Ultrastructural diversity in chiropteran salivary glands

  • Bernard Tandler
  • Carleton J. Phillips
  • Toshikazu Nagato
  • Kuniaki Toyoshima
Part of the Electron Microscopy in Biology and Medicine book series (EMBM, volume 6)

Abstract

Mammalian salivary glands, which producea huge variety of glycoproteins and mucosubstances, as well as engaging in intense transportof electrolytes, have an obvious appeal for morphologists, physiologists, and biochemists. Despite the versatility of these organs, studies onsalivary glands have been restricted largely toa few commonly available laboratory animals.Comparative studies, though still relativelysparse, have shown that salivary gland histologyis generally similar throughout the class Mammalia, but that both the acinar and duct cellsexhibit considerable ultrastructural variationbetween species [1–3]. To illustrate this morphological variability, the present chapter surveysultrastructural aspects of the parotid, submandibular, and accessory submandibular salivaryglands in bats, order Chiroptera.

Keywords

Sucrose DMSO Sodium Chloride Hexagonal Adenosine 

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References

  1. 1.
    Young JA, van Lennep EW; The Morphology of Salivary Glands. New York: Academic Press, 1978.Google Scholar
  2. 2.
    Pinkstaff CA: The cytology of salivary glands. Int Rev Cytol 63: 141–261, 1980.PubMedCrossRefGoogle Scholar
  3. 3.
    Phillips CJ, Tandler B: Mammalian evolution at thecellular level. In: Current Mammalogy. HH Genoways(ed), New York: Plenum Press, 1–66, 1987.Google Scholar
  4. 4.
    Palade GE: Intracellular aspects of the process of proteinsecretion. Science 189; 347–358, 1975.PubMedCrossRefGoogle Scholar
  5. 5.
    Case RM: Synthesis, intracellular transport and dischargeof exportable proteins in the pancreatic acinar and other cells. Biol Rev 53: 211–354, 1978.PubMedCrossRefGoogle Scholar
  6. 6.
    Tartakoff AM: The Secretory and Endocytic Paths. Mechanism and Specificity of Vesicular Traffic in the Cell Cytoplasm. New York: John Wiley & Sons, 46–170,1987.Google Scholar
  7. 7.
    Hill JE, Smith JD: Bats — A Natural History. Austin, TX: Univ Texas Press, 1984.Google Scholar
  8. 8.
    Pettigrew JD: Flying primates? Megabats have the advanced pathway from eye to midbrain. Science 231: 1304–1306, 1986.PubMedCrossRefGoogle Scholar
  9. 9.
    Rouse GW,Robson SK:An ultrastructural study of megachiropteran (Mammalia: Chiroptera) spermatozoa: implications for chiropteran phylogeny.J. Submicrosc Cytol 18: 137–152, 1986.PubMedGoogle Scholar
  10. 10.
    Findley JS, Wilson DE: Ecological significance of chiropteran morphology. In: Ecology of Bats. TH Kunz(ed), New York: Plenum Press, 243–260, 1982.Google Scholar
  11. 11.
    Phillips CJ, Grimes GW, Forman GL: Oral Biology.In: Biology of Bats of the New World Family Phyllostomatidae. Part II. RJ Baker, JK Jr Jones, DC Carter(eds), Lubbock, TX: Texas Tech Univ Press 121–246,1977.Google Scholar
  12. 12.
    Phillips CJ, Studholme KM, Forman GL: Comparativeultrastructure of gastric mucosae in four genera of bats(Mammalia: Chiroptera), with comments on gastric evolution. Ann Carnegie Mus (Pittsburgh) 53: 71–117, 1984.Google Scholar
  13. 13.
    Studholme KM, Yazulla S, Phillips CJ: Interspecificcomparisons of immunohistochemical localization ofretinal neurotransmitters in four species of bats. Brain Behav Evol 30: 160–173, 1987.PubMedCrossRefGoogle Scholar
  14. 14.
    Fleming TH: Foraging strategies of plant-visiting bats.In; Ecology of Bats. TH Kunz (ed), New York: Plenum Press, 327–367, 1982.Google Scholar
  15. 15.
    Heithuas ER: Coevolution between bats and plants. In: Ecology of Bats. TH Kunz (ed), New York: PlenumPress, 327–367, 1982.Google Scholar
  16. 16.
    Tandler B, Nagato T, Phillips CJ: Systematic implicationsof comparative ultrastructure of secretory acini in thesubmandibular salivary gland of Artibeus (Chiroptera: Phyllostomidae). J Mammal 67: 81–90, 1986.CrossRefGoogle Scholar
  17. 17.
    Phillips CJ, Nagato T, Tandler B: Comparative ultrastructure and evolutionary patterns of acinar secretory product of parotid salivary glands in neotropical bats. In: Studies in Neotropical Mammalogy: essays in Honor of Philip Hershkovitz, BD Patterson, RM Timm (eds),Chicago: Field Mus Nat Hist. 213–229, 1987.Google Scholar
  18. 18.
    Phillips CJ, Tandler B, Pinkstaff CA: Unique salivary glands in two genera of tropical microchiropteran bats: An example of evolutionary convergence in histology andhistochemistry. J Mammal 68: 235–242, 1987.CrossRefGoogle Scholar
  19. 19.
    Nagato T, Tandler B, Phillips CJ: Unusual smoothendoplasmic reticulum in submandibular acinar cells ofthe male round-eared bat, Tonatiasylvicola. J Ultrastruct Res 87: 275–284, 1984.CrossRefGoogle Scholar
  20. 20.
    Kalt, MR, Tandler B: A study of fixation of early amphibian embryos for electron microscopy. J Ultrastruct Res 36: 633–645, 1971.PubMedCrossRefGoogle Scholar
  21. 21.
    Phillips CJ: Field fixation and storage of museum tissuecollections suitable for electron microscopy. Acta Zool Fenn 170: 87–90, 1985.Google Scholar
  22. 22.
    Tandler B, Walter, RJ: Epon-Maraglas embedment forelectron microscopy. Stain Technol 52: 238–239, 1977.PubMedGoogle Scholar
  23. 23.
    Tandler B, Phillips CJ, Nagato T: Evolutionary aspects ofthe ultrastructure of the parotid gland in an omnivorous neotropical bat, Carollia perspicillata.Zool Scripta 17: 419–427, 1988.CrossRefGoogle Scholar
  24. 24.
    Forman GL, Phillips CJ: Preparation and fixation of tissues for histological, immunohistochemical, and electron microscopic studies. In: Ecological and Behavioral Methods for the Study of Bats. TH Kunz (ed), Washington,DC: Smithsonian Inst Press, 405–424, 1988.Google Scholar
  25. 25.
    Tandler B: Salivary glands and the secretory process. In:A Textbook of Oral Biology. JH Shaw, EA Sweeney, CC Cappucino, SM Meiler (eds), Philadelphia: WB Saunders Company, 547–592, 1978.Google Scholar
  26. 26.
    Tandler B: Ultrastructure of the human submaxillary gland. I. Architecture and histological relationships of thesecretory cells. Am J Anat III: 287–307, 1962.CrossRefGoogle Scholar
  27. 27.
    Tandler B, Cohan RP: Ultrastructure of the parotid glandin the little brown bat. Anat Rec 210: 491–502, 1984.PubMedCrossRefGoogle Scholar
  28. 28.
    Van Lennep EW, Kennerson AR, Compton JS: The ultrastructure of the sheep parotid gland. Cell Tissue Res 179: 377–392, 1977.PubMedCrossRefGoogle Scholar
  29. 29.
    Tandler B, Riva A: Salivary glands. In: Human Oral Embryology and Histology. IA Mjör, O Fejerskov (eds),Copenhagen: Munksgaard International Publishers, 243–284, 1986.Google Scholar
  30. 30.
    Nakagaki I, Goto T, Sasaki S, Imai Y: Histochemical and cytochemical localization of (Na+-K+)-activated adenosine triphosphatase in the acini of dog submandibular glands. J Histochem Cytochem 26: 835–845, 1978.PubMedCrossRefGoogle Scholar
  31. 31.
    Bundgaard M, Moller M, Poulsen JH: Localization ofsodium pump sites in cat salivary glands. J Physiol 273:339–353, 1977.PubMedGoogle Scholar
  32. 32.
    Shackleford JM, Wilborn WH: Ultrastructure of bovineparotid glands. J Morphol 127: 453–474. 1969.PubMedCrossRefGoogle Scholar
  33. 33.
    Tandler B, Hoppel CL: Peroxisome-desmosome complexes in mouse hepatic cells. Z Zeilforsch 110: 166–172,1970.Google Scholar
  34. 34.
    Zaar K, Gorgas K: Peroxisome-endoplasmic reticulumaggregates in the duck uropygial gland. Eur J Cell Biol 38: 322–327, 1985.Google Scholar
  35. 35.
    Bennick A: Structural and genetic aspects of proline-richproteins. J Dent Res 66: 457–461, 1987.Google Scholar
  36. 36.
    Schulte BA: Genetic and sex-related differences in thestructure of submandibular glycoconjugates. J Dent Res 66: 442–450, 1987.PubMedCrossRefGoogle Scholar
  37. 37.
    Kousvelari EE, Fox PC, Baum BJ: Regulatory aspects ofN-linked glycoproteins. J Dent Res 66: 552–556, 1987.PubMedCrossRefGoogle Scholar
  38. 38.
    Levine MJ, Reddy MS, Tabak LA, Loomis RE, Bergey EJ, Jones PC, Cohen RE, Stinson MW, Al-Hashimi I: Structural aspects of salivary glycoproteins. J Dental Res66: 436–441, 1987.CrossRefGoogle Scholar
  39. 39.
    Mineda T: An electron microscopic study on the parotid gland of the Japanese horseshoe-bat (Rhinolophus ferrumequinum nippon) in the functional and hibernating period. Aichi-Gakuin J Dent Sci 16: 139–146, 1978.Google Scholar
  40. 40.
    Phillips CJ: Salivary glands: comparative ultrastructure of secretory cells. Proc Nassau County Med Cent 3: 162–167,1976.Google Scholar
  41. 41.
    Mineda T: An electron microscopic investigation onthe submandibular gland of the Japanese horseshoe-bat (Rhinolophus ferrumequinum nippon) — Histologicaland histochemical studies. Aichi-Gakuin J Dent Sci 15:35–47, 1977.Google Scholar
  42. 42.
    König B Jr, Kühnel W: Licht-und elektronenmikroskopische Untersuchunger an der Glandula parotis und der Glandula submandibularis der Hauskatze. Z Mikrosk-Anat Forsch 100: 469–483, 1986.PubMedGoogle Scholar
  43. 43.
    Tandler B, Phillips CJ: Unusual secretory granules in theaccessory submandibular gland of long-winged bats. Anat Rec 211: 192A, 1985.Google Scholar
  44. 44.
    Pinkstaff CA, Tandler B, Cohan RP: Histology and histochemistry of the parotid and principal and accessory submandibular glands of the little brown bat. J Morphol 172: 271–285, 1982.PubMedCrossRefGoogle Scholar
  45. 45.
    Harvey WR, Cioffi M, Wolfersberger MG: Portasomes ascoupling factors in active ion transport and oxidative phosphorylation. Am Zool 21: 775–791, 1981.Google Scholar
  46. 46.
    Kikuchi S: A unique cell membrane with a lining ofrepeating subunits on the cytoplasmic side of presumably ion-transporting cells in the gill epithelium of Daphnia magna (Crustacea: Cladocera). J SubmicroscCytol 14:711–715, 1982.Google Scholar
  47. 47.
    Hand AR: Synthesis of secretory and plasma membrane glycoproteins by striated duct cells of rat salivary glands asvisualized by radioautography after 3H-fucose injection. Anat Rec 195: 317–340, 1979.PubMedCrossRefGoogle Scholar
  48. 48.
    Schachter M, Wheeler GD, Matthews RW, Peret MW, Moriwaki C: Ultrastructural immunolocalization of kallikrein in apical granules of striated duct cells of cat submandibular gland. J Histochem Cytochem 31: 345–347, 1983.PubMedCrossRefGoogle Scholar
  49. 49.
    Schramm U, Flegler C, Ginsbach G: Zur Ultrastrukturder Glandulaparotis und der Glandula submandibularis der Schleichkatze Herpestes edwardsi (Viverridae). Anat Anz 146: 113–132, 1979.PubMedGoogle Scholar
  50. 50.
    Garrett JR: The proper role of nerves in salivary secretion: a review. J Dent Res 66: 387–397, 1987.PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1990

Authors and Affiliations

  • Bernard Tandler
    • 1
  • Carleton J. Phillips
  • Toshikazu Nagato
  • Kuniaki Toyoshima
  1. 1.School of DentistryCase Western Reserve UniversityClevelandUSA

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