Normal Table of Xenopus development: a new graphical resource

Abstract

Normal tables of development are essential for studies of embryogenesis, serving as an important resource for model organisms, including the frog Xenopus laevis. Xenopus has long been used to study developmental and cell biology, and is an increasingly important model for human birth defects and disease, genomics, proteomics and toxicology. Scientists utilize Nieuwkoop and Faber's classic ‘Normal Table of Xenopus laevis (Daudin)’ and accompanying illustrations to enable experimental reproducibility and reuse the illustrations in new publications and teaching. However, it is no longer possible to obtain permission for these copyrighted illustrations. We present 133 new, high-quality illustrations of X. laevis development from fertilization to metamorphosis, with additional views that were not available in the original collection. All the images are available on Xenbase, the Xenopus knowledgebase (http://www.xenbase.org/entry/zahn.do), for download and reuse under an attributable, non-commercial creative commons license. Additionally, we have compiled a ‘Landmarks Table’ of key morphological features and marker gene expression that can be used to distinguish stages quickly and reliably (https://www.xenbase.org/entry/landmarks-table.do). This new open-access resource will facilitate Xenopus research and teaching in the decades to come.

References 91

1. 1.

   Almasoudi, S. H. and Schlosser, G. (2021 ). Otic neurogenesis in Xenopus laevis: proliferation, differentiation, and the role of Eya1. Front. Neuroanat. 15, 722374.

   Not in our library10.3389/fnana.2021.722374

2. 2.

   Aztekin, C., Hiscock, T. W., Gurdon, J., Jullien, J., Marioni, J. and Simons, B. D. (2021 ). Secreted inhibitors drive the loss of regeneration competence in Xenopus limbs. Development 148, dev199158.

   Not in our library10.1242/dev.199158

3. 3.

   Babalola, O. O., Truter, J. C. and Van Wyk, J. H. (2021 ). Lethal and teratogenic impacts of imazapyr, diquat dibromide, and glufosinate ammonium herbicide formulations using frog embryo teratogenesis assay-Xenopus (FETAX). Arch. Environ. Contam. Toxicol. 80, 708-716.

   Not in our library10.1007/s00244-020-00756-5

4. 4.

   Bard, J. (2012 ). A new ontology (structured hierarchy) of human developmental anatomy for the first 7 weeks (Carnegie stages 1-20). J. Anat. 221, 406-416.

   Not in our library10.1111/j.1469-7580.2012.01566.x

5. 5.

   Battistoni, M., Bacchetta, R., Di Renzo, F., Metruccio, F. and Menegola, E. (2020 ). Effect of nano-encapsulation of beta-carotene on Xenopus laevis embryos development (FETAX). Toxicol. Rep. 7, 510-519.

   Not in our library10.1016/j.toxrep.2020.04.004

6. 6.

   Beckers, A., Fuhl, F., Ott, T., Boldt, K., Brislinger, M. M., Walentek, P., Schuster-Gossler, K., Hegermann, J., Alten, L., Kremmer, E. et al. (2021 ). The highly conserved FOXJ1 target CFAP161 is dispensable for motile ciliary function in mouse and Xenopus. Sci. Rep. 11, 13333.

   Not in our library10.1038/s41598-021-92495-3

7. 7.

   Bergmann, C., Fliegauf, M., Bruchle, N. O., Frank, V., Olbrich, H., Kirschner, J., Schermer, B., Schmedding, I., Kispert, A., Kranzlin, B. et al. (2008 ). Loss of nephrocystin-3 function can cause embryonic lethality, Meckel-Gruber-like syndrome, situs inversus, and renal-hepatic-pancreatic dysplasia. Am. J. Hum. Genet. 82, 959-970.

   Not in our library10.1016/j.ajhg.2008.02.017

8. 8.

   Betley, J. N., Frith, M. C., Graber, J. H., Choo, S. and Deshler, J. O. (2002 ). A ubiquitous and conserved signal for RNA localization in chordates. Curr. Biol. 12, 1756-1761.

   Not in our library10.1016/s0960-9822(02)01220-4

9. 9.

   Breckenridge, R. A., Mohun, T. J. and Amaya, E. (2001 ). A role for BMP signalling in heart looping morphogenesis in Xenopus. Dev. Biol. 232, 191-203.

   Not in our library10.1006/dbio.2001.0164

10. 10.

    Brivanlou, A. H. and Harland, R. M. (1989 ). Expression of an engrailed-related protein is induced in the anterior neural ectoderm of early Xenopus embryos. Development 106, 611-617.

    Not in our library10.1242/dev.106.3.611

11. 11.

    Brown, D. D. and Cai, L. (2007 ). Amphibian metamorphosis. Dev. Biol. 306, 20-33.

    Not in our library10.1016/j.ydbio.2007.03.021

12. 12.

    Buchholz, D. R. and Shi, Y. B. (2018 ). Methods for investigating the larval period and metamorphosis in Xenopus. Cold Spring Harb. Protoc. 2018, pdb.top097667.

    Not in our library10.1101/pdb.top097667

13. 13.

    Choi, J., Ishizuya-Oka, A. and Buchholz, D. R. (2017 ). Growth, development, and intestinal remodeling occurs in the absence of thyroid hormone receptor alpha in tadpoles of Xenopus tropicalis. Endocrinology 158, 1623-1633.

    Not in our library10.1210/en.2016-1955

14. 14.
    Coordinated genomic control of ciliogenesis and cell movement by RFX2 · 2014

    No notice
15. 15.

    Cleaver, O., Tonissen, K. F., Saha, M. S. and Krieg, P. A. (1997 ). Neovascularization of the Xenopus embryo. Dev. Dyn. 210, 66-77. 10.1002/(SICI)1097-0177(199709)210:1<66::AID-AJA7>3.0.CO;2-#

    Not in our library10.1002/(sici)1097-0177(199709)210:1<66::aid-aja7>3.0.co;2-#

16. 16.

    Dang, Z. (2019 ). Endpoint sensitivity in amphibian metamorphosis assay. Ecotoxicol. Environ. Saf. 167, 513-519.

    Not in our library10.1016/j.ecoenv.2018.10.028

17. 17.

    De Bakker, B. S., Van Den Hoff, M. J. B., Vize, P. D. and Oostra, R. J. (2019 ). The pronephros; a fresh perspective. Integr. Comp. Biol. 59, 29-47.

    Not in our library10.1093/icb/icz001

18. 18.

    Dong, W., Lee, R. H., Xu, H., Yang, S., Pratt, K. G., Cao, V., Song, Y. K., Nurmikko, A. and Aizenman, C. D. (2009 ). Visual avoidance in Xenopus tadpoles is correlated with the maturation of visual responses in the optic tectum. J. Neurophysiol. 101, 803-815.

    Not in our library10.1152/jn.90848.2008

19. 19.

    Drysdale, T. A., Tonissen, K. F., Patterson, K. D., Crawford, M. J. and Krieg, P. A. (1994 ). Cardiac troponin I is a heart-specific marker in the Xenopus embryo: expression during abnormal heart morphogenesis. Dev. Biol. 165, 432-441.

    Not in our library10.1006/dbio.1994.1265

20. 20.

    Durston, A. J., Timmermans, J. P., Hage, W. J., Hendriks, H. F., De Vries, N. J., Heideveld, M. and Nieuwkoop, P. D. (1989 ). Retinoic acid causes an anteroposterior transformation in the developing central nervous system. Nature 340, 140-144.

    Not in our library10.1038/340140a0

21. 21.

    Dush, M. K. and Nascone-Yoder, N. M. (2019 ). Vangl2 coordinates cell rearrangements during gut elongation. Dev. Dyn. 248, 569-582.

    Not in our library10.1002/dvdy.61

22. 22.

    Fisher, M. E., Segerdell, E., Matentzoglu, N., Nenni, M. J., Fortriede, J. D., Chu, S., Pells, T. J., Osumi-Sutherland, D., Chaturvedi, P., James-Zorn, C. et al. (2022 ). The Xenopus phenotype ontology: bridging model organism phenotype data to human health and development. BMC Bioinformatics 23, 99.

    Not in our library10.1186/s12859-022-04636-8

23. 23.

    Fletcher, R. B. and Harland, R. M. (2008 ). The role of FGF signaling in the establishment and maintenance of mesodermal gene expression in Xenopus. Dev. Dyn. 237, 1243-1254.

    Not in our library10.1002/dvdy.21517

24. 24.

    Fort, D. J. and Mathis, M. (2018 ). Frog embryo teratogenesis Assay-Xenopus (FETAX): use in alternative preclinical safety assessment. Cold Spring Harb. Protoc. 2018.

    Not in our library10.1101/pdb.prot098319

25. 25.

    Gao, J. and Shen, W. (2021 ). Xenopus in revealing developmental toxicity and modeling human diseases. Environ. Pollut. 268, 115809.

    Not in our library10.1016/j.envpol.2020.115809

26. 26.

    Gawantka, V., Pollet, N., Delius, H., Vingron, M., Pfister, R., Nitsch, R., Blumenstock, C. and Niehrs, C. (1998 ). Gene expression screening in Xenopus identifies molecular pathways, predicts gene function and provides a global view of embryonic patterning. Mech. Dev. 77, 95-141.

    Not in our library10.1016/s0925-4773(98)00115-4

27. 27.

    Gur, M., Cohen, E. B.-T., Genin, O., Fainsod, A., Perles, Z. and Cinnamon, Y. (2017 ). Roles of the cilium-associated gene CCDC11 in left-right patterning and in laterality disorders in humans. Int. J. Dev. Biol. 61, 267-276.

    Not in our library10.1387/ijdb.160442yc

28. 28.

    Hausen, P. and Riebesell, M. (1991 ). The early development of Xenopus Laevis: an atlas of the histology. Verlag der Zeitschrift für Naturforschung, Tügingen.

    Not in our library10.1023/a:1024445010789

29. 29.

    Heller, N. and Brändli, A. W. (1997 ). Xenopus Pax-2 displays multiple splice forms during embryogenesis and pronephric kidney development. Mech. Dev. 69, 83-104.

    Not in our library10.1016/s0925-4773(97)00158-5

30. 30.

    Hoppler, S. and Conlon, F. L. (2020 ). Xenopus: experimental access to cardiovascular development, regeneration discovery, and cardiovascular heart-defect modeling. Cold Spring Harb. Perspect Biol 12, a037200.

    Not in our library10.1101/cshperspect.a037200

31. 31.

    Hopwood, N. (2007 ). A history of normal plates, tables and stages in vertebrate embryology. Int. J. Dev. Biol. 51, 1-26.

    Not in our library10.1387/ijdb.062189nh

32. 32.

    Hopwood, N. D., Pluck, A., Gurdon, J. B. and Dilworth, S. M. (1992 ). Expression of XMyoD protein in early Xenopus laevis embryos. Development 114, 31-38.

    Not in our library10.1242/dev.114.1.31

33. 33.

    Hunter, A., Kaufman, M. H., McKay, A., Baldock, R., Simmen, M. W. and Bard, J. B. (2003 ). An ontology of human developmental anatomy. J. Anat. 203, 347-355.

    Not in our library10.1046/j.1469-7580.2003.00224.x

34. 34.

    Illes, J. C., Winterbottom, E. and Isaacs, H. V. (2009 ). Cloning and expression analysis of the anterior parahox genes, Gsh1 and Gsh2 from Xenopus tropicalis. Dev. Dyn. 238, 194-203.

    Not in our library10.1002/dvdy.21816

35. 35.

    Islas-Flores, H., Pérez-Alvarez, I. and Gómez-Oliván, L. M. (2018 ). Evaluation of teratogenicity of pharmaceuticals using FETAX. Methods Mol. Biol. 1797, 299-307.

    Not in our library10.1007/978-1-4939-7883-0_15

36. 36.

    James-Zorn, C., Ponferrada, V., Fisher, M. E., Burns, K., Fortriede, J., Segerdell, E., Karimi, K., Lotay, V., Wang, D. Z., Chu, S. et al. (2018 ). Navigating Xenbase: an integrated Xenopus genomics and gene expression database. Methods Mol. Biol. 1757, 251-305.

    Not in our library10.1007/978-1-4939-7737-6_10

37. 37.

    Kazanskaya, O., Ohkawara, B., Heroult, M., Wu, W., Maltry, N., Augustin, H. G. and Niehrs, C. (2008 ). The Wnt signaling regulator R-spondin 3 promotes angioblast and vascular development. Development 135, 3655-3664.

    Not in our library10.1242/dev.027284

38. 38.

    Keller, R. and Sutherland, A. (2020 ). Convergent extension in the amphibian, Xenopus laevis. Curr. Top. Dev. Biol. 136, 271-317.

    Not in our library10.1016/bs.ctdb.2019.11.013

39. 39.

    Kelley, C., Yee, K., Harland, R. and Zon, L. I. (1994 ). Ventral expression of GATA-1 and GATA-2 in the Xenopus embryo defines induction of hematopoietic mesoderm. Dev. Biol. 165, 193-205.

    Not in our library10.1006/dbio.1994.1246

40. 40.

    Kennedy, A. E. and Dickinson, A. J. (2012 ). Median facial clefts in Xenopus laevis: roles of retinoic acid signaling and homeobox genes. Dev. Biol. 365, 229-240.

    Not in our library10.1016/j.ydbio.2012.02.033

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