Smoothened as a new therapeutic target for human osteosarcoma

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Hirotsu, Masataka ^a   Setoguchi, Takao ^a   Sasaki, Hiromi ^a   Matsunoshita, Yukihiro ^a   Gao, Hui ^a   Nagao, Hiroko ^a   Kunigou, Osamu ^a   Komiya, Setsuro ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN E; CYCLIN E1; CYCLOPAMINE; PLACEBO; PROTEIN PATCHED 1; RETINOBLASTOMA PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN 2; SHORT HAIRPIN RNA; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI2; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; GLI1 PROTEIN, HUMAN; SMALL INTERFERING RNA; SMO PROTEIN, HUMAN; TRANSCRIPTION FACTOR; VERATRUM ALKALOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL VIABILITY; COLONY FORMATION; CONTROLLED STUDY; DRUG TARGETING; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OSTEOSARCOMA; OSTEOSARCOMA CELL; REAL TIME POLYMERASE CHAIN REACTION; TUMOR BIOPSY; XENOGRAFT; ANIMAL; BIOPSY; CELL PROLIFERATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG SCREENING; GENE SILENCING; METABOLISM; NUDE MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION; SURVIVAL; TUMOR CELL LINE;

ERINACEIDAE;

ANIMALS; BIOPSY; CELL LINE, TUMOR; CELL PROLIFERATION; G1 PHASE; GENE KNOCKDOWN TECHNIQUES; HEDGEHOG PROTEINS; HUMANS; MICE; MICE, NUDE; OSTEOSARCOMA; RECEPTORS, G-PROTEIN-COUPLED; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TRANSCRIPTION FACTORS; VERATRUM ALKALOIDS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 76849102604     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-5     Document Type: Article

References (68)

1. Gibbs CP, Weber K, Scarborough MT. Malignant bone tumors. Instr Course Lect 2002, 51:413-428.
2. Igney FH, Krammer PH. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer 2002, 2:277-288. 10.1038/nrc776, 12001989.
3. Lafleur EA, Koshkina NV, Stewart J, Jia SF, Worth LL, Duan X, Kleinerman ES. Increased Fas expression reduces the metastatic potential of human osteosarcoma cells. Clin Cancer Res 2004, 10:8114-8119. 10.1158/1078-0432.CCR-04-0353, 15585647.
4. Horowitz JM, Park SH, Bogenmann E, Cheng JC, Yandell DW, Kaye FJ, Minna JD, Dryja TP, Weinberg RA. Frequent inactivation of the retinoblastoma anti-oncogene is restricted to a subset of human tumor cells. Proc Natl Acad Sci USA 1990, 87:2775-2779. 10.1073/pnas.87.7.2775, 53773, 2181449.
5. Ingham PW, McMahon AP. Hedgehog signaling in animal development: paradigms and principles. Genes Dev 2001, 15:3059-3087. 10.1101/gad.938601, 11731473.
6. Ruiz i Altaba A, Sanchez P, Dahmane N. Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat Rev Cancer 2002, 2:361-372. 10.1038/nrc796, 12044012.
7. McMahon AP, Ingham PW, Tabin CJ. Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol 2003, 53:1-114. full_text, 12509125.
8. Fogarty MP, Kessler JD, Wechsler-Reya RJ. Morphing into cancer: the role of developmental signaling pathways in brain tumor formation. J Neurobiol 2005, 64:458-475. 10.1002/neu.20166, 16041741.
9. Gorlin RJ. Nevoid basal cell carcinoma syndrome. Dermatol Clin 1995, 13:113-125.
10. Ruiz i Altaba A, Mas C, Stecca B. The Gli code: an information nexus regulating cell fate, stemness and cancer. Trends Cell Biol 2007, 17:438-447. 10.1016/j.tcb.2007.06.007, 2601665, 17845852.
11. Chen JK, Taipale J, Cooper MK, Beachy PA. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev 2002, 16:2743-2748. 10.1101/gad.1025302, 187469, 12414725.
12. Goodrich LV, Johnson RL, Milenkovic L, McMahon JA, Scott MP. Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev 1996, 10:301-312. 10.1101/gad.10.3.301, 8595881.
13. Hynes M, Stone DM, Dowd M, Pitts-Meek S, Goddard A, Gurney A, Rosenthal A. Control of cell pattern in the neural tube by the zinc finger transcription factor and oncogene Gli-1. Neuron 1997, 19:15-26. 10.1016/S0896-6273(00)80344-X, 9247260.
14. Sanchez P, Hernandez AM, Stecca B, Kahler AJ, DeGueme AM, Barrett A, Beyna M, Datta MW, Datta S, Ruiz i Altaba A. Inhibition of prostate cancer proliferation by interference with SONIC HEDGEHOG-GLI1 signaling. Proc Natl Acad Sci USA 2004, 101:12561-12566. 10.1073/pnas.0404956101, 514658, 15314219.
15. Chung MK, Kim HJ, Lee YS, Han ME, Yoon S, Baek SY, Kim BS, Kim JB, Oh SO. Hedgehog signaling regulates proliferation of prostate cancer cells via stathmin1. Clin Exp Med 2009,
16. Mao L, Xia YP, Zhou YN, Dai RL, Yang X, Duan SJ, Qiao X, Mei YW, Hu B, Cui H. A critical role of Sonic Hedgehog signaling in maintaining the tumorigenicity of neuroblastoma cells. Cancer Sci 2009, 100:1848-1855. 10.1111/j.1349-7006.2009.01262.x, 19622100.
17. Singh RR, Cho-Vega JH, Davuluri Y, Ma S, Kasbidi F, Milito C, Lennon PA, Drakos E, Medeiros LJ, Luthra R, Vega F. Sonic hedgehog signaling pathway is activated in ALK-positive anaplastic large cell lymphoma. Cancer Res 2009, 69:2550-2558. 10.1158/0008-5472.CAN-08-1808, 19244133.
18. Kasper M, Regl G, Frischauf AM, Aberger F. GLI transcription factors: mediators of oncogenic Hedgehog signalling. Eur J Cancer 2006, 42:437-445. 10.1016/j.ejca.2005.08.039, 16406505.
19. Rubin LL, de Sauvage FJ. Targeting the Hedgehog pathway in cancer. Nat Rev Drug Discov 2006, 5:1026-1033. 10.1038/nrd2086, 17139287.
20. Dierks C, Grbic J, Zirlik K, Beigi R, Englund NP, Guo GR, Veelken H, Engelhardt M, Mertelsmann R, Kelleher JF, et al. Essential role of stromally induced hedgehog signaling in B-cell malignancies. Nat Med 2007, 13:944-951. 10.1038/nm1614, 17632527.
21. Lindemann RK. Stroma-initiated hedgehog signaling takes center stage in B-cell lymphoma. Cancer Res 2008, 68:961-964. 10.1158/0008-5472.CAN-07-5500, 18281468.
22. Watkins DN, Peacock CD. Hedgehog signalling in foregut malignancy. Biochem Pharmacol 2004, 68:1055-1060. 10.1016/j.bcp.2004.04.025, 15313401.
23. Wong SY, Seol AD, So PL, Ermilov AN, Bichakjian CK, Epstein EH, Dlugosz AA, Reiter JF. Primary cilia can both mediate and suppress Hedgehog pathway-dependent tumorigenesis. Nat Med 2009, 15:1055-1061. 10.1038/nm.2011, 19701205.
24. Sasai K, Romer JT, Kimura H, Eberhart DE, Rice DS, Curran T. Medulloblastomas derived from Cxcr6 mutant mice respond to treatment with a smoothened inhibitor. Cancer Res 2007, 67:3871-3877. 10.1158/0008-5472.CAN-07-0493, 17413002.
25. Williams JA, Guicherit OM, Zaharian BI, Xu Y, Chai L, Wichterle H, Kon C, Gatchalian C, Porter JA, Rubin LL, Wang FY. Identification of a small molecule inhibitor of the hedgehog signaling pathway: effects on basal cell carcinoma-like lesions. Proc Natl Acad Sci USA 2003, 100:4616-4621. 10.1073/pnas.0732813100, 153604, 12679522.
26. Romer J, Curran T. Targeting medulloblastoma: small-molecule inhibitors of the Sonic Hedgehog pathway as potential cancer therapeutics. Cancer Res 2005, 65:4975-4978. 10.1158/0008-5472.CAN-05-0481, 15958535.
27. Sanchez P, Clement V, Ruiz i Altaba A. Therapeutic targeting of the Hedgehog-GLI pathway in prostate cancer. Cancer Res 2005, 65:2990-2992.
28. Romer JT, Kimura H, Magdaleno S, Sasai K, Fuller C, Baines H, Connelly M, Stewart CF, Gould S, Rubin LL, Curran T. Suppression of the Shh pathway using a small molecule inhibitor eliminates medulloblastoma in Ptc1(+/-)p53(-/-) mice. Cancer Cell 2004, 6:229-240. 10.1016/j.ccr.2004.08.019, 15380514.
29. Zhang X, Harrington N, Moraes RC, Wu MF, Hilsenbeck SG, Lewis MT. Cyclopamine inhibition of human breast cancer cell growth independent of Smoothened (Smo). Breast Cancer Res Treat 2009, 115:505-521. 10.1007/s10549-008-0093-3, 18563554.
30. Hegde GV, Munger CM, Emanuel K, Joshi AD, Greiner TC, Weisenburger DD, Vose JM, Joshi SS. Targeting of sonic hedgehog-GLI signaling: a potential strategy to improve therapy for mantle cell lymphoma. Mol Cancer Ther 2008, 7:1450-1460. 10.1158/1535-7163.MCT-07-2118, 18524848.
31. Lauth M, Bergstrom A, Shimokawa T, Toftgard R. Inhibition of GLI-mediated transcription and tumor cell growth by small-molecule antagonists. Proc Natl Acad Sci USA 2007, 104:8455-8460. 10.1073/pnas.0609699104, 1866313,1866313, 17494766.
32. Chen X, Horiuchi A, Kikuchi N, Osada R, Yoshida J, Shiozawa T, Konishi I. Hedgehog signal pathway is activated in ovarian carcinomas, correlating with cell proliferation: it's inhibition leads to growth suppression and apoptosis. Cancer Sci 2007, 98:68-76. 10.1111/j.1349-7006.2006.00353.x, 17083567.
33. Tabs S, Avci O. Induction of the differentiation and apoptosis of tumor cells in vivo with efficiency and selectivity. Eur J Dermatol 2004, 14:96-102.
34. Warzecha J, Gottig S, Chow KU, Bruning C, Percic D, Boehrer S, Brude E, Kurth A. Inhibition of osteosarcoma cell proliferation by the Hedgehog-inhibitor cyclopamine. J Chemother 2007, 19:554-561.
35. Kimura H, Ng JM, Curran T. Transient inhibition of the Hedgehog pathway in young mice causes permanent defects in bone structure. Cancer Cell 2008, 13:249-260. 10.1016/j.ccr.2008.01.027, 18328428.
36. Makimura H, Mizuno TM, Mastaitis JW, Agami R, Mobbs CV. Reducing hypothalamic AGRP by RNA interference increases metabolic rate and decreases body weight without influencing food intake. BMC Neurosci 2002, 3:18. 10.1186/1471-2202-3-18, 134599, 12423556.
37. Matsui Y, Kobayashi N, Nishikawa M, Takakura Y. Sequence-specific suppression of mdr1a/1b expression in mice via RNA interference. Pharm Res 2005, 22:2091-2098. 10.1007/s11095-005-8178-8, 16184445.
38. Soutschek J, Akinc A, Bramlage B, Charisse K, Constien R, Donoghue M, Elbashir S, Geick A, Hadwiger P, Harborth J, et al. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature 2004, 432:173-178. 10.1038/nature03121, 15538359.
39. Song E, Lee SK, Wang J, Ince N, Ouyang N, Min J, Chen J, Shankar P, Lieberman J. RNA interference targeting Fas protects mice from fulminant hepatitis. Nat Med 2003, 9:347-351. 10.1038/nm828, 12579197.
40. Zender L, Hutker S, Liedtke C, Tillmann HL, Zender S, Mundt B, Waltemathe M, Gosling T, Flemming P, Malek NP, et al. Caspase 8 small interfering RNA prevents acute liver failure in mice. Proc Natl Acad Sci USA 2003, 100:7797-7802. 10.1073/pnas.1330920100, 164667, 12810955.
41. Yano J, Hirabayashi K, Nakagawa S, Yamaguchi T, Nogawa M, Kashimori I, Naito H, Kitagawa H, Ishiyama K, Ohgi T, Irimura T. Antitumor activity of small interfering RNA/cationic liposome complex in mouse models of cancer. Clin Cancer Res 2004, 10:7721-7726. 10.1158/1078-0432.CCR-04-1049, 15570006.
42. Arimura S, Matsunaga A, Kitamura T, Aoki K, Aoki M, Taketo MM. Reduced level of smoothened suppresses intestinal tumorigenesis by down-regulation of Wnt signaling. Gastroenterology 2009, 137:629-638. 10.1053/j.gastro.2009.04.059, 19427313.
43. Haydon RC, Deyrup A, Ishikawa A, Heck R, Jiang W, Zhou L, Feng T, King D, Cheng H, Breyer B, et al. Cytoplasmic and/or nuclear accumulation of the beta-catenin protein is a frequent event in human osteosarcoma. Int J Cancer 2002, 102:338-342. 10.1002/ijc.10719, 12402302.
44. Iwaya K, Ogawa H, Kuroda M, Izumi M, Ishida T, Mukai K. Cytoplasmic and/or nuclear staining of beta-catenin is associated with lung metastasis. Clin Exp Metastasis 2003, 20:525-529. 10.1023/A:1025821229013, 14598886.
45. Kamura T, Hara T, Matsumoto M, Ishida N, Okumura F, Hatakeyama S, Yoshida M, Nakayama K, Nakayama KI. Cytoplasmic ubiquitin ligase KPC regulates proteolysis of p27(Kip1) at G1 phase. Nat Cell Biol 2004, 6:1229-1235. 10.1038/ncb1194, 15531880.
46. Hara T, Kamura T, Kotoshiba S, Takahashi H, Fujiwara K, Onoyama I, Shirakawa M, Mizushima N, Nakayama KI. Role of the UBL-UBA protein KPC2 in degradation of p27 at G1 phase of the cell cycle. Mol Cell Biol 2005, 25:9292-9303. 10.1128/MCB.25.21.9292-9303.2005, 1265808, 16227581.
47. Hwang HC, Clurman BE. Cyclin E in normal and neoplastic cell cycles. Oncogene 2005, 24:2776-2786. 10.1038/sj.onc.1208613, 15838514.
48. Swanton C. Cell-cycle targeted therapies. Lancet Oncol 2004, 5:27-36. 10.1016/S1470-2045(03)01321-4, 14700606.
49. Duman-Scheel M, Weng L, Xin S, Du W. Hedgehog regulates cell growth and proliferation by inducing Cyclin D and Cyclin E. Nature 2002, 417:299-304. 10.1038/417299a, 12015606.
50. Yoon JW, Kita Y, Frank DJ, Majewski RR, Konicek BA, Nobrega MA, Jacob H, Walterhouse D, Iannaccone P. Gene expression profiling leads to identification of GLI1-binding elements in target genes and a role for multiple downstream pathways in GLI1-induced cell transformation. J Biol Chem 2002, 277:5548-5555. 10.1074/jbc.M105708200, 11719506.
51. Mill P, Mo R, Fu H, Grachtchouk M, Kim PC, Dlugosz AA, Hui CC. Sonic hedgehog-dependent activation of Gli2 is essential for embryonic hair follicle development. Genes Dev 2003, 17:282-294. 10.1101/gad.1038103, 195973, 12533516.
52. Zhang L, Wang C. F-box protein Skp2: a novel transcriptional target of E2F. Oncogene 2006, 25:2615-2627. 10.1038/sj.onc.1209286, 1513044, 16331253.
53. Regl G, Kasper M, Schnidar H, Eichberger T, Neill GW, Ikram MS, Quinn AG, Philpott MP, Frischauf AM, Aberger F. The zinc-finger transcription factor GLI2 antagonizes contact inhibition and differentiation of human epidermal cells. Oncogene 2004, 23:1263-1274. 10.1038/sj.onc.1207240, 14691458.
54. Tsuda N, Ishiyama S, Li Y, Ioannides CG, Abbruzzese JL, Chang DZ. Synthetic microRNA designed to target glioma-associated antigen 1 transcription factor inhibits division and induces late apoptosis in pancreatic tumor cells. Clin Cancer Res 2006, 12:6557-6564. 10.1158/1078-0432.CCR-06-0588, 17085671.
55. Tanaka M, Setoguchi T, Hirotsu M, Gao H, Sasaki H, Matsunoshita Y, Komiya S. Inhibition of Notch pathway prevents osteosarcoma growth by cell cycle regulation. Br J Cancer 2009, 100:1957-1965. 10.1038/sj.bjc.6605060, 19455146.
56. Ross J, Li L. Recent advances in understanding extrinsic control of hematopoietic stem cell fate. Curr Opin Hematol 2006, 13:237-242. 10.1097/01.moh.0000231420.92782.8f, 16755219.
57. Tian H, Callahan CA, DuPree KJ, Darbonne WC, Ahn CP, Scales SJ, de Sauvage FJ. Hedgehog signaling is restricted to the stromal compartment during pancreatic carcinogenesis. Proc Natl Acad Sci USA 2009, 106:4254-4259. 10.1073/pnas.0813203106, 2647977,2647977, 19246386.
58. Yauch RL, Gould SE, Scales SJ, Tang T, Tian H, Ahn CP, Marshall D, Fu L, Januario T, Kallop D, et al. A paracrine requirement for hedgehog signalling in cancer. Nature 2008, 455:406-410. 10.1038/nature07275, 18754008.
59. Dierks C, Beigi R, Guo GR, Zirlik K, Stegert MR, Manley P, Trussell C, Schmitt-Graeff A, Landwerlin K, Veelken H, Warmuth M. Expansion of Bcr-Abl-positive leukemic stem cells is dependent on Hedgehog pathway activation. Cancer Cell 2008, 14:238-249. 10.1016/j.ccr.2008.08.003, 18772113.
60. Clarke MF, Fuller M. Stem cells and cancer: two faces of eve. Cell 2006, 124:1111-1115. 10.1016/j.cell.2006.03.011, 16564000.
61. Murase M, Kano M, Tsukahara T, Takahashi A, Torigoe T, Kawaguchi S, Kimura S, Wada T, Uchihashi Y, Kondo T, et al. Side population cells have the characteristics of cancer stem-like cells/cancer-initiating cells in bone sarcomas. Br J Cancer 2009, 101:1425-1432. 10.1038/sj.bjc.6605330, 19826427.
62. Levings PP, McGarry SV, Currie TP, Nickerson DM, McClellan S, Ghivizzani SC, Steindler DA, Gibbs CP. Expression of an exogenous human Oct-4 promoter identifies tumor-initiating cells in osteosarcoma. Cancer Res 2009, 69:5648-5655. 10.1158/0008-5472.CAN-08-3580, 19584295.
63. Fujii H, Honoki K, Tsujiuchi T, Kido A, Yoshitani K, Takakura Y. Sphere-forming stem-like cell populations with drug resistance in human sarcoma cell lines. Int J Oncol 2009, 34:1381-1386.
64. Wang L, Park P, Lin CY. Characterization of stem cell attributes in human osteosarcoma cell lines. Cancer Biol Ther 2009, 8(6).
65. Hirotsu M, Setoguchi T, Matsunoshita Y, Sasaki H, Nagao H, Gao H, Sugimura K, Komiya S. Tumour formation by single fibroblast growth factor receptor 3-positive rhabdomyosarcoma-initiating cells. Br J Cancer 2009, 101:2030-2037. 10.1038/sj.bjc.6605407, 19888223.
66. Zhao C, Chen A, Jamieson CH, Fereshteh M, Abrahamsson A, Blum J, Kwon HY, Kim J, Chute JP, Rizzieri D, et al. Hedgehog signalling is essential for maintenance of cancer stem cells in myeloid leukaemia. Nature 2009, 458:776-779. 10.1038/nature07737, 19169242.
67. Hotta T, Motoyama T, Watanabe H. Three human osteosarcoma cell lines exhibiting different phenotypic expressions. Acta Pathol Jpn 1992, 42:595-603.
68. Fan X, Mikolaenko I, Elhassan I, Ni X, Wang Y, Ball D, Brat DJ, Perry A, Eberhart CG. Notch1 and notch2 have opposite effects on embryonal brain tumor growth. Cancer Res 2004, 64:7787-7793. 10.1158/0008-5472.CAN-04-1446, 15520184.