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John Strouboulis
Hematopoiesis is the process responsible for the production of the many different blood cell types in our circulation from a small population of self-renewing, pluripotential hematopoietic stem cells (HSCs). HSCs commit and differentiate along specific lineages in response to specific signals and according to the action of lineage-restricted transcription factors which execute lineage decision, commitment and differentiation programs through the concerted regulation of target genes. The functional association of specific transcription factors with the differentiation of particular hematopoietic lineages has been revealed from gene knockout experiments, however, little is known about the molecular basis of their functions in directing hematopoietic development and differentiation. For example, whilst there is mounting evidence that transcription factors have dual roles as activators and repressors, little is known as to how they exert these seemingly opposite functions at the level of chromatin structure.
Our research aims to address the molecular basis of transcription factor function in hematopoiesis by focusing on specific transcription factors involved in the differentiation of the erythroid (red blood) lineage, such as GATA-1 and FOG-1. We are employing an in vivo biotinylation tagging approach as an efficient, high affinity method for the rapid isolation and characterization by mass spectrometry of transcription factor complexes implicated in erythroid differentiation and for the elucidation of gene target networks regulated by these complexes.
Amanatiadou EP, Papadopoulos GL, Strouboulis J,* Vizirianakis IS. (2015) GATA1 and PU.1 Bind to Ribosomal Protein Genes in Erythroid Cells: Implications for Ribosomopathies. PLoS One 10:e0140077. * Co-corresponding author.
Fan J. AX, Papadopoulos GL, Lin I-J, Hossain M, Hu J, Renne R, Strouboulis J,* Bungert J. (2014) Proteomic and Genomic Analysis of transcription factor TFII-I in erythroleukemia cells. Nucleic Acids Res. 42:7625-41. * Co-corresponding author.
Papadopoulos GL, Karkoulia E, Tsamardinos I, Porcher C, Ragoussis J, Bungert J, Strouboulis J. (2013) GATA-1 genome-wide occupancy associates with distinct epigenetic profiles during mouse fetal liver erythropoiesis. Nucleic Acids Res. 41:4938-48.
Rodriguez P, Bonte E, Krijgsveld J, Guyot B, Heck A, Vyas P, de Boer E, Grosveld F, Strouboulis J. (2005) GATA-1 forms distinct activating and repressive complexes in erythroid cells. EMBO J. 24:2354–2366.
de Boer Ε, Rodriguez P, Bonte E, Krijgsveld J, Katsantoni E, Heck A, Grosveld F, Strouboulis J. (2003) Efficient biotinylation and single-step purification of tagged transcription factors in mammalian cells and transgenic mice. Proceedings Nat. Acad. Sci. USA 100:7480-7485.
2018
Ioannou M, Papageorgiou DN, Ogryzko V, Strouboulis J. "Mammalian expression vectors for metabolic biotinylation tandem affinity tagging by co-expression in cis of a mammalian codon-optimized BirA biotin ligase". BMC Res Notes. 2018 Jun 14;11(1):390. doi: 10.1186/s13104-018-3500-9. [PubMed]
Shen Y, Nar R, Fan AX, Aryan M, Hossain MA, Gurumurthy A, Wassel PC, Tang M, Lu J, Strouboulis J, Bungert J. "Functional interrelationship between TFII-I and E2F transcription factors at specific cell cycle gene loci". J Cell Biochem. 2018 Jan;119(1):712-722. doi: 10.1002/jcb.26235. [PubMed]
2017
Chatzinikolaou G, Apostolou Z, Aid-Pavlidis T, Ioannidou A, Karakasilioti I, Papadopoulos GL, Aivaliotis M, Tsekrekou M, Strouboulis J, Kosteas T, Garinis GA. "ERCC1-XPF cooperates with CTCF and cohesin to facilitate the developmental silencing of imprinted genes". Nat Cell Biol. 2017 May;19(5):421-432. [PubMed]
2016
Papageorgiou DN, Karkoulia E, Amaral-Psarris A, Burda P, Kolodziej K, Demmers J, Bungert J, Stopka T, Strouboulis J. "Distinct and overlapping DNMT1 interactions with multiple transcription factors in erythroid cells: Evidence for co-repressor functions." Biochim Biophys Acta. 2016 Dec;1859(12):1515-1526. [PubMed]
Burda P, Vargova J, Curik N, Salek C, Papadopoulos GL, Strouboulis J, Stopka T. "GATA-1 Inhibits PU.1 Gene via DNA and Histone H3K9 Methylation of Its Distal Enhancer in Erythroleukemia". PLoS One. 2016 Mar 24;11(3):e0152234. [PubMed]
2015
Amanatiadou EP, Papadopoulos GL, Strouboulis J,* Vizirianakis IS. "GATA1 and PU.1 Bind to Ribosomal Protein Genes in Erythroid Cells: Implications for Ribosomopathies". PLoS One. 2015 Oct 8;10(10):e0140077. * Co-corresponding author. [PubMed]
Blobel GA, Bodine D, Brand M, Crispino J, de Bruijn MF, Nathan D, Papayannopoulou T, Porcher C, Strouboulis J, Zon L, Higgs DR, Stamatoyannopoulos G, Engel JD. 2015, "An international effort to cure a global health problem: A report on the 19th Hemoglobin Switching Conference." Exp Hematol. 2015 Oct;43(10):821-37. [PubMed]
Papadopoulos P, Gutiérrez L, Demmers J, Scheer E, Pourfarzad F, Papageorgiou DN, Karkoulia E, Strouboulis J, van de Werken HJ, van der Linden R, Vandenberghe P, Dekkers DH, Philipsen S, Grosveld F, Tora L. 2015, "TAF10 interacts with GATA1 transcription factor and controls mouse erythropoiesis." Mol Cell Biol. 2015 Apr 13. pii: MCB.01370-14. [PubMed]
2014
Fan AX, Papadopoulos GL, Hossain MA, Lin IJ, Hu J, Tang TM, Kilberg MS, Renne R, Strouboulis J*, Bungert J. 2014, "Genomic and proteomic analysis of transcription factor TFII-I reveals insight into the response to cellular stress", Nucleic Acids Res., 2014 2014, 42, pp. 7625-41. * Co-corresponding author [PubMed].
Shi L, Sierant MC, Gurdziel K, Zhu F, Cui S, Kolodziej KE, Strouboulis J, Guan Y, Tanabe O, Lim KC, Engel JD 2014, "Biased, Non-equivalent Gene-Proximal and -Distal Binding Motifs of Orphan Nuclear Receptor TR4 in Primary Human Erythroid Cells.", PLoS Genet., 2014 May 8; 10(5):e1004339. [PubMed].
2013
Papadopoulos GL, Karkoulia E, Tsamardinos I, Porcher C, Ragoussis J, Bungert J, Strouboulis J . 2013, "GATA-1 genome-wide occupancy associates with distinct epigenetic profiles in mouse fetal liver erythropoiesis.", Nucleic Acids Res., 2013, 41(9), pp. 4938-48. [PubMed].
Papageorgiou DN, Demmers J, Strouboulis J . 2013, "NP-40 reduces contamination by endogenous biotinylated carboxylases during purification of biotin tagged nuclear proteins.", Protein Expr Purif., 2013, 89, pp. 80-83. [PubMed].
2012
Stees, J.S., Varnf, F., Huang, S., Strouboulis J, and Bungert, J. 2012, "Recruitment of Transcription Complexes to Enhancers and the Role of Enhancer Transcription.", Biology, 1(3), 778-793
Brazão TF, Demmers J, van IJcken W, Strouboulis J, , Fornerod M, Romão L, Grosveld FG. 2012, "A new function of ROD1 in nonsense-mediated mRNA decay.", FEBS Lett., 2012, 586(8), pp. 1101-10. [PubMed].
Reynolds N, Latos P, Hynes-Allen A, Loos R, Leaford D, O'Shaughnessy A, Mosaku O, Signolet J, Brennecke P, Kalkan T, Costello I, Humphreys P, Mansfield W, Nakagawa K, Strouboulis J, , Behrens A, Bertone P, Hendrich B. 2012, "NuRD suppresses pluripotency gene expression to promote transcriptional heterogeneity and lineage commitment.", Cell Stem Cell., 2012 May 4; 10(5):583-94. [PubMed].
2011
Leotoing L, Chereau F, Baron S, Hube F, Valencia HJ, Bordereaux D, Demmers JA, Strouboulis J, , Baud V. 2011, "ABIN-2 is an activator of IKK{alpha}-mediated NF-{kappa}B transcriptional activity.", J Biol Chem., 2011, 286(37), pp. 32277-88. [PubMed].
Cui S, Kolodziej K, Obara N, Amaral-Psarris A, Demmers J, Shi L, Engel JD, Grosveld F, Strouboulis J*, , Tanabe O. 2011, "Nuclear Receptors TR2 and TR4 Recruit Multiple Epigenetic Transcriptional Co-repressors that Associate Specifically with the Embryonic {beta}-type Globin Promoters in Differentiated Adult Erythroid Cells.", Mol Cell Biol., Aug;31(16):3298-311 [PubMed]. *Co-corresponding author
Anantharaman A, Lin IJ, Barrow J, Liang SY, Masannat J, Strouboulis J, , Huang S, Bungert J. 2011, "Role of helix-loop-helix proteins during differentiation of erythroid cells.", Mol Cell Biol., 2011 Apr;31(7):1332-43. [PubMed].
2009
Tsiftsoglou AS, Vizirianakis IS, Strouboulis J ., 2009, "Erythropoiesis: Model systems, molecular regulators, and developmental programs", IUBMB Life.; 61(8):800-830., 2009 Jul 20:61(8), 800-830 [Pubmed]
Kolodziej KE, Pourfarzad F, de Boer E, Krpic S, Grosveld F, Strouboulis J. ., 2009, "Optimal use of tandem biotin and V5 tags in ChIP assays.", BMC Mol Biol.;, 2009 Feb 5, 10:6 [Pubmed]
2008
Hamlett I, Draper J, Strouboulis J, Iborra F, Porcher C, Vyas P. 2008 “Characterisation of megakaryocyte GATA1-interacting proteins: the co-repressor ETO2 and GATA1 interact to regulate terminal megakaryocyte maturation.” Blood. Oct 1;112(7) 2738-49. Pubmed
Liang S, Moghimi B, Yang TP, Strouboulis J, Bungert J 2008 “Locus control region mediated regulation of adult beta-globin gene expression”J Cell Biochem.2008 Sep 1;105(1):9-16.Pubmed
2007
Moerland, M., Anghelescu, N., Samyn, H., van Haperen, R., van Gent, T., Strouboulis, J., van Tol, A., Grosveld, F. and de Crom, R. 2007 “Inducible expression of phospholipid transfer protein (PLTP) in transgenic mice: acute effects of PLTP on lipoprotein metabolism.” Transgenic Res. 2007, 16(4), pp. 503-13. Pubmed
2006
Meier, N., Krpic, S., Rodriguez, P., Strouboulis, J., Monti, M., Krijgsveld, J., Gering, M., Patient, R., Hostert, A. and Grosveld,F. 2006 “Novel binding partners of Ldb1 are required for hematopoietic development”. Development. 2006 Dec;133(24):4913-23. PubMed
Rodriguez, P., Braun, H., Kolodziej, K.E., de Boer, E., Campbell, J., Bonte, E., Grosveld, F., Philipsen, S. and Strouboulis, J. 2006 “Isolation of transcription factor complexes by in vivo biotinylation tagging and direct binding to streptavidin beads”. Methods Mol Biol. 2006;338:305-23. PubMed
Horsman, S., Moorhouse, M., de Jager, V., van der Spek, P., Grosveld, F., Strouboulis, J., and Katsantoni, E. 2006 “TFT Mapper: A BLAST search tool for identification of Transcription Factors Target Genes”. BMC Bioinformatics. 2006 Mar 8;7:120. PubMed
Goardon, N., Lambert, J., Rodriguez, P., Herblot, S., Thibault, P., Dumenil, D., Strouboulis, J., Romeo, P-H and Hoang, T. 2006 “ETO2 coordinates cellular proliferation and differentiation during erythropoiesis”. EMBO J. 2006 Jan 25;25(2):357-66. PubMed
2005
Grosveld, F., Rodriguez, P., Meier, N., Krpic, S., Pourfarzad, F., Papadopoulos, P., Kolodziej, K.E., Patrinos, G., Hostert, A. and Strouboulis, J. 2005 “Isolation and characterization of hematopoietic transcription factor complexes by in vivo biotinylation tagging and mass spectrometry”. Ann N Y Acad Sci. 2005;1054:55-67. PubMed
Schuh, A.H., Tipping. A.J., Clark, A.J., Hamlett, I., Guyot, B., Iborra, F.J., Rodriguez, P., Strouboulis, J., Enver, T., Vyas, P. and Porcher C. 2005 “ETO-2 associates with SCL in erythroid cells and megakaryocytes and provides repressor functions in erythropoiesis”. Mol Cell Biol. 2005 Dec;25(23):10235-50. PubMed
Driegen, S., Ferreira, R., van Zon, A., Strouboulis, J., Jaegle, M., Grosveld, F., Philipsen, S. and Meijer, D. 2005 “A generic tool for biotinylation of tagged proteins in transgenic mice”. Transgenic Res. 2005 Aug;14(4):477-82. PubMed
Rodriguez, P., Bonte, E., Krijgsveld, J., Guyot, B., Heck, A., Vyas, P., de Boer, E., Grosveld, F. and Strouboulis, J. 2005 “GATA-1 forms distinct activating and repressive complexes in erythroid cells”. EMBO J. 2005 Jul 6;24(13):2354-66. PubMed
2004
Patrinos, P., de Krom, M., de Boer, E., Langeveld, A., Imam, A., Strouboulis, J., de Laat, W. and Grosveld, F. 2004 “Multiple interactions between regulatory regions are required to stabilize an Active Chromatin Hub”. Genes Dev. 2004 Jun 15;18(12):1495-509. PubMed
Katsantoni, E., de Krom, M., Imam, A. Kong-a-San, J., Grosveld, F., Anagnou, N.P. and Strouboulis, J. 2004 “An embryonic-specific repressor element located 3’ to the Ag-globin gene influences expression of the human b-globin locus in the embryonic stage”. Exp Hematol. 2004 Feb;32(2):224-33. PubMed
2003
Katsantoni, E., Langeveld, A., Wai, A., Drabek, D.,Grosveld, F., Anagnou, N.P.and Strouboulis, J. 2003 “Persistent γ-globin expression in adult transgenic mice is mediated by HPFH-2, HPFH-3, and HPFH-6 breakpoint sequences”. Blood. 2003 Nov 1;102(9):3412-9. PubMed
de Boer, Ε., Rodriguez, P., Bonte, E., Krijgsveld, J., Katsantoni, E., Heck, A., Grosveld, F. and Strouboulis, J. 2003 “Efficient biotinylation and single-step purification of tagged transcription factors in mammalian cells and transgenic mice”. Proc Natl Acad Sci U S A. 2003 Jun 24; 100(13):7480-5. PubMed
2002
de Krom, M., van de Corput, M., Grosveld,F. andStrouboulis, J. 2002 “Stochastic patterns in globin gene expression are established prior to transcriptional activation and are clonally inherited”. Mol Cell. 2002 Jun; 9(6):1319-26. PubMed
1999
Strouboulis, J., Damjanowski, S., Vermaak, D., Meric, F. and Wolffe, A.P. 1999 “Transcriptional repression by XPc1, a new Polycomb homolog in Xenopus laevis embryos, is independent of histone deacetylase” Mol Cell Biol. 1999 Jun;19(6):3958-68. PubMed
1998
Jones, P., Veenstra, G., Wade, P., Vermaak, D., Kass, S., Landsberger, N., Strouboulis, J. and Wolffe, A.P. 1998 “Xenopus MeCP2 exists in a complex with Sin3 and histone deacetylase linking transcriptional repression on methylated DNA to chromatin modification”.Nat Genet. 1998 Jun;19(2):187-91. PubMed
1997
Dillon, N., Trimborn, T., Strouboulis, J., Fraser, P. and Grosveld, F. 1997 “The effect of distance on long range chromatin interactions”. Mol Cell. 1997 Dec;1(1):131-9. PubMed
Grosveld, F., Dillon, N., Fraser, P., Strouboulis, J. and Wijgerde, M. 1997 “The regulation of human β-globin gene expression: the dynamics of transcriptional competition in the human β-globin locus”. NATO Advanced Study Institute on Regulation of Cell Growth, Differentiation and Genetics in Cancer, 1997.
1996
Milot, E., Strouboulis, J., Trimborn, T., Wijgerde, M., de Boer, E., Langeveld, A., Tan-Un, K.,Vergeer, W., Yannoutsos, N., Grosveld, F. and Fraser, P. 1996 “Heterochromatin effects on The frequency and duration of LCR-mediated gene transcription”. Cell. 1996 Oct 4;87(1):105-14. PubMed
Strouboulis, J.and Wolffe, A.P. 1996 “Functional compartmentalization of the nucleus”. J Cell Sci. 1996 Aug;109 ( Pt 8):1991-2000. PubMed
1995
Dillon, N., Strouboulis, J. and Grosveld, F. 1995 “The regulation of human β-globin gene expression: polarity of transcriptional competition in the.human β-globin locus”. Proceedings of the Ninth Conference on Hemoglobin Switching. Ed. G. Stamatoyannopoulos, Intercept Ltd., 1995, pp.23-28.
Ellis, J., Philipsen, S., Strouboulis, J., Pruzina, S., Tewari, R., Gillemans, N., Drabek, D., Harper, A., Grosveld, F. and Fraser, P. 1995 “The regulation of human β-globin gene expression: the roles of 5'HS1-4”. Proceedings of the Ninth Conference on Hemoglobin Switching. Ed. G. Stamatoyannopoulos, Intercept Ltd., 1995, pp.29-38
Grosveld, F., Fraser, P., Philipsen, S., Ellis, J., Wijgerde., M., Antoniou, M., Pruzina, S., Meijer, D., Zafarana, G., Strouboulis, J. and Dillon, N. 1995 “Transcriptional regulation of the β-globin gene cluster”. In: Sickle Cell Disease and Thalassaemias: new trends in therapy. Eds. Y. Beuzard, B. Lubin, J. Rosa. Colloque INSERM/John Libbey Eurotext Ltd., 1995, 234, pp. 19-25.
1994
Müller, A.M., Medvinsky, A., Strouboulis, J., Grosveld, F. and Dzierzak, E. 1994 “Development of hematopoietic stem cell activity in the mouse embryo”. Immunity. 1994 Jul;1(4):291-301. PubMed
1993
Grosveld, F., Antoniou, M., Berry, M., de Boer, E., Dillon, N., Ellis, J., Fraser, P., Hanscombe, O., Hurst, J., Imam, A., Lindenbaum, M., Philipsen, S., Pruzina, S., Strouboulis, J., Raguz-Bolognesi, S. and Talbot, D. 1993 “The Regulation of Human Globin Gene Switching”. Phil. Trans. R. Soc. Lond. B., 1993, 339, pp. 183-191.
Dillon, N., Antoniou, M., Berry, M., de Boer, E., Drabek, D., Ellis, J., Fraser, P., Hanscombe, O., Imam, A., Koken, M-A., Lindenbaum, M., Meijer, D., Philipsen, S., Pruzina, S., Raguz-Bolognesi, S., Strouboulis, J., Talbot, D., Whyatt, D. and Grosveld, F. 1993 “Regulation of the human β-globin expression domain”. In: The Chromosome. Eds. J.S. Heslop-Harrison and R.B. Flavell, Bios Scientific Publishers, 1993, pp. 149-159.
Grosveld, F., Antoniou, M., Berry, M., de Boer, E., Dillon, N., Ellis, J., Fraser, P., Hurst, J., Imam, A., Meijer, D., Philipsen, S., Pruzina, S., Strouboulis, J. and Whyatt, D. 1993 “Regulation of human globin gene switching”. Cold Spring Harbor Symposia on Quantitative Symposia, 1993, Vol. LVIII.
1992
Strouboulis, J., Dillon, N. and Grosveld, F. 1992 “Efficient joining of large DNA fragments for transgenesis”. Nucleic Acids Res. 1992 Nov 25;20(22):6109-10. PubMed
Strouboulis, J., Dillon, N. and Grosveld, F. 1992 “Developmental regulation of the complete 70kb human beta-globin locus in transgenic mice” Genes Dev. 1992 Oct;6(10):1857-64. PubMed
1991
Greaves, D.R., Talbot, D., Philipsen, S., Pruzina, S., de Boer, E., Hanscombe, O., Fraser, P., Antoniou, M., Lindenbaum, M., Dillon, N., Belhumeur, P., Strouboulis, J. and Grosveld, F. 1991 “Studies of the β-globin gene: creation of models for somatic gene therapy”. In: Application of Molecular Genetics to the Diagnosis of Inherited Disease. Royal College of Physicians of London, Ed. K.E. Davies, pp. 77-84.
Dillon, N., Fraser, P., Hanscombe, O., Greaves, D.R., Lindenbaum, M., Whyatt, D., Strouboulis, J., Hurst, J. and Grosveld, F. 1991 “Regulation of the human γ-globin to β-globin switch in transgenic mice”. In: The regulation of Hemoglobin Switching. Proceedings of 7th Hemoglobin Conference. Eds, G. Stamatoyannopoulos and A.W. Nienhuis. Johns Hopkins University Press, Maryland, 1991, pp. 34-44.
Grosveld, F., Antoniou, M., Berry, M., de Boer, E., Dillon, N., Ellis, J., Fraser, P., Greaves, D., Hanscombe, O., Hurst, J., Lindenbaum, M., Mignotte, V., Philipsen, S., Pruzina, S., Strouboulis, J., Talbot, D. and Whyatt, D. 1991 “The human β-globin Locus Control Region” Stohlman Lecture In: Modern Trends in Human Leukemia, 1991, Ed. R. Neth.
Grosveld, F., Antoniou, M., Berry, M., de Boer, E., Dillon, N., Ellis, J., Fraser, P., Greaves, D., Hanscombe, O., Hurst, J., Lindenbaum, M., Mignotte, V., Philipsen, S., Pruzina, S., Strouboulis, J., Talbot, D. and Whyatt, D. 1991 “The regulation of the human β-globin locus. In: Applications of Basic Science to Hematopoiesis and Treatment of Disease”. Ed. Donall Thomas, Raven Press, Ltd., New York, 1991, pp. 21-38.
1990
Samuel, K.P., Ascione, R., Kottarides, S.D., Seth, A.K., Lautenberger, J.A., Zuber, M., Strouboulis, J. and Papas, T.S. 1990 “Expression of animal and human retroviral gene products in Escherichia coli with the lambda pJL6 vector system”. Genet Anal Tech Appl. 1990 Nov;7(7):178-208. PubMed
Grosveld, F., Greaves, D., Philipsen, S., Pruzina, S., de Boer, E., Hanscombe, O., Belhumeur, P., Hurst, J., Fraser, P., Whyatt, D., Antoniou, M., Mignotte, V., Dillon, N., Lindenbaum, M. and Strouboulis, J. 1990 “Τhe Dominant Control Region of the human β-globin domain”. The New York Academy of Sciences, Sixth Cooley's Anemia Symposium Ed. Arthur Bank, 1990, 612, pp. 152-159.