Keywords:  GRHL1, zebrafish, desmosom, hair cell, DSG1

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EHU/UPV/UBC - The International Journal of Developmental Biology 59: 425-433  (2015)
doi: 10.1387/ijdb.150137db      /      © UBC Press        ( www.a360grados.net )

T-cell internal antigen 1 counteracts somatic RNA degradation during early Xenopus embryogenesis
Diana Bauermeister, Maike Claußen and Tomas Pieler

Institute of Developmental Biochemistry, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, Germany

Abstract: In Xenopus laevis, maternal transcripts that localize to the vegetal cortex of the oocyte are specifically inherited by prospective germ cells during cleavage stages. While a large fraction of maternal transcripts is degraded during the maternal to zygotic transition (MZT), transcripts associated with the germ-line are stable. A sequence in the dead end 1 3’UTR mediates vegetal localization in the oocyte as well as miR mediated clearance in somatic cells and germ cell specific stabilization during the MZT in embryos. We could identify Tia1 to co-precipitate with known components of vegetal localization RNPs in X. laevis oocytes. Tia1 interacts and co-localizes with various localization elements from vegetally localizing RNAs. In X. laevis embryos, ectopic expression of Tia1 counteracts somatic degradation of dnd1 localization element reporter RNAs and it can synergize with Dnd1 protein in reporter RNA stabilization. Ectopic Tia1 also protects several endogenous localizing and germ cell specific mRNAs from somatic degradation. Thus, proteins that protect germ-line transcripts from miR mediated decay during the MZT in embryos might bind these RNAs already in the oocyte.

Keywords:  primordial germ cell, microrna, rna localization, vegetal, germline

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EHU/UPV/UBC - The International Journal of Developmental Biology 59: 435-442  (2015)
doi: 10.1387/ijdb.150310ht      /      © UBC Press        ( www.a360grados.net )

Ras-Related Nuclear Protein is required for late developmental stages of retinal cells in zebrafish eyes
Cheng-Yung Lin¹, Hsing-Yen Huang², Po-Nien Lu², Chien-Wei Lin², Kuang-Ming Lu² and Huai-Jen Tsai¹

¹Institute of Biomedical Sciences, Mackay Medical College, New Taipei City and ²Institute of Molecular and Cellular Biology, National Taiwan University, Taipei, Taiwan

Abstract: Ras-related nuclear protein (Ran) is involved in cell division by regulating nucleocytoplasmic transport and modulating the assembly of tubulin. However, its function in embryonic development is unclear. We used zebrafish to study the roles of Ran in eye development. The ran transcripts were restrictedly expressed in head and eyes after the pharyngula stage. The microphthalmos, in which no ordered layers with differentiated retinal cells were detected, was observed in the ran-deficient embryos. They exhibited faster decline cyclinD1-expressed cells, suggesting that cell cycle regulation in retinae was defective. The apoptotic signals in the retinae of ran-deficient embryos remained low at early (24 hpf) stage. Early eye field specification markers, rx1 and pax6, were only slightly affected, and markers for establishing axon migration, fgf8 and pax2, were normally expressed, suggesting Ran is not required in the early stages of eye development. However, the early optic nerve differentiation marker p57kip2 was not expressed at middle (48 hpf) and late (72 hpf) stages. We also observed a decrease in the retinal neuron proteins HuC and Neurolin. The proneural gene ath5, which first determines the cell fate of the developing ganglion cell layer, was undetectable. Furthermore, we found that Ran was associated with ADP-ribosylation factor-like protein 6-interacting protein 1 (Arl6ip1), which plays a role in retinal development, suggesting that Ran associates with Arl6ip1 to regulate retinal development. Therefore, while the effects of Ran are minimal during early specification of the eye field, Ran is required for proliferation and differentiation of retinal cells at later developmental stages.

Keywords:  Ran, zebrafish, retinal cells, eye development

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EHU/UPV/UBC - The International Journal of Developmental Biology 59: 443-451  (2015)
doi: 10.1387/ijdb.150040ds      /      © UBC Press        ( www.a360grados.net )

Direct regulation of siamois by VegT is required for axis formation in Xenopus embryo
Hong-Yan Li^1,2,3, Warif El Yakoubi^1,2 and De-Li Shi^1,2

¹Sorbonne Universités, UPMC Univ Paris 06, Institut de Biologie Paris-Seine (IBPS), UMR 7622, Laboratory of Developmental Biology, Paris, France, ²CNRS, IBPS, UMR 7622, Laboratory of Developmental Biology, Paris, France and ³Laboratory for Evolution and Development, Department of Marine Biology, Ocean University of China, Qingdao, China

Abstract: The homeobox gene siamois is one of the earliest genes expressed in the Spemann organizer and plays a critical role in the formation of the dorsoventral axis. It is directly regulated by maternal Wnt signalling and functions as an essential zygotic intermediary between maternal factors and the formation of the Spemann organizer. The maternal T domain transcription factor VegT interacts with Wnt signalling and is also involved in the formation of the Spemann organizer. However, the molecular mechanism of this functional interaction is not fully understood. Here we show that VegT is required for siamois expression through direct binding to the T-box binding sites in the siamois promoter. Mutational analysis of each of the five consensus T-box binding sites suggests that the proximal site close to the transcription start site is essential for activation of siamois promoter by VegT, while individual mutation of the four distal sites has no effect. VegT and Wnt signalling also functionally interact and are mutually required for siamois expression. In particular, VegT synergizes with Tcf1, but not Tcf3 and Tcf4, to induce siamois expression, and this is independent of Tcf/Lef-binding sites or the proximal T-box binding site in the siamois promoter. We further extend previous observations by showing that VegT cooperates with maternal Wnt signalling in the formation of the dorsoventral axis. These results demonstrate that maternal VegT directly regulates siamois gene transcription in the formation of the Spemann organizer, and provide further insight into the mechanism underlying the functional interaction between VegT and Wnt signalling during development.

Keywords:  Dorsoventral axis, VegT, siamois, Wnt, Xenopus

Short Communications        ------------------------

EHU/UPV/UBC - The International Journal of Developmental Biology 59: 453-460  (2015)
doi: 10.1387/ijdb.140287ct      /      © UBC Press        ( www.a360grados.net )

Chicken primordial germ cell motility in response to stem cell factor sensing
Thanida Srihawong^1,2, Takashi Kuwana³, Kannika Siripattarapravat⁴ and Chanin Tirawattanawanich⁵

¹Center for Agricultural Biotechnology, Kasetsart University, NakhonPathom, Thailand, ²Center of Excellence on Agricultural Biotechnology (AG-BIO/PERDO-CHE), Bangkok, Thailand, ³International Institute of Avian Conservation Science, MNC, Department of the President’s Affairs, United Arab Emirates, ⁴Department of Pathology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand and ⁵Department of Physiology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand

Abstract: Avian primordial germ cells (PGCs) are destined to migrate a long distance from their extra embryonic region via the vascular system to the gonadal ridges where they form the germ cells. Although PGC migration is crucial for a genetic continuation to the next generation, the factors and mechanisms that control their migration remain largely unknown. In the present study the chemotactic effect of stem cell factor (SCF) was examined on chicken blood circulating PGCs (cPGC), employing 3D chemotaxis slides and time-lapsed imaging analyses as an in vitro study model. Upon in vitro exposure to an SCF gradient, 77.1% (54 out of 70) of cPGCs showed a clear response, of which 48.1% (26 out of 54) polarized with the consecutive formation of a persistent membrane protrusion and significant directional migration towards the gradient and the others showed transient membrane protrusions. In contrast, the controls and apparently SCF unresponsive cPGCs and c-kit-negative red blood cells (RBCs) showed only cytoplasmic cycling with random formations of membrane blebbing and no directional migration. Significant (p< 0.05) differences between the SCF-treated and control cPGCs and RBCs were found in the migration parameters of eccentricity, accumulated and Euclidean distances, and migration velocity. The SCF-treated PGCs also revealed a chemotactic response, as judged by their significant displacement of center of mass and Rayleigh test. Complete inhibition of all the SCF-induced responses in PGCs was found following pretreatment of the cPGCs with 10 µM of the c-kit inhibitor, STI57l, prior to SCF exposure. In addition, cPGCs were found to be positive for c-kit expression using a polyclonal goat anti-mouse c-kit primary antibody, suggesting that the cPGCs were capable of SCF sensing and the potential involvement of SCF/c-kit in the chemotactic migration. Therefore, SCF is suggested to function as a chemoattractant in the migration of chicken cPGC.

Keywords:  Chicken primordial germ cell, chemotaxis, stem cell factor, c-kit receptor, migration

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EHU/UPV/UBC - The International Journal of Developmental Biology 59: 461-464  (2015)
doi: 10.1387/ijdb.150280dr      /      © UBC Press        ( www.a360grados.net )

Angiogenesis and hyperbaric oxygen in the chick embryo chorioallantoic membrane
Umberto Montecorboli^{1, 2}, Tiziana Annese², Christian Marinaccio² and Domenico Ribatti^{2, 3}

¹Unit of Hyperbaric Medicine, Ospedale “San Paolo”, ²Department of Basic Medical Sciences, Neurosciences, and Sensory Organs, University of Bari Medical School and ³National Cancer Institute “Giovanni Paolo II”, Bari, Italy

Abstract: Hyperbaric Oxygen Therapy (HBOT) is increasingly applied in different areas of medical practice. The oxy-hyperbarism effects are not well understood in cancer malignancy. One unique feature of cancer is the presence of hypoxic regions that are insensitive to conventional therapies. It is possible to alter the hypoxic state and produce reactive oxygen species for better treatment outcome by HBOT. In the present study, we determined the effects of HBOT on angiogenesis, a signature of cancer progression, by using the chick chorioallantoic membrane (CAM) in vivo assy. CAMs were exposed to 2.0 ATA (atmospheres absolute) for 30 min of hyperbaric oxygen on the 6^th and 7^th days of incubation (ED6, ED7). On the 10-11^th day of incubation, CAMs were excised from eggs, fixed and analysed using APERIO ImageScope software. HBOT outcomes were evaluated quantifying the volumetric area occupied by blood vessels and calculating the number of blood vessel ramifications. Results indicated that CAMs treated at ED6 and ED7 had a significantly higher CAM vascularization and an increased number of blood vessel ramifications (+82% higher for ED6) compared to untreated CAMs (ED6=63.3&PlusMinus;2.5 and ED7=57.7&PlusMinus;5.5 vs. CTRL=34.7&PlusMinus;2.5). Thus, HBOT induces an angiogenic response in treated CAMs through a classic sprouting mechanism.

Keywords:  angiogenesis, chorioallantoic membrane, hyperbaric oxygen

Technical Article          ----------------------

EHU/UPV/UBC - The International Journal of Developmental Biology 59: 465-470  (2015)
doi: 10.1387/ijdb.150008rg      /      © UBC Press        ( www.a360grados.net )

Visualization of primordial germ cells in the fertilized pelagic eggs of the barfin flounder Verasper moseri
Rie Goto¹, Taiju Saito¹, Yutaka Kawakami¹, Tomoe Kitauchi¹, Misae Takagi¹, Takashi Todo², Katsutoshi Arai² and Etsuro Yamaha¹

¹Nanae Fresh Water Laboratory, Field Science Center for Northern Biosphere, Hokkaido University, Nanae, Kameda, Hokkaido 041-1105 and ²Faculty of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido 041-8611, Japan

Abstract: Primordial germ cells (PGCs) appear during early embryogenesis and differentiate into gametes through oogenesis or spermatogenesis. Teleost PGCs can be visualized by injecting RNA transcribed from the fusion product of a fluorescent protein gene attached to the 3’ untranslated region (3’UTR) of zebrafish nanos3 (zf-nos3). Although this method has been widely applied to teleost PGCs, the visualization of PGCs in pelagic species that have eggs with a hard chorion is more problematic due to the technical difficulty of microinjection into their eggs. In this study, we developed a reliable method for microinjection of fertilized eggs in a pelagic species, the barfin flounder. Using a microneedle with a constriction “brake”, we were able to introduce gfp-nos3 3’UTR mRNA into embryos and to determine the migration route of PGCs. We also isolated the barfin flounder nos3 (bf-nos3) gene to compare its 3’UTR sequence with that of zebrafish. The 3’UTR of the bf-nos3 sequence was longer than that of zf-nos3. However, PGCs were also visualized after injection of gfp-bf-nos3 3’UTR mRNA both in zebrafish and barfin flounder. These results suggest that the function of nos3 is conserved between these species regardless of the sequence differences. The method developed here for labeling PGCs with gfp-nos3 mRNA will provide a means to study PGC development in the embryos of a wide range of marine fish species.

Keywords:  teleost, PGC, flounder, pelagic egg, microinjection

Developmental Expression Patterns         --------------------

EHU/UPV/UBC - The International Journal of Developmental Biology 59: 471-478  (2015)
doi: 10.1387/ijdb.150192ao      /      © UBC Press        ( www.a360grados.net )

Expression of Sox genes in tooth development
Katsushige Kawasaki^1,2, Maiko Kawasaki², Momoko Watanabe¹, Erik Idrus^1,3, Takahiro Nagai¹, Shelly Oommen², Takeyasu Maeda¹, Nobuko Hagiwara⁴, Jianwen Que⁵, Paul T. Sharpe² and Atsushi Ohazama^1,2

¹Division of Oral Anatomy, Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan, ²Department of Craniofacial Development and Stem Cell Biology, Dental Institute, King's College London, Guy's Hospital, London, UK, ³Division of Preventive Dentistry, Department of Oral Health Science, Niigata University, Graduate School of Medical and Dental Sciences, ⁴Division of Cardiovascular Medicine, UC Davis School of Medicine, Davis, CA, USA and ⁵Department of Medicine and Columbia Center for Human Development, Columbia University, New York, NY, USA

Abstract: Members of the Sox gene family play roles in many biological processes including organogenesis. We carried out comparative in situ hybridization analysis of seventeen sox genes (Sox1-14, 17, 18, 21) during murine odontogenesis from the epithelial thickening to the cytodifferentiation stages. Localized expression of five Sox genes (Sox6, 9, 13, 14 and 21) was observed in tooth bud epithelium. Sox13 showed restricted expression in the primary enamel knots. At the early bell stage, three Sox genes (Sox8, 11, 17 and 21) were expressed in pre-ameloblasts, whereas two others (Sox5 and 18) showed expression in odontoblasts. Sox genes thus showed a dynamic spatio-temporal expression during tooth development.

Keywords:  Sox, tooth development, in situ hybridization

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EHU/UPV/UBC - The International Journal of Developmental Biology 59: 479-485  (2015)
doi: 10.1387/ijdb.150086pr      /      © UBC Press        ( www.a360grados.net )

Conditional pulmonary over-expression of Claudin 6 during embryogenesis delays lung morphogenesis
Felix R. Jimenez, Samuel T. Belgique, Joshua B. Lewis, Scott A. Albright, Cameron M. Jones, Brian M. Howell, Aleksander P. Mika, Tyson R. Jergensen, Jason R. Gassman, Ryan J. Morris, Juan A. Arroyo and Paul R. Reynolds

Lung and Placenta Research Laboratory, Brigham Young University, Physiology and Developmental Biology, Provo, Utah, USA

Abstract: Claudin 6 (Cldn6) is a tetraspanin protein expressed by barrier epithelial cells. In order to assess the effects of persistent tight junctions involving Cldn6 during lung development, a doxycycline (dox)-inducible conditional transgenic mouse was generated that up-regulates Cldn6 in the distal lung. Pups had unlimited access to dox from conception until sacrifice date at embryonic day (E) 18.5. Quantitative PCR, immunoblotting, and immunohistochemistry revealed significantly elevated Cldn6 expression in transgenic mice compared to non-transgenic controls. There were no differences in terms of lung size, lung weight, or whole body weight at the time of necropsy. Histological evaluations led to the discovery that E18.5 Cldn6 transgenic pups appeared to be in the early canalicular stage of development coincident with fewer, thickened respiratory airspaces. In contrast, controls appeared to have entered the saccular stage characterized by thin airspace walls and spherical architecture. Immunostaining for transcriptional regulators including TTF-1 and FoxA2 was conducted to assess cell differentiation and specific cell types were identified via staining for pro-surfactant protein C (alveolar type II epithelial cells) or Clara Cell Secretory Protein (cub or Clara cells). Lastly, cell turnover was qualitatively measured via staining for cell proliferation or apoptosis. These data suggest that Cldn6 is an important junctional protein potentially involved in the programming of epithelial cells during lung development. Furthermore, genetic down-regulation of Cldn6 as development proceeds may influence differentiation observed in the transition from the canalicular to the saccular lung.

Keywords:  claudin 6, lung, transgenic, mouse

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EHU/UPV/UBC - The International Journal of Developmental Biology 59: 487-496  (2015)
doi: 10.1387/ijdb.150363cx      /      © UBC Press        ( www.a360grados.net )

iTRAQ-based proteomic analysis of adaptive response in the regenerating limb of the Cynops orientalis newt
Xiao-Fang Geng^1,2,3, Jian-Lin Guo^2,3,4, Xia-Yan Zang^2,3,4, Jing-Yan Sun^2,3,4, Peng-Fei Li^2,3,4, Fu-Chun Zhang¹ and Cun-Shuan Xu^2,3,4

¹Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi, ² State Key Laboratory Cultivation Base for Cell Differentiation Regulation, Henan Normal University, Xinxiang, ³Henan Engineering Laboratory for Bioengineering and Drug Development, Henan Normal University, Xinxiang and ⁴College of Life Science, Henan Normal University, Xinxiang, China

Abstract:  The newt has the powerful capacity to regenerate lost limbs following amputation, and represents an excellent model organism to study regenerative processes. However, the molecular basis of the adaptive response in the regenerating limb of the Chinese fire-bellied newt Cynops orientalis immediately after amputation remains unclear. To better understand the adaptive response immediately after limb amputation at the protein level, we used isobaric tags for relative and absolute quantitation (iTRAQ) coupled with LC-MS/MS methods to analyze changes in the proteome of the regenerating newt limb that occurred 2 h and 8 h after amputation. We identified 152 proteins with more than 1.5-fold change in expression compared to control. GO annotation analysis classified these proteins into several categories such as signaling, Ca²⁺ binding and translocation, transcription and translation, immune response, cell death, cytoskeleton, metabolism, etc. Further ingenuity pathway analysis (IPA) showed that several signaling pathways were significantly changed at 2 h and 8 h after amputation, including EIF2 signaling, acute phase response signaling, tight junction signaling and calcium signaling, suggesting these pathways may be closely related to the adaptive response immediately after limb amputation. This work provides novel insights into understanding the molecular processes related to newt limb regeneration immediately after amputation, and a basis for further study of regenerative medicine.

Keywords:  Cynops orientalis, limb regeneration, proteomic, stress response, cell death

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EHU/UPV/UBC - The International Journal of Developmental Biology 59: 497-503  (2015)
doi: 10.1387/ijdb.150124sf      /      © UBC Press        ( www.a360grados.net )

External ear microRNA expression profiles during mouse development
Leda Torres¹, Ulises Juárez^1,2, Laura García^3,4, Juan Miranda-Ríos⁴ and Sara Frias^1,5

¹Laboratorio de Citogenética, Depto. de Investigación en Genética Humana, Instituto Nacional de Pediatría, ²Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, ³Posgrado en Ciencias Biomédicas, Universidad Nacional Autónoma de México, ⁴Unidad de Genética de la Nutrición, Depto. Biología Molecular y Biotecnología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México e Instituto Nacional de Pediatría and ⁵Unidad de Genética de la Nutrición. Depto. Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México e Instituto Nacional de Pediatría, México DF, México

Abstract:  MicroRNAs (miRNAs) comprise a class of approximately 22 nucleotide regulatory non-coding RNAs that play several roles in diverse biological processes. Recent reports suggest that embryonic development in mammals is accompanied by dynamic changes in miRNA expression; however, there is no information regarding the role of miRNAs in the development of the external ear. The aim of this study was to determine the stage-specific expression of miRNAs during mouse external ear development in order to identify potentially implicated miRNAs along with their possible targets. miRNA expression profiles from fetal mice pinnae and back skin tissues at 13.5 dpc and 14.5 dpc were obtained using an Affymetrix GeneChip miRNA 3.0 array. Biological triplicates for both tissues, each collected from a litter averaging 16 fetuses, were analyzed. The results were analyzed with Affymetrix’s Transcriptome Analysis Console software to identify differentially expressed miRNAs. We observed differential expression of 40 miRNAs including some predicted to target genes implicated in external ear development, such as mmu-miR-10a, a miRNA known to modulate Hoxa1 mRNA levels, and mmu-miR-200c and mmu-miR-205. To our knowledge, this is the first miRNA expression profiling study of external ear development in mammals. These data could set the basis to understand the implications of miRNAs in normal external ear development.

Keywords:  miRNA, pinnae, auricle, microtia, GEO (GSE64945)

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EHU/UPV/UBC - The International Journal of Developmental Biology 59: 505-509  (2015)
doi: 10.1387/ijdb.150136pr      /      © UBC Press        ( www.a360grados.net )

CILP1 is dynamically expressed in the developing musculoskeletal system of the trout
Cécile Ralliere, Maxence Fretaud, Violette Thermes and Pierre-Yves Rescan

INRA, UR1037 LPGP Fish Physiology and Genomics, Rennes, France

Abstract:  An in situ screen for genes expressed in the skeletal muscle of eyed-stage trout embryos led to the identification of a transcript encoding a polypeptide related to CILP1, a secreted glycoprotein present in the extracellular matrix. In situ hybridisation in developing trout embryos revealed that CILP1 expression was initially detected in fast muscle progenitors of the early somite. Later, CILP1 expression was down-regulated medio-laterally in differentiating fast muscle cells, to become finally restricted to the undifferentiated muscle progenitors forming the dermomyotome-like epithelium at the surface of the embryonic myotome. At the completion of somitogenesis, CILP1 expression was concentrated in the myoseptal/tendon cells that develop between adjacent myotomes but was excluded from the skeletogenic cells of the vertebral axis to which the most medial myoseptal/tendon cells attach. Overall, our work shows that muscle cells and myoseptal/tendon cells contribute dynamically and cooperatively to the production of CILP1 during ontogeny of the trout musculoskeletal system.

Keywords:  CILP1, somite, myotome, dermomyotome, myoseptal cell, teleost

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EHU/UPV/UBC - The International Journal of Developmental Biology 59: 511-517  (2015)
doi: 10.1387/ijdb.150178xh      /      © UBC Press        ( www.a360grados.net )

Developmental expression of the N-myc downstream regulated gene (Ndrg) family during Xenopus tropicalis embryogenesis
Chao Zhong¹, Yan-Kuan Zhou¹, Shan-Shan Yang², Jun-Fang Zhao¹, Xiao-Long Zhu¹, Zhen-Huang Chen¹, Pei-Chao Chen², Li-Quan Huang¹ and Xiao Huang¹

¹College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang and ²College of Life and Environmental Science, Wenzhou University, Wenzhou, Zhejiang, PR China

Abstract:  The N-myc downstream regulated gene (Ndrg) family consists of four main members Ndrg1, 2, 3, and 4. The Ndrg genes are involved in many vital biological events including development. However, comprehensive expression patterns of this gene family during vertebrate embryogenesis remain largely unknown. Here, we analyzed the Ndrg family from the evolutionary perspective and examined the expression patterns of the Ndrg genes during Xenopus tropicalis embryogenesis. Different Ndrg family members of vertebrates are separated into different homology clusters which can be further classified into two groups and each Ndrg family member is well conserved during evolution. The temporal and spatial expression patterns of Ndrg1, 2, 3 and 4 are different during early Xenopus tropicalis development. Ndrg1, 2 and 4 are maternally expressed genes while Ndrg3 is a zygotically expressed gene. The Ndrg genes are differentially expressed in the developing central nervous system, the developing sensory organs, and the developing excretory organs. Moreover, they also show other specific expression domains. Our results indicate that the Ndrg genes exhibit specific expression patterns and may play different roles during vertebrate embryogenesis.

Keywords:  N-myc downstream regulated gene (Ndrg) family, Xenopus tropicalis, expression pattern, embryogenesis

The International Journal of Developmental Biology
ISSN 1696-3547 (online) and 0214-6282 (print)