience

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.

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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

    Article  CAS  PubMed  Google Scholar 

  • Barr MM, Sternberg PW (1999) A polycystic kidney-disease gene homologue required for male mating behavior in C. elegans. Nature 401:386–389

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gitter AH, Oliver D, Thurm U (1993) Streptomycin inhibits nematocyte discharge in Hydra vulgaris by blockage of mechanosensitivity. Naturvissenschaften 80:273–276

    Article  CAS  Google Scholar 

  • Gitter AH, Oliver D, Thurm U (1994) Calcium- and voltage-dependence of nematocyst discharge in Hydra vulgaris. J Comp Physiol A 175:115–222

    Article  Google Scholar 

  • Grosvenor W, Kass-Simon G (1987) Feeding behavior in Hydra. I. Effects of Artemia homogenate on nematocyst discharge. Biol Bull 173:527–538

    Article  Google Scholar 

  • Grosvenor W, Rhoads DE, Kass-Simon G (1996) Chemoreceptive control of feeding processes in Hydra. Chem Senses 21:313–321

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hamill OP, McBride DW (1996) The pharmacology of mechanogated membrane ion channels. Pharm Rev 48(2):231–252

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kass-Simon G, Hufnagel LA (1992) Suspected chemoreceptors in coelenterates and ctenophores. Microsc Res Tech 22:265–284

    Article  CAS  PubMed  Google Scholar 

  • Kass-Simon G, Scapaticci AA Jr (2002) The behavioral and developmental physiology of nematocysts. Can J Zool 80:1772–1794

    Article  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Loomis WF (1955) Glutathione control of the specific feeding reactions of hydra. Ann NY Acad Sci 62:211–227

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ozbek S, Balasubramaniam PG, Holstein TW (2009) Cnidocyst structure and the biomechanics of discharge. Toxicon 54:1038–1045

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Plachetzki DC, Fong CR, Oakley TH (2012) Cnidocyte discharge is regulated by light and opsin-mediated phototransduction. BMC Biol 10:17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Retailleau K, Duprat F (2014) Polycystins and partners: proposed role in mechanosensitivity. J Physiol 592(Pt. 12):2453–2471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sidi S, Friedrich RW, Nicolson T (2003) NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96–99

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Venkatachalm K, Montell C (2007) TRP channels. Ann Rev Biochem 76:387–417

    Article  Google Scholar 

  • Venturini G (1987) The hydra GSH receptor. Pharmacological and radioligand binding studies. Comp Biochem Physiol 87C:321–324

    CAS  Google Scholar 

  • Walker RG, Willingham AT, Zucker CS (2000) A Drosophila mechanosensory transduction channel. Science 287:2229–2234

    Article  CAS  PubMed  Google Scholar 

  • Watson GM, Hessinger DA (1989) Cnidocyte mechanoreceptors are tuned to the movements of swimming prey by chemoreceptors. Science 243:1589–1591

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Watson GM, Hessinger DA (1994) Evidence for calcium channels involved in regulating nematocyst discharge. Comp Biochem Physiol Part A Physiol 107(3):473–481

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wilby OK (1976) Nematocyst discharge and the effects of antibiotics in feeding in hydra. Nature 262:387–388

    Article  CAS  PubMed  Google Scholar 

  • Wu L-J, Sweet T-B, Clapham DE (2010) Current progress in the mammalian TRP ion channel family. Pharmacol Rev 62:381–404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan S, Zhao L, Brueckner M, Sun Z (2015) Intraciliary calcium oscillations initiate vertebrate left–right asymmetry. Curr Biol 25:556–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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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).

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Correspondence to Susan McLaughlin.

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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

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