Hedgehog signaling restrains bladder cancer progression by eliciting stromal production of urothelial differentiation factors

Cancer Cell

Volumn 26, Issue 4, 2014, Pages 521-533

  Shin, Kunyoo ^a,c   Lim, Agnes ^a   Zhao, Chen ^a   Sahoo, Debashis ^a   Pan, Ying ^a,b   Spiekerkoetter, Edda ^a   Liao, Joseph C ^a,b   Beachy, Philip A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 5; SONIC HEDGEHOG PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BLADDER CANCER; BLADDER CARCINOGENESIS; CANCER INHIBITION; GENE EXPRESSION REGULATION; HUMAN; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; STROMA CELL; TRANSITIONAL CELL CARCINOMA; ANIMAL; BLADDER; BLADDER TUMOR; CELL DIFFERENTIATION; DISEASE COURSE; GENETICS; METABOLISM; PATHOLOGY;

ERINACEIDAE;

ANIMALS; CELL DIFFERENTIATION; DISEASE PROGRESSION; HEDGEHOG PROTEINS; HUMANS; MICE; SIGNAL TRANSDUCTION; STROMAL CELLS; URINARY BLADDER; URINARY BLADDER NEOPLASMS;

EID: 84907996793     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2014.09.001     Document Type: Article

References (51)

1. Ahn S., Joyner A.L. Invivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 2005, 437:894-897.
2. Bragdon B., Moseychuk O., Saldanha S., King D., Julian J., Nohe A. Bone morphogenetic proteins: a critical review. Cell. Signal. 2011, 23:609-620.
3. Bryan G.T. The pathogenesis of experimental bladder cancer. Cancer Res. 1977, 37:2813-2816.
4. Bryan G.T. Pathogenesis of human urinary bladder cancer. Environ. Health Perspect. 1983, 49:201-207.
5. Comprehensive molecular characterization of urothelial bladder carcinoma. Nature 2014, 507:315-322. Cancer Genome Atlas Research Network.
6. Chen J.K., Taipale J., Cooper M.K., Beachy P.A. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 2002, 16:2743-2748.
7. Chen J.K., Taipale J., Young K.E., Maiti T., Beachy P.A. Small molecule modulation of Smoothened activity. Proc. Natl. Acad. Sci. USA 2002, 99:14071-14076.
8. Choi W., Porten S., Kim S., Willis D., Plimack E.R., Hoffman-Censits J., Roth B., Cheng T., Tran M., Lee I.-L., et al. Identification of distinct basal and luminal subtypes of muscle-invasive bladder cancer with different sensitivities to frontline chemotherapy. Cancer Cell 2014, 25:152-165.
9. Cooper M.K., Porter J.A., Young K.E., Beachy P.A. Teratogen-mediated inhibition of target tissue response to Shh signaling. Science 1998, 280:1603-1607.
10. Crabtree G.R., Schreiber S.L. SnapShot: Ca2+-calcineurin-NFAT signaling. Cell 2009, 138:210-210.e211.
11. Cuny G.D., Yu P.B., Laha J.K., Xing X., Liu J.-F., Lai C.S., Deng D.Y., Sachidanandan C., Bloch K.D., Peterson R.T. Structure-activity relationship study of bone morphogenetic protein (BMP) signaling inhibitors. Bioorg. Med. Chem. Lett. 2008, 18:4388-4392.
12. Hahn H., Wicking C., Zaphiropoulous P.G., Gailani M.R., Shanley S., Chidambaram A., Vorechovsky I., Holmberg E., Unden A.B., Gillies S., et al. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 1996, 85:841-851.
13. Herter-Sprie G.S., Kung A.L., Wong K.-K. New cast for a new era: preclinical cancer drug development revisited. J.Clin. Invest. 2013, 123:3639-3645.
14. Huang W., Sherman B.T., Tan Q., Kir J., Liu D., Bryant D., Guo Y., Stephens R., Baseler M.W., Lane H.C., Lempicki R.A. DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res. 2007, 35:W169-W175.
15. Incardona J.P., Gaffield W., Kapur R.P., Roelink H. The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development 1998, 125:3553-3562.
16. Johnson R.L., Rothman A.L., Xie J., Goodrich L.V., Bare J.W., Bonifas J.M., Quinn A.G., Myers R.M., Cox D.R., Epstein E.H., Scott M.P. Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 1996, 272:1668-1671.
17. Kawai S., Sugiura T. Characterization of human bone morphogenetic protein (BMP)-4 and -7 gene promoters: activation of BMP promoters by Gli, a sonic hedgehog mediator. Bone 2001, 29:54-61.
18. Kaye S.B., Fehrenbacher L., Holloway R., Amit A., Karlan B., Slomovitz B., Sabbatini P., Fu L., Yauch R.L., Chang I., Reddy J.C. A phase II, randomized, placebo-controlled study of vismodegib as maintenance therapy in patients with ovarian cancer in second or third complete remission. Clin. Cancer Res. 2012, 18:6509-6518.
19. Kimura H., Stephen D., Joyner A., Curran T. Gli1 is important for medulloblastoma formation in Ptc1+/- mice. Oncogene 2005, 24:4026-4036.
20. Lai K., Kaspar B.K., Gage F.H., Schaffer D.V. Sonic hedgehog regulates adult neural progenitor proliferation invitro and invivo. Nat. Neurosci. 2003, 6:21-27.
21. Lee J.J., Perera R.M., Wang H., Wu D.-C., Liu X.S., Han S., Fitamant J., Jones P.D., Ghanta K.S., Kawano S., et al. Stromal response to Hedgehog signaling restrains pancreatic cancer progression. Proceedings of the National Academy of Sciences 2014, 111:E3091-E3100.
22. Li B., Dewey C.N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 2011, 12:323-338.
23. Liu J., Farmer J.D., Lane W.S., Friedman J., Weissman I., Schreiber S.L. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 1991, 66:807-815.
24. Long F., Zhang X.M., Karp S., Yang Y., McMahon A.P. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 2001, 128:5099-5108.
25. Miyazono K., Miyazawa K. Id: a target of BMP signaling. Sci. STKE 2002, 2002:pe40.
26. Miyazono K., Maeda S., Imamura T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 2005, 16:251-263.
27. Mysorekar I.U., Isaacson-Schmid M., Walker J.N., Mills J.C., Hultgren S.J. Bone morphogenetic protein 4 signaling regulates epithelial renewal in the urinary tract in response to uropathogenic infection. Cell Host Microbe 2009, 5:463-475.
28. Nagao M., Suzuki E., Yasuo K., Yahagi T., Seino Y. Mutagenicity of N-butyl-N-(4-hydroxybutyl)nitrosamine, a bladder carcinogen, and related compounds. Cancer Res. 1977, 37:399-407.
29. O'Toole C., Price Z.H., Ohnuki Y., Unsgaard B. Ultrastructure, karyology and immunology of a cell line originated from a human transitional-cell carcinoma. Br. J. Cancer 1978, 38:64-76.
30. Olive K.P., Jacobetz M.A., Davidson C.J., Gopinathan A., McIntyre D., Honess D., Madhu B., Goldgraben M.A., Caldwell M.E., Allard D., et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009, 324:1457-1461.
31. Özdemir B.C., Pentcheva-Hoang T., Carstens J.L., Zheng X., Wu C.-C., Simpson T.R., Laklai H., Sugimoto H., Kahlert C., Novitskiy S.V., et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 2014, 25:719-734.
32. Palma V., Lim D.A., Dahmane N., Sánchez P., Brionne T.C., Herzberg C.D., Gitton Y., Carleton A., Alvarez-Buylla A., Ruiz i Altaba A. Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 2005, 132:335-344.
33. Rhim A.D., Oberstein P.E., Thomas D.H., Mirek E.T., Palermo C.F., Sastra S.A., Dekleva E.N., Saunders T., Becerra C.P., Tattersall I.W., et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell 2014, 25:735-747.
34. Roberts D.J., Johnson R.L., Burke A.C., Nelson C.E., Morgan B.A., Tabin C. Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 1995, 121:3163-3174.
35. Roelink H., Porter J.A., Chiang C., Tanabe Y., Chang D.T., Beachy P.A., Jessell T.M. Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 1995, 81:445-455.
36. Ruch J.M., Kim E.J. Hedgehog signaling pathway and cancer therapeutics: progress to date. Drugs 2013, 73:613-623.
37. Rudin C.M., Hann C.L., Laterra J., Yauch R.L., Callahan C.A., Fu L., Holcomb T., Stinson J., Gould S.E., Coleman B., et al. Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449. N.Engl. J. Med. 2009, 361:1173-1178.
38. Samanta J., Kessler J.A. Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 2004, 131:4131-4142.
39. Schultheiss T.M., Burch J.B., Lassar A.B. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 1997, 11:451-462.
40. Sekulic A., Migden M.R., Oro A.E., Dirix L., Lewis K.D., Hainsworth J.D., Solomon J.A., Yoo S., Arron S.T., Friedlander P.A., et al. Efficacy and safety of vismodegib in advanced basal-cell carcinoma. N.Engl. J. Med. 2012, 366:2171-2179.
41. Shin K., Lee J., Guo N., Kim J., Lim A., Qu L., Mysorekar I.U., Beachy P.A. Hedgehog/Wnt feedback supports regenerative proliferation of epithelial stem cells in bladder. Nature 2011, 472:110-114.
42. Shin K., Lim A., Odegaard J.I., Honeycutt J.D., Kawano S., Hsieh M.H., Beachy P.A. Cellular origin of bladder neoplasia and tissue dynamics of its progression to invasive carcinoma. Nat. Cell Biol. 2014, 16:469-478.
43. Sievert K.D., Amend B., Nagele U., Schilling D., Bedke J., Horstmann M., Hennenlotter J., Kruck S., Stenzl A. Economic aspects of bladder cancer: what are the benefits and costs?. World J. Urol. 2009, 27:295-300.
44. Spiekerkoetter E., Tian X., Cai J., Hopper R.K., Sudheendra D., Li C.G., El-Bizri N., Sawada H., Haghighat R., Chan R., et al. FK506 activates BMPR2, rescues endothelial dysfunction, and reverses pulmonary hypertension. J.Clin. Invest. 2013, 123:3600-3613.
45. Taipale J., Beachy P.A. The Hedgehog and Wnt signalling pathways in cancer. Nature 2001, 411:349-354.
46. Tang J.Y., Mackay-Wiggan J.M., Aszterbaum M., Yauch R.L., Lindgren J., Chang K., Coppola C., Chanana A.M., Marji J., Bickers D.R., Epstein E.H. Inhibiting the hedgehog pathway in patients with the basal-cell nevus syndrome. N.Engl. J. Med. 2012, 366:2180-2188.
47. Teglund S., Toftgård R. Hedgehog beyond medulloblastoma and basal cell carcinoma. Biochim. Biophys. Acta 2010, 1805:181-208.
48. Thievessen I., Wolter M., Prior A., Seifert H.H., Schulz W.A. Hedgehog signaling in normal urothelial cells and in urothelial carcinoma cell lines. J.Cell. Physiol. 2005, 203:372-377.
49. Weaver M., Yingling J.M., Dunn N.R., Bellusci S., Hogan B.L. Bmp signaling regulates proximal-distal differentiation of endoderm in mouse lung development. Development 1999, 126:4005-4015.
50. Yauch R.L., Gould S.E., Scales S.J., Tang T., Tian H., Ahn C.P., Marshall D., Fu L., Januario T., Kallop D., et al. A paracrine requirement for hedgehog signalling in cancer. Nature 2008, 455:406-410.
51. Yu P.B., Deng D.Y., Lai C.S., Hong C.C., Cuny G.D., Bouxsein M.L., Hong D.W., McManus P.M., Katagiri T., Sachidanandan C., et al. BMP type I receptor inhibition reduces heterotopic [corrected] ossification. Nat. Med. 2008, 14:1363-1369.