Platelet microparticles infiltrating solid tumors transfer miRNAs that suppress tumor growth

Blood

Volumn 130, Issue 5, 2017, Pages 567-580

  Michael, James V ^a   Wurtzel, Jeremy G T ^a   Mao, Guang Fen ^a   Rao, A Koneti ^a   Kolpakov, Mikhail A ^a   Sabri, Abdelkarim ^a   Hoffman, Nicholas E ^a   Rajan, Sudarsan ^a   Tomar, Dhanendra ^a   Madesh, Muniswamy ^a   Nieman, Marvin T ^b   Yu, Johnny ^c,d   Edelstein, Leonard C ^c,d   Rowley, Jesse W ^e   Weyrich, Andrew S ^e   Goldfinger, Lawrence E ^a,f  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c THOMAS JEFFERSON UNIVERSITY HOSPITAL   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

^e UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^f FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 24; SMALL NUCLEOLAR RNA; MIRN24 MICRORNA, MOUSE; NADH DEHYDROGENASE SUBUNIT 2, MOUSE; PROTEASE-ACTIVATED RECEPTOR 4, MOUSE; PROTEINASE ACTIVATED RECEPTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; TUMOR PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; BLOOD VESSEL PERMEABILITY; CANCER INHIBITION; CELL INFILTRATION; CELL INTERACTION; CELL LYSATE; COLON CARCINOMA; DNA LIBRARY; ENZYME INHIBITION; EX VIVO STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE MICROPARTICLE; MOUSE; NIH 3T3 CELL LINE; NONHUMAN; OUTCOME ASSESSMENT; PLATELET MICROPARTICLE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSPORT; SOLID MALIGNANT NEOPLASM; TUMOR CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; ANIMAL; COLONIC NEOPLASMS; GENETICS; LUNG NEOPLASMS; METABOLISM; METASTASIS; PATHOLOGY; THROMBOCYTE; TRANSPLANTATION;

ANIMALS; BLOOD PLATELETS; CELL-DERIVED MICROPARTICLES; COLONIC NEOPLASMS; HUMANS; LUNG NEOPLASMS; MICE; MICRORNAS; NADH DEHYDROGENASE; NEOPLASM METASTASIS; NEOPLASM PROTEINS; RECEPTORS, PROTEINASE-ACTIVATED;

EID: 85026750320     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-11-751099     Document Type: Article

References (105)

1. Gasic GJ, Gasic TB, Stewart CC. Antimetastatic effects associated with platelet reduction. Proc Natl Acad Sci USA. 1968;61:46-52.
2. Camerer E, Qazi AA, Duong DN, Cornelissen I, Advincula R, Coughlin SR. Platelets, proteaseactivated receptors, and fibrinogen in hematogenous metastasis. Blood. 2004; 104(2):397-401.
3. Kim YJ, Borsig L, Varki NM, Varki A. P-selectin deficiency attenuates tumor growth and metastasis. Proc Natl Acad Sci USA. 1998; 95(16):9325-9330.
4. Labelle M, Begum S, Hynes RO. Platelets guide the formation of early metastatic niches. Proc Natl Acad Sci USA. 2014;111(30): E3053-E3061.
5. Gay LJ, Felding-Habermann B. Platelets alter tumor cell attributes to propel metastasis: programming in transit. Cancer Cell. 2011; 20(5):553-554.
6. Gay LJ, Felding-Habermann B. Contribution of platelets to tumour metastasis. Nat Rev Cancer. 2011;11(2):123-134.
7. Sabrkhany S, Griffioen AW, Oude Egbrink MG. The role of blood platelets in tumor angiogenesis. Biochim Biophys Acta. 2011;1815(2):189-196.
8. Bambace NM, Holmes CE. The platelet contribution to cancer progression. J Thromb Haemost. 2011;9(2):237-249.
9. Stone RL, Nick AM, McNeish IA, et al. Paraneoplastic thrombocytosis in ovarian cancer [published correction appears in N Engl J Med. 2012;367(18):1768]. N Engl J Med. 2012;366(7): 610-618.
10. Buergy D, Wenz F, Groden C, Brockmann MA. Tumor-platelet interaction in solid tumors. Int J Cancer. 2012;130(12):2747-2760.
11. Cho MS, Bottsford-Miller J, Vasquez HG, et al. Platelets increase the proliferation of ovarian cancer cells. Blood. 2012;120(24):4869-4872.
12. Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol. 1967; 13(3):269-288.
13. Horstman LL, Ahn YS. Platelet microparticles: a wide-angle perspective. Crit Rev Oncol Hematol. 1999;30(2):111-142.
14. VanWijk MJ, VanBavel E, Sturk A, Nieuwland R. Microparticles in cardiovascular diseases. Cardiovasc Res. 2003;59(2):277-287.
15. Rao AK, Rao DA. Platelets signal and tumors take off. Blood. 2012;120(24):4667-4668.
16. Varon D, Shai E. Role of platelet-derived microparticles in angiogenesis and tumor progression. Discov Med. 2009;8(43):237-241.
17. Hunter MP, Ismail N, Zhang X, et al. Detection of microRNA expression in human peripheral blood microvesicles [published correction appears in PLoS One. 2010;5(3)]. PLoS One. 2008;3(11): e3694.
18. Landry P, Plante I, Ouellet DL, Perron MP, Rousseau G, Provost P. Existence of a microRNA pathway in anucleate platelets. Nat Struct Mol Biol. 2009;16(9):961-966.
19. Diehl P, Fricke A, Sander L, et al. Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc Res. 2012;93(4): 633-644.
20. Edelstein LC, McKenzie SE, Shaw C, Holinstat MA, Kunapuli SP, Bray PF. MicroRNAs in platelet production and activation. J Thromb Haemost. 2013;11(suppl 1):340-350.
21. Willeit P, Zampetaki A, Dudek K, et al. Circulating microRNAs as novel biomarkers for platelet activation. Circ Res. 2013;112(4): 595-600.
22. Risitano A, Beaulieu LM, Vitseva O, Freedman JE. Platelets and platelet-like particles mediate intercellular RNA transfer. Blood. 2012;119(26): 6288-6295.
23. Laffont B, Corduan A, Plé H, et al. Activated platelets can deliver mRNA regulatory Ago2·microRNA complexes to endothelial cells via microparticles. Blood. 2013;122(2):253-261.
24. Liang H, Yan X, Pan Y, et al. MicroRNA-223 delivered by platelet-derived microvesicles promotes lung cancer cell invasion via targeting tumor suppressor EPB41L3. Mol Cancer. 2015; 14(1):58.
25. Chen Z, Ma T, Huang C, Hu T, Li J. The pivotal role of microRNA-155 in the control of cancer. J Cell Physiol. 2014;229(5):545-550.
26. Haneklaus M, Gerlic M, O'Neill LA, Masters SL. miR-223: infection, inflammation and cancer. J Intern Med. 2013;274(3):215-226.
27. He JF, Luo YM, Wan XH, Jiang D. Biogenesis of MiRNA-195 and its role in biogenesis, the cell cycle, and apoptosis. J Biochem Mol Toxicol. 2011;25(6):404-408.
28. Jurkovicova D, Magyerkova M, Kulcsar L, et al. miR-155 as a diagnostic and prognostic marker in hematological and solid malignancies. Neoplasma. 2014;61(3):241-251.
29. Li XL, Jones MF, Subramanian M, Lal A. Mutant p53 exerts oncogenic effects through microRNAs and their target gene networks. FEBS Lett. 2014;588(16):2610-2615.
30. van Jaarsveld MT, Helleman J, Berns EM, Wiemer EA. MicroRNAs in ovarian cancer biology and therapy resistance. Int J Biochem Cell Biol. 2010;42(8):1282-1290.
31. Vimalraj S, Miranda PJ, Ramyakrishna B, Selvamurugan N. Regulation of breast cancer and bone metastasis by microRNAs. Dis Markers. 2013;35(5):369-387.
32. Gao Y, Liu Y, Du L, et al. Down-regulation of miR-24-3p in colorectal cancer is associated with malignant behavior. Med Oncol. 2015;32(1):362.
33. Listing H, Mardin WA, Wohlfromm S, Mees ST, Haier J. MiR-23a/-24-induced gene silencing results in mesothelial cell integration of pancreatic cancer. Br J Cancer. 2015;112(1): 131-139.
34. Pan B, Chen Y, Song H, Xu Y, Wang R, Chen L. Mir-24-3p downregulation contributes to VP16-DDP resistance in small-cell lung cancer by targeting ATG4A. Oncotarget. 2015;6(1): 317-331.
35. Goto Y, Kojima S, Nishikawa R, et al. The microRNA-23b/27b/24-1 cluster is a disease progression marker and tumor suppressor in prostate cancer. Oncotarget. 2014;5(17): 7748-7759.
36. Inoguchi S, Seki N, Chiyomaru T, et al. Tumoursuppressive microRNA-24-1 inhibits cancer cell proliferation through targeting FOXM1 in bladder cancer. FEBS Lett. 2014;588(17):3170-3179.
37. Sochor M, Basova P, Pesta M, et al. Oncogenic microRNAs: miR-155, miR-19a, miR-181b, and miR-24 enable monitoring of early breast cancer in serum. BMC Cancer. 2014;14:448.
38. Duan Y, Hu L, Liu B, et al. Tumor suppressor miR-24 restrains gastric cancer progression by downregulating RegIV. Mol Cancer. 2014;13: 127.
39. Ma Y, She XG, Ming YZ, Wan QQ. miR-24 promotes the proliferation and invasion of HCC cells by targeting SOX7. Tumour Biol. 2014; 35(11):10731-10736.
40. Martin EC, Elliott S, Rhodes LV, et al. Preferential star strand biogenesis of pre-miR-24-2 targets PKC-alpha and suppresses cell survival in MCF-7 breast cancer cells. Mol Carcinog. 2014;53(1):38-48.
41. Yin JY, Tang Q, Qian W, et al. Increased expression of miR-24 is associated with acute myeloid leukemia with t(8;21). Int J Clin Exp Pathol. 2014;7(11):8032-8038.
42. Giglio S, Cirombella R, Amodeo R, Portaro L, Lavra L, Vecchione A. MicroRNA miR-24 promotes cell proliferation by targeting the CDKs inhibitors p27Kip1 and p16INK4a. J Cell Physiol. 2013;228(10):2015-2023.
43. Du WW, Fang L, Li M, et al. MicroRNA miR-24 enhances tumor invasion and metastasis by targeting PTPN9 and PTPRF to promote EGF signaling. J Cell Sci. 2013;126(Pt 6):1440-1453.
44. Katoh M. Cardio-miRNAs and onco-miRNAs: circulating miRNA-based diagnostics for noncancerous and cancerous diseases. Front Cell Dev Biol. 2014;2:61.
45. Mironova N, Patutina O, Brenner E, Kurilshikov A, Vlassov V, Zenkova M. MicroRNA drop in the bloodstream and microRNA boost in the tumour caused by treatment with ribonuclease A leads to an attenuation of tumour malignancy. PLoS One. 2013;8(12):e83482.
46. Pl é H, Landry P, Benham A, Coarfa C, Gunaratne PH, Provost P. The repertoire and features of human platelet microRNAs. PLoS One. 2012;7(12):e50746.
47. Michael JV, Wurtzel JGT, Goldfinger LE. Regulation of H-Ras-driven MAPK signaling, transformation and tumorigenesis, but not PI3K signaling and tumor progression, by plasma membrane microdomains. Oncogenesis. 2016; 5(5):e228.
48. Grosswendt S, Filipchyk A, Manzano M, et al. Unambiguous identification of miRNA:target site interactions by different types of ligation reactions. Mol Cell. 2014;54(6):1042-1054.
49. Gidlof O, van der Brug M, Ohman J, et al. Platelets activated during myocardial infarction release functional miRNA, which can be taken up by endothelial cells and regulate ICAM1 expression. Blood. 2013;121(19):3908-3917.
50. Baluk P, Hashizume H, McDonald DM. Cellular abnormalities of blood vessels as targets in cancer. Curr Opin Genet Dev. 2005;15(1): 102-111.
51. Mezouar S, Mege D, Darbousset R, et al. Involvement of platelet-derived microparticles in tumor progression and thrombosis. Semin Oncol. 2014;41(3):346-358.
52. Horstman LL, Jy W, Jimenez JJ, Bidot C, Ahn YS. New horizons in the analysis of circulating cell-derived microparticles. Keio J Med. 2004; 53(4):210-230.
53. Mause SF, Weber C. Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ Res. 2010;107(9):1047-1057.
54. Salanova B, Choi M, Rolle S, Wellner M, Luft FC, Kettritz R. Beta2-integrins and acquired glycoprotein IIb/IIIa (GPIIb/IIIa) receptors cooperate in NF-kappaB activation of human neutrophils. J Biol Chem. 2007;282(38): 27960-27969.
55. Lee S, Wurtzel JG, Singhal SS, Awasthi S, Goldfinger LE. RALBP1/RLIP76 depletion in mice suppresses tumor growth by inhibiting tumor neovascularization. Cancer Res. 2012; 72(20):5165-5173.
56. Rásó E, Tóv ari J, Tóth K, et al. Ectopic alphaIIbbeta3 integrin signaling involves 12-lipoxygenase-and PKC-mediated serine phosphorylation events in melanoma cells. Thromb Haemost. 2001;85(6):1037-1042.
57. Puerschel WC, Gawaz M, Worret WI, Ring J. Immunoreactivity of glycoprotein IIb is present in metastasized but not in non-metastasized primary malignant melanoma. Br J Dermatol. 1996;135(6):883-887.
58. Timar J, Trikha M, Szekeres K, Bazaz R, Honn K. Expression and function of the high affinity alphaIIbbeta3 integrin in murine melanoma cells. Clin Exp Metastasis. 1998;16(5):437-445.
59. Trikha M, Raso E, Cai Y, et al. Role of alphaII(b) beta3 integrin in prostate cancer metastasis. Prostate. 1998;35(3):185-192.
60. Michael JV, Wurtzel JG, Goldfinger LE. Inhibition of galectin-1 sensitizes HRAS-driven tumor growth to rapamycin treatment. Anticancer Res. 2016;36(10):5053-5061.
61. Misaki R, Morimatsu M, Uemura T, et al. Palmitoylated Ras proteins traffic through recycling endosomes to the plasma membrane during exocytosis. J Cell Biol. 2010;191(1): 23-29.
62. Wurtzel JG, Kumar P, Goldfinger LE. Palmitoylation regulates vesicular trafficking of R-Ras to membrane ruffles and effects on ruffling and cell spreading. Small GTPases. 2012;3(3):139-153.
63. Popov EG, Mejlumian AG, Gavrilov IYu, Gabbasov ZA, Pozin EYa. Evaluation of the ability of intact platelets to accumulate acridine orange. Experientia. 1988;44(7):616-618.
64. Hong W, Kondkar AA, Nagalla S, et al. Transfection of human platelets with short interfering RNA. Clin Transl Sci. 2011;4(3): 180-182.
65. Yu F, Jia X, Du F, et al. miR-155-deficient bone marrow promotes tumor metastasis. Mol Cancer Res. 2013;11(8):923-936.
66. Finnerty JR, Wang WX, Hébert SS, Wilfred BR, Mao G, Nelson PT. The miR-15/107 group of microRNA genes: evolutionary biology, cellular functions, and roles in human diseases. J Mol Biol. 2010;402(3):491-509.
67. Yang Y, Li M, Chang S, et al. MicroRNA-195 acts as a tumor suppressor by directly targeting Wnt3a in HepG2 hepatocellular carcinoma cells. Mol Med Rep. 2014;10(5):2643-2648.
68. Gay L, Miller MR, Ventura PB, et al. Mouse TU tagging: a chemical/genetic intersectional method for purifying cell type-specific nascent RNA. Genes Dev. 2013;27(1):98-115.
69. Obad S, dos Santos CO, Petri A, et al. Silencing of microRNA families by seed-targeting tiny LNAs. Nat Genet. 2011;43(4):371-378.
70. Cohen Z, Gonzales RF, Davis-Gorman GF, Copeland JG, McDonagh PF. Thrombin activity and platelet microparticle formation are increased in type 2 diabetic platelets: a potential correlation with caspase activation. Thromb Res. 2002;107(5):217-221.
71. Melki I, Tessandier N, Zufferey A, Boilard E. Platelet microvesicles in health and disease. Platelets. 2017;28(3):214-221.
72. Duvernay M, Young S, Gailani D, Schoenecker J, Hamm HE. Protease-activated receptor (PAR) 1 and PAR4 differentially regulate factor V expression from human platelets [published correction appears in Mol Pharmacol. 2013; 84(3):487]. Mol Pharmacol. 2013;83(4):781-792.
73. Telonis AG, Loher P, Jing Y, Londin E, Rigoutsos I. Beyond the one-locus-one-miRNA paradigm: microRNA isoforms enable deeper insights into breast cancer heterogeneity. Nucleic Acids Res. 2015;43(19):9158-9175.
74. Zhao H, Ardelt B, Ardelt W, Shogen K, Darzynkiewicz Z. The cytotoxic ribonuclease onconase targets RNA interference (siRNA). Cell Cycle. 2008;7(20):3258-3261.
75. Sikand K, Singh J, Ebron JS, Shukla GC. Housekeeping gene selection advisory: glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and b-actin are targets of miR-644a. PLoS One. 2012;7(10):e47510.
76. Bray PF, McKenzie SE, Edelstein LC, et al. The complex transcriptional landscape of the anucleate human platelet. BMC Genomics. 2013;14:1.
77. Bai B, Liu H, Laiho M. Small RNA expression and deep sequencing analyses of the nucleolus reveal the presence of nucleolus-associated microRNAs. FEBS Open Bio. 2014;4:441-449.
78. Bandiera S, Matégot R, Girard M, Demongeot J, Henrion-Caude A. MitomiRs delineating the intracellular localization of microRNAs at mitochondria. Free Radic Biol Med. 2013;64: 12-19.
79. Gusdon AM, Votyakova TV, Mathews CE. mt-Nd2a suppresses reactive oxygen species production by mitochondrial complexes I and III. J Biol Chem. 2008;283(16):10690-10697.
80. Yao Z, Jones AW, Fassone E, et al. PGC-1b mediates adaptive chemoresistance associated with mitochondrial DNA mutations. Oncogene. 2013;32(20):2592-2600.
81. Reininger AJ, Heijnen HF, Schumann H, Specht HM, Schramm W, Ruggeri ZM. Mechanism of platelet adhesion to von Willebrand factor and microparticle formation under high shear stress. Blood. 2006;107(9):3537-3545.
82. Schmidtke DW, Diamond SL. Direct observation of membrane tethers formed during neutrophil attachment to platelets or P-selectin under physiological flow. J Cell Biol. 2000;149(3): 719-730.
83. Kim R, Emi M, Tanabe K. Cancer cell immune escape and tumor progression by exploitation of anti-inflammatory and pro-inflammatory responses. Cancer Biol Ther. 2005;4(9): 924-933.
84. Nomura S, Ozaki Y, Ikeda Y. Function and role of microparticles in various clinical settings. Thromb Res. 2008;123(1):8-23.
85. Boon RA, Vickers KC. Intercellular transport of microRNAs. Arterioscler Thromb Vasc Biol. 2013;33(2):186-192.
86. Walsh TG, Metharom P, Berndt MC. The functional role of platelets in the regulation of angiogenesis. Platelets. 2015;26(3):199-211.
87. Lee EK, Gorospe M. Coding region: the neglected post-transcriptional code. RNA Biol. 2011;8(1):44-48.
88. Beitzinger M, Peters L, Zhu JY, Kremmer E, Meister G. Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol. 2007;4(2):76-84.
89. Fang Z, Rajewsky N. The impact of miRNA target sites in coding sequences and in 3'UTRs. PLoS One. 2011;6(3):e18067.
90. Agarwal V, Bell GW, Nam JW, Bartel DP. Predicting effective microRNA target sites in mammalian mRNAs. eLife. 2015;4:4.
91. Liang T, Yu J, Liu C, Guo L. An exploration of evolution, maturation, expression and function relationships in mir-23; 27; 24 cluster. PLoS One. 2014;9(8):e106223.
92. Sharma D, Brummel-Ziedins KE, Bouchard BA, Holmes CE. Platelets in tumor progression: a host factor that offers multiple potential targets in the treatment of cancer. J Cell Physiol. 2014; 229(8):1005-1015.
93. 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.
94. Gong J, Jaiswal R, Dalla P, Luk F, Bebawy M. Microparticles in cancer: A review of recent developments and the potential for clinical application. Semin Cell Dev Biol. 2015;40:35-40.
95. Gong J, Jaiswal R, Mathys JM, Combes V, Grau GE, Bebawy M. Microparticles and their emerging role in cancer multidrug resistance. Cancer Treat Rev. 2012;38(3):226-234.
96. Jaiswal R, Raymond Grau GE, Bebawy M. Cellular communication via microparticles: role in transfer of multidrug resistance in cancer. Future Oncol. 2014;10(4):655-669.
97. Chistiakov DA, Orekhov AN, Bobryshev YV. Endothelial barrier and its abnormalities in cardiovascular disease. Front Physiol. 2015;6: 365.
98. Hayon Y, Shai E, Varon D, Leker RR. The role of platelets and their microparticles in rehabilitation of ischemic brain tissue. CNS Neurol Disord Drug Targets. 2012;11(7):921-925.
99. Opal SM, van der Poll T. Endothelial barrier dysfunction in septic shock. J Intern Med. 2015; 277(3):277-293.
100. Reid VL, Webster NR. Role of microparticles in sepsis. Br J Anaesth. 2012;109(4):503-513.
101. Meziani F, Delabranche X, Asfar P, Toti F. Bench-to-bedside review: circulating microparticles-a new player in sepsis? Crit Care. 2010;14(5):236.
102. Tetta C, Bruno S, Fonsato V, Deregibus MC, Camussi G. The role of microvesicles in tissue repair. Organogenesis. 2011;7(2):105-115.
103. Shin ES, Sorenson CM, Sheibani N. Diabetes and retinal vascular dysfunction. J Ophthalmic Vis Res. 2014;9(3):362-373.
104. Randriamboavonjy V, Fleming I. Platelet function and signaling in diabetes mellitus. Curr Vasc Pharmacol. 2012;10(5):532-538.
105. Vazzana N, Ranalli P, Cuccurullo C, Davi G. Diabetes mellitus and thrombosis. Thromb Res. 2012;129(3):371-377.