In vitro and in vivo characterization of a novel hedgehog signaling antagonist in human glioblastoma cell lines

International Journal of Cancer

Volumn 131, Issue 2, 2012, Pages

  Ferruzzi, Pietro ^a   Mennillo, Federica ^a   De Rosa, Antonella ^a   Giordano, Cinzia ^a   Rossi, Marco ^a   Benedetti, Giovanni ^a   Magrini, Roberta ^a   Mohr, Gal La Pericot ^a   Miragliotta, Vincenzo ^a   Magnoni, Letizia ^a   Mori, Elisa ^a   Thomas, Russell ^a   Tunici, Patrizia ^a   Bakker, Annette ^a  

^a Siena Biotech SpA   (Italy)

Author keywords

gli; glioblastoma; Hedgehog; patched; smoothened; temozolomide

Indexed keywords

ANTINEOPLASTIC AGENT; BETA TUBULIN; FIBRONECTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; SEN 450; SMOOTHENED PROTEIN; TEMOZOLOMIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER RECURRENCE; CARCINOGENICITY; DRUG BIOAVAILABILITY; DRUG MECHANISM; DRUG PENETRATION; GENE; GENE EXPRESSION; GENE SEQUENCE; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MONOTHERAPY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCHED 1 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS INHIBITION; RECEPTOR GENE; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTHENED GENE; SONIC HEDGEHOG GENE; TUMOR DIFFERENTIATION; TUMOR VOLUME;

ANILIDES; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; DACARBAZINE; GENE EXPRESSION PROFILING; GLIOBLASTOMA; HEDGEHOG PROTEINS; HUMANS; MICE; MICE, NUDE; PYRIDINES; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; VERATRUM ALKALOIDS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84861614106     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.27349     Document Type: Article

References (46)

1. Kang KM, Kang SK,. Tumorigenesis of chemotherapeutic drug-resistant cancer stem-like cells in brain glioma. Stem Cell Dev 2007; 16: 837-47.
2. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, Cavenee WK, DePinho RA,. Malignant glioma: genetics and biology of a grave matter. Genes Dev 2001; 15: 1311-33.
3. Reya T, Morrison SJ, Clarke MF, Weissman IL,. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-11.
4. Park DM, Rich JN,. Biology of glioma cancer stem cells. Mol Cells 2009; 28: 7-12.
5. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB,. Identification of human brain tumor initiating cells. Nature 2004; 432: 396-401.
6. Dirks PB,. Brain tumor stem cells: The cancer stem cell hypothesis writ large. Mol Oncol 2010; 4: 420-30.
7. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS,. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006; 5: 67.
8. Liu L, Andrews LG, Tollefsbol TO,. Loss of the human polycomb group protein BMI1 promotes cancer-specific cell death. Oncogene 2006; 25: 4370-5.
9. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN,. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 756-60.
10. Eramo A, Ricci-Vitiani L, Zeuner A, Pallini R, Lotti F, Sette G, Pilozzi E, Larocca LM, Peschle C, De Maria R,. Chemotherapy resistence of glioblastoma stem cells. Cell Death Differ 2006; 13: 1238-41.
11. Ignatova TN, Kukekov VG, Laywell ED, Suslov ON, Vrionis FD, Steindler DA,. Human cortical glial tumors contain neural-stem-like cells expressing astroglial and neuronal markers in vitro. Glia 2002; 39: 193-206.
12. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, DiMeco F, Vescovi AL,. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004; 64: 7011-21.
13. Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann-Hogiu S, Farkas DL, Black KL, Yu JS,. Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 2004; 23: 9392-400.
14. Ruiz i, Altaba A, Sanchez P, Dahmane Nl,. Gli and Hedgehog in cancer: tumors, embryos and stem cells. Nat Rev Cancer 2002; 3: 24-33.
15. Bar EE, Chaudhry A, Lin A, Fan X, Schreck K, Matsui W, Vescovi AL, DiMeco F, Olivi A, Eberhart CG,. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 2007; 25: 2524-33.
16. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Altaba AR,. Hedgehog-Gli1 signaling regulates human glioma growth, cancer stem cell self-renewal and tumorigenicity. Curr Biol 2007; 17: 165-72.
17. Sasai K, Romer JT, Lee Y, Finkelstein D, Fuller C, McKinnon PJ, Curran T,. Shh pathway activity is down-regulated in cultured medulloblastoma cells: implications for preclinical studies. Cancer Res 2006; 66: 4215-22.
18. Yauch RL, Gould SE, Scales SJ, Tang T, Tian H, Ahn CP, Marshall D, Fu L, Januario T, Kallop D, Nannini-Pepe M, Kotkow K, et al. A paracrine requirement for hedgehog signaling in cancer. Nature 2008; 455: 406-10.
19. Rudin CM, Hann CL, Laterra J, Yauch RL, Callahan CA, Fu L, Holcomb T, Stinson J, Gould SE, Coleman B, LoRusso PM, Von Hoff DD, et al. Treatment of medulloblastoma with hedgehog pathway inhibitor. N Engl J Med 2009; 361: 1173-8.
20. Robarge KD, Brunton SA, Castanedo GM, Cui Y, Dina MS, Goldsmith R, Gould SE, Guichert O, Gunzner JL, Halladay J, Jia W, Khojasteh C, et al. GDC-0449-a potent inhibitor of hedgehog pathway. Bioorg Med Chem Lett 2009; 19: 5576-81.
21. Thomas RJ, Pericot Mohr G, Minetto G, Bakker A, Ferruzzi P,. The hedgehog pathway antagonists and therapeutic thereof. WO /2009/074300 2009.
22. Rubin L, Guicherit OM, Price S, Boyd EAl,. Mediators of hedgehog signaling pathways, compositions and uses related thereto. WO /2003/011219 2003.
23. Stecca B, Mas C, Clement C, Zbinden M, Correa R, Piguet V, Beermann F, Ruiz I, Altaba A,. Melanomas require HEDGEHOG/GLI signaling regulated by interaction between GLI1 and the RAS-MEK/AKT pathways. Proc Natl Acad Sci USA 2007; 114: 5895-900.
24. Chen JK, Taipale J, Cooper MK, Beachy PA,. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev 2002; 16: 2743-8.
25. Wu X, Walker J, Zhang J, Ding S, Schultz PG,. Purmorphamine induces osteogenesis by activation of the hedgehog signaling pathway. Chem Biol 2004; 11: 1229-38.
26. Euhus DM, Hudd C, LaRegina MC, Johnson FE,. Tumor measurement in the nude mouse. J Surg Oncol 1986; 31: 229-34.
27. Rieske P, Golanska E, Zakrzewska M, Piaskowski S, Hulas-Bigoszewska K, Wolanczyk M, Szybka M, Witusik-Perkowska M, Jaskolski DJ, Zakrzewski K, Biernat W, Krynska B, et al. BMC Cancer 2009; 9: 54.
28. Berman DM, Karhadkar SS, Maitra A, Montes De Oca R, Gerstenblith MR, Briggs K, Parker AR, Shimada Y, Eshleman JR, Watkins DN, Beachy PA,. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumors. Nature 2003; 425: 846-51.
29. Huangfu D, Liu A, Rakeman AS, Murcia NS, Niswander L, Anderson KV,. Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 2003; 426: 83-7.
30. Rohatgi R, Milenkovic L, Scott MP,. Patched1 regulates hedgehog signaling at the primary cilium. Science 2007; 317: 372-6.
31. Rohatgi R, Milenkovic L, Corcoran RB, Scott MP,. Hedgehog signal transduction by smoothened: pharmacologic evidence for a 2-step activation process Proc Natl Acad Sci USA 2009; 106: 3196-201.
32. Wang Y, Zhou Z, Walsh CT, McMahon AP,. Selective translocation of intracellular Smoothened to the primary cilium in response to hedgehog pathway modulation. Proc Natl Acad Sci USA 2009; 106: 2623-8.
33. Yang L, Xie G, Fan Q, Xie J,. Activation of the hedgehog-signaling pathway in human cancer and the clinical implications. Oncogene 2010; 29: 469-81.
34. Katayam M, Yoshida K, Ishimori H, Katayama M, Kawase T, Motoyama J, Kamiguchi H,. Patched and smoothened mRNA expression in human astrocytic tumors inversely correlates with histological malignancy. J Neuroncol 2002; 59: 107-15.
35. Dahmane N, Sanchez P, Gitton Y, Palma V, Sun T, Beyna M, Weiner H, Ruiz i, Altaba A,. The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumorigenesis. Development 2001; 128: 5201-12.
36. Sims-Mourtada J, Izzo JG, Apisarnthanarax S, Wu TT, Malhotra U, Luthra R, Liao Z, Komaki R, Van der Kogel A, Ajani J, Chao KS,. Hedgehog: an attribute to tumor regrowth after chemoradiotherapy and a target to improve radiation response. Clin Cancer Res 2006; 12: 6565-72.
37. Stone DM, Hynes M, Armanini M, Swanson TA, Gu Q, Johnson RL, Scott MP, Pennica D, Goddard A, Phillips H, Noll M, Hooper JE, et al. The tumor suppressor gene patched encodes a candidate receptor for sonic hedgehog. Nature 1996; 384: 129-34.
38. King PJ, Guasti L, Laufer E,. Hedgehog signaling in endocrine development and disease. J Endocrinol 2008; 198: 439-50.
39. Sasaki H, Hui C, Nakafuku M, Kondoh H,. A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 1997; 124: 1313-22.
40. Katoh Y, Katoh M,. Hedgehog target genes: mechanisms of carcinogenesis induced by aberrant hedgehog signaling activation. Curr Mol Med 2009; 9 873-86.
41. Ehtesham M, Sarangi A, Valadez JG, Chanthaphaychith S, Becher MW, Abel TW, Thompson RC, Cooper MK,. Ligand-dependent activation of the hedgehog pathway in glioma progenitor cells. Oncogene 2007; 26: 5752-61.
42. Wang K, Pan L, Xiaoming C, Daming C, Li C,. Gli1 inhibition induces cell-cycle arrest and enhanced apoptosis in brain glioma cell lines. J Neurooncol 2010; 98: 319-27.
43. Rossi M, Magnoni L, Miracco C, Mori E, Tosi P, Pirtoli L, Tini P, Oliveri G, Cosci E, Bakker A,. β-catenin and Gli1 are prognostic markers in glioblastoma. Cancer Biol Ther 2011; 11: 753-61.
44. Varnat F, Duquet A, Malerba M, Zbinden M, Mas C, Gervaz P, Ruiz I, Altaba A,. Human colon cancer ephitelial cells harbor active hedgehog-Gli signaling that is essential for tumor growth, recurrence, metastasis and stem cell survival and expansion. EMBO Mol Med 2009; 1: 338-51.
45. Charles N, and, Holland EC,. Brain tumor treatment increases the number of cancer stem-like cells. Exp Rev Neurother 2009; 9: 1447-9.
46. Mueller MT, Hermann PC, Witthauer J, Rubio-Viqueira B, Leicht SF, Huber S, Ellwart JW, Mustafa M, Bartenstein P, D'Haese JG, Schoenberg MH, Berger F, et al. Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology 2009; 137: 1102-13.