Skip to main content
Top
Published in: Brain Structure and Function 4/2006

01-08-2006 | Original Article

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

Authors: Nicole Tran, Gisela Servos, Syed G. Haider

Published in: Brain Structure and Function | Issue 4/2006

Login to get access

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.
Literature
go back to reference 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 68:1663–1673PubMedCrossRef 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 68:1663–1673PubMedCrossRef
go back to reference 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 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
go back to reference 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 66:1336–1341PubMedCrossRef 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 66:1336–1341PubMedCrossRef
go back to reference 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):195–215PubMed 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):195–215PubMed
go back to reference Ergün S, Kilic N, Fiedler W, Mukhopadhyay AK (1997) Vascular endothelial growth factor and its receptors in normal human testicular tissue. Mol Cell Endocrinol 131:9–20PubMedCrossRef Ergün S, Kilic N, Fiedler W, Mukhopadhyay AK (1997) Vascular endothelial growth factor and its receptors in normal human testicular tissue. Mol Cell Endocrinol 131:9–20PubMedCrossRef
go back to reference 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 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
go back to reference 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):393–399CrossRef 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):393–399CrossRef
go back to reference 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 15:558–564PubMed 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 15:558–564PubMed
go back to reference 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 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
go back to reference 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 29:81–94PubMedCrossRef 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 29:81–94PubMedCrossRef
go back to reference 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 147:463–471PubMed 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 147:463–471PubMed
go back to reference 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 15:57–65CrossRef 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 15:57–65CrossRef
go back to reference Ghinea N, Milgrom E (1995) Transport of protein hormones through the vascular endothelium. J Endocrinol 145(1):1–9PubMed Ghinea N, Milgrom E (1995) Transport of protein hormones through the vascular endothelium. J Endocrinol 145(1):1–9PubMed
go back to reference 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):1347–1358PubMedCrossRef 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):1347–1358PubMedCrossRef
go back to reference 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):87–97PubMedCrossRef 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):87–97PubMedCrossRef
go back to reference Giannessi F, Giambelluca MA, Scavuzzo AM, Ruffoli R (2005) Ultrastructure of testicular macrophages in aging mice. J Morphol 263:39–46PubMedCrossRef Giannessi F, Giambelluca MA, Scavuzzo AM, Ruffoli R (2005) Ultrastructure of testicular macrophages in aging mice. J Morphol 263:39–46PubMedCrossRef
go back to reference 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):535–541PubMed 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):535–541PubMed
go back to reference 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 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
go back to reference Hales DB (2002) Testicular macrophage modulation of Leydig cell steroidogenesis. J Reprod Immunol 57:3–18PubMedCrossRef Hales DB (2002) Testicular macrophage modulation of Leydig cell steroidogenesis. J Reprod Immunol 57:3–18PubMedCrossRef
go back to reference 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 26:348–353PubMedCrossRef 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 26:348–353PubMedCrossRef
go back to reference Handagama SMLCM, Ariyaratne HBS (2001) Differentiation of the adult Leydig cell population in the postnatal testis. Biol Reprod 65:660–671CrossRef Handagama SMLCM, Ariyaratne HBS (2001) Differentiation of the adult Leydig cell population in the postnatal testis. Biol Reprod 65:660–671CrossRef
go back to reference 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 124:762–770PubMedCrossRef 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 124:762–770PubMedCrossRef
go back to reference Huckins C (1978) Spermatogonial intercellular bridges in whole-mounted seminiferous tubules from normal and irradiated rodent testes. Am J Anat 153:97–121PubMedCrossRef Huckins C (1978) Spermatogonial intercellular bridges in whole-mounted seminiferous tubules from normal and irradiated rodent testes. Am J Anat 153:97–121PubMedCrossRef
go back to reference Hutson JC (1992) Development of cytoplasmic digitations between Leydig cells and testicular macrophages of the rat. Cell Tissue Res 267:385–389PubMedCrossRef Hutson JC (1992) Development of cytoplasmic digitations between Leydig cells and testicular macrophages of the rat. Cell Tissue Res 267:385–389PubMedCrossRef
go back to reference 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 271:241–255PubMedCrossRef 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 271:241–255PubMedCrossRef
go back to reference Kuopio T, Pelliniemi LJ (1989) Patchy basement membrane of rat Leydig cells shown by ultrastructural immunolabeling. Cell Tissue Res 256:45–51PubMedCrossRef Kuopio T, Pelliniemi LJ (1989) Patchy basement membrane of rat Leydig cells shown by ultrastructural immunolabeling. Cell Tissue Res 256:45–51PubMedCrossRef
go back to reference Larsen WJ (1983) Biological implications of gap junction structure, distribution and composition: a review. Tissue Cell 15:645–671PubMedCrossRef Larsen WJ (1983) Biological implications of gap junction structure, distribution and composition: a review. Tissue Cell 15:645–671PubMedCrossRef
go back to reference Lukyanenko YO, Chen JJ, Hutson JC (2001) Production of 25-hydroxycholesterol by testicular macrophages and its effects on Leydig cells. Biol Reprod 64:790–796PubMedCrossRef Lukyanenko YO, Chen JJ, Hutson JC (2001) Production of 25-hydroxycholesterol by testicular macrophages and its effects on Leydig cells. Biol Reprod 64:790–796PubMedCrossRef
go back to reference Lukyanenko YO, Chen JJ, Hutson JC (2002) Testosterone regulates 25-hydroxycholesterol production in testicular macrophages. Biol Reprod 67:1435–1438PubMedCrossRef Lukyanenko YO, Chen JJ, Hutson JC (2002) Testosterone regulates 25-hydroxycholesterol production in testicular macrophages. Biol Reprod 67:1435–1438PubMedCrossRef
go back to reference Miething A (1991) Intercellular bridges between megalospermatocytes in the human testis. Andrologia 23:91–97PubMedCrossRef Miething A (1991) Intercellular bridges between megalospermatocytes in the human testis. Andrologia 23:91–97PubMedCrossRef
go back to reference 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 14:953–958CrossRef 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 14:953–958CrossRef
go back to reference Paniagua R, Amat P, Nistal M, Martin A (1986) Ultrastructure of Leydig cells in human ageing testes. J Anat 146:173–183PubMed Paniagua R, Amat P, Nistal M, Martin A (1986) Ultrastructure of Leydig cells in human ageing testes. J Anat 146:173–183PubMed
go back to reference Pollard TD, Earnshaw WC (2002) Cell biology. SAUNDERS an imprint of Elsevier Science, Philadelphia, pp 525–534 Pollard TD, Earnshaw WC (2002) Cell biology. SAUNDERS an imprint of Elsevier Science, Philadelphia, pp 525–534
go back to reference 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 192:121–128PubMedCrossRef 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 192:121–128PubMedCrossRef
go back to reference Rodriguez JB, Garcia CM (1999) Apoptosis is physiologically restricted to a specialized cytoplasmic compartment in rat spermatids. Biol Reprod 61:1541–1547CrossRef Rodriguez JB, Garcia CM (1999) Apoptosis is physiologically restricted to a specialized cytoplasmic compartment in rat spermatids. Biol Reprod 61:1541–1547CrossRef
go back to reference 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 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
go back to reference 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):25–40PubMedCrossRef 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):25–40PubMedCrossRef
go back to reference Saez JM (1994) Leydig cells: endocrine, paracrine and autocrine regulation. Endocr Rev 15:574–626PubMedCrossRef Saez JM (1994) Leydig cells: endocrine, paracrine and autocrine regulation. Endocr Rev 15:574–626PubMedCrossRef
go back to reference 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 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
go back to reference Sivan BL, Bloch CL, Gutnick MJ, Fleidervish IA (2005) Electrotonic coupling in the anterior pituitary of a teleost fish. Endocrinology 146(3):1048–1052CrossRef Sivan BL, Bloch CL, Gutnick MJ, Fleidervish IA (2005) Electrotonic coupling in the anterior pituitary of a teleost fish. Endocrinology 146(3):1048–1052CrossRef
go back to reference Svechnikov KV, Sultana T, Söder O (2001) Age-dependent stimulation of Leydig cell steroidogenesis by interleukin-1 isoforms. Mol Cell Endocrinol 182:193–201PubMedCrossRef Svechnikov KV, Sultana T, Söder O (2001) Age-dependent stimulation of Leydig cell steroidogenesis by interleukin-1 isoforms. Mol Cell Endocrinol 182:193–201PubMedCrossRef
go back to reference Weber JE, Russell LD (1987) A study of intercellular bridges during spermatogenesis in the rat. Am J Anat 180:1–24PubMedCrossRef Weber JE, Russell LD (1987) A study of intercellular bridges during spermatogenesis in the rat. Am J Anat 180:1–24PubMedCrossRef
go back to reference Wrobel KH, Sinowatz F, Mademann R (1981) Intertubular topography in the bovine testis. Cell Tissue Res 217:289–310PubMedCrossRef Wrobel KH, Sinowatz F, Mademann R (1981) Intertubular topography in the bovine testis. Cell Tissue Res 217:289–310PubMedCrossRef
go back to reference Zirkin BR, Chen H (2000) Regulation of Leydig cell steroidogenic function during aging. Biol Reprod 63:977–981PubMedCrossRef Zirkin BR, Chen H (2000) Regulation of Leydig cell steroidogenic function during aging. Biol Reprod 63:977–981PubMedCrossRef
Metadata
Title
Ultrastructure of cell contacts of fetal and adult Leydig cells in the rat: a systematic study from birth to senium
Authors
Nicole Tran
Gisela Servos
Syed G. Haider
Publication date
01-08-2006
Publisher
Springer-Verlag
Published in
Brain Structure and Function / Issue 4/2006
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-006-0079-z

Other articles of this Issue 4/2006

Brain Structure and Function 4/2006 Go to the issue