Xenopus as a Model for GI/Pancreas Disease

Current Pathobiology Reports

Volumn 3, Issue 2, 2015, Pages 137-145

  Salanga, Matthew C ^a   Horb, Marko E ^a  

^a MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

Diabetes; Endoderm; GI tract; Lung; Oocyte; Pancreas; Xenopus

Indexed keywords

EID: 84977985950     PISSN: None     EISSN: 2167485X     Source Type: Journal    
DOI: 10.1007/s40139-015-0076-0     Document Type: Review

References (75)

1. CDC (2014) National Diabetes Statistics Report, 2014. pp 1–12
2. Blitz IL, Andelfinger G, Horb ME (2006) Germ layers to organs: Using Xenopus to study “later” development. Semin Cell Dev Biol 17:133–145. doi:10.1016/j.semcdb.2005.11.002
3. Hellsten U, Khokha MK, Grammer TC et al (2007) Accelerated gene evolution and subfunctionalization in the pseudotetraploid frog Xenopus laevis. BMC Biol 5:31. doi:10.1186/1741-7007-5-31
4. Hellsten U, Harland RM, Gilchrist MJ et al (2010) The Genome of the Western Clawed Frog Xenopus tropicalis. Science 328:633–636. doi:10.1126/science.1183670
5. Uno Y, Nishida C, Takagi C et al (2013) Homoeologous chromosomes of Xenopus laevis are highly conserved after whole-genome duplication. Heredity 111:430–436. doi:10.1038/hdy.2013.65
6. Schmitt SM, Gull M, Brändli AW (2014) Engineering Xenopus embryos for phenotypic drug discovery screening. Adv Drug Deliv Rev 69–70:225–246. doi:10.1016/j.addr.2014.02.004
7. Wheeler GN, Brändli AW (2009) Simple vertebrate models for chemical genetics and drug discovery screens: lessons from zebrafish and Xenopus. Dev Dyn 238:1287–1308. doi:10.1002/dvdy.21967
8. Moody SA (1987) Fates of the blastomeres of the 32-cell-stage Xenopus embryo. Dev Biol 122:300–319
9. Chalmers AD, Slack JM (2000) The Xenopus tadpole gut: fate maps and morphogenetic movements. Development 127:381–392
10. Changkyun Park E, Hayata T, Cho KWY, Han J-K (2007) Xenopus cDNA microarray identification of genes with endodermal organ expression. Dev Dyn 236:1633–1649. doi:10.1002/dvdy.21167
11. •• Jarikji Z, Horb LD, Shariff F, et al (2009) The tetraspanin Tm4sf3 is localized to the ventral pancreas and regulates fusion of the dorsal and ventral pancreatic buds. Development 136:1791–1800. doi:10.1242/dev.032235 This report shows differential behavior of dorsal versus ventral pancreatic bud cells with ventral cells being the primary migratory pool; they produced chimeric embryos between wild type and transgenic embryos to label individual buds and monitor their behavior. They also isolated individual dorsal or ventral pancreatic buds and identified differentially expressed genes
12. Bilogan CK, Horb ME (2012) Microarray analysis of Xenopus endoderm expressing Ptf1a. Genesis 50:853–870. doi:10.1002/dvg.22048
13. Rankin SA, Kormish J, Kofron M et al (2011) A gene regulatory network controlling hhex transcription in the anterior endoderm of the organizer. Dev Biol 351:297–310. doi:10.1016/j.ydbio.2010.11.037
14. Karpinka JB, Fortriede JD, Burns KA et al (2014) Xenbase, the Xenopus model organism database; new virtualized system, data types and genomes. Nucleic Acids Res. doi:10.1093/nar/gku956
15. Segerdell E, Ponferrada VG, James-Zorn C et al (2013) Enhanced XAO: the ontology of Xenopus anatomy and development underpins more accurate annotation of gene expression and queries on Xenbase. J Biomed Semantics 4:31. doi:10.1186/2041-1480-4-31
16. James-Zorn C, Ponferrada VG, Jarabek CJ et al (2013) Xenbase: expansion and updates of the Xenopus model organism database. Nucleic Acids Res 41:D865–D870. doi:10.1093/nar/gks1025
17. Yanai I, Peshkin L, Jorgensen P, Kirschner MW (2011) Mapping gene expression in two Xenopus species: evolutionary constraints and developmental flexibility. Dev Cell 20:483–496. doi:10.1016/j.devcel.2011.03.015
18. Wühr M, Freeman RM Jr, Presler M et al (2014) Deep proteomics of the Xenopus laevis egg using an mRNA-derived reference database. Curr Biol 24:1467–1475. doi:10.1016/j.cub.2014.05.044
19. Kwon T, Chung M-I, Gupta R et al (2014) Identifying direct targets of transcription factor Rfx2 that coordinate ciliogenesis and cell movement. Genom Data 2:192–194. doi:10.1016/j.gdata.2014.06.015
20. Sun L, Bertke MM, Champion MM et al (2014) Quantitative proteomics of Xenopus laevis embryos: expression kinetics of nearly 4000 proteins during early development. Sci Rep 4:4365. doi:10.1038/srep04365
21. Zorn AM, Wells JM (2009) Vertebrate endoderm development and organ formation. Annu Rev Cell Dev Biol 25:221–251. doi:10.1146/annurev.cellbio.042308.113344
22. Horb ME, Slack JMW (2001) Endoderm specification and differentiation in Xenopus embryos. Dev Biol 236:330–343. doi:10.1006/dbio.2001.0347
23. McLin VA, Rankin SA, Zorn AM (2007) Repression of Wnt/β-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development 134:2207–2217. doi:10.1242/dev.001230
24. • Zhang T, Guo X, Chen Y (2013) Retinoic acid-activated Ndrg1a represses Wnt/β-catenin signaling to allow Xenopus pancreas, oesophagus, stomach, and duodenum specification. PLoS One 8:e65058. doi:10.1371/journal.pone.0065058 This was the first study to use TALEN mediated genome editing in Xenopus to establish that Ndrg1 was required for proper development of anterior endodermal organs. They also showed that the morpholino knockdown phenotype was identical to the TALEN induced phenotype demonstrating the usefulness of both methods
25. Li Y, Rankin SA, Sinner D et al (2008) Sfrp5 coordinates foregut specification and morphogenesis by antagonizing both canonical and noncanonical Wnt11 signaling. Genes Dev 22:3050–3063. doi:10.1101/gad.1687308
26. Bilogan CK, Horb ME (2012) Xenopus staufen2 is required for anterior endodermal organ formation. Genesis 50:251–259. doi:10.1002/dvg.22000
27. Zhang Z, Rankin SA, Zorn AM (2013) Different thresholds of Wnt-Frizzled 7 signaling coordinate proliferation, morphogenesis and fate of endoderm progenitor cells. Dev Biol 378:1–12. doi:10.1016/j.ydbio.2013.02.024
28. •• Kenny AP, Rankin SA, Allbee AW, et al (2012) Sizzled-tolloid interactions maintain foregut progenitors by regulating fibronectin-dependent BMP signaling. Dev Cell 23:292–304. doi:10.1016/j.devcel.2012.07.002 In this study they compared isolated explants of anterior endoderm with and without mesoderm and identified Szl as being upregulted in endoderm only in the presence of mesoderm. They went on to show that BMP signaling from the mesoderm induces Szl expression in the endoderm, and Szl in turn controls deposition of fibronectin that is required to maintain BMP signaling
29. Chung M-I, Nascone-Yoder NM, Grover SA et al (2010) Direct activation of Shroom3 transcription by Pitx proteins drives epithelial morphogenesis in the developing gut. Development 137:1339–1349. doi:10.1242/dev.044610
30. • Dush MK, Nascone-Yoder NM (2013) Jun N-terminal kinase maintains tissue integrity during cell rearrangement in the gut. Development 140:1457–1466. doi:10.1242/dev.086850 In this study they demonstrated that JNK signaling maintains cell-cell adhesion during gut morphogenesis, while Rho kinase activity induces remodeling of cell-cell contacts leading to cell rearrangements
31. Rodríguez-Seguel E, Mah N, Naumann H et al (2013) Mutually exclusive signaling signatures define the hepatic and pancreatic progenitor cell lineage divergence. Genes Dev 27:1932–1946. doi:10.1101/gad.220244.113
32. Pearl EJ, Bilogan CK, Mukhi S et al (2009) Xenopus pancreas development. Dev Dyn 238:1271–1286. doi:10.1002/dvdy.21935
33. Jørgensen MC, Ahnfelt-Rønne J, Hald J et al (2007) An illustrated review of early pancreas development in the mouse. Endocr Rev 28:685–705. doi:10.1210/er.2007-0016
34. Polak M, Bouchareb-Banaei L, Scharfmann R, Czernichow P (2000) Early pattern of differentiation in the human pancreas. Diabetes 49:225–232
35. Cano DA, Hebrok M, Zenker M (2007) Pancreatic development and disease. Gastroenterology 132:745–762. doi:10.1053/j.gastro.2006.12.054
36. Horb LD, Horb ME (2010) BrunoL1 regulates endoderm proliferation through translational enhancement of cyclin A2 mRNA. Dev Biol 345:156–169. doi:10.1016/j.ydbio.2010.07.005
37. Horb LD, Jarkji ZH, Horb ME (2009) Xenopus Insm1 is essential for gastrointestinal and pancreatic endocrine cell development. Dev Dyn 238:2505–2510. doi:10.1002/dvdy.22071
38. Zhao H, Han D, Dawid IB et al (2012) Homeoprotein hhex-induced conversion of intestinal to ventral pancreatic precursors results in the formation of giant pancreata in Xenopus embryos. Proc Natl Acad Sci USA 109:8594–8599. doi:10.1073/pnas.1206547109/-/DCSupplemental
39. • Oropez D, Horb M (2012) Transient expression of Ngn3 in Xenopus endoderm promotes early and ectopic development of pancreatic beta and delta cells. Genesis 50:271–285. doi:10.1002/dvg.20828 This study demonstrated how Ngn3 activity in the anterior endoderm directs the differentiation of specific endocrine fates. They also showed how Xenopus can be used to identify downstream targets of Ngn3
40. Afelik S, Chen Y, Pieler T (2006) Combined ectopic expression of Pdx1 and Ptf1a/p48 results in the stable conversion of posterior endoderm into endocrine and exocrine pancreatic tissue. Genes Dev 20:1441–1446. doi:10.1101/gad.378706
41. Jarikji ZH, Vanamala S, Beck CW et al (2007) Differential ability of Ptf1a and Ptf1a-VP16 to convert stomach, duodenum and liver to pancreas. Dev Biol 304:786–799. doi:10.1016/j.ydbio.2007.01.027
42. Horb ME, Shen CN, Tosh D, Slack JMW (2003) Experimental conversion of liver to pancreas. Curr Biol 13:105–115
43. Mitchell J, Punthakee Z, Lo B et al (2004) Neonatal diabetes, with hypoplastic pancreas, intestinal atresia and gall bladder hypoplasia: search for the aetiology of a new autosomal recessive syndrome. Diabetologia 47:2160–2167. doi:10.1007/s00125-004-1576-3
44. Concepcion JP, Reh CS, Daniels M et al (2013) Neonatal diabetes, gallbladder agenesis, duodenal atresia, and intestinal malrotation caused by a novel homozygous mutation in RFX6. Pediatr Diabetes 15:67–72. doi:10.1111/pedi.12063
45. Smith SB, Qu H-Q, Taleb N et al (2010) Rfx6 directs islet formation and insulin production in mice and humans. Nature 463:775–780. doi:10.1038/nature08748
46. Pearl EJ, Jarikji Z, Horb ME (2011) Functional analysis of Rfx6 and mutant variants associated with neonatal diabetes. Dev Biol 351:135–145. doi:10.1016/j.ydbio.2010.12.043
47. Martin GM, Chen P-C, Devaraneni P, Shyng S-L (2013) Pharmacological rescue of trafficking-impaired ATP-sensitive potassium channels. Front Physiol 4:386. doi:10.3389/fphys.2013.00386
48. Thulé PM, Umpierrez G (2014) Sulfonylureas: a new look at old therapy. Curr Diab Rep 14:473. doi:10.1007/s11892-014-0473-5
49. Flanagan SE, Patch AM, Mackay DJG et al (2007) Mutations in ATP-sensitive K+ channel genes cause transient neonatal diabetes and permanent diabetes in childhood or adulthood. Diabetes 56:1930–1937. doi:10.2337/db07-0043
50. Bennett K, James C, Hussain K (2010) Pancreatic β-cell KATP channels: hypoglycaemia and hyperglycaemia. Rev Endocr Metab Disord 11:157–163. doi:10.1007/s11154-010-9144-2
51. Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30:687–696
52. Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the midblastula stage. Cell 30:675–686
53. Musa-Aziz R, Boron WF, Parker MD (2010) Using fluorometry and ion-sensitive microelectrodes to study the functional expression of heterologously-expressed ion channels and transporters in Xenopus oocytes. Methods 51:134–145. doi:10.1016/j.ymeth.2009.12.012
54. Sobczak K, Bangel-Ruland N, Leier G, Weber W-M (2010) Endogenous transport systems in the Xenopus laevis oocyte plasma membrane. Methods 51:183–189. doi:10.1016/j.ymeth.2009.12.001
55. Kloc M, Kubiak JZ (2014) Metamorphosis and organogenesis, in Xenopus development. Wiley, Oxford. doi:10.1002/9781118492833.part3
56. • Männikkö R, Stansfeld PJ, Ashcroft AS, et al (2011) A conserved tryptophan at the membrane-water interface acts as a gatekeeper for Kir6.2/SUR1 channels and causes neonatal diabetes when mutated. J Physiol 589:3071–3083. doi:10.1113/jphysiol.2011.209700 This study that identified the molecular basis for sulfonylurea resistance among patients harboring a W > A mutation in KATP channels using Xenopus oocytes. Demonstrates the usefulness of testing the functional relevance of specific point mutations on channel protein activity and the impact this has on specific drugs used for treatment
57. Proks P, de Wet H, Ashcroft FM (2013) Molecular mechanism of sulphonylurea block of KATP channels carrying mutations that impair ATP inhibition and cause neonatal diabetes. Diabetes 62:3909–3919. doi:10.2337/db13-0531
58. Proks P, de Wet H, Ashcroft FM (2014) Sulfonylureas suppress the stimulatory action of Mg-nucleotides on Kir6.2/SUR1 but not Kir6.2/SUR2A KATP channels: a mechanistic study. J Gen Physiol 144:469–486. doi:10.1007/BF00169252
59. Rose CS, James B (2013) Plasticity of lung development in the amphibian, Xenopus laevis. Biol Open 2:1324–1335. doi:10.1242/bio.20133772
60. •• Rankin SA, Thi Tran H, Wlizla M, et al. (2014) A molecular atlas of Xenopus respiratory system development. Dev Dyn. doi: 10.1002/dvdy.24180 This was the first study in Xenopus to show conservation of lung development in Xenopus and murine systems. It also examined the epistatic relationship between the various different signaling pathways in lung development
61. Rankin SA, Gallas AL, Neto A et al (2012) Suppression of Bmp4 signaling by the zinc-finger repressors Osr1 and Osr2 is required for Wnt/beta-catenin-mediated lung specification in Xenopus. Development 139:3010–3020. doi:10.1242/dev.078220
62. Wang JH, Deimling SJ, D’Alessandro NE et al (2011) Retinoic acid is a key regulatory switch determining the difference between lung andthyroid fates in Xenopus laevis. BMC Dev Biol 11:75. doi:10.1186/1471-213X-11-75
63. Rankin SA, Zorn AM (2014) Gene regulatory networks governing lung specification. J Cell Biochem 115:1343–1350. doi:10.1002/jcb.24810
64. Shifley ET, Kenny AP, Rankin SA, Zorn AM (2012) Prolonged FGF signaling is necessary for lung and liver induction in Xenopus. BMC Dev Biol 12:27. doi:10.1186/1471-213X-12-27
65. Kim H, Kim J-S (2014) A guide to genome engineering with programmable nucleases. Nat Rev Genet 15:321–334. doi:10.1038/nrg3686
66. Harrison MM, Jenkins BV, O’Connor-Giles KM, Wildonger J (2014) A CRISPR view of development. Genes Dev 28:1859–1872. doi:10.1101/gad.248252.114
67. Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:1262–1278. doi:10.1016/j.cell.2014.05.010
68. Peng Y, Clark KJ, Campbell JM et al (2014) Making designer mutants in model organisms. Development 141:4042–4054. doi:10.1242/dev.102186
69. • Guo X, Zhang T, Hu Z, et al (2014) Efficient RNA/Cas9-mediated genome editing in Xenopus tropicalis. Development 141:707–714. doi:10.1242/dev.099853 This is the first report to comprehensively cover CRISPR/Cas9 genome editing on multiple pancreatic, endoderm and disease related genes
70. Ishibashi S, Kroll KL, Amaya E (2008) A method for generating transgenic frog embryos. Methods Mol Biol 461:447–466. doi:10.1007/978-1-60327-483-8_31
71. Nakayama T, Fish MB, Fisher M et al (2013) Simple and efficient CRISPR/Cas9-mediated targeted mutagenesis in Xenopus tropicalis. Genesis 51:835–843. doi:10.1002/dvg.22720
72. Lei Y, Guo X, Liu Y et al (2012) Efficient targeted gene disruption in Xenopus embryos using engineered transcription activator-like effector nucleases (TALENs). Proc Natl Acad Sci 109:17484–17489. doi:10.1073/pnas.1215421109
73. Blitz IL, Biesinger J, Xie X, Cho KWY (2013) Biallelic genome modification in F 0 Xenopus tropicalis embryos using the CRISPR/Cas system. Genesis 51:827–834. doi:10.1002/dvg.22719
74. Nakade S, Tsubota T, Sakane Y et al (2014) Microhomology-mediated end-joining-dependent integration of donor DNA in cells and animals using TALENs and CRISPR/Cas9. Nat Commun 5:5560. doi:10.1038/ncomms6560
75. Pearl EJ, Grainger RM, Guille M, Horb ME (2012) Development of Xenopus Resource Centers: the National Xenopus resource and the European Xenopus Resource Center. Genesis 50:155–163. doi:10.1002/dvg.22013