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Mech Dev
2013 Jan 01;13011-12:613-27. doi: 10.1016/j.mod.2013.09.001.
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Retinoic acid homeostasis regulates meiotic entry in developing anuran gonads and in Bidder's organ through Raldh2 and Cyp26b1 proteins.
Piprek RP
,
Pecio A
,
Laskowska-Kaszub K
,
Kloc M
,
Kubiak JZ
,
Szymura JM
.
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The vitamin A (retinol) and its metabolites such as retinoic acid (RA) affect vertebrate gametogenesis. The level of RA in cells relies on the balance between its synthesis and degradation. The sex-dependent equilibrium is reached in different ways in various species. It is known that RA induces meiosis in developing gonads in mouse, chicken and urodel amphibians, but its role in anuran amphibians has not been studied. Here we show in six anuran species (Xenopus laevis, Bombina bombina, Hyla arborea, Bufo viridis, Rana arvalis and Rana temporaria) that cultured undifferentiated gonads were insensitive to RA treatment, but the RA induced ectopic meiosis in cultured larval testes. In larval testes of all studied species, the exogenous RA induced leptotene phase of I meiotic prophase in gonia, but only in H. arborea and B. viridis gonia progressed to zygotene phase. In the cultured developing ovaries, exogenous RA led to increase in the number of oocytes as compared to the control. Inhibition of either RA synthesis or RA-receptors prevented meiotic entry in larval gonads of all species. Exogenous RA rescued this inhibitory effect demonstrating that the balance in RA homeostasis plays a key role in meiotic entry in anuran gonads. The localization of two enzymes, Raldh2 and Cyp26b1, which antagonistically control RA levels and whose abundance suggests the sites of RA synthesis and degradation respectively, showed two distinct expression patterns specific for (i) X. laevis, H. arborea, R. arvalis, R. temporaria and (ii) B. bombina, B. viridis. Thus, RA, in correlation with specific expression patterns of Raldh2 and Cyp26b, induces meiosis during gonad development in anurans. In addition, in B. viridis, RA signalling seems important for development of the Bidder's organ containing oocytes both in males and females.
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24056063
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Fig. 1. Phylogenic tree of studied anuran species and their sex chromosome status (on the basis of Schmid and Steinlein, 2001 and Roelants et al., 2007).
Fig. 3. Effects of RA and ketoconazole on the undifferentiated gonads and testes of anuran amphibians. In the control undifferentiated gonads (Undiff.) as well as in the undifferentiated gonads and testes after 20-days culture with RA or ketoconazole, only gonial cells (g) were present and no meiocytes were observed. In the control testes only spermatogonia (sg) were present. In the testes after 20-days treatment with RA or ketoconazole meiocytes at phases leptotene (L) or zygotene/pachytene (Z) appeared besides spermatogonia. Scale bar 25 μm.
Fig. 4. Effects of citral and RAR antagonist (BMS453) on the ovaries of anuran amphibians including Bidder’s organs in Bufo viridis. In the control ovaries oogonia (og) as well as meiocytes at phases of leptotene (L), zygotene/pachytene (Z) as well as diplotene oocytes (D) were present. In the ovaries after 20-days culture with citral or RAR antagonist, only oogonia (og) were present and no meiocytes were visible. The control Bidder’s organs were filled with numerous diplotene oocytes (D), however, in the Bidder’s organs after 20-days treatment with citral or RAR antagonist the number of diplotene oocytes were lowered or only leptotene and zygotene/pachytene oocytes were present. Scale bar 25 μm.
Fig. 5. The immunolocalization of Raldh2 in the developing gonads of anuran amphibians. (A) The undifferentiated gonad (arrows) and adjacent tissues of X. laevis. The strongest signal of Raldh2 was visible in the somatic cells of the gonads (sc). (B) A slight signal of the Raldh2 in the testis of X. laevis. (C) A significant expression of Raldh2 in the X. laevis ovary, especially in the cortex (c) but also in the coelomic epithelium (ce). (D) The control gonad of X. laevis. (E) The undifferentiated gonads and adjacent tissues of H. arborea. The signal was visible in the proximal region of the gonad and in the coelomic epithelium. (F) The testis of H. arborea – the signal of Raldh2 was almost absent. (G) The larval H. arborea ovary and a strong signal of Raldh2. Oocytes were present in the cortex (Oc). (H) The control gonad of H. arborea. (I) The undifferentiated gonad of R. arvalis. Raldh2 was visible in both germ (gc) and the somatic cells (sc). (J) The R. arvalis testis – Raldh2 signal was weak. (K) The ovaries of R. arvalis – a strong signal of Raldh2 was observed in the superficialepithelium (se) as well as in the flattened follicular cells (fc) enclosing the germ cells. (L) The control gonad of R. arvalis. (M) The undifferentiated gonads of R. temporaria – Raldh2 was seen in the somatic and germ cells. (N) The testis of R. temporaria – a slight signal of Raldh2 was visible. (O) The R. temporaria ovary – Raldh2 was visible in the superficialepithelium and the follicular cells enclosing the germ cells. (P) The control gonad of R. temporaria. (Q) The undifferentiated gonads of B. bombina. The signal of Raldh2 was visible in the gonads (arrows), coelomic epithelium (ce) and kidney tubules (kt). (R) The testes and adjacent tissues of B. bombina. (S) The ovaries and adjacent tissues of B. bombina. The strong signal of Raldh2 was visible in the cortex (c) whereas was absent in the gonadal medulla (M). (T) The control gonads of B. bombina. (A′) A neglible signal of Raldh2 was present in the medial part of the genital ridge (arrows) of B. viridis at Gosner stage 29 – low level of the protein. (B′) The undifferentiated gonads of B. viridis in the medial part at Gosner stage 33 – low level of Raldh2. (C′) The testis of B. viridis at Gosner stage 44 – low level of Raldh2. (D′) The ovaries of B. viridis at Gosner stage 44 – an increase of Raldh2 signal. (E′) The control ovaries of B. viridis at Gosner stage 44. (F′) The anterior part of the genital ridge (future Bidder’s organ) of B. viridis, filled with oogonia at Gosner stage 29 – higher level of Raldh2 than in the medial part. (G′) The early Bidder’s organ of B. viridis just prior to the meiosis entry at Gosner stage 33 – higher level of Raldh2 than in the medial part. (H′) The Bidder’s organ of the B. viridis male at Gosner stage 44 containing many diplotene oocytes (D) – high signal of Raldh2 in the follicular cells (fc). (I′) The Bidder’s organ of the B. viridis female at Gosner stage 44. (J′) The control Bidder’s organ of B. viridis. Scale bar 40 μm.
Fig. 6. The immunolocalization of Cyp26b1 in the developing gonads of anuran amphibians. (A) The undifferentiated gonads (arrows) of X. laevis – the lack of Cyp26b1 stain. (B) The testis (arrows) – weak signal of Cyp26b1. (C) The ovaries (arrows) of X. laevis at – the absence of Cyp26b1 signal. (D) The undifferentiated gonads of H. arborea – The lack of Cyp26b1. (E) The testis of H. arborea in which slight signal of Cyp26b1 was observed. (F) The ovaries of H. arborea with the absence of Cyp26b1. (G) The undifferentiated gonads and adjacent tissues of R. arvalis. A slight signal of Cyp26b1 was seen in the nuclei of the germ cells. (H) The testes of R. arvalis – Cyp26b1 was almost undetectable. (I) The ovary of R. arvalis – Cyp26b1 – the absence of Cyp26b1. (J) The undifferentiated gonads of R. temporaria. The Cyp26b1 signal was evident in the germ cells (gc). (K) The testis of R. temporaria – a slight signal of Cyp26b1 was visible in the spermatogonia (sg). (L) The ovaries of R. temporaria with a low signal of Cyp26b1 in the germ cells. (M) The undifferentiated gonads and adjacent tissues of B. bombina – a slight signal of Cyp26b1 was seen. (N) In the testes tissues of B. bombina Cyp26b1 was visible in the somatic cells (presumably Sertoli cells) enclosing the germ cells. (O) The ovary tissues of B. bombina was characterized by the lack of Cyp26b1. (A′) The genital ridge (arrows) of B. viridis at the medial section (arrows) of B. viridis at Gosner stage 29. Cyp26b1 signal was strong especially in the somatic cells. (B′) The undifferentiated gonad of B. viridis in the medial part at Gosner stage 33. (C′) The testes (arrows) of B. viridis at the Gosner stage 44 - the Cyp26b1 was expressed in the somatic cells (Sertoli cells, Sc) enclosing germ cells. (D′) The ovary of B. viridis at the Gosner stage 44 – the lack of Cyp26b1. (E′) The genital ridge at the anterior part (future Bidder’s organ) – Cyp26b1 was observed. (F′) The beginning of the Bidder’s organ formation of B. viridis at Gosner stage 33 – the signal of Cyp26b1 was almost ceased. (G′) The later Bidder’s organ (arrows) of the B. viridis male at Gosner stage 44 – Cyp26b1 signal was strong in the cytoplasm of the oocytes (Oc). (H′) The Bidder’s organ of the B. viridis female was similar to this organ in a male. Scale bar 40 μm.
Fig. 7. Scheme of the Raldh2 and Cyp26b1 relations in the developing anuran gonads (transverse section) as well as in the Bidder’s organ and gonads of B. viridis (longitudinal section).
