The Mammalian Harderian Gland: Ultrastructure, Sexual Dimorphism, and Its Regulation by Light and Steroids

  • Mathew J. Nadakavukaren

Abstract

One of the earliest ultrastructural studies of the Harderian gland was by Chiquoine (1958), in which he examined the myoepithelial cells of the Harderian glands in mice, rabbits, and rats. Since then, there have been a number of reports of Harderian gland ultrastructure from a variety of animals. However, it is clear from a survey of Harderian gland literature that two groups of animals, the rodents and the birds, have received the most attention. General ultrastructure of the Harderian gland has been described in the armadillo (Weaker 1981), fowl (Rothwell et al. 1972; Kittner et al. 1978; Niedorf and Wolters 1978; Maxwell and Burns 1979), frog (DiMatteo et al. 1989), gerbil (Sakai and Yohro 1981; Johnston et al. 1983), golden hamster (Bucana and Nadakavukaren 1972a, b, c, 1973), lizard (Chieffi Baccari et al. 1990), mouse (Woodhouse and Rhodin 1963; Watanabe 1980; Strum and Shear 1982a; Johnston et al. 1985, 1987), rabbit (Björkman et al. 1960; Kühnel 1971; Wooding 1980), rat (Kelényi and Orbán 1965; Tsutsumi et al. 1966; Feria-Velasco and Tapia-Arizmendi 1974; Browns-cheidle and Niewenhuis 1978), toad (Minucci et al. 1989), and turkey (Maxwell and Burns 1979; Maxwell et al. 1986). Although Harderian glands are known to be present in a number of other species (see review by Sakai 1981), ultrastructural studies of these are currently lacking.

Keywords

Propionate Testosterone Turkey Luminal Androgen 

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References

  1. Abe J (1979) Scanning electron microscopic observations of the mammary gland myoepithelial cells of the rat under normal and experimental conditions. Kurume Med J 26:303–310PubMedCrossRefGoogle Scholar
  2. Abe J, Nakamura K, Murakami M (1981a) Scanning electron microscopy observations of the myoepithelial cells in rat Harderian gland. J Electron Microsc 30:100 (Abstr)Google Scholar
  3. Abe J, Sugita A, Hamasaki M, Nakamura K, Iwanaga S, Nagae K, Atsuji K, Tsunawaki A, Abe T, Matsumoto T, Yo S, Murakami M (1981b) Scanning electron microscopic observations of the myoepithelial cells of normal and contracting status in the rat Harderian gland. Kurume Med J 28:103–112PubMedCrossRefGoogle Scholar
  4. Bjorkman N, Nicander L, Schantz B (1960) On the histology and ultrastructure of the Harderian gland in rabbit. Z Zellforsch 52:93–104CrossRefGoogle Scholar
  5. Brownscheidle CM, Niewenhuis RJ (1978) Ultrastructure of the Harderian gland in male albino rats. Anat Rec 190:735–753PubMedCrossRefGoogle Scholar
  6. Bucana CD, Nadakavukaren MJ (1972a) Fine structure of the hamster Harderian gland. Z Zellforsch 129:178–187PubMedCrossRefGoogle Scholar
  7. Bucana CD, Nadakavukaren MJ (1972b) Innervation of the hamster Harderian gland. Science 175:205–206PubMedCrossRefGoogle Scholar
  8. Bucana CD, Nadakavukaren MJ (1972c) Ultrastructural investigation of the postnatal development of the hamster Harderian gland. I. Cell division. Z Zellforsch 135:149–153PubMedCrossRefGoogle Scholar
  9. Bucana CD, Nadakavukaren MJ (1973) Ultrastructural investigation of the postnatal development of the hamster Harderian gland. II. Male and female. Z Zellforsch 142:1–12PubMedCrossRefGoogle Scholar
  10. Carriere R (1985) Ultrastructural visualization of intracellular porphyrin in the rat Harderian gland. Anat Rec 213:496–504PubMedCrossRefGoogle Scholar
  11. Chieffi Baccari G, Minucci S, DiMatteo L, Chieffi G (1990) Harderian gland and the lacrimal gland of the lizard Podarcis S sicula: histology, histochemistry and ultrastructure. Anat Rec 226:269–278CrossRefGoogle Scholar
  12. Chiquoine AD (1958) The identification and electron microscopy of myoepithelial cells in the Harderian gland. Anat Rec 132:569–583PubMedCrossRefGoogle Scholar
  13. Christensen F, Dam H (1953) A sexual dimorphism of the Harderian gland in hamsters. Acta Physiol Scand 27:333–336CrossRefGoogle Scholar
  14. Clabough JW, Norvell JE (1973) Effects of castration, blinding and the pineal gland on the Harderian glands of the male golden hamster. Neuroendocrinology 12:344–353PubMedCrossRefGoogle Scholar
  15. Cohn SA (1955) Histochemical observations on the Harderian gland of the albino mouse. J His-tochem Cytochem 3:342–353CrossRefGoogle Scholar
  16. DiIorio DP, Nadakavukaren MJ (1984) Prevention by pinealectomy of short-photoperiod-induced ultrastructural changes in the hamster Harderian gland. Anat Rec 210:449–452CrossRefGoogle Scholar
  17. DiMatteo L, Minucci S, Chieffi Baccari G, Pellicciari C, d’Istria M, Chieffi G (1989) The Harderian gland of the frog, Rana esculenta during the annual cycle: histology, histochemistry and ultrastructure. Bas Appl Histochem 33:93–112Google Scholar
  18. Feria-Velasco A, Tapia-Arizmendi G (1974) Further studies on the ultrastructure of Harderian gland in adult rats. Proc Elec Microsc Soc Am 32:288–289Google Scholar
  19. Feria-Velasco A, Tapia-Arizmendi G, Malpica I (1978) Effects of the environmental light conditions on the ultrastructure of the Harderian gland in the newborn rat: biochemical correlation with the pineal gland. Arch Invest Med (Mexico) 9:67–84Google Scholar
  20. Gustafson JA, Pousette A (1975) Demonstration and partial characterization of cytosol receptors for testosterone. Biochemistry 14:3094–3101CrossRefGoogle Scholar
  21. Hoffman RA (1971) Influences of some endocrine glands, hormones and blinding on the histology and porphyrins of the Harderian glands of golden hamsters. Am J Anat 132:463–478PubMedCrossRefGoogle Scholar
  22. Hoffman RA, Vaughan MK, Reiter RJ (1989) Photic input and pineal-Harderian-thyroid gland interactions in golden hamsters. In: Reiter RJ, Pang SF (eds) Advances in pineal research vol 3. John Libbey, London, pp 225–230Google Scholar
  23. Hoh JH, Lin WL, Nadakavukaren MJ (1984) Sexual dimorphism in the Harderian gland proteins of the golden hamster. Comp Biochem Physiol 77B:729–731Google Scholar
  24. Huhtala A, Huikuri KT, Palkama A, Tervo T (1977) Innervation of the rat Harderian gland by adrenergic and cholinergic nerve fibers. Anat Rec 188:263–271PubMedCrossRefGoogle Scholar
  25. Johnston HS, McGadey J, Thompson GG, Moore MR, Payne AP (1983) The Harderian gland, its secretory duct and porphyrin content in the Mongolian gerbil (Meriones unguiculatus). J Anat 137:615–630PubMedGoogle Scholar
  26. Johnston HS, McGadey J, Thompson GG, Moore MR, Breed WG, Payne AP (1985) The Harderian gland, its secretory duct and porphyrin content in the plains mouse (Pseudomys australis). J Anat 140:337–350PubMedGoogle Scholar
  27. Johnston HS, McGadey J, Payne AP, Thompson GG, Moore MR (1987) The Harderian gland, its secretory duct and porphyrin content in the wood mouse (Apodemus sylvaticus). J Anat 153:17–30PubMedGoogle Scholar
  28. Kelényi G, Orban S (1965) Electron microscopy of the Harderian gland of the rat: maturation of the acinar cells and genesis of the secretory droplets. Acta Morphol 13:155–165Google Scholar
  29. Kittner Z, Oláh I, Törö I (1978) Histology and ultrastructure of the Harderian glands — accessory lacrimal gland of the chicken. Acta Biol Acad Hung 29:29–41Google Scholar
  30. Kühnel W (1971) Über den Feinbau und die stoffwechsel-möglichkeiten der Harderschen Drüse des Kaninchens. Verh Anat Ges 66:79–85PubMedGoogle Scholar
  31. Lin WL (1981) An ultrastructural and biochemical investigation of sexual dimorphism in the hamster Harderian gland. PhD Diss, Illinois State University, Normal, IllGoogle Scholar
  32. Lin WL, Nadakavukaren MJ (1979) The androgenic effect on the fine structure of the Harderian gland in the male hamster. Cell Tissue Res 198:119–127PubMedCrossRefGoogle Scholar
  33. Lin WL, Nadakavukaren MJ (1981) Harderian gland lipids of male and female golden hamsters. Comp Biochem Physiol 70B:627–630Google Scholar
  34. Lin WL, Nadakavukaren MJ (1982) Delta-aminolevulinate synthase activity in the Harderian glands of male and female golden hamsters. Comp Biochem Physiol 71B:539–540Google Scholar
  35. Maxwell MH, Burns RB (1979) The ultrastructure of the epithelium of the ducts of the Harderian and lacrimal glands of the turkey, fowl and duck. J Anat 128:445–459PubMedGoogle Scholar
  36. Maxwell MH, Rothwell B, Burns RB (1986) A fine structural study of the turkey Harderian gland. J Anat 148:147–157PubMedGoogle Scholar
  37. McCafferty RE, Clark TS (1969) Harderian gland ultrastructure of mouse followed porphyrin administration. Anat Rec 163:315 (Abstr)Google Scholar
  38. McMasters KM, Hoffman RA (1984) Harderian gland: regulation of sexual “type” by gonads and pineal gland. Biol Reprod 31:579 – 585Google Scholar
  39. Menendez-Pelaez A, Howes KA, Gonzalez-Brito A, Reiter RJ (1987a) N-acetyltransferase activity, hydroxyindole-O-methyltransferase activity and melatonin levels in the Harderian gland of the female Syrian hamster: changes during the light:dark cycle and the effect of 6-parachlorophenylalanine administration. Biochem Biophys Res Commun 145:1231–1238PubMedCrossRefGoogle Scholar
  40. Menendez-Pelaez A, Howes KA, Reiter RJ (1987b) Ultrastructural changes in the secretory cells of the male Syrian hamster’s Harderian gland after prolonged gonadectomy. Anat Rec 218:90A (Abstr)Google Scholar
  41. Menendez-Pelaez A, Santana C, Howes KA, Sabry I, Reiter RJ (1988) Effects of photoperiod or exogenous melatonin administration on the activity of N-acetyltransferase and hydoxyindole-O-methyltransferase and the melatonin content of the Harderian gland of two strains of female Syrian hamsters. J Pineal Res 5:293–300PubMedCrossRefGoogle Scholar
  42. Menendez-Pelaez A, Buzzell GR, Gonzalez-Brito A, Reiter RJ (1990) Androgenic control of N-acetyltransferase activity in the Harderian glands of the female Syrian hamster is mediated by 5-alpha-dihydrotestosterone. J Cell Biochem 42:95–100PubMedCrossRefGoogle Scholar
  43. Minucci S, Chieffi Baccari G, DiMatteo L, Chieffi G (1989) A sexual dimorphism of the Harderian gland of the toad, Bufo viridis. Bas Appl Histochem 33:299–310Google Scholar
  44. Nadakavukaren MJ, Lin WL (1983) Influence of short photoperiods on the ultrastructure of hamster Harderian glands. Cell Tissue Res 233:209–213PubMedCrossRefGoogle Scholar
  45. Niedorf HR, Wolters B (1978) Development of the Harderian gland in the chicken: light and electron microscopic investigations. Invest Cell Pathol 1:205–215PubMedGoogle Scholar
  46. Olcese J, Wesche A (1989) The Harderian gland. Comp Biochem Physiol 93A:655–665CrossRefGoogle Scholar
  47. Payne AP, McGadey J, Moore MR, Thompson GG (1977) Androgenic control of the Harderian gland in the male golden hamster. J Endocrinol 75:73–82PubMedCrossRefGoogle Scholar
  48. Payne AP, McGadey J, Johnston HS, Moore MR, Thompson GG (1982) Mast cells in the hamster Harderian gland: sex differences, hormonal control and relationship to porphyrin. J Anat 135:451–461PubMedGoogle Scholar
  49. Rothwell B, Wight PAL, Burns RB, MacKenzie GM (1972) The Harderian glands of the domestic fowl. 3. Ultrastructure. J Anat 112:233–250PubMedGoogle Scholar
  50. Sakai T (1981) The mammalian Harderian gland: morphology, biochemistry, function and phylogeny. Arch Histol Jpn 44:299–333PubMedCrossRefGoogle Scholar
  51. Sakai T, Yohro T (1981) A histological study of the Harderian gland of Mongolian gerbils, Meriones meridianus. Anat Rec 200:259–270PubMedCrossRefGoogle Scholar
  52. Spike RC, Johnston HS, McGadey J, Moore MR, Thompson GG, Payne AP (1985) Quantitative studies on the effects of hormones on structure and porphyrin biosynthesis in the Harderian gland of the female golden hamster. I. The effects of ovariectomy and androgen administration. J Anat 142:59–72PubMedGoogle Scholar
  53. Spike RC, Johnston HS, McGadey J, Moore MR, Thompson GG, Payne AP (1986) Quantitative studies on the effects of hormones on structure and porphyrin biosynthesis in the Harderian gland of the female golden hamster. II. The time course of changes after ovariectomy. J Anat 145:67–77PubMedGoogle Scholar
  54. Strum JM, Shear CR (1982a) Harderian glands in mice: fluorescence, peroxidase activity and fine structure. Tissue Cell 14:135–148PubMedCrossRefGoogle Scholar
  55. Strum JM, Shear CR (1982b) Constant light exposure induces damage and squamous metaplasia in Harderian glands of albino mice. Tissue Cell 14:149–161PubMedCrossRefGoogle Scholar
  56. Sun CY, Nadakavukaren MJ (1980) Effect of testosterone on the female hamster Harderian gland pigmentation and ultrastructure. Cell Tissue Res 207:511–517PubMedCrossRefGoogle Scholar
  57. Tashiro S, Smith CC, Badger E, Kezur E (1940) Chromadacryorrhea, a new criterion for biological assay of acetylcholine. Proc Soc Exp Biol Med 44:658–661Google Scholar
  58. Tsutsumi A, Iwata K, Ogawa K, Matsuura K (1966) Histochemical and electron miscroscopic observations on the Harderian gland of the albino rat. Arch Histol Jpn 27:553–567 (in Japanese)Google Scholar
  59. Vilchis F, Perez-Palacios G (1989) Steroid hormone receptors and the sexual phenotype of the Harderian gland in hamsters. J Endocrinol 121:149–156PubMedCrossRefGoogle Scholar
  60. Vilchis F, Hernandez A, Perez AE, Perez-Palacios G (1987) Hormone regulation of the rodent Harderian gland: binding properties of the androgen receptors in the male golden hamster. J Endocrinol 112:3–8PubMedCrossRefGoogle Scholar
  61. Watanabe M (1980) An autoradiographic, biochemical, and morphological study of the Harderian gland of the mouse. J Morphol 163:349–365PubMedCrossRefGoogle Scholar
  62. Watanabe M, Kihara T, Shimono R (1981) Electron microscopy of myoepithelial cells of the mouse Harderian gland. Bull Osaka Med Sch 27:1–7PubMedGoogle Scholar
  63. Weaker FJ (1981) Light microscopic and ultrastructural features of the Harderian gland of the nine-banded armadillo. J Anat 133:49–65PubMedGoogle Scholar
  64. Winterhager E, Kühnel W (1983) Membrane specializations of the cells of the Harderian gland of the rabbit with particular reference to the mechanism of exocytosis. Cell Tissue Res 231:623–636PubMedCrossRefGoogle Scholar
  65. Woodhouse MA, Rhodin JAG (1963) The ultrastructure of the Harderian gland of the mouse with particular reference to the formation of its secretory product. J Ultrastruct Res 9:76–78CrossRefGoogle Scholar
  66. Wooding FBP (1980) Lipid droplet secretion by the rabbit Harderian gland. J Ultrastruct Res 71:68–78PubMedCrossRefGoogle Scholar
  67. Woolley W, Worley J (1954) Sexual dimorphism in the Harderian gland of the hamster (Cricetus auratus)Anat Rec 118:416–417(Abstr)Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1992

Authors and Affiliations

  • Mathew J. Nadakavukaren
    • 1
  1. 1.Department of Biological SciencesIllinois State UniversityNormalUSA

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