Skip to main content
SpringerLink
Log in

Gap junctions and intercellular communication in the hepatopancreas of the crayfish (Orconectes propinquus) during molt

A freeze-fracture — electrophysiological study

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The crustacean hepatopancreas is a major metabolic center intimately involved in molting and vitellogenesis. Cells of the hepatopancreas exhibit one of the richest endowments of gap junctions known and are thus presumed to be linked for intercellular communication. In order to monitor hepatopancreatic activity during the molt cycle of crayfish (Orconectes propinquus), the electrical coupling between cells of the hepatopancreatic tubules was measured during postmolt, intermolt and premolt. Samples of hepatopancreas from each of these stages were fixed and freeze-fractured to correlate morphologic features of gap junctions with electrophysiological data. Analysis of the data revealed that ionic coupling was greater in postmolt and premolt tubule cells than in cells of intermolt animals. Platinum replicas of hepatopancreatocyte plasmalemmata revealed that in postmolt, gap junction plaques were smaller and more numerous than those in intermolt and premolt; however, the total area of gap junction plaques per unit membrane area analyzed was approximately the same for hepatopancreatocytes from all molt stages. Although the hepatopancreatic gap junctions exhibited no quantitative differences, those from post- and premolt animals were rounded with “tightly” packed particles, while plaques from intermolt animals were generally pleomorphic with loosely packed particles. Results of this study suggest that cells of the crayfish hepatopancreas are more coupled in pre- and postmolt, with macular plaques of tightly packed particles, perhaps as a response to the increased metabolic demands of molt, and less well coupled, with irregular plaques of loosely packed junctional particles, during intermolt. The only recognizable morphological correlates of increased cell coupling were tight packing of junctional particles into rounded plaques, while decreased coupling corresponded to junctions with loosely packed irregular aggregates of particles.

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

Similar content being viewed by others

References

  • Adiyodi RG, Adiyodi KG (1972) Hepatopancreas of Paratelphusa hydrodromous (Herbst): Histophysiology and the pattern of proteins in relation to reproduction and molt. Biol Bull 142:359–369

    Google Scholar 

  • Azarnia R, Loewenstein WR (1977) Intercellular communication and tissue growth. VIII. A genetic analysis of junctional communication and cancerous growth. J Membr Biol 34:1–28

    Google Scholar 

  • Azarnia R, Larsen WJ, Loewenstein WR (1974) The membrane junctions in communicating and noncommunicating cells, their hybrids and segregants. Proc Natl Acad Sci USA 71:880–884

    Google Scholar 

  • Blanchet MF, Charniaux-Cotton H (1972) Control of the onset and duration of stage D of the intermolt cycle by ecdysterone in the amphipod Crustacean Orchestia gammarella (Pallas); interaction with vitellogenesis, CR Acad Aci Paris D 272:307–310

    Google Scholar 

  • Bliss DE, Boyer JR (1964) Environmental regulation of growth in the decapod crustacean Gecarcinus lateralis. Gen Comp Endocrinol 4:15–41

    Google Scholar 

  • Bunt AH (1968) An ultrastructural study of the hepatopancreas of Procambarus clarkii (Girard) (Decapoda, Astacidea). Crustaceana 15:282–288

    Google Scholar 

  • Burghardt RC, Matheson RL (1982) Gap junction amplification in rat ovarian granulosa cells. I. A direct response to follicle-stimulating hormone. Dev Biol 94:206–215

    Google Scholar 

  • Caveney S, Blennerhassett MG (1980) Elevation of ionic conductance between insect epidermal cells by β-ecdysone in vitro. J Insect Physiol 26:13–25

    Google Scholar 

  • Carroll AJ, Wood EM (1978) The influence of eyestalk hormones on the hepatopancreas in the striped shore crab. J Cell Biol 79:202A

    Google Scholar 

  • Chuang-Tseng MP, Chuang HH, Sandri C, Akert K (1982) Gap junctions and impulse propagation in embryonic epithelium of amphibia. Cell Tissue Res 225:249–258

    Google Scholar 

  • Davis LE, Burnett AL (1964) A study of growth and cell differentiation in the hepatopancreas of the crayfish. Dev Biol 10:122–153

    Google Scholar 

  • Decker RS (1976) Hormonal regulation of gap junction differentiation. J Cell Biol 69:669–685

    Google Scholar 

  • Fingerman M, Dominiczak T, Myawaki M, Oguro C, Tamomoto Y (1967) Neuroendocrine control of the hepatopancreas in the crayfish Procambarus clarki. Physiol Zool 40:23–30

    Google Scholar 

  • Flower NE (1972) A new junctional structure in the epithelia of insects of the order Dictyoptera. J Cell Sci 10:683–691

    Google Scholar 

  • Gilula NB (1972) Cell junctions of the crayfish hepatopancreas. J Ultrastruct Res 38:215–216

    Google Scholar 

  • Gilula NB (1973) Development of cell junctions. Am Zool 13:1109–1117

    Google Scholar 

  • Gilula NB, Reeves OR, Steinbach A (1972) Metabolic coupling, ionic coupling, and cell contacts. Nature 235:262–265

    Google Scholar 

  • Gorell TA, Gilbert LI (1969) Stimulation of protein and RNA synthesis in the crayfish hepatopancreas by crustecdysone. Gen Comp Endocrinol 13:308–310

    Google Scholar 

  • Gorell TA, Gilbert LI (1971) Protein and RNA synthesis in the premolt crayfish, Orconectes virilis. Z Vergl Physiol 73:345–356

    Google Scholar 

  • Gorell TA, Gilbert LI (1972) Studies on hormone recognition by arthropod target tissues. Am Zool 12:347–356

    Google Scholar 

  • Gorell TA, Gilbert LI, Siddall JB (1972) Binding proteins for an ecdysone metabolite in the Crustacean hepatopancreas. Proc Natl Acad Sci USA 69:812–815

    Google Scholar 

  • Graf F (1978) Diversité structurale des jonctions intercellulaires communicantes (gap junctions) de l'épithélium des caecums postérieurs du Crustacé Orchestia. CR Acad Sci Paris D 287:41–44

    Google Scholar 

  • Hubert M, Chassard-Bouchaud C (1977) Sur la présence de réticulum endoplasmique lisse dans l'hépatopancréas de Carcinus maenas L. (Crustacé Décapode): évolution en fonction du cycle d'intermue. CR Acad Sci Paris D 285:698–692

    Google Scholar 

  • Huner JV, Barr JE (1981) Red swamp crayfish: Biology and exploitation. Louisiana State University Center for Wetland Resources, Baton Rouge, La. pp 33–37

    Google Scholar 

  • Johnson G, Quick D, Johnson R, Herman W (1974) Influence of hormones on gap junctions in horseshoe crabs. J Cell Biol 63:157a

    Google Scholar 

  • Johnson R, Hammer M, Sheridan J, Revel J-P (1974) Gap junction formation between reaggregated Novikoff hepatoma cells. Proc Natl Acad Sci USA 71:4536–4540

    Google Scholar 

  • Josephson RK, Schwab WE (1979) Electrical properties of an excitable epithelium. J Gen Physiol 74:213–236

    Google Scholar 

  • Lane NJ (1978) Intercellular junctions and cell contacts in invertebrates. In: Sturgess JM (ed) Electron microscopy 1978, Proc 9th Int Congress on Electron Microscopy, 3, State of the Art. The Imperial Press, Toronto, pp 673–691

    Google Scholar 

  • Lane NJ, Swales LS (1978a) Changes in the blood-brain barrier of the central nervous system in the blowfly during development with special reference to the formation and disaggregation of gap and tight junctions. I. Larval development. Dev Biol 62:389–414

    Google Scholar 

  • Lane NJ, Swales LS (1978b) Changes in the blood-brain barrier of the central nervous system in the blowfly during development with special reference to the formation and disaggregation of gap and tight junctions. II. Pupal development and adult flies. Dev Biol 62:415–431

    Google Scholar 

  • Lane NJ, Swales LS (1980) Dispersal of junctional particles, not internalization, during the in vivo disappearance of gap junctions. Cell 19:579–588

    Google Scholar 

  • Loizzi RF (1971) Interpretation of crayfish hepatopancreatic function based on fine structural analysis of epithelial cell lines and muscle network. Z Zellforsch 113:420–440

    Google Scholar 

  • Loizzi RF, Peterson DR (1971) Lipolytic sites in crayfish hepatopancreas and correlation with fine structure. Comp Biochem Physiol 39B:227–236

    Google Scholar 

  • McWhinnie MA, Kirchenberg RJ (1962) Crayfish hepatopancreas metabolism and the intermolt cycle. Comp Biochem Physiol 6:117–128

    Google Scholar 

  • McWhinnie MA, Kirchenberg RJ, Urbanski RJ, Schwarz JE (1972) Crustecdysone-mediated changes in crayfish. Am Zool 12:357–372

    Google Scholar 

  • Meda P, Perrelet A, Orci L (1979) Increase of gap junctions between pancreatic β-cells during stimulation of insulin secretion J Cell Biol 82:441–448

    Google Scholar 

  • Meda P, Findlay I, Kolod E, Orci L, Petersen OH (1983) Short and reversible uncoupling evokes little change in the gap junctions of pancreatic acinar cells. J Ultrastruct Res 83:69–84

    Google Scholar 

  • Page E, Upshaw-Earley J (1980) Order and dispersal of rat heart gap junctional arrays. J Cell Biol 87:192A

    Google Scholar 

  • Peracchia C (1973) Low resistance junctions in crayfish. II. Structural details and further evidence for intercellular channels by freeze-fracture and negative staining. J Cell Biol 57:66–76

    Google Scholar 

  • Peracchia C (1977) Gap junctions. Structural changes after uncoupling procedures J Cell Biol 72:628–641

    Google Scholar 

  • Peracchia C, Dulhunty AF (1976) Low resistance junctions in crayfish. Structural changes with functional uncoupling. J Cell Biol 70:419–439

    Google Scholar 

  • Revel J-P (1978) Morphological and chemical organization of gap junctions. In: Sturgess JM (ed) Electron microscopy 1978, Proc 9th Int Congress on Electron Microscopy, 3, State of the Art. The Imperial Press, Toronto, p 651–658

    Google Scholar 

  • Richard P (1980) Le métabolisme amino-acidé de Palaemon serratus: variations des acides aminés libres du muscle et de l'hépatopancréas du cours du cycle de mue. Comp Biochem Physiol 67A:553–560

    Google Scholar 

  • Schultz TW (1976) The ultrastructure of the hepatopancreatic caeca of Gammarus minus (Crustacea, Amphipoda). J Morphol 149:383–400

    Google Scholar 

  • Shibata Y, Page E (1980) Ca2+-induced dispersal of gap junctional arrays. J Cell Biol 87:192a

    Google Scholar 

  • Shivers RR, Brightman MW (1976) Trans-glial channels of crayfish ventral nerve roots in freeze-fracture. J Comp Neurol 167:1–26

    Google Scholar 

  • Spindler K-D, Keller R, O'Connor JD (1980) The role of ecdysteriods in the Crustacean molting cycle. In: Hoffman JA (ed) Progress in ecdysone research, Elsevier/North Holland, Amsterdam pp 247–280

    Google Scholar 

  • Stanier JE, Woodhouse MA, Griffin RL (1968) The fine structure of the hepatopancreas of Carcinus maenas (L) (Decapoda, Brachyura). Crustaceana 14:55–66

    Google Scholar 

  • Stephens GC (1955) Induction of molting in the crayfish, Cambarus, by modification of daily photoperiod. Biol Bull 108:235–241

    Google Scholar 

  • Van Harreveld A (1936) A physiological solution for freshwater crustaceans. Proc Soc Exp Biol Med 34:428–432

    Google Scholar 

  • Vonk HJ (1960) Digestion and metabolism. In: Waterman TH (ed) The physiology of Crustacea. Vol 1, Academic Press, New York

    Google Scholar 

  • Williams EH, DeHann RL (1981) Electrical coupling among heart cells in the absence of ultrastructurally defined gap junctions. J Membr Biol 60:237–248

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cell Science Laboratories, Department of Zoology, University of Western Ontario, London, Ontario, Canada

    Lorne K. McVicar &  Richard R. Shivers

Authors
  1. Lorne K. McVicar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard R. Shivers
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by the Natural Sciences and Engineering Research Council of Canada (RRS)

Rights and permissions

Reprints and permissions

About this article

Cite this article

McVicar, L.K., Shivers, R.R. Gap junctions and intercellular communication in the hepatopancreas of the crayfish (Orconectes propinquus) during molt. Cell Tissue Res. 240, 261–269 (1985). https://doi.org/10.1007/BF00222333

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00222333

Key words

Search

Navigation