Proteome analysis of multidrug-resistant, breast cancer–derived microparticles

References

• Biedler JL, Riehm H, Peterson RH, Spengler BA. Membrane-mediated drug resistance and phenotypic reversion to normal growth behavior of Chinese hamster cells. J Natl Cancer Inst. 1975; 55: 671–80.
   Google Scholar
• Fojo A, Akiyama S, Gottesman MM, Pastan I. Reduced drug accumulation in multiply drug-resistant human KB carcinoma cell lines. Cancer Res. 1985; 45: 3002–7.
   PubMed Web of Science ®Google Scholar
• Riordan JR, Deuchars K, Kartner N, Alon N, Trent J, Ling V. Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines. Nature. 1985; 316: 817–9. 10.1038/316817a0.
   PubMed Web of Science ®Google Scholar
• Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP–dependent transporters. Nat Rev Cancer. 2002; 2: 48–58.
   PubMed Web of Science ®Google Scholar
• Levchenko A, Mehta BM, Niu X, Kang G, Villafania L, Way D et al. Intercellular transfer of P-glycoprotein mediates acquired multidrug resistance in tumor cells. Proc Natl Acad Sci USA. 2005; 102: 1933–8.
   PubMed Web of Science ®Google Scholar
• Bebawy M, Combes V, Lee E, Jaiswal R, Gong J, Bonhoure A et al. Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells. Leukemia. 2009; 23: 1643–9.
   PubMed Web of Science ®Google Scholar
• Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007; 9: 654–9.
   PubMed Web of Science ®Google Scholar
• Bergsmedh A, Szeles A, Henriksson M, Bratt A, Folkman MJ, Spetz A-L et al. Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc Natl Acad Sci USA. 2001; 98: 6407–11.
   PubMed Web of Science ®Google Scholar
• Watkins SC, Salter RD. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity. 2005; 23: 309–18.
   PubMed Web of Science ®Google Scholar
• Sherer NM, Mothes W. Cytonemes and tunneling nanotubules in cell–cell communication and viral pathogenesis. Trends Cell Biol. 2008; 18: 414–20.
   PubMed Web of Science ®Google Scholar
• Jaiswal R, Gong J, Sambasivam S, Combes V, Mathys J-M, Davey R et al. Microparticle-associated nucleic acids mediate trait dominance in cancer. FASEB J. 2012; 26: 420–9.
   PubMed Web of Science ®Google Scholar
• Bebawy M, Morris MB, Roufogalis BD. A continuous fluorescence assay for the study of P-glycoprotein-mediated drug efflux using inside-out membrane vesicles. Anal Biochem. 1999; 268: 270–7.
   PubMed Web of Science ®Google Scholar
• Jaiswal R, Luk F, Dalla PV, Grau GER, Bebawy M. Breast cancer-derived microparticles display tissue selectivity in the transfer of resistance proteins to cells. PLoS One. 2013; 8: e61515.
   PubMed Web of Science ®Google Scholar
• Distler JH, Pisetsky DS, Huber LC, Kalden JR, Gay S, Distler O. Microparticles as regulators of inflammation: novel players of cellular crosstalk in the rheumatic diseases. Arthritis Rheum. 2005; 52: 3337–48.
   PubMed Web of Science ®Google Scholar
• Gong J, Jaiswal R, Mathys J-M, Combes V, Grau G, Bebawy M. Microparticles and their emerging role in cancer multidrug resistance. Cancer Treat Rev. 2012; 38: 226–34.
   PubMed Web of Science ®Google Scholar
• Zwicker JI, Liebman HA, Neuberg D, Lacroix R, Bauer KA, Furie BC et al. Tumor-derived tissue factor–bearing microparticles are associated with venous thromboembolic events in malignancy. Clin Cancer Res. 2009; 15: 6830–40.
   PubMed Web of Science ®Google Scholar
• Vasina E, Heemskerk JW, Weber C, Koenen RR. Platelets and platelet-derived microparticles in vascular inflammatory disease. Inflamm Allergy Drug Targets. 2010; 9: 346–54.
   Google Scholar
• Sabatier F, Darmon P, Hugel B, Combes V, Sanmarco M, Velut J-G et al. Type 1 and type 2 diabetic patients display different patterns of cellular microparticles. Diabetes. 2002; 51: 2840–5.
   PubMed Web of Science ®Google Scholar
• Mack M, Kleinschmidt A, Brühl H, Klier C, Nelson PJ, Cihak J et al. Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med. 2000; 6: 769–75.
   PubMed Web of Science ®Google Scholar
• Nieuwland R, van der Post JA, Lok CA, Kenter G, Sturk A. Microparticles and exosomes in gynecologic neoplasias. Semin Thromb Hemost. 2010; 36: 925–9.
   Google Scholar
• Jeon S, Kim NH, Kim JY, Lee AY. Stem cell factor induces ERM proteins phosphorylation through PI3K activation to mediate melanocyte proliferation and migration. Pigment Cell Melanoma Res. 2009; 22: 77–85.
   Web of Science ®Google Scholar
• Luciani F, Molinari A, Lozupone F, Calcabrini A, Lugini L, Stringaro A et al. P-glycoprotein–actin association through ERM family proteins: a role in P-glycoprotein function in human cells of lymphoid origin. Blood. 2002; 99: 641–8.
   PubMed Web of Science ®Google Scholar
• Killock DJ, Parsons M, Zarrouk M, Ameer-Beg SM, Ridley AJ, Haskard DO et al. In vitro and in vivo characterization of molecular interactions between calmodulin, ezrin/radixin/moesin, and L-selectin. J Biol Chem. 2009; 284: 8833–45.
   Web of Science ®Google Scholar
• Lu JF, Luk F, Gong J, Jaiswal R, Grau GE, Bebawy M. Microparticles mediate MRP1 intercellular transfer and the re-templating of intrinsic resistance pathways. Pharmacol Res. 2013; 76: 77–83.
   PubMed Web of Science ®Google Scholar
• Gong J, Luk F, Jaiswal R, George AM, Grau GER, Bebawy M. Microparticle drug sequestration provides a parallel pathway in the acquisition of cancer drug resistance. Eur J Pharmacol. 2013; 721: 116–25.
   PubMed Web of Science ®Google Scholar
• Jaiswal R, Luk F, Gong J, Mathys J-M, Grau G, Bebawy M. Microparticle conferred microRNA profiles-implications in the transfer and dominance of cancer traits. Mol Cancer. 2012; 11: 37.
   PubMed Web of Science ®Google Scholar
• Bogema DR, Deutscher AT, Woolley LK, Seymour LM, Raymond BB, Tacchi JL et al. Characterization of cleavage events in the multifunctional cilium adhesin Mhp684 (P146) reveals a mechanism by which Mycoplasma hyopneumoniae regulates surface topography. MBio. 2012; 3: e00282–11.
   Web of Science ®Google Scholar
• Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis. 1999; 20(18): 3551–67.
   PubMed Web of Science ®Google Scholar
• Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem. 2002; 74: 5383–92.
   PubMed Web of Science ®Google Scholar
• Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometrym. Anal Chem. 2003; 75: 4646–58.
   PubMed Web of Science ®Google Scholar
• Andaloussi SE, Mäger I, Breakefield XO, Wood MJ. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov. 2013; 12: 347–57.
   PubMed Web of Science ®Google Scholar
• Lloubes R, Bernadac A, Pommier S. Non classical secretion systems. Res Microbiol. 2013; 164: 655–63.
   Web of Science ®Google Scholar
• Lee Y, Andaloussi SE, Wood MJ. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet. 2012; 21: R125–34.
   PubMed Web of Science ®Google Scholar
• Kucharzewska P, Belting M. Emerging roles of extracellular vesicles in the adaptive response of tumour cells to microenvironmental stress. J Extracell Vesicles. 2013; 2 20304, doi: http://dx.doi.org/10.3402/jev.v2i0.20304.
   PubMedGoogle Scholar
• Dvorak H, Quay S, Orenstein N, Dvorak A, Hahn P, Bitzer A et al. Tumor shedding and coagulation. Science. 1981; 212: 923–4.
   PubMed Web of Science ®Google Scholar
• Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci USA. 2009; 106: 3794–9.
   PubMed Web of Science ®Google Scholar
• Zöller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule?. Nat Rev Cancer. 2011; 11: 254–67.
   PubMed Web of Science ®Google Scholar
• Wang L, Zhou X, Zhou T, Ma D, Chen S, Zhi X et al. Ecto-5'-nucleotidase promotes invasion, migration and adhesion of human breast cancer cells. J Cancer Res Clin Oncol. 2008; 134: 365–72.
   PubMed Web of Science ®Google Scholar
• Ujhazy P, Berleth ES, Pietkiewicz JM, Kitano H, Skaar JR, Ehrke MJ et al. Evidence for the involvement of ecto-5'-nucleotidase (CD73) in drug resistance. Int J Cance. 1996; 68: 493–500.
   PubMed Web of Science ®Google Scholar
• Kalinina E, Berozov T, Shtil A, Chernov N, Glasunova V, Novichkova M et al. Expression of genes of glutathione transferase isoforms GSTP1-1, GSTA4-4, and GSTK1-1 in tumor cells during the formation of drug resistance to cisplatin. Bull Exp Biol Med. 2012; 154: 64–7.
   PubMed Web of Science ®Google Scholar
• Meurice N, Wang L, Lipinski CA, Yang Z, Hulme C, Loftus JC. Structural conservation in band 4.1, ezrin, radixin, moesin (FERM) domains as a guide to identify inhibitors of the proline-rich tyrosine kinase 2. J Med Chem. 2009; 53: 669–77.
   Web of Science ®Google Scholar
• Amieva MR, Furthmayr H. Subcellular localization of moesin in dynamic filopodia, retraction fibers, and other structures involved in substrate exploration, attachment, and cell-cell contacts. Exp Cell Res. 1995; 219: 180–96.
   Web of Science ®Google Scholar
• Pearson MA, Reczek D, Bretscher A, Karplus PA. Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain. Cell. 2000; 101: 259–70.
   PubMed Web of Science ®Google Scholar
• Dixon J, Kaklamanis L, Turley H, Hickson I, Leek R, Harris A et al. Expression of aminopeptidase-n (CD 13) in normal tissues and malignant neoplasms of epithelial and lymphoid origin. J Clin Pathol. 1994; 47: 43–7.
   PubMed Web of Science ®Google Scholar
• Kuhajda FP. Fatty-acid synthase and human cancer: new perspectives on its role in tumor biology. Nutrition. 2000; 16: 202–8.
   PubMed Web of Science ®Google Scholar
• Critchley D. Cytoskeletal proteins talin and vinculin in integrin-mediated adhesion. Biochem Soc Trans. 2004; 32: 831–6.
   PubMed Web of Science ®Google Scholar
• Vié N, Copois V, Bascoul-Mollevi C, Denis V, Bec N, Robert B et al. Overexpression of phosphoserine aminotransferase PSAT1 stimulates cell growth and increases chemoresistance of colon cancer cells. Mol Cancer. 2008; 7: 14.
   PubMed Web of Science ®Google Scholar
• Ghosh P, Anderson J, Cohen N, Takeshita K, Atweh G, Lebowitz P. Expression of the leukemia-associated gene, p18, in normal and malignant tissues; inactivation of expression in a patient with cleaved B cell lymphoma/leukemia. Oncogene. 1993; 8: 2869.
   Web of Science ®Google Scholar
• Vadlamudi RK, Li F, Adam L, Nguyen D, Ohta Y, Stossel TP et al. Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat Cell Biol. 2002; 4: 681–90.
   PubMed Web of Science ®Google Scholar
• Honda K, Yamada T, Endo R, Ino Y, Gotoh M, Tsuda H et al. Actinin-4, a novel actin-bundling protein associated with cell motility and cancer invasion. J Cell Biol. 1998; 140: 1383–93.
   PubMed Web of Science ®Google Scholar
• Geiger B, Spatz JP, Bershadsky AD. Environmental sensing through focal adhesions. Nat Rev Mol Cell Biol. 2009; 10: 21–33.
   PubMed Web of Science ®Google Scholar
• Miletti-González KE, Chen S, Muthukumaran N, Saglimbeni GN, Wu X, Yang J et al. The CD44 receptor interacts with P-glycoprotein to promote cell migration and invasion in cancer. Cancer Res. 2005; 65: 6660–7.
   PubMed Web of Science ®Google Scholar
• Zhi X, Chen S, Zhou P, Shao Z, Wang L, Ou Z et al. RNA interference of ecto-5'-nucleotidase (CD73) inhibits human breast cancer cell growth and invasion. Clin Exp Metastasis. 2007; 24: 439–48.
   PubMed Web of Science ®Google Scholar
• Wang L, Tang S, Wang Y, Xu S, Yu J, Zhi X et al. Ecto-5'-nucleotidase (CD73) promotes tumor angiogenesis. Clin Exp Metastasis. 2013; 30: 671–80.
   PubMed Web of Science ®Google Scholar
• Rappa G, Lorico A, Flavell RA, Sartorelli AC. Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res. 1997; 57: 5232–7.
   PubMed Web of Science ®Google Scholar
• Fu D, Bebawy M, Kable EP, Roufogalis BD. Dynamic and intracellular trafficking of P-glycoprotein-EGFP fusion protein: implications in multidrug resistance in cancer. Int J Cancer. 2004; 109: 174–81.
   PubMed Web of Science ®Google Scholar
• Carreiras F, Lehmann M, Sichel F, Marvaldi J, Gauduchon P, Talaer L. Implication of the αvβ3 integrin in the adhesion of the ovarian-adenocarcinoma cell line IGROV1. Int J Cancer. 1995; 63: 530–6.
   Web of Science ®Google Scholar
• Chishti AH, Kim AC, Marfatia SM, Lutchman M, Hanspal M, Jindal H et al. The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem Sci. 1998; 23: 281–2.
   PubMed Web of Science ®Google Scholar
• Takeshita H, Kusuzaki K, Ashihara T, Gebhardt MC, Mankin HJ, Hirasawa Y. Actin organization associated with the expression of multidrug resistant phenotype in osteosarcoma cells and the effect of actin depolymerization on drug resistance. Cancer Lett. 1998; 126: 75–81.
   Web of Science ®Google Scholar
• Puddu P, Fais S, Luciani F, Gherardi G, Dupuis ML, Romagnoli G et al. Interferon-gamma up-regulates expression and activity of P-glycoprotein in human peripheral blood monocyte-derived macrophages. Lab Invest. 1999; 79: 1299–309.
   PubMed Web of Science ®Google Scholar
• Fu D, Roufogalis BD. Actin disruption inhibits endosomal traffic of P-glycoprotein-EGFP and resistance to daunorubicin accumulation. Am J Physiol Cell Physiol. 2007; 292: C1543–52.
   PubMed Web of Science ®Google Scholar
• Brambilla D, Zamboni S, Federici C, Lugini L, Lozupone F, Milito AD et al. P-glycoprotein binds to ezrin at amino acid residues 149–242 in the FERM domain and plays a key role in the multidrug resistance of human osteosarcoma. Int J Cancer. 2012; 130: 2824–34.
   Web of Science ®Google Scholar
• Birch M, Mitchell S, Hart IR. Isolation and characterization of human melanoma cell variants expressing high and low levels of CD44. Cancer Res. 1991; 51: 6660–7.
   PubMed Web of Science ®Google Scholar
• Bartolazzi A, Peach R, Aruffo A, Stamenkovic I. Interaction between CD44 and hyaluronate is directly implicated in the regulation of tumor development. J Exp Med. 1994; 180: 53–66.
   PubMed Web of Science ®Google Scholar
• Legg JW, Isacke CM. Identification and functional analysis of the ezrin-binding site in the hyaluronan receptor, CD44. Curr Biol. 1998; 8: 705–8.
   PubMed Web of Science ®Google Scholar
• Colone M, Calcabrini A, Toccacieli L, Bozzuto G, Stringaro A, Gentile M et al. The multidrug transporter P-glycoprotein: a mediator of melanoma invasion?. J Invest Dermatol. 2007; 128: 957–71.
   Web of Science ®Google Scholar
• Jaiswal R, Raymond Grau GE, Bebawy M. Cellular communication via microparticles: role in transfer of multidrug resistance in cancer. Future Oncol. 2014; 10: 655–69.
   Web of Science ®Google Scholar
• Mizejewski GJ. Role of integrins in cancer: survey of expression patterns. Proc Soc Exp Biol Med. 1999; 222: 124–38.
   PubMed Web of Science ®Google Scholar
• Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002; 110: 673–87.
   PubMed Web of Science ®Google Scholar
• Montanez E, Ussar S, Schifferer M, Bösl M, Zent R, Moser M et al. Kindlin-2 controls bidirectional signaling of integrins. Genes Dev. 2008; 22: 1325–30.
   PubMed Web of Science ®Google Scholar
• Saiki I, Yoneda J, Azuma I, Fujii H, Abe F, Nakajima M et al. Role of aminopeptidase N (CD13) in tumor-cell invasion and extracellular matrix degradationm. Int J Cancer. 1993; 54: 137–43.
   PubMed Web of Science ®Google Scholar