Cell and Tissue Research

, Volume 369, Issue 1, pp 143–157 | Cite as

Toolbox in a tadpole: Xenopus for kidney research

Review

Abstract

Xenopus is a versatile model organism increasingly used to study organogenesis and genetic diseases. The rapid embryonic development, targeted injections, loss- and gain-of-function experiments and an increasing supply of tools for functional in vivo analysis are unique advantages of the Xenopus system. Here, we review the vast array of methods available that have facilitated its transition into a translational model. We will focus primarily on how these methods have been employed in the study of kidney development, renal function and kidney disease. Future advances in the fields of genome editing, imaging and quantitative ’omics approaches are likely to enable exciting and novel applications for Xenopus to deepen our understanding of core principles of renal development and molecular mechanisms of human kidney disease. Thus, using Xenopus in clinically relevant research diversifies the narrowing pool of “standard” model organisms and provides unique opportunities for translational research.

Keywords

Kidney disease Renal development Xenopus Ciliopathies Model organism 

Notes

Acknowledgements

This work was supported by the Emmy Noether Programme to SSL (LI1817/2-1) and Project B07 of the collaborative research initiative (SFB 1140) to SSL by the German Research Foundation (DFG).

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. Allen BG, Weeks DL (2006) Using phiC31 integrase to make transgenic Xenopus laevis embryos. Nat Protoc 1:1248–1257PubMedCrossRefGoogle Scholar
  2. Amaya E, Kroll KL (1999) A method for generating transgenic frog embryos. Methods Mol Biol 97:393–414PubMedGoogle Scholar
  3. Bergmann C, Fliegauf M, Bruchle NO, Frank V, Olbrich H, Kirschner J, Schermer B, Schmedding I, Kispert A, Kranzlin B, Nurnberg G, Becker C, Grimm T, Girschick G, Lynch SA, Kelehan P, Senderek J, Neuhaus TJ, Stallmach T, Zentgraf H, Nurnberg P, Gretz N, Lo C, Lienkamp S, Schafer T, Walz G, Benzing T, Zerres K, Omran H (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 82:959–970PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bhattacharya D, Marfo CA, Li D, Lane M, Khokha MK (2015) CRISPR/Cas9: An inexpensive, efficient loss of function tool to screen human disease genes in Xenopus. Dev Biol 408:196–204PubMedPubMedCentralCrossRefGoogle Scholar
  5. Blitz IL, Biesinger J, Xie X, Cho KW (2013) Biallelic genome modification in F(0) Xenopus tropicalis embryos using the CRISPR/Cas system. Genesis 51:827–834PubMedPubMedCentralCrossRefGoogle Scholar
  6. Blitz IL, Fish MB, Cho KW (2016) Leapfrogging: primordial germ cell transplantation permits recovery of CRISPR/Cas9-induced mutations in essential genes. Development 143:2868–2875PubMedCrossRefGoogle Scholar
  7. Blum M, Schweickert A, Vick P, Wright CV, Danilchik MV (2014) Symmetry breakage in the vertebrate embryo: when does it happen and how does it work? Dev Biol 393:109–123PubMedPubMedCentralCrossRefGoogle Scholar
  8. Blum M, De Robertis EM, Wallingford JB, Niehrs C (2015) Morpholinos: antisense and sensibility. Dev Cell 35:145–149PubMedCrossRefGoogle Scholar
  9. Bonham JR, Dale G, Scott D, Wagget J (1985) Molecular forms of acetylcholinesterase in Hirschsprung’s disease. Clin Chim Acta 145:297–305PubMedCrossRefGoogle Scholar
  10. Bonnard C, Strobl AC, Shboul M, Lee H, Merriman B, Nelson SF, Ababneh OH, Uz E, Guran T, Kayserili H, Hamamy H, Reversade B (2012) Mutations in IRX5 impair craniofacial development and germ cell migration via SDF1. Nat Genet 44:709–713PubMedCrossRefGoogle Scholar
  11. Boskovski MT, Yuan S, Pedersen NB, Goth CK, Makova S, Clausen H, Brueckner M, Khokha MK (2013) The heterotaxy gene GALNT11 glycosylates Notch to orchestrate cilia type and laterality. Nature 504:456–459PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bowes JB, Snyder KA, Segerdell E, Jarabek CJ, Azam K, Zorn AM, Vize PD (2010) Xenbase: gene expression and improved integration. Nucleic Acids Res 38:D607–D612PubMedCrossRefGoogle Scholar
  13. Braun DA, Sadowski CE, Kohl S, Lovric S, Astrinidis SA, Pabst WL, Gee HY, Ashraf S, Lawson JA, Shril S, Airik M, Tan W, Schapiro D, Rao J, Choi WI, Hermle T, Kemper MJ, Pohl M, Ozaltin F, Konrad M, Bogdanovic R, Buscher R, Helmchen U, Serdaroglu E, Lifton RP, Antonin W, Hildebrandt F (2016) Mutations in nuclear pore genes NUP93, NUP205 and XPO5 cause steroid-resistant nephrotic syndrome. Nat Genet 48:457–465PubMedPubMedCentralCrossRefGoogle Scholar
  14. Brennan HC, Nijjar S, Jones EA (1998) The specification of the pronephric tubules and duct in Xenopus laevis. Mech Dev 75:127–137PubMedCrossRefGoogle Scholar
  15. Brennan HC, Nijjar S, Jones EA (1999) The specification and growth factor inducibility of the pronephric glomus in Xenopus laevis. Development 126:5847–5856PubMedGoogle Scholar
  16. Brooks ER, Wallingford JB (2012) Control of vertebrate intraflagellar transport by the planar cell polarity effector Fuz. J Cell Biol 198:37–45PubMedPubMedCentralCrossRefGoogle Scholar
  17. Brooks ER, Wallingford JB (2013) The Small GTPase Rsg1 is important for the cytoplasmic localization and axonemal dynamics of intraflagellar transport proteins. Cilia 2:13PubMedPubMedCentralCrossRefGoogle Scholar
  18. Caine ST, McLaughlin KA (2013) Regeneration of functional pronephric proximal tubules after partial nephrectomy in Xenopus laevis. Dev Dyn 242:219–229PubMedCrossRefGoogle Scholar
  19. Campbell EP, Quigley IK, Kintner C (2016) Foxn4 promotes gene expression required for the formation of multiple motile cilia. Development 143:4654–4664PubMedCrossRefGoogle Scholar
  20. Chan T-c, Ariizumi T, Asashima M (1999) A model system for organ engineering: transplantation of in vitro induced embryonic kidney. Naturwissenschaften 86:224–227PubMedCrossRefGoogle Scholar
  21. Christensen EI, Raciti D, Reggiani L, Verroust PJ, Brandli AW (2008) Gene expression analysis defines the proximal tubule as the compartment for endocytic receptor-mediated uptake in the Xenopus pronephric kidney. Pflugers Arch - Eur J Physiol 456:1163–1176CrossRefGoogle Scholar
  22. Dale L, Slack JM (1987) Fate map for the 32-cell stage of Xenopus laevis. Development 99:527–551PubMedGoogle Scholar
  23. Dale L, Smith JC, Slack JM (1985) Mesoderm induction in Xenopus laevis: a quantitative study using a cell lineage label and tissue-specific antibodies. J Embryol Exp Morpholog 89:289–312Google Scholar
  24. Del Viso F, Huang F, Myers J, Chalfant M, Zhang Y, Reza N, Bewersdorf J, Lusk CP, Khokha MK (2016) Congenital heart disease genetics uncovers context-dependent organization and function of Nucleoporins at Cilia. Dev Cell 38:478–492PubMedCrossRefGoogle Scholar
  25. Desgrange A, Cereghini S (2015) Nephron patterning: lessons from Xenopus, zebrafish, and mouse studies. Cell 4:483–499CrossRefGoogle Scholar
  26. Doherty JR, Johnson Hamlet MR, Kuliyev E, Mead PE (2007) A flk-1 promoter/enhancer reporter transgenic Xenopus laevis generated using the Sleeping Beauty transposon system: an in vivo model for vascular studies. Dev Dyn 236:2808–2817PubMedCrossRefGoogle Scholar
  27. Eisen JS, Smith JC (2008) Controlling morpholino experiments: don’t stop making antisense. Development 135:1735–1743PubMedCrossRefGoogle Scholar
  28. Elkan ER (1938) The Xenopus pregnancy test. BMJ 2(1253–1274):1252Google Scholar
  29. Elliott KL, Fritzsch B (2010) Transplantation of Xenopus laevis ears reveals the ability to form afferent and efferent connections with the spinal cord. Int J Dev Biol 54:1443–1451PubMedCrossRefGoogle Scholar
  30. Estevez R, Boettger T, Stein V, Birkenhager R, Otto E, Hildebrandt F, Jentsch TJ (2001) Barttin is a Cl- channel beta-subunit crucial for renal Cl- reabsorption and inner ear K+ secretion. Nature 414:558–561PubMedCrossRefGoogle Scholar
  31. Fakhro KA, Choi M, Ware SM, Belmont JW, Towbin JA, Lifton RP, Khokha MK, Brueckner M (2011) Rare copy number variations in congenital heart disease patients identify unique genes in left-right patterning. Proc Natl Acad Sci U S A 108:2915–2920PubMedPubMedCentralCrossRefGoogle Scholar
  32. Futel M, Leclerc C, Le Bouffant R, Buisson I, Neant I, Umbhauer M, Moreau M, Riou JF (2015) TRPP2-dependent Ca2+ signaling in dorso-lateral mesoderm is required for kidney field establishment in Xenopus. J Cell Sci 128:888–899PubMedCrossRefGoogle Scholar
  33. Gilchrist MJ, Christensen MB, Bronchain O, Brunet F, Chesneau A, Fenger U, Geach TJ, Ironfield HV, Kaya F, Kricha S, Lea R, Masse K, Neant I, Paillard E, Parain K, Perron M, Sinzelle L, Souopgui J, Thuret R, Ymlahi-Ouazzani Q, Pollet N (2009) Database of queryable gene expression patterns for Xenopus. Dev Dyn 238:1379–1388PubMedCrossRefGoogle Scholar
  34. Gordon CT, Xue S, Yigit G, Filali H, Chen K, Rosin N, Yoshiura KI, Oufadem M, Beck TJ, McGowan R, Magee AC, Altmuller J, Dion C, Thiele H, Gurzau AD, Nurnberg P, Meschede D, Muhlbauer W, Okamoto N, Varghese V, Irving R, Sigaudy S, Williams D, Ahmed SF, Bonnard C, Kong MK, Ratbi I, Fejjal N, Fikri M, Elalaoui SC, Reigstad H, Bole-Feysot C, Nitschke P, Ragge N, Levy N, Tuncbilek G, Teo AS, Cunningham ML, Sefiani A, Kayserili H, Murphy JM, Chatdokmaiprai C, Hillmer AM, Wattanasirichaigoon D, Lyonnet S, Magdinier F, Javed A, Blewitt ME, Amiel J, Wollnik B, Reversade B (2017) De novo mutations in SMCHD1 cause Bosma arhinia microphthalmia syndrome and abrogate nasal development. Nat Genet 49:249–255PubMedCrossRefGoogle Scholar
  35. Grainger RM, Herry JJ, Henderson RA (1988) Reinvestigation of the role of the optic vesicle in embryonic lens induction. Development 102:517–526PubMedGoogle Scholar
  36. Greger R (1996) The membrane transporters regulating epithelial NaCl secretion. Pflugers Arch - Eur J Physiol 432:579–588CrossRefGoogle Scholar
  37. Guo X, Zhang T, Hu Z, Zhang Y, Shi Z, Wang Q, Cui Y, Wang F, Zhao H, Chen Y (2014) Efficient RNA/Cas9-mediated genome editing in Xenopus tropicalis. Development 141:707–714PubMedCrossRefGoogle Scholar
  38. Gurdon JB, Elsdale TR, Fischberg M (1958) Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 182:65–65Google Scholar
  39. Hamlet MR, Yergeau DA, Kuliyev E, Takeda M, Taira M, Kawakami K, Mead PE (2006) Tol2 transposon-mediated transgenesis in Xenopus tropicalis. Genesis 44:438–445PubMedCrossRefGoogle Scholar
  40. Hannak E, Heald R (2006) Xorbit/CLASP links dynamic microtubules to chromosomes in the Xenopus meiotic spindle. J Cell Biol 172:19–25PubMedPubMedCentralCrossRefGoogle Scholar
  41. Heasman J (2002) Morpholino oligos: making sense of antisense? Dev Biol 243:209–214PubMedCrossRefGoogle Scholar
  42. Higa MM, Ullman KS, Prunuske AJ (2006) Studying nuclear disassembly in vitro using Xenopus egg extract. Methods 39:284–290PubMedCrossRefGoogle Scholar
  43. Hoff S, Halbritter J, Epting D, Frank V, Nguyen TM, van Reeuwijk J, Boehlke C, Schell C, Yasunaga T, Helmstadter M, Mergen M, Filhol E, Boldt K, Horn N, Ueffing M, Otto EA, Eisenberger T, Elting MW, van Wijk JA, Bockenhauer D, Sebire NJ, Rittig S, Vyberg M, Ring T, Pohl M, Pape L, Neuhaus TJ, Elshakhs NA, Koon SJ, Harris PC, Grahammer F, Huber TB, Kuehn EW, Kramer-Zucker A, Bolz HJ, Roepman R, Saunier S, Walz G, Hildebrandt F, Bergmann C, Lienkamp SS (2013) ANKS6 is a central component of a nephronophthisis module linking NEK8 to INVS and NPHP3. Nat Genet 45:951–956PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hoppler S, Vize PD (2012) Xenopus protocols: post-genomic approaches. Humana, New YorkCrossRefGoogle Scholar
  45. Ishibashi S, Kroll KL, Amaya E (2012) Generating transgenic frog embryos by restriction enzyme mediated integration (REMI). Methods Mol Biol 917:185–203PubMedCrossRefGoogle Scholar
  46. Ivics Z, Hackett PB, Plasterk RH, Izsvak Z (1997) Molecular reconstruction of sleeping beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91:501–510PubMedCrossRefGoogle Scholar
  47. Jaffe KM, Grimes DT, Schottenfeld-Roames J, Werner ME, Ku TS, Kim SK, Pelliccia JL, Morante NF, Mitchell BJ, Burdine RD (2016) c21orf59/kurly controls both cilia motility and polarization. Cell Rep 14:1841–1849PubMedPubMedCentralCrossRefGoogle Scholar
  48. Jevtic P, Milunovic-Jevtic A, Dilsaver MR, Gatlin JC, Levy DL (2016) Use of Xenopus cell-free extracts to study size regulation of subcellular structures. Int J Dev Biol 60:277–288PubMedPubMedCentralCrossRefGoogle Scholar
  49. Karpinka JB, Fortriede JD, Burns KA, James-Zorn C, Ponferrada VG, Lee J, Karimi K, Zorn AM, Vize PD (2015) Xenbase, the Xenopus model organism database; new virtualized system, data types and genomes. Nucleic Acids Res 43:D756–D763PubMedCrossRefGoogle Scholar
  50. Kelley CM, Yergeau DA, Zhu H, Kuliyev E, Mead PE (2012) Xenopus transgenics: methods using transposons. Methods Mol Biol 917:231–243PubMedCrossRefGoogle Scholar
  51. Kim SK, Shindo A, Park TJ, Oh EC, Ghosh S, Gray RS, Lewis RA, Johnson CA, Attie-Bittach T, Katsanis N, Wallingford JB (2010) Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 329:1337–1340PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kok FO, Shin M, Ni C-W, Gupta A, Grosse AS, van Impel A, Kirchmaier BC, Peterson-Maduro J, Kourkoulis G, Male I (2015) Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish. Dev Cell 32:97–108PubMedCrossRefGoogle Scholar
  53. Krogh A (1929) The progress of physiology. Science 70:200–204PubMedCrossRefGoogle Scholar
  54. Leclerc C, Webb SE, Miller AL, Moreau M (2008) An increase in intracellular Ca2+ is involved in pronephric tubule differentiation in the amphibian Xenopus laevis. Dev Biol 321:357–367PubMedCrossRefGoogle Scholar
  55. Lei Y, Guo X, Liu Y, Cao Y, Deng Y, Chen X, Cheng CH, Dawid IB, Chen Y, Zhao H (2012) Efficient targeted gene disruption in Xenopus embryos using engineered transcription activator-like effector nucleases (TALENs). Proc Natl Acad Sci U S A 109:17484–17489PubMedPubMedCentralCrossRefGoogle Scholar
  56. Li YE, Allen BG, Weeks DL (2012) Using PhiC31 integrase to mediate insertion of DNA in Xenopus embryos. Methods Mol Biol 917:219–230PubMedPubMedCentralCrossRefGoogle Scholar
  57. Lienkamp SS (2016) Using Xenopus to study genetic kidney diseases. Semin Cell Dev Biol 51:117–124PubMedCrossRefGoogle Scholar
  58. Lienkamp S, Ganner A, Boehlke C, Schmidt T, Arnold SJ, Schafer T, Romaker D, Schuler J, Hoff S, Powelske C, Eifler A, Kronig C, Bullerkotte A, Nitschke R, Kuehn EW, Kim E, Burkhardt H, Brox T, Ronneberger O, Gloy J, Walz G (2010) Inversin relays Frizzled-8 signals to promote proximal pronephros development. Proc Natl Acad Sci U S A 107:20388–20393PubMedPubMedCentralCrossRefGoogle Scholar
  59. Lienkamp SS, Liu K, Karner CM, Carroll TJ, Ronneberger O, Wallingford JB, Walz G (2012) Vertebrate kidney tubules elongate using a planar cell polarity-dependent, rosette-based mechanism of convergent extension. Nat Genet 44:1382–1387PubMedPubMedCentralCrossRefGoogle Scholar
  60. Loots GG, Bergmann A, Hum NR, Oldenburg CE, Wills AE, Hu N, Ovcharenko I, Harland RM (2013) Interrogating transcriptional regulatory sequences in Tol2-mediated Xenopus transgenics. PLoS ONE 8, e68548PubMedPubMedCentralCrossRefGoogle Scholar
  61. Love NR, Thuret R, Chen Y, Ishibashi S, Sabherwal N, Paredes R, Alves-Silva J, Dorey K, Noble AM, Guille MJ, Sasai Y, Papalopulu N, Amaya E (2011) pTransgenesis: a cross-species, modular transgenesis resource. Development 138:5451–5458PubMedPubMedCentralCrossRefGoogle Scholar
  62. Magalska A, Schellhaus AK, Moreno-Andres D, Zanini F, Schooley A, Sachdev R, Schwarz H, Madlung J, Antonin W (2014) RuvB-like ATPases function in chromatin decondensation at the end of mitosis. Dev Cell 31:305–318PubMedCrossRefGoogle Scholar
  63. Mitchell B, Jacobs R, Li J, Chien S, Kintner C (2007) A positive feedback mechanism governs the polarity and motion of motile cilia. Nature 447:97–101PubMedCrossRefGoogle Scholar
  64. Mitchell B, Stubbs JL, Huisman F, Taborek P, Yu C, Kintner C (2009) The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin. Curr Biol 19:924–929PubMedPubMedCentralCrossRefGoogle Scholar
  65. Mitchison HM, Valente EM (2017) Motile and non-motile cilia in human pathology: from function to phenotypes. J Pathol 241:294–309PubMedCrossRefGoogle Scholar
  66. Moody SA (1987) Fates of the blastomeres of the 32-cell-stage Xenopus embryo. Dev Biol 122:300–319PubMedCrossRefGoogle Scholar
  67. Moriya N, Uchiyama H, Asashima M (1993) Induction of pronephric tubules by activin and retinoic acid in presumptive ectoderm of Xenopus laevis. Develop Growth Differ 35:123–128CrossRefGoogle Scholar
  68. Naert T, Colpaert R, Van Nieuwenhuysen T, Dimitrakopoulou D, Leoen J, Haustraete J, Boel A, Steyaert W, Lepez T, Deforce D, Willaert A, Creytens D, Vleminckx K (2016) CRISPR/Cas9 mediated knockout of rb1 and rbl1 leads to rapid and penetrant retinoblastoma development in Xenopus tropicalis. Sci Rep 6:35264PubMedPubMedCentralCrossRefGoogle Scholar
  69. Nakade S, Tsubota T, Sakane Y, Kume S, Sakamoto N, Obara M, Daimon T, Sezutsu H, Yamamoto T, Sakuma T, Suzuki KT (2014) Microhomology-mediated end-joining-dependent integration of donor DNA in cells and animals using TALENs and CRISPR/Cas9. Nat Commun 5:5560PubMedPubMedCentralCrossRefGoogle Scholar
  70. Nakayama T, Fish MB, Fisher M, Oomen-Hajagos J, Thomsen GH, Grainger RM (2013) Simple and efficient CRISPR/Cas9-mediated targeted mutagenesis in Xenopus tropicalis. Genesis 51:835–843PubMedPubMedCentralCrossRefGoogle Scholar
  71. Nakayama T, Nakajima K, Cox A, Fisher M, Howell M, Fish MB, Yaoita Y, Grainger RM (2016) No privacy, a Xenopus tropicalis mutant, is a model of human Hermansky-Pudlak Syndrome and allows visualization of internal organogenesis during tadpole development. Dev BiolGoogle Scholar
  72. Nieuwkoop P (1969) The formation of the mesoderm in urodelean amphibians. Wilhelm Roux Arch Entwickl Mech Org 163:298–315PubMedCrossRefGoogle Scholar
  73. Ochi H, Tamai T, Nagano H, Kawaguchi A, Sudou N, Ogino H (2012) Evolution of a tissue-specific silencer underlies divergence in the expression of pax2 and pax8 paralogues. Nat Commun 3:848PubMedCrossRefGoogle Scholar
  74. Ogino H, McConnell WB, Grainger RM (2006) High-throughput transgenesis in Xenopus using I-SceI meganuclease. Nat Protoc 1:1703–1710PubMedCrossRefGoogle Scholar
  75. Osafune K, Nishinakamura R, Komazaki S, Asashima M (2002) In vitro induction of the pronephric duct in Xenopus explants. Develop Growth Differ 44:161–167CrossRefGoogle Scholar
  76. Pan FC, Chen Y, Loeber J, Henningfeld K, Pieler T (2006) I-SceI meganuclease-mediated transgenesis in Xenopus. Dev Dyn 235:247–252PubMedCrossRefGoogle Scholar
  77. Papke RL, Smith-Maxwell C (2009) High throughput electrophysiology with Xenopus oocytes. Comb Chem High Throughput Screen 12:38–50PubMedPubMedCentralCrossRefGoogle Scholar
  78. Pedersen A, Skjong C, Shawlot W (2005) Lim 1 is required for nephric duct extension and ureteric bud morphogenesis. Dev Biol 288:571–581PubMedCrossRefGoogle Scholar
  79. Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387PubMedCrossRefGoogle Scholar
  80. Raciti D, Reggiani L, Geffers L, Jiang Q, Bacchion F, Subrizi AE, Clements D, Tindal C, Davidson DR, Kaissling B, Brandli AW (2008) Organization of the pronephric kidney revealed by large-scale gene expression mapping. Genome Biol 9:R84PubMedPubMedCentralCrossRefGoogle Scholar
  81. Reid CD, Karra K, Chang J, Piskol R, Li Q, Li JB, Cherry JM, Baker JC (2016) XenMine: a genomic interaction tool for the Xenopus community. Dev BiolGoogle Scholar
  82. Reversade B, Escande-Beillard N, Dimopoulou A, Fischer B, Chng SC, Li Y, Shboul M, Tham PY, Kayserili H, Al-Gazali L, Shahwan M, Brancati F, Lee H, O’Connor BD, Schmidt-von Kegler M, Merriman B, Nelson SF, Masri A, Alkazaleh F, Guerra D, Ferrari P, Nanda A, Rajab A, Markie D, Gray M, Nelson J, Grix A, Sommer A, Savarirayan R, Janecke AR, Steichen E, Sillence D, Hausser I, Budde B, Nurnberg G, Nurnberg P, Seemann P, Kunkel D, Zambruno G, Dallapiccola B, Schuelke M, Robertson S, Hamamy H, Wollnik B, Van Maldergem L, Mundlos S, Kornak U (2009) Mutations in PYCR1 cause cutis laxa with progeroid features. Nat Genet 41:1016–1021PubMedCrossRefGoogle Scholar
  83. Sadaghiani B, Thiebaud CH (1987) Neural crest development in the Xenopus laevis embryo, studied by interspecific transplantation and scanning electron microscopy. Dev Biol 124:91–110PubMedCrossRefGoogle Scholar
  84. Schafer T, Putz M, Lienkamp S, Ganner A, Bergbreiter A, Ramachandran H, Gieloff V, Gerner M, Mattonet C, Czarnecki PG, Sayer JA, Otto EA, Hildebrandt F, Kramer-Zucker A, Walz G (2008) Genetic and physical interaction between the NPHP5 and NPHP6 gene products. Hum Mol Genet 17:3655–3662PubMedPubMedCentralCrossRefGoogle Scholar
  85. Schmitt SM, Gull M, Brandli AW (2014) Engineering Xenopus embryos for phenotypic drug discovery screening. Adv Drug Deliv Rev 69–70:225–246PubMedCrossRefGoogle Scholar
  86. Session AM, Uno Y, Kwon T, Chapman JA, Toyoda A, Takahashi S, Fukui A, Hikosaka A, Suzuki A, Kondo M, van Heeringen SJ, Quigley I, Heinz S, Ogino H, Ochi H, Hellsten U, Lyons JB, Simakov O, Putnam N, Stites J, Kuroki Y, Tanaka T, Michiue T, Watanabe M, Bogdanovic O, Lister R, Georgiou G, Paranjpe SS, van Kruijsbergen I, Shu S, Carlson J, Kinoshita T, Ohta Y, Mawaribuchi S, Jenkins J, Grimwood J, Schmutz J, Mitros T, Mozaffari SV, Suzuki Y, Haramoto Y, Yamamoto TS, Takagi C, Heald R, Miller K, Haudenschild C, Kitzman J, Nakayama T, Izutsu Y, Robert J, Fortriede J, Burns K, Lotay V, Karimi K, Yasuoka Y, Dichmann DS, Flajnik MF, Houston DW, Shendure J, DuPasquier L, Vize PD, Zorn AM, Ito M, Marcotte EM, Wallingford JB, Ito Y, Asashima M, Ueno N, Matsuda Y, Veenstra GJ, Fujiyama A, Harland RM, Taira M, Rokhsar DS (2016) Genome evolution in the allotetraploid frog Xenopus laevis. Nature 538:336–343PubMedPubMedCentralCrossRefGoogle Scholar
  87. Shi Z, Wang F, Cui Y, Liu Z, Guo X, Zhang Y, Deng Y, Zhao H, Chen Y (2015) Heritable CRISPR/Cas9-mediated targeted integration in Xenopus tropicalis. FASEB J 29:4914–4923PubMedCrossRefGoogle Scholar
  88. Silva P, Solomon RJ, Epstein FH (1996) The rectal gland of Squalus acanthias: a model for the transport of chloride. Kidney Int 49:1552–1556PubMedCrossRefGoogle Scholar
  89. Sinzelle L, Vallin J, Coen L, Chesneau A, Du Pasquier D, Pollet N, Demeneix B, Mazabraud A (2006) Generation of trangenic Xenopus laevis using the Sleeping Beauty transposon system. Transgenic Res 15:751–760PubMedCrossRefGoogle Scholar
  90. Sive HL, Grainger RM, Harland RM (2000) Early development of Xenopus laevis: a laboratory manual. Cold Spring Harbor Press, New York.Google Scholar
  91. Sive HL, Grainger RM, Harland RM (2007) Inducing ovulation in Xenopus laevis. CSH protocols 2007:pdb prot4734Google Scholar
  92. Skou JC (1957) The influence of some cations on an adenosine triphosphatase from peripheral nerves. Biochim Biophys Acta 23:394–401PubMedCrossRefGoogle Scholar
  93. Spemann H, Mangold H (1924) Über induktion von Embryonalanlagen durch Implantation artfremder Organisatoren. Dev Genes Evol 100:599–638Google Scholar
  94. Suzuki N, Hirano K, Ogino H, Ochi H (2015) Identification of distal enhancers for Six2 expression in pronephros. Int J Dev Biol 59:241–246Google Scholar
  95. Tandon P, Conlon F, Furlow JD, Horb ME (2016) Expanding the genetic toolkit in Xenopus: approaches and opportunities for human disease modeling. Dev BiolGoogle Scholar
  96. Toriyama M, Lee C, Taylor SP, Duran I, Cohn DH, Bruel AL, Tabler JM, Drew K, Kelly MR, Kim S, Park TJ, Braun DA, Pierquin G, Biver A, Wagner K, Malfroot A, Panigrahi I, Franco B, Al-Lami HA, Yeung Y, Choi YJ, University of Washington Center for Mendelian G, Duffourd Y, Faivre L, Riviere JB, Chen J, Liu KJ, Marcotte EM, Hildebrandt F, Thauvin-Robinet C, Krakow D, Jackson PK, Wallingford JB (2016) The ciliopathy-associated CPLANE proteins direct basal body recruitment of intraflagellar transport machinery. Nat Genet 48:648–656PubMedPubMedCentralCrossRefGoogle Scholar
  97. Uochi T, Asashima M (1998) XCIRP (Xenopus homolog of cold-inducible RNA-binding protein) is expressed transiently in developing pronephros and neural tissue. Gene 211:245–250PubMedCrossRefGoogle Scholar
  98. Vize PD, Jones EA, Pfister R (1995) Development of the Xenopus pronephric system. Dev Biol 171:531–540PubMedCrossRefGoogle Scholar
  99. Vize PD, McCoy KE, Zhou X (2009) Multichannel wholemount fluorescent and fluorescent/chromogenic in situ hybridization in Xenopus embryos. Nat Protoc 4:975–983PubMedCrossRefGoogle Scholar
  100. Vollmer B, Lorenz M, Moreno-Andres D, Bodenhofer M, De Magistris P, Astrinidis SA, Schooley A, Flotenmeyer M, Leptihn S, Antonin W (2015) Nup153 recruits the Nup107-160 complex to the inner nuclear membrane for interphasic nuclear pore complex assembly. Dev Cell 33:717–728PubMedCrossRefGoogle Scholar
  101. Wang F, Shi Z, Cui Y, Guo X, Shi YB, Chen Y (2015) Targeted gene disruption in Xenopus laevis using CRISPR/Cas9. Cell Biosci 5:15PubMedPubMedCentralCrossRefGoogle Scholar
  102. Wessely O, Tran U (2011) Xenopus pronephros development--past, present, and future. Pediatr Nephrol 26:1545–1551PubMedPubMedCentralCrossRefGoogle Scholar
  103. White JT, Zhang B, Cerqueira DM, Tran U, Wessely O (2010) Notch signaling, wt1 and foxc2 are key regulators of the podocyte gene regulatory network in Xenopus. Development 137:1863–1873PubMedPubMedCentralCrossRefGoogle Scholar
  104. Yasunaga T, Hoff S, Schell C, Helmstadter M, Kretz O, Kuechlin S, Yakulov TA, Engel C, Muller B, Bensch R, Ronneberger O, Huber TB, Lienkamp SS, Walz G (2015) The polarity protein Inturned links NPHP4 to Daam1 to control the subapical actin network in multiciliated cells. J Cell Biol 211:963–973PubMedPubMedCentralCrossRefGoogle Scholar
  105. Young JJ, Harland RM (2012) Targeted gene disruption with engineered zinc-finger nucleases (ZFNs). Methods Mol Biol 917:129–141PubMedCrossRefGoogle Scholar
  106. Yu Y, Ulbrich MH, Li MH, Buraei Z, Chen XZ, Ong AC, Tong L, Isacoff EY, Yang J (2009) Structural and molecular basis of the assembly of the TRPP2/PKD1 complex. Proc Natl Acad Sci U S A 106:11558–11563PubMedPubMedCentralCrossRefGoogle Scholar
  107. Zhang S, Mitchell BJ (2015) Basal bodies in Xenopus. Cilia 5:2PubMedCrossRefGoogle Scholar
  108. Zhou X, Vize PD (2004) Proximo-distal specialization of epithelial transport processes within the Xenopus pronephric kidney tubules. Dev Biol 271:322–338PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Medicine, Renal Division, Medical Center—Faculty of MedicineUniversity of FreiburgFreiburgGermany
  2. 2.BIOSS Centre of Biological Signalling StudiesUniversity of FreiburgFreiburgGermany

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