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Interrenal Organogenesis in the Zebrafish Model

Interrenal Organogenesis in the Zebrafish Model [Organogenesis 3:1, e1-e5, EPUB Ahead of Print: http://www.landesbioscience.com/journals/organogenesis/abstract.php?id=3965; 1 January 2007]; ©2007 Landes Bioscience Review Yi-Wen Liu Abstr Act In recent years, many genes that participate in the specification, differentiation and *Correspondence to: Liu Yi-Wen; Department of Life Science; Tunghai University; No. 181, Sec. 3; Taichung-Kan Road; Taichung 40704 Taiwan, steroidogenesis of the interrenal organ, the teleostean homologue of the adrenal cortex, ROC; Tel.: +886.4.2359.0121 ext. 2466; Fax: +886.4.2359.0296; have been identified and characterized in zebrafish. In‑depth studies of these genes Email: [email protected] have helped to delineate the morphogenetic steps of interrenal organ formation, as well This manuscript has been published online, prior to printing for Organogenesis, as some of the molecular and cellular mechanisms that govern these processes. The co‑ Volume 3, Issue 1. Definitive page numbers have not been assigned. The current development of interrenal tissue with the embryonic kidney (pronephros), surrounding citation is: Organogenesis 2007; 3(1): endothelium and invading chromaffin cells has been analyzed, by virtue of the amenability http://www.landesbioscience.com/journals/organogenesis/abstract.php?id=3965 of zebrafish embryos to a variety of genetic, developmental and histological approaches. Once the issue is complete and page numbers have been assigned, the citation will change accordingly. Moreover, zebrafish embryos can be subject to molecular as well as biochemical assays for the unraveling of the transcriptional regulation program underlying interrenal develop‑ ment. To this end, the key mechanisms that control organogenesis and steroidogenesis of KeY Words the zebrafish interrenal gland have been shown to resemble those in mammals, justifying interrenal, adrenal, pronephros, endothelium, the future utilization of zebrafish model for discovering novel genes associated with chromaffin, organogenesis, zebrafish adrenal development and disease. Ac Kno WLedgements The author would like to thank Dr. Woon- Introduct Ion Khiong Chan and Dr. Chou Chai for pioneering work on zebrafish interrenal The external fertilization and rapid development of the zebrafish embryo has made organ; Prof. Bon-chu Chung and her team it suitable for studying early vertebrate development. Due to the permeability and for inspiring discussions. This work was optic transparency of the zebrafish embryo, developing organ primordia in the whole supported by grants NSC94-2320-B-029-001 mount specimen can be readily detected by histochemistry, immunohistochemistry or and NSC95-2311-B-029-008 from National in situ hybridizations. Various cell types that integrate to constitute specific organs, Science Council (R.O.C). such as embryonic heart and kidney, can be labeled simultaneously by a combination of 3,4 histological approaches. Hence, the zebrafish is particularly useful for capitulating the dynamic processes of organ formation, especially cell migration events or morphogenetic movements of organ primordia. Furthermore, the establishment of transgenic fluorescent reporter lines has allowed the tracking of specific lineages as well as dissection of cellular processes with high resolution. For example, endothelium-specific transgenic reporter lines have enabled the elucidation of mechanisms underlying vessel formation, angiogen- 5-7 esis and endothelial tube assembly. Zebrafish mutants that are generated from either forward or reverse genetic approaches have offered great opportunity for understanding the interrelationships among gene, 8,9 development and disease. Large-scale chemical mutagenesis screens have identified numerous mutants with a wide spectrum of defects manifested in various organs, helping to elucidate specific signaling pathways leading to organogenesis such as heart and blood formation. The advent of antisense morpholino oligo knockdown approach, proven effec- tive and specific in the zebrafish embryo, has further facilitated the developmental analysis for any candidate genes of interest. Although the endocrine gland structures of fish and mammals are largely different, their developmental processes in organogenesis appear to share high similarities. Also, endocrine function is well conserved between teleosts and mammals, which could be reflected by the profiles of hormones, hormone receptors as well as transcriptional regu- lators. Interestingly, some zebrafish mutants or morphants faithfully phenocopy human endocrine disorders such as combined pituitary hormone deficiencies and neonatal diabetes mellitus. Hence, they promise to provide insights into the molecular etiology of their human disease counterparts. This short review highlights the teleostean counterpart of mammalian adrenal gland, the interrenal gland, based on recent findings in the zebrafish model. The ontogeny, e1 Organogenesis 2007; Vol. 3 Issue 1 ©2007 LANDES BIOSCIENCE. DO NOT DISTRIBUTE. Interrenal Organogenesis in the Zebrafish Model Figure 1. The detection of steroidogenic interrenal tissue by whole‑mount chromogenic 3b‑Hsd enzymatic activity assay in wild‑type control (upper panel) and ff1b antisense morpholino (ff1bMO) injected (lower panel) embryos. The embryos were treated with 0.003% phenylthiourea from 12 hpf onwards to prevent pigmentation. Dorso‑lateral views of embryos at 2 dpf are shown with anterior oriented to the right. The steroidogenic interre‑ nal cells are completely ablated in ff1b morphant. Red arrowhead indicates interrenal tissue (IR), lying above yolk sac in the mid‑trunk region. molecular determinants, cell migrations and tissue-tissue interactions are outlined, in order to discuss the relevance of zebrafish interrenal organ to mammalian adrenal gland. m o Lecu LLAr And c eLLu LAr c ontro Ls of Interren AL Figure 2. Early morphogenetic processes in the interrenal development of zebrafish. The parallel migrations of interrenal tissue, pronephros and o rg Anogenes Is chromaffin cells in this diagram are depicted based on the results of ref‑ FF1b marks and determines the onset of interrenal tissue. The erences 18, 20 and 39. The panels represent dorsal views of embryos, mode of tissue organization for teleostean interrenal organ is distinct at the indicated stages, oriented with anterior to the top. Through the sequential stages of interrenal specification, migration, steroidogenesis and from that of mammalian adrenal gland. The interrenal cells inter- chromaffin cell invasion, an assembled interrenal organ is evident by 3 dpf. mingle with, rather than encapsulate, the chromaffin cells which NC, notochord; 2S and 3S, the second and third somite, respectively. are functional equivalent of the adrenal medulla, and the assembled organ is embedded at the anterior portion of the head kidney. However, the molecular determinants for specifying steroidogenic primordia (Fig. 2), while both pronephros and interrenal tissue are 4,18 lineages have proven to be highly conserved between teleosts and derived from intermediate mesoderm. The interrenal tissues then mammals. Two Ftz-F1 genes, ff1b (nr5a1a) and ff1d (nr5a1b), have migrate out of the pronephric fields, before the initiation of steroido- been identified in zebrafish to be co-orthologues of mammalian SF1/ genesis. After separation, the interrenal and pronephric tissues stay 15-17 Ad4BP (NR5A1). While SF1 is obligatorily required for both in close proximity to one another throughout development, and adrenal and gonadal development, ff1b and ff1d appear to function both undergo central migration followed by fusion. Temporally, the predominantly in interrenal tissue and gonads, respectively. ff1b is the convergence of bilateral interrenal primordia well precedes the central earliest molecular marker detected in the developing interrenal tissue assembly of pronephros. Interestingly, both pronephros and inter- of zebrafish embryo. The knockdown of Ff1b by the antisense renal tissue receive endothelium-derived signals, albeit via different 19,20 morpholino oligo approach led to specific ablation of interrenal cells, mechanisms, as guidance cues for central migration. as revealed by the loss of either functional differentiation (Fig. 1) or The central migration of pronephric primordia, starting at around interrenal-specific RNA transcripts, indicating that Ff1b is absolutely 30 hours post-fertilization (hpf ), is temporally correlated with the 4,18,20 required for the initiation of interrenal primordium. angiogenesis of paired glomeruli. In the meantime, the developing Pronephros vs. interrenal tissue: Parallel morphogenetic move‑ interrenal cells are tightly associated with endothelium (Fig. 3A–F). This ments under differential endothelium‑derived controls. Temporal central fusion of glomeruli is disrupted upon the perturbations of blood and spatial analyses revealed that early interrenal tissues arise as flow, either genetically or pharmaceutically, implying a role of hemody- bilateral clusters of non-steroidogenic cells within the pronephric namic force for glomerular morphogenesis. Indeed, the endothelial www.landesbioscience.com Organogenesis e2 ©2007 LANDES BIOSCIENCE. DO NOT DISTRIBUTE. Interrenal Organogenesis in the Zebrafish Model Molecular interplays within interrenal primordium. The expression of ff1b is spatially closely associated with those of 18,21 transcription factor genes wilm’s tumor (wt) 1 and dax1 (nr0b1). ff1b‑ expressing interrenal primordia originate within the wt1‑ expressing pronephric field, while wt1 expression is essential for the develop- ment of both pronephric and interrenal tissues. Well after the specification stage, dax1 gene is transiently expressed at interrenal tissue, and is required for the expression of steroidogenic genes cyp11a and star. While SF1 is known to interact with WT1 and 22-24 DAX1 in the mammalian systems, it is tempting to hypothesize that similar molecular interplays might occur in the early zebrafish embryo. Alternative splicing of WT1 results in -KTS and +KTS isoforms which differ in protein properties as well as developmental 25-27 roles. In mammals, only the -KTS form of WT1 is able to bind to and transactivate Sf1 promoter, or to interact physically with SF1 to promote MIS expression. Splice variants with and without the KTS tripeptide-encoding sequence have been found for both wt1a and wt1b, the two WT1 homologues identified in zebrafish. However, the biochemical properties of these wt1 variants, in terms of their interaction with Ff1b or regulation upon ff1b promoter, have remained unclear. DAX1 is a corepressor for several nuclear receptors involved in the steroidogenic axis, notably SF1. DAX1 23,24 negatively regulates the transcriptional activities of SF1, as well as antagonizing the synergistic action between SF1 and heterodimeric partners such as WT1. While LXXLL-related motifs are necessary for the corepressing activities of DAX1, the zebrafish and tilapia Figure 3. (A–F) Interaction of interrenal and endothelial cells as revealed in Y1 Tg(fli1:EGFP) transgenic zebrafish. Single confocal sections showing the dax1 sequences lack the first and second of four LXXLL motifs interrenal tissues as stained by 3b‑Hsd activity assay (left panel: A and D), seen in mammals. It remains unclear whether these teleostean and the neighboring ECs as labeled by the green fluorescence (middle panel: Dax1 proteins could exert similar corepressing activities as their Y1 B and E), of the Tg(fli1:EGFP) embryos while staged at 29 hpf (A–C) and mammalian counterparts. 76 hpf (D–F) respectively. The merged images of 3b‑Hsd activity and GFP The homeodomain protein Prox1 has however been confirmed as are shown in the right panel (C and F). (A–C) are lateral views with anterior a novel Ff1b corepressor, and expressed at the developing zebrafish oriented to the right. (D–F) are dorsal views with anterior oriented to the interrenal tissue. Both prox1 and dax1 appear to function down- top. The interrenal cells are in close contact with ECs that are engaged in axial vessel assembly. PCV, posterior cardinal vein. Red arrowheads stream of ff1b in interrenal development, and to be implied in 21,32 indicate interrenal tissues, while yellow arrowheads indicate kidney steroidogenesis. While dax1 is only transiently expressed at m39 glomeruli. Bar, 50 mM. (G and H) ff1b expression in the clo mutant and around 32 hpf, prox1 expression at interrenal tissue starts from 28 m39 its wild type sibling. Embryos of clo mutant (H) and its wild‑type sibling hpf and persists up to three days post-fertilization (dpf ). Both prox1 (WT; G) were labeled by in situ hybridization for ff1b (dark blue) at 55 hpf. and dax1 morphants display reduced numbers of steroidogenic cells. Dorsal views of embryos are shown, with anterior oriented to the top. The m39 Although no similar coregulation of SF-1 by mammalian Prox1 has central migration of interrenal tissue is arrested in clo , resulting in persis‑ been reported, Prox1 was interestingly found to corepress another tent distribution of a pair of cell clusters on either side of midline. Reproduced with permission. Ftz-F1 protein Liver Receptor Homolog-1 (LRH-1; NR5A2), and thus suppress LRH-1-mediated activation of cholesterol 7-a-hydrox- 33,34 ylase gene. Both mammalian and zebrafish Prox1 proteins are cells (ECs) invading pronephros, by sprouting of dorsal aorta, are interacting physically with Ftz-F1s via LXXLL-related motifs. These regulated by blood circulation to express matrix-metalloproteinase-2, studies indicate that the corepressor function of Prox1 upon Ftz-F1 which in turn mediates the assembly of bilateral glomeruli at midline. appears to be conserved across the vertebrate species, yet diversified However, hemodynamic force does not contribute to the central in terms of the profile of target genes regulated. fusion of bilateral interrenal primordia, despite the close associa- Interrenal steroidogenesis. The interrenal tissue is the major tion of pronephros and interrenal tissue in the early embryo. In site of steroidogenesis in most teleosts, as is the adrenal cortex in 14,35 fact, the interrenal migration and fusion is normal even as axial mammals. In zebrafish, many steroidogenic genes have been vessel assembly or angiogenesis is severely compromised. However, cloned and identified, including side chain cleavage enzyme cyp11a1 36,37 38 interestingly, the interrenal central convergence is disrupted in the (p540scc) and steroidogenic acute regulatory protein (star), endothelium-free mutant cloche (clo; Fig. 3G and H), and can be both are known to mediate the rate-limiting steps of steroidogen- rescued while endothelium near interrenal area is partially restored esis. Cyp11a1 catalyzes the first step of adrenal steroidogenesis, by the forced expression of the Scl transcription factor. This argues while StAR regulates cholesterol shuttling across the mitochondrial for a role of endothelial signaling in guiding interrenal migration, membrane and the acute steroid production. Both cyp11a1 and star and provides one of the few pieces of evidence that beyond the are expressed at embryonic interrenal tissue, starting from approxi- vascular functions in supporting cell growth, tissue maintenance and mately 24 hpf, shortly after the specification and central convergence endocrine secretion, endothelium also plays a morphogenetic role in of interrenal primordia. However, the functional differentia- endocrine development. tion of interrenal tissue, marked by the chromogenic detection of e3 Organogenesis 2007; Vol. 3 Issue 1 ©2007 LANDES BIOSCIENCE. DO NOT DISTRIBUTE. Interrenal Organogenesis in the Zebrafish Model 3-beta-Hydroxysteroid dehydrogenase (3b-Hsd) enzymatic activity, specific markers for steroidogenic cells will allow chemical mutagen- esis screens for the discovery of novel genes associated with interrenal is not initiated until about 28 hpf. The expressions of steroidogenic genes are abolished upon the knockdown of Ff1b by antisense disorders, such as interrenal hypoplasia. Therefore the zebrafish interrenal model is promising to provide insights on the interplay morpholino injection, implying their direct transcriptional regulation 16,18 by Ff1b protein. In addition, the transcripts of cyp11a and star among gene, development and disease of mammalian adrenal gland, and even a platform for pharmaceutical screenings targeting adrenal are down-regulated at the interrenal tissue of dax1 morphant, while 21,32 the enzymatic activity of 3b-Hsd is reduced in prox1 morphant. functions. Collectively, the interrenal steoridogenesis in zebrafish embryo might References be mediated by a combinatorial action of transcriptional regulators. 1. Grunwald DJ, Eisen JS. Headwaters of the zebrafish—Emergence of a new model verte- brate. Nat Rev Genet 2002; 3:717-24. The gene expressions associated with pituitary control of interrenal 40,41 2. 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DAX-1 inhibits SF-1-mediated transactivation via a carboxy-ter- develop, forward genetic approach using zebrafish might help to minal domain that is deleted in adrenal hypoplasia congenita. Mol Cell Biol 1997; 17:1476-83. identify the unknown signal(s) that instruct migration and matura- 24. Crawford PA, Dorn C, Sadovsky Y, Milbrandt J. Nuclear receptor DAX-1 recruits nuclear tion of chromaffin cells. receptor corepressor N-CoR to steroidogenic factor 1. Mol Cell Biol 1998; 18:2949-56. 25. Haber DA, Sohn RL, Buckler AJ, Pelletier J, Call KM, Housman DE. Alternative splicing and genomic structure of the Wilms tumor gene WT1. Proc Natl Acad Sci USA 1991; c onc Lud Ing r em Ar Ks 88:9618-22. 26. Englert C. WT1—more than a transcription factor? Trends Biochem Sci 1998; 23:389-93. Since the identification of the ff1b gene, subsequent studies in 27. Hammes A, Guo JK, Lutsch G, Leheste JR, Landrock D, Ziegler U, Gubler MC, Schedl A. various groups combined to demonstrate that interrenal development Two splice variants of the Wilms’ tumor 1 gene have distinct functions during sex determina- in the zebrafish shares many conserved molecular and developmental tion and nephron formation. Cell 2001; 106:319-29. 28. Wilhelm D, Englert C. The Wilms tumor suppressor WT1 regulates early gonad develop- mechanisms with higher vertebrates. Moreover, various morphants ment by activation of Sf1. Genes Dev 2002; 16:1839-51. and genetic mutants can be successfully used to manipulate molec- 29. Bollig F, Mehringer R, Perner B, Hartung C, Schafer M, Schartl M, Volff JN, Winkler C, ular, cellular and hormonal signalings, for dissection of the regulatory Englert C. Identification and comparative expression analysis of a second wt1 gene in zebraf- ish. Dev Dyn 2006; 235:554-61. network that directs interrenal organogenesis. 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The pro-opiomelanocortin gene of the zebrafish (Danio rerio). Biochem Biophys Res Commun 2003; 303:1121-8. 41. Liu NA, Huang H, Yang Z, Herzog W, Hammerschmidt M, Lin S, Melmed S. Pituitary corticotroph ontogeny and regulation in transgenic zebrafish. Mol Endocrinol 2003; 17:959-66. 42. Logan DW, Bryson-Richardson RJ, Taylor MS, Currie P, Jackson IJ. Sequence characteriza- tion of teleost fish melanocortin receptors. Ann N Y Acad Sci 2003; 994:319-30. 43. Karpac J, Ostwald D, Bui S, Hunnewell P, Shankar M, Hochgeschwender U. Development, maintenance, and function of the adrenal gland in early postnatal proopiomelanocortin-null mutant mice. Endocrinology 2005; 146:2555-62. 44. Coll AP, Challis BG, Yeo GS, Snell K, Piper SJ, Halsall D, Thresher RR, O’Rahilly S. The effects of proopiomelanocortin deficiency on murine adrenal development and responsive- ness to adrenocorticotropin. Endocrinology 2004; 145:4721-7. 45. An M, Luo R, Henion PD. Differentiation and maturation of zebrafish dorsal root and sympathetic ganglion neurons. J Comp Neurol 2002; 446:267-75. 46. Unsicker K, Huber K, Schutz G, Kalcheim C. The chromaffin cell and its development. Neurochem Res 2005; 30:921-5. 47. Huber K. The sympathoadrenal cell lineage: Specification, diversification, and new perspec- tives. Dev Biol 2006; 298:335-43. e5 Organogenesis 2007; Vol. 3 Issue 1 ©2007 LANDES BIOSCIENCE. DO NOT DISTRIBUTE. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Organogenesis Taylor & Francis

Interrenal Organogenesis in the Zebrafish Model

Yi-Wen, Liu
Organogenesis , Volume 3 (1): 5 – Jan 1, 2007
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Taylor & Francis
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Copyright © 2007 Landes Bioscience
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1555-8592
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Abstract

[Organogenesis 3:1, e1-e5, EPUB Ahead of Print: http://www.landesbioscience.com/journals/organogenesis/abstract.php?id=3965; 1 January 2007]; ©2007 Landes Bioscience Review Yi-Wen Liu Abstr Act In recent years, many genes that participate in the specification, differentiation and *Correspondence to: Liu Yi-Wen; Department of Life Science; Tunghai University; No. 181, Sec. 3; Taichung-Kan Road; Taichung 40704 Taiwan, steroidogenesis of the interrenal organ, the teleostean homologue of the adrenal cortex, ROC; Tel.: +886.4.2359.0121 ext. 2466; Fax: +886.4.2359.0296; have been identified and characterized in zebrafish. In‑depth studies of these genes Email: [email protected] have helped to delineate the morphogenetic steps of interrenal organ formation, as well This manuscript has been published online, prior to printing for Organogenesis, as some of the molecular and cellular mechanisms that govern these processes. The co‑ Volume 3, Issue 1. Definitive page numbers have not been assigned. The current development of interrenal tissue with the embryonic kidney (pronephros), surrounding citation is: Organogenesis 2007; 3(1): endothelium and invading chromaffin cells has been analyzed, by virtue of the amenability http://www.landesbioscience.com/journals/organogenesis/abstract.php?id=3965 of zebrafish embryos to a variety of genetic, developmental and histological approaches. Once the issue is complete and page numbers have been assigned, the citation will change accordingly. Moreover, zebrafish embryos can be subject to molecular as well as biochemical assays for the unraveling of the transcriptional regulation program underlying interrenal develop‑ ment. To this end, the key mechanisms that control organogenesis and steroidogenesis of KeY Words the zebrafish interrenal gland have been shown to resemble those in mammals, justifying interrenal, adrenal, pronephros, endothelium, the future utilization of zebrafish model for discovering novel genes associated with chromaffin, organogenesis, zebrafish adrenal development and disease. Ac Kno WLedgements The author would like to thank Dr. Woon- Introduct Ion Khiong Chan and Dr. Chou Chai for pioneering work on zebrafish interrenal The external fertilization and rapid development of the zebrafish embryo has made organ; Prof. Bon-chu Chung and her team it suitable for studying early vertebrate development. Due to the permeability and for inspiring discussions. This work was optic transparency of the zebrafish embryo, developing organ primordia in the whole supported by grants NSC94-2320-B-029-001 mount specimen can be readily detected by histochemistry, immunohistochemistry or and NSC95-2311-B-029-008 from National in situ hybridizations. Various cell types that integrate to constitute specific organs, Science Council (R.O.C). such as embryonic heart and kidney, can be labeled simultaneously by a combination of 3,4 histological approaches. Hence, the zebrafish is particularly useful for capitulating the dynamic processes of organ formation, especially cell migration events or morphogenetic movements of organ primordia. Furthermore, the establishment of transgenic fluorescent reporter lines has allowed the tracking of specific lineages as well as dissection of cellular processes with high resolution. For example, endothelium-specific transgenic reporter lines have enabled the elucidation of mechanisms underlying vessel formation, angiogen- 5-7 esis and endothelial tube assembly. Zebrafish mutants that are generated from either forward or reverse genetic approaches have offered great opportunity for understanding the interrelationships among gene, 8,9 development and disease. Large-scale chemical mutagenesis screens have identified numerous mutants with a wide spectrum of defects manifested in various organs, helping to elucidate specific signaling pathways leading to organogenesis such as heart and blood formation. The advent of antisense morpholino oligo knockdown approach, proven effec- tive and specific in the zebrafish embryo, has further facilitated the developmental analysis for any candidate genes of interest. Although the endocrine gland structures of fish and mammals are largely different, their developmental processes in organogenesis appear to share high similarities. Also, endocrine function is well conserved between teleosts and mammals, which could be reflected by the profiles of hormones, hormone receptors as well as transcriptional regu- lators. Interestingly, some zebrafish mutants or morphants faithfully phenocopy human endocrine disorders such as combined pituitary hormone deficiencies and neonatal diabetes mellitus. Hence, they promise to provide insights into the molecular etiology of their human disease counterparts. This short review highlights the teleostean counterpart of mammalian adrenal gland, the interrenal gland, based on recent findings in the zebrafish model. The ontogeny, e1 Organogenesis 2007; Vol. 3 Issue 1 ©2007 LANDES BIOSCIENCE. DO NOT DISTRIBUTE. Interrenal Organogenesis in the Zebrafish Model Figure 1. The detection of steroidogenic interrenal tissue by whole‑mount chromogenic 3b‑Hsd enzymatic activity assay in wild‑type control (upper panel) and ff1b antisense morpholino (ff1bMO) injected (lower panel) embryos. The embryos were treated with 0.003% phenylthiourea from 12 hpf onwards to prevent pigmentation. Dorso‑lateral views of embryos at 2 dpf are shown with anterior oriented to the right. The steroidogenic interre‑ nal cells are completely ablated in ff1b morphant. Red arrowhead indicates interrenal tissue (IR), lying above yolk sac in the mid‑trunk region. molecular determinants, cell migrations and tissue-tissue interactions are outlined, in order to discuss the relevance of zebrafish interrenal organ to mammalian adrenal gland. m o Lecu LLAr And c eLLu LAr c ontro Ls of Interren AL Figure 2. Early morphogenetic processes in the interrenal development of zebrafish. The parallel migrations of interrenal tissue, pronephros and o rg Anogenes Is chromaffin cells in this diagram are depicted based on the results of ref‑ FF1b marks and determines the onset of interrenal tissue. The erences 18, 20 and 39. The panels represent dorsal views of embryos, mode of tissue organization for teleostean interrenal organ is distinct at the indicated stages, oriented with anterior to the top. Through the sequential stages of interrenal specification, migration, steroidogenesis and from that of mammalian adrenal gland. The interrenal cells inter- chromaffin cell invasion, an assembled interrenal organ is evident by 3 dpf. mingle with, rather than encapsulate, the chromaffin cells which NC, notochord; 2S and 3S, the second and third somite, respectively. are functional equivalent of the adrenal medulla, and the assembled organ is embedded at the anterior portion of the head kidney. However, the molecular determinants for specifying steroidogenic primordia (Fig. 2), while both pronephros and interrenal tissue are 4,18 lineages have proven to be highly conserved between teleosts and derived from intermediate mesoderm. The interrenal tissues then mammals. Two Ftz-F1 genes, ff1b (nr5a1a) and ff1d (nr5a1b), have migrate out of the pronephric fields, before the initiation of steroido- been identified in zebrafish to be co-orthologues of mammalian SF1/ genesis. After separation, the interrenal and pronephric tissues stay 15-17 Ad4BP (NR5A1). While SF1 is obligatorily required for both in close proximity to one another throughout development, and adrenal and gonadal development, ff1b and ff1d appear to function both undergo central migration followed by fusion. Temporally, the predominantly in interrenal tissue and gonads, respectively. ff1b is the convergence of bilateral interrenal primordia well precedes the central earliest molecular marker detected in the developing interrenal tissue assembly of pronephros. Interestingly, both pronephros and inter- of zebrafish embryo. The knockdown of Ff1b by the antisense renal tissue receive endothelium-derived signals, albeit via different 19,20 morpholino oligo approach led to specific ablation of interrenal cells, mechanisms, as guidance cues for central migration. as revealed by the loss of either functional differentiation (Fig. 1) or The central migration of pronephric primordia, starting at around interrenal-specific RNA transcripts, indicating that Ff1b is absolutely 30 hours post-fertilization (hpf ), is temporally correlated with the 4,18,20 required for the initiation of interrenal primordium. angiogenesis of paired glomeruli. In the meantime, the developing Pronephros vs. interrenal tissue: Parallel morphogenetic move‑ interrenal cells are tightly associated with endothelium (Fig. 3A–F). This ments under differential endothelium‑derived controls. Temporal central fusion of glomeruli is disrupted upon the perturbations of blood and spatial analyses revealed that early interrenal tissues arise as flow, either genetically or pharmaceutically, implying a role of hemody- bilateral clusters of non-steroidogenic cells within the pronephric namic force for glomerular morphogenesis. Indeed, the endothelial www.landesbioscience.com Organogenesis e2 ©2007 LANDES BIOSCIENCE. DO NOT DISTRIBUTE. Interrenal Organogenesis in the Zebrafish Model Molecular interplays within interrenal primordium. The expression of ff1b is spatially closely associated with those of 18,21 transcription factor genes wilm’s tumor (wt) 1 and dax1 (nr0b1). ff1b‑ expressing interrenal primordia originate within the wt1‑ expressing pronephric field, while wt1 expression is essential for the develop- ment of both pronephric and interrenal tissues. Well after the specification stage, dax1 gene is transiently expressed at interrenal tissue, and is required for the expression of steroidogenic genes cyp11a and star. While SF1 is known to interact with WT1 and 22-24 DAX1 in the mammalian systems, it is tempting to hypothesize that similar molecular interplays might occur in the early zebrafish embryo. Alternative splicing of WT1 results in -KTS and +KTS isoforms which differ in protein properties as well as developmental 25-27 roles. In mammals, only the -KTS form of WT1 is able to bind to and transactivate Sf1 promoter, or to interact physically with SF1 to promote MIS expression. Splice variants with and without the KTS tripeptide-encoding sequence have been found for both wt1a and wt1b, the two WT1 homologues identified in zebrafish. However, the biochemical properties of these wt1 variants, in terms of their interaction with Ff1b or regulation upon ff1b promoter, have remained unclear. DAX1 is a corepressor for several nuclear receptors involved in the steroidogenic axis, notably SF1. DAX1 23,24 negatively regulates the transcriptional activities of SF1, as well as antagonizing the synergistic action between SF1 and heterodimeric partners such as WT1. While LXXLL-related motifs are necessary for the corepressing activities of DAX1, the zebrafish and tilapia Figure 3. (A–F) Interaction of interrenal and endothelial cells as revealed in Y1 Tg(fli1:EGFP) transgenic zebrafish. Single confocal sections showing the dax1 sequences lack the first and second of four LXXLL motifs interrenal tissues as stained by 3b‑Hsd activity assay (left panel: A and D), seen in mammals. It remains unclear whether these teleostean and the neighboring ECs as labeled by the green fluorescence (middle panel: Dax1 proteins could exert similar corepressing activities as their Y1 B and E), of the Tg(fli1:EGFP) embryos while staged at 29 hpf (A–C) and mammalian counterparts. 76 hpf (D–F) respectively. The merged images of 3b‑Hsd activity and GFP The homeodomain protein Prox1 has however been confirmed as are shown in the right panel (C and F). (A–C) are lateral views with anterior a novel Ff1b corepressor, and expressed at the developing zebrafish oriented to the right. (D–F) are dorsal views with anterior oriented to the interrenal tissue. Both prox1 and dax1 appear to function down- top. The interrenal cells are in close contact with ECs that are engaged in axial vessel assembly. PCV, posterior cardinal vein. Red arrowheads stream of ff1b in interrenal development, and to be implied in 21,32 indicate interrenal tissues, while yellow arrowheads indicate kidney steroidogenesis. While dax1 is only transiently expressed at m39 glomeruli. Bar, 50 mM. (G and H) ff1b expression in the clo mutant and around 32 hpf, prox1 expression at interrenal tissue starts from 28 m39 its wild type sibling. Embryos of clo mutant (H) and its wild‑type sibling hpf and persists up to three days post-fertilization (dpf ). Both prox1 (WT; G) were labeled by in situ hybridization for ff1b (dark blue) at 55 hpf. and dax1 morphants display reduced numbers of steroidogenic cells. Dorsal views of embryos are shown, with anterior oriented to the top. The m39 Although no similar coregulation of SF-1 by mammalian Prox1 has central migration of interrenal tissue is arrested in clo , resulting in persis‑ been reported, Prox1 was interestingly found to corepress another tent distribution of a pair of cell clusters on either side of midline. Reproduced with permission. Ftz-F1 protein Liver Receptor Homolog-1 (LRH-1; NR5A2), and thus suppress LRH-1-mediated activation of cholesterol 7-a-hydrox- 33,34 ylase gene. Both mammalian and zebrafish Prox1 proteins are cells (ECs) invading pronephros, by sprouting of dorsal aorta, are interacting physically with Ftz-F1s via LXXLL-related motifs. These regulated by blood circulation to express matrix-metalloproteinase-2, studies indicate that the corepressor function of Prox1 upon Ftz-F1 which in turn mediates the assembly of bilateral glomeruli at midline. appears to be conserved across the vertebrate species, yet diversified However, hemodynamic force does not contribute to the central in terms of the profile of target genes regulated. fusion of bilateral interrenal primordia, despite the close associa- Interrenal steroidogenesis. The interrenal tissue is the major tion of pronephros and interrenal tissue in the early embryo. In site of steroidogenesis in most teleosts, as is the adrenal cortex in 14,35 fact, the interrenal migration and fusion is normal even as axial mammals. In zebrafish, many steroidogenic genes have been vessel assembly or angiogenesis is severely compromised. However, cloned and identified, including side chain cleavage enzyme cyp11a1 36,37 38 interestingly, the interrenal central convergence is disrupted in the (p540scc) and steroidogenic acute regulatory protein (star), endothelium-free mutant cloche (clo; Fig. 3G and H), and can be both are known to mediate the rate-limiting steps of steroidogen- rescued while endothelium near interrenal area is partially restored esis. Cyp11a1 catalyzes the first step of adrenal steroidogenesis, by the forced expression of the Scl transcription factor. This argues while StAR regulates cholesterol shuttling across the mitochondrial for a role of endothelial signaling in guiding interrenal migration, membrane and the acute steroid production. Both cyp11a1 and star and provides one of the few pieces of evidence that beyond the are expressed at embryonic interrenal tissue, starting from approxi- vascular functions in supporting cell growth, tissue maintenance and mately 24 hpf, shortly after the specification and central convergence endocrine secretion, endothelium also plays a morphogenetic role in of interrenal primordia. However, the functional differentia- endocrine development. tion of interrenal tissue, marked by the chromogenic detection of e3 Organogenesis 2007; Vol. 3 Issue 1 ©2007 LANDES BIOSCIENCE. DO NOT DISTRIBUTE. Interrenal Organogenesis in the Zebrafish Model 3-beta-Hydroxysteroid dehydrogenase (3b-Hsd) enzymatic activity, specific markers for steroidogenic cells will allow chemical mutagen- esis screens for the discovery of novel genes associated with interrenal is not initiated until about 28 hpf. 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Published: Jan 1, 2007

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