Abstract
Transgenic mice expressing high levels of the BclxL or Bcl2 proteins in the male germinal cells show a highly abnormal adult spermatogenesis accompanied by sterility. This appears to result from the prevention of an early and massive wave of apoptosis in the testis, which occurs among germinal cells during the first round of spermatogenesis. In contrast, sporadic apoptosis among spermatogonia, which occurs in normal adult testis, is not prevented in adult transgenic mice. The physiological early apoptotic wave in the testis is coincident, in timing and localization, with a temporary high expression of the apoptosis-promoting protein Bax, which disappears at sexual maturity. The critical role played by the intracellular balance, probably hormonally controlled, of the BclxL and Bax proteins (Bcl2 is apparently not expressed in normal mouse testis) in this early apoptotic wave is shown by the occurrence of a comparable testicular syndrome in mice defective in the bax gene. The apoptotic wave appears necessary for normal mature spermatogenesis to develop, probably because it maintains a critical cell number ratio between some germinal cell stages and Sertoli cells, whose normal functions and differentiation involve an elaborate network of communication.
MeSH Terms
Animals
Apoptosis/drug effects
Blotting, Western
Cell Differentiation
Cells, Cultured
Humans
Male
Mice
Mice, Transgenic
Proto-Oncogene Proteins/genetics,metabolism
Proto-Oncogene Proteins c-bcl-2/genetics,metabolism
Sexual Maturation
Spermatogenesis/drug effects
Spermatogonia/cytology
Spermatozoa/cytology
Testis/cytology
Testosterone/pharmacology
bcl-2-Associated X Protein
bcl-X Protein
Chemicals
BAX protein, human
BCL2L1 protein, human
Bax protein, mouse
Bcl2l1 protein, mouse
Proto-Oncogene Proteins
Proto-Oncogene Proteins c-bcl-2
bcl-2-Associated X Protein
bcl-X Protein
Testosterone
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Rodriguez I
Department of Pathology, Centre Médical Universitaire, Geneva, Switzerland.
Ody C
Araki K
Garcia I
Vassalli P
References (22)
22 references, click to expand
-
Spermatogonial apoptosis has three morphologically recognizable phases and shows no circadian rhythm during normal spermatogenesis in the rat.
Cell Prolif. 1992 May;25(3):241-50
PMID: 1596537
-
Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing Bcl-2 in spermatogonia.
Development. 1996 Jun;122(6):1703-9
PMID: 8674410
-
Hormonal control of apoptotic cell death in the testis: gonadotropins and androgens as testicular cell survival factors.
Mol Endocrinol. 1993 May;7(5):643-50
PMID: 8316250
-
Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis.
Endocrinology. 1993 Nov;133(5):2204-12
PMID: 8404672
-
The Sertoli-germ cell communication network in mammals.
Int Rev Cytol. 1993;147:25-96
PMID: 8225836
-
Immediate early up-regulation of bax expression by p53 but not TGF beta 1: a paradigm for distinct apoptotic pathways.
Oncogene. 1994 Jun;9(6):1791-8
PMID: 8183578
-
Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo.
Oncogene. 1994 Jun;9(6):1799-805
PMID: 8183579
-
Immunohistochemical localization of androgen receptors in the rat testis: evidence for stage-dependent expression and regulation by androgens.
Endocrinology. 1994 Sep;135(3):1227-34
PMID: 8070367
-
Immunohistochemical analysis of in vivo patterns of Bcl-X expression.
Cancer Res. 1994 Nov 1;54(21):5501-7
PMID: 7923184
-
Developmental stage- and spermatogenic cycle-specific expression of transcription factor GATA-1 in mouse Sertoli cells.
Development. 1994 Jul;120(7):1759-66
PMID: 7924983
-
Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia.
Neuron. 1994 Oct;13(4):1017-30
PMID: 7946326
-
T-cell apoptosis detected in situ during positive and negative selection in the thymus.
Nature. 1994 Nov 3;372(6501):100-3
PMID: 7969401
-
Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2.
Am J Pathol. 1994 Dec;145(6):1323-36
PMID: 7992838
-
Expression of members of the bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-xlong messenger ribonucleic acid levels.
Endocrinology. 1995 Jan;136(1):232-41
PMID: 7828536
-
Apoptosis in testis germ cells: developmental changes in gonadotropin dependence and localization to selective tubule stages.
Endocrinology. 1995 Jan;136(1):5-12
PMID: 7828558
-
Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death.
Cell. 1995 Jan 27;80(2):285-91
PMID: 7834748
-
Tumor suppressor p53 is a direct transcriptional activator of the human bax gene.
Cell. 1995 Jan 27;80(2):293-9
PMID: 7834749
-
Cloning of a bcl-2 homologue by interaction with adenovirus E1B 19K.
Nature. 1995 Apr 20;374(6524):731-3
PMID: 7715729
-
Regulators of cell death.
Trends Genet. 1995 Mar;11(3):101-5
PMID: 7732571
-
Bax-deficient mice with lymphoid hyperplasia and male germ cell death.
Science. 1995 Oct 6;270(5233):96-9
PMID: 7569956
-
A bcl-2 transgene expressed in hepatocytes protects mice from fulminant liver destruction but not from rapid death induced by anti-Fas antibody injection.
J Exp Med. 1996 Mar 1;183(3):1031-6
PMID: 8642244
-
Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.
J Cell Biol. 1992 Nov;119(3):493-501
PMID: 1400587