Inactivation or loss of TTP promotes invasion in head and neck cancer via transcript stabilization and secretion of MMP9, MMP2, and IL-6

Clinical Cancer Research

Volumn 19, Issue 5, 2013, Pages 1169-1179

  Van Tubergen, Elizabeth A ^a   Banerjee, Rajat ^a   Liu, Min ^a   Broek, Robert Vander ^a   Light, Emily ^b   Kuo, Shiuhyang ^a,c   Feinberg, Stephen E ^a,c   Willis, Amanda L ^c   Wolf, Gregory ^c   Carey, Thomas ^c   Bradford, Carol ^c   Prince, Mark ^c   Worden, Francis P ^c   Kirkwood, Keith L ^d   D'Silva, Nisha J ^a,c  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE A; GELATINASE B; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; RAP1 PROTEIN; TRISTETRAPROLIN;

3' UNTRANSLATED REGION; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CHORIOALLANTOIS; CONTROLLED STUDY; DOWN REGULATION; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; HEAD AND NECK CANCER; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROGNOSIS; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TISSUE MICROARRAY; UPREGULATION; WESTERN BLOTTING;

3' UNTRANSLATED REGIONS; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL MOVEMENT; CELL PROLIFERATION; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; HEAD AND NECK NEOPLASMS; HUMANS; IMMUNOPRECIPITATION; INTERLEUKIN-6; LUCIFERASES; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; NEOPLASM INVASIVENESS; NEOPLASM STAGING; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RAP1 GTP-BINDING PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING; TISSUE ARRAY ANALYSIS; TRISTETRAPROLIN; TUMOR CELLS, CULTURED;

EID: 84874867857     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-2927     Document Type: Article

References (45)

1. Leemans CR, Braakhuis BJ, Brakenhoff RH. The molecular biology of head and neck cancer. Nat Rev Cancer 2011;11: 9-22.
2. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010;60: 277-300.
3. Badache A, Hynes NE. Interleukin 6 inhibits proliferation and, in cooperation with an epidermal growth factor receptor autocrine loop, increases migration of T47D breast cancer cells. Cancer Res 2001;61: 383-91.
4. Kanazawa T, Nishino H, Hasegawa M, Ohta Y, Iino Y, Ichimura K, et al. Interleukin-6 directly influences proliferation and invasion potential of head and neck cancer cells. Eur Arch Otorhinolaryngol 2007;264: 815-21.
5. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144: 646-74.
6. Rundhaug JE. Matrix metalloproteinases, angiogenesis, and cancer: commentary re: A. C. Lockhart et al., Reduction of wound angiogenesis in patients treated with BMS-275291, a broad spectrum matrix metalloproteinase inhibitor. Clin Cancer Res 2003;9: 551-4.
7. Sharafinski ME, Ferris RL, Ferrone S, Grandis Jr. Epidermal growth factor receptor targeted therapy of squamous cell carcinoma of the head and neck. Head Neck 2010;32: 1412-21.
8. Sanduja S, Blanco FF, Dixon DA. The roles of TTP and BRF proteins in regulated mRNA decay. Wiley Interdiscip Rev RNA 2011;2: 42-57.
9. Carballo E, Lai WS, Blackshear PJ. Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA deadenylation and stability. Blood 2000; 95: 1891-9.
10. Taylor GA, Lai WS, Oakey RJ, Seldin MF, Shows TB, Eddy RL Jr, et al. The human TTP protein: sequence, alignment with related proteins, and chromosomal localization of the mouse and human genes. Nucleic Acids Res 1991;19: 3454.
11. Van Tubergen E, Vander Broek R, Lee J, Wolf G, Carey T, Bradford C, et al. Tristetraprolin regulates interleukin-6, which is correlated with tumor progression in patients with head and neck squamous cell carcinoma. Cancer 2011;117: 2677-89.
12. Stoecklin G, Stubbs T, Kedersha N, Wax S, Rigby WF, Blackwell TK, et al. MK2-induced tristetraprolin: 14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J 2004;23: 1313-24.
13. Rowe RG, Weiss SJ. Breaching the basement membrane: who, when and how? Trends Cell Biol 2008;18: 560-74.
14. Mitra RS, Goto M, Lee JS, Maldonado D, Taylor JM, Pan Q, et al. Rap1GAP promotes invasion via induction of matrix metalloproteinase 9 secretion, which is associated with poor survival in low N-stage squamous cell carcinoma. Cancer Res 2008;68: 3959-69.
15. Kumar B, Cordell KG, Lee JS, Worden FP, Prince ME, Tran HH, et al. EGFR, p16, HPV Titer, Bcl-xL and p53, sex, and smoking as indicators of response to therapy and survival in oropharyngeal cancer. J Clin Oncol 2008;26: 3128-37.
16. Worden FP, Kumar B, Lee JS, Wolf GT, Cordell KG, Taylor JM, et al. Chemoselection as a strategy for organ preservation in advanced oropharynx cancer: response and survival positively associated with HPV16 copy number. J Clin Oncol 2008;26: 3138-46.
17. Mitra RS, Zhang Z, Henson BS, Kurnit DM, Carey TE, D'Silva NJ. Rap1A and rap1B ras-family proteins are prominently expressed in the nucleus of squamous carcinomas: nuclear translocation of GTPbound active form. Oncogene 2003;22: 6243-56.
18. Izumi K, Terashi H, Marcelo CL, Feinberg SE. Development and characterization of a tissue-engineered human oral mucosa equivalent produced in a serum-free culture system. J Dent Res 2000;79: 798-805.
19. Ota I, Li XY, Hu Y, Weiss SJ. Induction of a MT1-MMP and MT2-MMPdependent basement membrane transmigration program in cancer cells by Snail1. Proc Natl Acad Sci U S A 2009;106: 20318-23.
20. Matschke K, Da Silva-Azevedo L, Hlushchuk R, Djonov V, Baum O. Annexins as cell-type-specific markers in the developing chicken chorionallantoic membrane. Cell Tissue Res 2006;323: 395-404.
21. Sabeh F, Ota I, Holmbeck K, Birkedal-Hansen H, Soloway P, Balbin M, et al. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J Cell Biol 2004; 167: 769-81.
22. Hagedorn M, Javerzat S, Gilges D, Meyre A, de Lafarge B, Eichmann A, et al. Accessing key steps of human tumor progression in vivo by using an avian embryo model. Proc Natl Acad Sci U S A 2005;102: 1643-8.
23. Zhao W, Liu M, D'Silva NJ, Kirkwood KL. Tristetraprolin regulates interleukin-6 expression through p38 MAPK-dependent affinity changes with mRNA 30 untranslated region. J Interferon Cytokine Res 2011;31: 629-37.
24. Palanisamy V, Jakymiw A, Van Tubergen EA, D'Silva NJ, Kirkwood KL. Control of cytokine mRNA expression by RNA-binding proteins and microRNAs. J Dent Res 2012;91: 651-8.
25. Banerjee R, Henson BS, Russo N, Tsodikov A, D'Silva NJ. Rap1 mediates galanin receptor 2-induced proliferation and survival in squamous cell carcinoma. Cell Signal 2011;23: 1110-8.
26. Banerjee R, Mani RS, Russo N, Scanlon CS, Tsodikov A, Jing X, et al. The tumor suppressor gene rap1GAP is silenced by miR-101-mediated EZH2 overexpression in invasive squamous cell carcinoma. Oncogene 2011;30: 4339-49.
27. Clement SL, Scheckel C, Stoecklin G, Lykke-Andersen J. Phosphorylation of tristetraprolin byMK2 impairs AU-rich elementmRNA decay by preventing deadenylase recruitment. Mol Cell Biol 2011; 31: 256-66.
28. Kumar S, Jiang MS, Adams JL, Lee JC. Pyridinylimidazole compound SB 203580 inhibits the activity but not the activation of p38 mitogenactivated protein kinase. Biochem Biophys Res Commun 1999;263: 825-31.
29. Lee JC, Laydon JT, McDonnell PC, Gallagher TF, Kumar S, Green D, et al. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 1994;372: 739-46.
30. Anand P, Shenoy R, Palmer JE, Baines AJ, Lai RY, Robertson J, et al. Clinical trial of the p38 MAPkinase inhibitor dilmapimod in neuropathic pain following nerve injury. Eur J Pain 2011;15: 1040-8.
31. Kakuguchi W, Kitamura T, Kuroshima T, Ishikawa M, Kitagawa Y, Totsuka Y, et al. HuR knockdown changes the oncogenic potential of oral cancer cells. Mol Cancer Res 2010;8: 520-8.
32. Xu N, Chen CY, Shyu AB. Versatile role for hnRNP D isoforms in the differential regulation of cytoplasmic mRNA turnover. Mol Cell Biol 2001;21: 6960-71.
33. Zhang L, Lee JE, Wilusz J, Wilusz CJ. The RNA-binding protein CUGBP1 regulates stability of tumor necrosis factor mRNA in muscle cells: implications for myotonic dystrophy. J Biol Chem 2008;283: 22457-63.
34. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002;295: 2387-92.
35. Al-Souhibani N, Al-Ahmadi W, Hesketh JE, Blackshear PJ, Khabar KS. The RNA-binding zinc-finger protein tristetraprolin regulates AU-rich mRNAs involved in breast cancer-related processes. Oncogene 2010; 29: 4205-15.
36. Suswam E, Li Y, Zhang X, Gillespie GY, Li X, Shacka JJ, et al. Tristetraprolin down-regulates interleukin-8 and vascular endothelial growth factor in malignant glioma cells. Cancer Res 2008;68: 674-82.
37. Carballo E, Blackshear PJ. Roles of tumor necrosis factor-alpha receptor subtypes in the pathogenesis of the tristetraprolin-deficiency syndrome. Blood 2001;98: 2389-95.
38. Al Ghouleh I, Magder S. NADPH oxidase-derived superoxide destabilizes LPS-induced interleukin-8 mRNAvia p38, Erk1/2MAPKand the destabilizing factor tristetraprolin1. Shock 2012;37: 433-40.
39. Zhang Z, Mitra RS, Henson BS, Datta NS, McCauley LK, Kumar P, et al. Rap1GAP inhibits tumor growth in oropharyngeal squamous cell carcinoma. Am J Pathol 2006;168: 585-96.
40. Scanlon CS, Van Tubergen EA, Inglehart RC, D'Silva NJ. Biomarkers of epithelial-mesenchymal transition in squamous cell carcinoma. J Dent Res 2013;92: 114-21
41. Lokman NA, Elder AS, Ricciardelli C, Oehler MK. Chick chorioallantoic membrane (CAM) assay as an in vivo model to study the effect of newly identified molecules on ovarian cancer invasion and metastasis. Int J Mol Sci 2012;13: 9959-70.
42. Rowe SL, Stegemann JP. Microstructure and mechanics of collagenfibrin matrices polymerized using ancrod snake venom enzyme. J Biomech Eng 2009;131: 061012.
43. Brennan SE, Kuwano Y, Alkharouf N, Blackshear PJ, Gorospe M, Wilson GM. The mRNA-destabilizing protein tristetraprolin is suppressed in many cancers, altering tumorigenic phenotypes and patient prognosis. Cancer Res 2009;69: 5168-76.
44. Lee HH, Son YJ, Lee WH, Park YW, Chae SW, Cho WJ, et al. Tristetraprolin regulates expression of VEGF and tumorigenesis in human colon cancer. Int J Cancer 2010;126: 1817-27.
45. Griseri P, Bourcier C, Hieblot C, Essafi-Benkhadir K, Chamorey E, Touriol C, et al. A synonymous polymorphism of the Tristetraprolin (TTP) gene, an AU-rich mRNA-binding protein, affects translation efficiency and response to Herceptin treatment in breast cancer patients. Hum Mol Genet 2011;20: 4556-68.