Skip to main content

Analysis of the p53/microRNA Network in Cancer

  • Chapter
  • First Online:
Systems Biology of MicroRNAs in Cancer

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1385))

Abstract

MicroRNAs (miRNAs) are important components of the signaling cascades that mediate and regulate tumor suppression exerted by p53. This review illustrates some of the main principles that underlie the mechanisms by which miRNAs participate in p53’s function and how they were identified. Furthermore, the current status of the research on the connection between p53 and miRNAs, as well as alterations in the p53/miRNA pathways found in cancer will be summarized and discussed. In addition, experimental and bioinformatic approaches which can be applied to study the connection between p53 and miRNAs are described. Although, some of the central miRNA-encoding genes that mediate the effects of p53, such as the miR-34 and miR-200 families, have been identified, much more analyses remain to be performed to fully elucidate the connections between p53 and miRNAs.

Analysis of the p53/microRNA network in cancer” by Kaller, Hünten, Siemens and Hermeking), please include the footnote to the abstract” This chapter is an update of the previously published work: Hünten S., Siemens H., Kaller M., Hermeking H. (2013) The p53/microRNA Network in Cancer: Experimental and Bioinformatics Approaches. In: Schmitz U., Wolkenhauer O., Vera J. (eds) MicroRNA Cancer Regulation

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Afanasyeva EA, Mestdagh P, Kumps C, Vandesompele J, Ehemann V, Theissen J, Fischer M, Zapatka M, Brors B, Savelyeva L, Sagulenko V, Speleman F, Schwab M, Westermann F (2011) MicroRNA miR-885-5p targets CDK2 and MCM5, activates p53 and inhibits proliferation and survival. Cell Death Differ 18(6):974–984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alexiou P, Maragkakis M, Papadopoulos GL, Reczko M, Hatzigeorgiou AG (2009) Lost in translation: an assessment and perspective for computational microRNA target identification. Bioinformatics 25(23):3049–3055

    Article  CAS  PubMed  Google Scholar 

  • Amaral FC, Torres N, Saggioro F, Neder L, Machado HR, Silva WA Jr, Moreira AC, Castro M (2009) MicroRNAs differentially expressed in ACTH-secreting pituitary tumors. J Clin Endocrinol Metab 94(1):320–323

    Article  CAS  PubMed  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11(10):R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP (2008) The impact of microRNAs on protein output. Nature 455(7209):64–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baffa R, Fassan M, Volinia S, O'Hara B, Liu CG, Palazzo JP, Gardiman M, Rugge M, Gomella LG, Croce CM, Rosenberg A (2009) MicroRNA expression profiling of human metastatic cancers identifies cancer gene targets. J Pathol 219(2):214–221

    Article  CAS  PubMed  Google Scholar 

  • Bahubeshi A, Tischkowitz M, Foulkes WD (2011) miRNA processing and human cancer: DICER1 cuts the mustard. Sci Transl Med 3(111):111ps146

    Article  Google Scholar 

  • Bandi N, Vassella E (2011) miR-34a and miR-15a/16 are co-regulated in non-small cell lung cancer and control cell cycle progression in a synergistic and Rb-dependent manner. Mol Cancer 10:55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bandi N, Zbinden S, Gugger M, Arnold M, Kocher V, Hasan L, Kappeler A, Brunner T, Vassella E (2009) miR-15a and miR-16 are implicated in cell cycle regulation in a Rb-dependent manner and are frequently deleted or down-regulated in non-small cell lung cancer. Cancer Res 69(13):5553–5559

    Article  CAS  PubMed  Google Scholar 

  • Beitzinger M, Peters L, Zhu JY, Kremmer E, Meister G (2007) Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol 4(2):76–84

    Article  CAS  PubMed  Google Scholar 

  • Bertolazzi G, Benos PV, Tumminello M, Coronnello C (2020) An improvement of ComiR algorithm for microRNA target prediction by exploiting coding region sequences of mRNAs. BMC Bioinformatics 21(Suppl 8):201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhattacharya R, Nicoloso M, Arvizo R, Wang E, Cortez A, Rossi S, Calin GA, Mukherjee P (2009) MiR-15a and MiR-16 control Bmi-1 expression in ovarian cancer. Cancer Res 69(23):9090–9095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bohlig L, Friedrich M, Engeland K (2011) p53 activates the PANK1/miRNA-107 gene leading to downregulation of CDK6 and p130 cell cycle proteins. Nucleic Acids Res 39(2):440–453

    Article  PubMed  Google Scholar 

  • Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE, Zhai Y, Giordano TJ, Qin ZS, Moore BB, MacDougald OA, Cho KR, Fearon ER (2007) p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 17(15):1298–1307

    Article  CAS  PubMed  Google Scholar 

  • Bonci D, Coppola V, Musumeci M, Addario A, Giuffrida R, Memeo L, D'Urso L, Pagliuca A, Biffoni M, Labbaye C, Bartucci M, Muto G, Peschle C, De Maria R (2008) The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med 14(11):1271–1277

    Article  CAS  PubMed  Google Scholar 

  • Bottoni A, Piccin D, Tagliati F, Luchin A, Zatelli MC, Degli Uberti EC (2005) miR-15a and miR-16-1 down-regulation in pituitary adenomas. J Cell Physiol 204(1):280–285

    Article  CAS  PubMed  Google Scholar 

  • Bou Kheir T, Futoma-Kazmierczak E, Jacobsen A, Krogh A, Bardram L, Hother C, Gronbaek K, Federspiel B, Lund AH, Friis-Hansen L (2011) miR-449 inhibits cell proliferation and is down-regulated in gastric cancer. Mol Cancer 10:29

    Article  PubMed  PubMed Central  Google Scholar 

  • Brabletz T (2012) MiR-34 and SNAIL: another double-negative feedback loop controlling cellular plasticity/EMT governed by p53. Cell Cycle 11(2):215

    Article  CAS  PubMed  Google Scholar 

  • Braun CJ, Zhang X, Savelyeva I, Wolff S, Moll UM, Schepeler T, Orntoft TF, Andersen CL, Dobbelstein M (2008) p53-responsive micrornas 192 and 215 are capable of inducing cell cycle arrest. Cancer Res 68(24):10094–10104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, Sedivy JM, Kinzler KW, Vogelstein B (1998) Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282(5393):1497–1501

    Article  CAS  PubMed  Google Scholar 

  • Cai KM, Bao XL, Kong XH, Jinag W, Mao MR, Chu JS, Huang YJ, Zhao XJ (2010) Hsa-miR-34c suppresses growth and invasion of human laryngeal carcinoma cells via targeting c-met. Int J Mol Med 25(4):565–571

    Article  CAS  PubMed  Google Scholar 

  • Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, Rassenti L, Kipps T, Negrini M, Bullrich F, Croce CM (2002) Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A 99(24):15524–15529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, Iorio MV, Visone R, Sever NI, Fabbri M, Iuliano R, Palumbo T, Pichiorri F, Roldo C, Garzon R, Sevignani C, Rassenti L, Alder H, Volinia S, Liu CG, Kipps TJ, Negrini M, Croce CM (2005) A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med 353(17):1793–1801

    Article  CAS  PubMed  Google Scholar 

  • Careccia S, Mainardi S, Pelosi A, Gurtner A, Diverio D, Riccioni R, Testa U, Pelosi E, Piaggio G, Sacchi A, Lavorgna S, Lo-Coco F, Blandino G, Levrero M, Rizzo MG (2009) A restricted signature of miRNAs distinguishes APL blasts from normal promyelocytes. Oncogene 28(45):4034–4040

    Article  CAS  PubMed  Google Scholar 

  • Cawley S, Bekiranov S, Ng HH, Kapranov P, Sekinger EA, Kampa D, Piccolboni A, Sementchenko V, Cheng J, Williams AJ, Wheeler R, Wong B, Drenkow J, Yamanaka M, Patel S, Brubaker S, Tammana H, Helt G, Struhl K, Gingeras TR (2004) Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 116(4):499–509

    Article  CAS  PubMed  Google Scholar 

  • Ceppi P, Mudduluru G, Kumarswamy R, Rapa I, Scagliotti GV, Papotti M, Allgayer H (2010) Loss of miR-200c expression induces an aggressive, invasive, and chemoresistant phenotype in non-small cell lung cancer. Mol Cancer Res 8(9):1207–1216

    Article  CAS  PubMed  Google Scholar 

  • Chae H, Rhee S, Nephew KP, Kim S (2015) BioVLAB-MMIA-NGS: microRNA-mRNA integrated analysis using high-throughput sequencing data. Bioinformatics 31(2):265–267

    Article  CAS  PubMed  Google Scholar 

  • Chakrabarti AM, Haberman N, Praznik A, Luscombe NM, Ule J (2018) Data science issues in studying protein–RNA interactions with CLIP technologies. Annual Review of Biomedical Data Science 1(1):235–261

    Article  Google Scholar 

  • Chang CJ, Chao CH, Xia W, Yang JY, Xiong Y, Li CW, Yu WH, Rehman SK, Hsu JL, Lee HH, Liu M, Chen CT, Yu D, Hung MC (2011) p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs. Nat Cell Biol 13(3):317–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang H, Yi B, Ma R, Zhang X, Zhao H, Xi Y (2016) CRISPR/cas9, a novel genomic tool to knock down microRNA in vitro and in vivo. Sci Rep 6:22312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH, Feldmann G, Yamakuchi M, Ferlito M, Lowenstein CJ, Arking DE, Beer MA, Maitra A, Mendell JT (2007) Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 26(5):745–752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen QR, Yu LR, Tsang P, Wei JS, Song YK, Cheuk A, Chung JY, Hewitt SM, Veenstra TD, Khan J (2011) Systematic proteome analysis identifies transcription factor YY1 as a direct target of miR-34a. J Proteome Res 10(2):479–487

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Hu H, Guan X, Xiong G, Wang Y, Wang K, Li J, Xu X, Yang K, Bai Y (2012) CpG island methylation status of miRNAs in esophageal squamous cell carcinoma. Int J Cancer 130(7):1607–1613

    Article  CAS  PubMed  Google Scholar 

  • Cheok CF, Verma CS, Baselga J, Lane DP (2011) Translating p53 into the clinic. Nat Rev Clin Oncol 8(1):25–37

    Article  CAS  PubMed  Google Scholar 

  • Chi SW, Zang JB, Mele A, Darnell RB (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460(7254):479–486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chim CS, Wong KY, Qi Y, Loong F, Lam WL, Wong LG, Jin DY, Costello JF, Liang R (2010) Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis 31(4):745–750

    Article  CAS  PubMed  Google Scholar 

  • Choi YJ, Lin CP, Ho JJ, He X, Okada N, Bu P, Zhong Y, Kim SY, Bennett MJ, Chen C, Ozturk A, Hicks GG, Hannon GJ, He L (2011) miR-34 miRNAs provide a barrier for somatic cell reprogramming. Nat Cell Biol 13(11):1353–1360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chou J, Kaller M, Jaeckel S, Rokavec M, Hermeking H (2022) AP4 suppresses DNA damage, chromosomal instability and senescence via inducing MDC1/Mediator of DNA damage checkpoint 1 and repressing MIR22HG/miR-22-3p. Mol Cancer 21(1):120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corcoran DL, Georgiev S, Mukherjee N, Gottwein E, Skalsky RL, Keene JD, Ohler U (2011) PARalyzer: definition of RNA binding sites from PAR-CLIP short-read sequence data. Genome Biol 12(8):R79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, Nikitin AY (2007) MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res 67(18):8433–8438

    Article  CAS  PubMed  Google Scholar 

  • Corney DC, Hwang CI, Matoso A, Vogt M, Flesken-Nikitin A, Godwin AK, Kamat AA, Sood AK, Ellenson LH, Hermeking H, Nikitin AY (2010) Frequent downregulation of miR-34 family in human ovarian cancers. Clin Cancer Res 16(4):1119–1128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coronnello C, Benos PV (2013) ComiR: combinatorial microRNA target prediction tool. Nucleic Acids Res 41(Web Server issue):W159–W164

    Article  PubMed  PubMed Central  Google Scholar 

  • Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26(12):1367–1372

    Article  CAS  PubMed  Google Scholar 

  • Cummins JM, He Y, Leary RJ, Pagliarini R, Diaz LA Jr, Sjoblom T, Barad O, Bentwich Z, Szafranska AE, Labourier E, Raymond CK, Roberts BS, Juhl H, Kinzler KW, Vogelstein B, Velculescu VE (2006) The colorectal microRNAome. Proc Natl Acad Sci U S A 103(10):3687–3692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davalos V, Moutinho C, Villanueva A, Boque R, Silva P, Carneiro F, Esteller M (2011) Dynamic epigenetic regulation of the microRNA-200 family mediates epithelial and mesenchymal transitions in human tumorigenesis. Oncogene 31(16):2062–2074

    Article  PubMed  PubMed Central  Google Scholar 

  • de Krijger I, Mekenkamp LJ, Punt CJ, Nagtegaal ID (2011) MicroRNAs in colorectal cancer metastasis. J Pathol 224(4):438–447

    Article  PubMed  Google Scholar 

  • Derheimer FA, Kastan MB (2010) Multiple roles of ATM in monitoring and maintaining DNA integrity. FEBS Lett 584(17):3675–3681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • di Gennaro A, Damiano V, Brisotto G, Armellin M, Perin T, Zucchetto A, Guardascione M, Spaink HP, Doglioni C, Snaar-Jagalska BE, Santarosa M, Maestro R (2018) A p53/miR-30a/ZEB2 axis controls triple negative breast cancer aggressiveness. Cell Death Differ 25(12):2165–2180

    Article  PubMed  PubMed Central  Google Scholar 

  • Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29(1):15–21

    Article  CAS  PubMed  Google Scholar 

  • Donehower LA, Soussi T, Korkut A, Liu Y, Schultz A, Cardenas M, Li X, Babur O, Hsu TK, Lichtarge O, Weinstein JN, Akbani R, Wheeler DA (2019) Integrated analysis of TP53 gene and Pathway alterations in the cancer genome atlas. Cell Rep 28(5):1370–1384 e1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan R, Pak C, Jin P (2007) Single nucleotide polymorphism associated with mature miR-125a alters the processing of pri-miRNA. Hum Mol Genet 16(9):1124–1131

    Article  CAS  PubMed  Google Scholar 

  • Dweep H, Gretz N, Sticht C (2014) miRWalk database for miRNA-target interactions. Methods Mol Biol 1182:289–305

    Article  PubMed  Google Scholar 

  • Earle JS, Luthra R, Romans A, Abraham R, Ensor J, Yao H, Hamilton SR (2010) Association of microRNA expression with microsatellite instability status in colorectal adenocarcinoma. J Mol Diagn 12(4):433–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fabbri M, Bottoni A, Shimizu M, Spizzo R, Nicoloso MS, Rossi S, Barbarotto E, Cimmino A, Adair B, Wojcik SE, Valeri N, Calore F, Sampath D, Fanini F, Vannini I, Musuraca G, Dell'Aquila M, Alder H, Davuluri RV, Rassenti LZ, Negrini M, Nakamura T, Amadori D, Kay NE, Rai KR, Keating MJ, Kipps TJ, Calin GA, Croce CM (2011) Association of a microRNA/TP53 feedback circuitry with pathogenesis and outcome of B-cell chronic lymphocytic leukemia. JAMA 305(1):59–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faber C, Horst D, Hlubek F, Kirchner T (2011) Overexpression of Dicer predicts poor survival in colorectal cancer. Eur J Cancer 47(9):1414–1419

    Article  CAS  PubMed  Google Scholar 

  • Fejes AP, Robertson G, Bilenky M, Varhol R, Bainbridge M, Jones SJ (2008) FindPeaks 3.1: a tool for identifying areas of enrichment from massively parallel short-read sequencing technology. Bioinformatics 24(15):1729–1730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng J, Liu T, Qin B, Zhang Y, Liu XS (2012) Identifying ChIP-seq enrichment using MACS. Nat Protoc 7(9):1728–1740

    Article  CAS  PubMed  Google Scholar 

  • Fischer M (2017) Census and evaluation of p53 target genes. Oncogene 36(28):3943–3956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer M, Quaas M, Steiner L, Engeland K (2016) The p53-p21-DREAM-CDE/CHR pathway regulates G2/M cell cycle genes. Nucleic Acids Res 44(1):164–174

    Article  CAS  PubMed  Google Scholar 

  • Fischer M, Steiner L, Engeland K (2014) The transcription factor p53: not a repressor, solely an activator. Cell Cycle 13(19):3037–3058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fornari F, Gramantieri L, Giovannini C, Veronese A, Ferracin M, Sabbioni S, Calin GA, Grazi GL, Croce CM, Tavolari S, Chieco P, Negrini M, Bolondi L (2009) MiR-122/cyclin G1 interaction modulates p53 activity and affects doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 69(14):5761–5767

    Article  CAS  PubMed  Google Scholar 

  • Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1):92–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galka-Marciniak P, Urbanek-Trzeciak MO, Nawrocka PM, Dutkiewicz A, Giefing M, Lewandowska MA, Kozlowski P (2019) Somatic mutations in miRNA genes in lung cancer-potential functional consequences of non-coding sequence variants. Cancers (Basel) 11(6):793

    Article  CAS  Google Scholar 

  • Garg S, Sharp PA (2016) GENE EXPRESSION. Single-cell variability guided by microRNAs Science 352(6292):1390–1391

    CAS  PubMed  Google Scholar 

  • Garibaldi F, Falcone E, Trisciuoglio D, Colombo T, Lisek K, Walerych D, Del Sal G, Paci P, Bossi G, Piaggio G, Gurtner A (2016) Mutant p53 inhibits miRNA biogenesis by interfering with the microprocessor complex. Oncogene 35(29):3760–3770

    Article  CAS  PubMed  Google Scholar 

  • Georges SA, Biery MC, Kim SY, Schelter JM, Guo J, Chang AN, Jackson AL, Carleton MO, Linsley PS, Cleary MA, Chau BN (2008) Coordinated regulation of cell cycle transcripts by p53-inducible microRNAs, miR-192 and miR-215. Cancer Res 68(24):10105–10112

    Article  CAS  PubMed  Google Scholar 

  • Green DR, Kroemer G (2009) Cytoplasmic functions of the tumour suppressor p53. Nature 458(7242):1127–1130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregorova J, Vychytilova-Faltejskova P, Sevcikova S (2021) Epigenetic regulation of MicroRNA clusters and families during tumor development. Cancers (Basel) 13(6):1333

    Article  CAS  Google Scholar 

  • Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10(5):593–601

    Article  CAS  PubMed  Google Scholar 

  • Hackenberg M, Rodriguez-Ezpeleta N, Aransay AM (2011) miRanalyzer: an update on the detection and analysis of microRNAs in high-throughput sequencing experiments. Nucleic Acids Res 39(Web Server issue):W132–W138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M Jr, Jungkamp AC, Munschauer M, Ulrich A, Wardle GS, Dewell S, Zavolan M, Tuschl T (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141(1):129–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hahn S, Jackstadt R, Siemens H, Hunten S, Hermeking H (2013) SNAIL and miR-34a feed-forward regulation of ZNF281/ZBP99 promotes epithelial-mesenchymal transition. EMBO J 32(23):3079–3095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison CJ, Mazzullo H, Cheung KL, Gerrard G, Jalali GR, Mehta A, Osier DG, Orchard KH (2003) Cytogenetics of multiple myeloma: interpretation of fluorescence in situ hybridization results. Br J Haematol 120(6):944–952

    Article  CAS  PubMed  Google Scholar 

  • He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, Jackson AL, Linsley PS, Chen C, Lowe SW, Cleary MA, Hannon GJ (2007a) A microRNA component of the p53 tumour suppressor network. Nature 447(7148):1130–1134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He X, He L, Hannon GJ (2007b) The guardian’s little helper: microRNAs in the p53 tumor suppressor network. Cancer Res 67(23):11099–11101

    Article  CAS  PubMed  Google Scholar 

  • Hendrickson DG, Hogan DJ, Herschlag D, Ferrell JE, Brown PO (2008) Systematic identification of mRNAs recruited to argonaute 2 by specific microRNAs and corresponding changes in transcript abundance. PLoS One 3(5):e2126

    Article  PubMed  PubMed Central  Google Scholar 

  • Hermeking H (2003) The 14-3-3 cancer connection. Nat Rev Cancer 3(12):931–943

    Article  CAS  PubMed  Google Scholar 

  • Hermeking H (2007) p53 enters the microRNA world. Cancer Cell 12(5):414–418

    Article  CAS  PubMed  Google Scholar 

  • Hermeking H (2010) The miR-34 family in cancer and apoptosis. Cell Death Differ 17(2):193–199

    Article  CAS  PubMed  Google Scholar 

  • Hermeking H (2012) MicroRNAs in the p53 network: micromanagement of tumour suppression. Nat Rev Cancer 12(9):613–626

    Article  CAS  PubMed  Google Scholar 

  • Herrera-Merchan A, Cerrato C, Luengo G, Dominguez O, Piris MA, Serrano M, Gonzalez S (2010) miR-33-mediated downregulation of p53 controls hematopoietic stem cell self-renewal. Cell Cycle 9(16):3277–3285

    Article  CAS  PubMed  Google Scholar 

  • Hill DA, Ivanovich J, Priest JR, Gurnett CA, Dehner LP, Desruisseau D, Jarzembowski JA, Wikenheiser-Brokamp KA, Suarez BK, Whelan AJ, Williams G, Bracamontes D, Messinger Y, Goodfellow PJ (2009) DICER1 mutations in familial pleuropulmonary blastoma. Science 325(5943):965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffman Y, Pilpel Y, Oren M (2014) microRNAs and Alu elements in the p53-Mdm2-Mdm4 regulatory network. J Mol Cell Biol 6(3):192–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoh J, Jin S, Parrado T, Edington J, Levine AJ, Ott J (2002) The p53MH algorithm and its application in detecting p53-responsive genes. Proc Natl Acad Sci U S A 99(13):8467–8472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu W, Chan CS, Wu R, Zhang C, Sun Y, Song JS, Tang LH, Levine AJ, Feng Z (2010) Negative regulation of tumor suppressor p53 by microRNA miR-504. Mol Cell 38(5):689–699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu X, Macdonald DM, Huettner PC, Feng Z, El Naqa IM, Schwarz JK, Mutch DG, Grigsby PW, Powell SN, Wang X (2009) A miR-200 microRNA cluster as prognostic marker in advanced ovarian cancer. Gynecol Oncol 114(3):457–464

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Lan W, Miller D (2017) Next-generation sequencing for MicroRNA expression profile. Methods Mol Biol 1617:169–177

    Article  CAS  PubMed  Google Scholar 

  • Hwang CI, Matoso A, Corney DC, Flesken-Nikitin A, Korner S, Wang W, Boccaccio C, Thorgeirsson SS, Comoglio PM, Hermeking H, Nikitin AY (2011) Wild-type p53 controls cell motility and invasion by dual regulation of MET expression. Proc Natl Acad Sci U S A 108(34):14240–14245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kahlert C, Klupp F, Brand K, Lasitschka F, Diederichs S, Kirchberg J, Rahbari N, Dutta S, Bork U, Fritzmann J, Reissfelder C, Koch M, Weitz J (2011) Invasion front-specific expression and prognostic significance of microRNA in colorectal liver metastases. Cancer Sci 102(10):1799–1807

    Article  CAS  PubMed  Google Scholar 

  • Kaller M, Liffers ST, Oeljeklaus S, Kuhlmann K, Roh S, Hoffmann R, Warscheid B, Hermeking H (2011) Genome-wide characterization of miR-34a induced changes in protein and mRNA expression by a combined pulsed SILAC and microarray analysis. Mol Cell Proteomics 10(8):M111 010462

    Article  PubMed  PubMed Central  Google Scholar 

  • Karaayvaz M, Pal T, Song B, Zhang C, Georgakopoulos P, Mehmood S, Burke S, Shroyer K, Ju J (2011) Prognostic significance of miR-215 in colon cancer. Clin Colorectal Cancer 10(4):340–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karginov FV, Conaco C, Xuan Z, Schmidt BH, Parker JS, Mandel G, Hannon GJ (2007) A biochemical approach to identifying microRNA targets. Proc Natl Acad Sci U S A 104(49):19291–19296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karube Y, Tanaka H, Osada H, Tomida S, Tatematsu Y, Yanagisawa K, Yatabe Y, Takamizawa J, Miyoshi S, Mitsudomi T, Takahashi T (2005) Reduced expression of Dicer associated with poor prognosis in lung cancer patients. Cancer Sci 96(2):111–115

    Article  CAS  PubMed  Google Scholar 

  • Kastenhuber ER, Lowe SW (2017) Putting p53 in context. Cell 170(6):1062–1078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaur S, Lotsari-Salomaa JE, Seppanen-Kaijansinkko R, Peltomaki P (2016) MicroRNA methylation in colorectal cancer. Adv Exp Med Biol 937:109–122

    Article  CAS  PubMed  Google Scholar 

  • Keck T, Brabletz T (2011) Under stress: p53 controls EMT and stemness in pancreatic epithelial cells. Cell Cycle 10(11):1715

    Article  CAS  PubMed  Google Scholar 

  • Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E (2007) The role of site accessibility in microRNA target recognition. Nat Genet 39(10):1278–1284

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14(4):R36

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim NH, Kim HS, Kim NG, Lee I, Choi HS, Li XY, Kang SE, Cha SY, Ryu JK, Na JM, Park C, Kim K, Lee S, Gumbiner BM, Yook JI, Weiss SJ (2011a) p53 and MicroRNA-34 are suppressors of canonical Wnt signaling. Sci Signal 4(197):ra71

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim NH, Kim HS, Li XY, Lee I, Choi HS, Kang SE, Cha SY, Ryu JK, Yoon D, Fearon ER, Rowe RG, Lee S, Maher CA, Weiss SJ, Yook JI (2011b) A p53/miRNA-34 axis regulates Snail1-dependent cancer cell epithelial-mesenchymal transition. J Cell Biol 195(3):417–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim T, Veronese A, Pichiorri F, Lee TJ, Jeon YJ, Volinia S, Pineau P, Marchio A, Palatini J, Suh SS, Alder H, Liu CG, Dejean A, Croce CM (2011c) p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J Exp Med 208(5):875–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klein U, Lia M, Crespo M, Siegel R, Shen Q, Mo T, Ambesi-Impiombato A, Califano A, Migliazza A, Bhagat G, Dalla-Favera R (2010) The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 17(1):28–40

    Article  CAS  PubMed  Google Scholar 

  • Kohlhammer H, Schwaenen C, Wessendorf S, Holzmann K, Kestler HA, Kienle D, Barth TF, Moller P, Ott G, Kalla J, Radlwimmer B, Pscherer A, Stilgenbauer S, Dohner H, Lichter P, Bentz M (2004) Genomic DNA-chip hybridization in t(11;14)-positive mantle cell lymphomas shows a high frequency of aberrations and allows a refined characterization of consensus regions. Blood 104(3):795–801

    Article  CAS  PubMed  Google Scholar 

  • Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N (2005) Combinatorial microRNA target predictions. Nat Genet 37(5):495–500

    Article  CAS  PubMed  Google Scholar 

  • Krell J, Stebbing J, Carissimi C, Dabrowska AF, de Giorgio A, Frampton AE, Harding V, Fulci V, Macino G, Colombo T, Castellano L (2016) TP53 regulates miRNA association with AGO2 to remodel the miRNA-mRNA interaction network. Genome Res 26(3):331–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krizhanovsky V, Lowe SW (2009) Stem cells: the promises and perils of p53. Nature 460(7259):1085–1086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kruse JP, Gu W (2009) Modes of p53 regulation. Cell 137(4):609–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kubo T, Toyooka S, Tsukuda K, Sakaguchi M, Fukazawa T, Soh J, Asano H, Ueno T, Muraoka T, Yamamoto H, Nasu Y, Kishimoto T, Pass HI, Matsui H, Huh NH, Miyoshi S (2011) Epigenetic silencing of microRNA-34b/c plays an important role in the pathogenesis of malignant pleural mesothelioma. Clin Cancer Res 17(15):4965–4974

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Lu Z, Takwi AA, Chen W, Callander NS, Ramos KS, Young KH, Li Y (2011) Negative regulation of the tumor suppressor p53 gene by microRNAs. Oncogene 30(7):843–853

    Article  CAS  PubMed  Google Scholar 

  • Kumar MS, Pester RE, Chen CY, Lane K, Chin C, Lu J, Kirsch DG, Golub TR, Jacks T (2009) Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev 23(23):2700–2704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar RM, Cahan P, Shalek AK, Satija R, Daley Keyser A, Li H, Zhang J, Pardee K, Gennert D, Trombetta JJ, Ferrante TC, Regev A, Daley GQ, Collins JJ (2014) Deconstructing transcriptional heterogeneity in pluripotent stem cells. Nature 516(7529):56–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • La T, Liu GZ, Farrelly M, Cole N, Feng YC, Zhang YY, Sherwin SK, Yari H, Tabatabaee H, Yan XG, Guo ST, Liu T, Thorne RF, Jin L, Zhang XD (2018) A p53-responsive miRNA network promotes cancer cell quiescence. Cancer Res 78(23):6666–6679

    Article  CAS  PubMed  Google Scholar 

  • Lagana A, Forte S, Giudice A, Arena MR, Puglisi PL, Giugno R, Pulvirenti A, Shasha D, Ferro A (2009) miRo: a miRNA knowledge base. Database (Oxford) 2009:bap008

    Article  CAS  Google Scholar 

  • Lal A, Thomas MP, Altschuler G, Navarro F, O'Day E, Li XL, Concepcion C, Han YC, Thiery J, Rajani DK, Deutsch A, Hofmann O, Ventura A, Hide W, Lieberman J (2011) Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling. PLoS Genet 7(11):e1002363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10(3):R25

    Article  PubMed  PubMed Central  Google Scholar 

  • Lataniotis L, Albrecht A, Kok FO, Monfries CAL, Benedetti L, Lawson ND, Hughes SM, Steinhofel K, Mayr M, Zampetaki A (2017) CRISPR/Cas9 editing reveals novel mechanisms of clustered microRNA regulation and function. Sci Rep 7(1):8585

    Article  PubMed  PubMed Central  Google Scholar 

  • Laudato S, Patil N, Abba ML, Leupold JH, Benner A, Gaiser T, Marx A, Allgayer H (2017) P53-induced miR-30e-5p inhibits colorectal cancer invasion and metastasis by targeting ITGA6 and ITGB1. Int J Cancer 141(9):1879–1890

    Article  CAS  PubMed  Google Scholar 

  • Law CW, Chen Y, Shi W, Smyth GK (2014) Voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol 15(2):R29

    Article  PubMed  PubMed Central  Google Scholar 

  • Leaderer D, Hoffman AE, Zheng T, Fu A, Weidhaas J, Paranjape T, Zhu Y (2011) Genetic and epigenetic association studies suggest a role of microRNA biogenesis gene exportin-5 (XPO5) in breast tumorigenesis. Int J Mol Epidemiol Genet 2(1):9–18

    CAS  PubMed  Google Scholar 

  • Lee KH, Lotterman C, Karikari C, Omura N, Feldmann G, Habbe N, Goggins MG, Mendell JT, Maitra A (2009) Epigenetic silencing of MicroRNA miR-107 regulates cyclin-dependent kinase 6 expression in pancreatic cancer. Pancreatology 9(3):293–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leite KR, Tomiyama A, Reis ST, Sousa-Canavez JM, Sanudo A, Camara-Lopes LH, Srougi M (2011) MicroRNA expression profiles in the progression of prostate cancer-from high-grade prostate intraepithelial neoplasia to metastasis. Urol Oncol

    Google Scholar 

  • Leucci E, Cocco M, Onnis A, De Falco G, van Cleef P, Bellan C, van Rijk A, Nyagol J, Byakika B, Lazzi S, Tosi P, van Krieken H, Leoncini L (2008) MYC translocation-negative classical Burkitt lymphoma cases: an alternative pathogenetic mechanism involving miRNA deregulation. J Pathol 216(4):440–450

    Article  CAS  PubMed  Google Scholar 

  • Leung AK, Sharp PA (2007) microRNAs: a safeguard against turmoil? Cell 130(4):581–585

    Article  CAS  PubMed  Google Scholar 

  • Leung AK, Sharp PA (2010) MicroRNA functions in stress responses. Mol Cell 40(2):205–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with burrows-Wheeler transform. Bioinformatics 25(14):1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Rokavec M, Jiang L, Horst D, Hermeking H (2017) Antagonistic effects of p53 and HIF1A on microRNA-34a regulation of PPP1R11 and STAT3 and Hypoxia-induced epithelial to mesenchymal transition in colorectal cancer cells. Gastroenterology 153(2):505–520

    Article  CAS  PubMed  Google Scholar 

  • Liberzon A (2014) A description of the molecular signatures database (MSigDB) web site. Methods Mol Biol 1150:153–160

    Article  CAS  PubMed  Google Scholar 

  • Liberzon A, Birger C, Thorvaldsdottir H, Ghandi M, Mesirov JP, Tamayo P (2015) The molecular signatures database (MSigDB) hallmark gene set collection. Cell Syst 1(6):417–425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, Brown D, Tang DG (2011) The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 17(2):211–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Zhang C, Zhao Y, Feng Z (2017) MicroRNA control of p53. J Cell Biochem 118(1):7–14

    Article  CAS  PubMed  Google Scholar 

  • Liu P (2018) MicroRNA expression analysis: next-generation sequencing. Methods Mol Biol 1783:171–183

    Article  PubMed  Google Scholar 

  • Lize M, Klimke A, Dobbelstein M (2011) MicroRNA-449 in cell fate determination. Cell Cycle 10(17):2874–2882

    Article  CAS  PubMed  Google Scholar 

  • Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Korner H, Knyazev P, Diebold J, Hermeking H (2008) Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 7(16):2591–2600

    Article  CAS  PubMed  Google Scholar 

  • Loganantharaj R, Randall TA (2017) The limitations of existing approaches in improving MicroRNA target prediction accuracy. Methods Mol Biol 1617:133–158

    Article  CAS  PubMed  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Baras AS, Halushka MK (2018) miRge 2.0 for comprehensive analysis of microRNA sequencing data. BMC Bioinformatics 19(1):275

    Article  PubMed  PubMed Central  Google Scholar 

  • Lujambio A, Calin GA, Villanueva A, Ropero S, Sanchez-Cespedes M, Blanco D, Montuenga LM, Rossi S, Nicoloso MS, Faller WJ, Gallagher WM, Eccles SA, Croce CM, Esteller M (2008) A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci U S A 105(36):13556–13561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mackowiak SD (2011) Identification of novel and known miRNAs in deep-sequencing data with miRDeep2. Curr Protoc Bioinformatics Chapter 12:Unit 12 10

    Google Scholar 

  • Martello G, Rosato A, Ferrari F, Manfrin A, Cordenonsi M, Dupont S, Enzo E, Guzzardo V, Rondina M, Spruce T, Parenti AR, Daidone MG, Bicciato S, Piccolo S (2010) A MicroRNA targeting dicer for metastasis control. Cell 141(7):1195–1207

    Article  CAS  PubMed  Google Scholar 

  • Martin MG, Payton JE, Link DC (2009) Dicer and outcomes in patients with acute myeloid leukemia (AML). Leuk Res 33(8):e127

    Article  PubMed  Google Scholar 

  • Marx V (2019) A dream of single-cell proteomics. Nat Methods 16(9):809–812

    Article  CAS  PubMed  Google Scholar 

  • Mayr C, Bartel DP (2009) Widespread shortening of 3'UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138(4):673–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayr C, Hemann MT, Bartel DP (2007) Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 315(5818):1576–1579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melo SA, Moutinho C, Ropero S, Calin GA, Rossi S, Spizzo R, Fernandez AF, Davalos V, Villanueva A, Montoya G, Yamamoto H, Schwartz S Jr, Esteller M (2010) A genetic defect in exportin-5 traps precursor microRNAs in the nucleus of cancer cells. Cancer Cell 18(4):303–315

    Article  CAS  PubMed  Google Scholar 

  • Menendez D, Inga A, Resnick MA (2009) The expanding universe of p53 targets. Nat Rev Cancer 9(10):724–737

    Article  CAS  PubMed  Google Scholar 

  • Merritt WM, Lin YG, Han LY, Kamat AA, Spannuth WA, Schmandt R, Urbauer D, Pennacchio LA, Cheng JF, Nick AM, Deavers MT, Mourad-Zeidan A, Wang H, Mueller P, Lenburg ME, Gray JW, Mok S, Birrer MJ, Lopez-Berestein G, Coleman RL, Bar-Eli M, Sood AK (2008) Dicer, Drosha, and outcomes in patients with ovarian cancer. N Engl J Med 359(25):2641–2650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Migliore C, Petrelli A, Ghiso E, Corso S, Capparuccia L, Eramo A, Comoglio PM, Giordano S (2008) MicroRNAs impair MET-mediated invasive growth. Cancer Res 68(24):10128–10136

    Article  CAS  PubMed  Google Scholar 

  • Miranda KC, Huynh T, Tay Y, Ang YS, Tam WL, Thomson AM, Lim B, Rigoutsos I (2006) A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 126(6):1203–1217

    Article  CAS  PubMed  Google Scholar 

  • Morales S, Monzo M, Navarro A (2017) Epigenetic regulation mechanisms of microRNA expression. Biomol Concepts 8(5-6):203–212

    Article  CAS  PubMed  Google Scholar 

  • Mudhasani R, Zhu Z, Hutvagner G, Eischen CM, Lyle S, Hall LL, Lawrence JB, Imbalzano AN, Jones SN (2008) Loss of miRNA biogenesis induces p19Arf-p53 signaling and senescence in primary cells. J Cell Biol 181(7):1055–1063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Musumeci M, Coppola V, Addario A, Patrizii M, Maugeri-Sacca M, Memeo L, Colarossi C, Francescangeli F, Biffoni M, Collura D, Giacobbe A, D'Urso L, Falchi M, Venneri MA, Muto G, De Maria R, Bonci D (2011) Control of tumor and microenvironment cross-talk by miR-15a and miR-16 in prostate cancer. Oncogene 30(41):4231–4242

    Article  CAS  PubMed  Google Scholar 

  • Neves R, Scheel C, Weinhold S, Honisch E, Iwaniuk KM, Trompeter HI, Niederacher D, Wernet P, Santourlidis S, Uhrberg M (2010) Role of DNA methylation in miR-200c/141 cluster silencing in invasive breast cancer cells. BMC Res Notes 3:219

    Article  PubMed  PubMed Central  Google Scholar 

  • Nishida N, Yokobori T, Mimori K, Sudo T, Tanaka F, Shibata K, Ishii H, Doki Y, Kuwano H, Mori M (2011) MicroRNA miR-125b is a prognostic marker in human colorectal cancer. Int J Oncol 38(5):1437–1443

    CAS  PubMed  Google Scholar 

  • Oner MG, Rokavec M, Kaller M, Bouznad N, Horst D, Kirchner T, Hermeking H (2018) Combined inactivation of TP53 and MIR34A promotes colorectal cancer development and progression in mice via increasing levels of IL6R and PAI1. Gastroenterology 155(6):1868–1882

    Article  PubMed  Google Scholar 

  • Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1(5):376–386

    Article  CAS  PubMed  Google Scholar 

  • Orom UA, Lund AH (2007) Isolation of microRNA targets using biotinylated synthetic microRNAs. Methods 43(2):162–165

    Article  CAS  PubMed  Google Scholar 

  • Orom UA, Lund AH (2010) Experimental identification of microRNA targets. Gene 451(1-2):1–5

    Article  PubMed  Google Scholar 

  • Ory B, Ellisen LW (2011) A microRNA-dependent circuit controlling p63/p73 homeostasis: p53 family cross-talk meets therapeutic opportunity. Oncotarget 2(3):259–264

    Article  PubMed  PubMed Central  Google Scholar 

  • Pallasch CP, Patz M, Park YJ, Hagist S, Eggle D, Claus R, Debey-Pascher S, Schulz A, Frenzel LP, Claasen J, Kutsch N, Krause G, Mayr C, Rosenwald A, Plass C, Schultze JL, Hallek M, Wendtner CM (2009) miRNA deregulation by epigenetic silencing disrupts suppression of the oncogene PLAG1 in chronic lymphocytic leukemia. Blood 114(15):3255–3264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pichiorri F, Suh SS, Rocci A, De Luca L, Taccioli C, Santhanam R, Zhou W, Benson DM Jr, Hofmainster C, Alder H, Garofalo M, Di Leva G, Volinia S, Lin HJ, Perrotti D, Kuehl M, Aqeilan RI, Palumbo A, Croce CM (2010) Downregulation of p53-inducible microRNAs 192, 194, and 215 impairs the p53/MDM2 autoregulatory loop in multiple myeloma development. Cancer Cell 18(4):367–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porkka KP, Ogg EL, Saramaki OR, Vessella RL, Pukkila H, Lahdesmaki H, van Weerden WM, Wolf M, Kallioniemi OP, Jenster G, Visakorpi T (2011) The miR-15a-miR-16-1 locus is homozygously deleted in a subset of prostate cancers. Genes Chromosomes Cancer 50(7):499–509

    Article  CAS  PubMed  Google Scholar 

  • Prosser HM, Koike-Yusa H, Cooper JD, Law FC, Bradley A (2011) A resource of vectors and ES cells for targeted deletion of microRNAs in mice. Nat Biotechnol 29(9):840–845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rakheja D, Chen KS, Liu Y, Shukla AA, Schmid V, Chang TC, Khokhar S, Wickiser JE, Karandikar NJ, Malter JS, Mendell JT, Amatruda JF (2014) Somatic mutations in DROSHA and DICER1 impair microRNA biogenesis through distinct mechanisms in Wilms tumours. Nat Commun 2:4802

    Article  CAS  PubMed  Google Scholar 

  • Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N, Bentwich Z, Oren M (2007) Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 26(5):731–743

    Article  CAS  PubMed  Google Scholar 

  • Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10(10):1507–1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riley T, Sontag E, Chen P, Levine A (2008) Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 9(5):402–412

    Article  CAS  PubMed  Google Scholar 

  • Roberts JT, Borchert GM (2017) Computational prediction of MicroRNA target genes, target prediction databases, and web resources. Methods Mol Biol 1617:109–122

    Article  CAS  PubMed  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140

    Article  CAS  PubMed  Google Scholar 

  • Rokavec M, Li H, Jiang L, Hermeking H (2014a) The p53/miR-34 axis in development and disease. J Mol Cell Biol 6(3):214–230

    Article  CAS  PubMed  Google Scholar 

  • Rokavec M, Oner MG, Li H, Jackstadt R, Jiang L, Lodygin D, Kaller M, Horst D, Ziegler PK, Schwitalla S, Slotta-Huspenina J, Bader FG, Greten FR, Hermeking H (2014b) IL-6R/STAT3/miR-34a feedback loop promotes EMT-mediated colorectal cancer invasion and metastasis. J Clin Invest 124(4):1853–1867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rokavec M, Bouznad N, Hermeking H (2019) Paracrine induction of epithelial-mesenchymal transition between colorectal cancer cells and its suppression by a p53/miR-192/215/NID1 axis. Cell Mol Gastroenterol Hepatol 7(4):783–802

    Article  PubMed  PubMed Central  Google Scholar 

  • Roldo C, Missiaglia E, Hagan JP, Falconi M, Capelli P, Bersani S, Calin GA, Volinia S, Liu CG, Scarpa A, Croce CM (2006) MicroRNA expression abnormalities in pancreatic endocrine and acinar tumors are associated with distinctive pathologic features and clinical behavior. J Clin Oncol 24(29):4677–4684

    Article  CAS  PubMed  Google Scholar 

  • Rubio-Somoza I, Weigel D, Franco-Zorilla JM, Garcia JA, Paz-Ares J (2011) ceRNAs: miRNA target mimic mimics. Cell 147(7):1431–1432

    Article  CAS  PubMed  Google Scholar 

  • Sachdeva M, Zhu S, Wu F, Wu H, Walia V, Kumar S, Elble R, Watabe K, Mo YY (2009) p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc Natl Acad Sci U S A 106(9):3207–3212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011) A ceRNA hypothesis: the Rosetta stone of a hidden RNA language? Cell 146(3):353–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmiedel JM, Klemm SL, Zheng Y, Sahay A, Bluthgen N, Marks DS, van Oudenaarden A (2015) Gene expression. MicroRNA control of protein expression noise. Science 348(6230):128–132

    Article  CAS  PubMed  Google Scholar 

  • Schubert J, Brabletz T (2011) p53 spreads out further: suppression of EMT and stemness by activating miR-200c expression. Cell Res 21(5):705–707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455(7209):58–63

    Article  CAS  PubMed  Google Scholar 

  • Shi L, Jackstadt R, Siemens H, Li H, Kirchner T, Hermeking H (2014) p53-induced miR-15a/16-1 and AP4 form a double-negative feedback loop to regulate epithelial-mesenchymal transition and metastasis in colorectal cancer. Cancer Res 74(2):532–542

    Article  CAS  PubMed  Google Scholar 

  • Shi X, Kaller M, Rokavec M, Kirchner T, Horst D, Hermeking H (2020) Characterization of a p53/miR-34a/CSF1R/STAT3 feedback loop in colorectal cancer. Cell Mol Gastroenterol Hepatol 10(2):391–418

    Article  PubMed  PubMed Central  Google Scholar 

  • Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D, Diehn M, Liu H, Panula SP, Chiao E, Dirbas FM, Somlo G, Pera RA, Lao K, Clarke MF (2009) Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 138(3):592–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shinozaki A, Sakatani T, Ushiku T, Hino R, Isogai M, Ishikawa S, Uozaki H, Takada K, Fukayama M (2010) Downregulation of microRNA-200 in EBV-associated gastric carcinoma. Cancer Res 70(11):4719–4727

    Article  CAS  PubMed  Google Scholar 

  • Siemens H, Jackstadt R, Hunten S, Kaller M, Menssen A, Gotz U, Hermeking H (2011) miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 10(24)

    Google Scholar 

  • Smeenk L, van Heeringen SJ, Koeppel M, van Driel MA, Bartels SJ, Akkers RC, Denissov S, Stunnenberg HG, Lohrum M (2008) Characterization of genome-wide p53-binding sites upon stress response. Nucleic Acids Res 36(11):3639–3654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snuderl M, Kannan K, Pfaff E, Wang S, Stafford JM, Serrano J, Heguy A, Ray K, Faustin A, Aminova O, Dolgalev I, Stapleton SL, Zagzag D, Chiriboga L, Gardner SL, Wisoff JH, Golfinos JG, Capper D, Hovestadt V, Rosenblum MK, Placantonakis DG, LeBoeuf SE, Papagiannakopoulos TY, Chavez L, Ahsan S, Eberhart CG, Pfister SM, Jones DTW, Karajannis MA (2018) Recurrent homozygous deletion of DROSHA and microduplication of PDE4DIP in pineoblastoma. Nat Commun 9(1):2868

    Article  PubMed  PubMed Central  Google Scholar 

  • Soussi T (2011) TP53 mutations in human cancer: database reassessment and prospects for the next decade. Adv Cancer Res 110:107–139

    Article  CAS  PubMed  Google Scholar 

  • Sticht C, De La Torre C, Parveen A, Gretz N (2018) miRWalk: an online resource for prediction of microRNA binding sites. PLoS One 13(10):e0206239

    Article  PubMed  PubMed Central  Google Scholar 

  • Stilgenbauer S, Nickolenko J, Wilhelm J, Wolf S, Weitz S, Dohner K, Boehm T, Dohner H, Lichter P (1998) Expressed sequences as candidates for a novel tumor suppressor gene at band 13q14 in B-cell chronic lymphocytic leukemia and mantle cell lymphoma. Oncogene 16(14):1891–1897

    Article  CAS  PubMed  Google Scholar 

  • Su X, Chakravarti D, Cho MS, Liu L, Gi YJ, Lin YL, Leung ML, El-Naggar A, Creighton CJ, Suraokar MB, Wistuba I, Flores ER (2010) TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature 467(7318):986–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102(43):15545–15550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suh SO, Chen Y, Zaman MS, Hirata H, Yamamura S, Shahryari V, Liu J, Tabatabai ZL, Kakar S, Deng G, Tanaka Y, Dahiya R (2011) MicroRNA-145 is regulated by DNA methylation and p53 gene mutation in prostate cancer. Carcinogenesis 32(5):772–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki H, Yamamoto E, Nojima M, Kai M, Yamano HO, Yoshikawa K, Kimura T, Kudo T, Harada E, Sugai T, Takamaru H, Niinuma T, Maruyama R, Yamamoto H, Tokino T, Imai K, Toyota M, Shinomura Y (2010) Methylation-associated silencing of microRNA-34b/c in gastric cancer and its involvement in an epigenetic field defect. Carcinogenesis 31(12):2066–2073

    Article  CAS  PubMed  Google Scholar 

  • Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K (2009) Modulation of microRNA processing by p53. Nature 460(7254):529–533

    Article  CAS  PubMed  Google Scholar 

  • Swarbrick A, Woods SL, Shaw A, Balakrishnan A, Phua Y, Nguyen A, Chanthery Y, Lim L, Ashton LJ, Judson RL, Huskey N, Blelloch R, Haber M, Norris MD, Lengyel P, Hackett CS, Preiss T, Chetcuti A, Sullivan CS, Marcusson EG, Weiss W, L'Etoile N, Goga A (2010) miR-380-5p represses p53 to control cellular survival and is associated with poor outcome in MYCN-amplified neuroblastoma. Nat Med 16(10):1134–1140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A, Meister G, Hermeking H (2007) Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 6(13):1586–1593

    Article  CAS  PubMed  Google Scholar 

  • 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 (2011) Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell 147(2):344–357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tay Y, Tan SM, Karreth FA, Lieberman J, Pandolfi PP (2014) Characterization of dual PTEN and p53-targeting microRNAs identifies microRNA-638/Dnm2 as a two-hit oncogenic locus. Cell Rep 8(3):714–722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tazawa H, Tsuchiya N, Izumiya M, Nakagama H (2007) Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci U S A 104(39):15472–15477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tellez CS, Juri DE, Do K, Bernauer AM, Thomas CL, Damiani LA, Tessema M, Leng S, Belinsky SA (2011) EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res 71(8):3087–3097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thorstensen L, Qvist H, Heim S, Liefers GJ, Nesland JM, Giercksky KE, Lothe RA (2000) Evaluation of 1p losses in primary carcinomas, local recurrences and peripheral metastases from colorectal cancer patients. Neoplasia 2(6):514–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian S, Huang S, Wu S, Guo W, Li J, He X (2010) MicroRNA-1285 inhibits the expression of p53 by directly targeting its 3′ untranslated region. Biochem Biophys Res Commun 396(2):435–439

    Article  CAS  PubMed  Google Scholar 

  • Torrezan GT, Ferreira EN, Nakahata AM, Barros BD, Castro MT, Correa BR, Krepischi AC, Olivieri EH, Cunha IW, Tabori U, Grundy PE, Costa CM, de Camargo B, Galante PA, Carraro DM (2014) Recurrent somatic mutation in DROSHA induces microRNA profile changes in Wilms tumour. Nat Commun 5:4039

    Article  CAS  PubMed  Google Scholar 

  • Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y, Tokino T (2008) Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res 68(11):4123–4132

    Article  CAS  PubMed  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velculescu VE, Zhang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene expression. Science 270(5235):484–487

    Article  CAS  PubMed  Google Scholar 

  • Vistain LF, Tay S (2021) Single-cell proteomics. Trends Biochem Sci:S0968-0004(0921)00027-X.

    Google Scholar 

  • Vogelstein B, Lane D, Levine AJ (2000) Surfing the p53 network. Nature 408(6810):307–310

    Article  CAS  PubMed  Google Scholar 

  • Vogt M, Munding J, Gruner M, Liffers ST, Verdoodt B, Hauk J, Steinstraesser L, Tannapfel A, Hermeking H (2011) Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch 458:313–322

    Article  PubMed  Google Scholar 

  • Vousden KH, Prives C (2009) Blinded by the light: the growing complexity of p53. Cell 137(3):413–431

    Article  CAS  PubMed  Google Scholar 

  • Vousden KH, Ryan KM (2009) p53 and metabolism. Nat Rev Cancer 9(10):691–700

    Article  CAS  PubMed  Google Scholar 

  • Wada M, Okamura T, Okada M, Teramura M, Masuda M, Motoji T, Mizoguchi H (1999) Frequent chromosome arm 13q deletion in aggressive non-Hodgkin's lymphoma. Leukemia 13(5):792–798

    Article  CAS  PubMed  Google Scholar 

  • Walz AL, Ooms A, Gadd S, Gerhard DS, Smith MA, Guidry Auvil JM, Meerzaman D, Chen QR, Hsu CH, Yan C, Nguyen C, Hu Y, Bowlby R, Brooks D, Ma Y, Mungall AJ, Moore RA, Schein J, Marra MA, Huff V, Dome JS, Chi YY, Mullighan CG, Ma J, Wheeler DA, Hampton OA, Jafari N, Ross N, Gastier-Foster JM, Perlman EJ (2015) Recurrent DGCR8, DROSHA, and SIX homeodomain mutations in favorable histology Wilms tumors. Cancer Cell 27(2):286–297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang N, Zheng J, Chen Z, Liu Y, Dura B, Kwak M, Xavier-Ferrucio J, Lu YC, Zhang M, Roden C, Cheng J, Krause DS, Ding Y, Fan R, Lu J (2019) Single-cell microRNA-mRNA co-sequencing reveals non-genetic heterogeneity and mechanisms of microRNA regulation. Nat Commun 10(1):95

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Chen Z, Gao Y, Li N, Li B, Tan F, Tan X, Lu N, Sun Y, Sun J, Sun N, He J (2011) DNA hypermethylation of microRNA-34b/c has prognostic value for stage non-small cell lung cancer. Cancer Biol Ther 11(5):490–496

    Article  CAS  PubMed  Google Scholar 

  • Wegert J, Ishaque N, Vardapour R, Georg C, Gu Z, Bieg M, Ziegler B, Bausenwein S, Nourkami N, Ludwig N, Keller A, Grimm C, Kneitz S, Williams RD, Chagtai T, Pritchard-Jones K, van Sluis P, Volckmann R, Koster J, Versteeg R, Acha T, O'Sullivan MJ, Bode PK, Niggli F, Tytgat GA, van Tinteren H, van den Heuvel-Eibrink MM, Meese E, Vokuhl C, Leuschner I, Graf N, Eils R, Pfister SM, Kool M, Gessler M (2015) Mutations in the SIX1/2 pathway and the DROSHA/DGCR8 miRNA microprocessor complex underlie high-risk blastemal type Wilms tumors. Cancer Cell 27(2):298–311

    Article  CAS  PubMed  Google Scholar 

  • Wei CL, Wu Q, Vega VB, Chiu KP, Ng P, Zhang T, Shahab A, Yong HC, Fu Y, Weng Z, Liu J, Zhao XD, Chew JL, Lee YL, Kuznetsov VA, Sung WK, Miller LD, Lim B, Liu ET, Yu Q, Ng HH, Ruan Y (2006) A global map of p53 transcription-factor binding sites in the human genome. Cell 124(1):207–219

    Article  CAS  PubMed  Google Scholar 

  • Welch C, Chen Y, Stallings RL (2007) MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 26(34):5017–5022

    Article  CAS  PubMed  Google Scholar 

  • Wiklund ED, Bramsen JB, Hulf T, Dyrskjot L, Ramanathan R, Hansen TB, Villadsen SB, Gao S, Ostenfeld MS, Borre M, Peter ME, Orntoft TF, Kjems J, Clark SJ (2011) Coordinated epigenetic repression of the miR-200 family and miR-205 in invasive bladder cancer. Int J Cancer 128(6):1327–1334

    Article  CAS  PubMed  Google Scholar 

  • Wong TS, Liu XB, Wong BY, Ng RW, Yuen AP, Wei WI (2008) Mature miR-184 as potential oncogenic microRNA of squamous cell carcinoma of tongue. Clin Cancer Res 14(9):2588–2592

    Article  CAS  PubMed  Google Scholar 

  • Xi Y, Formentini A, Chien M, Weir DB, Russo JJ, Ju J, Kornmann M (2006) Prognostic values of microRNAs in colorectal cancer. Biomark Insights 2:113–121

    PubMed  Google Scholar 

  • Xiao J, Lin H, Luo X, Wang Z (2011) miR-605 joins p53 network to form a p53:miR-605:Mdm2 positive feedback loop in response to stress. EMBO J 30(3):524–532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS (2009) MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137(4):647–658

    Article  CAS  PubMed  Google Scholar 

  • Yamakuchi M, Ferlito M, Lowenstein CJ (2008) miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci U S A 105(36):13421–13426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamakuchi M, Lotterman CD, Bao C, Hruban RH, Karim B, Mendell JT, Huso D, Lowenstein CJ (2010) P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proc Natl Acad Sci U S A 107(14):6334–6339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XJ, Ye H, Zeng CW, He B, Zhang H, Chen YQ (2010) Dysregulation of miR-15a and miR-214 in human pancreatic cancer. J Hematol Oncol 3:46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Lammers P, Torrance CJ, Bader AG (2013) TP53-independent function of miR-34a via HDAC1 and p21(CIP1/WAF1.). Mol Ther 21(9):1678–1686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank the members of the Hermeking Lab for discussions. Work in HH’s lab is supported by the Wilhelm-Sander-Stiftung, the Rudolf-Bartling-Stiftung, the Deutsche Krebshilfe, and the Deutsche Forschungsgemeinschaft (DFG).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Heiko Hermeking .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kaller, M., Hünten, S., Siemens, H., Hermeking, H. (2022). Analysis of the p53/microRNA Network in Cancer. In: Schmitz, U., Wolkenhauer, O., Vera-González, J. (eds) Systems Biology of MicroRNAs in Cancer. Advances in Experimental Medicine and Biology, vol 1385. Springer, Cham. https://doi.org/10.1007/978-3-031-08356-3_7

Download citation

Publish with us

Policies and ethics