Skip to main content

Advertisement

Log in

Ultrastructure of cell contacts of fetal and adult Leydig cells in the rat: a systematic study from birth to senium

  • Original Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Differentiation, development, and function of Leydig cells in the testis are regulated also by macrophages, vascular endothelial cells, and peritubular cells in the testis. The aim of the present study was to investigate the possible morphological substrates for communication between these cells. The cell contacts between adjacent Leydig cells, and between Leydig cells and other interstitial cells were studied electron microscopically in the rat testis of various age groups from birth to senium. Intercellular bridges with continuous cytoplasm were observed between fetal Leydig cells (FLCs) in the early postnatal period. Gap junctions were present in nearly every age group. A structural diversity as well as an increased occurrence of gap junctions with the maturity of the Leydig cells was noted. Coated pits were observed initially on pnd 30. From pnd 50 onwards, macrophages and Leydig cells were attached very closely to each other, when the cell processes of Leydig cells protruded either into the coated pits or into the deep invaginations of macrophages. To conclude, this is the first report on the presence of intercellular bridges between FLCs suggesting a possible functional synchronization of interconnected Leydig cells. The cell contacts observed here are possibly required for a precise communication between the Leydig cells and other interstitial cells.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anand RJK, Paust HJ, Altenpohl K, Mukhopadhyay AK (2003) Regulation of vascular endothelial growth factor production by Leydig cells in vitro: the role of protein kinase A and mitogen-activated protein kinase cascade. Biol Reprod 68:1663–1673

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Luo L, Zirkin BR (1996) Leydig cell structure and function during aging. In: Payne AH, Hardy MP, Russell LD (eds) The Leydig cell. Cache River Press, Vienna, pp 221–230

    Google Scholar 

  • Chen JJ, Lukyanenko Y, Hutson JC (2002) 25-Hydroxycholesterol is produced by testicular macrophages during the early postnatal period and influences differentiation of Leydig cells in vitro. Biol Reprod 66:1336–1341

    Article  PubMed  CAS  Google Scholar 

  • Dym M, Fawcett DW (1971) Further observations on the numbers of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biol Reprod 4(2):195–215

    PubMed  CAS  Google Scholar 

  • Ergün S, Kilic N, Fiedler W, Mukhopadhyay AK (1997) Vascular endothelial growth factor and its receptors in normal human testicular tissue. Mol Cell Endocrinol 131:9–20

    Article  PubMed  Google Scholar 

  • Freeman DA, Rommerts FFG (1996) Regulation of Leydig cell cholesterol transport. In: Payne AH, Hardy MP, Russell LD (eds) The Leydig cell. Cache River Press, Vienna, pp 231–240

    Google Scholar 

  • Gaytan F, Bellido C, Aguilar E, van Rooijen N (1994a) Requirement for testicular macrophages in Leydig cell proliferation and differentiation during prepubertal development in rats. Reprod Fertil 102(2):393–399

    Article  CAS  Google Scholar 

  • Gaytan F, Bellido C, Morales C, Reymundo C, Aguilar E, van Rooijen N (1994b) Effects of macrophage depletion at different times after treatment with ethylene dimethane sulfonate (EDS) on the regeneration of Leydig cells in the adult rat. J Androl 15:558–564

    PubMed  CAS  Google Scholar 

  • Gaytan F, Bellido C, Morales C, Reymundo C, Aguilar E, van Rooijen N (1994c) Selective depletion of testicular macrophages and prevention of Leydig cells repopulation after treatment with ethylene dimethane sulphonate (EDS) in rat. J Reprod Fertil 101:171–182

    Google Scholar 

  • Gaytan F, Bellido C, Morales C, Reymundo C, Aguilar E, Rooijen N (1995a) Response to Leydig cell apoptosis in the absence of testicular macrophages. J Reprod Immunol 29:81–94

    Article  PubMed  CAS  Google Scholar 

  • Gaytan F, Bellido C, Morales C, van Rooijen N, Aguilar E (1995b) Roles of testicular macrophages in the response of Leydig cells to gonadotrophins in young hypophysectomized rats. J Endocrinol 147:463–471

    PubMed  CAS  Google Scholar 

  • Gaytan F, Bellido C, Morales C, Garcia M, van Rooijen N, Aguilar E (1996) In vitro manipulation (depletion versus activation) of testicular macrophages: central and local effects. J Endocrinol 15:57–65

    Article  Google Scholar 

  • Ghinea N, Milgrom E (1995) Transport of protein hormones through the vascular endothelium. J Endocrinol 145(1):1–9

    PubMed  CAS  Google Scholar 

  • Ghinea N, Vu Hai MT, Groyer-Picard MT, Houllier A, Schoevaert D, Milgrom E (1992) Pathways of internalization of the hCG/LH receptor: immunoelectron microscopic studies in Leydig cells and transfected L-cells. J Cell Biol 118(6):1347–1358

    Article  PubMed  CAS  Google Scholar 

  • Ghinea N, Vu Hai MT, Groyer-Picard MT, Milgrom E (1994) How protein hormones reach their target cells. Receptor-mediated transcytosis of hCG through endothelial cells. J Cell Biol 125(1):87–97

    Article  PubMed  CAS  Google Scholar 

  • Giannessi F, Giambelluca MA, Scavuzzo AM, Ruffoli R (2005) Ultrastructure of testicular macrophages in aging mice. J Morphol 263:39–46

    Article  PubMed  Google Scholar 

  • Haider SG (2004) Cell biology of Leydig cells in the testis. Int Rev Cytol 233:181–241

    Article  PubMed  CAS  Google Scholar 

  • Haider SG, Laue D, Schwochau G, Hilscher B (1995) Morphological studies on the origin of adult-type Leydig cells in rat testis. Ital J Anat Embryol 100(Suppl 1):535–541

    PubMed  Google Scholar 

  • Hales DB (1996) Leydig cell–macrophage interactions: an overview. In: Payne AH, Hardy MP, Russell LD (eds) The Leydig cell. Cache River Press, Vienna, pp 451–466

    Google Scholar 

  • Hales DB (2002) Testicular macrophage modulation of Leydig cell steroidogenesis. J Reprod Immunol 57:3–18

    Article  PubMed  CAS  Google Scholar 

  • Hamer GT, Roepers-Gajadien HL, Gademan IS, Kal HB, Rooij DG (2003) Intercellular bridges and apoptosis in clones of male germ cells. Int J Androl 26:348–353

    Article  PubMed  Google Scholar 

  • Handagama SMLCM, Ariyaratne HBS (2001) Differentiation of the adult Leydig cell population in the postnatal testis. Biol Reprod 65:660–671

    Article  Google Scholar 

  • Hardy MP, Zirkin BR, Ewing LL (1989) Kinetic studies on the development of the adult population of Leydig cells in testes of the pubertal rat. Endocrinology 124:762–770

    Article  PubMed  CAS  Google Scholar 

  • Huckins C (1978) Spermatogonial intercellular bridges in whole-mounted seminiferous tubules from normal and irradiated rodent testes. Am J Anat 153:97–121

    Article  PubMed  CAS  Google Scholar 

  • Hutson JC (1992) Development of cytoplasmic digitations between Leydig cells and testicular macrophages of the rat. Cell Tissue Res 267:385–389

    Article  PubMed  CAS  Google Scholar 

  • Ichihara I, Kawamura H, Pelliniemi LJ (1993) Ultrastructure and morphometry of testicular Leydig cells and the interstitial components correlated with testosterone in aging rats. Cell Tissue Res 271:241–255

    Article  PubMed  CAS  Google Scholar 

  • Kuopio T, Pelliniemi LJ (1989) Patchy basement membrane of rat Leydig cells shown by ultrastructural immunolabeling. Cell Tissue Res 256:45–51

    Article  PubMed  CAS  Google Scholar 

  • Larsen WJ (1983) Biological implications of gap junction structure, distribution and composition: a review. Tissue Cell 15:645–671

    Article  PubMed  CAS  Google Scholar 

  • Lukyanenko YO, Chen JJ, Hutson JC (2001) Production of 25-hydroxycholesterol by testicular macrophages and its effects on Leydig cells. Biol Reprod 64:790–796

    Article  PubMed  CAS  Google Scholar 

  • Lukyanenko YO, Chen JJ, Hutson JC (2002) Testosterone regulates 25-hydroxycholesterol production in testicular macrophages. Biol Reprod 67:1435–1438

    Article  PubMed  CAS  Google Scholar 

  • Miething A (1991) Intercellular bridges between megalospermatocytes in the human testis. Andrologia 23:91–97

    Article  PubMed  CAS  Google Scholar 

  • Nes WD, Lukyanenko YO, Jia ZH, Quidea S, Howald WN, Pratum T, West R, Hutson JC (2000) Identification of the lipophilic factor produced by macrophages that stimulates steroidogenesis. Endocrinology 14:953–958

    Article  Google Scholar 

  • Paniagua R, Amat P, Nistal M, Martin A (1986) Ultrastructure of Leydig cells in human ageing testes. J Anat 146:173–183

    PubMed  CAS  Google Scholar 

  • Pollard TD, Earnshaw WC (2002) Cell biology. SAUNDERS an imprint of Elsevier Science, Philadelphia, pp 525–534

  • Ren HP, Russell LD (1991) Clonal development of interconnected germ cells in the rat and its relationship to the segmental and subsegmental organization of spermatogenesis. Am J Anat 192:121–128

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez JB, Garcia CM (1999) Apoptosis is physiologically restricted to a specialized cytoplasmic compartment in rat spermatids. Biol Reprod 61:1541–1547

    Article  Google Scholar 

  • Russell LD (1996) Mammalian Leydig cell structure. In: Payne AH, Hardy MP, Russell LD (eds) The Leydig cell. Cache River Press, Vienna, pp 43–96

    Google Scholar 

  • Russell LD, Vogl AW, Weber JE (1987) Actin localization in male germ cell intercellular bridges in the rat and ground squirrel and disruption of bridges by cytochalasin D. Am J Anat 180(1):25–40

    Article  PubMed  CAS  Google Scholar 

  • Saez JM (1994) Leydig cells: endocrine, paracrine and autocrine regulation. Endocr Rev 15:574–626

    Article  PubMed  CAS  Google Scholar 

  • Setchell BP, Palombi F (2004) Isolation of endothelial cells from the rat testis, and their effect on testosterone secretion by interstitial cells. In: 13th European workshop on molecular and cellular endocrinology of the testis in Dunblane, Scotland. Abstract C6

  • Sivan BL, Bloch CL, Gutnick MJ, Fleidervish IA (2005) Electrotonic coupling in the anterior pituitary of a teleost fish. Endocrinology 146(3):1048–1052

    Article  CAS  Google Scholar 

  • Skinner MK (1991) Cell–cell interactions in the testis. Endocr Rev 12:45–77

    Article  PubMed  CAS  Google Scholar 

  • Svechnikov KV, Sultana T, Söder O (2001) Age-dependent stimulation of Leydig cell steroidogenesis by interleukin-1 isoforms. Mol Cell Endocrinol 182:193–201

    Article  PubMed  CAS  Google Scholar 

  • Weber JE, Russell LD (1987) A study of intercellular bridges during spermatogenesis in the rat. Am J Anat 180:1–24

    Article  PubMed  CAS  Google Scholar 

  • Wrobel KH, Sinowatz F, Mademann R (1981) Intertubular topography in the bovine testis. Cell Tissue Res 217:289–310

    Article  PubMed  CAS  Google Scholar 

  • Zirkin BR, Chen H (2000) Regulation of Leydig cell steroidogenic function during aging. Biol Reprod 63:977–981

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Ms Gabriele Berthold for her excellent technical assistance. The work reported here would be submitted for the partial fulfillment of doctoral thesis by Nicole Tran to the Faculty of Medicine, Heinrich Heine University, Düsseldorf.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Syed G. Haider.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tran, N., Servos, G. & Haider, S.G. Ultrastructure of cell contacts of fetal and adult Leydig cells in the rat: a systematic study from birth to senium. Anat Embryol 211, 273–282 (2006). https://doi.org/10.1007/s00429-006-0079-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-006-0079-z

Keywords

Navigation