MiR-204 mediates post-transcriptional down-regulation of PHOX2B gene expression in neuroblastoma cells

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1849, Issue 8, 2015, Pages 1057-1065

  Bachetti, Tiziana ^a   Di Zanni, Eleonora ^a   Ravazzolo, Roberto ^a,b   Ceccherini, Isabella ^a  

^a G GASLINI INSTITUTE   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

Author keywords

3'UTR regulatory elements; Gene reporter assay; MiRNA; Neuroblastoma; PHOX2B; Post transcriptional control

Indexed keywords

HOMEODOMAIN PROTEIN; MESSENGER RNA; MICRORNA; MICRORNA 204; PAIRED LIKE HOMEOBOX 2B PROTEIN; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; MIRN204 MICRORNA, HUMAN; NBPHOX PROTEIN; TRANSCRIPTION FACTOR;

3' UNTRANSLATED REGION; ALLELE; ARTICLE; AU RICH ELEMENT; BACTERIAL STRAIN; COMPUTER MODEL; CONTROLLED STUDY; DOWN REGULATION; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION REGULATION; IN VITRO STUDY; NEUROBLASTOMA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REPORTER GENE; RNA PROCESSING; RNA STABILITY; SINGLE NUCLEOTIDE POLYMORPHISM; BRAIN TUMOR; CELL CULTURE; CHILD; GENETICS; HUMAN; MOLECULAR GENETICS; PATHOLOGY; PHYSIOLOGY;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; BRAIN NEOPLASMS; CELLS, CULTURED; CHILD; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MICRORNAS; MOLECULAR SEQUENCE DATA; NEUROBLASTOMA; RNA PROCESSING, POST-TRANSCRIPTIONAL; TRANSCRIPTION FACTORS;

EID: 84936878562     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2015.06.008     Document Type: Article

References (42)

1. Westermann F., Schwab M. Genetic parameters of neuroblastomas. Cancer Lett. 2002, 184:127-147.
2. Capasso M., Devoto M., Hou C., Asgharzadeh S., Glessner J.T., Attiyeh E.F., Mosse Y.P., Kim C., Diskin S.J., Cole K.A., Bosse K., Diamond M., Laudenslager M., Winter C., Bradfield J.P., Scott R.H., Jagannathan J., Garris M., McConville C., London W.B., Seeger R.C., Grant S.F., Li H., Rahman N., Rappaport E., Hakonarson H., Maris J.M. Common variations in BARD1 influence susceptibility to high-risk neuroblastoma. Nat. Genet. 2009, 41:718-723.
3. Maris J.M. Recent advances in neuroblastoma. N. Engl. J. Med. 2010, 362:2202-2211.
4. Pugh T.J., Morozova O., Attiyeh E.F., Asgharzadeh S., Wei J.S., Auclair D., Carter S.L., Cibulskis K., Hanna M., Kiezun A., Kim J., Lawrence M.S., Lichenstein L., McKenna A., Pedamallu C.S., Ramos A.H., Shefler E., Sivachenko A., Sougnez C., Stewart C., Ally A., Birol I., Chiu R., Corbett R.D., Hirst M., Jackman S.D., Kamoh B., Khodabakshi A.H., Krzywinski M., Lo A., Moore R.A., Mungall K.L., Qian J., Tam A., Thiessen N., Zhao Y., Cole K.A., Diamond M., Diskin S.J., Mosse Y.P., Wood A.C., Ji L., Sposto R., Badgett T., London W.B., Moyer Y., Gastier-Foster J.M., Smith M.A., Guidry Auvil J.M., Gerhard D.S., Hogarty M.D., Jones S.J., Lander E.S., Gabriel S.B., Getz G., Seeger R.C., Khan J., Marra M.A., Meyerson M., Maris J.M. The genetic landscape of high-risk neuroblastoma. Nat. Genet. 2013, 45:279-284.
5. Schleiermacher G., Janoueix-Lerosey I., Delattre O. Recent insights into the biology of neuroblastoma. Int. J. Cancer 2014, 135:2249-2261.
6. Molenaar J.J., Koster J., Zwijnenburg D.A., van Sluis P., Valentijn L.J., van der Ploeg I., Hamdi M., van Nes J., Westerman B.A., van Arkel J., Ebus M.E., Haneveld F., Lakeman A., Schild L., Molenaar P., Stroeken P., van Noesel M.M., Ora I., Santo E.E., Caron H.N., Westerhout E.M., Versteeg R. Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes. Nature 2012, 483:589-593.
7. Trochet D., Bourdeaut F., Janoueix-Lerosey I., Deville A., de Pontual L., Schleiermacher G., Coze C., Philip N., Frébourg T., Munnich A., Lyonnet S., Delattre O., Amiel J. Germline mutations of the paired-like homeobox 2B (PHOX2B) gene in neuroblastoma. Am. J. Hum. Genet. 2004, 74:761-764.
8. Mosse Y.P., Laudenslager M., Khazi D., Carlisle A.J., Winter C.L., Rappaport E., Maris J.M. Germline PHOX2B mutation in hereditary neuroblastoma. Am. J. Hum. Genet. 2004, 75:727-730.
9. Amiel J., Laudier B., Attié-Bitach T., Trang H., de Pontual L., Gener B., Trochet D., Etchevers H., Ray P., Simonneau M., Vekemans M., Munnich A., Gaultier C., Lyonnet S. Polyalanine expansion and frameshift mutations of the paired-like homeobox gene PHOX2B in congenital central hypoventilation syndrome. Nat. Genet. 2003, 33:459-461.
10. Matera I., Bachetti T., Puppo F., Di Duca M., Morandi F., Casiraghi G.M., Cilio M.R., Hennekam R., Hofstra R., Schöber J.G., Ravazzolo R., Ottonello G., Ceccherini I. PHOX2B mutations and polyalanine expansions correlate with the severity of the respiratory phenotype and associated symptoms in both congenital and late onset central hypoventilation syndrome. J. Med. Genet. 2004, 41:373-380.
11. Weese-Mayer D.E., Berry-Kravis E.M., Zhou L., Maher B.S., Silvestri J.M., Curran M.E., Marazita M.L. Idiopathic congenital central hypoventilation syndrome: analysis of genes pertinent to early autonomic nervous system embryologic development and identification of mutations in PHOX2b. Am. J. Med. Genet. A 2003, 123A:267-278.
12. Mossé Y.P., Laudenslager M., Longo L., Cole K.A., Wood A., Attiyeh E.F., Laquaglia M.J., Sennett R., Lynch J.E., Perri P., Laureys G., Speleman F., Kim C., Hou C., Hakonarson H., Torkamani A., Schork N.J., Brodeur G.M., Tonini G.P., Rappaport E., Devoto M., Maris J.M. Identification of ALK as a major familial neuroblastoma predisposition gene. Nature 2008, 455:930-935.
13. Janoueix-Lerosey I., Lequin D., Brugières L., Ribeiro A., de Pontual L., Combaret V., Raynal V., Puisieux A., Schleiermacher G., Pierron G., Valteau-Couanet D., Frebourg T., Michon J., Lyonnet S., Amiel J., Delattre O. Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma. Nature 2008, 455:967-970.
14. McConville C., Reid S., Baskcomb L., Douglas J., Rahman N. PHOX2B analysis in non-syndromic neuroblastoma cases shows novel mutations and genotype-phenotype associations. Am. J. Med. Genet. A 2006, 140:1297-1301.
15. Raabe E.H., Laudenslager M., Winter C., Wasserman N., Cole K., LaQuaglia M., Maris D.J., Mosse Y.P., Maris J.M. Prevalence and functional consequence of PHOX2B mutations in neuroblastoma. Oncogene 2008, 27:469-476.
16. Nagashimada M., Ohta H., Li C., Nakao K., Uesaka T., Brunet J.F., Amiel J., Trochet D., Wakayama T., Enomoto H. Autonomic neurocristopathy-associated mutations in PHOX2B dysregulate Sox10 expression. J. Clin. Invest. 2012, 122:3145-3158.
17. Wang W., Zhong Q., Teng L., Bhatnagar N., Sharma B., Zhang X., Luther W., Haynes L.P., Burgoyne R.D., Vidal M., Volchenboum S., Hill D.E., George R.E. Mutations that disrupt PHOXB interaction with the neuronal calcium sensor HPCAL1 impede cellular differentiation in neuroblastoma. Oncogene 2014, 33:3316-3324.
18. Pei D., Luther W., Wang W., Paw B.H., Stewart R.A., George R.E. Distinct neuroblastoma-associated alterations of PHOX2B impair sympathetic neuronal differentiation in zebrafish models. PLoS Genet. 2013, 9:e1003533.
19. Alam G., Cui H., Shi H., Yang L., Ding J., Mao L., Maltese W.A., Ding H.F. MYCN promotes the expansion of Phox2B-positive neuronal progenitors to drive neuroblastoma development. Am. J. Pathol. 2009, 175:856-866.
20. Longo L., Borghini S., Schena F., Parodi S., Albino D., Bachetti T., Da Prato L., Truini M., Gambini C., Tonini G.P., Ceccherini I., Perri P. PHOX2A and PHOX2B genes are highly co-expressed in human neuroblastoma. Int. J. Oncol. 2008, 33:985-991.
21. Bachetti T., Di Paolo D., Di Lascio S., Mirisola V., Brignole C., Bellotti M., Caffa I., Ferraris C., Fiore M., Fornasari D., Chiarle R., Borghini S., Pfeffer U., Ponzoni M., Ceccherini I., Perri P. PHOX2B-mediated regulation of ALK expression: in vitro identification of a functional relationship between two genes involved in neuroblastoma. PLoS ONE 2010, 5(10):e131085.
22. Abel F., Dalevi D., Nethander M., Jörnsten R., De Preter K., Vermeulen J., Stallings R., Kogner P., Maris J., Nilsson S. A 6-gene signature identifies four molecular subgroups of neuroblastoma. Cancer Cell Int. 2011, 14:11-19.
23. Di Leva G., Garofalo M., Croce C.M. MicroRNAs in cancer. Annu. Rev. Pathol. 2014, 9:287-314.
24. Stallings R.L., Foley N.H., Bryan K., Buckley P.G., Bray I. Therapeutic targeting of miRNAs in neuroblastoma. Expert Opin. Ther. Targets 2010, 14:951-962.
25. Chen Y., Stallings R.L. Differential patterns of microRNA expression in neuroblastoma are correlated with prognosis, differentiation, and apoptosis. Cancer Res. 2007, 67:976-983.
26. Schulte J.H., Horn S., Otto T., Samans B., Heukamp L.C., Eilers U.C., Krause M., Astrahantseff K., Klein-Hitpass L., Buettner R., Schramm A., Christiansen H., Eilers M., Eggert A., Berwanger B. MYCN regulates oncogenic microRNAs in neuroblastoma. Int. J. Cancer 2008, 122:699-704.
27. Chu V.R., Lee I. MicroRNA target signatures in advanced stage neuroblastoma. Neuroblastoma - Present and Future 2012, InTech, (Available from: http://www.intechopen.com/books/neuroblastoma-present-and-future/microrna-targetsignatures-in-advanced-stage-neuroblastoma). H. Shimada (Ed.).
28. Ray S.K. Emerging roles of microRNAs in malignant neuroblastoma. Clin. Exp. Pharmacol. 2013, 3:126.
29. Ryan J., Tivnan A., Fay J., Bryan K., Meehan M., Creevey L., Lynch J., Bray I.M., O'Meara A., Tracey L., Davidoff A.M., Stallings R.L. MicroRNA-204 increases sensitivity of neuroblastoma cells to cisplatin and is associated with a favourable clinical outcome. Br. J. Cancer 2012, 107:967-976.
30. Li W., Jin X., Zhang Q., Zhang G., Deng X., Ma L. Decreased expression of miR-204 is associated with poor prognosis in patients with breast cancer. Int. J. Clin. Exp. Pathol. 2014, 7:3287-3292.
31. Zhou X., Li L., Su J., Zhang G. Decreased miR-204 in H. pylori-associated gastric cancer promotes cancer cell proliferation and invasion by targeting SOX4. PLoS ONE 2014, 9:e101457.
32. Cargnin F., Flora A., Di Lascio S., Battaglioli E., Longhi R., Clementi F., Fornasari D. PHOX2B regulates its own expression by a transcriptional auto-regulatory mechanism. J. Biol. Chem. 2005, 280:37439-37448.
33. Sharova L.V., Sharov A.A., Nedorezov T., Piao Y., Shaik N., Ko M.S. Database for mRNA half-life of 19977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res. 2009, 16:45-58.
34. Acosta S., Lavarino C., Paris R., Garcia I., de Torres C., Rodríguez E., Beleta H., Mora J. Comprehensive characterization of neuroblastoma cell line subtypes reveals bilineage potential similar to neural crest stem cells. BMC Dev. Biol. 2009, 9:12.
35. Gao F.B. Posttranscriptional control of neuronal development by microRNA networks. Trends Neurosci. 2008, 31:20-26.
36. Conte I., Merella S., Garcia-Manteiga J.M., Migliore C., Lazarevic D., Carrella S., Marco-Ferreres R., Avellino R., Davidson N.P., Emmett W., Sanges R., Bockett N., Van Heel D., Meroni G., Bovolenta P., Stupka E., Banfi S. The combination of transcriptomics and informatics identifies pathways targeted by miR-204 during neurogenesis and axon guidance. Nucleic Acids Res. 2014, 42:7793-7806.
37. Deveci M., Çatalyürek U.V., Toland A.E. mrSNP: software to detect SNP effects on microRNA binding. BMC Bioinf. 2014, 15:73.
38. Capasso M., Diskin S., Cimmino F., Acierno G., Totaro F., Petrosino G., Pezone L., Diamond M., McDaniel L., Hakonarson H., Iolascon A., Devoto M., Maris J.M. Common genetic variants in NEFL influence gene expression and neuroblastoma risk. Cancer Res. 2014, 74:6913-6924.
39. Diskin S.J., Capasso M., Diamond M., Oldridge D.A., Conkrite K., Bosse K.R., Russell M.R., Iolascon A., Hakonarson H., Devoto M., Maris J.M. Rare variants in TP53 and susceptibility to neuroblastoma. J. Natl. Cancer Inst. 2014, 106:dju047.
40. Yu Z., Li Z., Jolicoeur N., Zhang L., Fortin Y., Wang E., Wu M., Shen S.H. Aberrant allele frequencies of the SNPs located in microRNA target sites are potentially associated with human cancers. Nucleic Acids Res. 2007, 35:4535-4541.
41. Beckers A., Van Peer G., Carter D.R., Mets E., Althoff K., Cheung B.B., Schulte J.H., Mestdagh P., Vandesompele J., Marshall G.M., De Preter K., Speleman F. MYCN-targeting miRNAs are predominantly downregulated during MYCN-driven neuroblastoma tumor formation. Oncotarget 2015, 6:5204-5216.
42. Sidarovich V., Adami V., Quattrone A. A cell-based high-throughput screen addressing 3'UTR-dependent regulation of the MYCN gene. Mol. Biotechnol. 2014, 56:631-643.