Functional kinomics identifies candidate therapeutic targets in head and neck cancer

Clinical Cancer Research

Volumn 20, Issue 16, 2014, Pages 4274-4288

  Moser, Russell ^a   Xu, Chang ^a,b   Kao, Michael ^b   Annis, James ^c   Lerma, Luisa Angelica ^b   Schaupp, Christopher M ^d   Gurley, Kay E ^a   Jang, In Sock ^e   Biktasova, Asel ^f   Yarbrough, Wendell G ^f   Margolin, Adam A ^e   Grandori, Carla ^a,c   Kemp, Christopher J ^a   Méndez, Eduardo ^a,b,g  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON MEDICAL CENTER   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e SAGE BIONETWORKS   (United States)

^f YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; FOCAL ADHESION KINASE; KINASE WEE1; MK 1775; P 4394; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; NUCLEAR PROTEIN; PROTEIN KINASE; PROTEIN KINASE INHIBITOR; PROTEIN P53; SMALL INTERFERING RNA; WEE1 PROTEIN, HUMAN; WEE1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATM GENE; CELL VIABILITY; CONTROLLED STUDY; ENZYME INHIBITION; FUNCTIONAL KINOMICS; G2 PHASE CELL CYCLE CHECKPOINT; GENETIC SCREENING; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MOLECULAR GENETICS; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; P19 GENE; PHASE TRANSITION; PRIMARY TUMOR; PRIORITY JOURNAL; PRKDC GENE; REGULATOR GENE; RNA INTERFERENCE; SENSITIVITY ANALYSIS; SPECIES COMPARISON; SQUAMOUS CELL CARCINOMA CELL LINE; TUMOR SUPPRESSOR GENE; VALIDATION PROCESS; ANIMAL; ANTAGONISTS AND INHIBITORS; CARCINOMA, SQUAMOUS CELL; CHEMISTRY; GENETICS; HEAD AND NECK NEOPLASMS; METABOLISM; MUTATION; NONOBESE DIABETIC MOUSE; SCID MOUSE;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL CYCLE PROTEINS; HEAD AND NECK NEOPLASMS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; MUTATION; NUCLEAR PROTEINS; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTEIN-TYROSINE KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84905985785     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-2858     Document Type: Article

References (50)

1. Bernier J, Domenge C, Ozsahin M, Matuszewska K, Lefebvre JL, Greiner RH, et al. Postoperative irradiation with or without concomitant chemotherapy for locally advanced head and neck cancer. N Engl J Med 2004;350:1945-52. (Pubitemid 38580197)
2. Machtay M, Moughan J, Trotti A, Garden AS, Weber RS, Cooper JS, et al. Factors associated with severe late toxicity after concurrent chemoradiation for locally advanced head and neck cancer: an RTOG analysis. J Clin Oncol 2008;26:3582-9.
3. Bonner JA, Harari PM, Giralt J, Azarnia N, Shin DM, Cohen RB, et al. Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N Engl J Med 2006;354:567-78. (Pubitemid 43209104)
4. Gasco M, Crook T. The p53 network in head and neck cancer. Oral Oncol 2003;39:222-31. (Pubitemid 36255688)
5. Hauser U, Balz V, Carey TE, Grenman R, Van Lierop A, Scheckenbach K, et al. Reliable detection of p53 aberrations in squamous cell carcinomas of the head and neck requires transcript analysis of the entire coding region. Head Neck 2002;24:868-73. (Pubitemid 34913258)
6. Muller PA, Vousden KH, Norman JC. p53 and its mutants in tumor cell migration and invasion. J Cell Biol 2011;192:209-18.
7. Poeta ML, Manola J, Goldwasser MA, Forastiere A, Benoit N, Califano JA, et al. TP53 mutations and survival in squamous-cell carcinoma of the head and neck. N Engl J Med 2007;357:2552-61. (Pubitemid 350294222)
8. Skinner HD, Sandulache VC, Ow TJ, Meyn RE, Yordy JS, Beadle BM, et al. TP53 disruptive mutations lead to head and neck cancer treatment failure through inhibition of radiation-induced senescence. Clin Cancer Res 2012;18:290 -300.
9. Xu C, Wang P, Liu Y, Zhang Y, Fan W, Upton MP, et al. Integrative genomics in combination with RNA interference identifies prognostic and functionally relevant gene targets for oral squamous cell carcinoma. PLoS Genet 2013;9:e1003169.
10. Bailey SL, Gurley KE, Hoon-Kim K, Kelly-Spratt KS, Kemp CJ. Tumor suppression by p53 in the absence of Atm. Mol Cancer Res 2008;6:1185-92.
11. Kelly-Spratt KS, Gurley KE, Yasui Y, Kemp CJ. p19Arf suppresses growth, progression, and metastasis of Hras-driven carcinomas through p53-dependent and -independent pathways. PLoS Biol 2004;2:E242.
12. Kemp CJ, Donehower LA, Bradley A, Balmain A. Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumors. Cell 1993;74:813-22. (Pubitemid 23270601)
13. Kemp CJ, Vo K, Gurley KE. Resistance to skin tumorigenesis in DNAPK-deficient SCID mice is not due to immunode ficiency but results from hypersensitivity to TPA-induced apoptosis. Carcinogenesis 1999;20:2051-6. (Pubitemid 29535304)
14. Zhao M, Sano D, Pickering CR, Jasser SA, Henderson YC, Clayman GL, et al. Assembly and initial characterization of a panel of 85 genomically validated cell lines from diverse head and neck tumor sites. Clin Cancer Res 2011;17:7248-64.
15. Ise K, Nakamura K, Nakao K, Shimizu S, Harada H, Ichise T, et al. Targeted deletion of the H-ras gene decreases tumor formation in mouse skin carcinogenesis. Oncogene 2000;19:2951-6. (Pubitemid 30389085)
16. Kemp CJ. Multistep skin cancer in mice as a model to study the evolution of cancer cells. Semin Cancer Biol 2005;15:460-73. (Pubitemid 41318046)
17. Ku TK, Nguyen DC, Karaman M, Gill P, Hacia JG, Crowe DL. Loss of p53 expression correlates with metastatic phenotype and transcriptional profile in a new mouse model of head and neck cancer. Mol Cancer Res 2007;5:351-62. (Pubitemid 46706997)
18. Ruddell A, Kelly-Spratt KS, Furuya M, Parghi SS, Kemp CJ. p19/Arf and p53 suppress sentinel lymph node lymphangiogenesis and carcinoma metastasis. Oncogene 2008;27:3145-55. (Pubitemid 351693168)
19. Wang YV, Leblanc M, Wade M, Jochemsen AG, Wahl GM. Increased radioresistance and accelerated B-cell lymphomas in mice with Mdmx mutations that prevent modifications by DNA damage-activated kinases. Cancer Cell 2009;16:33-43.
20. Kiyono T, Foster SA, Koop JI, McDougall JK, Galloway DA, Klingelhutz AJ. Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 1998;396:84-8. (Pubitemid 28520454)
21. Toyoshima M, Howie HL, Imakura M, Walsh RM, Annis JE, Chang AN, et al. Functional genomics identifies therapeutic targets for MYC-driven cancer. Proc Natl Acad Sci U S A 2012;109:9545-50.
22. Zhang JH, Chung TD, Oldenburg KR. A simple statistical parameter for use in evaluation and validation of high-throughput screening assays. J Biomol Screen 1999;4:67-73. (Pubitemid 29278954)
23. Birmingham A, Selfors LM, Forster T, Wrobel D, Kennedy CJ, Shanks E, et al. Statistical methods for analysis of high-throughput RNA interference screens. Nat Methods 2009;6:569-75.
24. Aarts M, Sharpe R, Garcia-Murillas I, Gevensleben H, Hurd MS, Shumway SD, et al. Forced mitotic entry of S-phase cells as a therapeutic strategy induced by inhibition of WEE1. Cancer Discov 2012;2:524-39.
25. Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M, et al. Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 2003;21:635-7. (Pubitemid 36638089)
26. Garnett MJ, Edelman EJ, Heidorn SJ, Greenman CD, Dastur A, Lau KW, et al. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 2012;483:570-5.
27. Palmer BD, Thompson AM, Booth RJ, Dobrusin EM, Kraker AJ, Lee HH, et al. 4-Phenylpyrrolo[3,4-c]carbazole-1,3(2H,6H)-dione inhibitors of the checkpoint kinase Wee1. Structure-activity relationships for chromophore modification and phenyl ring substitution. J Med Chem 2006;49:4896-911. (Pubitemid 44201048)
28. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 2011;39:D945-50.
29. Hirai H, Iwasawa Y, Okada M, Arai T, Nishibata T, Kobayashi M, et al. Small-molecule inhibition of Wee1 kinase by MK-1775 selectively sensitizes p53-deficient tumor cells to DNA-damaging agents. Mol Cancer Ther 2009;8:2992-3000.
30. Bridges KA, Hirai H, Buser CA, Brooks C, Liu H, Buchholz TA, et al. MK-1775, a novel Wee1 kinase inhibitor, radiosensitizes p53-defective human tumor cells. Clin Cancer Res 2011;17:5638-48.
31. Rajeshkumar NV, De Oliveira E, Ottenhof N, Watters J, Brooks D, Demuth T, et al. MK-1775, a potent Wee1 inhibitor, synergizes with gemcitabine to achieve tumor regressions, selectively in p53-deficient pancreatic cancer xenografts. Clin Cancer Res 2011;17:2799-806.
32. De Witt Hamer PC, Mir SE, Noske D, Van Noorden CJ, Wurdinger T. WEE1 kinase targeting combined with DNA-damaging cancer therapy catalyzes mitotic catastrophe. Clin Cancer Res 2011;17:4200-7.
33. Hirai H, Arai T, Okada M, Nishibata T, Kobayashi M, Sakai N, et al. MK-1775, a small-molecule Wee1 inhibitor, enhances anti-tumor efficacy of various DNA-damaging agents, including 5-fluorouracil. Cancer Biol Ther 2010;9:514-22.
34. Xu C, Liu Y, Wang P, Fan W, Rue TC, Upton MP, et al. Integrative analysis of DNA copy number and gene expression in metastatic oral squamous cell carcinoma identifies genes associated with poor survival. Mol Cancer 2010;9:143.
35. Dar AA, Goff LW, Majid S, Berlin J, El-Rifai W. Aurora kinase inhibitors-rising stars in cancer therapeutics? Mol Cancer Ther 2010;9:268-78.
36. Katayama H, Sen S. Aurora kinase inhibitors as anticancer molecules. Biochim Biophys Acta 2010;1799:829-39.
37. Ma CX, Janetka JW, Piwnica-Worms H. Death by releasing the breaks: CHK1 inhibitors as cancer therapeutics. Trends Mol Med 2011;17:88-96.
38. Doles J, Hemann MT. Nek4 status differentially alters sensitivity to distinct microtubule poisons. Cancer Res 2010;70:1033-41.
39. Moniz L, Dutt P, Haider N, Stambolic V. Nek family of kinases in cell cycle, checkpoint control, and cancer. Cell Div 2011;6:18.
40. Nguyen CL, Possemato R, Bauerlein EL, Xie A, Scully R, Hahn WC. Nek4 regulates entry into replicative senescence and the response to DNA damage in human fi broblasts. Mol Cell Biol 2012;32:3963-77.
41. Xi S, Zhang Q, Dyer KF, Lerner EC, Smithgall TE, Gooding WE, et al. Src kinases mediate STAT growth pathways in squamous cell carcinoma of the head and neck. J Biol Chem 2003;278:31574-83. (Pubitemid 37048335)
42. Debnath J, Chamorro M, Czar MJ, Schaeffer EM, Lenardo MJ, Varmus HE, et al. rlk/TXK encodes two forms of a novel cysteine string tyrosine kinase activated by Src family kinases. Mol Cell Biol 1999;19:1498-507. (Pubitemid 29046891)
43. Mano H, Yamashita Y, Miyazato A, Miura Y, Ozawa K. Tec protein-tyrosine kinase is an effector molecule of Lyn protein-tyrosine kinase. FASEB J 1996;10:637-42.
44. Wheeler SE, Morariu EM, Bednash JS, Otte CG, Seethala RR, Chiosea SI, et al. Lyn kinase mediates cell motility and tumor growth in EGFRvIII-expressing head and neck cancer. Clin Cancer Res 2012;18:2850-60.
45. Zhang Q, Thomas SM, Xi S, Smithgall TE, Siegfried JM, Kamens J, et al. SRC family kinases mediate epidermal growth factor receptor ligand cleavage, proliferation, and invasion of head and neck cancer cells. Cancer Res 2004;64:6166-73. (Pubitemid 39129418)
46. Matsumoto T, Jiang J, Kiguchi K, Ruffino L, Carbajal S, Beltran L, et al. Targeted expression of c-Src in epidermal basal cells leads to enhanced skin tumor promotion, malignant progression, and metastasis. Cancer Res 2003;63:4819-28. (Pubitemid 37022612)
47. McLean GW, Carragher NO, Avizienyte E, Evans J, Brunton VG, Frame MC. The role of focal-adhesion kinase in cancer - a new therapeutic opportunity. Nat Rev Cancer 2005;5:505-15. (Pubitemid 40942827)
48. Agochiya M, Brunton VG, Owens DW, Parkinson EK, Paraskeva C, Keith WN, et al. Increased dosage and amplification of the focal adhesion kinase gene in human cancer cells. Oncogene 1999;18:5646-53. (Pubitemid 29497599)
49. Egloff AM, Grandis JR. Targeting epidermal growth factor receptor and SRC pathways in head and neck cancer. Semin Oncol 2008;35:286-97. (Pubitemid 351787698)
50. Stabile LP, He G, Lui VW, Henry C, Gubish CT, Joyce S, et al. c-Src activation mediates erlotinib resistance in head and neck cancer by stimulating c-Met. Clin Cancer Res 2013;19:380-92.