Annexin A6 improves anti-migratory and anti-invasive properties of tyrosine kinase inhibitors in EGFR overexpressing human squamous epithelial cells.
Animals
Annexin A6
/ genetics
Apoptosis
Carcinoma, Squamous Cell
/ drug therapy
Cell Movement
Cell Proliferation
ErbB Receptors
/ antagonists & inhibitors
Gene Expression Regulation, Neoplastic
Humans
Mice
Neoplasm Invasiveness
Neoplasms, Glandular and Epithelial
/ drug therapy
Phosphorylation
Protein Kinase C-alpha
/ genetics
Protein Kinase Inhibitors
/ pharmacology
Tumor Cells, Cultured
Xenograft Model Antitumor Assays
A431 epithelial cells
EGFR
PKCα
TKIs
annexin A6
Journal
The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
25
07
2019
revised:
22
10
2019
accepted:
18
12
2019
pubmed:
24
12
2019
medline:
14
5
2021
entrez:
24
12
2019
Statut:
ppublish
Résumé
Annexin A6 (AnxA6), a member of the calcium (Ca
Substances chimiques
Annexin A6
0
Protein Kinase Inhibitors
0
EGFR protein, human
EC 2.7.10.1
ErbB Receptors
EC 2.7.10.1
Protein Kinase C-alpha
EC 2.7.11.13
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2961-2978Informations de copyright
© 2019 Federation of European Biochemical Societies.
Références
Burgess AW, Cho HS, Eigenbrot C, Ferguson KM, Garrett TP, Leahy DJ, Lemmon MA, Sliwkowski MX, Ward CW & Yokoyama S (2003) An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol Cell 12, 541-552.
Bergeron JJ, Di Guglielmo GM, Dahan S, Dominguez M & Posner BI (2016) Spatial and temporal regulation of receptor tyrosine kinase activation and intracellular signal transduction. Annu Rev Biochem 85, 573-597.
Bakker J, Spits M, Neefjes J & Berlin I (2017) The EGFR odyssey - from activation to destruction in space and time. J Cell Sci 130, 4087-4096.
Tomas A, Futter CE & Eden ER (2014) EGF receptor trafficking: consequences for signaling and cancer. Trends Cell Biol 24, 26-34.
Eden ER, White IJ, Tsapara A & Futter CE (2010) Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor interaction. Nat Cell Biol 12, 267-272.
Hunter T, Ling N & Cooper JA (1984) Protein kinase C phosphorylation of the EGF receptor at a threonine residue close to the cytoplasmic face of the plasma membrane. Nature 311, 480-483.
Livneh E, Dull TJ, Berent E, Prywes R, Ullrich A & Schlessinger J (1988) Release of a phorbol ester-induced mitogenic block by mutation at Thr-654 of the EGFR. Mol Cell Biol 8, 2302-2308.
Fabbro D, Küng W, Roos W, Regazzi R & Eppenberger U (1986) Epidermal growth factor binding and protein kinase C activities in human breast cancer cell lines: possible quantitative relationship. Cancer Res 46, 2720-2725.
Mackay HJ & Twelves CJ (2007) Targeting the protein kinase C family: are we there yet? Nat Rev Cancer 7, 554-562.
Wheeler DL, Dunn EF & Harari PM (2010) Understanding resistance to EGFR inhibitors on future treatment strategies. Nat Rev Clin Oncol 7, 493-507.
Pines G, Köstler WJ & Yarden Y (2010) Oncogenic mutant forms of EGFR: lessons in signal transduction and targets for cancer therapy. FEBS Lett 584, 2699-2706.
Han W & Lo HW (2012) Landscape of EGFR signaling network in human cancers: biology and therapeutic response in relation to receptor subcellular locations. Cancer Lett 318, 124-134.
Wang S & Li J (2019) Second-generation EGFR and ErbB tyrosine kinase inhibitors as first-line treatments for non-small cell lung cancer. Onco Targets Ther 12, 6535-6548.
Tagliamento M, Genova C, Rijavec E, Rossi G, Biello F, Dal Bello MG, Alama A, Coco S, Boccardo S & Grossi F (2018) Afatinib and erlotinib in the treatment of squamous-cell lung cancer. Expert Opin Pharmacother 19, 2055-2062.
Tan DSW, Chong FT, Leong HS, Toh SY, Lau DP, Kwang XL, Zhang X, Sundaram GM, Tan GS, Chang MM et al. (2017) Long noncoding RNA EGFR-AS1 mediates epidermal growth factor receptor addiction and modulates treatment response in squamous cell carcinoma. Nat Med 23, 1167-1175.
Cohen EE, Davis DW, Karrison TG, Seiwert TY, Wong SJ, Nattam S, Kozloff MF, Clark JI, Yan DH, Liu W et al. (2009) Erlotinib and bevacizumab in patients with recurrent or metastatic squamous-cell carcinoma of the head and neck: a phase I/II study. Lancet Oncol 10, 247-257.
Arteaga CL & Engelman JA (2014) ERBB receptors: from oncogene discovery to basic science to mechanism-based cancer therapeutics. Cancer Cell 25, 282-303.
Timpson P, Wilson AS, Lehrbach GM, Sutherland RL, Musgrove EA & Daly RJ (2007) Aberrant expression of cortactin in head and neck squamous cell carcinoma cells is associated with enhanced cell proliferation and resistance to the EGFR inhibitor gefitinib. Cancer Res 67, 9304-9314.
Neilsen BK, Frodyma DE, Lewis RE & Fisher KW (2017) KSR as a therapeutic target for Ras-dependent cancers. Expert Opin Ther Targets 21, 499-509.
Kolch W (2005) Coordinating ERK/MAPK signaling through scaffolds and inhibitors. Nat Rev Mol Cell Biol 6, 827-837.
Yamada T, Takeuchi S, Fujita N, Nakamura A, Wang W, Li Q, Oda M, Mitsudomi T, Yatabe Y, Sekido Y et al. (2013) Akt kinase-interacting protein 1, a novel therapeutic target for lung cancer with EGFR-activating and gatekeeper mutations. Oncogene 32, 4427-4435.
Cui Y, Zhu T, Song X, Liu J, Liu S & Zhao R (2018) Downregulation of caveolin-1 increased EGFR-TKIs sensitivity in lung adenocarcinoma cell line with EGFR mutation. Biochem Biophys Res Commun 495, 733-739.
Agelaki S, Spiliotaki M, Markomanolaki H, Kallergi G, Mavroudis D, Georgoulias V & Stournaras C (2009) Caveolin-1 regulates EGFR signaling in MCF-7 breast cancer cells and enhances gefitinib-induced tumor cell inhibition. Cancer Biol Ther 8, 1470-1477.
McKay MM, Freeman AK & Morrison DK (2011) Complexity in KSR function revealed by Raf inhibitor and KSR structure studies. Small GTPases 2, 276-281.
Eden ER, Sanchez-Heras E, Tsapara A, Sobota A, Levine TP & Futter CE (2016) Annexin A1 tethers membrane contact sites that mediate ER to endosome cholesterol transport. Dev Cell 37, 473-483.
Futter CE & White IJ (2007) Annexins and endocytosis. Traffic 8, 951-958.
Grewal T & Enrich C (2009) Annexins-modulators of EGF receptor signaling and trafficking. Cell Signal 21, 847-858.
Hoque M, Rentero C, Cairns R, Tebar F, Enrich C & Grewal T (2014) Annexins - scaffolds modulating PKC localization and signaling. Cell Signal 26, 1213-1225.
Koumangoye RB, Nangami GN, Thompson PD, Agboto VK, Ochieng J & Sakwe AM (2013) Reduced annexin A6 expression promotes the degradation of activated epidermal growth factor receptor and sensitizes invasive breast cancer cells to EGFR-targeted tyrosine kinase inhibitors. Mol Cancer 12, 167.
Gerke V, Creutz CE & Moss SE (2005) Annexins: linking Ca2+ signaling to membrane dynamics. Nat Rev Mol Cell Biol 6, 449-461.
Enrich C, Rentero C, Vilà de Muga S, Reverter M, Mulay V, Wood P, Koese M & Grewal T (2011) Annexin A6 - linking Ca2+ signaling with cholesterol transport. Biochim Biophys Acta Mol Cell Res 1813, 935-947.
Grewal T, Koese M, Rentero C & Enrich C (2010) Molecules in focus: annexin A6 - regulator of the EGFR/Ras signaling pathway and cholesterol homeostasis. Int J Biochem Cell Biol 42, 580-584.
Cubells L, Vilà de Muga S, Tebar F, Wood P, Evans R, Ingelmo-Torres M, Calvo M, Gaus K, Tebar F, Pol A et al. (2007) Annexin A6 induced alterations in cholesterol transport and caveolin export from the Golgi complex. Traffic 8, 1568-1589.
Grewal T, Evans R, Rentero C, Tebar F, Cubells L, de Diego I, Kirchhoff MF, Hughes WE, Heeren J, Rye KA et al. (2005) Annexin A6 stimulates the membrane recruitment of p120GAP to modulate Ras and Raf-1 activity. Oncogene 24, 5809-5820.
Vilà de Muga S, Timpson P, Cubells L, Evans R, Hayes TE, Rentero C, Hegemann A, Reverter M, Leschner J, Pol A et al. (2009) Annexin A6 inhibits Ras signaling in breast cancer cells. Oncogene 28, 363-377.
Grewal T & Enrich C (2006) Molecular mechanisms involved in Ras inactivation: the annexin A6-p120GAP complex. BioEssays 28, 1211-1220.
Rentero C, Evans R, Wood P, Tebar F, Vilà de Muga S, Cubells L, de Diego I, Hayes TE, Hughes WE, Pol A et al. (2006) Inhibition of H-Ras and MAPK is compensated by PKC-dependent pathways in annexin A6 expressing cells. Cell Signal 18, 1006-1016.
Koese M, Rentero C, Kota BP, Hoque M, Cairns R, Wood P, Vilà de Muga S, Reverter M, Alvarez-Guaita A, Monastyrskaya K et al. (2013) Annexin A6 is a scaffold for PKCα to promote EGFR inactivation. Oncogene 32, 2858-2872.
García-Melero A, Reverter M, Hoque M, Meneses-Salas E, Koese M, Conway JR, Johnsen CH, Alvarez-Guaita A, Morales-Paytuvi F, Elmaghrabi YA et al. (2016) Annexin A6 and late endosomal cholesterol modulate integrin recycling and cell migration. J Biol Chem 291, 1320-1335.
Smythe E, Smith PD, Jacob SM, Theobald J & Moss SE (1994) Endocytosis occurs independently of annexin VI in human A431 cells. J Cell Biol 124, 301-306.
Lynch DH & Yang XD (2002) Therapeutic potential of ABX-EGF: a fully human anti-epidermal growth factor receptor monoclonal antibody for cancer treatment. Semin Oncol 29 (Suppl 4), 47-50.
Wakeling AE, Guy SP, Woodburn JR, Ashton SE, Curry BJ, Barker AJ & Gibson KH (2002) ZD1839 (Iressa): an orally active inhibitor of epidermal growth factor signaling with potential for cancer therapy. Cancer Res 62, 5749-5754.
Theobald J, Hanby A, Patel K & Moss SE (1995) Annexin VI has tumour-suppressor activity in human A431 squamous epithelial carcinoma cells. Br J Cancer 71, 786-788.
Marais R, Light Y, Mason C, Paterson H, Olson MF & Marshall CJ (1998) Requirement of the Ras-GTP-Raf complexes for activation of Raf-1 by protein kinase C. Science 280, 109-112 (erratum appears in Science 280, 987).
Agell N, Bachs O, Rocamora N & Villalonga P (2002) Modulation of the Ras/Raf/MEK/ERK pathway by Ca(2+) and calmodulin. Cell Signal 14, 649-654.
Schönwasser DC, Marais RM, Marshall CJ & Parker PJ (1998) Activation of the mitogen-activated protein kinase/extracellular signal-regulated kinase pathway by conventional, novel and atypical protein kinase C isotypes. Mol Cell Biol 18, 790-798.
Yamaguchi K, Ogita K, Nakamura S & Nishizuka Y (1995) The protein kinase C isoforms leading to MAP-kinase activation in CHO cells. Biochem Biophys Res Commun 210, 639-647.
Kim Y, Apetri M, Luo B, Settleman JE & Anderson KS (2015) Differential effects of tyrosine kinase inhibitors in normal and oncogenic EGFR signaling and downstream effectors. Mol Cancer Res 13, 765-774.
Matar P, Rojo F, Cassia R, Moreno-Bueno G, Di Cosimo S, Tabernero J, Guzmán M, Rodriguez S, Arribas J, Palacios J & et al. (2004) Combined epidermal growth factor receptor targeting with the tyrosine kinase inhibitor gefitinib (ZD1839) and the monoclonal antibody cetuximab (IMC-C225): superiority over single-agent receptor targeting. Clin Cancer Res 10, 6487-6501.
Mukohara T, Engelman JA, Hanna NH, Yeap BY, Kobayashi S, Lindeman N, Halmos B, Pearlberg J, Tsuchihashi Z, Cantley LC et al. (2005) Differential effects of gefitinib and cetuximab on non-small cell lung cancers bearing epidermal growth factor receptor mutations. J Natl Cancer Inst 97, 1185-1194.
Yeo WL, Riely GJ, Yeap BY, Lau MW, Warner JL, Bodio K, Huberman MS, Kris MG, Tenen DG, Pao W et al. (2010) Erlotinib at a dose of 25 mg daily for non-small cell lung cancers with EGFR mutations. J Thorac Oncol 5, 1048-1053.
Yang Z, Bagheri-Yarmand R, Wang RA, Adam L, Papadimitrakopoulou VV, Clayman GL, El-Naggar A, Lotan R, Barnes CJ, Hong WK & et al. (2004) The epidermal growth factor receptor tyrosine kinase inhibitor ZD1839 (Iressa) suppresses c-Src and Pak1 pathways and invasiveness of human cancer cells. Clin Cancer Res 10, 658-667.
Li J, Kleeff J, Giese N, Büchler MW, Korc M & Friess H (2004) Gefitinib (Iressa, ZD 1839), a selective epidermal growth factor receptor tyrosine kinase inhibitor, inhibits pancreatic cancer cell growth, invasion, and colony formation. Int J Oncol 25, 203-210.
Nunes AS, Barros AS, Costa EC, Moreira AF & Correia IJ (2019) 3D tumor spheroids as in vitro models to mimic in vivo human solid tumors resistance to therapeutic drugs. Biotechnol Bioeng 116, 206-226.
Garg R, Benedetti LG, Abera MB, Wang H, Abba M & Kazanietz MG (2014) Protein kinase C and cancer: what we know and what we do not. Oncogene 33, 5225-5237.
Qi H, Liu S, Guo C, Wang J, Greenaway FT & Sun MZ (2015) Role of annexin A6 in cancer. Oncol Lett 10, 1947-1952.
Lund KA, Lazar CS, Chen WS, Walsh BJ, Welsh JB, Herbst JJ, Walton GM, Rosenfeld MG, Gill GN & Wiley HS (1990) Phosphorylation of the epidermal growth factor receptor at threonine 654 inhibits ligand-induced internalization and down-regulation. J Biol Chem 265, 20517-20523.
Bao J, Alroy I, Waterman H, Schejter ED, Brodie CH, Gruenberg J & Yarden Y (2000) Threonine phosphorylation diverts internalized epidermal growth factor receptors from a degradative pathway to the recycling endosome. J Biol Chem 275, 26178-26186.
Jameson KL, Mazur PK, Zehnder AM, Zhang J, Zarnegar B, Sage J & Khavari PA (2013) IQGAP1 scaffold-kinase interactions blockade selectively targets RAS-MAP kinase-driven tumors. Nat Med 19, 626-630.
Hofman P, Butori C, Havet K, Hofman V, Selva E, Guevara N, Santini J & Van Obberghen-Schilling E (2018) Prognostic significance of cortactin levels in head and neck squamous cell carcinoma: comparison with epidermal growth factor receptor status. Br J Cancer 98, 956-964.
Raulf N, Lucarelli P, Thavaraj S, Brown S, Vicencio JM, Sauter T & Tavassoli M (2018) Annexin A1 regulates EGFR activity and alters EGFR-containing tumour-derived exosomes in head and neck cancers. Eur J Cancer 102, 52-68.
Berns K, Sonnenblick A, Gennissen A, Brohée S, Hijmans EM, Evers B, Fumagalli D, Desmedt C, Loibl S, Denkert C et al. (2016) Loss of ARID1A activates AnxA1, which serves as a predictive biomarker for trastuzumab resistance. Clin Cancer Res 22, 5238-5248.
Gibbs LD, Chaudhary P, Mansheim K, Hare RJ, Mantsch RA & Vishwanatha JK (2018) AnxA2 expression in African American triple-negative breast cancer. Breast Cancer Res Treat 174, 113-120.
Zhang Y, Bi J, Zhu H, Shi M & Zeng X (2018) AnxA2 could act as a moderator of EGFR-directed therapy resistance in triple negative breast cancer. Biosci Biotechnol Biochem 82, 1733-1741.
Shetty PK, Thamake SI, Biswas S, Johansson SL & Vishwanatha JK (2012) Reciprocal regulation of annexin A2 and EGFR with Her-2 in Her-2 negative and Herceptin-resistant breast cancer. PLoS ONE 7, e44299.
Yi Y, Zeng S, Wang Z, Wu M, Ma Y, Ye X, Zhang B & Liu H (2018) Cancer-associated fibroblasts promote epithelial-mesenchymal transition and EGFR-TKI resistance of non-small cell lung cancers via HGF/IGF-1/AnxA2 signaling. Biochim Biophys Acta Mol Basis Dis 1864, 793-803.
Grewal T, Hoque M, Conway JRW, Reverter M, Wahba M, Beevi SS, Timpson P, Enrich C & Rentero C (2017) Annexin A6-a multifunctional scaffold in cell motility. Cell Adh Migr 11, 288-304.
Reverter M, Rentero C, Garcia-Melero A, Hoque M, Vilà de Muga S, Alvarez-Guaita A, Conway JR, Wood P, Cairns R, Lykopoulou L et al. (2014) Cholesterol regulates syntaxin 6 trafficking at trans-Golgi network endosomal boundaries. Cell Rep 7, 883-897.
Reverter M, Rentero C, de Muga SV, Alvarez-Guaita A, Mulay V, Cairns R, Wood P, Monastyrskaya K, Pol A, Tebar F et al. (2011) Cholesterol transport from late endosomes to the Golgi regulates t-SNARE trafficking, assembly, and function. Mol Biol Cell 22, 4108-4123.
Alvarez-Guaita A, Vilà de Muga S, Owen DM, Williamson D, Magenau A, García-Melero A, Reverter M, Hoque M, Cairns R, Cornely R et al. (2015) Evidence for annexin A6-dependent plasma membrane remodeling of lipid domains. Br J Pharmacol 172, 1677-1690.
Balbis A & Posner BI (2010) Compartmentalization of EGFR in cellular membranes: role of membrane rafts. J Cell Biochem 109, 1103-1108.
Irwin ME, Mueller KL, Bohin N, Ge Y & Boerner JL (2011) Lipid raft localization of EGFR alters the response of cancer cells to the EGFR tyrosine kinase inhibitor gefitinib. J Cell Physiol 226, 2316-2328.
Chen Q, Pan Z, Zhao M, Wang Q, Qiao C, Miao L & Ding X (2018) High cholesterol in lipid rafts reduces the sensitivity to EGFR-TKI therapy in non-small cell lung cancer. J Cell Physiol 233, 6722-6732.
Widatalla SE, Korolkova OY, Whalen DS, Goodwin JS, Williams KP, Ochieng J & Sakwe AM (2018) Lapatinib induced Annexin A6 up-regulation as an adaptive response of triple negative breast cancer cells to EGFR tyrosine kinase inhibitors. Carcinogenesis 40, 998-1009.
Leca J, Martinez S, Lac S, Nigri J, Secq V, Rubis M, Bressy C, Sergé A, Lavaut MN, Dusetti N et al. (2016) Cancer-associated fibroblast-derived annexin A6+ extracellular vesicles support pancreatic cancer aggressiveness. J Clin Invest 126, 4140-4156.
Keklikoglou I, Cianciaruso C, Güç E, Squadrito ML, Spring LM, Tazzyman S, Lambein L, Poissonnier A, Ferraro GB, Baer C et al. (2019) Chemotherapy elicits pro-metastatic extracellular vesicles in breast cancer models. Nat Cell Biol 21, 190-202.
Quattrocelli M, Barefield DY, Warner JL, Vo AH, Hadhazy M, Earley JU, Demonbreun AR & McNally EM (2017) Intermittent glucocorticoid steroid dosing enhances muscle repair without eliciting muscle atrophy. J Clin Invest 127, 2418-2432.
O'Sullivan D, Dowling P, Joyce H, McAuley E, McCann A, Henry M, McGovern B, Barham P, Kelleher FC, Murphy J et al. (2017) A novel inhibitory anti-invasive Mab isolated from phenotypic screening highlights AnxA6 as a functionally relevant target protein in pancreatic cancer. Br J Cancer 117, 1326-1335.
Grewal T, Heeren J, Mewawala D, Schnitgerhans T, Wendt D, Salomon G, Enrich C, Beisiegel U & Jäckle S (2000) Annexin VI stimulates endocytosis and is involved in the trafficking of LDL to the prelysosomal compartment. J Biol Chem 275, 33806-33813.
de Diego I, Schwartz F, Siegfried H, Dauterstedt P, Heeren J, Beisiegel U, Enrich C & Grewal T (2002) Cholesterol modulates the membrane binding and intracellular distribution of annexin 6. J Biol Chem 277, 32187-32194.
Swarbrick A, Roy E, Allen T & Bishop JM (2008) Id1 cooperates with oncogenic Ras to induce metastatic mammary carcinoma by subversion of the cellular senescence response. Proc Natl Acad Sci USA 105, 5402-5407.
Zhou Q, Phoa AF, Abbassi RH, Hoque M, Reekie TA, Font JS, Ryan RM, Stringer BW, Day BW, Johns TG et al. (2017) Structural optimization and pharmacological evaluation of inhibitors targeting dual-specificity tyrosine phosphorylation-regulated kinases (DYRK) and CDC-like kinases (CLK) in glioblastoma. J Med Chem 60, 2052-2070.
Friedrich J, Seidel C, Ebner R & Kunz-Schughart LA (2009) Spheroid-based drug screen: considerations and practical approach. Nat Protoc 4, 309-324.