Skip to main content
SpringerLink
Log in

Suppression of neuronal excitability by the secretion of the lamprey (Lampetra japonica) provides a mechanism for its evolutionary stability

  • Neuroscience
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

Lampreys are one of the most primitive vertebrates still living today. They attach themselves to the body surface of the host fish through their sucker-like mouths and suck blood of the host for days. Recent fossil evidence has indicated that morphology of lampreys in the late Devonian period, over 360 million years ago, already possessed the present day major characteristics, suggesting the evolutionary stability of a highly specialized parasitic feeding habit. Obviously, nociceptive responses and hemostasis of the host are two major barriers to long-term feeding of the parasitic lamprey. It has been found, to counteract hemostasis of the host, that paired buccal glands of lampreys secrete antihemostatic compounds to prevent blood of the host from coagulation. However, it is not known how lampreys make the host lose nociceptive responses. Here, we prepared components of the crude extract from the buccal glands of the lampreys (Lampetra japonica). Then, we show that crude extract and one of its purified components reduce the firing frequency of neuronal action potentials probably through inhibiting the voltage-dependent Na+ channels. As the voltage-gated Na+ channels are highly conserved throughout evolution, we argue that the secretion of the lampreys could exert the similar effect on the Na+ channels of their host fish as well. Therefore, together with its antihemostatic effect, the secretion due to its inhibitory effect on neuronal excitability might provide a mechanism for the parasitic lampreys to keep their evolutionary stability.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AP:

Action potential

BGSP-1:

Buccal gland secretion protein-1

CRISP:

Cysteine-rich secretory proteins

CRBGP:

Cysteine-rich buccal gland protein

DRG:

Dorsal root ganglion

L. japonica :

Lampetra japonica

SDS-PAGE:

Sodium dodecyl sulfate-polyacrylamide gel

TTX-R:

Tetrodotoxin-resistant

TTX-S:

Tetrodotoxin-sensitive

References

  1. Akopian AN, Sivilotti L, Wood JN (1996) A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379:257–262

    Article  PubMed  CAS  Google Scholar 

  2. Ashley PJ, Sneddon LU, McCrohan CR (2007) Nociception in fish: stimulus-response properties of receptors on the head of trout Oncorhynchus mykiss. Brain Res 1166:47–54

    Article  PubMed  CAS  Google Scholar 

  3. Baxter EW (1956) Observations on the buccal glands of lampreys (petromyzonidae). Proc Zool Soc Lond 127:95–118

    Google Scholar 

  4. Catterall WA, Goldin AL, Waxman SG (2005) Nomenclature and structure–function relationships of voltage-gated sodium channels. Pharmacol Rev 57:397–409

    Article  PubMed  CAS  Google Scholar 

  5. Chen X, Chi S, Liu M, Yang W, Wei T, Qi Z, Yang F (2005) Inhibitory effect of ganglioside GD1b on K+ current in hippocampal neurons and its involvement in apoptosis suppression. J Lipid Res 46:2580–2585

    Article  PubMed  CAS  Google Scholar 

  6. Chopra SS, Watanabe H, Zhong TP, Roden DM (2007) Molecular cloning and analysis of zebrafish voltage-gated sodium channel beta subunit genes: implications for the evolution of electrical signaling in vertebrates. BMC Evol Biol 7:113

    Article  PubMed  Google Scholar 

  7. Coste B, Crest M, Delmas P (2007) Pharmacological dissection and distribution of NaN/Nav1.9, T-type Ca2+ currents, and mechanically activated cation currents in different populations of DRG neurons. J Gen Physiol 129:57–77

    Article  PubMed  CAS  Google Scholar 

  8. Dan A, Pereira MH, Pesquero JL, Diotaiuti L, Beirao PS (1999) Action of the saliva of Triatoma infestans (Heteroptera: Reduviidae) on sodium channels. J Med Ent 36:875–879

    CAS  Google Scholar 

  9. DiGregorio DA, Peskoff A, Vergara JL (1999) Measurement of action potential-induced presynaptic calcium domains at a cultured neuromuscular junction. J Neurosci 19:7846–7859

    PubMed  CAS  Google Scholar 

  10. Dunlop R, Laming P (2005) Mechanoreceptive and nociceptive responses in the central nervous system of goldfish (Carassius auratus) and trout (Oncorhynchus mykiss). J Pain 6:561–568

    Article  PubMed  Google Scholar 

  11. Farmer GJ (1980) Biology and physiology of feeding in adult lampreys. Can J Fish Aquat Sci 37:1751–1761

    Article  Google Scholar 

  12. Forey P, Janvier P (1993) Agnathans and the origin of jawed vertebrates. Nature 361:129–134

    Article  Google Scholar 

  13. Gage SH, Gage MG (1927) The anticoagulant action of the secretion of the buccal glands of the lampreys (Petromyzon, Lampetra and Enlosphenun). Science 66:282

    Article  PubMed  Google Scholar 

  14. Gess RW, Coates MI, Rubidge BS (2006) A lamprey from the Devonian period of South Africa. Nature 443:981–984

    Article  PubMed  CAS  Google Scholar 

  15. Goldin AL (2002) Evolution of voltage-gated Na+ channels. J Exp Biol 205:575–584

    PubMed  CAS  Google Scholar 

  16. Guo M, Teng M, Niu L, Liu Q, Huang Q, Hao Q (2005) Crystal structure of the cysteine-rich secretory protein stecrisp reveals that the cysteine-rich domain has a K+ channel inhibitor-like fold. J Biol Chem 280:12405–12412

    Article  PubMed  CAS  Google Scholar 

  17. Heavner JE (2007) Local anesthetics. Curr Opin Anaesthesiol 20:336–342

    Article  PubMed  Google Scholar 

  18. Hille B (2001) Ion channel of excitable membranes. Sinauer, Sunderland, MA

    Google Scholar 

  19. Ito N, Mita M, Takahashi Y, Matsushima A, Watanabe YG, Hirano S, Odani S (2007) Novel cysteine-rich secretory protein in the buccal gland secretion of the parasitic lamprey, Lethenteron japonicum. Biochem Biophys Res Commun 358:35–40

    Article  PubMed  CAS  Google Scholar 

  20. Janvier P (2006) Palaeontology: modern look for ancient lamprey. Nature 443:921–924

    Article  PubMed  CAS  Google Scholar 

  21. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  22. Lennon RE (1954) Feeding mechanism of the sea lamprey and its effect on host fishes. Fish Bull US Dep Interior 98:247–293

    Google Scholar 

  23. Liu L, Yang T, Bruno MJ, Andersen OS, Simon SA (2004) Voltage-gated ion channels in nociceptors: modulation by cGMP. J Neurophysiol 92:2323–2332

    Article  PubMed  CAS  Google Scholar 

  24. Lopreato GF, Lu Y, Southwell A, Atkinson NS, Hillis DM, Wilcox TP, Zakon HH (2001) Evolution and divergence of sodium channel genes in vertebrates. Proc Natl Acad Sci USA 98:7588–7592

    Article  PubMed  CAS  Google Scholar 

  25. Melnick IV, Santos SF, Safronov BV (2004) Mechanism of spike frequency adaptation in substantia gelatinosa neurons of rat. J Physio 559:383–395

    Article  CAS  Google Scholar 

  26. Morrissette J, Krätzschmar J, Haendler B, El-Hayek R, Mochca-Morales J, Martin BM, Patel JR, Moss RL, Schleuning WD, Coronado R, Possani LD (1995) Primary structure and properties of helothermine, a peptide toxin that blocks ryanodine receptors. Biophys J 68:2280–2288

    Article  PubMed  CAS  Google Scholar 

  27. Novak AE, Jost MC, Lu Y, Taylor AD, Zakon HH, Ribera AB (2006) Gene duplications and evolution of vertebrate voltage-gated sodium channels. J Mol Evol 63:208–221

    Article  PubMed  CAS  Google Scholar 

  28. Olschewski A, Hempelmann G, Vogel W, Safronov BV (2001) Suppression of potassium conductance by droperidol has influence on excitability of spinal sensory neurons. Anesthesiology 94:280–289

    Article  PubMed  CAS  Google Scholar 

  29. Ribeiro JM, Francischetti IM (2003) Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu Rev Entomol 48:73–88

    Article  PubMed  CAS  Google Scholar 

  30. Rovainen CM (1996) Feeding and breathing in lampreys. Brain Behav Evol 48:297–305

    Article  PubMed  CAS  Google Scholar 

  31. Roy ML, Narahashi T (1992) Differential properties of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. J Neurosci 12:2104–2111

    PubMed  CAS  Google Scholar 

  32. Schreiber MC, Karlo JC, Kovalick GE (1997) A novel cDNA from Drosophila encoding a protein with similarity to mammalian cysteine-rich secretory proteins, wasp venom antigen 5, and plant group 1 pathogenesis-related proteins. Gene 191:135–141

    Article  PubMed  CAS  Google Scholar 

  33. Shikamoto Y, Suto K, Yamazaki Y, Morita T, Mizuno H (2005) Crystal structure of a CRISP family Ca2+-channel blocker derived from snake venom. J Mol Biol 350:735–743

    Article  PubMed  CAS  Google Scholar 

  34. Sneddon LU, Braithwaite VA, Gentle MJ (2003) Do fishes have nociceptors? Evidence for the evolution of a vertebrate sensory system. Proc Biol Sci 270:1115–1121

    Article  PubMed  Google Scholar 

  35. Spafford JD, Spencer AN, Gallin WJ (1999) Genomic organization of a voltage-gated Na+ channel in a hydrozoan jellyfish: insights into the evolution of voltage-gated Na+ channel genes. Receptors Channels 6:493–506

    PubMed  CAS  Google Scholar 

  36. Wang F, Li H, Liu MN, Song H, Han HM, Wang QL, Yin CC, Zhou YC, Qi Z, Shu YY, Lin ZJ, Jiang T (2006) Structural and functional analysis of natrin, a venom protein that targets various ion channels. Biochem Biophys Res Commun 351:443–448

    Article  PubMed  CAS  Google Scholar 

  37. Wang J, Shen B, Guo M, Lou X, Duan Y, Cheng XP, Teng M, Niu L, Liu Q, Huang Q, Hao Q (2005) Blocking effect and crystal structure of natrin toxin, a cysteine-rich secretory protein from Naja atra venom that targets the BKCa channel. Biochemistry 44:10145–10152

    Article  PubMed  CAS  Google Scholar 

  38. Xiao R, Li QW, Perrett S, He RQ (2007) Characterisation of the fibrinogenolytic properties of the buccal gland secretion from Lampetra japonica. Biochimie 89:383–392

    Article  PubMed  CAS  Google Scholar 

  39. Zimmermann K, Leffler A, Babes A, Cendan CM, Carr RW, Kobayashi J, Nau C, Wood JN, Reeh PW (2007) Sensory neuron sodium channel Nav1.8 is essential for pain at low temperatures. Nature 447:855–858

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Basic Research Program of China (2005CB522804, 2006CB911003, 2006CB500703).

Author information

Authors and Affiliations

  1. State Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, The Chinese Academy of Sciences, 15 Datun Rd, Beijing, 100101, China

    Shaopeng Chi, Rong Xiao, Rongqiao He & Zhi Qi

  2. School of Life Sciences, Liaoning Normal University, Dalian, 116029, China

    Qingwei Li & Liwei Zhou

  3. Graduate University of Chinese Academy of Sciences, 19A Yuquan Rd, Beijing, 100039, China

    Rong Xiao

Authors
  1. Shaopeng Chi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rong Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qingwei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Liwei Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rongqiao He
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhi Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Rongqiao He or Zhi Qi.

Additional information

Shaopeng Chi, Rong Xiao, and Qingwei Li contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chi, S., Xiao, R., Li, Q. et al. Suppression of neuronal excitability by the secretion of the lamprey (Lampetra japonica) provides a mechanism for its evolutionary stability. Pflugers Arch - Eur J Physiol 458, 537–545 (2009). https://doi.org/10.1007/s00424-008-0631-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-008-0631-1

Keywords

Search

Navigation