Loss of Sertoli-germ cell adhesion determines the rapid germ cell elimination during the seasonal regression of the seminiferous epithelium of the large hairy armadillo Chaetophractus villosus.
The armadillo Chaetophractus villosus is a seasonal breeder whose seminiferous epithelium undergoes rapid regression with massive germ cell loss, leaving the tubules with only Sertoli cells and spermatogonia. Here, we addressed the question of whether this regression entails 1) the disassembly of cell junctions (immunolocalization of nectin-3, Cadm1, N-cadherin, and beta-catenin, and transmission electron microscopy [TEM]); 2) apoptosis (immunolocalization of cytochrome c and caspase 3; TUNEL assay); and 3) the involvement of Sertoli cells in germ cell phagocytosis (TEM). We showed a dramatic reduction in the extension of vimentin filaments associated with desmosomelike junctions at the interface between Sertoli and germ cells, and an increased diffusion of the immunosignals of nectin-3, Cadm1, N-cadherin, and beta-catenin. Together, these results suggest loss of Sertoli-germ cell adhesion, which in turn might determine postmeiotic cell sloughing at the beginning of epithelium regression. Then, loss of Sertoli-germ cell adhesion triggers cell death. Cytochrome c is released from mitochondria, but although postmeiotic cells were negative for late apoptotic markers, at advanced regression spermatocytes were positive for all apoptotic markers. Transmission electron microscopy analysis showed cytoplasmic engulfment of cell debris and lipid droplets within Sertoli cells, a sign of their phagocytic activity, which contributes to the elimination of the residual meiocytes still present in the latest regression phases. These findings are novel and add new players to the mechanisms of seminiferous epithelium regression occurring in seasonal breeders, and they introduce the armadillo as an interesting model for studying seasonal spermatogenesis.
Laboratorio de Biología Cromosómica, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, Argentina.
Juan Pablo
JP
Luaces
Luis Francisco
LF
Rossi
Roberta Beatriz
RB
Sciurano
Paola
P
Rebuzzini
Valeria
V
Merico
Maurizio
M
Zuccotti
Maria Susana
MS
Merani
Silvia
S
Garagna
D000818:Animals; D017209:Apoptosis / Q000502:physiology; D001135:Armadillos / Q000502:physiology*; D015820:Cadherins / Q000378:metabolism; D053148:Caspase 3 / Q000378:metabolism; D002448:Cell Adhesion / Q000502:physiology*; D015815:Cell Adhesion Molecules / Q000378:metabolism; D045304:Cytochromes c / Q000378:metabolism; D005854:Germ Cells / Q000502:physiology*; D007150:Immunohistochemistry; D020287:In Situ Nick-End Labeling; D007365:Intercellular Junctions / Q000502:physiology; D008297:Male; D008540:Meiosis / Q000502:physiology; D046529:Microscopy, Electron, Transmission; D000075983:Nectins; D010587:Phagocytosis / Q000502:physiology; D012621:Seasons; D012670:Seminiferous Epithelium / Q000502:physiology*; D012708:Sertoli Cells / Q000502:physiology*; D051176:beta Catenin / Q000378:metabolism
D015820:Cadherins; D015815:Cell Adhesion Molecules; D000075983:Nectins; D051176:beta Catenin; D045304:Cytochromes c; D053148:Caspase 3
Cadm1; N-cadherin and β-catenin; adhesion molecules; anoikis; apoptosis; intermediate filaments; nectin-3; phagocytosis; seasonal reproduction; spermatogenesis; testosterone