Genomic Analysis of Smoothened Inhibitor Resistance in Basal Cell Carcinoma

Cancer Cell

Volumn 27, Issue 3, 2015, Pages 327-341

  Sharpe, Hayley J ^a   Pau, Gregoire ^a   Dijkgraaf, Gerrit J ^a   Basset Seguin, Nicole ^b   Modrusan, Zora ^a   Januario, Thomas ^a   Tsui, Vickie ^a   Durham, Alison B ^c   Dlugosz, Andrzej A ^c   Haverty, Peter M ^a   Bourgon, Richard ^a   Tang, Jean Y ^d   Sarin, Kavita Y ^d   Dirix, Luc ^e   Fisher, David C ^f   Rudin, Charles M ^g   Sofen, Howard ^h   Migden, Michael R ⁱ   Yauch, Robert L ^a   de Sauvage, Frederic J ^a  

^a GENENTECH INC   (United States)

^b SAINT LOUIS HOSPITAL   (France)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^f DANA FARBER CANCER INSTITUTE   (United States)

^g MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VISMODEGIB; ANILIDE; CELL SURFACE RECEPTOR; G PROTEIN COUPLED RECEPTOR; GLI2 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; NUCLEAR PROTEIN; PATCHED RECEPTORS; PYRIDINE DERIVATIVE; REPRESSOR PROTEIN; SMO PROTEIN, HUMAN; SONIC HEDGEHOG PROTEIN; SUFU PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASAL CELL CARCINOMA; CANCER RESISTANCE; CLINICAL ARTICLE; CONTROLLED STUDY; GENE; GENE MUTATION; GENOMICS; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PTCH1 GENE; SMO GENE; BINDING SITE; CARCINOMA, BASAL CELL; CHEMICAL STRUCTURE; CHEMISTRY; COPY NUMBER VARIATION; DNA SEQUENCE; DRUG RESISTANCE; EXOME; GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN TERTIARY STRUCTURE; SKIN NEOPLASMS;

ERINACEIDAE;

ANILIDES; BINDING SITES; CARCINOMA, BASAL CELL; DNA COPY NUMBER VARIATIONS; DNA MUTATIONAL ANALYSIS; DRUG RESISTANCE, NEOPLASM; EXOME; HEDGEHOG PROTEINS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MODELS, MOLECULAR; MUTATION; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; PYRIDINES; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; REPRESSOR PROTEINS; SEQUENCE ANALYSIS, DNA; SKIN NEOPLASMS;

EID: 84924262003     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.02.001     Document Type: Article

References (50)

1. Amakye D., Jagani Z., Dorsch M. Unraveling the therapeutic potential of the Hedgehog pathway in cancer. Nat. Med. 2013, 19:1410-1422.
2. Atwood S.X., Li M., Lee A., Tang J.Y., Oro A.E. GLI activation by atypical protein kinase C ι/λ regulates the growth of basal cell carcinomas. Nature 2013, 494:484-488.
3. Brastianos P.K., Horowitz P.M., Santagata S., Jones R.T., McKenna A., Getz G., Ligon K.L., Palescandolo E., Van Hummelen P., Ducar M.D., et al. Genomic sequencing of meningiomas identifies oncogenic SMO and AKT1 mutations. Nat. Genet. 2013, 45:285-289.
4. Brinkhuizen T., Reinders M.G., van Geel M., Hendriksen A.J., Paulussen A.D., Winnepenninckx V.J., Keymeulen K.B., Soetekouw P.M., van Steensel M.A., Mosterd K. Acquired resistance to the Hedgehog pathway inhibitor vismodegib due to smoothened mutations in treatment of locally advanced basal cell carcinoma. J.Am. Acad. Dermatol. 2014, 71:1005-1008.
5. Buonamici S., Williams J., Morrissey M., Wang A., Guo R., Vattay A., Hsiao K., Yuan J., Green J., Ospina B., et al. Interfering with resistance to smoothened antagonists by inhibition of the PI3K pathway in medulloblastoma. Sci. Transl. Med. 2010, 2:51ra70.
6. Chang A.L., Oro A.E. Initial assessment of tumor regrowth after vismodegib in advanced Basal cell carcinoma. Arch. Dermatol. 2012, 148:1324-1325.
7. Clark V.E., Erson-Omay E.Z., Serin A., Yin J., Cotney J., Ozduman K., Avşar T., Li J., Murray P.B., Henegariu O., et al. Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO. Science 2013, 339:1077-1080.
8. Das Thakur M., Stuart D.D. The evolution of melanoma resistance reveals therapeutic opportunities. Cancer Res. 2013, 73:6106-6110.
9. Dijkgraaf G.J., Alicke B., Weinmann L., Januario T., West K., Modrusan Z., Burdick D., Goldsmith R., Robarge K., Sutherlin D., et al. Small molecule inhibition of GDC-0449 refractory smoothened mutants and downstream mechanisms of drug resistance. Cancer Res. 2011, 71:435-444.
10. Gether U., Ballesteros J.A., Seifert R., Sanders-Bush E., Weinstein H., Kobilka B.K. Structural instability of a constitutively active G protein-coupled receptor. Agonist-independent activation due to conformational flexibility. J.Biol. Chem. 1997, 272:2587-2590.
11. González-Pérez A., López-Bigas N. Improving the assessment of the outcome of nonsynonymous SNVs with a consensus deleteriousness score, Condel. Am. J. Hum. Genet. 2011, 88:440-449.
12. Greenman C.D., Bignell G., Butler A., Edkins S., Hinton J., Beare D., Swamy S., Santarius T., Chen L., Widaa S., et al. PICNIC: an algorithm to predict absolute allelic copy number variation with microarray cancer data. Biostatistics 2010, 11:164-175.
13. 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.
14. Inukai M., Toyooka S., Ito S., Asano H., Ichihara S., Soh J., Suehisa H., Ouchida M., Aoe K., Aoe M., et al. Presence of epidermal growth factor receptor gene T790M mutation as a minor clone in non-small cell lung cancer. Cancer Res. 2006, 66:7854-7858.
15. Jayaraman S.S., Rayhan D.J., Hazany S., Kolodney M.S. Mutational landscape of basal cell carcinomas by whole-exome sequencing. J.Invest. Dermatol. 2014, 134:213-220.
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. Kandoth C., McLellan M.D., Vandin F., Ye K., Niu B., Lu C., Xie M., Zhang Q., McMichael J.F., Wyczalkowski M.A., et al. Mutational landscape and significance across 12 major cancer types. Nature 2013, 502:333-339.
18. Katritch V., Cherezov V., Stevens R.C. Structure-function of the G protein-coupled receptor superfamily. Annu. Rev. Pharmacol. Toxicol. 2013, 53:531-556.
19. Kool M., Jones D.T., Jäger N., Northcott P.A., Pugh T.J., Hovestadt V., Piro R.M., Esparza L.A., Markant S.L., Remke M., et al. Genome sequencing of SHH medulloblastoma predicts genotype-related response to smoothened inhibition. Cancer Cell 2014, 25:393-405. ICGC PedBrain Tumor Project.
20. Lackner M.R., Wilson T.R., Settleman J. Mechanisms of acquired resistance to targeted cancer therapies. Future Oncol. 2012, 8:999-1014.
21. Lawrence M.S., Stojanov P., Polak P., Kryukov G.V., Cibulskis K., Sivachenko A., Carter S.L., Stewart C., Mermel C.H., Roberts S.A., et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 2013, 499:214-218.
22. Lee Y., Kawagoe R., Sasai K., Li Y., Russell H.R., Curran T., McKinnon P.J. Loss of suppressor-of-fused function promotes tumorigenesis. Oncogene 2007, 26:6442-6447.
23. Long J., Li B., Rodriguez-Blanco J., Pastori C., Volmar C.H., Wahlestedt C., Capobianco A., Bai F., Pei X.H., Ayad N.G., Robbins D.J. The BET bromodomain inhibitor I-BET151 acts downstream of Smoothened to abrogate the growth of Hedgehog driven cancers. J.Biol. Chem. 2014, 289:35494-35502.
24. LoRusso P.M., Rudin C.M., Reddy J.C., Tibes R., Weiss G.J., Borad M.J., Hann C.L., Brahmer J.R., Chang I., Darbonne W.C., et al. Phase I trial of hedgehog pathway inhibitor vismodegib (GDC-0449) in patients with refractory, locally advanced or metastatic solid tumors. Clin. Cancer Res. 2011, 17:2502-2511.
25. Metcalfe C., Alicke B., Crow A., Lamoureux M., Dijkgraaf G.J., Peale F., Gould S.E., de Sauvage F.J. PTEN loss mitigates the response of medulloblastoma to Hedgehog pathway inhibition. Cancer Res. 2013, 73:7034-7042.
26. Miller J.H. Mutagenic specificity of ultraviolet light. J.Mol. Biol. 1985, 182:45-65.
27. Nedelcu D., Liu J., Xu Y., Jao C., Salic A. Oxysterol binding to the extracellular domain of Smoothened in Hedgehog signaling. Nat. Chem. Biol. 2013, 9:557-564.
28. Negrini S., Gorgoulis V.G., Halazonetis T.D. Genomic instability-an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol. 2010, 11:220-228.
29. Nik-Zainal S., Van Loo P., Wedge D.C., Alexandrov L.B., Greenman C.D., Lau K.W., Raine K., Jones D., Marshall J., Ramakrishna M., et al. The life history of 21 breast cancers. Cell 2012, 149:994-1007. Breast Cancer Working Group of the International Cancer Genome Consortium.
30. Oro A.E., Higgins K.M., Hu Z., Bonifas J.M., Epstein E.H., Scott M.P. Basal cell carcinomas in mice overexpressing sonic hedgehog. Science 1997, 276:817-821.
31. Pastorino L., Ghiorzo P., Nasti S., Battistuzzi L., Cusano R., Marzocchi C., Garrè M.L., Clementi M., Scarrà G.B. Identification of a SUFU germline mutation in a family with Gorlin syndrome. Am. J. Med. Genet. A. 2009, 149A:1539-1543.
32. Pesz K.A., Bieniek A., Makowska I., Sasiadek M.M. Basal cell carcinoma of the skin: whole genome screening by comparative genome hybridization revisited. J.Cutan. Pathol. 2013, 40:25-29.
33. Pricl S., Cortelazzi B., Dal Col V., Marson D., Laurini E., Fermeglia M., Licitra L., Pilotti S., Bossi P., Perrone F. Smoothened (SMO) receptor mutations dictate resistance to vismodegib in basal cell carcinoma. Mol. Oncol. 2014, 9:389-397.
34. Reifenberger J., Wolter M., Weber R.G., Megahed M., Ruzicka T., Lichter P., Reifenberger G. Missense mutations in SMOH in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system. Cancer Res. 1998, 58:1798-1803.
35. Reifenberger J., Wolter M., Knobbe C.B., Köhler B., Schönicke A., Scharwächter C., Kumar K., Blaschke B., Ruzicka T., Reifenberger G. Somatic mutations in the PTCH, SMOH, SUFUH and TP53 genes in sporadic basal cell carcinomas. Br. J. Dermatol. 2005, 152:43-51.
36. Sasai K., Romer J.T., Lee Y., Finkelstein D., Fuller C., McKinnon P.J., Curran T. Shh pathway activity is down-regulated in cultured medulloblastoma cells: implications for preclinical studies. Cancer Res. 2006, 66:4215-4222.
37. 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.
38. Smith M.J., Beetz C., Williams S.G., Bhaskar S.S., O'Sullivan J., Anderson B., Daly S.B., Urquhart J.E., Bholah Z., Oudit D., et al. Germline mutations in SUFU cause Gorlin syndrome-associated childhood medulloblastoma and redefine the risk associated with PTCH1 mutations. J.Clin. Oncol. 2014, Published online November 17, 2014. 10.1200/JCO.2014.58.2569.
39. Stjernqvist S., Rydén T., Greenman C.D. Model-integrated estimation of normal tissue contamination for cancer SNP allelic copy number data. Cancer Inform. 2011, 10:159-173.
40. Stone D.M., Murone M., Luoh S., Ye W., Armanini M.P., Gurney A., Phillips H., Brush J., Goddard A., de Sauvage F.J., Rosenthal A. Characterization of the human suppressor of fused, a negative regulator of the zinc-finger transcription factor Gli. J.Cell Sci. 1999, 112:4437-4448.
41. Svärd J., Heby-Henricson K., Persson-Lek M., Rozell B., Lauth M., Bergström A., Ericson J., Toftgård R., Teglund S. Genetic elimination of Suppressor of fused reveals an essential repressor function in the mammalian Hedgehog signaling pathway. Dev. Cell 2006, 10:187-197.
42. Sweeney R.T., McClary A.C., Myers B.R., Biscocho J., Neahring L., Kwei K.A., Qu K., Gong X., Ng T., Jones C.D., et al. Identification of recurrent SMO and BRAF mutations in ameloblastomas. Nat. Genet. 2014, 46:722-725.
43. Tang Y., Gholamin S., Schubert S., Willardson M.I., Lee A., Bandopadhayay P., Bergthold G., Masoud S., Nguyen B., Vue N., et al. Epigenetic targeting of Hedgehog pathway transcriptional output through BET bromodomain inhibition. Nat. Med. 2014, 20:732-740.
44. Taylor M.D., Liu L., Raffel C., Hui C.C., Mainprize T.G., Zhang X., Agatep R., Chiappa S., Gao L., Lowrance A., et al. Mutations in SUFU predispose to medulloblastoma. Nat. Genet. 2002, 31:306-310.
45. Wang G.Y., So P.L., Wang L., Libove E., Wang J., Epstein E.H. Establishment of murine basal cell carcinoma allografts: a potential model for preclinical drug testing and for molecular analysis. J.Invest. Dermatol. 2011, 131:2298-2305.
46. Wang C., Wu H., Katritch V., Han G.W., Huang X.P., Liu W., Siu F.Y., Roth B.L., Cherezov V., Stevens R.C. Structure of the human smoothened receptor bound to an antitumour agent. Nature 2013, 497:338-343.
47. Wechsler-Reya R.J., Scott M.P. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 1999, 22:103-114.
48. Wong H., Alicke B., West K.A., Pacheco P., La H., Januario T., Yauch R.L., de Sauvage F.J., Gould S.E. Pharmacokinetic-pharmacodynamic analysis of vismodegib in preclinical models of mutational and ligand-dependent Hedgehog pathway activation. Clin. Cancer Res. 2011, 17:4682-4692.
49. Xie J., Murone M., Luoh S.M., Ryan A., Gu Q., Zhang C., Bonifas J.M., Lam C.W., Hynes M., Goddard A., et al. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 1998, 391:90-92.
50. Yauch R.L., Dijkgraaf G.J., Alicke B., Januario T., Ahn C.P., Holcomb T., Pujara K., Stinson J., Callahan C.A., Tang T., et al. Smoothened mutation confers resistance to a Hedgehog pathway inhibitor in medulloblastoma. Science 2009, 326:572-574.