Selective extracellular vesicle exclusion of miR-142-3p by oral cancer cells promotes both internal and extracellular malignant phenotypes

Oncotarget

Volumn 8, Issue 9, 2017, Pages 15252-15266

  Dickman, Christopher T D ^a   Lawson, James ^a   Jabalee, James ^a   MacLellan, Sara A ^a   LePard, Nancy E ^a   Bennewith, Kevin L ^a,b   Garnis, Cathie ^a,b  

^a BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Exosome; MiRNA; Oral dysplasia; Oral squamous cell carcinoma; TGFBR1

Indexed keywords

MICRORNA; MICRORNA 142 3P; MICRORNA 150 5P; MICRORNA 223 3P; MICRORNA 451A; RAB27A PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG; MIRN142 MICRORNA, HUMAN; TGFBR1 PROTEIN, HUMAN; TGFBR1 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CELL GROWTH; CELL LEVEL; COLONY FORMATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXOSOME; HUMAN; HUMAN CELL; MALIGNANT NEOPLASM; MOUSE; MOUTH CANCER; MOUTH DISEASE; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; ORAL DYSPLASIA; RNA TRANSPORT; SMALL EXTRACELLULAR VESICLE; TUMOR PROMOTION; ANIMAL; APOPTOSIS; CELL MOTION; CELL PROLIFERATION; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MOUTH TUMOR; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; SQUAMOUS CELL CARCINOMA; TUMOR CELL CULTURE; TUMOR INVASION;

ANIMALS; APOPTOSIS; BIOMARKERS, TUMOR; CARCINOMA, SQUAMOUS CELL; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; EXTRACELLULAR VESICLES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, INBRED NOD; MICE, SCID; MICRORNAS; MOUTH NEOPLASMS; NEOPLASM INVASIVENESS; PROTEIN SERINE-THREONINE KINASES; RECEPTOR, TRANSFORMING GROWTH FACTOR-BETA TYPE I; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85014121702     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.14862     Document Type: Article

References (78)

1. Di Vizio D, Kim J, Hager MH, Morello M, Yang W, Lafargue CJ, True LD, Rubin MA, Adam RM, Beroukhim R, Demichelis F, Freeman MR. Oncosome formation in prostate cancer: association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res. 2009; 69:5601-5609.
2. Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006; Chapter 3:3.22. 21-23.22. 29.
3. Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014; 30:255-289.
4. Kowal J, Arras G, Colombo M, Jouve M, Morath JP, Primdal-Bengtson B, Dingli F, Loew D, Tkach M, Thery C. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci USA. 2016; 113:E968-977.
5. Minciacchi VR, Freeman MR, Di Vizio D. Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol. 2015; 40:41-51.
6. Gorenchtein M, Poh CF, Saini R, Garnis C. MicroRNAs in an oral cancer context-from basic biology to clinical utility. J Dent Res. 2012; 91:440-446.
7. Towle R, Gorenchtein M, Garnis C, Dickman C, Zhu Y. Dysregulation of microRNAs across oral squamous cell carcinoma fields in non-smokers. J Interdiscipl Med Dent Sci. 2014; 2:2.
8. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, Huang Y, Hu X, Su F, Lieberman J, Song E. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell. 2007; 131:1109-1123.
9. Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol. 2008; 110:13-21.
10. Logozzi M, De Milito A, Lugini L, Borghi M, Calabro L, Spada M, Perdicchio M, Marino ML, Federici C, Iessi E, Brambilla D, Venturi G, Lozupone F, et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS ONE. 2009; 4:e5219.
11. Llorente A, Skotland T, Sylvanne T, Kauhanen D, Rog T, Orlowski A, Vattulainen I, Ekroos K, Sandvig K. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim Biophys Acta. 2013; 1831:1302-1309.
12. Marleau AM, Chen CS, Joyce JA, Tullis RH. Exosome removal as a therapeutic adjuvant in cancer. J Transl Med. 2012; 10:134.
13. Ohno S, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N, Fujita K, Mizutani T, Ohgi T, Ochiya T, Gotoh N, Kuroda M. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther. 2013; 21:185-191.
14. Hood JL, San RS, Wickline SA. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res. 2011; 71:3792-3801.
15. Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, Deregibus MC, Tetta C, Bussolati B, Camussi G. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res. 2011; 71:5346-5356.
16. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol. 2009; 11:1143-1149.
17. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT, Carter BS, Krichevsky AM, Breakefield XO. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008; 10:1470-1476.
18. 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; 9:654-659.
19. Villarroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, Perez-Hernandez D, Vazquez J, Martin-Cofreces N, Martinez-Herrera DJ, Pascual-Montano A, Mittelbrunn M, Sanchez-Madrid F. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun. 2013; 4.
20. Guduric-Fuchs J, O'Connor A, Camp B, O'Neill CL, Medina RJ, Simpson DA. Selective extracellular vesiclemediated export of an overlapping set of microRNAs from multiple cell types. BMC Genomics. 2012; 13:1.
21. Villarroya-Beltri C, Baixauli F, Gutierrez-Vazquez C, Sanchez-Madrid F, Mittelbrunn M. Sorting it out: regulation of exosome loading. Semin Cancer Biol. 2014; 28:3-13.
22. Batagov AO, Kuznetsov VA, Kurochkin IV. Identification of nucleotide patterns enriched in secreted RNAs as putative cis-acting elements targeting them to exosome nanovesicles. BMC Genomics. 2011; 12:S18.
23. Rabinowits G, Gercel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin lung cancer. 2009; 10:42-46.
24. Michael A, Bajracharya SD, Yuen PST, Zhou H, Star RA, Illei GG, Alevizos I. Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis. 2010; 16:34-38.
25. Ye SB, Li ZL, Luo DH, Huang BJ, Chen YS, Zhang XS, Cui J, Zeng YX, Li J. Tumor-derived exosomes promote tumor progression and T-cell dysfunction through the regulation of enriched exosomal microRNAs in human nasopharyngeal carcinoma. Oncotarget. 2014; 5:5439-5452. doi: 10.18632/oncotarget.2118.
26. Li L, Li C, Wang S, Wang Z, Jiang J, Wang W, Li X, Chen J, Liu K, Zhu G. Exosomes Derived from Hypoxic Oral Squamous Cell Carcinoma Cells Deliver miR-21 to Normoxic Cells to Elicit a Prometastatic Phenotype. Cancer Res. 2016; 76:1770-1780.
27. Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, Sun F, Lu J, Yin Y, Cai X, Sun Q, Wang K, Ba Y, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell. 2010; 39:133-144.
28. Kosaka N, Iguchi H, Hagiwara K, Yoshioka Y, Takeshita F, Ochiya T. Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic microRNAs regulate cancer cell metastasis. J Biol Chem. 2013; 288:10849-10859.
29. Umezu T, Ohyashiki K, Kuroda M, Ohyashiki JH. Leukemia cell to endothelial cell communication via exosomal miRNAs. Oncogene. 2013; 32:2747-2755.
30. van Balkom BW, De Jong OG, Smits M, Brummelman J, den Ouden K, de Bree PM, van Eijndhoven MA, Pegtel DM, Stoorvogel W, Würdinger T. Endothelial cells require miR-214 to secrete exosomes that suppress senescence and induce angiogenesis in human and mouse endothelial cells. Blood. 2013; 121:3997-4006.
31. Aucher A, Rudnicka D, Davis DM. MicroRNAs transfer from human macrophages to hepato-carcinoma cells and inhibit proliferation. J Immunol. 2013; 191:6250-6260.
32. Ohshima K, Inoue K, Fujiwara A, Hatakeyama K, Kanto K, Watanabe Y, Muramatsu K, Fukuda Y, Ogura S, Yamaguchi K, Mochizuki T. Let-7 MicroRNA Family Is Selectively Secreted into the Extracellular Environment via Exosomes in a Metastatic Gastric Cancer Cell Line. PLoS ONE. 2010; 5:e13247.
33. Ostenfeld MS, Jeppesen DK, Laurberg JR, Boysen AT, Bramsen JB, Primdal-Bengtson B, Hendrix A, Lamy P, Dagnaes-Hansen F, Rasmussen MH, Bui KH, Fristrup N, Christensen EI, et al. Cellular disposal of miR23b by RAB27-dependent exosome release is linked to acquisition of metastatic properties. Cancer Res. 2014; 74:5758-5771.
34. Zhou QB, Gallagher R, Ufret-Vincenty R, Li XY, Olson EN, Wang SS. Regulation of angiogenesis and choroidal neovascularization by members of microRNA-23 similar to 27 similar to 24 clusters. Proc Natl Acad Sci USA. 2011; 108:8287-8292.
35. Kuehbacher A, Urbich C, Zeiher AM, Dimmeler S. Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ Res. 2007; 101:59-68.
36. Rani S, O'Brien K, Kelleher FC, Corcoran C, Germano S, Radomski MW, Crown J, O'Driscoll L. Isolation of exosomes for subsequent mRNA, MicroRNA, and protein profiling. Gene Expression Profiling: Springer. 2011; 181-195.
37. Mathivanan S, Simpson RJ. ExoCarta: A compendium of exosomal proteins and RNA. Proteomics. 2009; 9:4997-5000.
38. Gould SJ, Raposo G. As we wait: coping with an imperfect nomenclature for extracellular vesicles. J Extracell Vesicles. 2013; 2.
39. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brügger B, Simons M. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008; 319:1244-1247.
40. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP, Goud B, Benaroch P, Hacohen N, et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol. 2010; 12:19-30.
41. Towle R, Truong D, Hogg K, Robinson WP, Poh CF, Garnis C. Global analysis of DNA methylation changes during progression of oral cancer. Oral Oncol. 2013; 49:1033-1042.
42. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL, Tait JF, Tewari M. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA. 2011; 108:5003-5008.
43. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011; 39:7223-7233.
44. Mitchell JA, Aronson AR, Mork JG, Folk LC, Humphrey SM, Ward JM. Gene indexing: characterization and analysis of NLM's GeneRIFs. AMIA Annu Symp Proc. 2003; 2003:460.
45. Lei Z, Xu G, Wang L, Yang H, Liu X, Zhao J, Zhang HT. MiR-142-3p represses TGF-β-induced growth inhibition through repression of TGFβR1 in non-small cell lung cancer. FASEB J. 2014; 28:2696-2704.
46. Network CGAR. Integrated genomic analyses of ovarian carcinoma. Nature. 2011; 474:609-615.
47. Dickman CT, Towle R, Saini R, Garnis C. Molecular characterization of immortalized normal and dysplastic oral cell lines. J Oral Pathol Med. 2014; 44:329-336.
48. Tsui IF, Garnis C. Integrative molecular characterization of head and neck cancer cell model genomes. Head Neck. 2010; 32:1143-1160.
49. Yamano Y, Uzawa K, Shinozuka K, Fushimi K, Ishigami T, Nomura H, Ogawara K, Shiiba M, Yokoe H, Tanzawa H. Hyaluronan-mediated motility: a target in oral squamous cell carcinoma. Int J Oncol. 2008; 32:1001-1009.
50. Xu S, Wei J, Wang F, Kong LY, Ling XY, Nduom E, Gabrusiewicz K, Doucette T, Yang Y, Yaghi NK, Fajt V, Levine JM, Qiao W, et al. Effect of miR-142-3p on the M2 macrophage and therapeutic efficacy against murine glioblastoma. J Natl Cancer Inst. 2014; 106:dju162.
51. Bourguignon LY, Singleton PA, Zhu H, Zhou B. Hyaluronan promotes signaling interaction between CD44 and the transforming growth factor β receptor I in metastatic breast tumor cells. J Biol Chem. 2002; 277:39703-39712.
52. Ota T, Fujii M, Sugizaki T, Ishii M, Miyazawa K, Aburatani H, Miyazono K. Targets of transcriptional regulation by two distinct type I receptors for transforming growth factor-β in human umbilical vein endothelial cells. J Cell Physiol. 2002; 193:299-318.
53. Arnaoutova I, George J, Kleinman HK, Benton G. The endothelial cell tube formation assay on basement membrane turns 20: state of the science and the art. Angiogenesis. 2009; 12:267-274.
54. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011; 473:298-307.
55. Zhang T, Sun Q, Liu T, Chen J, Du S, Ren C, Liao G, Yuan Y. MiR-451 increases radiosensitivity of nasopharyngeal carcinoma cells by targeting ras-related protein 14 (RAB14). Tumor Biol. 2014; 35:12593-12599.
56. Feng JL, Yang YZ, Zhang P, Wang F, Ma YL, Qin HL, Wang Y. miR-150 functions as a tumour suppressor in human colorectal cancer by targeting c-Myb. J Cell Mol Med. 2014; 18:2125-2134.
57. Pinatel EM, Orso F, Penna E, Cimino D, Elia AR, Circosta P, Dentelli P, Brizzi MF, Provero P, Taverna D. miR-223 Is a Coordinator of Breast Cancer Progression as Revealed by Bioinformatics Predictions. PLoS ONE. 2014; 9.
58. Tsitsiou E, Lindsay MA. microRNAs and the immune response. Curr Opin Pharmacol. 2009; 9:514-520.
59. Chen Q, Wang H, Liu Y, Song Y, Lai L, Han Q, Cao X, Wang Q. Inducible microRNA-223 down-regulation promotes TLR-triggered IL-6 and IL-1beta production in macrophages by targeting STAT3. PLoS ONE. 2012; 7:e42971.
60. Wu C, Li M, Hu C, Duan H. Clinical significance of serum miR-223, miR-25 and miR-375 in patients with esophageal squamous cell carcinoma. Mol Biol Rep. 2014; 41:1257-1266.
61. Wang JS, Wang FB, Zhang QG, Shen ZZ, Shao ZM. Enhanced expression of Rab27A gene by breast cancer cells promoting invasiveness and the metastasis potential by secretion of insulin-like growth factor-II. Molecular cancer research. 2008; 6:372-382.
62. Wang Q, Ni Q, Wang X, Zhu H, Wang Z, Huang J. High expression of RAB27A and TP53 in pancreatic cancer predicts poor survival. Med Oncol. 2015; 32:1-9.
63. Wang HJ, Zhao Y, Zhang CB, Li MY, Jiang CL, Li YL. Rab27a Was Identified as a Prognostic Biomaker by mRNA Profiling, Correlated with Malignant Progression and Subtype Preference in Gliomas. PLoS ONE. 2014; 9.
64. Yoshiba S, Ito D, Nagumo T, Shirota T, Hatori M, Shintani S. Hypoxia induces resistance to 5-fluorouracil in oral cancer cells via G phase cell cycle arrest. Oral Oncol. 2009; 45:109-115.
65. Sasabe E, Zhou X, Li D, Oku N, Yamamoto T, Osaki T. The involvement of hypoxia-inducible factor-1alpha in the susceptibility to gamma-rays and chemotherapeutic drugs of oral squamous cell carcinoma cells. Int J Cancer. 2007; 120:268-277.
66. Soufla G, Sifakis S, Baritaki S, Zafiropoulos A, Koumantakis E, Spandidos DA. VEGF, FGF2, TGFB1 and TGFBR1 mRNA expression levels correlate with the malignant transformation of the uterine cervix. Cancer Lett. 2005; 221:105-118.
67. Languino LR, Singh A, Prisco M, Inman GJ, Luginbuhl A, Curry JM, South AP. Exosome-mediated transfer from the tumor microenvironment increases TGFβ signaling in squamous cell carcinoma. Am J Transl Res. 2016; 8:2432-2437.
68. Ten Dijke P, Arthur HM. Extracellular control of TGFbeta signalling in vascular development and disease. Nat Rev Mol Cell Biol. 2007; 8:857-869.
69. Pardali E, Goumans MJ, ten Dijke P. Signaling by members of the TGF-β family in vascular morphogenesis and disease. Trends Cell Biol. 2010; 20:556-567.
70. Liu Z, Kobayashi K, van Dinther M, van Heiningen SH, Valdimarsdottir G, van Laar T, Scharpfenecker M, Lowik CW, Goumans MJ, Ten Dijke P, Pardali E. VEGF and inhibitors of TGFbeta type-I receptor kinase synergistically promote blood-vessel formation by inducing alpha5-integrin expression. J Cell Sci. 2009; 122:3294-3302.
71. Bobrie A, Colombo M, Krumeich S, Raposo G, Théry C. Diverse subpopulations of vesicles secreted by different intracellular mechanisms are present in exosome preparations obtained by differential ultracentrifugation. J Extracell Vesicles. 2012; 1.
72. Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, Garcia-Santos G, Ghajar C, Nitadori-Hoshino A, Hoffman C, Badal K, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 2012; 18:883-891.
73. Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, Molina H, Kohsaka S, Di Giannatale A, Ceder S, Singh S, Williams C, Soplop N, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015; 527:329-335.
74. Wei Z, Batagov AO, Carter DR, Krichevsky AM. Fetal Bovine Serum RNA Interferes with the Cell Culture derived Extracellular RNA. Sci Rep. 2016; 6:31175.
75. Shelke GV, Lasser C, Gho YS, Lotvall J. Importance of exosome depletion protocols to eliminate functional and RNA-containing extracellular vesicles from fetal bovine serum. J Extracell Vesicles. 2014; 3.
76. Mestdagh P, Van Vlierberghe P, De Weer A, Muth D, Westermann F, Speleman F, Vandesompele J. A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol. 2009; 10:R64.
77. Towle R, Tsui IFL, Zhu YQ, MacLellan S, Poh CF, Garnis C. Recurring DNA copy number gain at chromosome 9p13 plays a role in the activation of multiple candidate oncogenes in progressing oral premalignant lesions. Cancer Med. 2014; 3:1170-1184.
78. Halvorsen EC, Hamilton MJ, Young A, Wadsworth BJ, LePard NE, Lee HN, Firmino N, Collier JL, Bennewith KL. Maraviroc decreases CCL8-mediated migration of CCR5(+) regulatory T cells and reduces metastatic tumor growth in the lungs. Oncoimmunology. 2016; 5:e1150398.