An EGFR-ERK-SOX9 signaling cascade links urothelial development and regeneration to cancer

Cancer Research

Volumn 71, Issue 11, 2011, Pages 3812-3821

  Ling, Shizhang ^a   Chang, Xiaofei ^a   Schultz, Luciana ^b   Lee, Thomas K ^a   Chaux, Alcides ^a   Marchionni, Luigi ^a   Netto, George J ^a   Sidransky, David ^a   Berman, David M ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Pathology   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGEN; CYCLOPHOSPHAMIDE; EPIDERMAL GROWTH FACTOR RECEPTOR; HYDROGEN PEROXIDE; LIGAND; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; TESTIS DETERMINING FACTOR; TRANSCRIPTION FACTOR SOX9;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CARCINOGENICITY; CELL INVASION; CELL MIGRATION; DRUG EXPOSURE; ENZYME ACTIVATION; ENZYME INHIBITION; GENE CONTROL; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE SILENCING; HISTOGENESIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MATURATION; MOUSE; NONHUMAN; OSMOTIC STRESS; PERINATAL PERIOD; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TISSUE INJURY; TISSUE REGENERATION; TISSUE REPAIR; TRANSITIONAL CELL CARCINOMA; UPREGULATION; UROTHELIUM;

ANIMALS; CELL LINE, TUMOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; IMMUNOHISTOCHEMISTRY; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; RECEPTOR, EPIDERMAL GROWTH FACTOR; REGENERATION; SOX9 TRANSCRIPTION FACTOR; UROLOGIC NEOPLASMS; UROTHELIUM;

EID: 79957883840     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3072     Document Type: Article

References (50)

1. Beachy PA, Karhadkar SS, Berman DM. Mending and malignancy. Nature 2004;431:402. (Pubitemid 39329562)
2. Kundu JK, Surh YJ. Inflammation: gearing the journey to cancer. Mutat Res 2008;659:15-30.
3. Michaud DS. Chronic inflammation and bladder cancer. Urol Oncol 2007;25:260-8. (Pubitemid 46670749)
4. Martin P, Parkhurst SM. Parallels between tissue repair and embryo morphogenesis. J Embryol Exp Morphol 2004;131:3021-34. (Pubitemid 39077428)
5. Ingber DE, Levin M. What lies at the interface of regenerative medicine and developmental biology?J Embryol Exp Morphol 2007;134:2541-7.
6. Lefebvre V, Dumitriu B, Penzo-Mendez A, Han Y, Pallavi B. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol 2007;39: 2195-214. (Pubitemid 47484275)
7. Thomsen MK, Francis JC, Swain A. The role of Sox9 in prostate development. Differentiation 2008;76:728-35. (Pubitemid 352032748)
8. Wang H, Leav I, Ibaragi S, Wegner M, Hu GF, Lu ML, et al. SOX9 is expressed in human fetal prostate epithelium and enhances prostate cancer invasion. Cancer Res 2008;68:1625-30. (Pubitemid 351416545)
9. Schaeffer EM, Marchionni L, Huang Z, Simons B, Blackman A, Yu W, Parmigiani G, Berman DM. Androgen-induced programs for prostate epithelial growth and invasion arise in embryogenesis and are reactivated in cancer. Oncogene 2008;27:7180-91.
10. Murakami S, Kan M, McKeehan WL, de Crombrugghe B. Up-regulation of the chondrogenic Sox9 gene by fibroblast growth factors is mediated by the mitogen-activated protein kinase pathway. Proc Natl Acad Sci U S A 2000;97:1113-8. (Pubitemid 30080821)
11. Rossi MR, Masters JRW, Park S, Todd JH, Garrett SH, Sens MA, et al. The immortalized UROtsa cell line as a potential cell culture model of human urothelium. Environ Health Perspect 2001;109:801-8. (Pubitemid 32910302)
12. Summerhayes IC, Franks LM. Effects of donor age on neoplastic transformation of adult mouse bladder epithelium in vitro. J Natl Cancer Inst 1979;62:1017-23. (Pubitemid 9174372)
13. Kleeberger W, Bova GS, Nielsen ME, Herawi M, Chuang AY, Epstein JI, et al. Roles for the stem cell associated intermediate filament nestin in prostate cancer migration and metastasis. Cancer Res 2007;67: 9199-206. (Pubitemid 47535906)
14. Klein J, Rey P, Dansey R, Karanes C, Abella E, Cassells L, Hamm C, et al. Cyclophosphamide and paclitaxel as initial or salvage regimen for the mobilization of peripheral blood progenitor cells. Bone Marrow Transplant 1999;24:959-63. (Pubitemid 29532867)
15. Berman DM, Desai N, Wang X, Karhadkar SS, Reynon M, Abate-Shen C, et al. Roles for Hedgehog signaling in androgen production and prostate ductal morphogenesis. Dev Biol 2004;267:387-98. (Pubitemid 38328580)
16. Grishina IB, Kim SY, Ferrara C, Makarenkova HP, Walden PD. BMP7 inhibits branching morphogenesis in the prostate gland and interferes with Notch signaling. Dev Biol 2005;288:334-47. (Pubitemid 41790747)
17. Albini A, Iwamoto Y, Kleinman HK, Martin GR, Aaronson SA, Kozlowski JM, et al. A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 1987;47:3239-45. (Pubitemid 17082655)
18. Cheung WL, Albadine R, Chan T, Sharma R, Netto GJ. Phosphorylated H2AX in noninvasive low grade urothelial carcinoma of the bladder: correlation with tumor recurrence. J Urol 2009;181:1387-92.
19. Schultz L, Albadine R, Hicks J, Jadallah S, DeMarzo AM, Chen YB, et al. Expression status and prognostic significance of mammalian target of rapamycin pathway members in urothelial carcinoma of urinary bladder after cystectomy. Cancer 2010;116:5517-26.
20. Jezernik K, Pipan N. Blood-urine barrier formation in mouse urinary bladder development. Anat Rec 1993;235:533-8. (Pubitemid 23096917)
21. Lewis SA. Everything you wanted to know about the bladder epithelium but were afraid to ask. Am J Physiol Renal Physiol 2000;278: F867-74.
22. Brandt W, Matsui W, Rosenberg J, He X, Ling S, Schaeffer E, et al. Urothelial carcinoma: stem cells on the edge. Cancer Metastasis Rev 2009;28:291-304.
23. Farsund T. Cell kinetics of mouse urinary bladder epithelium. II. Changes in proliferation and nuclear DNA content during necrosis regeneration, and hyperplasia caused by a single dose of cyclophosphamide. Virchows Arch B Cell Pathol 1976;21:279-98.
24. Anton E. Delayed toxicity of cyclophosphamide on the bladder of DBA/2 and C57BL/6 female mouse. Int J Exp Pathol 2002;83:47-53. (Pubitemid 34638946)
25. Wang Z, Chen JK, Wang SW, Moeckel G, Harris RC. Importance of functional EGF receptors in recovery from acute nephrotoxic injury. J Am Soc Nephrol 2003;14:3147-54. (Pubitemid 37509292)
26. Eblin KE, Bredfeldt TG, Buffington S, Gandolfi AJ. Mitogenic signal transduction caused by monomethylarsonous acid in human bladder cells: role in arsenic-induced carcinogenesis. Toxicol Sci 2007;95: 321-30. (Pubitemid 46152604)
27. Messing EM, Hanson P, Ulrich P, Erturk E. Epidermal growth factor- interactions with normal and malignant urothelium: in vivo and in situ studies. J Urol 1987;138:1329-35. (Pubitemid 17157580)
28. Chow NH, Liu HS, Yang HB, Chan SH, Su IJ. Expression patterns of erbB receptor family in normal urothelium and transitional cell carcinoma. An immunohistochemical study. Virchows Arch 1997;430: 461-6.
29. Sun TT. Altered phenotype of cultured urothelial and other stratified epithelial cells: implications for wound healing. Am J Physiol Renal Physiol 2006;291:F9-21.
30. Eblin KE, Bredfeldt TG, Gandolfi AJ. Immortalized human urothelial cells as a model of arsenic-induced bladder cancer. Toxicology 2008;248:67-76.
31. Freeman MR, Yoo JJ, Raab G, Soker S, Adam RM, Schneck FX, et al. Heparin-binding EGF-like growth factor is an autocrine growth factor for human urothelial cells and is synthesized by epithelial and smooth muscle cells in the human bladder. J Clin Invest 1997;99:1028-36. (Pubitemid 27123640)
32. Lezama R, Diaz-Tellez A, Ramos-Mandujano G, Oropeza L, Pasantes- Morales H. Epidermal growth factor receptor is a common element in the signaling pathways activated by cell volume changes in isosmotic, hyposmotic or hyperosmotic conditions. Neurochem Res 2005;30: 1589-97. (Pubitemid 41813723)
33. Goldkorn T, Balaban N, Matsukuma K, Chea V, Gould R, Last J, et al. EGF-receptor phosphorylation and signaling are targeted by H2O2 redox stress. Am J Respir Cell Mol Biol 1998;19:786-98. (Pubitemid 128353678)
34. Yin J, Xu K, Zhang J, Kumar A, Yu FS. Wound-induced ATP release and EGF receptor activation in epithelial cells. J Cell Sci 2007;120: 815-25. (Pubitemid 46523483)
35. Wu XR. Urothelial tumorigenesis: a tale of divergent pathways. Nat Rev Cancer 2005;5:713-25.
36. Wang Y, Sul HS. Pref-1 regulates mesenchymal cell commitment and differentiation through Sox9. Cell Metab 2009;9:287-302.
37. de Crombrugghe B, Lefebvre V, Behringer RR, Bi W, Murakami S, Huang W. Transcriptional mechanisms of chondrocyte differentiation. Matrix Biol 2000;9:389-94.
38. Moniot B, Biau S, Faure S, Nielsen CM, Berta P, Roberts DJ, et al. SOX9 specifies the pyloric sphincter epithelium through mesenchymal- epithelial signals. J Embryol Exp Morphol 2004;131:3795-804. (Pubitemid 39199386)
39. Okubo T, Knoepfler PS, Eisenman RN, Hogan BLM. Nmyc plays an essential role during lung development as a dosage-sensitive regulator of progenitor cell proliferation and differentiation. J Embryol Exp Morphol 2005;132:1363-74. (Pubitemid 40528795)
40. Lavelle J, Meyers S, Ramage R, Bastacky S, Doty D, Apodaca G, et al. Bladder permeability barrier: recovery from selective injury of surface epithelial cells. Am J Physiol Renal Physiol 2002;283:F242-53.
41. Messing EM. Clinical implications of the expression of epidermal growth factor receptors in human transitional cell carcinoma. Cancer Res 1990;50:2530-7. (Pubitemid 20134522)
42. Baskin LS, Sutherland RS, Thomson AA, Nguyen HT, Morgan DM, Hayward SW, et al. Growth factors in bladder wound healing. J Urol 1997;157:2388-95. (Pubitemid 27208727)
43. Mysorekar IU, Mulvey MA, Hultgren SJ, Gordon JI. Molecular regulation of urothelial renewal and host defenses during infection with uropathogenic Escherichia coli. J Biol Chem 2002;277:7412-9. (Pubitemid 34953138)
44. He X, Marchionni L, Hansel DE, Yu W, Sood A, Yang J, et al. Differentiation of a highly tumorigenic basal cell compartment in urothelial carcinoma. Stem Cells 2009;27:1487-95.
45. Dvorak HF. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986;315:1650-9 (Pubitemid 17052899)
46. Beachy PA, Karhadkar SS, Berman DM. Tissue repair and stem cell renewal in carcinogenesis. Nature 2004;432:324-31. (Pubitemid 39551660)
47. Burin GJ, Gibb HJ, Hill RN. Human bladder cancer: evidence for a potential irritation-induced mechanism. Food Chem Toxicol 1995;33:785-95.
48. Gelfand M, Weinberg RW, Castle WM. Relation between carcinoma of the bladder and infestation with Schistosoma haematobium. Lancet 1967;1:1249-51.
49. Smith AH, Goycolea M, Haque R, Biggs ML. Marked increase in bladder and lung cancer mortality in a region of northern chile due to arsenic in drinking water. Am J Epidemiol 1998; 147:660-9. (Pubitemid 28180309)
50. Sens DA, Park S, Gurel V, Sens MA, Garrett SH, Somji S. Inorganic cadmium- and arsenite-induced malignant transformation of human bladder urothelial cells. Toxicol Sci 2004;79:56-63. (Pubitemid 38660248)