Cytokeratin 15 marks basal epithelia in developing ureters and is upregulated in a subset of urothelial cell carcinomas

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Tai, Guangping ^a,b   Ranjzad, Parisa ^a   Marriage, Fiona ^a   Rehman, Samrina ^b,c   Denley, Helen ^d   Dixon, Jill ^b   Mitchell, Karen ^b   Day, Philip J R ^a   Woolf, Adrian S ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d MANCHESTER ROYAL INFIRMARY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 15; PHOSPHOPROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTOME; TRP63 PROTEIN, MOUSE; UPK3A PROTEIN, MOUSE; UROPLAKIN 3;

AGED; ANIMAL; ANIMAL EMBRYO; BASAL CELL CARCINOMA; BLADDER TUMOR; CELL DIFFERENTIATION; CYTOLOGY; EMBRYOLOGY; EPITHELIUM CELL; FEMALE; FETUS; GENE EXPRESSION REGULATION; GENETICS; HOMOZYGOTE; HUMAN; MALE; METABOLISM; MIDDLE AGED; MORPHOGENESIS; MOUSE; PATHOLOGY; TISSUE MICROARRAY; URETER; UROTHELIUM;

AGED; ANIMALS; CARCINOMA, BASAL CELL; CELL DIFFERENTIATION; EMBRYO, MAMMALIAN; EPITHELIAL CELLS; FEMALE; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMOZYGOTE; HUMANS; KERATIN-15; MALE; MICE; MIDDLE AGED; MORPHOGENESIS; PHOSPHOPROTEINS; TISSUE ARRAY ANALYSIS; TRANS-ACTIVATORS; TRANSCRIPTOME; URETER; URINARY BLADDER NEOPLASMS; UROPLAKIN III; UROTHELIUM;

EID: 84894149930     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081167     Document Type: Article

References (45)

1. Lye CM, Fasano L, Woolf AS (2010) Ureter myogenesis: putting Teashirt into context. J Am Soc Nephrol 21: 24-30. doi:10.1681/ASN.2008111206. PubMed: 19926888.
2. Woolf AS, Davies JA (2013) Cell biology of ureter development. J Am Soc Nephrol 24: 19-25. doi:10.1681/ASN.2012020127. PubMed: 23123402.
3. Zhao H, Kegg H, Grady S, Truong HT, Robinson ML et al. (2004) Role of fibroblast growth factor receptors 1 and 2 in the ureteric bud. Dev Biol 276: 403-415. doi:10.1016/j.ydbio.2004.09.002. PubMed: 15581874. (Pubitemid 39592403)
4. Michos O, Cebrian C, Hyink D, Grieshammer U, Williams L et al. (2010) Kidney development in the absence of Gdnf and Spry1 requires Fgf10. PLOS Genet 6: e1000809. PubMed: 20084103.
5. Pitera JE, Woolf AS, Basson MA, Scambler PJ (2012) Sprouty1 haploinsufficiency prevents renal agenesis in a model of Fraser syndrome. J Am Soc Nephrol 23: 1790-1796. doi:10.1681/ASN.2012020146. PubMed: 23064016.
6. Yu J, Carroll TJ, McMahon AP (2002) Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development 129: 5301-5312. PubMed: 12399320. (Pubitemid 35460691)
7. Caubit X, Lye CM, Martin E, Coré N, Long DA et al. (2008) Teashirt 3 is necessary for ureteral smooth muscle differentiation downstream of SHH and BMP4. Development 135: 3301-3310. doi:10.1242/dev.022442. PubMed: 18776146.
8. Jenkins D, Woolf AS (2007) Uroplakins: new molecular players in the biology of urinary tract malformations. Kidney Int 71: 195-200. doi:10.1038/sj.ki.5002053. PubMed: 17183244. (Pubitemid 46164745)
9. Wu XR, Kong XP, Pellicer A, Kreibich G, Sun TT (2009) Uroplakins in urothelial biology, function, and disease. Kidney Int 75: 1153-1165. doi:10.1038/ki.2009.73. PubMed: 19340092.
10. Kong XT, Deng FM, Hu P, Liang FX, Zhou G et al. (2004) Roles of uroplakins in plaque formation, umbrella cell enlargement, and urinary tract diseases. J Cell Biol 167: 1195-1204. doi:10.1083/jcb.200406025. PubMed: 15611339. (Pubitemid 40066633)
11. Jenkins D, Bitner-Glindzicz M, Malcolm S, Hu CC, Allison J et al. (2005) De novo Uroplakin IIIa heterozygous mutations cause human renal adysplasia leading to severe kidney failure. J Am Soc Nephrol 16: 2141-2149. doi:10.1681/ASN.2004090776. PubMed: 15888565. (Pubitemid 41716446)
12. Whitbread LA, Powell BC (1998) Expression of the intermediate filament keratin gene, K15, in the basal cell layers of epithelia and the hair follicle. Exp Cell Res 244: 448-459. doi:10.1006/excr.1998.4217. PubMed: 9806795. (Pubitemid 28507060)
13. Waseem A, Dogan B, Tidman N, Alam Y, Purkis P et al. (1999) Keratin 15 expression in stratified epithelia: downregulation in activated keratinocytes. J Invest Dermatol 112: 362-369. doi:10.1046/j.1523-1747.1999.00535.x. PubMed: 10084315. (Pubitemid 29125114)
14. Liu Y, Lyle S, Yang Z, Cotsarelis G (2003) Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J Invest Dermatol 121: 963-968. doi:10.1046/j.1523-1747.2003.12600.x. PubMed: 14708593. (Pubitemid 37430960)
15. Ito M, Liu Y, Yang Z, Nguyen J, Liang F, Morris RJ, Cotsarelis G (2005) Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 11: 1351-1354. doi:10.1038/nm1328. PubMed: 16288281. (Pubitemid 41752917)
16. Garza LA, Yang CC, Zhao T, Blatt HB, Lee M et al. (2011) Bald scalp in men with androgenetic alopecia retains hair follicle stem cells but lacks CD200-rich and CD34-positive hair follicle progenitor cells. J Clin Invest 121: 613-622. doi:10.1172/JCI44478. PubMed: 21206086.
17. Wang GY, Wang J, Mancianti ML, Epstein EH Jr (2011) Basal cell carcinomas arise from hair follicle stem cells in Ptch1(+/-) mice. Cancer Cell 19: 114-124. doi:10.1016/j.ccr.2010.11.007. PubMed: 21215705.
18. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N et al. (1999) p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398: 714-718. doi:10.1038/19539. PubMed: 10227294. (Pubitemid 29197650)
19. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR et al. (1999) p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398: 708-713. doi:10.1038/19531. PubMed: 10227293. (Pubitemid 29197649)
20. Burgu B, Medina Ortiz WE, Pitera JE, Woolf AS et al. (2007) Vascular endothelial growth factor mediates hypoxic stimulated embryonic bladder growth in organ culture. J Urol 177: 1552-1557. doi:10.1016/j.juro.2006.12.011. PubMed: 17382777. (Pubitemid 46442735)
21. Long DA, Kolatsi-Joannou M, Price KL, Dessapt-Baradez C, Huang JL et al. (2013) Albuminuria is associated with too few glomeruli and too much testosterone. Kidney Int 83: 1118-1129. doi:10.1038/ki.2013.45. PubMed: 23447063.
22. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80. doi:10.1186/gb-2004-5-10-r80. PubMed: 15461798.
23. Pearson RD, Liu X, Sanguinetti G, Milo M, Lawrence ND et al. (2009) puma: a bioconductor package for propagating uncertainty in microarray analysis. BMC Bioinformatics 10: 211. doi:10.1186/1471-2105-10-211. PubMed: 19589155.
24. Cheng W, Jacobs WB, Zhang JJ, Moro A, Park JH et al. (2006) ΔNp63 plays an anti-apoptotic role in ventral bladder development. Development 133: 4783-4792. doi:10.1242/dev.02621. PubMed: 17079275. (Pubitemid 46063090)
25. Qiao J, Uzzo R, Obara-Ishihara T, Degenstein L, Fuchs E et al. (1999) FGF-7 modulates ureteric bud growth and nephron number in the developing kidney. Development 126: 547-554. PubMed: 9876183. (Pubitemid 29082041)
26. Bassuk JA, Cochrane K, Mitchell ME (2003) Induction of urothelial cell proliferation by fibroblast growth factor-7 in RAG1-deficient mice. Adv Exp Med Biol 539: 623-633. PubMed: 15176316.
27. Leube RE, Bader BL, Bosch FX, Zimbelmann R, Achtstaetter T et al. (1988) Molecular characterization and expression of the stratification-related cytokeratins 4 and 15. J Cell Biol 106: 1249-1261. doi:10.1083/jcb.106.4.1249. PubMed: 2452170.
28. Smedts F, Ramaekers F, Leube RE, Keijser K, Link M et al. (1993) Expression of keratins 1, 6, 15, 16, and 20 in normal cervical epithelium, squamous metaplasia, cervical intraepithelial neoplasia, and cervical carcinoma. Am J Pathol 142: 403-412. (Pubitemid 23057453)
29. Figueira EC, Di Girolamo N, Coroneo MT, Wakefield D (2007) The phenotype of limbal epithelial stem cells. Invest Ophthalmol Vis Sci 48: 144-156. doi:10.1167/iovs.06-0346. PubMed: 17197527. (Pubitemid 47251397)
30. Peters B, Kirfel J, Büssow H, Vidal M, Magin TM (2001) Complete cytolysis and neonatal lethality in keratin 5 knockout mice reveal its fundamental role in skin integrity and in epidermolysis bullosa simplex. Mol Cell Biol 12: 1775-1789. doi:10.1091/mbc.12.6.1775. PubMed: 11408584. (Pubitemid 33049729)
31. Glazier DB, Zaontz MR (1998) Epidermolysis bullosa: a review of the associated urological complications. J Urol 159: 2122-2125. doi:10.1016/S0022- 5347(01)63291-9. PubMed: 9598555. (Pubitemid 29190792)
32. Keyes WM, Pecoraro M, Aranda V, Vernersson-Lindahl E, Li W et al. (2011) ΔNp63α is an oncogene that targets chromatin remodeler Lsh to drive skin stem cell proliferation and tomourigenesis. Cell Stem Cell 8: 164-176. doi:10.1016/j.stem.2010.12.009. PubMed: 21295273.
33. Karni-Schmidt O, Castillo-Martin M, Shen TH, Gladoun N, Domingo-Domenech J et al. (2011) Distinct expression profiles of p63 variants during urothelial development and bladder cancer progression. Am J Pathol 178: 1350-1360. doi:10.1016/j.ajpath.2010.11.061. PubMed: 21356385.
34. Pignon JC, Grisanzio C, Geng Y, Song J, Shivdasani RA et al. (2013) p63-expressing cells are the stem cells of developing prostate, bladder, and colorectal epithelia. Proc Natl Acad Sci U S A 110: 8105-8110. doi:10.1073/pnas.1221216110. PubMed: 23620512.
35. Signoretti S, Pires MM, Lindauer M, Horner JW, Grisanzio C et al. (2005) p63 regulates commitment to the prostate cell lineage. Proc Natl Acad Sci U S A 102: 11355-11360. doi:10.1073/pnas.0500165102. PubMed: 16051706. (Pubitemid 41153824)
36. Wilkins S, Zhang KW, Mahfuz I, Quantin R, D'Cruz N et al. (2012) Insertion/deletion polymorphisms in the ΔNp63 promoter are a risk factor for bladder exstrophy epispadias complex. PLOS Genet 8: e1003070. PubMed: 23284286.
37. Kouwenhoven EN, van Heeringen SJ, Tena JJ, Oti M, Dutilh BE et al. (2010) Genome-wide profiling of p63 DNA-binding sites identifies an element that regulates gene expression during limb development in the 7q21 SHFM1 locus. PLoS Genet 6: e1001065.
38. Lughezzani G, Burger M, Margulis V, Matin SF, Novara G et al. (2012) Prognostic factors in upper urinary tract urothelial carcinomas: a comprehensive review of the current literature. Eur Urol 62: 100-114. doi:10.1016/j.eururo. 2012.02.030. PubMed: 22381168.
39. Green DA, Rink M, Xylinas E, Matin SF, Stenzl A et al. (2013) Urothelial carcinoma of the bladder and the upper tract: disparate twins. J Urol 189: 1214-1221. doi:10.1016/j.juro.2012.05.079. PubMed: 23023150.
40. Kim JJ (2012) Recent advances in treatment of advanced urothelial carcinoma. Curr Urol Rep 13: 147-152. doi:10.1007/s11934-012-0238-0. PubMed: 22367511.
41. Burger M, Catto JW, Dalbagni G, Grossman HB, Herr H et al. (2013) Epidemiology and risk factors of urothelial bladder cancer. Eur Urol 63: 234-241. doi:10.1016/j.eururo.2012.07.033. PubMed: 22877502.
42. Yates DR, Catto JW (2013) Distinct patterns and behaviour of urothelial carcinoma with respect to anatomical location: how molecular biomarkers can augment clinico-pathological predictors in upper urinary tract tumours. World J Urol 31: 21-29. doi:10.1007/s00345-012-0946-6. PubMed: 22986906.
43. Gabriel U, Li L, Bolenz C, Steidler A, Kränzlin B, Saile M et al. (2012) New insights into the influence of cigarette smoking on urothelial carcinogenesis: smoking-induced gene expression in tomour-free urothelium might discriminate muscle-invasive from nonmuscle-invasive urothelial bladder cancer. Mol Carcinog 51: 907-915. doi:10.1002/mc.20860. PubMed: 21976419.
44. Elsamman E, Fukumori T, Ewis AA, Ali N, Kajimoto K et al. (2006) Differences in gene expression between noninvasive and invasive transitional cell carcinoma of the human bladder using complementary deoxyribonucleic acid microarray: preliminary results. Urol Oncol 24: 109-115. doi:10.1016/j.urolonc. 2005.07.011. PubMed: 16520272. (Pubitemid 43348356)
45. Choi W, Shah JB, Tran M, Svatek R, Marquis L et al. (2012) p63 expression defines a lethal subset of muscle-invasive bladder cancers. PLOS ONE 7: e30206. doi:10.1371/journal.pone.0030206. PubMed: 22253920.