Canonical Wnt signaling regulates Nkx3.1 expression and luminal epithelial differentiation during prostate organogenesis

Developmental Dynamics

Volumn 242, Issue 10, 2013, Pages 1160-1171

  Kruithof de Julio, Marianna ^a   Shibata, Maho ^a   Desai, Nishita ^b   Reynon, Melissa ^b   Halili, M Vivienne ^b   Hu, Ya Ping ^b   Price, Sandy M ^b   Abate Shen, Cory ^a   Shen, Michael M ^a  

^a NewYork Presbyterian Hospital   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Epithelial mesenchymal interactions; Prostate development; Urogenital sinus

Indexed keywords

BETA GALACTOSIDASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX3.1; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EPITHELIUM CELL; EXPLANT; GENE EXPRESSION; GENE TARGETING; GENETIC ANALYSIS; MESENCHYME; MOUSE; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROSTATE; PROTEIN EXPRESSION; REGULATORY MECHANISM; REPORTER GENE; TRANSGENE; UROGENITAL SINUS; WNT SIGNALING PATHWAY;

MUS;

EPITHELIAL-MESENCHYMAL INTERACTIONS; PROSTATE DEVELOPMENT; UROGENITAL SINUS;

ANIMALS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MALE; MICE; MICE, TRANSGENIC; ORGANOGENESIS; PROSTATE; TRANSCRIPTION FACTORS; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84884726374     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24008     Document Type: Article

References (55)

1. Berman DM, Desai N, Wang X, Karhadkar SS, Reynon M, Abate-Shen C, Beachy PA, Shen MM. 2004. Roles for Hedgehog signaling in androgen production and prostate ductal morphogenesis. Dev Biol 267:387-398.
2. Bhatia-Gaur R, Donjacour AA, Sciavolino PJ, Kim M, Desai N, Young P, Norton CR, Gridley T, Cardiff RD, Cunha GR, Abate-Shen C, Shen MM. 1999. Roles for Nkx3.1 in prostate development and cancer. Genes Dev 13:966-977.
3. Bridgewater D, Cox B, Cain J, Lau A, Athaide V, Gill PS, Kuure S, Sainio K, Rosenblum ND. 2008. Canonical WNT/beta-catenin signaling is required for ureteric branching. Dev Biol 317:83-94.
4. Bunting M, Bernstein KE, Greer JM, Capecchi MR, Thomas KR. 1999. Targeting genes for self-excision in the germ line. Genes Dev 13:1524-1528.
5. Cardoso WV, Lu J. 2006. Regulation of early lung morphogenesis: questions, facts and controversies. Development 133:1611-1624.
6. Chen H, Mutton LN, Prins GS, Bieberich CJ. 2005. Distinct regulatory elements mediate the dynamic expression pattern of Nkx3.1. Dev Dyn 234:961-973.
7. Cunha GR. 2008. Mesenchymal-epithelial interactions: past, present, and future. Differentiation 76:578-586.
8. Cunha GR, Donjacour AA, Cooke PS, Mee S, Bigsby RM, Higgins SJ, Sugimura Y. 1987. The endocrinology and developmental biology of the prostate. Endocrine Rev 8:338-362.
9. Deng C, Wynshaw-Boris A, Zhou F, Kuo A, Leder P. 1996. Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell 84:911-921.
10. Doles JD, Vezina CM, Lipinski RJ, Peterson RE, Bushman W. 2005. Growth, morphogenesis, and differentiation during mouse prostate development in situ, in renal grafts, and in vitro. Prostate 65:390-399.
11. Donjacour AA, Thomson AA, Cunha GR. 2003. FGF-10 plays an essential role in the growth of the fetal prostate. Dev Biol 261:39-54.
12. Ferrer-Vaquer A, Piliszek A, Tian G, Aho RJ, Dufort D, Hadjantonakis AK. 2010. A sensitive and bright single-cell resolution live imaging reporter of Wnt/beta-catenin signaling in the mouse. BMC Dev Biol 10:121.
13. Francis JC, Thomsen MK, Taketo MM, Swain A. 2013. beta-catenin is required for prostate development and cooperates with Pten loss to drive invasive carcinoma. PLoS Genet 9:e1003180.
14. Gao N, Ishii K, Mirosevich J, Kuwajima S, Oppenheimer SR, Roberts RL, Jiang M, Yu X, Shappell SB, Caprioli RM, Stoffel M, Hayward SW, Matusik RJ. 2005. Forkhead box A1 regulates prostate ductal morphogenesis and promotes epithelial cell maturation. Development 132:3431-3443.
15. Haara O, Fujimori S, Schmidt-Ullrich R, Hartmann C, Thesleff I, Mikkola ML. 2011. Ectodysplasin and Wnt pathways are required for salivary gland branching morphogenesis. Development 138:2681-2691.
16. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. 2002. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22:1172-1183.
17. Karner CM, Merkel CE, Dodge M, Ma Z, Lu J, Chen C, Lum L, Carroll TJ. 2010. Tankyrase is necessary for canonical Wnt signaling during kidney development. Dev Dyn 239:2014-2023.
18. Keil KP, Mehta V, Abler LL, Joshi PS, Schmitz CT, Vezina CM. 2012. Visualization and quantification of mouse prostate development by in situ hybridization. Differentiation 84:232-239.
19. Kim MJ, Bhatia-Gaur R, Banach-Petrosky WA, Desai N, Wang Y, Hayward SW, Cunha GR, Cardiff RD, Shen MM, Abate-Shen C. 2002a. Nkx3.1 mutant mice recapitulate early stages of prostate carcinogenesis. Cancer Res 62:2999-3004.
20. Kim MJ, Cardiff RD, Desai N, Banach-Petrosky WA, Parsons R, Shen MM, Abate-Shen C. 2002b. Cooperativity of Nkx3.1 and Pten loss of function in a mouse model of prostate carcinogenesis. Proc Natl Acad Sci U S A 99:2884-2889.
21. Kypta RM, Waxman J. 2012. Wnt/beta-catenin signalling in prostate cancer. Nat Rev Urol:dx/ 10.1038/nrurol.2012.1116 [Epub ahead of print].
22. Logan CY, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781-810.
23. Lopes ES, Foster BA, Donjacour AA, Cunha GR. 1996. Initiation of secretory activity of rat prostatic epithelium in organ culture. Endocrinology 137:4225-4234.
24. Lu W, Luo Y, Kan M, McKeehan WL. 1999. Fibroblast growth factor-10. A second candidate stromal to epithelial cell andromedin in prostate. J Biol Chem 274:12827-12834.
25. Lung B, Cunha GR. 1981. Development of seminal vesicles and coagulating glands in neonatal mice. I. The morphogenetic effects of various hormonal conditions. Anat Rec 199:73-88.
26. Mao B, Wu W, Li Y, Hoppe D, Stannek P, Glinka A, Niehrs C. 2001. LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature 411:321-325.
27. Mehta V, Abler LL, Keil KP, Schmitz CT, Joshi PS, Vezina CM. 2011. Atlas of Wnt and R-spondin gene expression in the developing male mouse lower urogenital tract. Dev Dyn 240:2548-2560.
28. Mehta V, Schmitz CT, Keil KP, Joshi PS, Abler LL, Lin TM, Taketo MM, Sun X, Vezina CM. 2013. Beta-catenin (CTNNB1) induces Bmp expression in urogenital sinus epithelium and participates in prostatic bud initiation and patterning. Dev Biol 376:125-135.
29. Moran JL, Levorse JM, Vogt TF. 1999. Limbs move beyond the radical fringe. Nature 399:742-743.
30. Nagy A, Gertsenstein M, Vintersten K, Behringer R. 2003. Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
31. Olson EN, Arnold HH, Rigby PW, Wold BJ. 1996. Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell 85:1-4.
32. Patel N, Sharpe PT, Miletich I. 2011. Coordination of epithelial branching and salivary gland lumen formation by Wnt and FGF signals. Dev Biol 358:156-167.
33. Pham CT, MacIvor DM, Hug BA, Heusel JW, Ley TJ. 1996. Long-range disruption of gene expression by a selectable marker cassette. Proc Natl Acad Sci U S A 93:13090-13095.
34. Prins GS, Putz O. 2008. Molecular signaling pathways that regulate prostate gland development. Differentiation 76:641-659.
35. Pritchard C, Mecham B, Dumpit R, Coleman I, Bhattacharjee M, Chen Q, Sikes RA, Nelson PS. 2009. Conserved gene expression programs integrate mammalian prostate development and tumorigenesis. Cancer Res 69:1739-1747.
36. Pu Y, Huang L, Birch L, Prins GS. 2007. Androgen regulation of prostate morphoregulatory gene expression: Fgf10-dependent and -independent pathways. Endocrinology 148:1697-1706.
37. Schaeffer EM, Marchionni L, Huang Z, Simons B, Blackman A, Yu W, Parmigiani G, Berman DM. 2008. Androgen-induced programs for prostate epithelial growth and invasion arise in embryogenesis and are reactivated in cancer. Oncogene 27:7180-7191.
38. Schneider A, Brand T, Zweigerdt R, Arnold H. 2000. Targeted disruption of the Nkx3.1 gene in mice results in morphogenetic defects of minor salivary glands: parallels to glandular duct morphogenesis in prostate. Mech Dev 95:163-174.
39. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376:62-66.
40. Shen MM, Abate-Shen C. 2010. Molecular genetics of prostate cancer: new prospects for old challenges. Genes Dev 24:1967-2000.
41. Simons BW, Hurley PJ, Huang Z, Ross AE, Miller R, Marchionni L, Berman DM, Schaeffer EM. 2012. Wnt signaling though beta-catenin is required for prostate lineage specification. Dev Biol 371:246-255.
42. Sternlicht MD, Kouros-Mehr H, Lu P, Werb Z. 2006. Hormonal and local control of mammary branching morphogenesis. Differentiation 74:365-381.
43. Sugimura Y, Cunha GR, Donjacour AA. 1986. Morphogenesis of ductal networks in the mouse prostate. Biol Reprod 34:961-971.
44. Sun Y, Campisi J, Higano C, Beer TM, Porter P, Coleman I, True L, Nelson PS. 2012. Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat Med 18:1359-1368.
45. Tanaka M, Komuro I, Inagaki H, Jenkins NA, Copeland NG, Izumo S. 2000. Nkx3.1, a murine homolog of Drosophila bagpipe, regulates epithelial ductal branching and proliferation of the prostate and palatine glands. Dev Dyn 219:248-260.
46. Taylor RA, Wang H, Wilkinson SE, Richards MG, Britt KL, Vaillant F, Lindeman GJ, Visvader JE, Cunha GR, St John J, Risbridger GP. 2009. Lineage enforcement by inductive mesenchyme on adult epithelial stem cells across developmental germ layers. Stem Cells 27:3032-3042.
47. Tenniswood M. 1986. Role of epithelial-stromal interactions in the control of gene expression in the prostate: an hypothesis. Prostate 9:375-385.
48. Thomson AA. 2008. Mesenchymal mechanisms in prostate organogenesis. Differentiation 76:587-598.
49. Thomson AA, Cunha GR. 1999. Prostatic growth and development are regulated by FGF10. Development 126:3693-3701.
50. Tybulewicz VL, Crawford CE, Jackson PK, Bronson RT, Mulligan RC. 1991. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell 65:1153-1163.
51. Wang BE, Wang XD, Ernst JA, Polakis P, Gao WQ. 2008. Regulation of epithelial branching morphogenesis and cancer cell growth of the prostate by Wnt signaling. PLoS ONE 3:e2186.
52. Wang X, Kruithof-de Julio M, Economides KD, Walker D, Yu H, Halili MV, Hu Y-P, Price SM, Abate-Shen C, Shen MM. 2009. A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature 461:495-500.
53. Wu X, Daniels G, Shapiro E, Xu K, Huang H, Li Y, Logan S, Greco MA, Peng Y, Monaco ME, Melamed J, Lepor H, Grishina I, Lee P. 2011. LEF1 identifies androgen-independent epithelium in the developing prostate. Mol Endocrinol 25:1018-1026.
54. Yu X, Wang Y, Jiang M, Bierie B, Roy-Burman P, Shen MM, Taketo MM, Wills M, Matusik RJ. 2009. Activation of beta-Catenin in mouse prostate causes HGPIN and continuous prostate growth after castration. Prostate 69:249-262.
55. Zhang TJ, Hoffman BG, Ruiz de Algara T, Helgason CD. 2006. SAGE reveals expression of Wnt signalling pathway members during mouse prostate development. Gene Expr Patterns 6:310-324.