Ableson kinases negatively regulate invadopodia function and invasion in head and neck squamous cell carcinoma by inhibiting an HB-EGF autocrine loop

Oncogene

Volumn 32, Issue 40, 2013, Pages 4766-4777

  Hayes, K E ^a   Walk, E L ^a   Ammer, A G ^a   Kelley, L C ^b   Martin, K H ^a   Weed, S A ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

abl; cortactin; head and neck cancer; imatinib mesylate; invadopodia; invasion

Indexed keywords

ABELSON KINASE; COLLAGEN; CORTACTIN; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; IMATINIB; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; CELL INVASION; CELL STIMULATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME ACTIVITY; FIBROBLAST; HEAD AND NECK SQUAMOUS CELL CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TUMOR CELL; TUMOR INVASION;

ANTINEOPLASTIC AGENTS; BENZAMIDES; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; EXTRACELLULAR MATRIX; HEAD AND NECK NEOPLASMS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOPLASM INVASIVENESS; PIPERAZINES; PROTEIN KINASES; PYRIMIDINES; SRC-FAMILY KINASES;

EID: 84885181020     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.513     Document Type: Article

References (87)

1. Pryor DI, Solomon B, Porceddu SV. The emerging era of personalized therapy in squamous cell carcinoma of the head and neck. Asia Pac J Clin Oncol 2011; 7: 236-251.
2. Leemans CR, Braakhuis BJ, Brakenhoff RH. The molecular biology of head and neck cancer. Nat Rev Cancer 2011; 11: 9-22.
3. Kalyankrishna S, Grandis JR. Epidermal growth factor receptor biology in head and neck cancer. J Clin Oncol 2006; 24: 2666-2672.
4. Hama T, Yuza Y, Saito Y, O-uchi J, Kondo S, Okabe M et al. Prognostic significance of epidermal growth factor receptor phosphorylation and mutation in head and neck squamous cell carcinoma. Oncologist 2009; 14: 900-908.
5. Hama T, Yuza Y, Suda T, Saito Y, Norizoe C, Kato T et al. Functional mutation analysis of EGFR family genes and corresponding lymph node metastases in head and neck squamous cell carcinoma. Clin Exp Metastasis 2012; 29: 19-25.
6. Uribe P, Gonzalez S. Epidermal growth factor receptor (EGFR) and squamous cell carcinoma of the skin: Molecular bases for EGFR-targeted therapy. Pathology-Research and Practice 20116/15 207: 337-342.
7. Fung C, Grandis JR. Emerging drugs to treat squamous cell carcinomas of the head and neck. Expert Opin Emerg Drugs 2010; 15: 355-373.
8. Neiva KG, Zhang Z, Miyazawa M, Warner KA, Karl E, Nor JE. Cross talk initiated by endothelial cells enhances migration and inhibits anoikis of squamous cell carcinoma cells through STAT3/Akt/ERK signaling. Neoplasia 2009; 11: 583-593.
9. Koppikar P, Choi SH, Egloff AM, Cai Q, Suzuki S, Freilino M et al. Combined inhibition of c-Src and epidermal growth factor receptor abrogates growth and invasion of head and neck squamous cell carcinoma. Clin Cancer Res 2008; 14: 4284-4291.
10. Yang JL, Qu XJ, Russell PJ, Goldstein D. Interferon-alpha promotes the anti-proliferative effect of Erlotinib (OSI-774) on human colon cancer cell lines. Cancer Lett 2005; 225: 61-74.
11. Huang YT, Hwang JJ, Lee LT, Liebow C, Lee PP, Ke FC et al. Inhibitory effects of a luteinizing hormone-releasing hormone agonist on basal and epidermal growth factor-induced cell proliferation and metastasis-associated properties in human epidermoid carcinoma A431 cells. Int J Cancer 2002; 99: 505-513.
12. Guarino M. Src signaling in cancer invasion. J Cell Physiol 2010; 223: 14-26.
13. Kim LC, Song L, Haura EB. Src kinases as therapeutic targets for cancer. Nat Rev Clin Oncol 2009; 6: 587-595.
14. Summy JM, Gallick GE. Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev 2003; 22: 337-358.
15. Shor AC, Keschman EA, Lee FY, Muro-Cacho C, Letson GD, Trent JC et al. Dasatinib inhibits migration and invasion in diverse human sarcoma cell lines and induces apoptosis in bone sarcoma cells de pendent on SRC kinase for survival. Cancer Res 2007; 67: 2800-2808.
16. Chen YS, Wu MJ, Huang CY, Lin SC, Chuang TH, Yu CC et al. CD133/Src axis mediates tumor initiating property and epithelial-mesenchymal transition of head and neck cancer. PLoS One 2011; 6: E28053.
17. Johnson FM, Saigal B, Talpaz M, Donato NJ. Dasatinib (BMS-354825) tyrosine kinase inhibitor suppresses invasion and induces cell cycle arrest and apoptosis of head and neck squamous cell carcinoma and non-small cell lung cancer cells. Clin Cancer Res 2005; 11(19 Pt 1): 6924-6932.
18. Sen B, Saigal B, Parikh N, Gallick G, Johnson FM. Sustained Src inhibition results in signal transducer and activator of transcription 3 (STAT3) activation and cancer cell survival via altered Janus-activated kinase-STAT3 binding. Cancer Res 2009; 69: 1958-1965.
19. Zhang S, Yu D. Targeting Src family kinases in anti-cancer therapies: Turning promise into triumph. Trends Pharmacol Sci 2012, 333: 122-128.
20. Mayer EL, Krop IE. Advances in targeting SRC in the treatment of breast cancer and other solid malignancies. Clin Cancer Res 2010; 16: 3526-3532.
21. Wheeler DL, Iida M, Kruser TJ, Nechrebecki MM, Dunn EF, Armstrong EA et al. Epidermal growth factor receptor cooperates with Src family kinases in acquired resistance to cetuximab. Cancer Biol Ther 2009; 8: 696-703.
22. Haura EB, Tanvetyanon T, Chiappori A, Williams C, Simon G, Antonia S et al. Phase I/II study of the Src inhibitor dasatinib in combination with erlotinib in advanced non-small-cell lung cancer. J Clin Oncol 2010; 28: 1387-1394.
23. Araujo JC, Mathew P, Armstrong AJ, Braud EL, Posadas E, Lonberg M et al. Dasatinib combined with docetaxel for castration-resistant prostate cancer: Results from a phase 1-2 study. Cancer 2012; 118: 63-71.
24. Murphy DA, Courtneidge SA. The ?ins? and ?outs? of podosomes and invadopodia: Characteristics, formation and function. Nat Rev Mol Cell Biol 2011; 12: 413-426.
25. Linder S, Wiesner C, Himmel M. de grading Devices: Invadosomes in proteolytic cell invasion. Annu Rev Cell Dev Biol 2011; 27: 185-211.
26. Poincloux R, Lizarraga F, Chavrier P. Matrix invasion by tumour cells: A focus on MT1-MMP trafficking to invadopodia. J Cell Sci 2009; 122(Pt 17): 3015-3024.
27. Artym VV, Zhang Y, Seillier-Moiseiwitsch F, Yamada KM, Mueller SC. Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: De fining the stages of invadopodia formation and function. Cancer Res 2006; 66: 3034-3043.
28. Oser M, Yamaguchi H, Mader CC, Bravo-Cordero JJ, Arias M, Chen X et al. Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J Cell Biol 2009; 186: 571-587.
29. de staing O, Block MR, Planus E, Albiges-Rizo C. Invadosome regulation by adhesion signaling. Curr Opin Cell Biol 2011; 23: 597-606.
30. Ren G, Crampton MS, Yap AS. Cortactin: Coordinating adhesion and the actin cytoskeleton at cellular protrusions. Cell Motil Cytoskeleton 2009; 66: 865-873.
31. Buccione R, Caldieri G, Ayala I. Invadopodia: Specialized tumor cell structures for the focal de gradation of the extracellular matrix. Cancer Metastasis Rev 2009; 28: 137-149.
32. Kirkbride KC, Sung BH, Sinha S, Weaver AM. Cortactin: A multifunctional regulator of cellular invasiveness. Cell Adh Migr 2011, Mar-Apr 5: 187-198.
33. Weaver AM, Karginov AV, Kinley AW, Weed SA, Li Y, Parsons JT et al. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol 2001; 11: 370-374.
34. Ammer AG, Weed SA. Cortactin branches out: Roles in regulating protrusive actin dynamics. Cell Motil Cytoskeleton 2008; 65: 687-707.
35. Martinez-Quiles N, Ho HY, Kirschner MW, Ramesh N, Geha RS. Erk/Src phosphorylation of cortactin acts as a switch on-switch off mechanism that controls its ability to activate N-WASP. Mol Cell Biol 2004; 24: 5269-5280.
36. Kelley LC, Ammer AG, Hayes KE, Martin KH, Machida K, Jia L et al. Oncogenic Src requires a wild-type counterpart to regulate invadopodia maturation. J Cell Sci 2010; 123(Pt 22): 3923-3932.
37. Oser M, Mader CC, Gil-Henn H, Magalhaes M, Bravo-Cordero JJ, Koleske AJ et al. Specific tyrosine phosphorylation sites on cortactin regulate Nck1-dependent actin polymerization in invadopodia. J Cell Sci 2010; 123(Pt 21): 3662-3673.
38. Tehrani S, Tomasevic N, Weed S, Sakowicz R, Cooper JA. Src phosphorylation of cortactin enhances actin assembly. Proc Natl Acad Sci USA 2007; 104: 11933-11938.
39. Yamaguchi H, Lorenz M, Kempiak S, Sarmiento C, Coniglio S, Symons M et al. Molecular mechanisms of invadopodium formation: The role of the N-WASP-Arp2/3 complex pathway and cofilin. J Cell Biol 2005; 168: 441-452.
40. Ayala I, Baldassarre M, Giacchetti G, Caldieri G, Tete S, Luini A et al. Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix de gradation. J Cell Sci 2008; 121(Pt 3): 369-378.
41. Webb BA, Jia L, Eves R, Mak AS. Dissecting the functional domain requirements of cortactin in invadopodia formation. Eur J Cell Biol 2007; 86: 189-206.
42. Colicelli J. ABL tyrosine kinases: Evolution of function, regulation, and specificity. Sci Signal 2010; 3: Re6.
43. Bradley WD, Koleske AJ. Regulation of cell migration and morphogenesis by Ablfamily kinases: Emerging mechanisms and physiological contexts. J Cell Sci 2009; 122(Pt 19): 3441-3454.
44. Plattner R, Pendergast AM. Activation and signaling of the Abl tyrosine kinase: Bidirectional link with phosphoinositide signaling. Cell Cycle 2003, Jul-Aug 2: 273-274.
45. Ernst T, Hochhaus A. Chronic myeloid leukemia: Clinical impact of BCR-ABL1 mutations and other lesions associated with disease progression. Semin Oncol 2012; 39: 58-66.
46. Wang Y, Gu M, Mi Y, Qiu L, Bian S, Wang J. Clinical characteristics and outcomes of mixed phenotype acute leukemia with Philadelphia chromosome positive and/or bcr-abl positive in adult. Int J Hematol 2011; 94: 552-555.
47. Srinivasan D, Plattner R. Activation of Abl tyrosine kinases promotes invasion of aggressive breast cancer cells. Cancer Res 2006; 66: 5648-5655.
48. Srinivasan D, Sims JT, Plattner R. Aggressive breast cancer cells are de pendent on activated Abl kinases for proliferation, anchorage-independent growth and survival. Oncogene 2008; 27: 1095-1105.
49. Lin J, Sun T, Ji L, de ng W, Roth J, Minna J et al. Oncogenic activation of c-Abl in non-small cell lung cancer cells lacking FUS1 expression: Inhibition of c-Abl by the tumor suppressor gene product Fus1. Oncogene 2007; 26: 6989-6996.
50. Furlan A, Stagni V, Hussain A, Richelme S, Conti F, Prodosmo A et al. Abl interconnects oncogenic Met and p53 core pathways in cancer cells. Cell Death Differ 2011; 18: 1608-1616.
51. Mader CC, Oser M, Magalhaes MA, Bravo-Cordero JJ, Condeelis J, Koleske AJ et al. An EGFR-Src-Arg-cortactin pathway mediates functional maturation of invadopodia and breast cancer cell invasion. Cancer Res 2011; 71: 1730-1741.
52. Lapetina S, Mader CC, Machida K, Mayer BJ, Koleske AJ. Arg interacts with cortactin to promote adhesion-dependent cell edge protrusion. J Cell Biol 2009; 185: 503-519.
53. Ganguly SS, Fiore LS, Sims JT, Friend JW, Srinivasan D, Thacker MA et al. c-Abl and Arg are activated in human primary melanomas, promote melanoma cell invasion via distinct pathways, and drive metastatic progression. Oncogene 2011; Sep: 5.
54. Plattner R, Kadlec L, de mali KA, Kazlauskas A, Pendergast AM. c-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev 1999; 13: 2400-2411.
55. Smith-Pearson PS, Greuber EK, Yogalingam G, Pendergast AM. Abl kinases are required for invadopodia formation and chemokine-induced invasion. J Biol Chem 2010; 285: 40201-40211.
56. Sibony-Benyamini H, Gil-Henn H. Invadopodia: The leading force. Eur J Cell Biol 2012; 91: 896-901.
57. Tsao AS, Liu S, Fujimoto J, Wistuba II, Lee JJ, Marom EM et al. Phase II trials of imatinib mesylate and docetaxel in patients with metastatic non-small cell lung cancer and head and neck squamous cell carcinoma. J Thorac Oncol 2011; 6: 2104-2111.
58. Clark ES, Whigham AS, Yarbrough WG, Weaver AM. Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix de gradation in invadopodia. Cancer Res 2007; 67: 4227-4235.
59. Blake RA, Broome MA, Liu X, Wu J, Gishizky M, Sun L et al. SU6656, a selective src family kinase inhibitor, used to probe growth factor signaling. Mol Cell Biol 2000; 20: 9018-9027.
60. Johnson FM, Saigal B, Donato NJ. Induction of heparin-binding EGF-like growth factor and activation of EGF receptor in imatinib mesylate-treated squamous carcinoma cells. J Cell Physiol 2005; 205: 218-227.
61. Hennequin LF, Allen J, Breed J, Curwen J, Fennell M, Green TP et al. N-(5-chloro-1,3-benzodioxol-4-yl)-7-[2-(4-methylpiperazin-1-yl)ethoxy] -5-(tetrahydro-2H-pyran-4-yloxy) quinazolin-4-amine, a novel, highly selective, orally available, dual-specific c-Src/Abl kinase inhibitor. J Med Chem 2006; 49: 6465-6488.
62. Summy JM, Gallick GE. Treatment for advanced tumors: SRC reclaims center stage. Clin Cancer Res 2006; 12: 1398-1401.
63. Rothschild BL, Shim AH, Ammer AG, Kelley LC, Irby KB, Head JA et al. Cortactin overexpression regulates actin-related protein 2/3 complex activity, motility, and invasion in carcinomas with chromosome 11q13 amplification. Cancer Res 2006; 66: 8017-8025.
64. Noren NK, Foos G, Hauser CA, Pasquale EB. The EphB4 receptor suppresses breast cancer cell tumorigenicity through an Abl-Crk pathway. Nat Cell Biol 2006; 8: 815-825.
65. Allington TM, Galliher-Beckley AJ, Schiemann WP. Activated Abl kinase inhibits oncogenic transforming growth factor-beta signaling and tumorigenesis in mammary tumors. FASEB J 2009; 23: 4231-4243.
66. Frasca F, Vigneri P, Vella V, Vigneri R, Wang JY. Tyrosine kinase inhibitor STI571 enhances thyroid cancer cell motile response to hepatocyte growth factor. Oncogene 2001; 20: 3845-3856.
67. Huang C, Liu J, Haudenschild CC, Zhan X. The role of tyrosine phosphorylation of cortactin in the locomotion of endothelial cells. J Biol Chem 1998; 273: 25770-25776.
68. Boyle SN, Michaud GA, Schweitzer B, Predki PF, Koleske AJ. A critical role for cortactin phosphorylation by Abl-family kinases in PDGF-induced dorsal-wave formation. Curr Biol 2007; 17: 445-451.
69. Plattner R, Koleske AJ, Kazlauskas A, Pendergast AM. Bidirectional signaling links the Abelson kinases to the platelet-derived growth factor receptor. Mol Cell Biol 2004; 24: 2573-2583.
70. Head JA, Jiang D, Li M, Zorn LJ, Schaefer EM, Parsons JT et al. Cortactin tyrosine phosphorylation requires Rac1 activity and association with the cortical actin cytoskeleton. Mol Biol Cell 2003; 14: 3216-3229.
71. Kelley LC, Hayes KE, Ammer AG, Martin KH, Weed SA. Cortactin phosphorylated by ERK1/2 localizes to sites of dynamic actin regulation and is required for carcinoma lamellipodia persistence. PLoS One 2010; 5: E13847.
72. O-charoenrat P, Modjtahedi H, Rhys-Evans P, Court WJ, Box GM, Eccles SA. Epidermal growth factor-like ligands differentially up-regulate matrix metalloproteinase 9 in head and neck squamous carcinoma cells. Cancer Res 2000; 60: 1121-1128.
73. Ohnishi Y, Inoue H, Furukawa M, Kakudo K, Nozaki M. Heparin-binding epidermal growth factor-like growth factor is a potent regulator of invasion activity in oral squamous cell carcinoma. Oncol Rep 2012; 27: 954-958.
74. Ammer AG, Kelley LC, Hayes KE, Evans JV, Lopez-Skinner LA, Martin KH et al. Saracatinib impairs head and neck squamous cell carcinoma invasion by disrupting invadopodia function. J Cancer Sci Ther 2009; 1: 52-61.
75. Liberatore RA, Goff SP, Nunes I. NF-kappaB activity is constitutively elevated in c-Abl null fibroblasts. Proc Natl Acad Sci USA 2009; 106: 17823-17828.
76. Wang F, Liu R, Lee SW, Sloss CM, Couget J, Cusack JC et al. like growth factor is an early response gene to chemotherapy and contributes to chemotherapy resistance. Oncogene 2007; 26: 2006-2016.
77. Hatakeyama H, Cheng H, Wirth P, Counsell A, Marcrom SR, Wood CB et al. Regulation of heparin-binding EGF-like growth factor by miR-212 and acquired cetuximab-resistance in head and neck squamous cell carcinoma. PLoS One 2010; 5: E12702.
78. Yanagawa T, Harada H, Iwasa S, Tabuchi K, Omura K, Suzuki H et al. c-Abl expression in oral squamous cell carcinomas. Oral Oncol 2000; 36: 89-94.
79. Fury MG, Baxi S, Shen R, Kelly KW, Lipson BL, Carlson D et al. Phase II study of saracatinib (AZD0530) for patients with recurrent or metastatic head and neck squamous cell carcinoma (HNSCC). Anticancer Res 2011; 31: 249-253.
80. Brooks HD, Glisson BS, Bekele BN, Johnson FM, Ginsberg LE, El-Naggar A et al. Phase 2 study of dasatinib in the treatment of head and neck squamous cell carcinoma. Cancer 2011; 117: 2112-2119.
81. Montero JC, Seoane S, Ocana A, Pandiella A. Inhibition of SRC family kinases and receptor tyrosine kinases by dasatinib: Possible combinations in solid tumors. Clin Cancer Res 2011; 17: 5546-5552.
82. Lara Jr PN, Longmate J, Evans CP, Quinn DI, Twardowski P, Chatta G et al. A phase II trial of the Src-kinase inhibitor AZD0530 in patients with advanced castrationresistant prostate cancer: A California Cancer Consortium study. Anticancer Drugs 2009; 20: 179-184.
83. Gucalp A, Sparano JA, Caravelli J, Santamauro J, Patil S, Abbruzzi A et al. Phase II trial of saracatinib (AZD0530), an oral SRC-inhibitor for the treatment of patients with hormone receptor-negative metastatic breast cancer. Clin Breast Cancer 2011; 11: 306-311.
84. Cai L, Makhov AM, Schafer DA, Bear JE. Coronin 1B antagonizes cortactin and remodels Arp2/3-containing actin branches in lamellipodia. Cell 2008; 134: 828-842.
85. Poppe M, Feller SM, Romer G, Wessler S. Phosphorylation of Helicobacter pylori CagA by c-Abl leads to cell motility. Oncogene 2007; 26: 3462-3472.
86. Antoku S, Saksela K, Rivera GM, Mayer BJA crucial role in cell spreading for the interaction of Abl PxxP motifs with Crk and Nck adaptors. J Cell Sci 2008; 121(Pt 18): 3071-3082.
87. Martin KH, Hayes KE, Walk EL, Ammer AG, Markwell SM, Weed SA. Quantitative measurement of invadopodia-mediated extracellular matrix proteolysis in single and multicellular contexts. J Vis Exp 2012; 66: E4119.