Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Examination of basement membrane components associated with the bovine seminiferous tubule basal lamina

Veronica Glattauer A B E , Helen F. Irving-Rodgers C , Raymond J. Rodgers C , Sally Stockwell A D , Alan G. Brownlee A D , Jerome A. Werkmeister A B and John A. M. Ramshaw A B
+ Author Affiliations
- Author Affiliations

A CSIRO Food Futures National Research Flagship, Austrlia.

B CSIRO Molecular and Health Technologies, Bayview Avenue, Clayton, Vic. 3169, Australia.

C Research Centre for Reproductive Health, Department of Obstetrics and Gynaecology, University of Adelaide, Adelaide, SA 5005, Australia.

D CSIRO Livestock Industries, Queensland Biosciences Precinct, St Lucia, Qld 4067, Australia.

E Corresponding author. Email: veronica.glattauer@csiro.au

Reproduction, Fertility and Development 19(3) 473-481 https://doi.org/10.1071/RD06013
Submitted: 21 February 2006  Accepted: 15 January 2007   Published: 19 March 2007

Abstract

Immunohistology has been used to examine the distribution of certain components of the basement membrane (BM) associated with bovine spermatogonial germ cells that are located within the seminiferous tubules. Histology was performed on testis tissue from Brahman cattle (Bos indicus) of three different age groups: pre-pubescent (4–6 months), juvenile (8–10 months) and adult (18–24 months) animals. There were no major changes in the BM composition apparent between these three age groups, except for certain lectin staining. These data suggest that the predominant collagen type IV component may have an α3 and α4 composition, although other chains, including the α5 and α6 chains, were also present. Possibly the main laminin type present was laminin 121 (α1β2γ1), although other variants were also present. Both nidogen-1 and perlecan, which are normal BM components, were also found as part of the seminiferous tubule BM. Interstitial collagens, such as type I, III and VI collagens, were found in the peritubular space, but were not part of the BM itself, although type VI collagen was most visible in the peritubular zone adjacent to the tubules. Examination of the BM with a range of lectins gave strong staining for (glcNAc)2 entities, weak positive staining for α-l-fuc, but little or no staining for α-galNAc and (glcNAc)3 at all ages, whereas staining for α-gal, β-gal(1→3)galNAc and α-man showed developmental changes.

Additional keyword: cell transfer.


Acknowledgements

We wish to thank Dr Y. Sado, Dr Y. Ninomiya, Dr L. Sorokin, Dr M. Dziadek and Dr P. A. Underwood for the gifts of antibodies, Stephanie Morris for assistance with immunohistology and Laura Jenkinson for assistance with lectin histology.


References

Akama, T. O. , Nakagawa, H. , Sugihara, K. , Narisawa, S. , Ohyama, C. , Nisimura, S.-I. , O'Brien, D. A. , Moremen, K. W. , Millan, J. L. , and Fukuda, M. N. (2002). Germ cell survival through carbohydrate-mediated interaction with Sertoli cells. Science 295, 124–127.
Crossref | GoogleScholarGoogle Scholar | PubMed | Hay E. D. 1991 ‘Cell Biology of the Extracellular Matrix.’ 2nd edn. (Plenum Press: New York.)

Hill, J. R. , and Dobrinski, I. (2006). Male germ cell transplantation in livestock. Reprod. Fertil. Dev. 18, 13–18.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hohenester, E. , and Engel, J. (2002). Domain structure and organisation in extracellular matrix proteins. Matrix Biol. 21, 115–128.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Honaramooz, A. , Megee, S. O. , and Dobrinski, I. (2002). Germ cell transplantation in pigs. Biol. Reprod. 66, 21–28.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Honaramooz, A. , Behboodi, E. , Blash, S. , Megee, S. O. , and Dobrinski, I. (2003). Germ cell transplantation in goats. Mol. Reprod. Dev. 64, 422–428.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hudson, B. G. , Reeders, S. T. , and Tryggvason, K. (1993). Type IV collagen: structure, gene organization, and role in human diseases. Molecular basis of Goodpasture and Alport syndromes and diffuse leiomyomatosis. J. Biol. Chem. 268, 26 033–26 036.
PubMed |

Iozzo, R. V. (2005). Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell Biol. 6, 646–656.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Irving-Rodgers, H. F. , and Rodgers, R. J. (2005). Extracellular matrix in ovarian follicular development and disease. Cell Tissue Res. 322, 89–98.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Irving-Rodgers, H. F. , Harland, M. L. , and Rodgers, R. J. (2004). A novel basal lamina matrix of the stratified epithelium of the ovarian follicle. Matrix Biol. 23, 207–217.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Izadyar, F. , Spierenberg, G. T. , Creemers, L. B. , den Ouden, K. , and de Rooij, D. G. (2002). Isolation and purification of type A spermatogonia from the bovine testis. Reproduction 124, 85–94.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Kahsai, T. Z. , Enders, G. C. , Gunwar, S. , Brunmark, C. , Wieslander, J. , Kalluri, R. , Zhou, J. , Noelken, M. E. , and Hudson, B. G. (1997). Seminiferous tubule basement membrane. Composition and organization of type IV collagen chains, and the linkage of alpha3(IV) and alpha5(IV) chains. J. Biol. Chem. 272, 17 023–17 032.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Manning, J. C. , Seyrek, K. , Kaltner, H. , Andre, S. , Sinowatz, F. , and Gabius, H.-J. (2004). Glycomic profiling of developmental changes in bovine testis by lectin histochemistry and further analysis of the most prominent alteration on the level of the glycoproteome by lectin blotting and lectin affinity chromatography. Histol. Histopathol. 19, 1043–1060.
PubMed |

McClive, P. J. , and Sinclair, A. H. (2003). Type II and type IX collagen transcript isoforms are expressed during mouse testis development. Biol. Reprod. 68, 1742–1747.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Newman, S. , Reverter, A. , and Johnston, D. J. (2002). Purebred-crossbred performance and genetic evaluation of postweaning growth and carcass traits in Bos indicus × Bos taurus crosses in Australia. J. Anim. Sci. 80, 1801–1808.
PubMed |

Oatley, J. M. , de Avila, D. M. , McLean, D. J. , Griswold, M. D. , and Reeves, J. J. (2002). Transplantation of bovine germinal cells into mouse testes. J. Anim. Sci. 80, 1925–1931.
PubMed |

Parreira, G. G. , Ogawa, T. , Avarbock, M. R. , Franca, L. R. , Brinster, R. L. , and Russell, L. D. (1998). Development of germ cell transplants in mice. Biol. Reprod. 59, 1360–1370.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Petajaniemi, N. , Korhonen, M. , Kortesmaa, J. , Tryggvason, K. , and Sekiguchi, K. , et al. (2002). Localization of laminin α4-chain in developing and adult human tissues. J. Histochem. Cytochem. 50, 1113–1130.
PubMed |

Pollanen, P. P. , Kallajoki, M. , Risteli, L. , Risteli, J. , and Suominen, J. J. (1985). Laminin and type IV collagen in the human testis. Int. J. Androl. 8, 337–347.
PubMed |

Poschl, E. , Schlotzer-Schrehardt, U. , Brachvogel, B. , Saito, K. , Ninomiya, Y. , and Mayer, U. (2004). Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131, 1619–1628.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ryu, B. Y. , Kubota, H. , Avarbock, M. R. , and Brinster, R. L. (2005). Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. Proc. Natl Acad. Sci. USA 102, 14 302–14 307.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Saito, K. , Naito, I. , Seki, T. , Oohashi, T. , Kimura, E. , Momota, R. , Kishiro, Y. , Sado, Y. , Yoshioka, H. , and Ninomiya, Y. (2000). Differential expression of mouse alpha5(IV) and alpha6(IV) collagen genes in epithelial basement membranes. J. Biochem. (Tokyo) 128, 427–434.
PubMed |

Santamaria, L. , Martinez-Onsurbe, P. , Paniagua, R. , and Nistal, M. (1990). Laminin, type IV collagen, and fibronectin in normal and cryptorchid human testes. An immunohistochemical study. Int. J. Androl. 13, 135–146.
PubMed |

Santoro, G. , Romeo, C. , Impellizzeri, P. , Gentile, C. , Anastasi, G. , and Santoro, A. (2000). Ultrastructural and immunohistochemical study of basal lamina of the testis in adolescent varicocele. Fertil. Steril. 73, 699–705.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sasaki, T. , Fassler, R. , and Hohenester, E. (2004). Laminin: the crux of basement membrane assembly. J. Cell Biol. 164, 959–963.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sato, K. , Yomogida, K. , Wada, T. , Yorihuzi, T. , Nishimune, Y. , Hosokawa, N. , and Nagata, K. (2002). Type XXVI collagen, a new member of the collagen family, is specifically expressed in the testis and ovary. J. Biol. Chem. 277, 37 678–37 684.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shinohara, T. , Avarbock, M. R. , and Brinster, R. L. (1999). β1 and α6-integrin are surface markers on mouse spermatogonial stem cells. Proc. Natl Acad. Sci. USA 96, 5504–5509.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Siu, M. K. , Lee, W. M. , and Cheng, C. Y. (2003). The interplay of collagen IV, tumor necrosis factor-alpha, gelatinase B (matrix metalloprotease-9), and tissue inhibitor of metalloproteases-1 in the basal lamina regulates Sertoli cell-tight junction dynamics in the rat testis. Endocrinology 144, 371–387.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tryggvason, K. , and Kivirikko, K. I. (1978). Heterogeneity of pepsin-solubilized human glomerular basement membrane collagen. Nephron 21, 230–235.
PubMed |

Virtanen, I. , Lohi, J. , Tani, T. , Korhonen, M. , Burgeson, R. E. , Lehto, V. P. , and Leivo, I. (1997). Distinct changes in the laminin composition of basement membranes in human seminiferous tubules during development and degeneration. Am. J. Pathol. 150, 1421–1431.
PubMed |

Werkmeister, J. A. , and Ramshaw, J. A. M. (1991). Multiple antigenic determinants on type III collagen. Biochem. J. 274, 895–898.
PubMed |

Werkmeister, J. A. , Ramshaw, J. A. M. , and Ellender, G. (1990). Characterisation of a monoclonal antibody against native human type I collagen. Eur. J. Biochem. 187, 439–443.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Werkmeister, J. A. , Tebb, T. A. , White, J. F. , and Ramshaw, J. A. M. (1993). Monoclonal antibodies to type VI collagen demonstrate new tissue augmentation of a collagen-based biomaterial implant. J. Histochem. Cytochem. 41, 1701–1706.
PubMed |

Yurchenco, P. D. , Amenta, P. S. , and Patton, B. L. (2004). Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol. 22, 521–538.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Zhang, Z. , Shao, S. , and Meistrich, M. L. (2006). Irradiated mouse testes efficiently support spermatogenesis derived from donor germ cells of mice and rats. J. Androl. 27, 365–375.
Crossref | GoogleScholarGoogle Scholar | PubMed |