Microparticles and their emerging role in cancer multidrug resistance

Cancer Treatment Reviews

Volumn 38, Issue 3, 2012, Pages 226-234

  Gong, J ^a   Jaiswal, R ^a   Mathys, J M ^b   Combes, V ^a   Grau, G E R ^a   Bebawy, M ^c  

^a University of Sydney   (Australia)

^b ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^c UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

Cancer; Intercellular transfer; Microparticles; Multidrug resistance; Multidrug Resistance Associated Protein 1; P glycoprotein

Indexed keywords

ABC TRANSPORTER; ANTINEOPLASTIC AGENT; BIRICODAR; CELL ADHESION MOLECULE; CYCLOSPORIN; DACTINOMYCIN; DAUNORUBICIN; DOXORUBICIN; ETOPOSIDE; GLYCOPROTEIN P; GLYCOPROTEIN P INHIBITOR; MICRORNA; MULTIDRUG RESISTANCE PROTEIN 1; PACLITAXEL; TENIPOSIDE; VINBLASTINE; VINCRISTINE; ZOSUQUIDAR;

ANGIOGENESIS; CANCER CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER RELAPSE; CANCER SURVIVAL; CELL INTERACTION; GENE AMPLIFICATION; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HYDROPHILICITY; HYDROPHOBICITY; IMMUNOSURVEILLANCE; MEMBRANE MICROPARTICLE; MOLECULARLY TARGETED THERAPY; MULTIDRUG RESISTANCE; NEOPLASM; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; REVIEW; RNA STABILITY; TRANSCRIPTION REGULATION; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; TUMOR VOLUME;

EID: 84855379514     PISSN: 03057372     EISSN: 15321967     Source Type: Journal    
DOI: 10.1016/j.ctrv.2011.06.005     Document Type: Review

References (135)

1. Luqmani Y.A. Mechanisms of drug resistance in cancer chemotherapy. Med Princ Pract 2005, 14(Suppl 1):35-48.
2. Lage H. An overview of cancer multidrug resistance: a still unsolved problem. Cell Mol Life Sci 2008, 65:3145-3167.
3. Callaghan R., Crowley E., Potter S., Kerr I.D. P-glycoprotein: so many ways to turn it on. J Clin Pharm 2008, 48:365-378.
4. Gottesman M.M. Mechanisms of cancer drug resistance. Annu Rev Med 2002, 53:615-627.
5. Lehnert M. Clinical multidrug resistance in cancer: a multifactorial problem. Eur J Cancer 1996, 32A:912-920.
6. Hilton J. Role of aldehyde dehydrogenase in cyclophosphamide-resistant L1210 leukemia. Cancer Res 1984, 44:5156-5160.
7. Andersson B.S., Mroue M., Britten R.A., Murray D. The role of DNA damage in the resistance of human chronic myeloid leukemia cells to cyclophosphamide analogues. Cancer Res 1994, 54:5394-5400.
8. Simon S.M., Schindler M. Cell biological mechanisms of multidrug resistance in tumors. Proc Natl Acad Sci U S A 1994, 91:3497-3504.
9. Lowe S.W., Ruley H.E., Jacks T., Housman D.E. P53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 1993, 74:957-967.
10. Biedler J.L., Riehm H. Cellular resistance to actinomycin D in Chinese hamster cells in vitro: cross-resistance, radioautographic, and cytogenetic studies. Cancer Res 1970, 30:1174-1184.
11. Pearce H.L., Safa A.R., Bach N.J., Winter M.A., Cirtain M.C., Beck W.T. Essential features of the P-glycoprotein pharmacophore as defined by a series of reserpine analogs that modulate multidrug resistance. Proc Natl Acad Sci U S A 1989, 86(13):5128-5132.
12. Ak Y., Demirel G., Gülbas Z. MDR1, MRP1 and LRP expression in patients with untreated acute leukaemia: correlation with 99mTc-MIBI bone marrow scintigraphy. Nucl Med Commun 2007, 28(7):541-546.
13. Bebawy M., Morris M.B., Roufogalis B.D. A continuous fluorescence assay for the study of P-glycoprotein-mediated drug efflux using inside-out membrane vesicles. Anal Biochem 1999, 268:270-277.
14. Damiani D., Michelutti A., Michieli M., et al. P-glycoprotein, lung resistance-related protein and multidrug resistance-associated protein in de novo adult acute lymphoblastic leukaemia. Br J Haematol 2002, 116(3):519-527.
15. Juszczyński P., Niewiarowski W., Krykowski E., Robak T., Warzocha K. Expression of the multidrug resistance-associated protein (mrp) gene in chronic lymphocytic leukemia. Leuk Lymphoma 2002, 43(1):153-158.
16. Lee C.H. Reversing agents for ATP-binding cassette (ABC) transporters: application in modulating multidrug resistance (MDR). Curr Med Chem 2004, 4:43-52.
17. Tatusov R.L., Koonin E.V., Lipman D.J. A genomic perspective on protein families. Science 1997, 278(5338):631-637.
18. Higgins C.F. ABC transporters: from microorganisms to man. Annu Rev Cell Biol 1992, 8:67-113.
19. van Veen H.W., Konings W.N. Multidrug transporters from bacteria to man: similarities in structure and function. Semin Cancer Biol 1997, 8(3):183-191.
20. Wilson C.M., Serrano A.E., Wasley A., Bogenschutz M.P., Shankar A.H., Wirth D.F. Amplification of a gene related to mammalian mdr genes in drug-resistant Plasmodium falciparum. Science 1989, 244(4909):1184-1186.
21. Descoteaux S., Ayala P., Orozco E., Samuelson J. Primary sequences of two P-glycoprotein genes of Entamoeba histolytica. Mol Biochem Parasitol 1992, 54(2):201-211.
22. Henderson D.M., Sifri C.D., Rodgers M., Wirth D.F., Hendrickson N., Ullman B. Multidrug resistance in Leishmania donovani is conferred by amplification of a gene homologous to the mammalian mdr1 gene. Mol Cell Biol 1992, 12(6):2855-2865.
23. Prasad R., De Wergifosse P., Goffeau A., Balzi E. Molecular cloning and characterization of a novel gene of Candida albicans, CDR1, conferring multiple resistance to drugs and antifungals. Curr Genet 1995, 27(4):320-329.
24. Tusnády G.E., Bakos E., Váradi A., Sarkadi B. Membrane topology distinguishes a subfamily of the ATP-binding cassette (ABC) transporters. FEBS Lett 1997, 402(1):1-3.
25. Li Z.S., Lu Y.P., Zhen R.G., Szczypka M., Thiele D.J., Rea P.A. A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato)cadmium. Proc Natl Acad Sci U S A 1997, 94(1):42-47.
26. Cui Z., Hirata D., Tsuchiya E., Osada H., Miyakawa T. The multidrug resistance-associated protein (MRP) subfamily (Yrs1/Yor1) of Saccharomyces cerevisiae is important for the tolerance to a broad range of organic anions. J Biol Chem 1996, 271(25):14712-14716.
27. Callahan H.L., Beverley S.M. Heavy metal resistance: a new role for P-glycoproteins in Leishmania. J Biol Chem 1991, 266(28):18427-18430.
28. Grondin K., Haimeur A., Mukhopadhyay R., Rosen B.P., Ouellette M. Co-amplification of the gamma-glutamylcysteine synthetase gene gsh1 and of the ABC transporter gene pgpA in arsenite-resistant Leishmania tarentolae. EMBO J 1997, 16(11):3057-3065.
29. Broeks A., Gerrard B., Allikmets R., Dean M., Plasterk R.H. Homologues of the human multidrug resistance genes MRP and MDR contribute to heavy metal resistance in the soil nematode Caenorhabditis elegans. EMBO J 1996, 15(22):6132-6143.
30. van Veen H.W., Callaghan R., Soceneantu L., Sardini A., Konings W.N., Higgins C.F. A bacterial antibiotic-resistance gene that complements the human multidrug-resistance P-glycoprotein gene. Nature 1998, 391(6664):291-295.
31. Balram C., Sharma A., Sivathasan C., Lee E.J.D. Frequency of C3435T single nucleotide MDR1 genetic polymorphism in an Asian population: phenotypic-genotypic correlates. Br J Clin Pharmacol 2003, 56:78-83.
32. Loscher W., Potschka H. Drug resistance in brain diseases and the role of drug efflux transporters. Nat Rev Neurosci 2005, 6:591-602.
33. Willingham M.C., Richert N.D., Cornwell M.M., Tsuruo T., Hamada H., Gottesman M.M., et al. Immunocytochemical localization of P170 at the plasma membrane of multidrug-resistant human cells. J Histochem Cytochem 1987, 35(12):1451-1456.
34. Molinari A., Cianfriglia M., Meschini S., Calcabrini A., Arancia G. P-glycoprotein expression in the Golgi apparatus of multidrug-resistant cells. Int J Cancer 1994, 59(6):789-795.
35. Ling H.E., Guo-Qing L.I.U. Interaction of multidrug resistance reversal agents with P-glycoprotein ATPase activity on the blood-brain barrier. Acta Pharmacol Sin 2002, 21(5):423-429.
36. Bart J., Groen H.J., Hendrikse N.H., van der Graaf W.T., Vaalburg W., de Vries E.G. The blood-brain barrier and oncology: new insights into function and modulation. Cancer Treat Rev 2000, 26(6):449-462.
37. Zochbauer S., Gsur A., Brunner R., Kyrle P.A., Lechner K., Pirker R. P-glycoprotein expression as unfavorable prognostic factor in acute myeloid leukemia. Leukemia 1994, 8(6):974-977.
38. Marie J.P., Zittoun R., Sikic B.I. Multidrug resistance (mdr1) gene expression in adult acute leukemias: correlations with treatment outcome and in vitro drug sensitivity. Blood 1991, 78(3):586-592.
39. Pirker R., Wallner J., Geissler K., et al. MDR1 gene expression and treatment outcome in acute myeloid leukemia. J Natl Cancer Inst 1991, 83(10):708-712.
40. Sato H., Preisler H., Day R., et al. MDR1 transcript levels as an indication of resistant disease in acute myelogenous leukaemia. Br J Haematol 1990, 75(3):340-345.
41. Leith C.P., Kopecky K.J., Chen I.M., et al. Frequency and clinical significance of the expression of the multidrug resistance proteins MDR1/P-glycoprotein, MRP1, and LRP in acute myeloid leukemia: a Southwest Oncology Group Study. Blood 1999, 94(3):1086-1099.
42. Leith C.P., Kopecky K.J., Godwin J., et al. Acute myeloid leukemia in the elderly: assessment of multidrug resistance (MDR1) and cytogenetics distinguishes biologic subgroups with remarkably distinct responses to standard chemotherapy. A Southwest Oncology Group study. Blood 1997, 89(9):3323-3329.
43. Goasguen J.E., Dossot J.M., Fardel O., et al. Expression of the multidrug resistance-associated P-glycoprotein (P-170) in 59 cases of de novo acute lymphoblastic leukemia: prognostic implications. Blood 1993, 81(9):2394-2398.
44. Chan H.S., Thorner P.S., Haddad G., Ling V. Immunohistochemical detection of P-glycoprotein: prognostic correlation in soft tissue sarcoma of childhood. J Clin Oncol 1990, 8(4):689-704.
45. Chan H.S., Haddad G., Thorner P.S., et al. P-glycoprotein expression as a predictor of the outcome of therapy for neuroblastoma. N Engl J Med 1991, 325(23):1608-1614.
46. Baldini N., Scotlandi K., Barbanti-Brodano G., et al. Expression of P-glycoprotein in high-grade osteosarcomas in relation to clinical outcome. N Engl J Med 1995, 333(21):1380-1385.
47. Linn S.C., Giaccone G., van Diest P.J., et al. Prognostic relevance of P-glycoprotein expression in breast cancer. Ann Oncol 1995, 6(7):679-685.
48. Gong Y.P., Liu T., Jia Y.Q., Qin L., Deng C.Q., Yang R.Y.O. Comparison of Pgp- and MRP-mediated multidrug resistance in leukemia cell lines. Int J Hematol 2002, 75:154-160.
49. Versantvoort C.H., Broxterman H.J., Pinedo H.M. Energy dependent processes involved in reduced drug accumulation in multidrug resistant human lung cancer cell lines without P-glycoprotein expression. Cancer Res 1992, 52:17-23.
50. Doubre H., Césari D., Mairovitz A., et al. Multidrug resistance-associated protein (MRP1) is overexpressed in DNA aneuploid carcinomatous cells in non-small cell lung cancer (NSCLC). Int J Cancer 2005, 113:568-574.
51. Munoz M., Henderson M., Haber M., Norris M. Role of the MRP1/ABCC1 Multidrug Transporter Protein in Cancer. IUBMB Life 2007, 59:752-757.
52. Zaman G.J., Flens M.J., van Leusden M.R., et al. The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc Natl Acad Sci USA 1994, 91:8822-8826.
53. Evers R., Zaman G.J., van Deemter L., et al. Basolateral localization and export activity of the human multidrug resistance-associated protein in polarized pig kidney cells. J Clin Invest 1996, 97:1211-1218.
54. Leslie E.M., Deeley R.G., Cole S.P. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 2005, 204:216-237.
55. Wright S.R., Boag A.H., Valdimarsson G., et al. Immunohistochemical detection of multidrug resistance protein in human lung cancer and normal lung. Clin Cancer Res 1998, 4:2279-2289.
56. Almquist K.C., Loe D.W., Hipfner D.R., Mackie J.E., Cole S.P., Deeley R.G. Characterization of the M(r) 190, 000 multidrug resistance protein (MRP) in drug-selected and transfected human tumor cell. Cancer Res 1995, 55:102-110.
57. Rajagopal A., Simon S.M. Subcellular localization and activity of multidrug resistance proteins. Mol Biol Cell 2003, 14:3389-3399.
58. Gennuso F., Fernetti C., Tirolo C., et al. Bilirubin protects astrocytes from its own toxicity by inducing up-regulation and translocation of multidrug esistanceassociated protein 1 (Mrp1). Proc Natl Acad Sci USA 2004, 101:2470-2475.
59. Van Luyn M.J., Muller M., Renes J., et al. Transport of glutathione conjugates into secretory vesicles is mediated by the multidrug-resistance protein 1. Int J Cancer 1998, 76:55-62.
60. Hsia T.C., Shen Y.Y., Yen R.F., Kao C.H., Changlai S.P. Comparing whole body 18F-2-deoxyglucose positron emission tomography and technetium-99m methylene diophosphate bone scan to detect bone metastases in patients with non-small cell lung cancer. Neoplasma 2002, 49(4):267-271.
61. Nooter K., de la Riviere G.B., Klijn J., Stoter G., Foekens J. Multidrug resistance protein in recurrent breast cancer. Lancet 1997, 349(9069):1885-1886.
62. Sullivan G.F., Amenta P.S., Villanueva J.D., Alvarez C.J., Yang J.M., Hait W.N. The expression of drug resistance gene products during the progression of human prostate cancer. Clin Cancer Res 1998, 4(6):1393-1403.
63. Norris M.D., Bordow S.B., Marshall G.M., Haber P.S., Cohn S.L., Haber M. Expression of the gene for multidrug-resistance-associated protein and outcome in patients with neuroblastoma. N Engl J Med 1996, 334(4):231-238.
64. Childs S., Ling V. The MDR superfamily of genes and its biological implications. Important Adv Oncol 1994, 21-36.
65. Fardel O., Lecureur V., Guillouzo A. The P-glycoprotein multidrug transporter. Gen Pharmacol 1996, 27:1283-1291.
66. Sharom F.J. The P-glycoprotein efflux pump: how does it transport drugs?. J Membr Biol 1997, 160:161-175.
67. Riordan J.R., Deuchars K., Kartner N., Alon N., Trent J., Ling V. Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines. Nature 1985, 316:817-819.
68. Shen D.W., Fojo A., Chin J.E., et al. Human multidrug-resistant cell lines: increased mdr1 expression can precede gene amplification. Science 1986, 232:643-645.
69. Gottesman M.M., Hrycyna C.A., Schoenlein P.V., Germann U.A., Pastan I. Genetic analysis of the multidrug transporter. Annu Rev Genet 1995, 29:607-649.
70. Labialle S., Gayet L., Marthinet E., Rigal D., Baggetto L.G. Transcriptional regulators of the human multidrug resistance 1 gene: recent views. Biochem Pharmacol 2002, 64:943-948.
71. Bakos E., Homolya L. Portrait of multifaceted transporter, the multidrug resistance-associated protein 1 (MRP1/ABCC1). Pflügers Archiv Eur J Physiol 2007, 453(5):621-641.
72. Jin J., Wang F.P., Wei H., Liu G. Reversal of multidrug resistance of cancer through inhibition of P-glycoprotein by 5-bromotetrandrine. Cancer Chemother Pharmacol 2005, 55(2):179-188.
73. Berger W., Setinek U., Hollaus P., et al. Multidrug resistance markers P-glycoprotein, multidrug resistance protein 1, and lung resistance protein in non-small cell lung cancer: prognostic implications. J Cancer Res Clin Oncol 2005, 131(6):355-363.
74. Benyahia B., Huguet S., Declèves X., et al. Multidrug resistance-associated protein MRP1expression in human gliomas: chemosensitization to vincristine and etoposide by indomethacin in human glioma cell lines overexpressing MRP1. J Neurooncol 2004, 66(1-2):65-70.
75. Pérez-Tomás R. Multidrug resistance: retrospect and prospects in anti-cancer drug treatment. Curr Med Chem 2006, 13(16):1859-1876.
76. Régina A., Demeule M., Laplante A., et al. Multidrug resistance in brain tumors: roles of the blood-brain barrier. Cancer Metastasis Rev 2001, 20(1-2):13-25.
77. Tsuruo T., Hamada H., Sato S., Heike Y. Inhibition of multidrug-resistant human tumor growth in athymic mice by anti-P-glycoprotein monoclonal antibodies. Jpn J Cancer Res 1989, 80:627-631.
78. Twentyman P.R. Transport proteins in drug resistance: biology and approaches to circumvention. J Intern Med Suppl 1997, 740:133-137.
79. Sikic B.I. Pharmacologic approaches to reversing multidrug resistance. Semin Hematol 1997, 34:40-47.
80. Sikic B.I., Fisher G.A., Lum B.L., Halsey J., Beketic-Oreskovic L., Chen G. Modulation and prevention of multidrug resistance by inhibitors of P-glycoprotein. Cancer Chemother Pharmacol 1997, 40(Suppl):S9-S13.
81. Szakacs G., Paterson J.K., Ludwig J.A., Booth-Genthe C., Gottesman M.M. Targeting multidrug resistance in cancer. Nat Rev Drug Discov 2006, 5:219-234.
82. Ruff P., Vorobiof D.A., Jordaan J.P., et al. A randomized, placebo-controlled, double-blind phase 2 study of docetaxel compared to docetaxel plus zosuquidar (LY335979) in women with metastatic or locally recurrent breast cancer who have received one prior chemotherapy regimen. Cancer Chemother Pharmacol 2009, 64(4):763-768.
83. Sharom F.J. ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics 2008, 9(1):105-127.
84. Wang S., Ryder H., Pretswell I., et al. Studies on quinazolinones as dual inhibitors of Pgp and MRP1 in multidrug resistance. Bioorg Med Chem Lett 2002, 12(4):571-574.
85. Watkins S.C., Salter R.D. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 2005, 23(3):309-318.
86. Darland D.C., D'Amore P.A. Cell-cell interactions in vascular development. Curr Top Dev Biol 2001, 52:107-149.
87. Levchenko A., Mehta B.M., Niu X., et al. Intercellular transfer of P-glycoprotein mediates acquired multidrug resistance in tumor cells. Proc Natl Acad Sci U S A 2005, 102:1933-1938.
88. Mack M., Kleinschmidt A., Bruhl H., 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(7):769-775.
89. Coltel N., Combes V., Wassmer S.C., Chimini G., Grau G.E. Cell vesiculation and immunopathology: implications in cerebral malaria. Microbes Infect 2006, 8(8):2305-2316.
90. Smalley D.M., Root K.E., Cho H., Ross M.M., Ley K. Proteomic discovery of 21 proteins expressed in human plasma-derived but not platelet-derived microparticles. Thromb Haemost 2007, 97(1):67-80.
91. Combes V., Coltel N., Alibert M., et al. ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology. Am J Pathol 2005, 166(1):295-302.
92. Pankoui-Mfonkeu J.B., Gouado I., Fotso Kuaté H., et al. Elevated cell-specific microparticles are a biological marker for cerebral dysfunctions in human severe malaria. PLoS ONE 2010, 5(10):e13415.
93. Freyssinet J.M. Cellular microparticles: what are they bad or good for?. J Thromb Haemost 2003, 1(7):1655-1662.
94. Burnier L., Fontana P., Kwak B.R., Angelillo-Scherrer A. Cell-derived microparticles in haemostasis and vascular medicine. Thromb Haemost 2009, 101:439-451.
95. Beyer C., Pisetsky D.S. The role of microparticles in the pathogenesis of rheumatic diseases. Nat Rev 2010, 6:21-29.
96. Daleke D.L. Regulation of transbilayer plasma membrane phospholipid asymmetry. J Lipid Res 2003, 44:233-242.
97. Coltel N., Combes V., Wassmer S.C., Chimini G., Grau G.E. Cell vesiculation and immunopathology: implications in cerebral malaria. Microbes Infect 2006, 8(8):2305-2316.
98. Combes V., El-Assaad F., Faille D., Jambou R., Hunt N.H., Grau G.E. Microvesiculation and cell interactions at the brain-endothelial interface in cerebral malaria pathogenesis. Prog Neurobiol 2010, 91(2):140-151.
99. Horstman L.L., Ahn Y.S. Platelet microparticles: a wide-angle perspective. Crit Rev Oncol Hematol 1999, 30:111-142.
100. George J.N., Thoi L.L., McManus L.M., Reimann T.A. Isolation of human platelet membrane microparticles from plasma and serum. Blood 1982, 60:834-840.
101. Burnier L., Fontana P., Kwak B.R., Angelillo-Scherrer A. Cell-derived microparticles in haemostasis and vascular medicine. Thromb Haemost 2009, 101:439-451.
102. Nomura S., Ozaki Y., Ikeda Y. Function and role of microparticles in various clinical settings. Thromb Res 2008, 123:8-23.
103. Ginestra A., Monea S., Seghezzi G., et al. Urokinase plasminogen activator and gelatinases are associated with membrane vesicles shed by human HT1080 fibrosarcoma cells. J Biol Chem 1997, 272(27):17216-17222.
104. Dolo V., D'Ascenzo S., Violini S., et al. Matrix-degrading proteinases are shed in membrane vesicles by ovarian cancer cells in vivo and in vitro. Clin Exp Metastasis 1999, 17:131-140.
105. Kim C.W., Lee H.M., Lee T.H., Kang C., Kleinman H.K., Gho Y.S. Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res 2002, 62:6312-6317.
106. Angelucci A., D'Ascenzo S., Festuccia C., et al. Vesicle-associated urokinase plasminogen activator promotes invasion in prostate cancer cell lines. Clin Exp Metastasis 2000, 18:163-170.
107. Dvorak H.F., Van DeWater L., Bitzer A.M., et al. Procoagulant activity associated with plasma membrane vesicles shed by cultured tumor cells. Cancer Res 1983, 43:4434-4442.
108. Distler J.H., Huber L.C., Gay S., Distler O., Pisetsky D.S. Microparticles as mediators of cellular cross-talk in inflammatory disease. Autoimmunity 2006, 39(8):683-690.
109. Bebawy M., Combes V., Lee E., et al. Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells. Leukemia 2009, 23(9):1643-1649.
110. Lane J.D., Allan V.J., Woodman P.G. Active relocation of chromatin and endoplasmic reticulum into blebs in late apoptotic cells. J Cell Sci 2005, 118(Pt 17):4059-4071.
111. Schiller M., Bekeredjian-Ding I., Heyder P., Blank N., Ho A.D., Lorenz H.M. Autoantigens are translocated into small apoptotic bodies during early stages of apoptosis. Cell Death Differ 2008, 15(1):183-191.
112. Reich C.F., Pisetsky D.S. The content of DNA and RNA in microparticles released by Jurkat and HL-60 cells undergoing in vitro apoptosis. Exp Cell Res 2009, 315(5):760-768.
113. Ng E.K., Tsui N.B., Lam N.Y., et al. Presence of filterable and nonfilterable mRNA in the plasma of cancer patients and healthy individuals. Clin Chem 2002, 48(8):1212-1217.
114. El-Hefnawy T., Raja S., Kelly L., et al. Characterization of amplifiable, circulating RNA in plasma and its potential as a tool for cancer diagnostics. Clin Chem 2004, 50(3):564-573.
115. Zhao Y., Srivastava D. A developmental view of microRNA function. Trends Biochem Sci 2007, 32(4):189-197.
116. Griffiths-Jones S. The microRNA Registry. Nucleic Acids Res 2004, 32:D109-11. [Database issue].
117. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120(1):15-20.
118. Schickel R., Boyerinas B., Park S.M., Peter M.E. MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene 2008, 27(45):5959-5974.
119. Tsang W.P., Kwok T.T. Let-7a microRNA suppresses therapeutics-induced cancer cell death by targeting caspase-3. Apoptosis 2008, 13(10):1215-1222.
120. Si M.L., Zhu S., Wu H., Lu Z., Wu F., Mo Y.Y. MiR-21-mediated tumor growth. Oncogene 2007, 26(19):2799-2803.
121. Mishra P.J., Humeniuk R., Longo-Sorbello G.S., Banerjee D., Bertino J.R. A miR-24 microRNA binding-site polymorphism in dihydrofolate reductase gene leads to methotrexate resistance. Proc Natl Acad Sci U S A 2007, 104(33):13513-13518.
122. Yang H., Kong W., He L., et al. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res 2008, 68(2):425-433.
123. Kovalchuk O., Filkowski J., Meservy J., et al. Involvement of microRNA-451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin. Mol Cancer Ther 2008, 7(7):2152-2159.
124. Pogribney I.P., Filkowski J.N., Tryndyak V.P., Golubov A., Shpyleva S.I., Kovalchuk O. Alterations of microRNAs and their targets are associated with acquired resistance of MCF-7 breast cancer cells to cisplatin. Int J Cancer 2010, 127(8):1785-1794.
125. Zhu H., Wu H., Liu X., et al. Role of MicroRNA miR-27a and miR-451 in the regulation of MDR1/P-glycoprotein expression in human cancer cells. Biochem Pharmacol 2008, 76(5):582-588.
126. Liang Z., Wu H., Xia J., et al. Involvement of miR-326 in chemotherapy resistance of breast cancer through modulating expression of multidrug resistance-associated protein 1. Biochem Pharmacol 2010, 79(6):817-824.
127. Hunter M.P., Ismail N., Zhang X., et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE 2008, 3(11):e3694.
128. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007, 9(6):654-659.
129. Yuan A., Farber E.L., Rapoport A.L., et al. Transfer of microRNAs by embryonic stem cell microvesicles. PLoS ONE 2009, 4(3):e4722.
130. Perron M.P., Provost P. Protein components of the microRNA pathway and human diseases. Methods Mol Biol 2009, 487:369-385.
131. Jinek M., Doudna J.A. A three-dimensional view of the molecular machinery of RNA interference. Nature 2009, 457(7228):405-412.
132. Nelson K.M., Weiss G.J. MicroRNAs and cancer: past, present, and potential future. Mol Cancer Ther 2008, 7(12):3655-3660.
133. Bebawy M., Morris M.B., Roufogalis B.D. Selective modulation of P-glycoprotein-mediated drug resistance. Br J Cancer 2001, 85:1998-2003.
134. Wassmer S.C., Cianciolo G.J., Combes V., Grau G.E. Inhibition of endothelial activation: a new way to treat cerebral malaria?. PLoS Med 2005, 2(9):e245.
135. Penet M.F., Abou-Hamdan M., Coltel N., et al. Protection against cerebral malaria by the low-molecular-weight thiol pantethine. Proc Natl Acad Sci U S A 2008, 105(4):1321-1326.