MicroRNAome profiling in benign and malignant neurofibromatosis type 1-associated nerve sheath tumors: Evidences of PTEN pathway alterations in early NF1 tumorigenesis

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Masliah Planchon, Julien ^a   Pasmant, Eric ^a,b   Luscan, Armelle ^a,b   Laurendeau, Ingrid ^a,b   Ortonne, Nicolas ^c   Hivelin, Mikael ^c,d   Varin, Jennifer ^a,b   Valeyrie Allanore, Laurence ^c   Dumaine, Valérie ^b   Lantieri, Laurent ^c,d   Leroy, Karen ^c   Parfait, Béatrice ^a,b   Wolkenstein, Pierre ^c   Vidaud, Michel ^a,b   Vidaud, Dominique ^a,b   Bièche, Ivan ^a,e  

^a INSERM   (France)

^b Institut Cochin   (France)

^c HENRI MONDOR HOSPITAL   (France)

^d HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^e INSTITUT CURIE   (France)

Author keywords

MicroRNAs; MPNST; Neurofibroma; Neurofibromatosis type 1; NF1; PTEN

Indexed keywords

LET 7B; MICRORNA; MICRORNA 10B; MICRORNA 143; MICRORNA 145; MICRORNA 20A; MICRORNA 210; MICRORNA 9; MIR 106B; MIR 10A; MIR 129 3P; MIR 181A; MIR 195; MIR 196B; MIR 19A; MIR 301A; MIR 370; MIR 486 3P; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RAS PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARCINOGENESIS; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DERMAL NEUROFIBROMA; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE REPRESSION; HOX GENE; HUMAN; HUMAN TISSUE; MALIGNANT PERIPHERAL NERVE SHEATH TUMOR; NERVE SHEATH TUMOR; NEUROFIBROMA; NEUROFIBROMATOSIS; PTEN GENE; UPREGULATION;

ARGONAUTE PROTEINS; CELL LINE, TUMOR; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; HUMANS; MICRORNAS; NEUROFIBROMA, PLEXIFORM; NEUROFIBROMATOSIS 1; PROTEINS; PTEN PHOSPHOHYDROLASE; RIBONUCLEASE III; SEQUENCE HOMOLOGY, NUCLEIC ACID; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84880113353     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-473     Document Type: Article

References (50)

1. Sabbagh A, Pasmant E, Laurendeau I, Parfait B, Barbarot S, Guillot B, Combemale P, Ferkal S, Vidaud M, Aubourg P, Vidaud D, Wolkenstein P. Unravelling the genetic basis of variable clinical expression in neurofibromatosis 1. Hum Mol Genet 2009, 18:2768-2778. 10.1093/hmg/ddp212, 2722187, 19417008.
2. Pasmant E, Sabbagh A, Masliah-Planchon J, Ortonne N, Laurendeau I, Melin L, Ferkal S, Hernandez L, Leroy K, Valeyrie-Allanore L, Parfait B, Vidaud D, Bièche I, Lantieri L, Wolkenstein P, Vidaud M. NF France Network Role of Noncoding RNA ANRIL in Genesis of Plexiform Neurofibromas in Neurofibromatosis Type 1. J Natl Cancer Inst 2011, 103:1713-1722. 10.1093/jnci/djr416, 22034633, NF France Network.
3. Mantripragada KK, Spurlock G, Kluwe L, Chuzhanova N, Ferner RE, Frayling IM, Dumanski JP, Guha A, Mautner V, Upadhyaya M. High-resolution DNA copy number profiling of malignant peripheral nerve sheath tumors using targeted microarray-based comparative genomic hybridization. Clin Cancer Res 2008, 14:1015-1024. 10.1158/1078-0432.CCR-07-1305, 18281533.
4. Subramanian S, Thayanithy V, West RB, Lee CH, Beck AH, Zhu S, Downs-Kelly E, Montgomery K, Goldblum JR, Hogendoorn PC, Corless CL, Oliveira AM, Dry SM, Nielsen TO, Rubin BP, Fletcher JA, Fletcher CD, van de Rijn M. Genome-wide transcriptome analyses reveal p53 inactivation mediated loss of mir-34a expression in malignant peripheral nerve sheath tumours. J Pathol 2010, 220:58-70. 10.1002/path.2633, 19890883.
5. Pasmant E, Ortonne N, Rittié L, Laurendeau I, Lévy P, Lazar V, Parfait B, Leroy K, Dessen P, Valeyrie-Allanore L, Perbal B, Wolkenstein P, Vidaud M, Vidaud D, Bièche I. Differential expression of CCN1/CYR61, CCN3/NOV, CCN4/WISP1, and CCN5/WISP2 in neurofibromatosis type 1 tumorigenesis. J Neuropathol Exp Neurol 2010, 69:60-69. 10.1097/NEN.0b013e3181c79bff, 20010302.
6. Lévy P, Vidaud D, Leroy K, Laurendeau I, Wechsler J, Bolasco G, Parfait B, Wolkenstein P, Vidaud M, Bièche I. Molecular profiling of malignant peripheral nerve sheath tumors associated with neurofibromatosis type 1, based on large-scale real-time RT-PCR. Mol Cancer 2004, 3:20. 10.1186/1476-4598-3-20, 493279, 15255999.
7. Vogel KS, Klesse LJ, Velasco-Miguel S, Meyers K, Rushing EJ, Parada LF. Mouse tumor model for neurofibromatosis type 1. Science 1999, 286:2176-2179. 10.1126/science.286.5447.2176, 3079436, 10591653.
8. Gregorian C, Nakashima J, Dry SM, Nghiemphu PL, Smith KB, Ao Y, Dang J, Lawson G, Mellinghoff IK, Mischel PS, Phelps M, Parada LF, Liu X, Sofroniew MV, Eilber FC, Wu H. PTEN dosage is essential for neurofibroma development and malignant transformation. Proc Natl Acad Sci U S A 2009, 106:19479-19484. 10.1073/pnas.0910398106, 2765459, 19846776.
9. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854. 10.1016/0092-8674(93)90529-Y, 8252621.
10. Small EM, O'Rourke JR, Moresi V, Sutherland LB, McAnally J, Gerard RD, Richardson JA, Olson EN. Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486. Proc Natl Acad Sci U S A 2010, 107:4218-4223. 10.1073/pnas.1000300107, 2840099, 20142475.
11. Meng F, Wehbe-Janek H, Henson R, Smith H, Patel T. Epigenetic regulation of microRNA-370 by interleukin-6 in malignant human cholangiocytes. Oncogene 2008, 27:378-386. 10.1038/sj.onc.1210648, 17621267.
12. Chen X, Guo X, Zhang H, Xiang Y, Chen J, Yin Y, Cai X, Wang K, Wang G, Ba Y, Zhu L, Wang J, Yang R, Zhang Y, Ren Z, Zen K, Zhang J, Zhang CY. Role of mir-143 targeting KRAS in colorectal tumorigenesis. Oncogene 2009, 28:1385-1392. 10.1038/onc.2008.474, 19137007.
13. Shin KH, Bae SD, Hong HS, Kim RH, Kang MK, Park NH. MiR-181a shows tumor suppressive effect against oral squamous cell carcinoma cells by downregulating K-RAS. Biochem Biophys Res Commun 2011, 404:896-902. 10.1016/j.bbrc.2010.12.055, 21167132.
14. Wang Y, Yu Y, Tsuyada A, Ren X, Wu X, Stubblefield K, Rankin-Gee EK, Wang SE. Transforming growth factor-β regulates the sphere-initiating stem cell-like feature in breast cancer through miRNA-181 and ATM. Oncogene 2011, 30:1470-1480. 10.1038/onc.2010.531, 3063856, 21102523.
15. Kent OA, Chivukula RR, Mullendore M, Wentzel EA, Feldmann G, Lee KH, Liu S, Leach SD, Maitra A, Mendell JT. Repression of the miR-143/145 cluster by oncogenic Ras initiates a tumor-promoting feed-forward pathway. Genes Dev 2010, 24:2754-2759. 10.1101/gad.1950610, 3003192, 21159816.
16. Liu L, Chen L, Xu Y, Li R, Du X. MicroRNA-195 promotes apoptosis and suppresses tumorigenicity of human colorectal cancer cells. Biochem Biophys Res Commun 2010, 400:236-240. 10.1016/j.bbrc.2010.08.046, 20727858.
17. Xu T, Zhu Y, Xiong Y, Ge YY, Yun JP, Zhuang SM. MicroRNA-195 suppresses tumorigenicity and regulates G1/S transition of human hepatocellular carcinoma cells. Hepatology 2009, 50:113-121. 10.1002/hep.22919, 19441017.
18. Kim HA, Ratner N, Roberts TM, Stiles CD. Schwann cell proliferative responses to cAMP and Nf1 are mediated by cyclin D1. J Neurosci 2001, 21:1110-1116.
19. Hurteau GJ, Carlson JA, Spivack SD, Brock GJ. Overexpression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin. Cancer Res 2007, 67:7972-7976. 10.1158/0008-5472.CAN-07-1058, 17804704.
20. Sekiya Y, Ogawa T, Iizuka M, Yoshizato K, Ikeda K, Kawada N. Down-regulation of cyclin E1 expression by microRNA-195 accounts for interferon-β-induced inhibition of hepatic stellate cell proliferation. J Cell Physiol 2011, 226:2535-2542. 10.1002/jcp.22598, 21792910.
21. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, Labourier E, Reinert KL, Brown D, Slack FJ. Ras is regulated by the let-7 microRNA family. Cell 2005, 120:635-647. 10.1016/j.cell.2005.01.014, 15766527.
22. Peter ME. Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle 2009, 8:843-852. 10.4161/cc.8.6.7907, 2688687, 19221491.
23. Keng VW, Rahrmann EP, Watson AL, Tschida BR, Moertel CL, Jessen WJ, Rizvi TA, Collins MH, Ratner N, Largaespada DA. PTEN and NF1 inactivation in Schwann cells produces a severe phenotype in the peripheral nervous system that promotes the development and malignant progression of peripheral nerve sheath tumors. Cancer Res 2012, 72:3405-3413. 10.1158/0008-5472.CAN-11-4092, 3428071, 22700876.
24. Qin X, Wang X, Wang Y, Tang Z, Cui Q, Xi J, Li YS, Chien S, Wang N. MicroRNA-19a mediates the suppressive effect of laminar flow on cyclin D1 expression in human umbilical vein endothelial cells. Proc Natl Acad Sci U S A 2010, 107:3240-3244. 10.1073/pnas.0914882107, 2840357, 20133739.
25. Huang X, Ding L, Bennewith KL, Tong RT, Welford SM, Ang KK, Story M, Le QT, Giaccia AJ. Hypoxia-inducible miR-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell 2009, 35:856-867. 10.1016/j.molcel.2009.09.006, 2782615, 19782034.
26. Shi W, Gerster K, Alajez NM, Tsang J, Waldron L, Pintilie M, Hui AB, Sykes J, P'ng C, Miller N, McCready D, Fyles A, Liu FF. MicroRNA-301 mediates proliferation and invasion in human breast cancer. Cancer Res 2011, 71:2926-2937. 10.1158/0008-5472.CAN-10-3369, 21393507.
27. Roura S, Miravet S, Piedra J, García de Herreros A, Duñach M. Regulation of E-cadherin/catenin association by tyrosine phosphorylation. J Biol Chem 1999, 274:36734-36740. 10.1074/jbc.274.51.36734, 10593980.
28. Han L, Witmer PD, Casey E, Valle D, Sukumar S. DNA methylation regulates microRNA expression. Cancer Biol Ther 2007, 6:1284-1288.
29. Lewis BP, Shih I-H, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 2003, 115:787-798. 10.1016/S0092-8674(03)01018-3, 14697198.
30. Schultz J, Lorenz P, Gross G, Ibrahim S, Kunz M. MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growth. Cell Res 2008, 18:549-557. 10.1038/cr.2008.45, 18379589.
31. Trompeter HI, Abbad H, Iwaniuk KM, Hafner M, Renwick N, Tuschl T, Schira J, Müller HW, Wernet P. MicroRNAs MiR-17, MiR-20a, and MiR-106b act in concert to modulate E2F activity on cell cycle arrest during neuronal lineage differentiation of USSC. PLoS One 2011, 6:e16138. 10.1371/journal.pone.0016138, 3024412, 21283765.
32. Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS, Hobbs RM, Sportoletti P, Varmeh S, Egia A, Fedele G, Rameh L, Loda M, Pandolfi PP. Identification of the miR-106b 25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal 2010, 3:ra29. 10.1126/scisignal.2000594, 2982149, 20388916.
33. Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007, 449:682-688. 10.1038/nature06174, 17898713.
34. Ozawa T, Araki N, Yunoue S, Tokuo H, Feng L, Patrakitkomjorn S, Hara T, Ichikawa Y, Matsumoto K, Fujii K, Saya H. The neurofibromatosis type 1 gene product neurofibromin enhances cell motility by regulating actin filament dynamics via the Rho-ROCK-LIMK2-cofilin pathway. J Biol Chem 2005, 280:39524-39533. 10.1074/jbc.M503707200, 16169856.
35. Yekta S, Shih I-H, Bartel DP. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004, 304:594-596. 10.1126/science.1097434, 15105502.
36. Kumar MS, Lu J, Mercer KL, Golub TR, Jacks T. Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet 2007, 39:673-677. 10.1038/ng2003, 17401365.
37. Tay Y, Kats L, Salmena L, Weiss D, Tan SM, Ala U, Karreth F, Poliseno L, Provero P, Di Cunto F, Lieberman J, Rigoutsos I, Pandolfi PP. Coding-Independent Regulation of the Tumor Suppressor PTEN by Competing Endogenous mRNAs. Cell 2011, 147:344-357. 10.1016/j.cell.2011.09.029, 3235920, 22000013.
38. Negrini S, Gorgoulis VG, Halazonetis TD. Genomic instability-an evolving hallmark of cancer. Nat Rev Mol Cell Biol 2010, 11:220-228. 10.1038/nrm2858, 20177397.
39. Nagel R, le Sage C, Diosdado B, van der Waal M, Oude Vrielink JA, Bolijn A, Meijer GA, Agami R. Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res 2008, 68:5795-5802. 10.1158/0008-5472.CAN-08-0951, 18632633.
40. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, Teruya-Feldstein J, Reinhardt F, Onder TT, Valastyan S, Westermann F, Speleman F, Vandesompele J, Weinberg RA. MiR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 2010, 12:247-256. 2845545, 20173740.
41. Lee YS, Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev 2007, 21:1025-1030. 10.1101/gad.1540407, 1855228, 17437991.
42. Thuault S, Valcourt U, Petersen M, Manfioletti G, Heldin CH, Moustakas A. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition. J Cell Biol 2006, 174:175-183. 10.1083/jcb.200512110, 2064178, 16831886.
43. Nishino J, Kim I, Chada K, Morrison SJ. Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell 2008, 135:227-239. 10.1016/j.cell.2008.09.017, 2582221, 18957199.
44. Chai G, Liu N, Ma J, Li H, Oblinger JL, Prahalad AK, Gong M, Chang LS, Wallace M, Muir D, Guha A, Phipps RJ, Hock JM, Yu X. MicroRNA-10b regulates tumorigenesis in neurofibromatosis type 1. Cancer Sci 2010, 101:1997-2004. 10.1111/j.1349-7006.2010.01616.x, 20550523.
45. Rotkrua P, Akiyama Y, Hashimoto Y, Otsubo T, Yuasa Y. MiR-9 downregulates CDX2 expression in gastric cancer cells. Int J Cancer 2011, 129:2611-2620. 10.1002/ijc.25923, 21225631.
46. Shah N, Sukumar S. The HOX genes and their roles in oncogenesis. Nat Rev Cancer 2010, 10:361-371. 10.1038/nrc2826, 20357775.
47. Wu J, Qian J, Li C, Kwok L, Cheng F, Liu P, Perdomo C, Kotton D, Vaziri C, Anderlind C, Spira A, Cardoso WV, Lü J. MiR-129 regulates cell proliferation by downregulating Cdk6 expression. Cell Cycle 2010, 9:1809-1818. 10.4161/cc.9.9.11535, 20404570.
48. Li D, Zhao Y, Liu C, Chen X, Qi Y, Jiang Y, Zou C, Zhang X, Liu S, Wang X, Zhao D, Sun Q, Zeng Z, Dress A, Lin MC, Kung HF, Rui H, Liu LZ, Mao F, Jiang BH, Lai L. Analysis of miR-195 and miR-497 expression, regulation and role in breast cancer. Clin Cancer Res 2011, 17:1722-1730. 10.1158/1078-0432.CCR-10-1800, 21350001.
49. Peltier HJ, Latham GJ. Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA 2008, 14:844-852. 10.1261/rna.939908, 2327352, 18375788.
50. Pasmant E, Masliah-Planchon J, Lévy P, Laurendeau I, Ortonne N, Parfait B, Valeyrie-Allanore L, Leroy K, Wolkenstein P, Vidaud M, Vidaud D, Bièche I. Identification of genes potentially involved in the increased risk of malignancy in NF1-microdeleted patients. Mol Med 2011, 17:79-87. 3022985, 20844836.