Cellular basis of urothelial squamous metaplasia: Roles of lineage heterogeneity and cell replacement

Journal of Cell Biology

Volumn 171, Issue 5, 2005, Pages 835-844

  Liang, Feng Xia ^a   Bosland, Maarten C ^a   Huang, Hongying ^a   Romih, Rok ^b   Baptiste, Solange ^a   Deng, Fang Ming ^a   Wu, Xue Ru ^a   Shapiro, Ellen ^a   Sun, Tung Tien ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

KERATIN; UROPLAKIN;

ANIMAL TISSUE; ARTICLE; CELL HETEROGENEITY; CELL LINEAGE; CELL MIGRATION; KERATINIZATION; METAPLASIA; NONHUMAN; PRIORITY JOURNAL; RETINOL DEFICIENCY; SQUAMOUS CELL METAPLASIA; UROTHELIUM;

ANIMALS; BIOLOGICAL MARKERS; CATTLE; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; EPITHELIAL CELLS; FEMALE; KERATINS; MALE; METAPLASIA; MICE; URETER; URINARY BLADDER; UROTHELIUM; VITAMIN A;

ANIMALIA; MAMMALIA;

EID: 28544434424     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200505035     Document Type: Article

References (69)

1. Akdas, A., and L. Turkeri. 1991. The impact of squamous metaplasia in transitional cell carcinoma of the bladder. Int. Urol. Nephrol. 23:333-336.
2. Apodaca, G. 2004. The uroepithelium: not just a passive barrier. Traffic. 5:117-128.
3. Atala, A. 2002. Future trends in bladder reconstructive surgery. Semin. Pediatr. Surg. 11:134-142.
4. Baker, L.A., and R.A. Gomez. 1998. Embryonic development of the ureter. Semin. Nephrol. 18:569-584.
5. Batourina, E., C. Choi, N. Paragas, N. Bello, T. Hensle, F.D. Costantini, A. Schuchardt, R.L. Bacallao, and C.L. Mendelsohn. 2002. Distal ureter morphogenesis depends on epithelial cell remodeling mediated by vitamin A and Ret. Nat. Genet. 32:109-115.
6. Batourina, E., S. Tsai, S. Lambert, P. Sprenkle, R. Viana, S. Dutta, T. Hensle, F. Wang, K. Niederreither, A.P. McMahon, T.J. Carroll, and C.L. Mendelsohn. 2005. Apoptosis induced by vitamin A signaling is crucial for connecting the ureters to the bladder. Nat. Genet. 37:1082-1089.
7. Chen, Y., X. Guo, F.M. Deng, F.X. Liang, W. Sun, M. Ren, T. Izumi, D.D. Sabatini, T.T. Sun, and G. Kreibich. 2003. Rab27b is associated with fusiform vesicles and may be involved in targeting uroplakins to urothelial apical membranes. Proc. Natl. Acad. Sci. USA. 100:14012-14017.
8. Cohen, S.M., and L.B. Ellwein. 1990. Cell proliferation in carcinogenesis. Science. 249:1007-1011.
9. Cotsarelis, G., S.Z. Cheng, G. Dong, T.-T. Sun, and R.M. Lavker. 1989. Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: implications on epithelial stem cells. Cell. 57:201-209.
10. Coulson, W.F. 1989. Clinical importance of squamous metaplasia in invasive transitional cell carcinoma of the bladder. J. Clin. Pathol. 42:1227-1228.
11. Cunha, G.R., H. Fujii, B.L. Neubauer, J.M. Shannon, L. Sawyer, and B.A. Reese. 1983. Epithelial-mesenchymal interactions in prostatic development. I. morphological observations of prostatic induction by urogenital sinus mesenchyme in epithelium of the adult rodent urinary bladder. J. Cell Biol. 96:1662-1670.
12. Cunha, G.R., P. Young, S.J. Higgins, and P.S. Cooke. 1991. Neonatal seminal vesicle mesenchyme induces a new morphological and functional phenotype in the epithelia of adult ureter and ductus deferens. Development. 111:145-158.
13. Darwiche, N., G. Celli, L. Sly, F. Lancillotti, and L.M. De Luca. 1993. Retinoid status controls the appearance of reserve cells and keratin expression in mouse cervical epithelium. Cancer Res. 53:2287-2299.
14. De Luca, L.M., R.L. Shores, E.F. Spangler, and M.L. Wenk. 1989. Inhibition of initiator-promoter-induced skin tumorigenesis in female SENCAR mice fed a vitamin A-deficient diet and reappearance of tumors in mice fed a diet adequate in retinoid or beta-carotene. Cancer Res. 49:5400-5406.
15. Deng, F.M., F.X. Liang, L. Tu, K.A. Resing, P. Hu, M. Supino, C.C. Hu, G. Zhou, M. Ding, G. Kreibich, and T.T. Sun. 2002. Uroplakin IIIb, a urothelial differentiation marker, dimerizes with uroplakin Ib as an early step of urothelial plaque assembly. J. Cell Biol. 159:685-694.
16. Donjacour, A.A., and G.R. Cunha. 1993. Assessment of prostatic protein secretion in tissue recombinants made of urogenital sinus mesenchyme and urothelium from normal or androgen-insensitive mice. Endocrinology. 132:2342-2350.
17. Doran, T.I., A. Vidrich, and T.-T. Sun. 1980. Intrinsic and extrinsic regulation of the differentiation of skin, corneal and esophageal epithelial cells. Cell. 22:17-25.
18. Eichner, R., P. Bonitz, and T.-T. Sun. 1984. Classification of epidermal keratins according to their immunoreactivity, isoelectric point, and mode of expression. J. Cell Biol. 98:1388-1396.
19. Foster, C.S., A. Dodson, A.D. Desmond, and M. Fordham. 2004. Embryology and anatomy of the urinary bladder. In Pathology of the Urinary Bladder. W.B. Saunders Co., Philadelphia. 1-14.
20. Gijbels, M.J., F. van der Ham, A.M. van Bennekum, H.F. Hendriks, and P.J. Roholl. 1992. Alterations in cytokeratin expression precede histological changes in epithelia of vitamin A-deficient rats. Cell Tissue Res. 268:197-203.
21. Gillen, P., P. Keeling, P.J. Byrne, A.B. West, and T.P. Hennessy. 1988. Experimental columnar metaplasia in the canine oesophagus. Br. J. Surg. 75:113-115.
22. Gosling, J.A., and J.S. Dixon. 1995. Embryology and anatomy. In The Bladder. J.M. Fitzpatrick and R.J. Krane, editors. Churchill Livingstone, Edinburgh. 1-16.
23. Hicks, R.M. 1965. The fine structure of the transitional epithelium of rat ureter. J. Cell Biol. 26:25-48.
24. Hicks, R.M. 1968. Hyperplasia and cornification of the transitional epithelium in the vitamin A-deficient rat. Changes in fine structure of the cells. J. Ultrastruct. Res. 22:206-230.
25. Hu, P., F.M. Deng, F.X. Liang, C.M. Hu, A.B. Auerbach, E. Shapiro, X.R. Wu, B. Kachar, and T.T. Sun. 2000. Ablation of uroplakin III gene results in small urothelial plaques, urothelial leakage, and vesicoureteral reflux. J. Cell Biol. 151:961-972.
26. Hu, P., S. Meyers, F.X. Liang, F.M. Deng, B. Kachar, M.L. Zeidel, and T.T. Sun. 2002. Role of membrane proteins in permeability barrier function: uroplakin ablation elevates urothelial permeability. Am. J. Physiol. Renal Physiol. 283:F1200-F1207.
27. Hu, C.C., F.X. Liang, G. Zhou, L. Tu, C.H. Tang, J. Zhou, G. Kreibich, and T.T. Sun. 2005. Assembly of urothelial plaques: tetraspanin function in membrane protein trafficking. Mol. Biol. Cell. 16:3937-3950.
28. Ito, N., M. Hirose, T. Shirai, H. Tsuda, K. Nakanishi, and S. Fukushima. 1981. Lesions of the urinary bladder epithelium in 125 autopsy cases. Acta. Pathol. Jpn. 31:545-557.
29. Jost, S.P. 1986. Renewal of normal urothelium in adult mice. Virchows Arch. B. Cell Pathol. Incl. Mol. Pathol. 51:65-70.
30. Kong, X.T., F.M. Deng, P. Hu, F.X. Liang, G. Zhou, A.B. Auerbach, N. Genieser, P.K. Nelson, E.S. Robbins, E. Shapiro, et al. 2004. Roles of uroplakins in plaque formation, umbrella cell enlargement, and urinary tract diseases. J. Cell Biol. 167:1195-1204.
31. Kumagai, H., K. Mukaisho, H. Sugihara, M. Bamba, T. Miyashita, K. Miwa, and T. Hattori. 2003. Cell kinetic study on histogenesis of Barrett's esophagus using rat reflux model. Scand. J. Gastroenterol. 38:687-692.
32. Leube, R.E., and T.J. Rustad. 1991. Squamous cell metaplasia in the human lung: molecular characteristics of epithelial stratification. Virchows Arch. B. Cell Pathol. Incl. Mol. Pathol. 61:227-253.
33. Lewis, S.A. 2000. Everything you wanted to know about the bladder epithelium but were afraid to ask. Am. J. Physiol. Renal Physiol. 278:F867-F874.
34. Li, Y., W. Liu, S.W. Hayward, G.R. Cunha, and L.S. Baskin. 2000. Plasticity of the urothelial phenotype: effects of gastro-intestinal mesenchyme/stroma and implications for urinary tract reconstruction. Differentiation. 66:126-135.
35. Liang, F.X., I. Riedel, F.M. Deng, G. Zhou, C. Xu, X.R. Wu, X.P. Kong, R. Moll, and T.T. Sun. 2001. Organization of uroplakin subunits: transmembrane topology, pair formation and plaque composition. Biochem. J. 355:13-18.
36. Lin, J.H., X.R. Wu, G. Kreibich, and T.T. Sun. 1994. Precursor sequence, processing, and urothelium-specific expression of a major 15-kDa protein subunit of asymmetric unit membrane. J. Biol. Chem. 269:1775-1784.
37. Long, E.D., and R.T. Shepherd. 1983. The incidence and significance of vaginal metaplasia of the bladder trigone in adult women. Br. J. Urol. 55:189-194.
38. Mitchell, M.E. 2003. Bladder augmentation in children: where have we been and where are we going? BJU Int. 92:29-34.
39. Molloy, C.J., and J.D. Laskin. 1988. Effect of retinoid deficiency on keratin expression in mouse bladder. Exp. Mol. Pathol. 49:128-140.
40. Monis, B., and A.R. Eynard. 1980. Incidence of urothelial tumors in rats deficient in essential fatty acids. J. Natl. Cancer Inst. 64:73-79.
41. Nasiell, M. 1963. The general appearance of the bronchial epithelium in bronchial carcinoma: a histopathological study with some cytological viewpoints. Acta. Cytol. 7:97-106.
42. Nortier, J.L., M.C. Martinez, H.H. Schmeiser, V.M. Arlt, C.A. Bieler, M. Petein, M.F. Depierreux, L. De Pauw, D. Abramowicz, P. Vereerstraeten, and J.L. Vanherweghem. 2000. Urothelial carcinoma associated with the use of a Chinese herb (Aristolochia fangchi). N. Engl. J. Med. 342:1686-1692.
43. Pang, Y.Y., A. Schermer, J. Yu, and T.-T. Sun. 1993. Suprabasal change and subsequent formation of disulfide-stabilized homo- and hetero-dimers of keratins during esophageal epithelial differentiation. J. Cell Sci. 104:727-740.
44. Peters, J.H., J.A. Hagen, and S.R. DeMeester. 2004. Barrett's esophagus. J. Gastrointest. Surg. 8:1-17.
45. Ponnamperuma, R.M., S.M. Kirchhof, L. Trifiletti, and L.M. De Luca. 1999. Ovariectomy increases squamous metaplasia of the uterine horns and survival of SENCAR mice fed a vitamin A-deficient diet. Am. J. Clin. Nutr. 70:502-508.
46. Rheinwald, J.G., and H. Green. 1975. Formation of a keratinizing epithelium in culture by a cloned cell line derived from a teratoma. Cell. 6:317-330.
47. Romih, R., P. Korosec, W. de Mello Jr., and K. Jezernik. 2005. Differentiation of epithelial cells in the urinary tract. Cell Tissue Res. 320:259-268.
48. Sakata, T., T. Masui, M. St John, and S.M. Cohen. 1988. Uracil-induced calculi and proliferative lesions of the mouse urinary bladder. Carcinogenesis. 9:1271-1276.
49. Schermer, A., S. Galvin, and T.-T. Sun. 1986. Differentiation-related expression of a major 64K corneal keratin in vivo and in culture suggests limbal location of corneal epithelial stem cells. J. Cell Biol. 103:49-62.
50. Shirai, T., S. Fukushima, M. Hirose, M. Ohshima, and N. Ito. 1987. Epithelial lesions of the urinary bladder in three hundred and thirteen autopsy cases. Jpn. J. Cancer Res. 78:1073-1080.
51. Southgate, J., W. Cross, I. Eardley, D.F. Thomas, and L.K. Trejdosiewicz. 2003. Bladder reconstruction - from cells to materials. Proc. Inst. Mech. Eng. [H]. 217:311-316.
52. Staack, A., S.W. Hayward, L.S. Baskin, and G.R. Cunha. 2005. Molecular, cellular and developmental biology of urothelium as a basis of bladder regeneration. Differentiation. 73:121-133.
53. Staehelin, L.A., F.J. Chlapowski, and M.A. Bonneville. 1972. Lumenal plasma membrane of the urinary bladder. I. Three-dimensional reconstruction from freeze-etch images. J. Cell Biol. 53:73-91.
54. Stephenson, T.J., L. Henry, S.C. Harris, D.D. Giri, M. Fox, and J.C. Underwood. 1989. Pseudomembranous trigonitis of the bladder: hormonal aetiology. J. Clin. Pathol. 42:922-926.
55. Su, J.S., K. Arima, M. Hasegawa, O.E. Franco, M. Yanagawa, Y. Sugimura, and J. Kawamura. 2003. Proliferative status is a risk index for recurrence in primary superficial (pTa/T1) low-grade urothelial bladder carcinoma. Hinyokika Kiyo. 49:649-658.
56. Sun, T.-T., R. Eichner, D. Cooper, A. Schermer, W.G. Nelson, and R.A. Weiss. 1984. Classification, expression, and possible mechanisms of evolution of mammalian epithelial keratins: a unifying model. In The Cancer Cell: The Transformed Phenotype. Vol. 1. A. Levine, W. Topp, G. Vande Woude, and J.D. Watson, editors. Cold Spring Harbor Laboratory, New York. 169-176.
57. Sun, T.-T., F.X. Liang, and X.R. Wu. 1999. Uroplakins as markers of urothelial differentiation. Adv. Exp. Med. Biol. 462:7-18.
58. Surya, B., J. Yu, M. Manabe, and T.T. Sun. 1990. Assessing the differentiation state of cultured bovine urothelial cells: elevated synthesis of stratification-related K5 and K6 keratins and persistent expression of uroplakin I. J. Cell Sci. 97:419-432.
59. Thomas, J.C., R.T. DeMarco, and J.C. Pope IV. 2005. Molecular biology of ureteral bud and trigonal development. Curr. Urol. Rep. 6:146-151.
60. Tseng, S.C., D. Hatchell, N. Tierney, A.J. Huang, and T.T. Sun. 1984. Expression of specific keratin markers by rabbit corneal, conjunctival, and esophageal epithelia during vitamin A deficiency. J. Cell Biol. 99:2279-2286.
61. Tu, L., T.T. Sun, and G. Kreibich. 2002. Specific heterodimer formation is a prerequisite for uroplakins to exit from the endoplasmic reticulum. Mol. Biol. Cell. 13:4221-4230.
62. Varley, C.L., J. Stahlschmidt, B. Smith, M. Stower, and J. Southgate. 2004. Activation of peroxisome proliferator-activated receptor-gamma reverses squamous metaplasia and induces transitional differentiation in normal human urothelial cells. Am. J. Pathol. 164:1789-1798.
63. Wolbach, S.B., and P.R. Howe. 1925. Tissue changes following deprivation of fat-soluble A vitamin. J. Exp. Med. 42:753-777.
64. Woodcock-Mitchell, J., R. Eichner, W.G. Nelson, and T.-T. Sun. 1982. Immunolocalization of keratin polypeptides in human epidermis using monoclonal antibodies. J. Cell Biol. 95:580-588.
65. Wu, X.R., and T.-T. Sun. 1993. Molecular cloning of a 47 kDa tissue-specific and differentiation-dependent urothelial cell surface glycoprotein. J. Cell Sci. 106:31-43.
66. Wu, X.R., M. Manabe, J. Yu, and T.-T. Sun. 1990. Large scale purification and immunolocalization of bovine uroplakins I, II, and III. Molecular markers of urothelial differentiation. J. Biol. Chem. 265:19170-19179.
67. Wu, X.R., J.H. Lin, T. Walz, M. Haner, J. Yu, U. Aebi, and T.T. Sun. 1994. Mammalian uroplakins. A group of highly conserved urothelial differentiation-related membrane proteins. J. Biol. Chem. 269:13716-13724.
68. Yu, J., J.H. Lin, X.R. Wu, and T.T. Sun. 1994. Uroplakins Ia and Ib, two major differentiation products of bladder epithelium, belong to a family of four transmembrane domain (4TM) proteins. J. Cell Biol. 125:171-182.
69. Zhang, Z.T., J. Pak, E. Shapiro, T.-T. Sun, and X.R. Wu. 1999. Urothelium-specific expression of an oncogene in transgenic mice induced the formation of carcinoma in situ and invasive transitional cell carcinoma. Cancer Res. 59:3512-3517.