Our Publications


Kozlovski I, Agami R.
More or less - the same? mRNA fluctuations are balanced during translation.
EMBO J. 2019 Dec 2;38(23):e103651.

Sun J, Nagel R, Zaal EA, Ugalde AP, Han R, Proost N, Song JY, Pataskar A, Burylo A, Fu H, Poelarends GJ, van de Ven M, van Tellingen O, Berkers CR, Agami R.
SLC1A3 contributes to L-asparaginase resistance in solid tumors.
EMBO J. 2019 Oct 4;38(21):e102147. doi: 10.15252/embj.2019102147.

Korkmaz G, Manber Z, Lopes R, Prekovic S, Schuurman K, Kim Y, Teunissen H, Flach K, Wit E, Galli GG, Zwart W, Elkon R, Agami R.
A CRISPR-Cas9 screen identifies essential CTCF anchor sites for estrogen receptor-driven breast cancer cell proliferation.
Nucleic Acids Res. 2019 Oct 10;47(18):9557-9572. doi: 10.1093/nar/gkz675.

Milne K, Sun J, Zaal EA, Mowat J, Celie PHN, Fish A, Berkers CR, Forlani G, Loayza-Puch F, Jamieson C, Agami R.
A fragment-like approach to PYCR1 inhibition.
Bioorg Med Chem Lett. 2019 Sep 15;29(18):2626-2631.

Kampen KR, Fancello L, Girardi T, Rinaldi G, Planque M, Sulima SO, Loayza-Puch F, Verbelen B, Vereecke S, Verbeeck J, Op de Beeck J, Royaert J, Vermeersch P, Cassiman D, Cools J, Agami R, Fiers M, Fendt SM, De Keersmaecker K.
Translatome analysis reveals altered serine and glycine metabolism in T-cell acute lymphoblastic leukemia cells.
Nat Commun. 2019 Jun 11;10(1):2542. doi: 10.1038/s41467-019-10508-2.

Gregersen LH, Mitter R, Ugalde AP, Nojima T, Proudfoot NJ, Agami R, Stewart A, Svejstrup JQ.
SCAF4 and SCAF8, mRNA Anti-Terminator Proteins.
Cell. 2019 Jun 13;177(7):1797-1813.e18. doi: 10.1016/j.cell.2019.04.038.


Kozlovski I, Agami R.
Queuing up the ribosome: nutrition and the microbiome control protein synthesis.
EMBO J. 2018 Sep 14;37(18). pii: e100405.

Lopes R, Korkmaz G, Revilla SA, van Vliet R, Nagel R, Custers L, Kim Y, van Breugel PC, Zwart W, Moumbeini B, Manber Z, Elkon R, Agami R.
CUEDC1 is a primary target of ERa essential for the growth of breast cancer cells.
Cancer Lett. 2018 Nov 1;436:87-95.

Han R, Li L, Ugalde AP, Tal A, Manber Z, Barbera EP, Chiara VD, Elkon R, Agami R.
Functional CRISPR screen identifies AP1-associated enhancer regulating FOXF1 to modulate oncogene-induced senescence.
Genome Biol. 2018 Aug 17;19(1):118.

Li L, van Breugel PC, Loayza-Puch F, Ugalde AP, Korkmaz G, Messika-Gold N, Han R, Lopes R, Barbera EP, Teunissen H, de Wit E, Soares RJ, Nielsen BS, Holmstrøm K, Martínez-Herrera DJ, Huarte M, Louloupi A, Drost J, Elkon R, Agami R.
LncRNA-OIS1 regulates DPP4 activation to modulate senescence induced by RAS..
Nucleic Acids Res. 2018 Feb 22. doi: 10.1093/nar/gky087.

Gavish-Izakson M, Velpula BB, Elkon R, Prados-Carvajal R, Barnabas GD, Ugalde AP, Agami R, Geiger T, Huertas P, Ziv Y, Shiloh Y.
Nuclear poly(A)-binding protein 1 is an ATM target and essential for DNA double-strand break repair.
Nucleic Acids Res. 2018 Jan 25;46(2):730-747.

Huang Q, Yan J, Agami R.
Long non-coding RNAs in metastasis.
Cancer Metastasis Rev. 2018 Mar;37(1):75-81.


Han R, Slobodin B, Agami R.
The methylated way to translation.
Oncotarget. 2017 Oct 25;8(55):93313-93314.

Elkon R, Agami R.
Characterization of noncoding regulatory DNA in the human genome.
Nat Biotechnol. 2017 Aug 8;35(8):732-746.

Slobodin B, Han R, Calderone V, Vrielink JA, Loayza-Puch F, Elkon R, Agami R.
Transcription Impacts the Efficiency of mRNA Translation via Co-transcriptional N6-adenosine Methylation.
Cell. 2017 Apr 6;169(2):326-337.e12.

Lopes R, Agami R, Korkmaz G.
GRO-seq, A Tool for Identification of Transcripts Regulating Gene Expression.
Nat Rev Mol Cell Biol. 2016 Sep;17(9):597-604.

Loayza-Puch F, Rooijers K, Zijlstra J, Moumbeini B, Zaal EA, Oude Vrielink JF, Lopes R, Ugalde AP, Berkers CR, Agami R.
TGFβ1-induced leucine limitation uncovered by differential ribosome codon reading.
Methods Mol Biol. 2017;1543:45-55


Lopes R, Korkmaz G, Agami R.
Applying CRISPR-Cas9 tools to identify and characterize transcriptional enhancers.
Nat Rev Mol Cell Biol. 2016 Sep;17(9):597-604.

Loayza-Puch F, Agami R.
Monitoring amino acid deficiencies in cancer.
Cell Cycle. 2016 Sep;15(17):2229-30.

Loayza-Puch F, Rooijers K, Buil LC, Zijlstra J, F Oude Vrielink J, Lopes R, Ugalde AP, van Breugel P, Hofland I, Wesseling J, van Tellingen O, Bex A, Agami R.
Tumour-specific proline vulnerability uncovered by differential ribosome codon reading.
Nature. 2016 Feb 15. doi: 10.1038/nature16982.

Hoffman Y, Bublik DR, Ugalde AP, Elkon R, Biniashvili T, Agami R, Oren M, Pilpel Y.
3'UTR Shortening Potentiates MicroRNA-Based Repression of Pro-differentiation Genes in Proliferating Human Cells.
PLoS Genet. 2016 Aug;12(8):e1006254.

Korkmaz G, Lopes R, Ugalde AP, Nevedomskaya E, Han R, Myacheva K, Zwart W, Elkon R, Agami R.
Functional genetic screens for enhancer elements in the human genome using CRISPR-Cas9.
Nat Biotechnol. 2016 Jan 11.

Paper highlighted in TheScientist Finding Enhancers with CRISPR
News and Views Mapping regulatory elements

Melo CA, Léveillé N, Rooijers K, Wijchers PJ, Geeven G, Tal A, Melo SA, de Laat W, Agami R.
A p53-bound enhancer region controls a long intergenic noncoding RNA required for p53 stress response.
Oncogene. 2016 Jan 18.


Creemers EE, Bawazeer AC, Ugalde AP, van Deutekom HW, van der Made I, de Groot NE, Adriaens ME, Cook S, Bezzina C, Hübner N, van der Velden J, Elkon R, Agami R, Pinto YM.
Genome-Wide Polyadenylation Maps Reveal Dynamic mRNA 3'-End Formation in the Failing Human Heart.
Circ Res. 2015 Dec 15.

Elkon R, Loayza-Puch F, Korkmaz G, Lopes R, van Breugel PC, Bleijerveld OB, Altelaar AM, Wolf E, Lorenzin F, Eilers M, Agami R.
Myc coordinates transcription and translation to enhance transformation and suppress invasiveness.
EMBO Rep. 2015 Nov 4.

Konovalova S, Hilander T, Loayza-Puch F, Rooijers K, Agami R, Tyynismaa H.
Exposure to arginine analog canavanine induces aberrant mitochondrial translation products, mitoribosome stalling, and instability of the mitochondrial proteome.
Int J Biochem Cell Biol. 2015 Aug;

Léveillé N, Melo CA, Agami R.
Enhancer-associated RNAs as therapeutic targets.
Expert Opin Biol Ther. 2015 May;15

Léveillé N, Melo CA, Rooijers K, Díaz-Lagares A, Melo SA, Korkmaz G, Lopes R, Akbari Moqadam F, Maia AR, Wijchers PJ, Geeven G, den Boer ML, Kalluri R, de Laat W, Esteller M, Agami R.
Genome-wide profiling of p53-regulated enhancer RNAs uncovers a subset of enhancers controlled by a lncRNA.
Nat Commun. 2015 Mar 27


Dinami R, Ercolani C, Petti E, Piazza S, Ciani Y, Sestito R, Sacconi A, Biagioni F, le Sage C, Agami R, Benetti R, Mottolese M, Schneider C, Blandino G, Schoeftner S.
miR-155 drives telomere fragility in human breast cancer by targeting TRF1.
NCancer Res. 2014 Aug 1;74(15):4145-56.


Loayza-Puch F, Agami R.
Lncing protein translation to metastasis.
EMBO J. 2013 Oct 16

Rooijers K, Loayza-Puch F, Nijtmans LG, Agami R.
Ribosome profiling reveals features of normal and disease-associated mitochondrial translation.
Nat Commun. 2013

Melo CA, Léveillé N, Agami R.
eRNAs reach the heart of transcription.
Cell Res. 2013 Oct

Elkon R, Ugalde AP, Agami R.
Alternative cleavage and polyadenylation: extent, regulation and function.
Nat Rev Genet. 2013 Jul

Lieberman J, Slack F, Pandolfi PP, Chinnaiyan A, Agami R, Mendell JT.
Noncoding RNAs and cancer.
Cell. 2013 Mar 28

Loayza-Puch F, Drost J, Rooijers K, Lopes R, Elkon R, Agami R.
p53 induces transcriptional and translational programs to suppress cell proliferation and growth.
Genome Biol. 2013 Apr 17

Melo, C.A., Drost, J., Wijchers, P.J., van de Werken, H., de Wit, E., Vrielink, J.A., Elkon, R., Melo, S.A., Leveille, N., Kalluri, R., de Laat, W., and Agami, R.
eRNAs Are Required for p53-Dependent Enhancer Activity and Gene Transcription.
Molecular Cell 2013 Feb 7.


Morris AR, Bos A, Diosdado B, Rooijers K, Elkon R, Bolijn AS, Carvalho B, Meijer GA, Agami R.
Alternative Cleavage and Polyadenylation during Colorectal Cancer Development.
Clin Cancer Res. 2012 Oct 1;18(19):5256-66. doi: 10.1158/1078-0432.CCR-12-0543. Epub 2012 Aug 8.

Elkon R, Drost J, van Haaften G, Jenal M, Schrier M, Vrielink JA, Agami R.
E2F mediates enhanced alternative polyadenylation in proliferation.
Genome Biol. 2012 Jul 2;13(7):R59. [Epub ahead of print]

Jenal M, Elkon R, Loayza-Puch F, van Haaften G, Kühn U, Menzies FM, Vrielink JA, Bos AJ, Drost J, Rooijers K, Rubinsztein DC, Agami R.
The poly(a)-binding protein nuclear 1 suppresses alternative cleavage and polyadenylation sites.
Cell. 2012 Apr 27;149(3):538-53. Epub 2012 Apr 12.

Wilting SM, Snijders PJ, Verlaat W, Jaspers A, van de Wiel MA, van Wieringen WN, Meijer GA, Kenter GG, Yi Y, le Sage C, Agami R, Meijer CJ, Steenbergen RD.
Altered microRNA expression associated with chromosomal changes contributes to cervical carcinogenesis.
Oncogene. 2012 Feb 13.

Korkmaz G, le Sage C, Tekirdag KA, Agami R, Gozuacik D.
AmiR-376b controls starvation and mTOR inhibition-related autophagy by targeting ATG4C and BECN1.
Autophagy. 2012 Feb 1;8(2):165-76.


Léveillé N, Elkon R, Davalos V, Manoharan V, Hollingworth D, Oude Vrielink J, le Sage C, Melo CA, Horlings HM, Wesseling J, Ule J, Esteller M, Ramos A, Agami R.
Selective inhibition of microRNA accessibility by RBM38 is required for p53 activity.
Nat Commun. 2011 Oct 25;2:513. doi: 10.1038/ncomms1519.

Gomez-Benito M, Loayza-Puch F, Oude Vrielink JA, Odero MD, Agami R.
3'UTR-mediated gene silencing of the Mixed Lineage Leukemia (MLL) gene.
PLoS One. 2011;6(10):e25449.

van Kouwenhove M, Kedde M, Agami R.
MicroRNA regulation by RNA-binding proteins and its implications for cancer.
Nat Rev Cancer. 2011 Aug 5;11(9):644-56. doi: 10.1038/nrc3107. Review.<

Denby L, Ramdas V, McBride MW, Wang J, Robinson H, McClure J, Crawford W, Lu R, Hillyard DZ, Khanin R, Agami R, Dominiczak AF, Sharpe CC, Baker AH.
miR-21 and miR-214 are consistently modulated during renal injury in rodent models.
Am J Pathol. 2011 Aug;179(2):661-72. Epub 2011 May 31.

Lerner M, Lundgren J, Akhoondi S, Jahn A, Ng HF, Moqadam FA, Oude Vrielink JA, Agami R, Den Boer ML, Grandér D, Sangfelt O.
MiRNA-27a controls FBW7/hCDC4-dependent cyclin E degradation and cell cycle progression.
Cell Cycle. 2011 Jul 1;10(13):2172-83. Epub 2011 Jul 1.

Caporali A, Meloni M, Völlenkle C, Bonci D, Sala-Newby GB, Addis R, Spinetti G, Losa S, Masson R, Baker AH, Agami R, le Sage C, Condorelli G, Madeddu P, Martelli F, Emanueli C.
Deregulation of microRNA-503 contributes to diabetes mellitus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia.
Circulation. 2011 Jan 25;123(3):282-91. Epub 2011 Jan 10 :->


Kedde M, van Kouwenhove M, Zwart W, Oude Vrielink JA, Elkon R, Agami R.
A Pumilio-induced RNA structure switch in p27-3' UTR controls miR-221 and miR-222 accessibility.
Nat Cell Biol. 2010 Sep 5. :-> PDF

Mantovani F, Drost J, Voorhoeve PM, Del Sal G, Agami R.
Gene regulation and tumor suppression by the bromodomain-containing protein BRD7.
Cell Cycle. 2010 Jul 15;9(14):2777-81. Epub 2010 Jul 7. :-> PDF

Agami R.
microRNAs, RNA binding proteins and cancer.
Eur J Clin Invest. 2010 Apr;40(4):370-4.

Elkon R, Zlotorynski E, Zeller KI, Agami R.
Major role for mRNA stability in shaping the kinetics of gene induction.
BMC Genomics. 2010 Apr 21;11:259.
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van Haaften G, Agami R.
Tumorigenicity of the miR-17-92 cluster distilled.
Genes Dev. 2010 Jan 1;24(1):1-4.

Drost J, Mantovani F, Tocco F, Elkon R, Comel A, Holstege H, Kerkhoven R, Jonkers J, Voorhoeve PM, Agami R, Del Sal G.BRD7 is a candidate tumour suppressor gene required for p53 function.
Nat Cell Biol. 2010 Apr;12(4):380-9. Epub 2010 Mar 14.
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van Haaften G, Agami R.
Tumorigenicity of the miR-17-92 cluster distilled.
Genes Dev. 2010 Jan 1;24(1):1-4.

Drost J, Agami R.
Transformation locked in a loop.
Cell. 2009 Nov 13;139(4):654-6.

Nagel R, Clijsters L, Agami R.
The miRNA-192/194 cluster regulates the Period gene family and the circadian clock.
FEBS J. 2009 Aug 13.

Huse JT, Brennan C, Hambardzumyan D, Wee B, Pena J, Rouhanifard SH, Sohn-Lee C, le Sage C, Agami R, Tuschl T, Holland EC.
The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo.
Genes Dev. 2009 Jun 1;23(11):1327-37.

Scheel AH, Beyer U, Agami R, Dobbelstein M.
Immunofluorescence-based screening identifies germ cell associated microRNA 302 as an antagonist to p63 expression.
Cell Cycle. 2009 May 1;8(9):1426-32. Epub 2009 May 27.

Bartolomé RA, Ferreiro S, Miquilena-Colina ME, Martínez-Prats L, Soto-Montenegro ML, García-Bernal D, Vaquero JJ, Agami R, Delgado R, Desco M, Sánchez-Mateos P, Teixidó J.
The chemokine receptor CXCR4 and the metalloproteinase MT1-MMP are mutually required during melanoma metastasis to lungs.
Am J Pathol. 2009 Feb;174(2):602-12. Epub 2009 Jan 15.

Elkon R, Agami R.
Removal of AU bias from microarray mRNA expression data enhances computational identification of active microRNAs.
PLoS Comput Biol. 2008 Oct 3;4(10):e1000189.


Zlotorynski E, Agami R.
A PASport to cellular proliferation.
Cell. 2008 Jul 25;134(2):208-10. Preview.

Kedde M, Agami R.
Interplay between microRNAs and RNA-binding proteins determines developmental processes.
Cell Cycle. 2008 Apr;7(7):899-903. Epub 2008 Jan 24. Review.

Duursma AM, Kedde M, Schrier M, le Sage C, Agami R.
miR-148 targets human DNMT3b protein coding region.
RNA. 2008 May;14(5):872-7. Epub 2008 Mar 26.

Huang Q, Gumireddy K, Schrier M, le Sage C, Nagel R, Nair S, Egan DA, Li A, Huang G, Klein-Szanto AJ, Gimotty PA, Katsaros D, Coukos G, Zhang L, Puré E, Agami R.
The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis.
Nat Cell Biol. 2008 Feb;10(2):202-10. Epub 2008 Jan 13.


Kedde M, Strasser MJ, Boldajipour B, Vrielink JA, Slanchev K, le Sage C, Nagel R, Voorhoeve PM, van Duijse J, Ørom UA, Lund AH, Perrakis A, Raz E, Agami R.
RNA-binding protein Dnd1 inhibits microRNA access to target mRNA.
Cell. 2007 Dec 28;131(7):1273-86.

le sage C, Nagel R, Agami R.
Diverse Ways to Control p27(Kip1) Function: miRNAs Come into Play.
Cell Cycle. 2007 Aug 16;6(22) [Epub ahead of print]

le Sage C, Nagel R, Egan DA, Schrier M, Mesman E, Mangiola A, Anile C, Maira G, Mercatelli N, Ciafrè SA, Farace MG, Agami R.
Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation.
EMBO J. 2007 Aug 8;26(15):3699-708. Epub 2007 Jul 12.

Agami R.
All roads lead to IKKepsilon.
Cell. 2007 Jun 15;129(6):1043-5.

agiv Y, Bai L, Wei DG, Agami R, Savage PB, Teyton L, Bendelac A.
A distal effect of microsomal triglyceride transfer protein deficiency on the lysosomal recycling of CD1d.
J Exp Med. 2007 Apr 16;204(4):921-8. Epub 2007 Apr 2.

Voorhoeve PM and Agami R.
Classifying microRNAs in cancer: The good, the bad and the ugly
BBA - Reviews on Cancer. Jun;1775(2):274-82.


Kedde M, le Sage C, Duursma A, Zlotorynski E, van Leeuwen B, Nijkamp W, Beijersbergen R, and Agami R.
Telomerase-independent Regulation of ATR by Human Telomerase RNA
J. Biol. Chem., Vol. 281, Issue 52, 40503-40514, December 29, 2006

le Sage C. and Agami R.
Immense promeses for tiny molecules: Uncovering miRNA functions.
Cell Cycle. 2006 Jul 1;5(13):1415-1421.

Voorhoeve PM, le Sage C, Schrier M, Gillis AJM, Stoop H, Nagel R, Liu YP, van Duijse Y, Drost J, Griekspoor A, Zlotorynski E, Yabuta N, De Vita G,Nojima H, Looijenga, LHJ and Agami R.
A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors.
Cell. 2006 Mar 24;124(6):1169-81.


Duursma A, Agami R.
CDK-dependent stabilization of Cdc6: linking growth and stress signals to activation of DNA replication.
Cell Cycle. 2005 Dec;4(12):1725-8. Epub 2005 Dec 22.

Schwartz M, Zlotorynski E, Goldberg M, Ozeri E, Rahat A, le Sage C, Chen BP, Chen DJ, Agami R, Kerem B.
Homologous recombination and nonhomologous end-joining repair pathways regulate fragile site stability.
Genes Dev. 2005 Nov 15;19(22):2715-26.

Duursma A, Agami R.
p53-dependent regulation of Cdc6 protein stability controls cellular proliferation.
Mol Cell Biol. 2005 Aug;25(16):6937-47.

Kolfschoten IG, van Leeuwen B, Berns K, Mullenders J, Beijersbergen RL, Bernards R, Voorhoeve PM, Agami R.
A Genetic Screen Identifies PITX1 as a Suppressor of RAS Activity and Tumorigenicity.
Cell. 2005 Jun 17;121(6):849-58.

Einav Y, Agami R, Canaani D.
shRNA-mediated RNA interference as a tool for genetic synthetic lethality screening in mouse embryo fibroblasts.
FEBS Lett. Jan 3;579(1):199-202.


Gagrica, S., Hauser, S., Kolfschoten, I., Osterloh, L., Agami, R., and Gaubatz, S.
Inhibition of oncogenic transformation by mammalian Lin-9, a pRB-associated protein.
EMBO J 23, 4627-4638.

Zhong, X., Shen, Y., Ballar, P., Apostolou, A., Agami, R., and Fang, S. .
AAA ATPase p97/valosin-containing protein interacts with gp78, a ubiquitin ligase for endoplasmic reticulum-associated degradation.
J Biol Chem 279, 45676-45684.

Berns K, Hijmans EM, Mullenders J, Brummelkamp TR, Velds A, Heimerikx M, Kerkhoven RM, Madiredjo M, Nijkamp W, Weigelt B, Agami R, Ge W, Cavet G, Linsley PS, Beijersbergen RL, Bernards R.
A large-scale RNAi screen in human cells identifies new components of the p53 pathway.
Nature 428, 431-437.

Voorhoeve, P. M., and Agami, R.
Unraveling human tumor suppressor pathways: a tale of the INK4A locus.
Cell Cycle 3, 616-620.


Voorhoeve, P. M., and Agami, R.
The tumor suppressive functions of the human INK4A locus.
Cancer Cell, 4, 311-319.

Kolfschoten I., and Agami, R.
Allelic gene inactivation: pinpointing the problem.
Gene Therapy, 10, 1931-1932.

Duursma A. M. and Agami, R.
Ras interference as cancer therapy.
Seminars in Cancer Biology, 13, 267-273.

van de Wetering, M., Oving, I., Muncan, V., Pon Fong, M. T., Brantjes, H., van Leenen, D., Holstege, F. C., Brummelkamp, T. R., Agami, R., and Clevers, H.
Specific inhibition of gene expression using a stably integrated, inducible small-interfering-RNA vector.
EMBO Rep., 4, 609-615.

Lens, S. M., Wolthuis, R. M., Klompmaker, R., Kauw, J., Agami, R., Brummelkamp, T., Kops, G., and Medema, R. H.
Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension.
EMBO J., 22, 2934-2947.

Voorhoeve, P. M., and Agami, R.
Knockdown stands up.
Trends Biotechnol, 21, 2-4.


Agami, R. RNAi and related mechanisms and their potential use for therapy.
Curr Opin Chem Biol. 2002 Dec;6(6):829-34.

Brummelkamp, T. R., Bernards, R. and Agami, R.
Stable suppression of tumorigenicity by virus-mediated RNA interference.
Cancer Cell, 2, 243-247.

Brummelkamp, T. R., Bernards, R. and Agami, R.
A system for stable expression of short interfering RNAs in mammalian cells.
Science, 295.

Agami, R. and Bernards, R.
Convergence of mitogenic and DNA damage signaling in the G1 phase of the cell cycle.
Cancer letters, 177, 111-118.

Agami, R. and Bernards, R.
Distinct initiation and maintenance mechanisms cooperate to induce G1 cell cycle arrest in response to DNA damage.
Cell, 102, 55-66.