Modulation of membrane properties of lung cancer cells by azurin enhances the sensitivity to EGFR-targeted therapy and decreased β1 integrin-mediated adhesion

References

• Streuli CH, Akhtar N. Signal co-operation between integrins and other receptor systems. Biochem J 2009; 418:491-506; PMID:19228122; http://dx.doi.org/10.1042/BJ20081948
   PubMed Web of Science ®Google Scholar
• Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 2010; 10:9-22; PMID:20029421; http://dx.doi.org/10.1038/nrc2748
   PubMed Web of Science ®Google Scholar
• Rathinam R, Alahari SK. Important role of integrins in the cancer biology. Cancer 2010; 29:223-37; PMID:20492711
   PubMed Web of Science ®Google Scholar
• Pontier SM, Muller WJ. Integrins in mammary stem cell biology and breast cancer progression - a role in cancer stem cells? J Cell Sci 2009; 122:207-14; PMID:19118213; http://dx.doi.org/10.1242/jcs.040394
   PubMed Web of Science ®Google Scholar
• Dingemans A-MC, van den Boogaart V, Vosse BA, van Suylen R-J, Griffioen AW, Thijssen VL. Integrin expression profiling identifies integrin alpha5 and beta1 as prognostic factors in early stage non-small cell lung cancer. Mol Cancer 2010; 9:152; PMID:20565758; http://dx.doi.org/10.1186/1476-4598-9-152
   PubMed Web of Science ®Google Scholar
• Morello V, Cabodi S, Sigismund S, Camacho-Leal MP, Repetto D, Volante M, Papotti M, Turco E, Defilippi P. β1 integrin controls EGFR signaling and tumorigenic properties of lung cancer cells. Oncogene 2011; 30:4087-96; PMID:21478906; http://dx.doi.org/10.1038/onc.2011.107
   PubMed Web of Science ®Google Scholar
• Yamada T, Hiraoka Y, Ikehata M, Kimbara K, Avner BS, Gupta TK Das, Chakrabarty AM. Apoptosis or growth arrest: modulation of tumor suppressor p53 specificity by bacterial redox protein azurin. PNAS 2004; 101:4770-5; PMID:15044691; http://dx.doi.org/10.1073/pnas.0400899101
   PubMed Web of Science ®Google Scholar
• Punj V, Bhattacharyya S, Saint-dic D, Vasu C, Cunningham EA, Graves J. Bacterial cupredoxin azurin as an inducer of apoptosis and regression in human breast cancer. Oncogene 2004; 23:2367-78; PMID:14981543; http://dx.doi.org/10.1038/sj.onc.1207376
   PubMed Web of Science ®Google Scholar
• Yamada T, Fialho AM, Punj V, Bratescu L, Gupta TK Das, Chakrabarty AM. Internalization of bacterial redox protein azurin in mammalian cells: entry domain and specificity. Cell Microbiol 2005; 7:1418-31; PMID:16153242; http://dx.doi.org/10.1111/j.1462-5822.2005.00567.x
   PubMed Web of Science ®Google Scholar
• Chaudhari A, Mahfouz M, Fialho AM, Yamada T, Granja AT, Zhu Y, Hashimoto W, Schlarb-Ridley B, Cho W, Das Gupta TK, et al. Cupredoxin-cancer interrelationship: azurin binding with EphB2, interference in EphB2 tyrosine phosphorylation, and inhibition of cancer growth. Biochemistry 2007; 46:1799-810; PMID:17249693; http://dx.doi.org/10.1021/bi061661x
   PubMed Web of Science ®Google Scholar
• Taylor BN, Mehta RR, Yamada T, Lekmine F, Christov K, Chakrabarty AM, Green A, Bratescu L, Shilkaitis A, Beattie CW, et al. Noncationic peptides obtained from azurin preferentially enter cancer cells. Cancer Res 2009; 69:537-46; PMID:19147567; http://dx.doi.org/10.1158/0008-5472.CAN-08-2932
   PubMed Web of Science ®Google Scholar
• Mehta RR, Yamada T, Taylor BN, Christov K, King ML, Majumdar D, Lekmine F, Tiruppathi C, Shilkaitis A, Bratescu L, et al. A cell penetrating peptide derived from azurin inhibits angiogenesis and tumor growth by inhibiting phosphorylation of VEGFR-2, FAK and Akt. Angiogenesis 2011; 14:355-69; PMID:21667138; http://dx.doi.org/10.1007/s10456-011-9220-6
   PubMed Web of Science ®Google Scholar
• Yamada T, Christov K, Das Gupta TK BC. Mechanism of action of p28, a first-in-class, non-HDM2 mediated peptide inhibitor of p53 ubiquitination. In: J Clin Oncol 2011; 29. page suppl; abstr e13513.
   Web of Science ®Google Scholar
• Warso M a, Richards JM, Mehta D, Christov K, Schaeffer C, Rae Bressler L, Yamada T, Majumdar D, Kennedy S a, Beattie CW, et al. A first-in-class, first-in-human, phase I trial of p28, a non-HDM2-mediated peptide inhibitor of p53 ubiquitination in patients with advanced solid tumours. Br J Cancer 2013; 108:1061-70; PMID:23449360; http://dx.doi.org/10.1038/bjc.2013.74
   PubMed Web of Science ®Google Scholar
• Yamada T, Christov K, Shilkaitis A, Bratescu L, Green A, Santini S, Bizzarri AR, Cannistraro S, Gupta TKD, Beattie CW. p28, A first in class peptide inhibitor of cop1 binding to p53. Br J Cancer 2013; 108:2495-504; PMID:23736031; http://dx.doi.org/10.1038/bjc.2013.266
   PubMed Web of Science ®Google Scholar
• Yamada T, Mehta RR, Lekmine F, Christov K, King ML, Majumdar D, Shilkaitis A, Green A, Bratescu L, Beattie CW, et al. A peptide fragment of azurin induces a p53-mediated cell cycle arrest in human breast cancer cells. Mol Cancer Ther 2009; 8:2947-58; PMID:19808975; http://dx.doi.org/10.1158/1535-7163.MCT-09-0444
   PubMed Web of Science ®Google Scholar
• Bernardes N, Ribeiro AS, Abreu S, Vieira AF, Carreto L, Santos M, Seruca R, Paredes J, Fialho AM. High-throughput molecular profiling of a P-cadherin overexpressing breast cancer model reveals new targets for the anti-cancer bacterial protein azurin. Int J Biochem Cell Biol 2014; 50:1-9; PMID:24509127; http://dx.doi.org/10.1016/j.biocel.2014.01.023
   PubMed Web of Science ®Google Scholar
• Paredes J, Figueiredo J, Albergaria A, Oliveira P, Carvalho J, Ribeiro AS, Caldeira J, Costa AM, Simões-Correia J, Oliveira MJ, et al. Epithelial E- and P-cadherins: Role and clinical significance in cancer. Biochim Biophys Acta 2012; 1826:297-311; PMID:22613680
   PubMed Web of Science ®Google Scholar
• Kanda R, Kawahara A, Watari K, Murakami Y, Sonoda K, Maeda M, Fujita H, Kage M, Uramoto H, Costa C, et al. Erlotinib Resistance in Lung Cancer Cells Mediated by Integrin β1/Src/Akt-Driven Bypass Signaling. Cancer Res 2013; 73:6243-53; PMID:23872583; http://dx.doi.org/10.1158/0008-5472.CAN-12-4502
   PubMed Web of Science ®Google Scholar
• Ju L, Zhou C, Li W, Yan L. Integrin beta1 over-expression associates with resistance to tyrosine kinase inhibitor gefitinib in non-small cell lung cancer. J Cell Biochem 2010; 111:1565-74; PMID:21053345; http://dx.doi.org/10.1002/jcb.22888
   PubMed Web of Science ®Google Scholar
• Gaspar D, Freire JM, Pacheco TR, Barata JT, Castanho MARB. Apoptotic human neutrophil peptide-1 anti-tumor activity revealed by cellular biomechanics. Biochim Biophys Acta - Mol Cell Res 2015; 1853:308-16; PMID:25447543; http://dx.doi.org/10.1016/j.bbamcr.2014.11.006
   PubMed Web of Science ®Google Scholar
• Ju L, Zhou C. Integrin beta 1 enhances the epithelial- mesenchymal transition in association with gefitinib resistance of non-small cell lung cancer. Cancer Biomark 2013; 13:329-36; PMID:24440972
   PubMed Web of Science ®Google Scholar
• Zhang X, Fournier M V, Ware JL, Bissell MJ, Yacoub A, Zehner ZE. Inhibition of vimentin or beta1 integrin reverts morphology of prostate tumor cells grown in laminin-rich extracellular matrix gels and reduces tumor growth in vivo. Mol Cancer Ther 2009; 8:499-508; PMID:19276168; http://dx.doi.org/10.1158/1535-7163.MCT-08-0544
   PubMed Web of Science ®Google Scholar
• Carpenter PM, Dao AV, Arain ZS, Chang MK, Nguyen HP, Arain S, Wang-Rodriguez J, Kwon S-Y, Wilczynski SP. Motility induction in breast carcinoma by mammary epithelial laminin 332 (laminin 5). Mol Cancer Res 2009; 7:462-75; PMID:19351903; http://dx.doi.org/10.1158/1541-7786.MCR-08-0148
   PubMed Web of Science ®Google Scholar
• Okamura M, Yamaji S, Nagashima Y, Nishikawa M, Yoshimoto N, Kido Y, Iemoto Y, Aoki I, Ishigatsubo Y. Prognostic value of integrin beta 1-ILK-pAkt signaling pathway in non-small cell lung cancer. Hum Pathol 2007; 38:1081-91; PMID:17442374; http://dx.doi.org/10.1016/j.humpath.2007.01.003
   PubMed Web of Science ®Google Scholar
• Bernardes N, Ribeiro AS, Abreu S, Mota B, Matos RG, Arraiano CM, Seruca R, Paredes J, Fialho AM. The bacterial protein azurin impairs invasion and FAK/Src signaling in P-cadherin-overexpressing breast cancer models. PLoS One 2013; 19:e69023; http://dx.doi.org/10.1371/journal.pone.0069023
   Google Scholar
• Giannelli G, Azzariti a, Fransvea E, Porcelli L, Antonaci S, Paradiso a. Laminin-5 offsets the efficacy of gefitinib (‘Iressa’) in hepatocellular carcinoma cells. Br J Cancer 2004; 91:1964-9; PMID:15545972; http://dx.doi.org/10.1038/sj.bjc.6602231
   PubMed Web of Science ®Google Scholar
• Rintoul RC, Sethi T. Extracellular matrix regulation of drug resistance in small-cell lung cancer. Clin Sci (Lond) 2002; 102:417-24; PMID:11914104; http://dx.doi.org/10.1042/cs1020417
   PubMed Web of Science ®Google Scholar
• Helleman J, Jansen MPHM, Burger C, van der Burg MEL, Berns EMJJ. Integrated genomics of chemotherapy resistant ovarian cancer: A role for extracellular matrix, TGFbeta and regulating microRNAs. Int J Biochem Cell Biol 2010; 42:25-30; PMID:19854294; http://dx.doi.org/10.1016/j.biocel.2009.10.016
   PubMed Web of Science ®Google Scholar
• Sharma S, Santiskulvong C, Rao J, Gimzewski JK, Dorigo O. The role of Rho GTPase in cell stiffness and cisplatin resistance in ovarian cancer cells. Integr Biol (Camb) 2014; 6:611-7; PMID:24718685; http://dx.doi.org/10.1039/c3ib40246k
   PubMed Web of Science ®Google Scholar
• Kim KS, Cho CH, Park EK, Jung MH, Yoon KS, Park HK. AFM-Detected apoptotic changes in morphology and biophysical property caused by paclitaxel in Ishikawa and HeLa cells. PLoS One 2012; 7:e30066; PMID:22272274; http://dx.doi.org/10.1371/journal.pone.0030066
   PubMed Web of Science ®Google Scholar
• Kao FS, Pan YR, Hsu RQ, Chen HM. Efficacy verification and microscopic observations of an anticancer peptide, CB1a, on single lung cancer cell. Biochim Biophys Acta - Biomembr 2012; 1818:2927-35; PMID:22846508; http://dx.doi.org/10.1016/j.bbamem.2012.07.019
   PubMed Web of Science ®Google Scholar
• Corbin EA, Kong F, Lim CT, King WP, Bashir R. Biophysical properties of human breast cancer cells measured using silicon MEMS resonators and atomic force microscopy. Lab Chip 2015; 15:839-47; PMID:25473785; http://dx.doi.org/10.1039/C4LC01179A
   PubMed Web of Science ®Google Scholar
• Prabhune M, Belge G, Dotzauer A, Bullerdiek J, Radmacher M. Comparison of mechanical properties of normal and malignant thyroid cells. Micron 2012; 43:1267-72; PMID:22522060; http://dx.doi.org/10.1016/j.micron.2012.03.023
   PubMed Web of Science ®Google Scholar
• Peetla C, Vijayaraghavalu S, Labhasetwar V. Biophysics of cell membrane lipids in cancer drug resistance: implications for drug transport and drug delivery with nanoparticles. Adv Drug Deliv Rev 2013; 65:1686-98; PMID:24055719; http://dx.doi.org/10.1016/j.addr.2013.09.004
   PubMed Web of Science ®Google Scholar
• Busk M, Pytelasv R, Sheppardsil D. Characterization of the Integrin avP6 as a Fibronectin-binding Protein. J Biol Chem 1992; 267(9):5790-6; PMID:1532572
   PubMed Web of Science ®Google Scholar
• Pinto SN, Silva LC, de Almeida RFM, Prieto M. Membrane domain formation, interdigitation, and morphological alterations induced by the very long chain asymmetric C24:1 ceramide. Biophys J 2008; 95:2867-79; PMID:18586849; http://dx.doi.org/10.1529/biophysj.108.129858
   PubMed Web of Science ®Google Scholar
• Johnson KL, Kendall K, Roberts aD. Surface Energy and the Contact of Elastic Solids. Proc R Soc A Math Phys Eng Sci 1971; 324:301-13; http://dx.doi.org/10.1098/rspa.1971.0141
   Web of Science ®Google Scholar