miR-638 promotes melanoma metastasis and protects melanoma cells from apoptosis and autophagy

Oncotarget

Volumn 6, Issue 5, 2015, Pages 2966-2980

  Bhattacharya, Animesh ^a   Schmitz, Ulf ^b   Raatz, Yvonne ^a   Schönherr, Madeleine ^a   Kottek, Tina ^a   Schauer, Marianne ^a   Franz, Sandra ^a   Saalbach, Anja ^a   Anderegg, Ulf ^a   Wolkenhauer, Olaf ^b   Schadendorf, Dirk ^c   Simon, Jan ^a   Magin, Thomas ^a   Vera, Julio ^d   Kunz, Manfred ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY OF ROSTOCK   (Germany)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Apoptosis; Melanoma; Metastasis; MicroRNA; p53 pathway

Indexed keywords

MESSENGER RNA; MICRORNA; MICRORNA 638; PROTEIN P53; REGULATOR PROTEIN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR ASSOCIATED PROTEIN 2 ALPHA; UNCLASSIFIED DRUG; MIRN638 MICRORNA, HUMAN; NUCLEAR PROTEIN; TFAP2A PROTEIN, HUMAN; TP53 PROTEIN, HUMAN; TP53INP2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR AP 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CONTROL; CANCER GROWTH; CANCER INHIBITION; CARCINOGENICITY; CELL INVASION; CELL PROLIFERATION; CELL PROTECTION; CONTROLLED STUDY; GENE; GENE DELETION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MELANOMA CELL; MELANOMA METASTASIS; METASTATIC MELANOMA; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PRIMARY TUMOR; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN RNA BINDING; SIGNAL TRANSDUCTION; TP53INP2 GENE; TRANSCRIPTION REGULATION; ANIMAL; CELL MOTION; DISEASE COURSE; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; MELANOMA; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; RNA INTERFERENCE; SCID MOUSE; SECONDARY; SKIN TUMOR; TIME; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; APOPTOSIS; AUTOPHAGY; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE PROGRESSION; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELANOMA; MICE, INBRED NOD; MICE, SCID; MICRORNAS; NEOPLASM INVASIVENESS; NUCLEAR PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TIME FACTORS; TRANSCRIPTION FACTOR AP-2; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84923307872     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3070     Document Type: Article

References (38)

1. Miller A J, Mihm M C, Jr.Miller A J, Mihm M C, Jr.Melanoma. N.Engl.J.Med. 2006; 355(1):51-65.
2. Curtin J A, Fridlyand J, Kageshita T, Patel H N, Busam K J, Kutzner H, Cho K H, Aiba S, Brocker E B, LeBoit P E, Pinkel D, and Bastian B C.Curtin J A, Fridlyand J, Kageshita T, Patel H N, Busam K J, Kutzner H, Cho K H, Aiba S, Brocker E B, LeBoit P E, Pinkel D, and Bastian B C.Distinct sets of genetic alterations in melanoma. N.Engl.J.Med. 2005; 353(20):2135-2147.
3. Lito P, Rosen N, and Solit D B.Lito P, Rosen N, and Solit D B.Tumor adaptation and resistance to RAF inhibitors. Nat. Med. 2013; 19(11):1401-1409.
4. Nazarian R, Shi H, Wang Q, Kong X, Koya R C, Lee H, Chen Z, Lee M K, Attar N, Sazegar H, Chodon T, Nelson S F, McArthur G et al.Nazarian R, Shi H, Wang Q, Kong X, Koya R C, Lee H, Chen Z, Lee M K, Attar N, Sazegar H, Chodon T, Nelson S F, McArthur G et al.Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature. 2010; 468(7326):973-977.
5. Calin G A, Croce C M.Calin G A, Croce C M.MicroRNA signatures in human cancers. Nat.Rev.Cancer. 2006; 6(11):857-866.
6. Penna E, Orso F, Cimino D, Tenaglia E, Lembo A, Quaglino E, Poliseno L, Haimovic A, Osella-Abate S, De P C, Pinatel E, Stadler M B, Provero P et al.Penna E, Orso F, Cimino D, Tenaglia E, Lembo A, Quaglino E, Poliseno L, Haimovic A, Osella-Abate S, De P C, Pinatel E, Stadler M B, Provero P et al.microRNA-214 contributes to melanoma tumour progression through suppression of TFAP2C. EMBO J. 2011; 30(10):1990-2007.
7. Gaziel-Sovran A, Segura M F, Di M R, Collins M K, Hanniford D, Vega-Saenz de M E, Rakus J F, Dankert J F, Shang S, Kerbel R S, Bhardwaj N, Shao Y, Darvishian F et al.Gaziel-Sovran A, Segura M F, Di M R, Collins M K, Hanniford D, Vega-Saenz de M E, Rakus J F, Dankert J F, Shang S, Kerbel R S, Bhardwaj N, Shao Y, Darvishian F et al.miR-30b/30d regulation of GalNAc transferases enhances invasion and immunosuppression during metastasis. Cancer Cell. 2011; 20(1):104-118.
8. Segura M F, Hanniford D, Menendez S, Reavie L, Zou X, Alvarez-Diaz S, Zakrzewski J, Blochin E, Rose A, Bogunovic D, Polsky D, Wei J, Lee P et al.Segura M F, Hanniford D, Menendez S, Reavie L, Zou X, Alvarez-Diaz S, Zakrzewski J, Blochin E, Rose A, Bogunovic D, Polsky D, Wei J, Lee P et al.Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc.Natl. Acad.Sci.U.S.A. 2009; 106(6):1814-1819.
9. Medina P P, Nolde M, and Slack F J.Medina P P, Nolde M, and Slack F J.OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature. 2010; 467(7311):86-90.
10. Esquela-Kerscher A, Slack F J.Esquela-Kerscher A, Slack F J.Oncomirs -microRNAs with a role in cancer. Nat.Rev. Cancer. 2006; 6(4):259-269.
11. Feng H, Liu K W, Guo P, Zhang P, Cheng T, McNiven M A, Johnson G R, Hu B, and Cheng S Y.Feng H, Liu K W, Guo P, Zhang P, Cheng T, McNiven M A, Johnson G R, Hu B, and Cheng S Y.Dynamin 2 mediates PDGFRalpha-SHP-2-promoted glioblastoma growth and invasion. Oncogene. 2012; 31(21):2691-2702.
12. Eppinga R D, Krueger E W, Weller S G, Zhang L, Cao H, and McNiven M A.Eppinga R D, Krueger E W, Weller S G, Zhang L, Cao H, and McNiven M A.Increased expression of the large GTPase dynamin 2 potentiates metastatic migration and invasion of pancreatic ductal carcinoma. Oncogene. 2012; 31(10):1228-1241.
13. Dweep H, Sticht C, Pandey P, and Gretz N.Dweep H, Sticht C, Pandey P, and Gretz N.miRWalk--database: prediction of possible miRNA binding sites by "walking" the genes of three genomes. J.Biomed.Inform. 2011; 44(5):839-847.
14. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von M C, and Jensen L J.Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von M C, and Jensen L J.STRING v9.1: proteinprotein interaction networks, with increased coverage and integration. Nucleic Acids Res. 2013; 41(Database issue):D808-D815.
15. Le B A, Portales-Casamar E, Vetter G, Moes M, Zindy P J, Saumet A, Arenillas D, Theillet C, Wasserman W W, Lecellier C H, and Friederich E.Le B A, Portales-Casamar E, Vetter G, Moes M, Zindy P J, Saumet A, Arenillas D, Theillet C, Wasserman W W, Lecellier C H, and Friederich E.MIR@NT@N: a framework integrating transcription factors, microRNAs and their targets to identify subnetwork motifs in a meta-regulation network model. BMC. Bioinformatics. 2011; 12 67
16. Lai X, Schmitz U, Gupta S K, Bhattacharya A, Kunz M, Wolkenhauer O, and Vera J.Lai X, Schmitz U, Gupta S K, Bhattacharya A, Kunz M, Wolkenhauer O, and Vera J.Computational analysis of target hub gene repression regulated by multiple and cooperative miRNAs. Nucleic Acids Res. 2012; 40(18):8818-8834.
17. Vera J, Schmitz U, Lai X, Engelmann D, Khan F M, Wolkenhauer O, and Putzer B M.Vera J, Schmitz U, Lai X, Engelmann D, Khan F M, Wolkenhauer O, and Putzer B M.Kinetic modeling-based detection of genetic signatures that provide chemoresistance via the E2F1-p73/DNp73-miR-205 network. Cancer Res. 2013; 73(12):3511-3524.
18. McPherson L A, Loktev A V, and Weigel R J.McPherson L A, Loktev A V, and Weigel R J.Tumor suppressor activity of AP2alpha mediated through a direct interaction with p53. J.Biol.Chem. 2002; 277(47):45028-45033.
19. Wajapeyee N, Somasundaram K.Wajapeyee N, Somasundaram K.Cell cycle arrest and apoptosis induction by activator protein 2alpha (AP-2alpha) and the role of p53 and p21WAF1/CIP1 in AP-2alpha-mediated growth inhibition. J.Biol.Chem. 2003; 278(52):52093-52101.
20. Zhang X, Wei J, Zhou L, Zhou C, Shi J, Yuan Q, Yang M, and Lin D.Zhang X, Wei J, Zhou L, Zhou C, Shi J, Yuan Q, Yang M, and Lin D.A functional BRCA1 coding sequence genetic variant contributes to risk of esophageal squamous cell carcinoma. Carcinogenesis. 2013; 34(10):2309-2313.
21. Nowak J, Archange C, Tardivel-Lacombe J, Pontarotti P, Pebusque M J, Vaccaro M I, Velasco G, Dagorn J C, and Iovanna J L.Nowak J, Archange C, Tardivel-Lacombe J, Pontarotti P, Pebusque M J, Vaccaro M I, Velasco G, Dagorn J C, and Iovanna J L.The TP53INP2 protein is required for autophagy in mammalian cells. Mol.Biol.Cell. 2009; 20(3):870-881.
22. Marino M L, Pellegrini P, Di L G, Djavaheri-Mergny M, Brnjic S, Zhang X, Hagg M, Linder S, Fais S, Codogno P, and De M A.Marino M L, Pellegrini P, Di L G, Djavaheri-Mergny M, Brnjic S, Zhang X, Hagg M, Linder S, Fais S, Codogno P, and De M A.Autophagy is a protective mechanism for human melanoma cells under acidic stress. J.Biol.Chem. 2012; 287(36):30664-30676.
23. White E.White E.Deconvoluting the context-dependent role for autophagy in cancer. Nat.Rev.Cancer. 2012; 12(6):401-410.
24. Corazzari M, Fimia G M, Lovat P, and Piacentini M.Corazzari M, Fimia G M, Lovat P, and Piacentini M.Why is autophagy important for melanoma? Molecular mechanisms and therapeutic implications. Semin.Cancer Biol. 2013; 23(5):337-343.
25. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen E L, Mizushima N, Ohsumi Y, Cattoretti G, and Levine B.Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen E L, Mizushima N, Ohsumi Y, Cattoretti G, and Levine B.Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J.Clin.Invest. 2003; 112(12):1809-1820.
26. Galluzzi L, Vicencio J M, Kepp O, Tasdemir E, Maiuri M C, and Kroemer G.Galluzzi L, Vicencio J M, Kepp O, Tasdemir E, Maiuri M C, and Kroemer G.To die or not to die: that is the autophagic question. Curr.Mol.Med. 2008; 8(2):78-91.
27. Shahbazi J, Lock R, and Liu T.Shahbazi J, Lock R, and Liu T.Tumor Protein 53-Induced Nuclear Protein 1 Enhances p53 Function and Represses Tumorigenesis. Front Genet. 2013; 4 80
28. Seillier M, Peuget S, Gayet O, Gauthier C, N'Guessan P, Monte M, Carrier A, Iovanna J L, and Dusetti N J.Seillier M, Peuget S, Gayet O, Gauthier C, N'Guessan P, Monte M, Carrier A, Iovanna J L, and Dusetti N J.TP53INP1, a tumor suppressor, interacts with LC3 and ATG8-family proteins through the LC3-interacting region (LIR) and promotes autophagy-dependent cell death. Cell Death.Differ. 2012; 19(9):1525-1535.
29. Lu M, Breyssens H, Salter V, Zhong S, Hu Y, Baer C, Ratnayaka I, Sullivan A, Brown N R, Endicott J, Knapp S, Kessler B M, Middleton M R et al.Lu M, Breyssens H, Salter V, Zhong S, Hu Y, Baer C, Ratnayaka I, Sullivan A, Brown N R, Endicott J, Knapp S, Kessler B M, Middleton M R et al.Restoring p53 function in human melanoma cells by inhibiting MDM2 and cyclin B1/CDK1-phosphorylated nuclear iASPP. Cancer Cell. 2013; 23(5):618-633.
30. Bar-Eli M.Gene regulation in melanoma progression by the AP-2 transcription factor. Pigment Cell Res. 2001; 14(2):78-85.
31. Berger A J, Davis D W, Tellez C, Prieto V G, Gershenwald J E, Johnson M M, Rimm D L, and Bar-Eli M.Berger A J, Davis D W, Tellez C, Prieto V G, Gershenwald J E, Johnson M M, Rimm D L, and Bar-Eli M.Automated quantitative analysis of activator protein-2alpha subcellular expression in melanoma tissue microarrays correlates with survival prediction. Cancer Res. 2005; 65(23):11185-11192.
32. Karjalainen J M, Kellokoski J K, Mannermaa A J, Kujala H E, Moisio K I, Mitchell P J, Eskelinen M J, Alhava E M, and Kosma V M.Karjalainen J M, Kellokoski J K, Mannermaa A J, Kujala H E, Moisio K I, Mitchell P J, Eskelinen M J, Alhava E M, and Kosma V M.Failure in post-transcriptional processing is a possible inactivation mechanism of AP-2alpha in cutaneous melanoma. Br.J.Cancer. 2000; 82(12):2015-2021.
33. Melnikova V O, Bar-Eli M.Melnikova V O, Bar-Eli M.Transcriptional control of the melanoma malignant phenotype. Cancer Biol.Ther. 2008; 7(7):997-1003.
34. Jean D, Gershenwald J E, Huang S, Luca M, Hudson M J, Tainsky M A, and Bar-Eli M.Jean D, Gershenwald J E, Huang S, Luca M, Hudson M J, Tainsky M A, and Bar-Eli M.Loss of AP-2 results in up-regulation of MCAM/MUC18 and an increase in tumor growth and metastasis of human melanoma cells. J.Biol.Chem. 1998; 273(26):16501-16508.
35. Gershenwald J E, Sumner W, Calderone T, Wang Z, Huang S, and Bar-Eli M.Gershenwald J E, Sumner W, Calderone T, Wang Z, Huang S, and Bar-Eli M.Dominant-negative transcription factor AP-2 augments SB-2 melanoma tumor growth in vivo. Oncogene. 2001; 20(26):3363-3375.
36. Du P, Kibbe W A, and Lin S M.Du P, Kibbe W A, and Lin S M.lumi: a pipeline for processing Illumina microarray. Bioinformatics. 2008; 24(13):1547-1548.
37. Bhattacharya A, Schmitz U, Wolkenhauer O, Schonherr M, Raatz Y, and Kunz M.Bhattacharya A, Schmitz U, Wolkenhauer O, Schonherr M, Raatz Y, and Kunz M.Regulation of cell cycle checkpoint kinase WEE1 by miR-195 in malignant melanoma. Oncogene. 2013; 32(26):3175-3183.
38. Quintana E, Shackleton M, Sabel M S, Fullen D R, Johnson T M, and Morrison S J.Quintana E, Shackleton M, Sabel M S, Fullen D R, Johnson T M, and Morrison S J.Efficient tumour formation by single human melanoma cells. Nature. 2008; 456(7222):593-598.