Kruppel-like factor 5 is required for formation and differentiation of the bladder urothelium

Developmental Biology

Volumn 358, Issue 1, 2011, Pages 79-90

  Bell, Sheila M ^a   Zhang, Liqian ^a   Mendell, Angela ^a   Xu, Yan ^a   Haitchi, Hans Michael ^a,b   Lessard, James L ^a   Whitsett, Jeffrey A ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Bladder; GRHL3; KLF5; Micro CT; Urothelium; Vesicoureteral reflux

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; KRUPPEL LIKE FACTOR 5; MESSENGER RNA; SONIC HEDGEHOG PROTEIN;

ALLELE; ANIMAL TISSUE; ARTICLE; BLADDER EPITHELIUM; BLADDER NECK; CELL DIFFERENTIATION; DETRUSOR MUSCLE; EMBRYO; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; FETUS; GENE DELETION; HYDRONEPHROSIS; HYDROURETER; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSGENE; URETHRA; UROTHELIUM; VESICOURETERAL REFLUX;

MURINAE;

EID: 80052619766     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.07.020     Document Type: Article

References (73)

1. Acharya P., Beckel J., Ruiz W.G., Wang E., Rojas R., Birder L., Apodaca G. Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium. Am. J. Physiol. Renal Physiol. 2004, 287:F305-F318.
2. Airik R., Bussen M., Singh M.K., Petry M., Kispert A. Tbx18 regulates the development of the ureteral mesenchyme. J. Clin. Invest. 2006, 116:663-674.
3. Airik R., Trowe M.O., Foik A., Farin H.F., Petry M., Schuster-Gossler K., Schweizer M., Scherer G., Kist R., Kispert A. Hydroureternephrosis due to loss of Sox9-regulated smooth muscle cell differentiation of the ureteric mesenchyme. Hum. Mol. Genet. 2010, 19:4918-4929.
4. Auden A., Caddy J., Wilanowski T., Ting S.B., Cunningham J.M., Jane S.M. Spatial and temporal expression of the grainyhead-like transcription factor family during murine development. Gene Expr. Patterns 2006, 6:964-970.
5. Ayres P.H., Shinohara Y., Frith C.H. Morphological observations on the epithelium of the developing urinary bladder of the mouse and rat. J. Urol. 1985, 133:506-512.
6. Baskin L.S., Hayward S.W., Young P.F., Cunha G.R. Ontogeny of the rat bladder: smooth muscle and epithelial differentiation. Acta Anat. 1996, 155:163-171.
7. Bateman N.W., Tan D., Pestell R.G., Black J.D., Black A.R. Intestinal tumor progression is associated with altered function of KLF5. J. Biol. Chem. 2004, 279:12093-12101.
8. Cartharius K., Frech K., Grote K., Klocke B., Haltmeier M., Klingenhoff A., Frisch M., Bayerlein M., Werner T. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 2005, 21:2933-2942.
9. Chang C.P., McDill B.W., Neilson J.R., Joist H.E., Epstein J.A., Crabtree G.R., Chen F. Calcineurin is required in urinary tract mesenchyme for the development of the pyeloureteral peristaltic machinery. J. Clin. Invest. 2004, 113:1051-1058.
10. Chen C., Benjamin M.S., Sun X., Otto K.B., Guo P., Dong X.Y., Bao Y., Zhou Z., Cheng X., Simons J.W., Dong J.T. KLF5 promotes cell proliferation and tumorigenesis through gene regulation and the TSU-Pr1 human bladder cancer cell line. Int. J. Cancer 2006, 118:1346-1355.
11. Cheng W., Jacobs W.B., Zhang J.J., Moro A., Park J.H., Kushida M., Qiu W., Mills A.A., Kim P.C. DeltaNp63 plays an anti-apoptotic role in ventral bladder development. Development 2006, 133:4783-4792.
12. Cheng W., Yeung C.K., Ng Y.K., Zhang J.R., Hui C.C., Kim P.C. Sonic Hedgehog mediator Gli2 regulates bladder mesenchymal patterning. J. Urol. 2008, 180:1543-1550.
13. Council L., Hameed O. Differential expression of immunohistochemical markers in bladder smooth muscle and myofibroblasts, and the potential utility of desmin, smoothelin, and vimentin in staging of bladder carcinoma. Mod. Pathol. 2009, 22:639-650.
14. Degenhardt K., Wright A.C., Horng D., Padmanabhan A., Epstein J.A. Rapid 3D phenotyping of cardiovascular development in mouse embryos by micro-CT with iodine staining. Circ. Cardiovasc. Imaging 2010, 3:314-322.
15. Denes F.T., Arap M.A., Giron A.M., Silva F.A., Arap S. Comprehensive surgical treatment of prune belly syndrome: 17years' experience with 32 patients. Urology 2004, 64:789-793. (discussion 793-4).
16. Drake M.J., Fry C.H., Eyden B. Structural characterization of myofibroblasts in the bladder. BJU Int. 2006, 97:29-32.
17. Ema M., Mori D., Niwa H., Hasegawa Y., Yamanaka Y., Hitoshi S., Mimura J., Kawabe Y., Hosoya T., Morita M., Shimosato D., Uchida K., Suzuki N., Yanagisawa J., Sogawa K., Rossant J., Yamamoto M., Takahashi S., Fujii-Kuriyama Y. Kruppel-like factor 5 is essential for blastocyst development and the normal self-renewal of mouse ESCs. Cell Stem Cell 2008, 3:555-567.
18. Erman A., Veranic P., Psenicnik M., Jezernik K. Superficial cell differentiation during embryonic and postnatal development of mouse urothelium. Tissue Cell 2006, 38:293-301.
19. Feldman R.J., Sementchenko V.I., Watson D.K. The epithelial-specific Ets factors occupy a unique position in defining epithelial proliferation, differentiation and carcinogenesis. Anticancer. Res. 2003, 23:2125-2131.
20. Finch P.W., Cunha G.R., Rubin J.S., Wong J., Ron D. Pattern of keratinocyte growth factor and keratinocyte growth factor receptor expression during mouse fetal development suggests a role in mediating morphogenetic mesenchymal-epithelial interactions. Dev. Dyn. 1995, 203:223-240.
21. Fry C.H., Sui G.P., Kanai A.J., Wu C. The function of suburothelial myofibroblasts in the bladder. Neurourol. Urodyn. 2007, 26:914-919.
22. Haraguchi R., Motoyama J., Sasaki H., Satoh Y., Miyagawa S., Nakagata N., Moon A., Yamada G. Molecular analysis of coordinated bladder and urogenital organ formation by Hedgehog signaling. Development 2007, 134:525-533.
23. Harfe B.D., Scherz P.J., Nissim S., Tian H., McMahon A.P., Tabin C.J. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 2004, 118:517-528.
24. Harris K.S., Zhang Z., McManus M.T., Harfe B.D., Sun X. Dicer function is essential for lung epithelium morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2208-2213.
25. Hu P., Deng F.M., Liang F.X., Hu C.M., Auerbach A.B., Shapiro E., Wu X.R., Kachar B., Sun T.T. Ablation of uroplakin III gene results in small urothelial plaques, urothelial leakage, and vesicoureteral reflux. J. Cell Biol. 2000, 151:961-972.
26. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
27. Iizuka-Kogo A., Ishidao T., Akiyama T., Senda T. Abnormal development of urogenital organs in Dlgh1-deficient mice. Development 2007, 134:1799-1807.
28. Ingraham S.E., Saha M., Carpenter A.R., Robinson M., Ismail I., Singh S., Hains D., Robinson M.L., Hirselj D.A., Koff S.A., Bates C.M., McHugh K.M. Pathogenesis of renal injury in the megabladder mouse: a genetic model of congenital obstructive nephropathy. Pediatr. Res. 2010, 68:500-507.
29. Jain S., Pulikuri S., Zhu Y., Qi C., Kanwar Y.S., Yeldandi A.V., Rao M.S., Reddy J.K. Differential expression of the peroxisome proliferator-activated receptor gamma (PPARgamma) and its coactivators steroid receptor coactivator-1 and PPAR-binding protein PBP in the brown fat, urinary bladder, colon, and breast of the mouse. Am. J. Pathol. 1998, 153:349-354.
30. Jiang J., Chan Y.S., Loh Y.H., Cai J., Tong G.Q., Lim C.A., Robson P., Zhong S., Ng H.H. A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat. Cell Biol. 2008, 10:353-360.
31. Kerecuk L., Schreuder M.F., Woolf A.S. Renal tract malformations: perspectives for nephrologists. Nat. Clin. Pract. Nephrol. 2008, 4:312-325.
32. Kohno Y., Okamoto T., Ishibe T., Nagayama S., Shima Y., Nishijo K., Shibata K.R., Fukiage K., Otsuka S., Uejima D., Araki N., Naka N., Nakashima Y., Aoyama T., Nakayama T., Nakamura T., Toguchida J. Expression of claudin7 is tightly associated with epithelial structures in synovial sarcomas and regulated by an Ets family transcription factor, ELF3. J. Biol. Chem. 2006, 281:38941-38950.
33. Kong X.T., Deng F.M., Hu P., Liang F.X., Zhou G., Auerbach A.B., Genieser N., Nelson P.K., Robbins E.S., Shapiro E., Kachar B., Sun T.T. Roles of uroplakins in plaque formation, umbrella cell enlargement, and urinary tract diseases. J. Cell Biol. 2004, 167:1195-1204.
34. Li B., Mackay D.R., Dai Q., Li T.W., Nair M., Fallahi M., Schonbaum C.P., Fantes J., Mahowald A.P., Waterman M.L., Fuchs E., Dai X. The LEF1/beta-catenin complex activates movo1, a mouse homolog of Drosophila ovo required for epidermal appendage differentiation. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:6064-6069.
35. Li J., Shiroyanagi Y., Lin G., Haqq C., Lin C.S., Lue T.F., Willingham E., Baskin L.S. Serum response factor, its cofactors, and epithelial-mesenchymal signaling in urinary bladder smooth muscle formation. Differentiation 2006, 74:30-39.
36. McCloskey K.D. Interstitial cells in the urinary bladder-localization and function. Neurourol. Urodyn. 2010, 29:82-87.
37. McConnell B.B., Ghaleb A.M., Nandan M.O., Yang V.W. The diverse functions of Kruppel-like factors 4 and 5 in epithelial biology and pathobiology. BioEssays 2007, 29:549-557.
38. Mendelsohn C., Lohnes D., Decimo D., Lufkin T., LeMeur M., Chambon P., Mark M. Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 1994, 120:2749-2771.
39. Murawski I.J., Myburgh D.B., Favor J., Gupta I.R. Vesico-ureteric reflux and urinary tract development in the Pax2 1Neu+/- mouse. Am. J. Physiol. Renal Physiol. 2007, 293:F1736-F1745.
40. Murawski I.J., Gupta I.R. Gene discovery and vesicoureteric reflux. Pediatr. Nephrol. 2008, 23:1021-1027.
41. Murer L., Benetti E., Artifoni L. Embryology and genetics of primary vesico-ureteric reflux and associated renal dysplasia. Pediatr. Nephrol. 2007, 22:788-797.
42. Mysorekar I.U., Mulvey M.A., Hultgren S.J., Gordon J.I. Molecular regulation of urothelial renewal and host defenses during infection with uropathogenic Escherichia coli. J. Biol. Chem. 2002, 277:7412-7419.
43. Nair M., Teng A., Bilanchone V., Agrawal A., Li B., Dai X. Ovol1 regulates the growth arrest of embryonic epidermal progenitor cells and represses c-myc transcription. J. Cell Biol. 2006, 173:253-264.
44. Nandan M.O., Yoon H.S., Zhao W., Ouko L.A., Chanchevalap S., Yang V.W. Kruppel-like factor 5 mediates the transforming activity of oncogenic H-Ras. Oncogene 2004, 23:3404-3413.
45. Nandan M.O., Chanchevalap S., Dalton W.B., Yang V.W. Kruppel-like factor 5 promotes mitosis by activating the cyclin B1/Cdc2 complex during oncogenic Ras-mediated transformation. FEBS Lett. 2005, 579:4757-4762.
46. Nandan M.O., Yang V.W. The role of Kruppel-like factors in the reprogramming of somatic cells to induced pluripotent stem cells. Histol. Histopathol. 2009, 24:1343-1355.
47. Ng A.Y., Waring P., Ristevski S., Wang C., Wilson T., Pritchard M., Hertzog P., Kola I. Inactivation of the transcription factor Elf3 in mice results in dysmorphogenesis and altered differentiation of intestinal epithelium. Gastroenterology 2002, 122:1455-1466.
48. Nie X., Sun J., Gordon R.E., Cai C.L., Xu P.X. SIX1 acts synergistically with TBX18 in mediating ureteral smooth muscle formation. Development 2010, 137:755-765.
49. Oettgen P., Alani R.M., Barcinski M.A., Brown L., Akbarali Y., Boltax J., Kunsch C., Munger K., Libermann T.A. Isolation and characterization of a novel epithelium-specific transcription factor, ESE-1, a member of the ets family. Mol. Cell. Biol. 1997, 17:4419-4433.
50. Oishi Y., Manabe I., Tobe K., Tsushima K., Shindo T., Fujiu K., Nishimura G., Maemura K., Yamauchi T., Kubota N., Suzuki R., Kitamura T., Akira S., Kadowaki T., Nagai R. Kruppel-like transcription factor KLF5 is a key regulator of adipocyte differentiation. Cell Metab. 2005, 1:27-39.
51. Parisi S., Cozzuto L., Tarantino C., Passaro F., Ciriello S., Aloia L., Antonini D., De Simone V., Pastore L., Russo T. Direct targets of Klf5 transcription factor contribute to the maintenance of mouse embryonic stem cell undifferentiated state. BMC Biol. 2010, 8:128.
52. Pedersen A., Skjong C., Shawlot W. Lim 1 is required for nephric duct extension and ureteric bud morphogenesis. Dev. Biol. 2005, 288:571-581.
53. Romih R., Korosec P., de Mello W., Jezernik K. Differentiation of epithelial cells in the urinary tract. Cell Tissue Res. 2005, 320:259-268.
54. Seifert A.W., Harfe B.D., Cohn M.J. Cell lineage analysis demonstrates an endodermal origin of the distual urethra and perineum. Dev. Biol. 2008, 318:143-152.
55. Signoretti S., Pires M.M., Lindauer M., Horner J.W., Grisanzio C., Dhar S., Majumder P., McKeon F., Kantoff P.W., Sellers W.R., Loda M. p63 regulates commitment to the prostate cell lineage. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:11355-11360.
56. Singh S., Robinson M., Nahi F., Coley B., Robinson M.L., Bates C.M., Kornacker K., McHugh K.M. Identification of a unique transgenic mouse line that develops megabladder, obstructive uropathy, and renal dysfunction. J. Am. Soc. Nephrol. 2007, 18:461-471.
57. Smith F.J., Porter R.M., Corden L.D., Lunny D.P., Lane E.B., McLean W.H. Cloning of human, murine, and marsupial keratin 7 and a survey of K7 expression in the mouse. Biochem. Biophys. Res. Commun. 2002, 297:818-827.
58. Srinivas S., Wu Z., Chen C.M., D'Agati V., Costantini F. Dominant effects of RET receptor misexpression and ligand-independent RET signaling on ureteric bud development. Development 1999, 126:1375-1386.
59. Sun R., Chen X., Yang V.W. Intestinal-enriched Kruppel-like factor (Kruppel-like factor 5) is a positive regulator of cellular proliferation. J. Biol. Chem. 2001, 276:6897-6900.
60. Tash J.A., David S.G., Vaughan E.E., Herzlinger D.A. Fibroblast growth factor-7 regulates stratification of the bladder urothelium. J. Urol. 2001, 166:2536-2541.
61. Tasian G., Cunha G., Baskin L. Smooth muscle differentiation and patterning in the urinary bladder. Differentiation 2010, 80:106-117.
62. Teng A., Nair M., Wells J., Segre J.A., Dai X. Strain-dependent perinatal lethality of Ovol1-deficient mice and identification of Ovol2 as a downstream target of Ovol1 in skin epidermis. Biochim. Biophys. Acta 2007, 1772:89-95.
63. Ting S.B., Caddy J., Hislop N., Wilanowski T., Auden A., Zhao L.L., Ellis S., Kaur P., Uchida Y., Holleran W.M., Elias P.M., Cunningham J.M., Jane S.M. A homolog of Drosophila grainy head is essential for epidermal integrity in mice. Science 2005, 308:411-413.
64. Varley C.L., Stahlschmidt J., Lee W.C., Holder J., Diggle C., Selby P.J., Trejdosiewicz L.K., Southgate J. Role of PPARgamma and EGFR signalling in the urothelial terminal differentiation programme. J Cell Sci. 2004, 117:2029-2036.
65. Varley C.L., Garthwaite M.A., Cross W., Hinley J., Trejdosiewicz L.K., Southgate J. PPARgamma-regulated tight junction development during human urothelial cytodifferentiation. J. Cell. Physiol. 2006, 208:407-417.
66. Varley C.L., Bacon E.J., Holder J.C., Southgate J. FOXA1 and IRF-1 intermediary transcriptional regulators of PPARgamma-induced urothelial cytodifferentiation. Cell Death Differ. 2009, 16:103-114.
67. Wan H., Luo F., Wert S.E., Zhang L., Xu Y., Ikegami M., Maeda Y., Bell S.M., Whitsett J.A. Kruppel-like factor 5 is required for perinatal lung morphogenesis and function. Development 2008, 135:2563-2572.
68. Wu X.R., Kong X.P., Pellicer A., Kreibich G., Sun T.T. Uroplakins in urothelial biology, function, and disease. Kidney Int. 2009, 75:1153-1165.
69. Xu Y., Saegusa C., Schehr A., Grant S., Whitsett J.A., Ikegami M. C/EBP{alpha} is required for pulmonary cytoprotection during hyperoxia. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 297:L286-L298.
70. Yang Y., Goldstein B.G., Nakagawa H., Katz J.P. Kruppel-like factor 5 activates MEK/ERK signaling via EGFR in primary squamous epithelial cells. FASEB J. 2007, 21:543-550.
71. Yu J., Carroll T.J., McMahon A.P. Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development 2002, 129:5301-5312.
72. Yu O.H., Murawski I.J., Myburgh D.B., Gupta I.R. Overexpression of RET leads to vesicoureteric reflux in mice. Am. J. Physiol. Renal Physiol. 2004, 287:F1123-F1130.
73. Yu Z., Mannik J., Soto A., Lin K.K., Andersen B. The epidermal differentiation-associated grainyhead gene Get1/Grhl3 also regulates urothelial differentiation. EMBO J. 2009, 28:1890-1903.