HCEMM-BRC Metabolic Systems Biology Research Group

Group Leader

Balázs Papp

Group Leader

PERSONAL INFORMATION

Name: Balázs Papp, Ph.D.
Address: Institute of Biochemistry, Biological Research Center of the Hungarian Academy of Sciences, 
Web: http://brc.hu/sysbiol/
Date of birth: 4th November, 1977, Debrecen (Hungary)
ORCID: 0000-0003-3093-8852

CURRENT POSITIONS

2008 – Principal investigator, Institute of Biochemistry, Biological Research Centre, Szeged.
2019 – Senior group leader, Hungarian Centre of Excellence for Molecular Medicine

EDUCATION

2004 PhD, Faculty of Science, Eötvös Loránd University, Budapest, Hungary
2001 MSc in Biology, Faculty of Science, University of Debrecen, Debrecen, Hungary

AWARDS, SCHOLARSHIPS

2016 Academia Europaea member
2013 Szent-Györgyi Talentum Award
2013 Wellcome Trust International Senior Research Fellow
2009 Lendület Programme Grant of the Hungarian Academy of Sciences
2008 János Bolyai Researh Scholarship
2007 Junior Prima Prize (Hungary)
2005 Systems Biology Young Investigator Award, Gosau, Austria
2004 I. prize, Postgraduate Publication Award (Hungary)
2001 Pro Scientia Medal (Hungary)
2001 I. prize, National Conference for Student Scientists (Hungary)
2000 Scholarship of the Republic of Hungary

GRANTS

2019 “Frontline” – Research Excellence Programme (KKP_19) grant, National Research, Development and Innovation Office (NKFIH), Hungary

2017 Funding for research groups with internationally outstanding high impact results (KH_17) National Research, Development and Innovation Office (NKFIH), Hungary
2017 GINOP-2.3.2-26 (Hungary), PI
2016 GINOP-2.3.2-15 (Hungary)
2013 Wellcome Trust International Senior Research Fellowship
2010 EU FP7 Initial Training Network (METAFLUX), participant
2009 Lendület („Momentum”) grant of the Hungarian Academy of Sciences
2008 Human Frontiers Science Programme Organization Career Development Award

SCIENTOMETRIC INDICATORS

Number of publications: 72

D1 and Q1: 60
Number of first and last authored publications (including co-corresponding): 35
Q1 and D1: 25
Total number of citations: 8102 (Google Scholar)/ MTMT: all 5417, independent 4989
Hirsch-index: 36 (Google Scholar)/ MTMT: 31

Publications

2019:

  1. Apjok, G., Boross, G., Nyerges, Á., Fekete, G., Lázár, V., Papp, B., Pál, C., Csörgő, B.
    Limited evolutionary conservation of the phenotypic effects of antibiotic resistance mutations.
    Biol. Evol. https://doi.org/10.1093/molbev/msz109
  2. Guzmán, GI.,Sandberg, TE., LaCroix, RA., Nyerges, Á., Papp, H., de Raad, M., King, ZA., Hefner, Y.,Northen, TR., Notebaart, RA., Pál, C., Palsson, BO., Papp, B., Feist, AM.
    Enzyme promiscuity shapes adaptation to novel growth substrates.
    Syst. Biol. (2019)15:e8462 https://doi.org/10.15252/msb.20188462
  3. Manczinger, M., Boross, G., Kemény, L., Müller, V., Lenz, TL., Papp, B.*, Pál, C.*
    Pathogen diversity drives the evolution of generalist MHC-II alleles in human populations.
    PLoS Biol. 17(1): e3000131 https://doi.org/10.1371/journal.pbio.3000131
  4. Kintses, B.*,Méhi, O., Ari, E., Számel, M., Györkei, Á., Jangir, PK., Nagy, I., Pál, F., Fekete, G., Tengölics, R.,Nyerges, Á., Likó, I., Bálint, A., Molnár, T., Bálint, B., Vásárhelyi, BM., Bustamante, M., Papp, B.*, Pál, C.*
    Phylogenetic barriers to horizontal transfer of antimicrobial peptide resistance genes in the human gut microbiota.
    Nat Microbiol 4, pages 447–458 (2019) https://doi.org/10.1038/s41564-018-0313-5

2018:

  1. Nyerges, Á.,Csörgő, B., Draskovits, G., Kintses, B., Szili, P., Ferenc, G., Révész, T., Ari, E., Nagy, I., Bálint, B.,Vásárhelyi, BM., Bihari, P., Számel, M., Balogh, D., Papp, H., Kalapis, D., Papp, B., Pál, C.
    Directed evolution of multiple genomic loci allows the prediction of antibiotic resistance.
    PNAS 115 (25) E5726-E5735 doi: 10.1073/pnas.1801646115
  2. Lázár, V., Martins, A., Spohn, R., Daruka, L., Grézal, G., Fekete, G., Számel, M., Jangir, P.K., Kintses, B., Csörgő, B., Nyerges, Á, Györkei, Á., Kincses, A., Dér, A., Walter ,F.R., Deli , M.A., Urbán, E., Hegedűs, Z., Olajos G., Méhi, O., Bálint, B., Nagy, I., Martinek, T. A., Papp B.*, Pál C*.
    Antibiotic-resistant bacteria show widespread collateral sensitivity to antimicrobial peptides
    Microbiol https://doi.org/10.1038/s41564-018-0164-0
  3. Zampieri, M.*, Szappanos, B.*, Maria Virginia Buchieri, Trauner, A., Piazza, I., Picotti, P., Gagneux, S., Borrell, S., Gicquel, B., Lelievre, J., Balazs Papp, Uwe Sauer
    High-throughput metabolomic analysis predicts mode of action of uncharacterized antimicrobial compounds
    Science Translational Medicine 21 Feb 2018: Vol. 10, Issue 429, eaal3973 DOI: 10.1126/scitranslmed.aal3973
  4. Natan, E., Endoh, T., Haim-Vilmovsky, L., Flock, T., Chalancon, G., Hopper, J.T.S, Kintses, B., Horvath, P., Daruka, L., Fekete, G., Pál, C., Papp, B., Oszi, E., Magyar, Z., Marsh, J.A., Elcock, A.H., Babu, M.M., Robinson, C.V., Sugimoto ,N., Teichmann, S. A
    Cotranslational protein assembly imposes evolutionary constraints on homomeric proteins
    Nature Structural & Molecular Biology 25, 279–288 https://doi.org/10.1038/s41594-018-0029-5
  5. Farkas, Z., Kalapis, D., Bódi, Z., Szamecz, B., Daraba, A., Almási, K., Kovács, K., Boross, G., Pál, F., Horvath, P., Balassa, T., Molnar, Cs., Pettkó-Szandtner, A., Klement, É., Rutkai, E., Szvetnik, A., Papp, B., Pál, C.
    Hsp70-associated chaperones have a critical role in buffering protein production costs.
    Elife 2018 Jan 29;7. DOI: 10.7554/eLife.29845
  6. Marín de Mas, I.,Aguilar, E., Zodda, E., Balcells, C., Marin, S., Dallmann, G., Thomson, TM., Papp, B.*,Cascante, M.*
    Model-driven discovery of long-chain fatty acid metabolic reprogramming in heterogeneous prostate cancer cells.
    PLoS Comput. Biol. January 2, 2018 https://doi.org/10.1371/journal.pcbi.1005914
  7. Notebaart, RA., Kintses, B., Feist, AM., Papp, B. Underground metabolism: network-level perspective and biotechnological potential. Curr. Opin. Biotechnol. 49, 108-114 https://doi.org/10.1016/j.copbio.2017.07.015

2017:

  1. Pál, Cs.,Papp, B. Evolution of complex adaptations in molecular systems.
    Nature Ecology & Evolution 1, 1084–1092 https://doi.org/10.1038/s41559-017-0228-1
  2. Bódi, Z., Farkas, Z., Nevozhay, D., Kalapis, D., Lázár, V., Csörgő, B., Nyerges, Á., Szamecz, B., Fekete, G., Papp, B., Araújo, H., Oliveira, J.L., Moura, G., Santos, M.A.S., Székely, T. Balázsi, G., Pál, C. Phenotypic heterogeneity promotes adaptive evolutionPLoS Biol 15(5): e2000644.  https://doi.org/10.1371/journal.pbio.2000644
  1. Fritzemeier, J.C., Hartleb, D., Szappanos, B., Papp, B., Lercher, M.J. Erroneous energy-generating cycles in published genome scale metabolic networks: identification and removal. PLoS Comput Biol 13(4): e1005494 https://doi.org/10.1371/journal.pcbi.1005494
  1. Boross, G.,Papp, B.
    No evidence that protein noise-induced epigenetic epistasis constrains gene expression evolution.
    Molecular Biology and Evolution. (2017) 34 (2): 380-390. https://doi.org/10.1093/molbev/msw236
  2. Marín de Mas, I.,Fanchon, E., Papp, B., Roca, J., Cascante, M.
    Molecular mechanisms underlying COPD-muscle dysfunction unveiled through a systems medicine approach.
    Bioinformatics 33:95-103 https://doi.org/10.1093/bioinformatics/btw566

2016:

  1. Papp, B.,Lázár, V.
    Antibiotics: New recipe for targeting resistance.
    Nature Chemical Biology 12, 891–892 (2016) doi:10.1038/nchembio.2215
  2. Szappanos B.,Fritzemeier, J., Csörgő, B., Lázár, V., Xiaowen Lu,, Fekete, G., Bálint, B., Herczeg, R., Nagy, I.,Notebaart, R A., Lercher, M J., Pál, C.*, Papp, B.*
    Adaptive evolution of complex innovations through stepwise metabolic niche expansion
    Nature Communications 7: 11607 https://doi.org/10.1038/ncomms11607
  3. Karcagi, I.,Draskovits, G., Umenhoffer, K., Fekete, G., Kovács, K., Méhi, O., Balikó, G, Szappanos, B., Györfy, Z.,Fehér, T, Bogos, B., Blattner, F.R., Pál, C.*, Pósfai, G.*, Papp, B.*
    Indispensability of horizontally transferred genes and its impact on bacterial genome streamlining.
    Mol Biol Evol 33: 1257-1269.

2015:

  1. Pál, C, Papp, B, Lázár, V,
    Collateral sensitivity of antibiotic-resistant microbes
    Trends in Microbiology 23: 401-407 https://doi.org/10.1016/j.tim.2015.02.009

2014:

  1. Méhi, O, Bogos, B, Csörgő, B, Pál, F, Nyerges, Á, Papp, B, Pál, C,
    Perturbation of Iron Homeostasis Promotes the Evolution of Antibiotic Resistance.
    Mol Biol Evol 31: 2793-2804 https://doi.org/10.1093/molbev/msu223
  2. Notebaart, RA*,Szappanos, B, Kintses, B, Pál, F, Györkei, Á, Bogos, B, Lázár, V, Spohn, R, Csörgő, B,Wagner, A, Ruppin, E, Pál, C*, Papp, B*
    Network-level architecture and the evolutionary potential of underground metabolism.
    PNAS 111: 11762–11767 https://doi.org/10.1073/pnas.1406102111
  3. Szamecz, B,Boross, G, Kalapis, D, Kovács, K, Fekete, G, Farkas, Z, Lázár, V, Hrtyan, M, Kemmeren, P,Groot Koerkamp MJA, Rutkai, E, Holstege, FCP, Papp, B*, Pál, C*
    The genomic landscape of compensatory evolution.
    PLoS Biol 12(8): e1001935 https://doi.org/10.1371/journal.pbio.1001935
  4. Lázár, V,Nagy, I, Spohn, R, Csörgő, B, Györkei, A, Nyerges, Á, Horváth, B, Vörös, A, Busa-Fekete, R, Hrtyan, M,Bogos, B, Méhi, O, Fekete, G, Szappanos, B, Kégl, B, Papp, B*, Pál, C*
    Genome-wide analysis captures the determinants of the antibiotic cross-resistance interaction network.
    Nature Communications 5: 4352 doi: 10.1038/ncomms5352
  5. Ocampo, PS,Lázár, V, Papp, B, Arnoldini, M, Abel Zur Wiesch, P, Busa-Fekete, R, Fekete, G, Pál, C,Ackermann, M, Bonhoeffer, S
    Antagonism between bacteriostatic and bactericidal antibiotics is prevalent.
    Antimicrob Agents Chemotherapy 2014 May 27. pii: AAC.02463-14. doi: 10.1128/AAC.02463-14
  6. Csaba Pál,Balázs Papp, Pósfai, G
    The dawn of evolutionary genome engineering
    Nature Reviews Genetics 15: 504-512 doi:10.1038/nrg3746
  7. Benjamin VanderSluis,David C Hess, Colin Pesyna, Elias W Krumholz, Tahin Syed, Balázs Szappanos,Corey Nislow, Balázs Papp, Olga G Troyanskaya, Chad L Myers, Amy A Caudy
    Broad metabolic sensitivity profiling of a prototrophic yeast deletion collection
    Genome Biology 2014, 15:R64 https://doi.org/10.1186/gb-2014-15-4-r64
  8. Marín de Mas, I., Aguilar, E., Jayaraman, A., Polat, I.H., Martín-Bernabé, A., Bharat, R., Foguet, C., Milà, E., Papp, B., Centelles, J.J., Cascante, M. Cancer cell metabolism as new targets for novel designed therapiesFuture Med Chem. 6:1791-810

2013:

  1. Lázár, V, Singh, G P, Spohn, R, Nagy, I, Horváth, B, Hrtyan, M, Busa-Fekete, R, Bogos, B, Méhi, O, Csörgő, B, Pósfai, G, Fekete, G, Szappanos, B, Kégl, B, Papp, B*, Pál, C* Bacterial evolution of antibiotic hypersensitivity. Molecular Systems Biology 9:700 https://doi.org/10.1038/msb.2013.57
  1. Pál, C, Papp, B. From passengers to drivers: Impact of bacterial transposable elements on evolvability. Mob Genet Elements 3:e23617 DOI:10.4161/mge.23617
  1. Abrusán G, Szilágyi A, Zhang Y, Papp, B. Turning gold into ‘junk’: transposable elements utilize central proteins of cellular networks. Nucleic Acids Research 41:3190-200. DOI:10.1093/nar/gkt011

2012:

  1. Szalay-Bekő, M., Palotai, R., Szappanos, B., Kovács, I.A., Papp, B., Csermely, P. ModuLand Plug-in for Cytoscape: Determination of Hierarchical Layers of Overlapping Network Modules and Community Centrality. Bioinformatics 28: 2202 https://doi.org/10.1093/bioinformatics/bts352
  1. Fehér, T., Bogos, B., Méhi, O., Fekete, G., Csörgő, B., Kovács, K., Pósfai, G., Papp, B., Hurst, L.D., Pál, C. Competition between Transposable Elements and Mutator Genes in Bacteria Mol Biol Evol 29: 3153 doi:10.1093/molbev/mss122
  1. Sharifpoor, S., van Dyk, D., Costanzo, M., Baryshnikova, A., Friesen, H., Douglas, A.C., Youn, J.Y., Vandersluis, B., Myers, C.L., Papp, B., Boone, C., Andrews , B.J. Functional wiring of the yeast kinome revealed by global analysis of genetic network motifs. Genome Res 22: 791 doi:10.1101/gr.129213.111

2011:

  1. Papp, B., Notebaart, R.A., Pál, C. Systems-biology approaches for predicting genomic evolution. Nature Rev. Genet. 12: 591. doi:10.1038/nrg3033
  1. Papp, B., Pál, C. Systems biology of epistasis: shedding light on genetic interaction “hubs”. Cell Cycle 10: 2623. https://doi.org/10.4161/cc.10.21.17853
  1. Papp, B., Szappanos, B., Notebaart, R.A. Use of genome-scale metabolic models in evolutionary systems biology. Methods Mol. Biol. 759: 483. DOI 10.1007/978-1-61779-173-4_27
  1. Yizhak, K., Tuller, T., Papp, B., Eytan, R. Metabolic modeling of endosymbiont genome reduction on a temporal scale. Mol Sys Biol. 7: 479. https://doi.org/10.1038/msb.2011.11
  1. Szappanos, B., Kovács, K., Szamecz, B., Honti, F., Costanzo, M., Baryshnikova, A., Gelius-Dietrich, G., Lercher, M.J., Jelasity, M., Myers, C.L., Andrews, B.J., Boone, C., Oliver, S.G., Pál, C., Papp, B. An integrated approach to characterize genetic interaction networks in yeast metabolism. Nature Genetics 43: 656 doi:10.1038/ng.846

2010:

  1. VanderSluis, B., Bellay, J., Musso, G., Costanzo, M., Papp, B., Vizeacoumar, F.J., Baryshnikova, A., Andrews, B., Boone, C., Myers, C.L. Genetic interactions reveal the evolutionary trajectories of duplicate genesMol Sys Biol. 6: 429. https://doi.org/10.1038/msb.2010.82
  1. Costanzo et al. The Genetic Landscape of a Cell. Science 327: 425-431. DOI: 10.1126/science.1180823

2009:

  1. Kovacs, K., Hurst, L.D.*, Papp, B.* Stochasticity in Protein Levels Drives Colinearity of Gene Order in Metabolic Operons of Escherichia coli. PloS Biol. 7: e1000115. https://doi.org/10.1371/journal.pbio.1000115
  1. Papp, B., Teusink, B., Notebaart, R.A. A critical view of metabolic network adaptationsHFSP J. 3: 24-35. https://doi.org/10.2976/1.3020599

2008:

  1. Kun, A., Papp, B.*, Szathmary, E. Computational identification of obligatorily autocatalytic replicators embedded in metabolic networks. Genome Biol. 9: R51. https://doi.org/10.1186/gb-2008-9-3-r51
  1. Notebaart, R.A., Teusink, B., Siezen, R.J., Papp, B. Co-regulation of metabolic genes is better explained by flux coupling than by network distance. PloS Comp. Biol. 4: 157-163. DOI: 10.1371/journal.pcbi.0040026

2007:

  1. Pinney, J.W., Papp, B., Hyland, C., Wambua, L., Westhead, D.R., McConkey, G.A. Metabolic reconstruction and analysis for parasite genomes. Trends Parasitol 23: 548-554. doi:10.1016/j.pt.2007.08.013
  1. Feher, T., Papp, B., Pal, C., Posfai, G. Systematic Genome Reductions: Theoretical and Experimental Approaches. Chemical Reviews 107: 3498-3513 DOI: 10.1021/cr0683111
  1. Miskey, C., Papp, B., Mates, L., Sinzelle, L., Keller, H., Izsvak, Z., Ivics, Z. The Ancient Mariner Sails Again: Transposition of the Human Hsmar1 Element by a Reconstructed Transposase and Activities of the SETMAR Protein on Transposon Ends. Mol. Cell. Biol. 27: 4589-600. DOI: 10.1128/MCB.02027-06
  1. Harrison, R.*, Papp, B.*, Pal, C., Oliver SG., Delneri D. Plasticity of genetic interactions in metabolic networks of yeast. PNAS 104: 2307-12. https://doi.org/10.1073/pnas.0607153104
  1. Bundy, J.G., Papp, B., Harmston, R., Browne, R.A., Clayson, E.M., Burton, N., Reece, R.J, Oliver, S.G., Brindle, K.M. Evaluation of predicted network modules in yeast metabolism using NMR-based metabolite profiling. Genome Res. 17: 510-19. doi:10.1101/gr.5662207

2006:

  1. Pal, C., Papp, B., Lercher M.J. An integrated view on protein evolution. Nature Rev. Genet. 7: 337-348. doi:10.1038/nrg1838
  2. Sopko, R., Papp, B., Oliver, S.G., Andrews, B.J. Phenotypic activation to discover biological pathways and kinase substrates. Cell Cycle 5: 1397-402. DOI: 10.4161/cc.5.13.2922
  1. Pal, C.*, Papp, B.*, Lercher, MJ., Csermely, P., Oliver, SG., Laurence, D. Hurst. Chance and necessity in the evolution of minimal metabolic networks. Nature 440: 667-670. doi:10.1038/nature04568
  1. Sopko, R., Huang, D., Preston, N., Chua, G., Papp, B., Kafadar, K., Snyder, M., Oliver, S.G., Cyert, M., Hughes, T.R., Boone, C., Andrews, B. Mapping pathways and phenotypes by systematic gene overexpression. Mol. Cell 21: 319-30. DOI 10.1016/j.molcel.2005.12.011

2005:

  1. Pal, C., Papp, B., Lercher M.J. Adaptive evolution of bacterial metabolic networks by horizontal gene transferNature Genetics 37: 1372-5. DOI 10.1016/j.molcel.2005.12.011
  1. Pal, C., Papp, B., Lercher M.J. Horizontal gene transfer depends on gene content of the host. Bioinformatics 21: ii222-223 https://doi.org/10.1093/bioinformatics/bti1136
  1. Lovell, S.C., Papp, B. Report. Bioinformatics: from molecules to systems. A Discussion Meeting held at The Royal Society on 4 and 5 April 2005. Journal of The Royal Society Interface (DOI: 10.1098/rsif.2005.0053).
  1. Papp, B., Oliver, S.G. Genome-wide analysis of the context-dependence of regulatory networks. Genome Biology 6: 206. doi: 10.1186/gb-2005-6-2-206 Soti, C., Pal, C., Papp, B., Csermely, P. Molecular chaperones as regulatory elements of cellular networks. Current Opinion in Cell Biology 17: 210-215. DOI 10.1016/j.ceb.2005.02.012

2004:

  1. Papp, B., Pal, C., Hurst, L.D. Metabolic network analysis of the causes and evolution of enzyme dispensability in yeast. Nature 429: 661-4. doi:10.1038/nature02636

2003:

  1. Papp, B., Pal, C., Hurst, L.D. Dosage sensitivity and the evolution of gene family size in yeast. Nature 424: 194-7. doi:10.1038/nature01771
  2. Papp, B., Pal, C., Hurst, L.D. Evolution of cis-regulatory elements in duplicated genes of yeast. Trends Genet. 19: 417-22. doi:10.1016/S0168-9525(03)00174-4
  1. Pal, C., Papp, B., Hurst, L.D. Genomic function: Rate of evolution and gene dispensabilityNature 421: 496-7. DOI: 10.1038/421496b

2001:

  1. Pal, C., Papp, B., Hurst, L.D. Does the recombination rate affect the efficiency of purifying selection? The yeast genome provides a partial answer. Mol Biol Evol. 18: 2323-6. https://doi.org/10.1093/oxfordjournals.molbev.a003779
  1. Papp, B., Pal, C., Hurst, L.D., Highly expressed genes in yeast evolve slowly. Genetics 158: 927-931.

2000:

  1. Pal, C., Papp, B., Selfish cells threaten multicellular life. Trends Ecol Evol 15: 351-352.

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