Skip to main content
SpringerLink
Log in

Immunohistochemical localization of a calcium pump and calbindin-D28k in the oviduct of the laying hen

  • Published:
Histochemistry Aims and scope Submit manuscript

Summary

The localization of a plasma membrane calcium pump in the oviduct of the laying hen was investigated by immunohistochemical techniques, utilizing a monoclonal antibody (5F10) produced against the human erythrocyte calcium pump. This antibody was shown to react with an epitope of the pump in oviductal tissue, and prominent staining was observed on the microvilli of the tubular gland cells of the hen shell gland (uterus) and the isthmus. The Ca2+ pump was not detectable in the infundibulum or the magnum. Calbindin-D28k, also localized by immunohistochemical means, was observed to be present in the tubular gland cells of the shell gland and the distal isthmus (adjacent to shell gland) but not in either the proximal isthmus (adjacent to the magnum), the magnum or the infundibulum. The localization of the Ca2+ pump in the oviduct corresponds to known sites of mineral deposition during egg shell formation. The distribution of calbindin-D28k differed, co-localizing with the Ca2+ pump in the shell gland and distal isthmus but not in the proximal isthmus. This might reflect a greater rate of active Ca2+ secretion in the distal isthmus and shell gland as compared to the proximal isthmus.

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

  • Bar A, Hurwitz S (1987) Vitamin D metabolism and calbindin (calcium-binding protein) in aged laying hens. J Nutr 117:1775–1779

    Google Scholar 

  • Bar A, Cohen A, Eisner U, Risenfeld J, Hurwitz S (1978) Differential response of calcium transport systems in laying hens to exogenous and endogenous changes in vitamin D status. J Nutr 108:1322–1328

    Google Scholar 

  • Borke JL, Caride A, Verma AK, Penniston JT, Kumar R (1989a) Plasma membrane calcium pump and 28-kDa calcium binding protein in cells of rat kidney distal tubules. Am J Physiol 257:F842-F849

    Google Scholar 

  • Borke JL, Caride AJ, Yaksh TL, Penniston JT, Kumar R (1989b) Cerebrospinal fluid calcium homeostasis: evidence for a plasma membrane Ca2+-pump in mammalian choroid plexus. Brain Research 489:355–360

    Google Scholar 

  • Borke JL, Caride A, Verma AK, Kelley LK, Smith CH, Penniston JT, Kumar R (1989c) Calcium pump epitopes in placental trophoblast basal plasma membranes. Am J Physiol 257:C341-C346

    Google Scholar 

  • Borke JL, Caride A, Verma AK, Penniston JP, Kumar R (1990) Cellular and segmental distribution of Ca2+-pump epitopes in rat intestine. Pflugers Arch 417:120–122

    Google Scholar 

  • Breen PC, DeBruyn PH (1969) Fine structure of the secretory cells of uterus (shell gland) of the chicken. J Morphol 128:35–65

    Google Scholar 

  • Bronner F, Pansu D, Stein WE (1986) An analysis of intestinal calcium transport across the rat intestine. Am J Physiol 250:G561-G569

    Google Scholar 

  • Burley RW, Vadehra DV (1989) The avian egg: chemistry and biology. John Wiley and Sons, New York, pp 472

    Google Scholar 

  • Chandra S, Fullmer CS, Smith CA, Wasserman RH, Morrison GH (1990) Ion microscopic imaging of calcium transport in the intestinal tissue of vitamin D-deficient and vitamin D-replete chickens: a 44Ca stable isotope study. Proc Natl Acad Sci USA 87:5715–5719

    Google Scholar 

  • Corradino RA, Wasserman RH, Pubols MH, Chang SI (1968) Vitamin D3 induction of a calcium-binding protein in the uterus of the laying hen. Arch Biochem Biophys 125:378–380

    Google Scholar 

  • Coty WA, McConkey CL Jr (1982) A high-affinity calcium-stimulated ATPase activity in the hen oviduct shell gland. Arch Biochem Biophys 219:444–453

    Google Scholar 

  • de Jaegere S, Wuytack F, Eggermont JA, Herboomen H, Casteels R (1990) Molecular cloning and sequencing of the plasma-membrane Ca2+ pump of pig smooth muscle. Biochem J 271:655–660

    Google Scholar 

  • Eastin WC Jr, Spaziani E (1978) On the control of calcium secretion in the avian shell gland (uterus). Biol Reprod 19:493–504

    Google Scholar 

  • Fullmer CS, Brindak ME, Bar A, Wasserman RH (1976) The purification of calcium-binding protein from the uterus of the laying hen. Proc Soc Exp Biol Med 152:237–241

    Google Scholar 

  • Gay CV, Schraer H (1971) Autoradiographic localization of calcium in the mucosal cells of the avian oviduct. Calcif Tissue Res 7:201–211

    Google Scholar 

  • Graf E, Verma AK, Gorski JP, Lopaschuk G, Niggli V, Zurini M, Carafoli E, Penniston JT (1982) Molecular properties of calcium pumping ATPase from human erythrocytes. Biochemistry 21:4511–4516

    Google Scholar 

  • Hurwitz S, Cohen I, Bar A (1970) The transmembrane electrical potential difference in the uterus (shell gland) of birds. Comp Biochem Physiol 35:873–878

    Google Scholar 

  • Jande SS, Tolnai S, Lawson DEM (1981) Immunohistochemical localization of vitamin D-dependent calcium-binding protein in duodenum, kidney, uterus and cerebellum of chickens. Histochemistry 71:99–116

    Google Scholar 

  • Johnston HS, Aitken RNC, Wyburn GM (1963) The fine structure of the uterus of the domestic fowl. J Anat 97:333–344

    Google Scholar 

  • Kelley LK, Borke JL, Verma AK, Kumar R, Penniston JT, Smith CH (1990) The calcium-transporting ATPase and the calcium or magnesium-dependent nucleotide phosphatase activities of human placental trophoblast basal plasma membrane are separate enzyme activites. J Biol Chem 265:5453–5459

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage R4. Nature 227:680–685

    Google Scholar 

  • Lippiello L, Wasserman RH (1975) Fluorescent antibody localization of the vitamin D-dependent calcium-binding protein in the oviduct of the laying hen. J Histochem Cytochem 23:111–116

    Google Scholar 

  • Lundholm CE (1982) Effect of p-p′-DDE administered in vivo and in vitro on Ca2+ binding and Ca2+ - Mg2+-ATPase activity in egg shell gland mucosa of ducks. Acta Pharmacol Toxicol 50:121–129

    Google Scholar 

  • Miller DS, Kinter WB, Peakall DB (1976) Enzymatic basis for DDE-induced eggshell thinning in a sensitive bird. Nature 259:122–124

    Google Scholar 

  • Nevalainen TJ (1969) Electron microscopc observations on the shell gland mucosa of calcium-deficient hens (Gallus domesticus). Anat Rec 164:127–140

    Google Scholar 

  • Niggli V, Penniston JT, Carafoli E (1979) Purification of the Ca2+ - Mg2+-ATPAse from human erythrocyte membranes using a calmodulin affinity column. J Biol Chem 254:9955–9958

    Google Scholar 

  • Nys Y, Parkes CO, Thomasset M (1986) Effects of suppression and resumption of shell formation and parathyroid hormone on uterine calcium-binding protein, carbonic anhydrase activity, and intestinal calcium absorption in hens. Gen Comp Endocrinol 64:293–299

    Google Scholar 

  • Pearson TW, Pryor TJ, Goldner AM (1977) Calcium transport across avian uterus. III. Comparison of laying and nonlaying birds. Am J Physiol 232:E437-E443

    Google Scholar 

  • Penniston JT (1983) Plasma membrane Ca2+-ATPases as active Ca2+ pumps. In: Cheung WY (ed) Calcium and cell function, vol 4. Academic Press, New York, pp 99–149

    Google Scholar 

  • Pike JW, Alvarado RH (1975) Ca2+-Mg2+-activated ATPase in the shell gland of Japanese quail (Coturnix coturnix japonica). Comp Biochem Physiol 51B:121–129

    Google Scholar 

  • Schraer R, Schraer H (1970) The avian shell gland: a study in calcium translocation. In: Schraer H (ed) Biological calcification: cellular and molecular aspects. Appleton-Century-Crofts, New York, pp 347–373

    Google Scholar 

  • Schraer H, Schraer R (1971) Calcium transfer across the avian shell gland. In: Nichols G Jr, Wasserman RH (eds) Cellular mechanisms for calcium transfer and homeostasis. Academic Press, New York, pp 351–369

    Google Scholar 

  • Simkiss K, Taylor TG (1971) Shell formation. In: Bell DJ, Freeman BM (eds) Physiology and biochemistry of the domestic fowl, vol 3. Academic Press, New York, pp 1331–1343

    Google Scholar 

  • Solomon SE, Fryer JR, Baird T (1975) The ultrastructural localization of calcium in the avian egg shell. J Microsc 105:215–222

    Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Google Scholar 

  • Wasserman RH, Fullmer CS (1983) Calcium transport proteins, calcium absorption and vitamin D. Annu Rev Physiol 45:375–390

    Google Scholar 

  • Wasserman RH, Fullmer CS (1989) On the molecular mechanism of intestinal calcium transport. Adv Exp Med Biol 249:45–65

    Google Scholar 

  • Wasserman RH, Taylor AN (1966) Vitamin D3-induced calcium-binding protein in chick intestinal mucosa. Science 142:791–793

    Google Scholar 

  • Watanabe E, Kobayashi S, Terashima Y, Itoh H (1989) Adenosine triphosphatase in the uterus and duodenum of chicken hens during eggshell formation. Poult Sci 68:564–568

    Google Scholar 

  • Wyburn GM, Johnston HS, Draper MH, Davidson MF (1973) The ultrastructure of the shell forming region of the oviduct and the development of the shell of Gallus domesticus. Q J Exp Physiol 58:143–151

    Google Scholar 

  • Yamamoto T, Ozawa H, Nagai H (1985) Histochemical studies of Ca-ATPase, succinate and NAD+-dependent isocitrate dehydrogenases in the shell gland of laying Japanese quails: with special reference to calcium-transporting cells. Histochemistry 83:221–226

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology, VRT717, New York State College of Veterinary Medicine, Cornell University, 14853, Ithaca, NY, USA

    R. H. Wasserman, M. E. Brindak & C. S. Fullmer

  2. Department of Pathology, New York State College of Veterinary Medicine, Cornell University, 14853, Ithaca, NY, USA

    C. A. Smith, C. M. Smith & L. Krook

  3. Department of Biochemistry and Molecular Biology, Mayo Clinic and Foundation, 55905, Rochester, MN, USA

    J. T. Penniston & R. Kumar

  4. Department of Medicine, Division of Nephrology, Mayo Clinic and Foundation, 55905, Rochester, MN, USA

    R. Kumar

Authors
  1. R. H. Wasserman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. A. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. M. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. E. Brindak
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. S. Fullmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. L. Krook
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. T. Penniston
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. R. Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wasserman, R.H., Smith, C.A., Smith, C.M. et al. Immunohistochemical localization of a calcium pump and calbindin-D28k in the oviduct of the laying hen. Histochemistry 96, 413–418 (1991). https://doi.org/10.1007/BF00315999

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00315999

Keywords

Search

Navigation