Elf5 is a principal cell lineage specific transcription factor in the kidney that contributes to Aqp2 and Avpr2 gene expression

Developmental Biology

Volumn 424, Issue 1, 2017, Pages 77-89

  Grassmeyer, Justin ^a   Mukherjee, Malini ^a   deRiso, Jennifer ^a   Hettinger, Casey ^a   Bailey, Monica ^b   Sinha, Satrajit ^c   Visvader, Jane E ^d   Zhao, Haotian ^a,e   Fogarty, Eric ^a,e   Surendran, Kameswaran ^a,e  

^a SANFORD RESEARCH   (United States)

^b AUGUSTANA UNIVERSITY   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

Collecting ducts; Intercalated cell; Notch; RBPJ; Renal development

Indexed keywords

AQUAPORIN 2; NOTCH1 RECEPTOR; RBPJ PROTEIN; REGULATOR PROTEIN; TRANSCRIPTION FACTOR EHF; TRANSCRIPTION FACTOR ELF5; TRANSCRIPTION FACTOR ETS; UNCLASSIFIED DRUG; CRE RECOMBINASE; DNA BINDING PROTEIN; EHF PROTEIN, MOUSE; ELF3 PROTEIN, MOUSE; ELF5 PROTEIN, MOUSE; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; INTEGRASE; NOTCH RECEPTOR; RBPJ PROTEIN, MOUSE; TRANSCRIPTION FACTOR; VASOPRESSIN RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; AQUAPORIN 2 GENE; ARGININE VASOPRESSIN RECEPTOR 2 GENE; ARTICLE; CELL LINEAGE; CONTROLLED STUDY; ECTOPIC EXPRESSION; EMBRYO; GENE EXPRESSION; KIDNEY COLLECTING TUBULE; KIDNEY DEVELOPMENT; MOUSE; NONHUMAN; NOTCH SIGNALING PATHWAY; PROMOTER REGION; SIGNAL TRANSDUCTION; ANIMAL; CELL COUNT; CELL LINE; CYTOLOGY; DOWN REGULATION; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; METABOLISM; TRANSGENIC MOUSE; UPREGULATION; URETER;

ANIMALS; AQUAPORIN 2; CELL COUNT; CELL LINE; CELL LINEAGE; DNA-BINDING PROTEINS; DOWN-REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; INTEGRASES; KIDNEY; KIDNEY TUBULES, COLLECTING; MICE, TRANSGENIC; PROMOTER REGIONS, GENETIC; RECEPTORS, NOTCH; RECEPTORS, VASOPRESSIN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UP-REGULATION; URETER;

EID: 85013173242     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2017.02.007     Document Type: Article

References (63)

1. Bastani, B., Immunocytochemical localization of the vacuolar H(+)-ATPase pump in the kidney. Histol. Histopathol. 12:3 (1997), 769–779.
2. Bens, M., et al. Corticosteroid-dependent sodium transport in a novel immortalized mouse collecting duct principal cell line. J. Am. Soc. Nephrol. 10:5 (1999), 923–934.
3. Blomqvist, S.R., et al. Distal renal tubular acidosis in mice that lack the forkhead transcription factor Foxi1. J. Clin. Invest. 113:11 (2004), 1560–1570.
4. Bray, S., Notch signalling in Drosophila: three ways to use a pathway. Semin. Cell Dev. Biol. 9:6 (1998), 591–597.
5. Brown, D., Kumpulainen, T., Immunocytochemical localization of carbonic anhydrase on ultrathin frozen sections with protein A-gold. Histochemistry 83:2 (1985), 153–158.
6. Brown, D., Breton, S., Mitochondria-rich, proton-secreting epithelial cells. J. Exp. Biol. 199:Pt 11 (1996), 2345–2358.
7. Brown, D., Weyer, P., Orci, L., Vasopressin stimulates endocytosis in kidney collecting duct principal cells. Eur. J. Cell Biol. 46:2 (1988), 336–341.
8. Chakrabarti, R., et al. Elf5 regulates mammary gland stem/progenitor cell fate by influencing notch signaling. Stem Cells 30:7 (2012), 1496–1508.
9. Choi, Y.S., et al. Generation and analysis of Elf5-LacZ mouse: unique and dynamic expression of Elf5 (ESE-2) in the inner root sheath of cycling hair follicles. Histochem. Cell Biol. 129:1 (2008), 85–94.
10. Choi, Y.S., et al. Elf5 conditional knockout mice reveal its role as a master regulator in mammary alveolar development: failure of Stat5 activation and functional differentiation in the absence of Elf5. Dev. Biol. 329:2 (2009), 227–241.
11. Christensen, B.M., et al. Changes in cellular composition of kidney collecting duct cells in rats with lithium-induced NDI. Am. J. Physiol. Cell Physiol. 286:4 (2004), C952–C964.
12. Clapp, W.L., et al. Morphologic heterogeneity along the rat inner medullary collecting duct. Lab. Invest. 60:2 (1989), 219–230.
13. Costantini, F., Kopan, R., Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development. Dev. Cell 18:5 (2010), 698–712.
14. De Strooper, B., et al. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398:6727 (1999), 518–522.
15. Dressler, G.R., Advances in early kidney specification, development and patterning. Development 136:23 (2009), 3863–3874.
16. Edgar, R., Domrachev, M., Lash, A.E., Gene expression Omnibus: ncbi gene expression and hybridization array data repository. Nucleic Acids Res. 30:1 (2002), 207–210.
17. Emmons, C., Kurtz, I., Functional characterization of three intercalated cell subtypes in the rabbit outer cortical collecting duct. J. Clin. Invest. 93:1 (1994), 417–423.
18. Fejes-Toth, G., et al. Differential expression of AE1 in renal HCO3-secreting and -reabsorbing intercalated cells. J. Biol. Chem. 269:43 (1994), 26717–26721.
19. Fejes-Toth, G., Naray-Fejes-Toth, A., Differentiation of renal beta-intercalated cells to alpha-intercalated and principal cells in culture. Proc. Natl. Acad. Sci. USA 89:12 (1992), 5487–5491.
20. Gekle, M., et al. Characterization of two MDCK-cell subtypes as a model system to study principal cell and intercalated cell properties. Pflug. Arch. 428:2 (1994), 157–162.
21. Georgas, K., et al. Analysis of early nephron patterning reveals a role for distal RV proliferation in fusion to the ureteric tip via a cap mesenchyme-derived connecting segment. Dev. Biol. 332:2 (2009), 273–286.
22. Guo, Q., et al. Adam10 mediates the choice between principal cells and intercalated cells in the kidney. J. Am. Soc. Nephrol. 26:1 (2015), 149–159.
23. Heitzler, P., Simpson, P., The choice of cell fate in the epidermis of Drosophila. Cell 64:6 (1991), 1083–1092.
24. Janicke, M., Carney, T.J., Hammerschmidt, M., Foxi3 transcription factors and Notch signaling control the formation of skin ionocytes from epidermal precursors of the zebrafish embryo. Dev. Biol. 307:2 (2007), 258–271.
25. Jeong, H.W., et al. Inactivation of Notch signaling in the renal collecting duct causes nephrogenic diabetes insipidus in mice. J. Clin. Invest 119:11 (2009), 3290–3300.
26. Kageyama, R., et al. Dynamic Notch signaling in neural progenitor cells and a revised view of lateral inhibition. Nat. Neurosci. 11:11 (2008), 1247–1251.
27. Kaissling, B., Ultrastructural characterization of the connecting tubule and the different segments of the collecting duct system in the rabbit kidney. Curr. Probl. Clin. Biochem. 8 (1977), 435–446.
28. Kim, J., Tisher, C.C., Madsen, K.M., Differentiation of intercalated cells in developing rat kidney: an immunohistochemical study. Am. J. Physiol. 266:6 Pt 2 (1994), F977–F990.
29. Kobayashi, A., et al. Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3:2 (2008), 169–181.
30. Kopan, R., Ilagan, M.X., The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137:2 (2009), 216–233.
31. Kurth, I., et al. The forkhead transcription factor Foxi1 directly activates the AE4 promoter. Biochem J. 393:Pt 1 (2006), 277–283.
32. Kyrousi, C., et al. Mcidas and GemC1 are key regulators for the generation of multiciliated ependymal cells in the adult neurogenic niche. Development 142:21 (2015), 3661–3674.
33. Li, Y., et al. Zebrafish nephrogenesis is regulated by interactions between retinoic acid, mecom, and Notch signaling. Dev. Biol. 386:1 (2014), 111–122.
34. Liu, Y., et al. Notch signaling controls the differentiation of transporting epithelia and multiciliated cells in the zebrafish pronephros. Development 134:6 (2007), 1111–1122.
35. Ma, M., Jiang, Y.J., Jagged2a-notch signaling mediates cell fate choice in the zebrafish pronephric duct. PLoS Genet., 3(1), 2007, e18.
36. Madisen, L., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13:1 (2010), 133–140.
37. Madsen, K.M., Clapp, W.L., Verlander, J.W., Structure and function of the inner medullary collecting duct. Kidney Int. 34:4 (1988), 441–454.
38. Morimoto, M., et al. Canonical Notch signaling in the developing lung is required for determination of arterial smooth muscle cells and selection of Clara versus ciliated cell fate. J. Cell Sci. 123:Pt 2 (2010), 213–224.
39. Oxburgh, L., et al. TGFbeta superfamily signals are required for morphogenesis of the kidney mesenchyme progenitor population. Development 131:18 (2004), 4593–4605.
40. Packard, A., et al. Luminal mitosis drives epithelial cell dispersal within the branching ureteric bud. Dev. Cell 27:3 (2013), 319–330.
41. Pearton, D.J., et al. Elf5 regulation in the trophectoderm. Dev. Biol. 360:2 (2011), 343–350.
42. Pearton, D.J., et al. Elf5 counteracts precocious trophoblast differentiation by maintaining Sox2 and 3 and inhibiting Hand1 expression. Dev. Biol. 392:2 (2014), 344–357.
43. Perl, A.K., et al. Early restriction of peripheral and proximal cell lineages during formation of the lung. Proc. Natl. Acad. Sci. USA 99:16 (2002), 10482–10487.
44. Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res, 29(9), 2001, e45.
45. Quigley, I.K., Stubbs, J.L., Kintner, C., Specification of ion transport cells in the Xenopus larval skin. Development 138:4 (2011), 705–714.
46. Rios, A.C., et al. In situ identification of bipotent stem cells in the mammary gland. Nature 506:7488 (2014), 322–327.
47. Schenk, L.K., et al. Quantitative proteomics identifies vasopressin-responsive nuclear proteins in collecting duct cells. J. Am. Soc. Nephrol. 23:6 (2012), 1008–1018.
48. Shao, X., Somlo, S., Igarashi, P., Epithelial-specific Cre/lox recombination in the developing kidney and genitourinary tract. J. Am. Soc. Nephrol. 13:7 (2002), 1837–1846.
49. Steiner, H., et al. A loss of function mutation of presenilin-2 interferes with amyloid beta-peptide production and notch signaling. J. Biol. Chem. 274:40 (1999), 28669–28673.
50. Stratman, J.L., Barnes, W.M., Simon, T.C., Universal PCR genotyping assay that achieves single copy sensitivity with any primer pair. Transgenic Res. 12:4 (2003), 521–522.
51. Stubbs, J.L., et al. Multicilin promotes centriole assembly and ciliogenesis during multiciliate cell differentiation. Nat. Cell Biol. 14:2 (2012), 140–147.
52. Surendran, K., et al. The contribution of Notch1 to nephron segmentation in the developing kidney is revealed in a sensitized Notch2 background and can be augmented by reducing Mint dosage. Dev. Biol. 337:2 (2010), 386–395.
53. Surendran, K., et al. Reduced Notch signaling leads to renal cysts and papillary microadenomas. J. Am. Soc. Nephrol. 21:5 (2010), 819–832.
54. Tai, G., Hohenstein, P., Davies, J.A., Making immortalized cell lines from embryonic mouse kidney. Methods Mol. Biol. 886 (2012), 165–171.
55. Thiagarajan, R.D., et al. Identification of anchor genes during kidney development defines ontological relationships, molecular subcompartments and regulatory pathways. PLoS One, 6(2), 2011, e17286.
56. Trepiccione, F., et al. Evaluation of cellular plasticity in the collecting duct during recovery from lithium-induced nephrogenic diabetes insipidus. Am. J. Physiol. Ren. Physiol. 305:6 (2013), F919–F929.
57. Vidarsson, H., et al. The forkhead transcription factor Foxi1 is a master regulator of vacuolar H-ATPase proton pump subunits in the inner ear, kidney and epididymis. PLoS One, 4(2), 2009, e4471.
58. Wei, G.H., et al. Genome-wide analysis of ETS-family DNA-binding in vitro and in vivo. EMBO J. 29:13 (2010), 2147–2160.
59. Xiao, Z., et al. Dot1l deficiency leads to increased intercalated cells and upregulation of V-ATPase B1 in mice. Exp. Cell Res. 344:2 (2016), 167–175.
60. Ye, X., et al. Genetic mosaic analysis reveals a major role for frizzled 4 and frizzled 8 in controlling ureteric growth in the developing kidney. Development 138:6 (2011), 1161–1172.
61. Yu, J., et al. Identification of molecular compartments and genetic circuitry in the developing mammalian kidney. Development 139:10 (2012), 1863–1873.
62. Yu, J., Carroll, T.J., McMahon, A.P., Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development 129:22 (2002), 5301–5312.
63. Yu, L., et al. GATA2 regulates body water homeostasis through maintaining aquaporin 2 expression in renal collecting ducts. Mol. Cell Biol. 34:11 (2014), 1929–1941.