Vps4A functions as a tumor suppressor by regulating the secretion and uptake of exosomal microRNAs in human hepatoma cells

Hepatology

Volumn 61, Issue 4, 2015, Pages 1284-1294

  Wei, Jin xing ^a   Lv, Li hong ^a   Wan, Yun le ^b   Cao, Yang ^c   Li, Guo lin ^a   Lin, Hao ming ^a   Zhou, Rui ^d   Shang, Chang zhen ^a   Cao, Jun ^a   He, Hai ^a   Han, Qing fang ^a   Liu, Pei qing ^a   Zhou, Gang ^e   Min, Jun ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b THE SIXTH AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^c Guangzhou Key Laboratory of Basic and Applied Research of Oral Regenerative Medicine   (China)

^d THE THIRD AFFILIATED HOSPITAL OF SOUTHERN MEDICAL UNIVERSITY   (China)

^e AUGUSTA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SERINE THREONINE KINASE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING ASSOCIATED PROTEIN 4A; ESCRT PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; VPS4A PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOGENESIS; BIOLOGICAL ACTIVITY; CANCER GROWTH; CANCER PROGNOSIS; CANCER SIZE; CANCER SURVIVAL; CARCINOGENESIS; CELL ACTIVITY; CELL ISOLATION; CELL SIZE; CELLULAR SECRETION; CONTROLLED STUDY; DOWN REGULATION; ENZYME REGULATION; EXOSOME; GENE EXPRESSION; GENE IDENTIFICATION; GENE OVEREXPRESSION; HEPATOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INCUBATION TIME; LYMPH NODE METASTASIS; MOUSE; NONHUMAN; ONCOLOGICAL PARAMETERS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RNA SEQUENCE; RNA STRUCTURE; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; TUMOR INVASION; UPREGULATION; LIVER CELL CARCINOMA; LIVER TUMOR; PHYSIOLOGY; SECRETION (PROCESS); TUMOR CELL CULTURE; TUMOR SUPPRESSOR GENE;

CARCINOMA, HEPATOCELLULAR; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; EXOSOMES; GENES, TUMOR SUPPRESSOR; HUMANS; LIVER NEOPLASMS; MICRORNAS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84925344610     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27660     Document Type: Article

References (40)

1. Maluccio M, Covey A. Recent progress in understanding, diagnosing, and treating hepatocellular carcinoma. CA Cancer J Clin 2012;62:394-399.
2. Kong YW, Ferland-McCollough D, Jackson TJ, Bushell M. microRNAs in cancer management. Lancet Oncol 2012;13:e249-e258.
3. Giordano S, Columbano A. MicroRNAs: new tools for diagnosis, prognosis, and therapy in hepatocellular carcinoma? Hepatology 2013;57:840-847.
4. You JS, Jones PA. Cancer genetics and epigenetics: two sides of the same coin? Cancer Cell 2012;22:9-20.
5. Rana S, Malinowska K, Zoller M. Exosomal tumor microRNA modulates premetastatic organ cells. Neoplasia 2013;15:281-295.
6. van den Boorn JG, Dassler J, Coch C, Schlee M, Hartmann G. Exosomes as nucleic acid nanocarriers. Adv Drug Deliv Rev 2013;65:331-335.
7. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013;200:373-383.
8. Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, Chiu E, et al. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 2012;151:1542-1556.
9. Kogure T, Lin WL, Yan IK, Braconi C, Patel T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 2011;54:1237-1248.
10. Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 2012;18:883-891.
11. Shifrin DJ, Demory BM, Coffey RJ, Tyska MJ. Extracellular vesicles: communication, coercion, and conditioning. Mol Biol Cell 2013;24:1253-1259.
12. Henne WM, Buchkovich NJ, Emr SD. The ESCRT pathway. Dev Cell 2011;21:77-91.
13. Stuffers S, Brech A, Stenmark H. ESCRT proteins in physiology and disease. Exp Cell Res 2009;315:1619-1626.
14. Caballe A, Martin-Serrano J. ESCRT machinery and cytokinesis: the road to daughter cell separation. Traffic 2011;12:1318-1326.
15. Hurley JH, Hanson PI. Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat Rev Mol Cell Biol 2010;11:556-566.
16. Watanabe T, Sorensen EM, Naito A, Schott M, Kim S, Ahlquist P. Involvement of host cellular multivesicular body functions in hepatitis B virus budding. Proc Natl Acad Sci USA 2007;104:10205-10210.
17. Corless L, Crump CM, Griffin SD, Harris M. Vps4 and the ESCRT-III complex are required for the release of infectious hepatitis C virus particles. J Gen Virol 2010;91:362-372.
18. Rodahl LM, Haglund K, Sem-Jacobsen C, Wendler F, Vincent JP, Lindmo K, et al. Disruption of Vps4 and JNK function in Drosophila causes tumour growth. PLoS One 2009;4:e4354.
19. Rani S, O'Brien K, Kelleher FC, Corcoran C, Germano S, Radomski MW, et al. Isolation of exosomes for subsequent mRNA, microRNA, and protein profiling. Methods Mol Biol 2011;784:181-195.
20. Lv LH, Wan YL, Lin Y, Zhang W, Yang M, Li GL, et al. Anticancer drugs cause release of exosomes with heat shock proteins from human hepatocellular carcinoma cells that elicit effective natural killer cell antitumor responses in vitro. J Biol Chem 2012;287:15874-15885.
21. Babst M, Davies BA, Katzmann DJ. Regulation of Vps4 during MVB sorting and cytokinesis. Traffic 2011;12:1298-1305.
22. Adell MAY, Vogel GF, Pakdel M, Muller M, Lindner H, Hess MW, et al. Coordinated binding of Vps4 to ESCRT-III drives membrane neck constriction during MVB vesicle formation. J Cell Biol 2014;205:33-49.
23. Nickerson DP, West M, Henry R, Odorizzi G. Regulators of Vps4 ATPase activity at endosomes differentially influence the size and rate of formation of intralumenal vesicles. Mol Biol Cell 2010;21:1023-1032.
24. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 2012;119:756-766.
25. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9:654-659.
26. Hu G, Drescher KM, Chen XM. Exosomal miRNAs: biological properties and therapeutic potential. Front Genet 2012;3:56.
27. 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;11:1143-1223.
28. Zhang Z, Liu S, Shi R, Zhao G. miR-27 promotes human gastric cancer cell metastasis by inducing epithelial-to-mesenchymal transition. Cancer Genet 2011;204:486-491.
29. Chen L, Li H, Han L, Zhang K, Wang G, Wang Y, et al. Expression and function of miR-27b in human glioma. Oncol Rep 2011;26:1617-1621.
30. Park YT, Jeong JY, Lee MJ, Kim KI, Kim TH, Kwon YD, et al. MicroRNAs overexpressed in ovarian ALDH1-positive cells are associated with chemoresistance. J Ovarian Res 2013;6:18.
31. Chen ZL, Zhao XH, Wang JW, Li BZ, Wang Z, Sun J, et al. microRNA-92a promotes lymph node metastasis of human esophageal squamous cell carcinoma via E-cadherin. J Biol Chem 2011;286:10725-10734.
32. Shigoka M, Tsuchida A, Matsudo T, Nagakawa Y, Saito H, Suzuki Y, et al. Deregulation of miR-92a expression is implicated in hepatocellular carcinoma development. Pathol Int 2010;60:351-357.
33. Zhou T, Zhang G, Liu Z, Xia S, Tian H. Overexpression of miR-92a correlates with tumor metastasis and poor prognosis in patients with colorectal cancer. Int J Colorectal Dis 2013;28:19-24.
34. Uhlmann S, Mannsperger H, Zhang JD, Horvat EA, Schmidt C, Kublbeck M, et al. Global microRNA level regulation of EGFR-driven cell-cycle protein network in breast cancer. Mol Syst Biol 2012;8:570.
35. Yang J, Gao T, Tang J, Cai H, Lin L, Fu S. Loss of microRNA-132 predicts poor prognosis in patients with primary osteosarcoma. Mol Cell Biochem 2013;381:9-15.
36. Zhang S, Hao J, Xie F, Hu X, Liu C, Tong J, et al. Downregulation of miR-132 by promoter methylation contributes to pancreatic cancer development. Carcinogenesis 2011;32:1183-1189.
37. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA 2012;109:E2110-E2116.
38. Vivanco I, Sawyers CL. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2002;2:489-501.
39. Xu Y, Li N, Xiang R, Sun P. Emerging roles of the p38 MAPK and PI3K/AKT/mTOR pathways in oncogene-induced senescence. Trends Biochem Sci 2014;39:268-276.
40. Thoresen SB, Campsteijn C, Vietri M, Schink KO, Liestol K, Andersen JS, et al. ANCHR mediates Aurora-B-dependent abscission checkpoint control through retention of VPS4. Nat Cell Biol 2014;16:550-560.