Publications

Recent selected publications

1. In vitro capture and characterization of embryonic rosette-stage pluripotency between naive and primed states. Neagu A, van Genderen E, Escudero I, Verwegen L, Kurek D, Lehmann J, Stel J, Dirks RAM, van Mierlo G, Maas A, Eleveld C, Ge Y, den Dekker AT, Brouwer RWW, van IJcken WFJ, Modic M, Drukker M, Jansen JH, Rivron NC, Baart EB, Marks H, Ten Berge D.
Nat Cell Biol. 2020; 22(5):534-545. PMID: 32367046

2. Integrative Proteomic Profiling Reveals PRC2-Dependent Epigenetic Crosstalk Maintains Ground-State Pluripotency. van Mierlo G, Dirks RAM, De Clerck L, Brinkman AB, Huth M, Kloet SL, Saksouk N, Kroeze LI, Willems S, Farlik M, Bock C, Jansen JH, Deforce D, Vermeulen M, Déjardin J, Dhaenens M, Marks H.
Cell Stem Cell. 2019; 24(1):123-137.e8. PMID: 30472157

3. The Complexity of PRC2 Subcomplexes. van Mierlo G, Veenstra GJC, Vermeulen M, Marks H.
Trends Cell Biol. 2019; 29(8):660-671. PMID: 31178244

4. Miniaturised interaction proteomics on a microfluidic platform with ultra-low input requirements. Furlan C, Dirks RAM, Thomas PC, Jones RC, Wang J, Lynch M, Marks H^, Vermeulen M. (^corresponding/ shared last author)
Nat Commun. 2019; 10(1):1525. PMID: 30948724

5. Epigenetic modulation of a hardwired 3D chromatin landscape in two naive states of pluripotency. Atlasi Y, Megchelenbrink W, Peng T, Habibi E, Joshi O, Wang SY, Wang C, Logie C, Poser I, Marks H, Stunnenberg HG.
Nat Cell Biol. 2019 May;21(5):568-578. PMID: 31036938

6. MTF2 recruits Polycomb Repressive Complex 2 by helical-shape-selective DNA binding. Perino M, van Mierlo G, Karemaker ID, van Genesen S, Vermeulen M, Marks H, van Heeringen SJ, Veenstra GJC.
Nat Genet. 2018; 50(7):1002-1010. PMID: 29808031

7. Dynamics of gene silencing during X inactivation using allele-specific RNA-seq. Marks H*, Kerstens HH, Barakat TS, Splinter E, Dirks RA, van Mierlo G, Joshi O, Wang SY, Babak T, Albers CA, Kalkan T, Smith A, Jouneau A, de Laat W, Gribnau J, Stunnenberg HG. (*corresponding author)
Genome Biol. 2015; 16(1):149.  PMID: 26235224

8. Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells. Habibi E, Brinkman AB, Arand J, Kroeze LI, Kerstens HH, Matarese F, Lepikhov K, Gut M, Brun-Heath I, Hubner NC, Benedetti R, Altucci L, Jansen JH, Walter J, Gut IG, Marks H*, Stunnenberg HG. (*corresponding author)
Cell Stem Cell. 2013 Sep 5;13(3):360-9. PMID: 23850244

9. The transcriptional and epigenomic foundations of ground state pluripotency. Marks H, Kalkan T, Menafra R, Denissov S, Jones K, Hofemeister H, Nichols J, Kranz A, Stewart AF, Smith A, Stunnenberg HG.
Cell. 2012; 149(3):590-604. PMID: 22541430

10. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, Butter F, Lee KK, Olsen JV, Hyman AA, Stunnenberg HG, Mann M.
Cell. 2010; 142(6):967-80. PMID: 20850016

 

All publications

  1. Peng, T, Zhai, Y, Atlasi, Y, Ter Huurne, M, Marks, H, Stunnenberg, HG et al.. STARR-seq identifies active, chromatin-masked, and dormant enhancers in pluripotent mouse embryonic stem cells. Genome Biol. 2020;21 (1):243. doi: 10.1186/s13059-020-02156-3. PubMed PMID:32912294 PubMed Central PMC7488044.
  2. Raas, MWD, Zijlmans, DW, Marks, H. Overcoming epigenetic roadblocks. Nat Chem Biol. 2020; :. doi: 10.1038/s41589-020-0629-3. PubMed PMID:32807970 .
  3. Perino, M, van Mierlo, G, Loh, C, Wardle, SMT, Zijlmans, DW, Marks, H et al.. Two Functional Axes of Feedback-Enforced PRC2 Recruitment in Mouse Embryonic Stem Cells. Stem Cell Reports. 2020; :. doi: 10.1016/j.stemcr.2020.07.007. PubMed PMID:32763159 .
  4. Smits, JPH, Dirks, RAM, Qu, J, Oortveld, MAW, Brinkman, AB, Zeeuwen, PLJM et al.. Terminal keratinocyte differentiation in vitro is associated with a stable DNA methylome. Exp Dermatol. 2020; :. doi: 10.1111/exd.14153. PubMed PMID:32681572 .
  5. Neagu, A, van Genderen, E, Escudero, I, Verwegen, L, Kurek, D, Lehmann, J et al.. In vitro capture and characterization of embryonic rosette-stage pluripotency between naive and primed states. Nat Cell Biol. 2020;22 (5):534-545. doi: 10.1038/s41556-020-0508-x. PubMed PMID:32367046 .
  6. Bell, E, Curry, EW, Megchelenbrink, W, Jouneau, L, Brochard, V, Tomaz, RA et al.. Dynamic CpG methylation delineates subregions within super-enhancers selectively decommissioned at the exit from naive pluripotency. Nat Commun. 2020;11 (1):1112. doi: 10.1038/s41467-020-14916-7. PubMed PMID:32111830 PubMed Central PMC7048827.
  7. Ter Huurne, M, Peng, T, Yi, G, van Mierlo, G, Marks, H, Stunnenberg, HG et al.. Critical Role for P53 in Regulating the Cell Cycle of Ground State Embryonic Stem Cells. Stem Cell Reports. 2020;14 (2):175-183. doi: 10.1016/j.stemcr.2020.01.001. PubMed PMID:32004494 PubMed Central PMC7013234.
  8. De Clerck, L, Taelman, J, Popovic, M, Willems, S, Van der Jeught, M, Heindryckx, B et al.. Untargeted histone profiling during naive conversion uncovers conserved modification markers between mouse and human. Sci Rep. 2019;9 (1):17240. doi: 10.1038/s41598-019-53681-6. PubMed PMID:31754138 PubMed Central PMC6872658.
  9. van Mierlo, G, Wester, RA, Marks, H. A Mass Spectrometry Survey of Chromatin-Associated Proteins in Pluripotency and Early Lineage Commitment. Proteomics. 2019;19 (14):e1900047. doi: 10.1002/pmic.201900047. PubMed PMID:31219242 .
  10. van Mierlo, G, Veenstra, GJC, Vermeulen, M, Marks, H. The Complexity of PRC2 Subcomplexes. Trends Cell Biol. 2019;29 (8):660-671. doi: 10.1016/j.tcb.2019.05.004. PubMed PMID:31178244 .
  11. Atlasi, Y, Megchelenbrink, W, Peng, T, Habibi, E, Joshi, O, Wang, SY et al.. Publisher Correction: Epigenetic modulation of a hardwired 3D chromatin landscape in two naive states of pluripotency. Nat Cell Biol. 2019;21 (7):911-912. doi: 10.1038/s41556-019-0341-2. PubMed PMID:31097792 .
  12. Atlasi, Y, Megchelenbrink, W, Peng, T, Habibi, E, Joshi, O, Wang, SY et al.. Epigenetic modulation of a hardwired 3D chromatin landscape in two naive states of pluripotency. Nat Cell Biol. 2019;21 (5):568-578. doi: 10.1038/s41556-019-0310-9. PubMed PMID:31036938 .
  13. Furlan, C, Dirks, RAM, Thomas, PC, Jones, RC, Wang, J, Lynch, M et al.. Miniaturised interaction proteomics on a microfluidic platform with ultra-low input requirements. Nat Commun. 2019;10 (1):1525. doi: 10.1038/s41467-019-09533-y. PubMed PMID:30948724 PubMed Central PMC6449397.
  14. Dirks, RAM, van Mierlo, G, Kerstens, HHD, Bernardo, AS, Kobolák, J, Bock, I et al.. Allele-specific RNA-seq expression profiling of imprinted genes in mouse isogenic pluripotent states. Epigenetics Chromatin. 2019;12 (1):14. doi: 10.1186/s13072-019-0259-8. PubMed PMID:30767785 PubMed Central PMC6376749.
  15. van Mierlo, G, Dirks, RAM, De Clerck, L, Brinkman, AB, Huth, M, Kloet, SL et al.. Integrative Proteomic Profiling Reveals PRC2-Dependent Epigenetic Crosstalk Maintains Ground-State Pluripotency. Cell Stem Cell. 2019;24 (1):123-137.e8. doi: 10.1016/j.stem.2018.10.017. PubMed PMID:30472157 .
  16. van Mierlo, G, Wester, RA, Marks, H. Quantitative subcellular proteomics using SILAC reveals enhanced metabolic buffering in the pluripotent ground state. Stem Cell Res. 2018;33 :135-145. doi: 10.1016/j.scr.2018.09.017. PubMed PMID:30352361 .
  17. Bernardo, AS, Jouneau, A, Marks, H, Kensche, P, Kobolak, J, Freude, K et al.. Mammalian embryo comparison identifies novel pluripotency genes associated with the naïve or primed state. Biol Open. 2018;7 (8):. doi: 10.1242/bio.033282. PubMed PMID:30026265 PubMed Central PMC6124576.
  18. Perino, M, van Mierlo, G, Karemaker, ID, van Genesen, S, Vermeulen, M, Marks, H et al.. MTF2 recruits Polycomb Repressive Complex 2 by helical-shape-selective DNA binding. Nat Genet. 2018;50 (7):1002-1010. doi: 10.1038/s41588-018-0134-8. PubMed PMID:29808031 .
  19. Fisher, CL, Marks, H, Cho, LT, Andrews, R, Wormald, S, Carroll, T et al.. An efficient method for generation of bi-allelic null mutant mouse embryonic stem cells and its application for investigating epigenetic modifiers. Nucleic Acids Res. 2017;45 (21):e174. doi: 10.1093/nar/gkx811. PubMed PMID:28981838 PubMed Central PMC5716182.
  20. Kalkan, T, Olova, N, Roode, M, Mulas, C, Lee, HJ, Nett, I et al.. Tracking the embryonic stem cell transition from ground state pluripotency. Development. 2017;144 (7):1221-1234. doi: 10.1242/dev.142711. PubMed PMID:28174249 PubMed Central PMC5399622.
  21. Dirks, RA, Stunnenberg, HG, Marks, H. Genome-wide epigenomic profiling for biomarker discovery. Clin Epigenetics. 2016;8 :122. doi: 10.1186/s13148-016-0284-4. PubMed PMID:27895806 PubMed Central PMC5117701.
  22. Marks, H, Kerstens, HH, Barakat, TS, Splinter, E, Dirks, RA, van Mierlo, G et al.. Erratum to: Dynamics of gene silencing during X inactivation using allele-specific RNA-seq. Genome Biol. 2016;17 :22. doi: 10.1186/s13059-016-0885-4. PubMed PMID:26850229 PubMed Central PMC4743200.
  23. Marks, H, Kerstens, HH, Barakat, TS, Splinter, E, Dirks, RA, van Mierlo, G et al.. Dynamics of gene silencing during X inactivation using allele-specific RNA-seq. Genome Biol. 2015;16 :149. doi: 10.1186/s13059-015-0698-x. PubMed PMID:26235224 PubMed Central PMC4546214.
  24. Yang, SH, Kalkan, T, Morissroe, C, Marks, H, Stunnenberg, H, Smith, A et al.. Otx2 and Oct4 drive early enhancer activation during embryonic stem cell transition from naive pluripotency. Cell Rep. 2014;7 (6):1968-81. doi: 10.1016/j.celrep.2014.05.037. PubMed PMID:24931607 PubMed Central PMC4074343.
  25. Veillard, AC, Marks, H, Bernardo, AS, Jouneau, L, Laloë, D, Boulanger, L et al.. Stable methylation at promoters distinguishes epiblast stem cells from embryonic stem cells and the in vivo epiblasts. Stem Cells Dev. 2014;23 (17):2014-29. doi: 10.1089/scd.2013.0639. PubMed PMID:24738887 PubMed Central PMC4142781.
  26. Denissov, S, Hofemeister, H, Marks, H, Kranz, A, Ciotta, G, Singh, S et al.. Mll2 is required for H3K4 trimethylation on bivalent promoters in embryonic stem cells, whereas Mll1 is redundant. Development. 2014;141 (3):526-37. doi: 10.1242/dev.102681. PubMed PMID:24423662 .
  27. Marks, H, Stunnenberg, HG. Transcription regulation and chromatin structure in the pluripotent ground state. Biochim Biophys Acta. 2014;1839 (3):129-37. doi: 10.1016/j.bbagrm.2013.09.005. PubMed PMID:24096207 .
  28. Habibi, E, Brinkman, AB, Arand, J, Kroeze, LI, Kerstens, HH, Matarese, F et al.. Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells. Cell Stem Cell. 2013;13 (3):360-9. doi: 10.1016/j.stem.2013.06.002. PubMed PMID:23850244 .
  29. Nielsen, FG, Kooyman, M, Kensche, P, Marks, H, Stunnenberg, H, Huynen, M et al.. The PinkThing for analysing ChIP profiling data in their genomic context. BMC Res Notes. 2013;6 :133. doi: 10.1186/1756-0500-6-133. PubMed PMID:23557140 PubMed Central PMC3674928.
  30. Marks, H, Kalkan, T, Menafra, R, Denissov, S, Jones, K, Hofemeister, H et al.. The transcriptional and epigenomic foundations of ground state pluripotency. Cell. 2012;149 (3):590-604. doi: 10.1016/j.cell.2012.03.026. PubMed PMID:22541430 PubMed Central PMC3398752.
  31. Brinkman, AB, Gu, H, Bartels, SJ, Zhang, Y, Matarese, F, Simmer, F et al.. Sequential ChIP-bisulfite sequencing enables direct genome-scale investigation of chromatin and DNA methylation cross-talk. Genome Res. 2012;22 (6):1128-38. doi: 10.1101/gr.133728.111. PubMed PMID:22466170 PubMed Central PMC3371717.
  32. Huang, R, Jaritz, M, Guenzl, P, Vlatkovic, I, Sommer, A, Tamir, IM et al.. An RNA-Seq strategy to detect the complete coding and non-coding transcriptome including full-length imprinted macro ncRNAs. PLoS One. 2011;6 (11):e27288. doi: 10.1371/journal.pone.0027288. PubMed PMID:22102886 PubMed Central PMC3213133.
  33. Seitan, VC, Hao, B, Tachibana-Konwalski, K, Lavagnolli, T, Mira-Bontenbal, H, Brown, KE et al.. A role for cohesin in T-cell-receptor rearrangement and thymocyte differentiation. Nature. 2011;476 (7361):467-71. doi: 10.1038/nature10312. PubMed PMID:21832993 PubMed Central PMC3179485.
  34. Petkov, SG, Marks, H, Klein, T, Garcia, RS, Gao, Y, Stunnenberg, H et al.. In vitro culture and characterization of putative porcine embryonic germ cells derived from domestic breeds and Yucatan mini pig embryos at Days 20-24 of gestation. Stem Cell Res. 2011;6 (3):226-37. doi: 10.1016/j.scr.2011.01.003. PubMed PMID:21419743 .
  35. Kramer, JM, Kochinke, K, Oortveld, MA, Marks, H, Kramer, D, de Jong, EK et al.. Epigenetic regulation of learning and memory by Drosophila EHMT/G9a. PLoS Biol. 2011;9 (1):e1000569. doi: 10.1371/journal.pbio.1000569. PubMed PMID:21245904 PubMed Central PMC3014924.
  36. Vermeulen, M, Eberl, HC, Matarese, F, Marks, H, Denissov, S, Butter, F et al.. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell. 2010;142 (6):967-80. doi: 10.1016/j.cell.2010.08.020. PubMed PMID:20850016 .
  37. Marks, H, Veenstra, GJ, Stunnenberg, HG. Insightful tales from single embryonic cells. Cell Stem Cell. 2010;6 (5):397-8. doi: 10.1016/j.stem.2010.04.008. PubMed PMID:20452308 .
  38. Dieu, BT, Marks, H, Zwart, MP, Vlak, JM. Evaluation of white spot syndrome virus variable DNA loci as molecular markers of virus spread at intermediate spatiotemporal scales. J Gen Virol. 2010;91 (Pt 5):1164-72. doi: 10.1099/vir.0.018028-0. PubMed PMID:20089797 .
  39. Marks, H, Chow, JC, Denissov, S, Françoijs, KJ, Brockdorff, N, Heard, E et al.. High-resolution analysis of epigenetic changes associated with X inactivation. Genome Res. 2009;19 (8):1361-73. doi: 10.1101/gr.092643.109. PubMed PMID:19581487 PubMed Central PMC2720191.
  40. van der Deen, M, Marks, H, Willemse, BW, Postma, DS, Müller, M, Smit, EF et al.. Diminished expression of multidrug resistance-associated protein 1 (MRP1) in bronchial epithelium of COPD patients. Virchows Arch. 2006;449 (6):682-8. doi: 10.1007/s00428-006-0240-3. PubMed PMID:17072643 .
  41. Marks, H, Ren, XY, Sandbrink, H, van Hulten, MC, Vlak, JM. In silico identification of putative promoter motifs of White Spot Syndrome Virus. BMC Bioinformatics. 2006;7 :309. doi: 10.1186/1471-2105-7-309. PubMed PMID:16784526 PubMed Central PMC1550435.
  42. Marks, H, Vorst, O, van Houwelingen, AMML, van Hulten, MCW, Vlak, JM. Gene-expression profiling of White spot syndrome virus in vivo. J Gen Virol. 2005;86 (Pt 7):2081-2100. doi: 10.1099/vir.0.80895-0. PubMed PMID:15958687 .
  43. Marks, H, van Duijse, JJ, Zuidema, D, van Hulten, MC, Vlak, JM. Fitness and virulence of an ancestral White Spot Syndrome Virus isolate from shrimp. Virus Res. 2005;110 (1-2):9-20. doi: 10.1016/j.virusres.2005.01.002. PubMed PMID:15845251 .
  44. Dieu, BTM, Marks, H, Siebenga, JJ, Goldbach, RW, Zuidema, D, Duong, TP et al.. Molecular epidemiology of white spot syndrome virus within Vietnam. J Gen Virol. 2004;85 (Pt 12):3607-3618. doi: 10.1099/vir.0.80344-0. PubMed PMID:15557233 .
  45. Marks, H, Goldbach, RW, Vlak, JM, van Hulten, MC. Genetic variation among isolates of White spot syndrome virus. Arch Virol. 2004;149 (4):673-97. doi: 10.1007/s00705-003-0248-9. PubMed PMID:15045557 .
  46. Nalçacioğlu, R, Marks, H, Vlak, JM, Demirbaĝ, Z, van Oers, MM. Promoter analysis of the Chilo iridescent virus DNA polymerase and major capsid protein genes. Virology. 2003;317 (2):321-9. doi: 10.1016/j.virol.2003.08.007. PubMed PMID:14698670 .
  47. Gopinath, K, Bertens, P, Pouwels, J, Marks, H, Van Lent, J, Wellink, J et al.. Intracellular distribution of cowpea mosaic virus movement protein as visualised by green fluorescent protein fusions. Arch Virol. 2003;148 (11):2099-114. doi: 10.1007/s00705-003-0180-z. PubMed PMID:14579172 .
  48. Marks, H, Mennens, M, Vlak, JM, van Hulten, MCW. Transcriptional analysis of the white spot syndrome virus major virion protein genes. J Gen Virol. 2003;84 (Pt 6):1517-1523. doi: 10.1099/vir.0.19018-0. PubMed PMID:12771421 .
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