Cell-derived microparticles: New targets in the therapeutic management of disease

Journal of Pharmacy and Pharmaceutical Sciences

Volumn 16, Issue 2, 2013, Pages 238-253

  Roseblade, Ariane ^a   Luk, Frederick ^a   Rawling, Tristan ^a   Ung, Alison ^a   Grau, Georges E R ^b   Bebawy, Mary ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ALLICIN; ALOXISTATIN; BENIDIPINE; CALCIMYCIN; CALPASTATIN; CALPEPTIN; CYSTAMINE; LMP 420; ME2TS; NIFEDIPINE; PANTETHINE; PHOSPHOLIPID; PR2TS; TICLOPIDINE; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; UNCLASSIFIED DRUG; [1 [(1 FORMYL 2 PHENYLETHYL)CARBAMOYL] 2 METHYLPROPYL]CARBAMIC ACID BENZYL ESTER;

APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; BRAIN MALARIA; CELL COMMUNICATION; CELL DISRUPTION; CELL SURVIVAL; CYTOSKELETON; DIABETES MELLITUS; ENDOCRINE FUNCTION; ENZYME ACTIVITY; EXOSOME; GAP JUNCTION; HOMEOSTASIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MEMBRANE MICROPARTICLE; METABOLIC REGULATION; MULTIDRUG RESISTANCE; NEOPLASM; PATHOGENESIS; PHENOTYPE; SCOTT SYNDROME; SIGNAL TRANSDUCTION;

ANIMALS; BLOOD COAGULATION DISORDERS; CELL-DERIVED MICROPARTICLES; DIABETES MELLITUS; DRUG RESISTANCE, NEOPLASM; HIV INFECTIONS; HUMANS; MALARIA, CEREBRAL; NEOPLASMS;

EID: 84890204562     PISSN: None     EISSN: 14821826     Source Type: Journal    
DOI: 10.18433/j3989x     Document Type: Article

References (145)

1. Deatherage BL, Cookson BT. Membrane Vesicle Release in Bacteria, Eukaryotes, and Archaea: a Conserved yet Underappreciated Aspect of Microbial Life. Infection and immunity. 2012;80(6):1948-57.
2. György B, Szabó TG, Pásztói M, Pál Z, Misják P, Aradi B, et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cellular and molecular life sciences. 2011;68(16):2667-88.
3. 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(4):e61515.
4. Jaiswal R, Luk F, Gong J, Mathys JM, Grau GER, Bebawy M. Microparticle conferred microRNA profiles-implications in the transfer and dominance of cancer traits. Molecular cancer. 2012;11(1):37-48.
5. Jimenez JJ, Jy W, Mauro LM, Soderland C, Horstman LL, Ahn YS. Endothelial cells release phenotypically and quantitatively distinct microparticles in activation and apoptosis. Thrombosis Research. 2003;109(4):175-80.
6. Gutiérrez-Vázquez C, Villarroya-Beltri C, Mittelbrunn M, Sánchez-Madrid F. Transfer of extracellular vesicles during immune cell-cell interactions. Immunological Reviews. 2013;251(1):125-42.
7. Wolf P. The nature and significance of platelet products in human plasma. British journal of haematology. 1967;13(3):269-88.
8. Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nature Reviews Immunology. 2009;9(8):581-93.
9. Morel O, Jesel L, Freyssinet JM, Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arteriosclerosis, thrombosis, and vascular biology. 2011;31(1):15-26.
10. Antonyak MA, Li B, Boroughs LK, Johnson JL, Druso JE, Bryant KL, et al. Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proceedings of the National Academy of Sciences. 2011;108(12):4852-7.
11. Leroyer A, Tedgui A, Boulanger C. Role of microparticles in atherothrombosis. Journal of internal medicine. 2008;263(5):528-37.
12. Boilard E, Nigrovic PA, Larabee K, Watts GF, Coblyn JS, Weinblatt ME, et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science Signaling. 2010;327(5965):580-3.
13. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated Platelets Release Two Types of Membrane Vesicles: Microvesicles by Surface Shedding and Exosomes Derived From Exocytosis of Multivesicular Bodies and ∝- Granules. Blood. 1999;94(11):3791-9.
14. Doeuvre L, Plawinski L, Toti F, Anglés-Cano E. Cell-derived microparticles: a new challenge in neuroscience. Journal of Neurochemistry. 2009;110(2):457-68.
15. Morel O, Toti F, Hugel B, Bakouboula B, Camoin-Jau L, Dignat-George F, et al. Procoagulant Microparticles Disrupting the Vascular Homeostasis Equation? Arteriosclerosis, thrombosis, and vascular biology. 2006;26(12):2594-604.
16. Pilzer D, Gasser O, Moskovich O, Schifferli JA, Fishelson Z. Emission of membrane vesicles: roles in complement resistance, immunity and cancer. Springer seminars in immunopathology. 2005;27(3):375-87.
17. Morel O, Toti F, Hugel B, Freyssinet JM. Cellular microparticles: a disseminated storage pool of bioactive vascular effectors. Current opinion in hematology. 2004;11(3):156-64.
18. Leroyer AS, Anfosso F, Lacroix R, Sabatier F, Simoncini S, Njock SM, et al. Endothelialderived microparticles: Biological conveyors at the crossroad of inflammation, thrombosis and angiogenesis. Thrombosis & Haemostasis. 2010;104(3):456-63.
19. Higgins CF. ABC transporters: from microorganisms to man. Annual review of cell biology. 1992;8(1):67-113.
20. Mack M, Kleinschmidt A, Bruhl 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. Nature medicine. 2000;6(7):769-75.
21. Distler JHW, Huber LC, Gay S, Distler O, Pisetsky DS. Microparticles as mediators of cellular cross-talk in inflammatory disease. Autoimmunity. 2006;39(8):683-90.
22. Furie B, Furie BC. Mechanisms of thrombus formation. New England Journal of Medicine. 2008;359(9):938-49.
23. 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(9):1643-9.
24. Zahra S, Anderson JAM, Stirling D, Ludlam CA. Microparticles, malignancy and thrombosis. British journal of haematology. 2011;152(6):688-700.
25. Hristov M, Erl W, Linder S, Weber PC. Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro. Blood. 2004;104(9):2761-6.
26. Elmore S. Apoptosis: a review of programmed cell death. Toxicologic pathology. 2007;35(4):495-516.
27. Savill J, Dransfield I, Gregory C, Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nature Reviews Immunology. 2002;2(12):965-75.
28. Holmgren L, Szeles A, Rajnavölgyi E, Folkman J, Klein G, Ernberg I, et al. Horizontal transfer of DNA by the uptake of apoptotic bodies. Blood. 1999;93(11):3956-63.
29. Bergsmedh A, Szeles A, Henriksson M, Bratt A, Folkman MJ, Spetz A-L, et al. Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proceedings of the National Academy of Sciences. 2001;98(11):6407-11.
30. Azevedo LCP. Microparticles and Exosomes: Are They Part of Important Pathways in Sepsis Pathophysiology? Fernandez R, editor: In Tech; 2012. 155-67 p.
31. Beyer C, Pisetsky DS. The role of microparticles in the pathogenesis of rheumatic diseases. Nature Reviews Rheumatology. 2009;6(1):21-9.
32. Henson PM, Bratton DL, Fadok VA. Apoptotic cell removal. Current Biology. 2001;11(19):R795-R805.
33. Coltel N, Combes V, Wassmer SC, Chimini G, Grau GE. Cell vesiculation and immunopathology: implications in cerebral malaria. Microbes and infection. 2006;8(8):2305-16.
34. Hurley JH, Boura E, Carlson L-A, Rózycki B. Membrane budding. Cell. 2010;143(6):875-87.
35. Vidal M, Sainte-Marie J, Philippot JR, Bienvenue A. Asymmetric distribution of phospholipids in the membrane of vesicles released during in vitro maturation of guinea pig reticulocytes: Evidence precluding a role for "aminophospholipid translocase". Journal of Cellular Physiology. 1989;140(3):455-62.
36. Deregibus MC, Cantaluppi V, Calogero R, Iacono ML, Tetta C, Biancone L, et al. Endothelial progenitor cell-derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood. 2007;110(7):2440-8.
37. 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. Nature cell biology. 2007;9(6):654-9.
38. Al-Nedawi K, Meehan B, Rak J. Microvesicles: messengers and mediators of tumor progression. Cell Cycle. 2009;8(13):2014-8.
39. Prado N, Marazuela EG, Segura E, Fernández- García H, Villalba M, Théry C, et al. Exosomes from bronchoalveolar fluid of tolerized mice prevent allergic reaction. The Journal of immunology. 2008;181(2):1519-25.
40. Andre F, Schartz NE, Movassagh M, Flament C, Pautier P, Morice P, et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet. 2002;360(9329):295-305.
41. Admyre C, Johansson SM, Qazi KR, Filén J-J, Lahesmaa R, Norman M, et al. Exosomes with immune modulatory features are present in human breast milk. The Journal of immunology. 2007;179(3):1969-78.
42. Pisitkun T, Shen R-F, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(36):13368-73.
43. Caby M-P, Lankar D, Vincendeau-Scherrer C, Raposo G, Bonnerot C. Exosomal-like vesicles are present in human blood plasma. International immunology. 2005;17(7):879-87.
44. Dignat-George F, Boulanger CM. The many faces of endothelial microparticles. Arteriosclerosis, thrombosis, and vascular biology. 2011;31(1):27-33.
45. Montoro-García S, Shantsila E, Marín F, Blann A, Lip GYH. Circulating microparticles: new insights into the biochemical basis of microparticle release and activity. Basic research in cardiology. 2011;106(6):911-23.
46. Zwaal R, Comfurius P, Bevers E. Surface exposure of phosphatidylserine in pathological cells. Cellular and molecular life sciences. 2005;62(9):971-88.
47. Freyssinet JM. Cellular microparticles: what are they bad or good for? Journal of Thrombosis and Haemostasis. 2003;1(7):1655-62.
48. VanWijk MJ, VanBavel E, Sturk A, Nieuwland R. Microparticles in cardiovascular diseases. Cardiovascular research. 2003;59(2):277-87.
49. Combes V, Simon AC, Grau GE, Arnoux D, Camoin L, Sabatier F, et al. In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. Journal of Clinical Investigation. 1999;104(1):93-102.
50. Sapet C, Simoncini S, Loriod B, Puthier D, Sampol J, Nguyen C, et al. Thrombin-induced endothelial microparticle generation: identification of a novel pathway involving ROCK-II activation by caspase-2. Blood. 2006;108(6):1868-76.
51. Szotowski B, Antoniak S, Goldin-Lang P, Tran Q-V, Pels K, Rosenthal P, et al. Antioxidative treatment inhibits the release of thrombogenic tissue factor from irradiation-and cytokineinduced endothelial cells. Cardiovascular research. 2007;73(4):806-12.
52. Comfurius P, Senden JMG, Tilly RHJ, Schroit AJ, Bevers EM, Zwaal RFA. Loss of membrane phospholipid asymmetry in platelets and red cells may be associated with calcium-induced shedding of plasma membrane and inhibition of aminophospholipid translocase. Biochimica et Biophysica Acta (BBA)-Biomembranes. 1990;1026(2):153-60.
53. Dachary-Prigent J, Pasquet JM, Freyssinet JM, Nurden AT. Calcium involvement in aminophospholipid exposure and microparticle formation during platelet activation: a study using Ca2+-ATPase inhibitors. Biochemistry. 1995;34(36):11625-34.
54. Smeets EF, Comfurius P, Bevers EM, Zwaal RF. Calcium-induced transbilayer scrambling of fluorescent phospholipid analogs in platelets and erythrocytes. Biochimica et Biophysica Acta (BBA)-Biomembranes. 1994;1195(2):281-6.
55. Piccin A, Murphy WG, Smith OP. Circulating microparticles: pathophysiology and clinical implications. Blood reviews. 2007;21(3):157-71.
56. Freyssinet JM, Toti F. Formation of procoagulant microparticles and properties. Thromb Res. 2010;125 Suppl 1(0):S46-8.
57. Burnier L, Fontana P, Kwak BR, Angelillo- Scherrer A. Cell-derived microparticles in haemostasis and vascular medicine. Thromb Haemost. 2009;101(3):439-51.
58. Hugel B, Martínez MC, Kunzelmann C, Freyssinet JM. Membrane microparticles: two sides of the coin. Physiology. 2005;20(1):22-7.
59. Baron M, Boulanger CM, Staels B, Tailleux A. Cell-derived microparticles in atherosclerosis: biomarkers and targets for pharmacological modulation? Journal of Cellular and Molecular Medicine. 2012;16(7):1365-76.
60. Bevers EM, Comfurius P, Dekkers DWC, Zwaal RFA. Lipid translocation across the plasma membrane of mammalian cells. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids. 1999;1439(3):317-30.
61. Chang C-P, Zhao J, Wiedmer T, Sims P. Contribution of platelet microparticle formation and granule secretion to the transmembrane migration of phosphatidylserine. Journal of Biological Chemistry. 1993;268(10):7171-8.
62. Manno S, Takakuwa Y, Mohandas N. Identification of a functional role for lipid asymmetry in biological membranes: Phosphatidylserine-skeletal protein interactions modulate membrane stability. Proceedings of the National Academy of Sciences. 2002;99(4):1943-8.
63. Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF. Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nature cell biology. 2001;3(4):339-45.
64. Bukowska A, Lendeckel U, Bode-Böger SM, Goette A. Physiologic and pathophysiologic role of calpain: implications for the occurrence of atrial fibrillation. Cardiovascular therapeutics. 2012;30(3):e115-e27.
65. Chakraborti S, Alam MN, Paik D, Shaikh S, Chakraborti T. Implications of calpains in health and diseases. Indian J Biochem Biophys. 2012;49(5):316-28.
66. Hanna RA, Campbell RL, Davies PL. Calciumbound structure of calpain and its mechanism of inhibition by calpastatin. Nature. 2008;456(7220):409-12.
67. Fox J, Austin C, Reynolds C, Steffen P. Evidence that agonist-induced activation of calpain causes the shedding of procoagulant-containing microvesicles from the membrane of aggregating platelets. Journal of Biological Chemistry. 1991;266(20):13289-95.
68. Pasquet JM, Dachary-Prigent J, Nurden AT. Calcium influx is a determining factor of calpain activation and microparticle formation in platelets. European Journal of Biochemistry. 1996;239(3):647-54.
69. Carragher N. Calpain inhibition: a therapeutic strategy targeting multiple disease states. Current pharmaceutical design. 2006;12(5):615-38.
70. Randriamboavonjy V, Fleming I. All cut up! The consequences of calpain activation on platelet function. Vascular Pharmacology. 2012;56(5- 6):201-15.
71. Perrin B, Huttenlocher A. Calpain. The international journal of biochemistry & cell biology. 2002;34(7):722-5.
72. Storr SJ, Carragher NO, Frame MC, Parr T, Martin SG. The calpain system and cancer. Nature Reviews Cancer. 2011;11(5):364-74.
73. Morel O, Morel N, Freyssinet JM, Toti F. Platelet microparticles and vascular cells interactions: a checkpoint between the haemostatic and thrombotic responses. Platelets. 2008;19(1):9-23.
74. Mostefai H, Andriantsitohaina R, Martinez M. Plasma membrane microparticles in angiogenesis: role in ischemic diseases and in cancer. Physiological research. 2008;57(3):311-20.
75. Müller I, Klocke A, Alex M, Kotzsch M, Luther T, Morgenstern E, et al. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. The FASEB Journal. 2003;17(3):476-8.
76. Hrachovinová I, Cambien B, Hafezi-Moghadam A, Kappelmayer J, Camphausen RT, Widom A, et al. Interaction of P-selectin and PSGL-1 generates microparticles that correct hemostasis in a mouse model of hemophilia A. Nature medicine. 2003;9(8):1020-5.
77. Satta N, Freyssinet J-M, Toti F. The significance of human monocyte thrombomodulin during membrane vesiculation and after stimulation by lipopolysaccharide. British journal of haematology. 1997;96(3):534-42.
78. Pérez-Casal M, Downey C, Fukudome K, Marx G, Toh CH. Activated protein C induces the release of microparticle-associated endothelial protein C receptor. Blood. 2005;105(4):1515-22.
79. Lacroix R, Sabatier F, Mialhe A, Basire A, Pannell R, Borghi H, et al. Activation of plasminogen into plasmin at the surface of endothelial microparticles: a mechanism that modulates angiogenic properties of endothelial progenitor cells in vitro. Blood. 2007;110(7):2432-9.
80. Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One. 2008;3(11):e3694.
81. Fauci AS. Host factors and the pathogenesis of HIV-induced disease. Nature. 1996;384(6609):529-34.
82. WHO. Diabetes. 2011 [cited 2013]; Available from: http://www.who.int/mediacentre/factsheets/fs312 /en/print.html.
83. Nomura S, Takahashi N, Inami N, Kajiura T, Yamada K, Nakamori H, et al. Probucol and ticlopidine: effect on platelet and monocyte activation markers in hyperlipidemic patients with and without type 2 diabetes. Atherosclerosis. 2004;174(2):329-35.
84. WHO. Malaria Fact sheet N°94 2013 [cited 2013 16 May 2013]; Available from: http://www.who.int/mediacentre/factsheets/fs094/en/index.html.
85. van der Heyde HC, Nolan J, Combes V, Gramaglia I, Grau GE. A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to microcirculatory dysfunction. Trends in parasitology. 2006;22(11):503-8.
86. Penet MF, Abou-Hamdan M, Coltel N, Cornille E, Grau GE, De Reggi M, et al. Protection against cerebral malaria by the low-molecularweight thiol pantethine. Proceedings of the National Academy of Sciences. 2008;105(4):1321-6.
87. Schofield L, Grau GE. Immunological processes in malaria pathogenesis. Nature Reviews Immunology. 2005;5(9):722-35.
88. Mfonkeu JBP, Gouado I, Kuaté HF, Zambou O, Zollo PHA, Grau GER, et al. Elevated cellspecific microparticles are a biological marker for cerebral dysfunctions in human severe malaria. PLoS One. 2010;5(10):e13415.
89. Combes V, Coltel N, Alibert M, Van Eck M, Raymond C, Juhan-Vague I, et al. ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology. The American journal of pathology. 2005;166(1):295-302.
90. Combes V, El-Assaad F, Faille D, Jambou R, Hunt NH, Grau GER. Microvesiculation and cell interactions at the brain-endothelial interface in cerebral malaria pathogenesis. Progress in neurobiology. 2010;91(2):140-51.
91. Wassmer SC, Combes V, Grau GER. Platelets and microparticles in cerebral malaria: the unusual suspects. Drug Discovery Today: Disease Mechanisms. 2011;8(1-2):e15-e23.
92. Friend C, Marovitz W, Henle G, Henle W, Tsuei D, Hirschhorn K, et al. Observations on cell lines derived from a patient with Hodgkin's disease. Cancer Research. 1978;38(8):2581-91.
93. Van Doormaal F, Kleinjan A, Di Nisio M, Büller H, Nieuwland R. Cell-derived microvesicles and cancer. Neth J Med. 2009;67(7):266-73.
94. Furie B, Furie BC. Thrombus formation in vivo. Journal of Clinical Investigation. 2005;115(12):3355-62.
95. Kim H, Song K, Park Y, Kang Y, Lee Y, Lee K, et al. Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor. European Journal of Cancer. 2003;39(2):184-91.
96. Abid Hussein MN, Boing AN, Sturk A, Hau CM, Nieuwland R. Inhibition of microparticle release triggers endothelial cell apoptosis and detachment. Thromb Haemost. 2007;98(5):1096-107.
97. Inal JM, Ansa-Addo EA, Stratton D, Kholia S, Antwi-Baffour SS, Jorfi S, et al. Microvesicles in health and disease. Archivum immunologiae et therapiae experimentalis. 2012:1-15.
98. Graves LE, Ariztia EV, Navari JR, Matzel HJ, Stack MS, Fishman DA. Proinvasive properties of ovarian cancer ascites-derived membrane vesicles. Cancer Research. 2004;64(19):7045-9.
99. Rak J, Guha A. Extracellular vesicles-vehicles that spread cancer genes. Bioessays. 2012;34(6):489-97.
100. Jaiswal R, Gong J, Sambasivam S, Combes V, Mathys J-M, Davey R, et al. Microparticleassociated nucleic acids mediate trait dominance in cancer. The FASEB Journal. 2012;26(1):420-9.
101. Gong J, Jaiswal R, Mathys JM, Combes V, Grau G, Bebawy M. Microparticles and their emerging role in cancer multidrug resistance. Cancer treatment reviews. 2012;38(3):226-34.
102. Zaman G, Flens M, Van Leusden M, De Haas M, Mülder H, Lankelma J, et al. The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proceedings of the National Academy of Sciences. 1994;91(19):8822-6.
103. Sharom FJ. ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics. 2008;9(1):105-27.
104. Gong YP, Liu T, Jia YQ, Qin L, Deng CQ, Yang RYO. Comparison of Pgp-and MRP-mediated multidrug resistance in leukemia cell lines. International journal of hematology. 2002;75(2):154-60.
105. Pasquier J, Galas L, Boulangé-Lecomte C, Rioult D, Bultelle F, Magal P, et al. Different Modalities of Intercellular Membrane Exchanges Mediate Cell-to-cell P-glycoprotein Transfers in MCF-7 Breast Cancer Cells. Journal of Biological Chemistry. 2012;287(10):7374-87.
106. Longo-Sorbello G, Bertino JR. Current understanding of methotrexate pharmacology and efficacy in acute leukemias. Use of newer antifolates in clinical trials. haematologica. 2001;86(2):121-7.
107. Lage H. An overview of cancer multidrug resistance: A still unsolved problem. Cellular and molecular life sciences. 2008;65(20):3145-67.
108. Ganapathi R, Grabowski D, Turinic R, Valenzuela R. Correlation between potency of calmodulin inhibitors and effects on cellular levels and cytotoxic activity of doxorubicin (adriamycin) in resistant P388 mouse leukemia cells. European Journal of Cancer and Clinical Oncology. 1984;20(6):799-806.
109. Hollt V, Kouba M, Dietel M, Vogt G. Stereoisomers of calcium antagonists which differ markedly in their potencies as calcium blockers are equally effective in modulating drug transport by P-glycoprotein. Biochemical Pharmacology. 1992;43(12):2601-8.
110. Tsuruo T, Iida H, Tsukagoshi S, Sakurai Y. Overcoming of vincristine resistance in P388 leukemia in vivo and in vitro through enhanced cytotoxicity of vincristine and vinblastine by verapamil. Cancer Research. 1981;41(5):1967-72.
111. Nooter K, Oostrum R, Deurloo J. Effects of verapamil on the pharmacokinetics of daunomycin in the rat. Cancer chemotherapy and pharmacology. 1987;20(2):176-8.
112. Ozols RF, Cunnion RE, Klecker Jr RW, Hamilton TC, Ostchega Y, Parrillo JE, et al. Verapamil and adriamycin in the treatment of drug-resistant ovarian cancer patients. Journal of Clinical Oncology. 1987;5(4):641-7.
113. Gottesman MM, Pastan I, Ambudkar SV. Pglycoprotein and multidrug resistance. Current opinion in genetics & development. 1996;6(5):610-7.
114. Gottesman MM. Mechanisms of cancer drug resistance. Annual review of medicine. 2002;53(1):615-27.
115. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. Nanotubular highways for intercellular organelle transport. Science. 2004;303(5660):1007-10.
116. 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. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(6):1933-8.
117. Barteneva NS, Fasler-Kan E, Bernimoulin M, Stern JN, Ponomarev ED, Duckett L, et al. Circulating microparticles: square the circle. BMC Cell Biol. 2013;14(1):23.
118. Donkor IO. Calpain inhibitors: a survey of compounds reported in the patent and scientific literature. Expert opinion on therapeutic patents. 2011;21(5):601-36.
119. Rendu F, Brohard-Bohn B, Pain S, Bachelot- Loza C, Auger J. Thiosulfinates inhibit platelet aggregation and microparticle shedding at a calpain-dependent step. THROMBOSIS AND HAEMOSTASIS-STUTTGART-. 2001;86(5):1284-91.
120. Sorimachi H, Ishiura S, Suzuki K. Structure and physiological function of calpains. Biochemical Journal. 1997;328(Pt 3):721-32.
121. Harbeson SL, Abelleira SM, Akiyama A, Barrett III R, Carroll RM, Straub JA, et al. Stereospecific Synthesis of Peptidyl. alpha.-Keto Amides as Inhibitors of Calpain. Journal of Medicinal Chemistry. 1994;37(18):2918-29.
122. Li Z, Ortega-Vilain A-C, Patil GS, Chu D-L, Foreman J, Eveleth DD, et al. Novel peptidyl α- keto amide inhibitors of calpains and other cysteine proteases. Journal of Medicinal Chemistry. 1996;39(20):4089-98.
123. Tamai M, Hanada K, Adachi T, Oguma K, Kashiwagi K, Omura S, et al. Papain inhibitions by optically active E-64 analogs. J Biochem. 1981;90(1):255-7.
124. Giordano C, Gallina C, Consalvi V, Scandurra R. Irreversible inactivation of papain and cathepsin B by epoxidic substrate analogues. European journal of medicinal chemistry. 1990;25(6):479-87.
125. Sugita H, Ishiura S, Suzuki K, Imahori K. Inhibition of epoxide derivatives on chicken calcium-activated neutral protease (CANP) in vitro and in vivo. J Biochem. 1980;87(1):339-41.
126. Shirasaki Y, Nakamura M, Yamaguchi M, Miyashita H, Sakai O, Inoue J. Exploration of orally available calpain inhibitors 2: peptidyl hemiacetal derivatives. Journal of Medicinal Chemistry. 2006;49(13):3926-32.
127. Donkor I. A survey of calpain inhibitors. Current Medicinal Chemistry. 2000;7(12):1171-88.
128. Inoue J, Nakamura M, Cui Y-S, Sakai Y, Sakai O, Hill JR, et al. Structure-activity relationship study and drug profile of N-(4- fluorophenylsulfonyl)-L-valyl-L-leucinal (SJA6017) as a potent calpain inhibitor. Journal of Medicinal Chemistry. 2003;46(5):868-71.
129. Todd B, Moore D, Deivanayagam C, Lin G-d, Chattopadhyay D, Maki M, et al. A structural model for the inhibition of calpain by calpastatin: crystal structures of the native domain VI of calpain and its complexes with calpastatin peptide and a small molecule inhibitor. Journal of molecular biology. 2003;328(1):131-46.
130. Wang KK, Nath R, Posner A, Raser KJ, Buroker- Kilgore M, Hajimohammadreza I, et al. An alpha-mercaptoacrylic acid derivative is a selective nonpeptide cell-permeable calpain inhibitor and is neuroprotective. Proc Natl Acad Sci U S A. 1996;93(13):6687-92.
131. Croce K, Flaumenhaft R, Rivers M, Furie B, Furie BC, Herman IM, et al. Inhibition of calpain blocks platelet secretion, aggregation, and spreading. Journal of Biological Chemistry. 1999;274(51):36321-7.
132. Fox J, Reynolds CC, Austin CD. The role of calpain in stimulus-response coupling: evidence that calpain mediates agonist-induced expression of procoagulant activity in platelets. Blood. 1990;76(12):2510-9.
133. Goll DE, Thompson VF, Li H, Wei W, CONG J. The calpain system. Physiological reviews. 2003;83(3):731-801.
134. Badol P, David-Dufilho M, Auger J, Whiteheart SW, Rendu F. Thiosulfinates modulate platelet activation by reaction with surface free sulfhydryls and internal thiol-containing proteins. Platelets. 2007;18(7):481-90.
135. Kendler BS. Garlic (Allium sativum) and onion (Allium cepa): A review of their relationship to cardiovascular disease. Preventive medicine. 1987;16(5):670-85.
136. Lee YJ, Jy W, Horstman LL, Janania J, Reyes Y, Kelley RE, et al. Elevated platelet microparticles in transient ischemic attacks, lacunar infarcts, and multiinfarct dementias. Thrombosis Research. 1993;72(4):295-304.
137. Nomura S, Ozaki Y, Ikeda Y. Function and role of microparticles in various clinical settings. Thrombosis Research. 2008;123(1):8-23.
138. Nomura S, Inami N, Kimura Y, Omoto S, Shouzu A, Nishikawa M, et al. Effect of nifedipine on adiponectin in hypertensive patients with type 2 diabetes mellitus. Journal of human hypertension. 2006;21(1):38-44.
139. Nomura S, Shouzu A, Omoto S, Nishikawa M, Iwasaka T. Benidipine improves oxidized LDLdependent monocyte and endothelial dysfunction in hypertensive patients with type 2 diabetes mellitus. Journal of human hypertension. 2005;19(7):551-7.
140. Robinson RA, Worfolk L, Tracy P. Endotoxin enhances the expression of monocyte prothrombinase activity. Blood. 1992;79(2):406-16.
141. Shouzu A, Nomura S, Omoto S, Hayakawa T, Nishikawa M, Iwasaka T. Effect of ticlopidine on monocyte-derived microparticles and activated platelet markers in diabetes mellitus. Clinical and Applied Thrombosis/Hemostasis. 2004;10(2):167-73.
142. Wassmer SC, Cianciolo GJ, Combes V, Grau GE. Inhibition of endothelial activation: a new way to treat cerebral malaria? PLoS medicine. 2005;2(9):e245.
143. Antonyak MA, Wilson KF, Cerione RA. R(h)oads to microvesicles. Small GTPases. 2012;3(4):219-24.
144. Morgan-Fisher M, Wewer UM, Yoneda A. Regulation of ROCK activity in cancer. J Histochem Cytochem. 2013;61(3):185-98.
145. Liao JK, Seto M, Noma K. Rho kinase (ROCK) inhibitors. J Cardiovasc Pharmacol. 2007;50(1):17-24.