Hedgehog signaling drives radioresistance and stroma-driven tumor repopulation in head and neck squamous cancers

Cancer Research

Volumn 74, Issue 23, 2014, Pages 7024-7036

  Gan, Gregory N ^a   Eagles, Justin ^a   Keysar, Stephen B ^a   Wang, Guoliang ^a   Glogowska, Magdalena J ^a   Altunbas, Cem ^a   Anderson, Ryan T ^a   Le, Phuong N ^a   Morton, J Jason ^a   Frederick, Barbara ^a   Raben, David ^a   Wang, Xiao Jing ^a   Jimeno, Antonio ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPAMINE; MAMMALIAN TARGET OF RAPAMYCIN; S6 KINASE; S6 KINASE 1; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; UNCLASSIFIED DRUG; GLI1 PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; RIBOSOMAL PROTEIN S6 KINASE, 70KD, POLYPEPTIDE 1; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR; VERATRUM ALKALOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER RADIOTHERAPY; CELL SURVIVAL; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE; GENE EXPRESSION REGULATION; GENE REPRESSION; GLI1 GENE; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; SNAI1 GENE; TUMOR GROWTH; TUMOR VOLUME; UPREGULATION; ZEB2 GENE; ANIMAL; CARCINOMA, SQUAMOUS CELL; DRUG EFFECTS; HEAD AND NECK NEOPLASMS; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; RADIATION DOSE; STROMA CELL; TUMOR CELL LINE;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; HEAD AND NECK NEOPLASMS; HEDGEHOG PROTEINS; HUMANS; MICE; MICE, NUDE; RADIATION TOLERANCE; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; STROMAL CELLS; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; UP-REGULATION; VERATRUM ALKALOIDS;

EID: 84918582219     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-1346     Document Type: Article

References (43)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63:11-30.
2. Hall E, Giaccia A. Radiobiology for the Radiologist. 7th ed. Philadelphia, PA: Lippincott Williams and Wilkins; 2012.
3. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009;9:265-73.
4. Ohta H, Aoyagi K, Fukaya M, Danjoh I, Ohta A, Isohata N, et al. Cross talk between hedgehog and epithelial-mesenchymal transition pathways in gastric pit cells and in diffuse-type gastric cancers. Br J Cancer 2009;100:389-98.
5. Isohata N, Aoyagi K, Mabuchi T, Daiko H, Fukaya M, Ohta H, et al. Hedgehog and epithelial-mesenchymal transition signaling in normal and malignant epithelial cells of the esophagus. Int J Cancer 2009;125:1212-21.
6. Wang Y, Ding Q, Yen CJ, Xia W, Izzo JG, Lang JY, et al. The crosstalk of mTOR/S6K1 and Hedgehog pathways. Cancer Cell 2012;21:374-87.
7. Kawamoto A, Yokoe T, Tanaka K, Saigusa S, Toiyama Y, Yasuda H, et al. Radiation induces epithelial-mesenchymal transition in colorectal cancer cells. Oncol Rep 2012;27:51-7.
8. Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY, et al. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 2009;27:2059-68.
9. Tsukamoto H, Shibata K, Kajiyama H, Terauchi M, Nawa A, Kikkawa F. Irradiation-induced epithelial-mesenchymal transition (EMT) related to invasive potential in endometrial carcinoma cells. Gynecol Oncol 2007;107:500-4.
10. Chung CH, Dignam JJ, Hammond ME, Klimowicz AC, Petrillo SK, Magliocco A, et al. Glioma-associated oncogene family zinc finger 1 expression and metastasis in patients with head and neck squamous cell carcinoma treated with radiation therapy (RTOG 9003). J Clin Oncol 2011;29:1326-34.
11. Keysar SB, Le PN, Anderson RT, Morton JJ, Bowles DW, Paylor JJ, et al. Hedgehog signaling alters reliance on EGF receptor signaling and mediates anti-EGFR therapeutic resistance in head and neck cancer. Cancer Res 2013;73:3381-92.
12. Jimeno A, Kulesza P, Kincaid E, Bouaroud N, Chan A, Forastiere A, et al. C-fos assessment as a marker of anti-epidermal growth factor receptor effect. Cancer Res 2006;66:2385-90.
13. Yonesaka K, Zejnullahu K, Lindeman N, Homes AJ, Jackman DM, Zhao F, et al. Autocrine production of amphiregulin predicts sensitivity to both gefitinib and cetuximab in EGFRwild-type cancers. Clin Cancer Res 2008;14:6963-73.
14. Amador ML, Oppenheimer D, Perea S, Maitra A, Cusatis G, Iacobuzio-Donahue C, et al. An epidermal growth factor receptor intron 1 polymorphism mediates response to epidermal growth factor receptor inhibitors. Cancer Res 2004;64:9139-43.
15. Frederick MJ, Holton PR, Hudson M, Wang M, Clayman GL. Expression of apoptosis-related genes in human head and neck squamous cell carcinomas undergoing p53-mediated programmed cell death. Clin Cancer Res 1999;5:361-9.
16. Frederick BA, Helfrich BA, Coldren CD, Zheng D, Chan D, Bunn PA Jr, et al. Epithelial to mesenchymal transition predicts gefitinib resistance in cell lines of head and neck squamous cell carcinoma and non-small cell lung carcinoma. Mol Cancer Ther 2007;6:1683-91.
17. Rangan SR. A new human cell line (FaDu) from a hypopharyngeal carcinoma. Cancer 1972;29:117-21.
18. Keysar SB, Astling DP, Anderson RT, Vogler BW, Bowles DW, Morton JJ, et al. A patient tumor transplant model of squamous cell cancer identifies PI3K inhibitors as candidate therapeutics in defined molecular bins. Mol Oncol 2013;7:776-90.
19. 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.
20. Huntzicker EG, Estay IS, Zhen H, Lokteva LA, Jackson PK, Oro AE. Dual degradation signals control Gli protein stability and tumor formation. Genes Dev 2006;20:276-81.
21. Ma J, Tian L, Cheng J, Chen Z, Xu B, Wang L, et al. Sonic hedgehog signaling pathway supports cancer cell growth during cancer radiotherapy. PLoS ONE 2013;8:e65032.
22. Feldmann G, Dhara S, Fendrich V, Bedja D, Beaty R, Mullendore M, et al. Blockade of hedgehog signaling inhibits pancreatic cancer invasion and metastases: a new paradigm for combination therapy in solid cancers. Cancer Res 2007;67:2187-96.
23. Sims-Mourtada J, Izzo JG, Apisarnthanarax S, Wu TT, Malhotra U, Luthra R, et al. Hedgehog: an attribute to tumor regrowth after chemoradiotherapy and a target to improve radiation response. Clin Cancer Res 2006;12:6565-72.
24. 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.
25. Cooper JS, Pajak TF, Forastiere AA, Jacobs J, Campbell BH, Saxman SB, et al. Postoperative concurrent radiotherapy and chemotherapy for high-risk squamous-cell carcinoma of the head and neck. N Engl J Med 2004;350:1937-44.
26. Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 2012;22:725-36.
27. Zeng J, Aziz K, Chettiar ST, Aftab BT, Armour M, Gajula R, et al. Hedgehog pathway inhibition radiosensitizes non-small cell lung cancers. Int J Radiat Oncol Biol Phys 2013;86:143-9.
28. Deng Y, Zhou J, Fang L, Cai Y, Ke J, Xie X, et al. ALDH1 is an independent prognostic factor for patients with stages II-III rectal cancer after receiving radiochemotherapy. Br J Cancer 2014;110:430-4.
29. Huang CF, Xu XR, Wu TF, Sun ZJ, Zhang WF. Correlation of ALDH1, CD44, OCT4 and SOX2 in tongue squamous cell carcinoma and their association with disease progression and prognosis. J Oral Pathol Med 2014;43:492-8.
30. Kim YH, Kim G, Kwon CI, Kim JW, Park PW, Hahm KB. TWIST1 and SNAI1 as markers of poor prognosis in human colorectal cancer are associated with the expression of ALDH1 and TGF-beta1. Oncol Rep 2014;31:1380-8.
31. Fingas CD, Bronk SF, Werneburg NW, Mott JL, Guicciardi ME, Cazanave SC, et al. Myofibroblast-derived PDGF-BB promotes Hedgehog survival signaling in cholangiocarcinoma cells. Hepatology 2011;54:2076-88.
32. Harris LG, Pannell LK, Singh S, Samant RS, Shevde LA. Increased vascularity and spontaneous metastasis of breast cancer by hedgehog signaling mediated upregulation of cyr61. Oncogene 2012;31:3370-80.
33. Mills LD, Zhang Y, Marler RJ, Herreros-Villanueva M, Zhang L, Almada LL, et al. Loss of the transcription factor GLI1 identifies a signaling network in the tumor microenvironment mediating KRAS-induced transformation. J Biol Chem 2013;288:11786-94.
34. Levina E, Chen M, Carkner R, Shtutman M, Buttyan R. Paracrine Hedgehog increases the steroidogenic potential of prostate stromal cells in a Gli-dependent manner. Prostate 2012;72:817-24.
35. Walter K, Omura N, Hong SM, Griffith M, Vincent A, Borges M, et al. Overexpression of smoothened activates the sonic hedgehog signaling pathway in pancreatic cancer-associated fibroblasts. Clin Cancer Res 2010;16:1781-9.
36. Choe C, Shin YS, Kim SH, Jeon MJ, Choi SJ, Lee J, et al. Tumorstromal interactions with direct cell contacts enhance motility of nonsmall cell lung cancer cells through the hedgehog signaling pathway. Anticancer Res 2013;33:3715-23.
37. Hwang RF, Moore TT, Hattersley MM, Scarpitti M, Yang B, Devereaux E, et al. Inhibition of the hedgehog pathway targets the tumorassociated stroma in pancreatic cancer. Mol Cancer Res 2012;10:1147-57.
38. Sun Y, Campisi J, Higano C, Beer TM, Porter P, Coleman I, et al. Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat Med 2012;18:1359-68.
39. Pickhard AC, Margraf J, Knopf A, Stark T, Piontek G, Beck C, et al. Inhibition of radiation induced migration of human head and neck squamous cell carcinoma cells by blocking of EGF receptor pathways. BMC Cancer 2011;11:388.
40. Boehme KA, Kulikov R, Blattner C. p53 stabilization in response to DNA damage requires Akt/PKB and DNA-PK. Proc Natl Acad SciUS A 2008;105:7785-90.
41. Liu J, Kuo WL, Seiwert TY, Lingen M, Ciaccio MF, Jones RB, et al. Effect of complementary pathway blockade on efficacy of combination enzastaurin and rapamycin. Head Neck 2011;33:1774-82.
42. Fury MG, Lee NY, Sherman E, Ho AL, Rao S, Heguy A, et al. A phase 1 study of everolimus +weekly cisplatin +intensity modulated radiation therapy in head-and-neck cancer. Int J Radiat Oncol Biol Phys 2013;87:479-86.
43. Fury MG, Sherman E, Ho AL, Xiao H, Tsai F, Nwankwo O, et al. A phase 1 study of everolimus plus docetaxel plus cisplatin as induction chemotherapy for patients with locally and/or regionally advanced head and neck cancer. Cancer 2013;119:1823-31.