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Molecular Systems Biology

Cover image for Vol. 9 Issue 1

2013

Volume 9, Issue 1

  1. Reviews

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      Evolution and functional cross-talk of protein post-translational modifications

      Pedro Beltrao, Peer Bork, Nevan J. Krogan and Vera van Noort

      Version of Record online: 20 DEC 2013 | DOI: 10.1002/msb.201304521

      Thumbnail image of graphical abstract

      Advances in proteomics have opened new avenues for the analysis of the evolution of protein post-translational modifications (PTMs) and have enabled the large-scale functional characterization of a range of different modifications types.

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      Interaction proteome of human Hippo signaling: modular control of the co-activator YAP1

      Simon Hauri, Alexander Wepf, Audrey van Drogen, Markku Varjosalo, Nic Tapon, Ruedi Aebersold and Matthias Gstaiger

      Version of Record online: 20 DEC 2013 | DOI: 10.1002/msb.201304750

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      Systematic characterization of the human Hippo pathway protein interactome by quantitative mass spectrometry generates a high-resolution network of 480 interactions among 270 proteins and reveals three major modules linked to the transcriptional coactivator YAP1.

  3. Report

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      Glutamine-driven oxidative phosphorylation is a major ATP source in transformed mammalian cells in both normoxia and hypoxia

      Jing Fan, Jurre J Kamphorst, Robin Mathew, Michelle K Chung, Eileen White, Tomer Shlomi and Joshua D Rabinowitz

      Version of Record online: 3 DEC 2013 | DOI: 10.1038/msb.2013.65

      The impact of oncogene activation and hypoxia on energy metabolism is analyzed by integrating quantitative measurements into a redox-balanced metabolic flux model. Glutamine-driven oxidative phosphorylation is found to be a major ATP source even in oncogene-expressing or hypoxic cells.

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      Timescales and bottlenecks in miRNA-dependent gene regulation

      Jean Hausser, Afzal Pasha Syed, Nathalie Selevsek, Erik van Nimwegen, Lukasz Jaskiewicz, Ruedi Aebersold and Mihaela Zavolan

      Version of Record online: 3 DEC 2013 | DOI: 10.1038/msb.2013.68

      Application of a kinetic model of miRNA-mediated gene regulation to experimental data sets shows that the timescale of regulation is slower than previously assumed, due to bottlenecks imposed by miRNA turnover in the RNA-induced silencing complex and by slow protein decay.

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      Transcriptional regulation is insufficient to explain substrate-induced flux changes in Bacillus subtilis

      Victor Chubukov, Markus Uhr, Ludovic Le Chat, Roelco J Kleijn, Matthieu Jules, Hannes Link, Stephane Aymerich, Jörg Stelling and Uwe Sauer

      Version of Record online: 26 NOV 2013 | DOI: 10.1038/msb.2013.66

      Regulation of enzyme expression is one key mechanism by which cells control their metabolic programs. In this work, a quantitative analysis of metabolism in a model bacterium under different conditions shows that expression alone cannot explain the majority of the observed metabolic changes.

  5. News & Views

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      Imaging the transcriptome

      Timothée Lionnet

      Version of Record online: 26 NOV 2013 | DOI: 10.1038/msb.2013.67

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      Metabolic reconstruction identifies strain-specific regulation of virulence in Toxoplasma gondii

      Carl Song, Melissa A Chiasson, Nirvana Nursimulu, Stacy S Hung, James Wasmuth, Michael E Grigg and John Parkinson

      Version of Record online: 19 NOV 2013 | DOI: 10.1038/msb.2013.62

      The first metabolic reconstruction for Toxoplasma gondiiiCS382’ is presented. Model simulations and drug assays identified strain-specific differences in growth rates that may reflect an evolutionary strategy, potentiating broad host range.

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      Cell size control is sirtuin(ly) exciting

      Jill Wright and Brandt L Schneider

      Version of Record online: 12 NOV 2013 | DOI: 10.1038/msb.2013.64

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      A pharmaco-epistasis strategy reveals a new cell size controlling pathway in yeast

      Fabien Moretto, Isabelle Sagot, Bertrand Daignan-Fornier and Benoît Pinson

      Version of Record online: 12 NOV 2013 | DOI: 10.1038/msb.2013.60

      Pharmaco-epistasis analyses using drugs mimicking cell size mutations in yeast uncovered a novel pathway in cell size homeostasis regulation. This pathway involves the sirtuin Sir2, the large ribosomal subunit (60S) and the Swi4/Swi6 transcription factors.

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      Promoter decoding of transcription factor dynamics

      Amie D Moody and Eric Batchelor

      Version of Record online: 5 NOV 2013 | DOI: 10.1038/msb.2013.63

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      Perturbation of the mutated EGFR interactome identifies vulnerabilities and resistance mechanisms

      Jiannong Li, Keiryn Bennett, Alexey Stukalov, Bin Fang, Guolin Zhang, Takeshi Yoshida, Isamu Okamoto, Jae-Young Kim, Lanxi Song, Yun Bai, Xiaoning Qian, Bhupendra Rawal, Michael Schell, Florian Grebien, Georg Winter, Uwe Rix, Steven Eschrich, Jacques Colinge, John Koomen, Giulio Superti-Furga and Eric B Haura

      Version of Record online: 5 NOV 2013 | DOI: 10.1038/msb.2013.61

      A ‘lung cancer’-specific mutant EGFR interactome was generated by a global analysis of protein–protein interactions and phosphorylation. After functional screening, nine proteins were identified as essential for the viability of EGFR-mutant lung cancer cells.

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      Promoter decoding of transcription factor dynamics involves a trade-off between noise and control of gene expression

      Anders S Hansen and Erin K O'Shea

      Version of Record online: 5 NOV 2013 | DOI: 10.1038/msb.2013.56

      The relationship between the dynamics of transcription factor activity, differential gene expression and noise in gene expression is analyzed in yeast to understand how different genetic programs can be activated by controlling the dynamics of a single transcription factor.

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      Promoters maintain their relative activity levels under different growth conditions

      Leeat Keren, Ora Zackay, Maya Lotan-Pompan, Uri Barenholz, Erez Dekel, Vered Sasson, Guy Aidelberg, Anat Bren, Danny Zeevi, Adina Weinberger, Uri Alon, Ron Milo and Eran Segal

      Version of Record online: 29 OCT 2013 | DOI: 10.1038/msb.2013.59

      Libraries of S. cerevisiae and E. coli promoter reporters measured under different conditions reveal scaling relationships between expression profiles across conditions and suggest that most changes in activity are due to global effects.

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      Design of orthogonal genetic switches based on a crosstalk map of σs, anti-σs, and promoters

      Virgil A Rhodius, Thomas H Segall-Shapiro, Brian D Sharon, Amar Ghodasara, Ekaterina Orlova, Hannah Tabakh, David H Burkhardt, Kevin Clancy, Todd C Peterson, Carol A Gross and Christopher A Voigt

      Version of Record online: 29 OCT 2013 | DOI: 10.1038/msb.2013.58

      The interaction specificities of extracytoplasmic function (ECF) sigma (σ) factors with promoters and their negative regulators (anti-σs) were mapped to identify non-crossreacting parts. These orthogonal sets represent a synthetic biology toolbox of genetic switches.

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      Bacterial evolution of antibiotic hypersensitivity

      Viktória Lázár, Gajinder Pal Singh, Réka Spohn, István Nagy, Balázs Horváth, Mónika Hrtyan, Róbert Busa-Fekete, Balázs Bogos, Orsolya Méhi, Bálint Csörgő, György Pósfai, Gergely Fekete, Balázs Szappanos, Balázs Kégl, Balázs Papp and Csaba Pál

      Version of Record online: 29 OCT 2013 | DOI: 10.1038/msb.2013.57

      Understanding how adaptation to a given antibiotic increases the sensitivity to other antibiotics is of great medical importance for the understanding of evolutionary trade-offs. Here, the first experimental map of such collateral sensitivity is presented, along with insights into the underlying mechanisms.

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      Root systems analysis branches out

      Klaus Palme and William Teale

      Version of Record online: 22 OCT 2013 | DOI: 10.1038/msb.2013.51

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      Sequential induction of auxin efflux and influx carriers regulates lateral root emergence

      Benjamin Péret, Alistair M Middleton, Andrew P French, Antoine Larrieu, Anthony Bishopp, Maria Njo, Darren M Wells, Silvana Porco, Nathan Mellor, Leah R Band, Ilda Casimiro, Jürgen Kleine-Vehn, Steffen Vanneste, Ilkka Sairanen, Romain Mallet, Göran Sandberg, Karin Ljung, Tom Beeckman, Eva Benkova, Jiří Friml, Eric Kramer, John R King, Ive De Smet, Tony Pridmore, Markus Owen and Malcolm J Bennett

      Version of Record online: 22 OCT 2013 | DOI: 10.1038/msb.2013.43

      Emergence of a new lateral root primordium through the outer layers of the parental root requires the sequential auxin-mediated induction of two auxin transporters. This positive feedback regulatory loop coordinates patterned gene expression in outer tissues.

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      Temporal control of self-organized pattern formation without morphogen gradients in bacteria

      Stephen Payne, Bochong Li, Yangxiaolu Cao, David Schaeffer, Marc D Ryser and Lingchong You

      Version of Record online: 8 OCT 2013 | DOI: 10.1038/msb.2013.55

      The generation of self-organized ring patterns of gene expression in the absence of a morphogen gradient was demonstrated using bacteria programmed by a synthetic gene circuit. This work presents a timing mechanism of pattern formation.

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      A negative genetic interaction map in isogenic cancer cell lines reveals cancer cell vulnerabilities

      Franco J Vizeacoumar, Roland Arnold, Frederick S Vizeacoumar, Megha Chandrashekhar, Alla Buzina, Jordan T F Young, Julian H M Kwan, Azin Sayad, Patricia Mero, Steffen Lawo, Hiromasa Tanaka, Kevin R Brown, Anastasia Baryshnikova, Anthony B Mak, Yaroslav Fedyshyn, Yadong Wang, Glauber C Brito, Dahlia Kasimer, Taras Makhnevych, Troy Ketela, Alessandro Datti, Mohan Babu, Andrew Emili, Laurence Pelletier, Jeff Wrana, Zev Wainberg, Philip M Kim, Robert Rottapel, Catherine A O'Brien, Brenda Andrews, Charles Boone and Jason Moffat

      Version of Record online: 8 OCT 2013 | DOI: 10.1038/msb.2013.54

      This study defines a network of synthetic sick/lethal interactions with a set of query genes in a series of isogenic cancer cell lines. Analysis of differential essentiality reveals general properties in genetic interaction networks derived from studies on model organisms.

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      Natural sequence variants of yeast environmental sensors confer cell-to-cell expression variability

      Steffen Fehrmann, Hélène Bottin-Duplus, Andri Leonidou, Esther Mollereau, Audrey Barthelaix, Wu Wei, Lars M Steinmetz and Gaël Yvert

      Version of Record online: 8 OCT 2013 | DOI: 10.1038/msb.2013.53

      DNA polymorphisms that change cell-to-cell variability in gene expression are identified in a screen for ‘Probabilistic Trait Loci’ in yeast. By modifying transmembrane transporter genes, these natural variants modulate intraclonal phenotypic diversification.

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      A competitive protein interaction network buffers Oct4-mediated differentiation to promote pluripotency in embryonic stem cells

      Silvia Muñoz Descalzo, Pau Rué, Fernando Faunes, Penelope Hayward, Lars Martin Jakt, Tina Balayo, Jordi Garcia-Ojalvo and Alfonso Martinez Arias

      Version of Record online: 8 OCT 2013 | DOI: 10.1038/msb.2013.49

      The dynamic competition for complex formation between the pluripotency network components Oct4, Nanog, Tcf3, and β-catenin prevents embryonic stem cell differentiation by controlling the levels of free Oct4.

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      Genome-scale models of metabolism and gene expression extend and refine growth phenotype prediction

      Edward J O'Brien, Joshua A Lerman, Roger L Chang, Daniel R Hyduke and Bernhard Ø Palsson

      Version of Record online: 1 OCT 2013 | DOI: 10.1038/msb.2013.52

      A constraint-based approach for integrative modeling of metabolism and gene expression is developed. New constraints on molecular catalysis increase both the accuracy and scope of computable phenotypes corresponding to optimal microbial growth.

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      Human disease locus discovery and mapping to molecular pathways through phylogenetic profiling

      Yuval Tabach, Tamar Golan, Abrahan Hernández-Hernández, Arielle R Messer, Tomoyuki Fukuda, Anna Kouznetsova, Jian-Guo Liu, Ingrid Lilienthal, Carmit Levy and Gary Ruvkun

      Version of Record online: 1 OCT 2013 | DOI: 10.1038/msb.2013.50

      By analyzing the conservation of human proteins across 87 species, we sorted proteins into clusters of coevolution. Some clusters are enriched for genes assigned to particular human diseases or molecular pathways; the other genes in the same cluster may function in related pathways and diseases.

  13. Review

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      Biomedically relevant circuit-design strategies in mammalian synthetic biology

      William Bacchus, Dominique Aubel and Martin Fussenegger

      Version of Record online: 24 SEP 2013 | DOI: 10.1038/msb.2013.48

      This review covers the burgeoning field of mammalian synthetic biology. New designs for potential clinical applications are discussed with examples of circuits that directly interface with endogenous cellular activities, enable intercellular communication or function as prothetic networks.

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      Dissection of a Krox20 positive feedback loop driving cell fate choices in hindbrain patterning

      Yassine X Bouchoucha, Jürgen Reingruber, Charlotte Labalette, Michel A Wassef, Elodie Thierion, Carole Desmarquet-Trin Dinh, David Holcman, Pascale Gilardi-Hebenstreit and Patrick Charnay

      Version of Record online: 24 SEP 2013 | DOI: 10.1038/msb.2013.46

      A positive autoregulatory loop required for the expression of the transcription factor Krox20 was dissected using in vivo quantitative data and biophysical modelling to demonstrate how Krox20 controls cell fate decision and rhombomere size in the hindbrain.

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      Protein synthesis rate is the predominant regulator of protein expression during differentiation

      Anders R Kristensen, Joerg Gsponer and Leonard J Foster

      Version of Record online: 17 SEP 2013 | DOI: 10.1038/msb.2013.47

      The contribution of transcription, protein synthesis and degradation rates to the control of protein expression during differentiation was analyzed using quantitative proteomics and transcriptomics data. Protein synthesis rate was identified as the main determinant of protein expression.

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      Barriers to transmission of transcriptional noise in a c-fos c-jun pathway

      Khyati Shah and Sanjay Tyagi

      Version of Record online: 10 SEP 2013 | DOI: 10.1038/msb.2013.45

      In higher eukaryotes, chromatin limits the transmission of transcriptional noise by insulating downstream genes from cell-to-cell variations in transcription factor heterodimers. In addition, heterodimers are shown to exhibit reduced cell-to-cell variation compared to their parent mRNAs.

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      Chromosome segregation by the Escherichia coli Min system

      Barbara Di Ventura, Benoît Knecht, Helena Andreas, William J Godinez, Miriam Fritsche, Karl Rohr, Walter Nickel, Dieter W Heermann and Victor Sourjik

      Version of Record online: 10 SEP 2013 | DOI: 10.1038/msb.2013.44

      The existence and nature of an active chromosome segregation apparatus in bacteria has been a long-standing debate. A novel Brownian ratchet-type mechanism of chromosome segregation mediated by the Min system is identified in E. coli.

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      A map of cell type-specific auxin responses

      Bastiaan O R Bargmann, Steffen Vanneste, Gabriel Krouk, Tal Nawy, Idan Efroni, Eilon Shani, Goh Choe, Jiří Friml, Dominique C Bergmann, Mark Estelle and Kenneth D Birnbaum

      Version of Record online: 10 SEP 2013 | DOI: 10.1038/msb.2013.40

      The transcriptional response to auxin was analyzed in four root cell types. The newly obtained data were cross-referenced with spatial expression maps to examine auxin's role in regulating gene expression in the root meristem.

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      Generalized bacterial genome editing using mobile group II introns and Cre-lox

      Peter J Enyeart, Steven M Chirieleison, Mai N Dao, Jiri Perutka, Erik M Quandt, Jun Yao, Jacob T Whitt, Adrian T Keatinge-Clay, Alan M Lambowitz and Andrew D Ellington

      Version of Record online: 3 SEP 2013 | DOI: 10.1038/msb.2013.41

      A general bacterial genome engineering framework, ‘Genome Editing via Targetrons and Recombinases’ (GETR), is presented. GETR combines mobile group II introns (targetrons) and the Cre/lox system to allow genomic manipulations at a large scale.

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      Multilevel selection analysis of a microbial social trait

      Laura de Vargas Roditi, Kerry E Boyle and Joao B Xavier

      Version of Record online: 20 AUG 2013 | DOI: 10.1038/msb.2013.42

      The evolution of cooperation in colonies of swarming bacteria is analyzed by manipulating the cost-to-benefit ratio of cooperation to show that ‘constitutive’ cooperation is favored only when relatedness is high, in contrast to ‘prudent’ cooperation.

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      Bacterial cheating drives the population dynamics of cooperative antibiotic resistance plasmids

      Eugene A Yurtsev, Hui Xiao Chao, Manoshi S Datta, Tatiana Artemova and Jeff Gore

      Version of Record online: 6 AUG 2013 | DOI: 10.1038/msb.2013.39

      Analysis of the cooperative nature of antibiotic inactivation reveals factors enabling coexistence of resistant and sensitive cells, showing that social interactions affect the spread of antibiotic resistance.

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      A yeast one-hybrid and microfluidics-based pipeline to map mammalian gene regulatory networks

      Carine Gubelmann, Sebastian M Waszak, Alina Isakova, Wiebke Holcombe, Korneel Hens, Antonina Iagovitina, Jean-Daniel Feuz, Sunil K Raghav, Jovan Simicevic and Bart Deplancke

      Version of Record online: 6 AUG 2013 | DOI: 10.1038/msb.2013.38

      A combined cross-platform approach is presented to experimentally identify and characterize interactions between mouse transcription factors and regulatory elements at unprecedented resolution and throughput.

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      Targeted proteomics reveals strain-specific changes in the mouse insulin and central metabolic pathways after a sustained high-fat diet

      Eduard Sabidó, Yibo Wu, Lucia Bautista, Thomas Porstmann, Ching-Yun Chang, Olga Vitek, Markus Stoffel and Ruedi Aebersold

      Version of Record online: 16 JUL 2013 | DOI: 10.1038/msb.2013.36

      Quantitative measurement of proteins involved in insulin signaling and central metabolism in C57BL/6J and 129Sv mice subjected to a sustained high-fat diet reveals that the two strains diverge early in their response to the feeding regimen.

  15. Corrigendum

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      Apoptosis and other immune biomarkers predict influenza vaccine responsiveness

      David Furman, Vladimir Jojic, Brian Kidd, Shai Shen-Orr, Jordan Price, Justin Jarrell, Tiffany Tse, Huang Huang, Peder Lund, Holden T Maecker, Paul J Utz, Cornelia L Dekker, Daphne Koller and Mark M Davis

      Version of Record online: 2 JUL 2013 | DOI: 10.1038/msb.2013.37

      This article corrects:

      Apoptosis and other immune biomarkers predict influenza vaccine responsiveness

      Vol. 9, Issue 1, Version of Record online: 16 APR 2013

  16. Article

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      Insulin/IGF-1-mediated longevity is marked by reduced protein metabolism

      Gerdine J Stout, Edwin C A Stigter, Paul B Essers, Klaas W Mulder, Annemieke Kolkman, Dorien S Snijders, Niels J F van den Broek, Marco C Betist, Hendrik C Korswagen, Alyson W MacInnes and Arjan B Brenkman

      Version of Record online: 2 JUL 2013 | DOI: 10.1038/msb.2013.35

      Quantitative proteomics, lifespan analysis, and biochemical assays were utilized to show that Insulin/IGF-1-mediated longevity in C. elegans is strongly associated with a daf-16 dependent global reduction in protein metabolism.

  17. Report

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      In vitro integration of ribosomal RNA synthesis, ribosome assembly, and translation

      Michael C Jewett, Brian R Fritz, Laura E Timmerman and George M Church

      Version of Record online: 25 JUN 2013 | DOI: 10.1038/msb.2013.31

      This report describes an integrated method for in vitro construction of Escherichia coli ribosomes under near-physiological conditions. This method enables coupling of ribosome synthesis and assembly in a single, integrated system.

  18. Article

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      Efficient translation initiation dictates codon usage at gene start

      Kajetan Bentele, Paul Saffert, Robert Rauscher, Zoya Ignatova and Nils Blüthgen

      Version of Record online: 18 JUN 2013 | DOI: 10.1038/msb.2013.32

      Rare codons are enriched at gene start in many genomes. Genome analysis and experimental testing show that this enrichment evolved to keep the ribosome binding site free from stable mRNA structures, in order to facilitate efficient translation initiation.

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      Dissecting a complex chemical stress: chemogenomic profiling of plant hydrolysates

      Jeffrey M Skerker, Dacia Leon, Morgan N Price, Jordan S Mar, Daniel R Tarjan, Kelly M Wetmore, Adam M Deutschbauer, Jason K Baumohl, Stefan Bauer, Ana B Ibáñez, Valerie D Mitchell, Cindy H Wu, Ping Hu, Terry Hazen and Adam P Arkin

      Version of Record online: 18 JUN 2013 | DOI: 10.1038/msb.2013.30

      Complex chemical stress arises during the production of biofuels. Large-scale mutant fitness profiling was used to identify bacterial and yeast tolerance genes and to model fitness in a complex hydrolysate mixture. The resulting model can be used to engineer more tolerant strains.

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      Integrative genomics of gene and metabolic regulation by estrogen receptors α and β, and their coregulators

      Zeynep Madak-Erdogan, Tze-Howe Charn, Yan Jiang, Edison T Liu, John A Katzenellenbogen and Benita S Katzenellenbogen

      Version of Record online: 18 JUN 2013 | DOI: 10.1038/msb.2013.28

      To define how the estrogen receptors α and β control specific responses in breast cancer cells, genome-wide patterns of chromatin binding of the ERα and ERβ receptors and their coregulators, SRC3 and RIP140, were determined and integrated with gene expression data and functional analyses.

  19. Errata

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      RNAi screening reveals a large signaling network controlling the Golgi apparatus in human cells

      Joanne Chia, Germaine Goh, Victor Racine, Susanne Ng, Pankaj Kumar and Frederic Bard

      Version of Record online: 11 JUN 2013 | DOI: 10.1038/msb.2013.34

      This article corrects:
  20. News & Views

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      The HDAC interaction network

      Ilana Livyatan and Eran Meshorer

      Version of Record online: 11 JUN 2013 | DOI: 10.1038/msb.2013.33

  21. Article

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      Network quantification of EGFR signaling unveils potential for targeted combination therapy

      Bertram Klinger, Anja Sieber, Raphaela Fritsche-Guenther, Franziska Witzel, Leanne Berry, Dirk Schumacher, Yibing Yan, Pawel Durek, Mark Merchant, Reinhold Schäfer, Christine Sers and Nils Blüthgen

      Version of Record online: 11 JUN 2013 | DOI: 10.1038/msb.2013.29

      Analysis of the signaling response of colon cancer cells to systematic perturbations reveals an EGF receptor-mediated cross-talk between the MAPK and AKT pathways. Accordingly, the predicted combinatorial treatment is shown to inhibit tumor growth in vivo.

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      The functional interactome landscape of the human histone deacetylase family

      Preeti Joshi, Todd M Greco, Amanda J Guise, Yang Luo, Fang Yu, Alexey I Nesvizhskii and Ileana M Cristea

      Version of Record online: 11 JUN 2013 | DOI: 10.1038/msb.2013.26

      This study presents the first global protein interaction network for all 11 human HDACs in T cells and an integrative mass spectrometry approach for profiling relative interaction stability within isolated protein complexes.

  22. Report

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      Synthetic mammalian transgene negative autoregulation

      Vinay Shimoga, Jacob T White, Yi Li, Eduardo Sontag and Leonidas Bleris

      Version of Record online: 4 JUN 2013 | DOI: 10.1038/msb.2013.27

      The effect of negative feedback on global and local sources of uncertainty is studied with synthetic circuits stably integrated in human cells. Negative feedback is shown to be the most efficient way to mitigate the effects of global fluctuations by introducing a single additional regulatory link.

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      Phosphoproteome dynamics reveal novel ERK1/2 MAP kinase substrates with broad spectrum of functions

      Mathieu Courcelles, Christophe Frémin, Laure Voisin, Sébastien Lemieux, Sylvain Meloche and Pierre Thibault

      Version of Record online: 28 MAY 2013 | DOI: 10.1038/msb.2013.25

      Quantitative phosphoproteomics was used to measure the dynamic changes in phosphorylation of ERK1/2 MAP kinases consensus sequences in epithelial cells and to identify 128 novel candidate substrates involved in a broad spectrum of biological functions.

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      The Neurospora photoreceptor VIVID exerts negative and positive control on light sensing to achieve adaptation

      Elan Gin, Axel C R Diernfellner, Michael Brunner and Thomas Höfer

      Version of Record online: 28 MAY 2013 | DOI: 10.1038/msb.2013.24

      Light adaptation in Neurospora is mediated by the photoreceptor VIVID, which exerts both a negative and positive effect on light sensing. These apparently paradoxical roles of VIVID are explained by the dynamics of a network motif that utilizes futile cycling.

  24. Report

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      A global S. cerevisiae small ubiquitin-related modifier (SUMO) system interactome

      Tharan Srikumar, Megan C Lewicki and Brian Raught

      Version of Record online: 28 MAY 2013 | DOI: 10.1038/msb.2013.23

      A global physical interaction map of the SUMO system was generated to study its functional organization. This resource was used to validate several E3-specific substrates and uncover novel roles for Ubc9 and Ulp2 in ribosomal DNA maintenance.

  25. Review

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      Computational meta'omics for microbial community studies

      Nicola Segata, Daniela Boernigen, Timothy L Tickle, Xochitl C Morgan, Wendy S Garrett and Curtis Huttenhower

      Version of Record online: 14 MAY 2013 | DOI: 10.1038/msb.2013.22

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      Nucleotide degradation and ribose salvage in yeast

      Yi-Fan Xu, Fabien Létisse, Farnaz Absalan, Wenyun Lu, Ekaterina Kuznetsova, Greg Brown, Amy A Caudy, Alexander F Yakunin, James R Broach and Joshua D Rabinowitz

      Version of Record online: 14 MAY 2013 | DOI: 10.1038/msb.2013.21

      Metabolomics, genetics and biochemistry were combined to obtain the first complete map of the nucleotide degradation and ribose salvage pathway in yeast. This pathway promotes yeast survival in starvation and oxidative stress.

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      The selective control of glycolysis, gluconeogenesis and glycogenesis by temporal insulin patterns

      Rei Noguchi, Hiroyuki Kubota, Katsuyuki Yugi, Yu Toyoshima, Yasunori Komori, Tomoyoshi Soga and Shinya Kuroda

      Version of Record online: 14 MAY 2013 | DOI: 10.1038/msb.2013.19

      The regulation of glucose metabolism by pulse stimulations of insulin is compared with the effect of ramp stimulations. Specific network motifs mediate the differential response to these temporal patterns of stimulations that mimic in vivo patterns of insulin secretion.

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      Characterization of drug-induced transcriptional modules: towards drug repositioning and functional understanding

      Murat Iskar, Georg Zeller, Peter Blattmann, Monica Campillos, Michael Kuhn, Katarzyna H Kaminska, Heiko Runz, Anne-Claude Gavin, Rainer Pepperkok, Vera van Noort and Peer Bork

      Version of Record online: 30 APR 2013 | DOI: 10.1038/msb.2013.20

      Drug-induced transcriptional modules (biclusters) were identified and annotated in three human cell lines and rat liver. These were used to assess conservation across systems and to infer and experimentally validate novel drug effects and gene functions.

  27. Review

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      Basic and applied uses of genome-scale metabolic network reconstructions of Escherichia coli

      Douglas McCloskey, Bernhard Ø Palsson and Adam M Feist

      Version of Record online: 30 APR 2013 | DOI: 10.1038/msb.2013.18

      This review summarizes the applications enabled by genome-scale models of metabolism for the bacterium E. coli. It provides an overview of the applications along with a critical assessment of their successes and limitations, and a perspective on likely future developments in the field.

  28. Article

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      Systematic identification of proteins that elicit drug side effects

      Michael Kuhn, Mumna Al Banchaabouchi, Monica Campillos, Lars Juhl Jensen, Cornelius Gross, Anne-Claude Gavin and Peer Bork

      Version of Record online: 30 APR 2013 | DOI: 10.1038/msb.2013.10

      Protein–side effects associations are identified by integrating drug–target data with side effects information from drug labels. Benchmarking against the literature and validation with an in vivo mouse model shows that these pairs correspond to causal relations.

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      Global remodelling of cellular microenvironment due to loss of collagen VII

      Victoria Küttner, Claudia Mack, Kristoffer TG Rigbolt, Johannes S Kern, Oliver Schilling, Hauke Busch, Leena Bruckner-Tuderman and Jörn Dengjel

      Version of Record online: 16 APR 2013 | DOI: 10.1038/msb.2013.17

      Loss of collagen VII causes recessive dystrophic epidermolysis bullosa. Quantitative proteomics analysis of the extracellular matrix and secretome of human fibroblasts derived from pathologically altered skin reveals a global remodelling of the cellular microenvironment.

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      Indirect and suboptimal control of gene expression is widespread in bacteria

      Morgan N Price, Adam M Deutschbauer, Jeffrey M Skerker, Kelly M Wetmore, Troy Ruths, Jordan S Mar, Jennifer V Kuehl, Wenjun Shao and Adam P Arkin

      Version of Record online: 16 APR 2013 | DOI: 10.1038/msb.2013.16

      This study shows that, in bacteria grown in the laboratory, there is little correlation between when genes are important for fitness and when they are more highly expressed. Most genes thus appear to be regulated by signals that are not related to their function.

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      Apoptosis and other immune biomarkers predict influenza vaccine responsiveness

      David Furman, Vladimir Jojic, Brian Kidd, Shai Shen-Orr, Jordan Price, Justin Jarrell, Tiffany Tse, Huang Huang, Peder Lund, Holden T Maecker, Paul J Utz, Cornelia L Dekker, Daphne Koller and Mark M Davis

      Version of Record online: 16 APR 2013 | DOI: 10.1038/msb.2013.15

      A systems analysis of immune biomarkers in 89 young and older adults revealed age-dependent and age-independent features, including markers of apoptosis that correlated with antibody responses to a seasonal influenza vaccine.

      Corrected by:

      Corrigendum: Apoptosis and other immune biomarkers predict influenza vaccine responsiveness

      Vol. 10, Issue 9, Version of Record online: 8 SEP 2014

    5. You have full text access to this OnlineOpen article
      Dissecting specific and global transcriptional regulation of bacterial gene expression

      Luca Gerosa, Karl Kochanowski, Matthias Heinemann and Uwe Sauer

      Version of Record online: 16 APR 2013 | DOI: 10.1038/msb.2013.14

      An experimental-computational approach is applied to dissect the contribution of specific transcription factor-mediated versus global growth-dependent regulation to bacterial gene expression, and obtain a quantitative understanding of dynamic adaptations in arginine biosynthesis of E. coli.

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      Increasing population growth by asymmetric segregation of a limiting resource during cell division

      Nurit Avraham, Ilya Soifer, Miri Carmi and Naama Barkai

      Version of Record online: 16 APR 2013 | DOI: 10.1038/msb.2013.13

      When stressed by metal depletion, budding yeast adopt an asymmetric division pattern whereby vacuoles are maintained within dividing mother cells while the vacuoles-deprived daughter cells arrest division. This linear growth mode represents a bet-hedging strategy beneficial at the population level.

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      Construction of human activity-based phosphorylation networks

      Robert H Newman, Jianfei Hu, Hee-Sool Rho, Zhi Xie, Crystal Woodard, John Neiswinger, Christopher Cooper, Matthew Shirley, Hillary M Clark, Shaohui Hu, Woochang Hwang, Jun Seop Jeong, George Wu, Jimmy Lin, Xinxin Gao, Qiang Ni, Renu Goel, Shuli Xia, Hongkai Ji, Kevin N Dalby, Morris J Birnbaum, Philip A Cole, Stefan Knapp, Alexey G Ryazanov, Donald J Zack, Seth Blackshaw, Tony Pawson, Anne-Claude Gingras, Stephen Desiderio, Akhilesh Pandey, Benjamin E Turk, Jin Zhang, Heng Zhu and Jiang Qian

      Version of Record online: 2 APR 2013 | DOI: 10.1038/msb.2013.12

      A high-resolution map of human phosphorylation networks was constructed by integrating experimentally determined kinase-substrate relationships with other resources, such as in vivo phosphorylation sites.

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      Temporal system-level organization of the switch from glycolytic to gluconeogenic operation in yeast

      Guillermo G Zampar, Anne Kümmel, Jennifer Ewald, Stefan Jol, Bastian Niebel, Paola Picotti, Ruedi Aebersold, Uwe Sauer, Nicola Zamboni and Matthias Heinemann

      Version of Record online: 2 APR 2013 | DOI: 10.1038/msb.2013.11

      Metabolome, proteome and physiology measurements were combined with mathematical modeling to unravel the temporal regulation of the metabolic fluxes during the diauxic shift in Saccharomyces cerevisiae.

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      SH3 interactome conserves general function over specific form

      Xiaofeng Xin, David Gfeller, Jackie Cheng, Raffi Tonikian, Lin Sun, Ailan Guo, Lianet Lopez, Alevtina Pavlenco, Adenrele Akintobi, Yingnan Zhang, Jean-François Rual, Bridget Currell, Somasekar Seshagiri, Tong Hao, Xinping Yang, Yun A Shen, Kourosh Salehi-Ashtiani, Jingjing Li, Aaron T Cheng, Dryden Bouamalay, Adrien Lugari, David E Hill, Mark L Grimes, David G Drubin, Barth D Grant, Marc Vidal, Charles Boone, Sachdev S Sidhu and Gary D Bader

      Version of Record online: 2 APR 2013 | DOI: 10.1038/msb.2013.9

      The Caenorhabditis elegans SH3 domain interactome was mapped and compared with the yeast SH3 interactome. Orthologous SH3 domain-mediated interactions are highly rewired, but the general function of the SH3 domain network is conserved between the two species

    10. You have full text access to this OnlineOpen article
      Plant stem cell maintenance involves direct transcriptional repression of differentiation program

      Ram Kishor Yadav, Mariano Perales, Jérémy Gruel, Carolyn Ohno, Marcus Heisler, Thomas Girke, Henrik Jönsson and G Venugopala Reddy

      Version of Record online: 2 APR 2013 | DOI: 10.1038/msb.2013.8

      The plant stem cell regulator WUSCHEL is shown to repress differentiation-promoting transcription factors. This regulatory network is analyzed with a computational model of the three-dimensional shoot stem cell niche and a combination of genetic perturbation and live imaging.

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      Dissecting the energy metabolism in Mycoplasma pneumoniae through genome-scale metabolic modeling

      Judith A H Wodke, Jacek Puchałka, Maria Lluch-Senar, Josep Marcos, Eva Yus, Miguel Godinho, Ricardo Gutiérrez-Gallego, Vitor A P Martins dos Santos, Luis Serrano, Edda Klipp and Tobias Maier

      Version of Record online: 2 APR 2013 | DOI: 10.1038/msb.2013.6

      A new genome-scale metabolic reconstruction of M. pneumonia is used in combination with external metabolite measurement and protein abundance measurements to quantitatively explore the energy metabolism of this genome-reduce human pathogen.

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      Network balance via CRY signalling controls the Arabidopsis circadian clock over ambient temperatures

      Peter D Gould, Nicolas Ugarte, Mirela Domijan, Maria Costa, Julia Foreman, Dana MacGregor, Ken Rose, Jayne Griffiths, Andrew J Millar, Bärbel Finkenstädt, Steven Penfield, David A Rand, Karen J Halliday and Anthony J W Hall

      Version of Record online: 19 MAR 2013 | DOI: 10.1038/msb.2013.7

      Temperature compensation of the Arabidopsis circadian clock is shown to be mediated by the interaction of light and temperature at the level of the crytochrome photoreceptors. These findings reveal that light and temperature share common input mechanisms to the circadian network.

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      Integration of clinical data with a genome-scale metabolic model of the human adipocyte

      Adil Mardinoglu, Rasmus Agren, Caroline Kampf, Anna Asplund, Intawat Nookaew, Peter Jacobson, Andrew J Walley, Philippe Froguel, Lena M Carlsson, Mathias Uhlen and Jens Nielsen

      Version of Record online: 19 MAR 2013 | DOI: 10.1038/msb.2013.5

      Combining large-scale immunohistochemical analysis and proteomics data, 7340 gene products are identified in human adipocytes. Based on this data, a genome-scale metabolic model is reconstructed and used to integrate clinical and transcriptome data from lean and obese subjects.

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      Cell type-specific nuclear pores: a case in point for context-dependent stoichiometry of molecular machines

      Alessandro Ori, Niccolò Banterle, Murat Iskar, Amparo Andrés-Pons, Claudia Escher, Huy Khanh Bui, Lenore Sparks, Victor Solis-Mezarino, Oliver Rinner, Peer Bork, Edward A Lemke and Martin Beck

      Version of Record online: 19 MAR 2013 | DOI: 10.1038/msb.2013.4

      The stoichiometry of the human nuclear pore complex is revealed by targeted mass spectrometry and super-resolution microscopy. The analysis reveals that the composition of the nuclear pore and other nuclear protein complexes is remodeled as a function of the cell type.

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      A fluorescent reporter for mapping cellular protein-protein interactions in time and space

      Daniel Moreno, Joachim Neller, Hans A Kestler, Johann Kraus, Alexander Dünkler and Nils Johnsson

      Version of Record online: 19 MAR 2013 | DOI: 10.1038/msb.2013.3

      A method based on a combination of the Split-Ubiquitin system with two spectrally different fluorescent proteins (SPLIFF) is shown to enable measurement of protein interactions in vivo with high spatial and temporal resolution in yeast.

  29. Report

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      Epigenetic epistatic interactions constrain the evolution of gene expression

      Solip Park and Ben Lehner

      Version of Record online: 19 FEB 2013 | DOI: 10.1038/msb.2013.2

      Harmful epistatic (genetic) interactions not only occur between mutations, but also when genes change in expression. Gene expression dynamics in yeast suggests that this ‘epigenetic’ epistasis constrains evolution, with the tight regulation of network hubs promoting a robust, ‘canalized’ phenotype.

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      Programming biological models in Python using PySB

      Carlos F Lopez, Jeremy L Muhlich, John A Bachman and Peter K Sorger

      Version of Record online: 19 FEB 2013 | DOI: 10.1038/msb.2013.1

      PySB is a framework for creating biological models as Python programs using a high-level, action-oriented vocabulary that promotes transparency, extensibility and reusability. PySB interoperates with many existing modeling tools and supports distributed model development.

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      Evolutionary potential, cross-stress behavior and the genetic basis of acquired stress resistance in Escherichia coli

      Martin Dragosits, Vadim Mozhayskiy, Semarhy Quinones-Soto, Jiyeon Park and Ilias Tagkopoulos

      Version of Record online: 5 FEB 2013 | DOI: 10.1038/msb.2012.76

      Escherichia coli cells were evolved over 500 generations and profiled in four abiotic stressors to observe several cases of emerging cross-stress behavior whereby adaptation to one stressful environment provided fitness advantage when exposed to a second stressor.

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      Properties of cell death models calibrated and compared using Bayesian approaches

      Hoda Eydgahi, William W Chen, Jeremy L Muhlich, Dennis Vitkup, John N Tsitsiklis and Peter K Sorger

      Version of Record online: 5 FEB 2013 | DOI: 10.1038/msb.2012.69

      A Bayesian framework is used to calibrate a mass-action model of receptor-mediated apoptosis. Despite parameter non-identifiability and model ‘sloppiness’, Bayes factor analysis discriminates between two alternative models of mitochondrial outer membrane permeabilization.

  31. Editorial

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      Reading and writing omes

      George M Church

      Version of Record online: 22 JAN 2013 | DOI: 10.1038/msb.2012.75

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      Genome-wide analysis of FOXO3 mediated transcription regulation through RNA polymerase II profiling

      Astrid Eijkelenboom, Michal Mokry, Elzo de Wit, Lydia M Smits, Paulien E Polderman, Miranda H van Triest, Ruben van Boxtel, Almut Schulze, Wouter de Laat, Edwin Cuppen and Boudewijn M T Burgering

      Version of Record online: 22 JAN 2013 | DOI: 10.1038/msb.2012.74

      By comparative analysis of RNA polymerase II and FOXO3 ChIP-sequencing, combined with 4C-sequencing and ChIPs on histone modifications, general mechanisms of FOXO3-mediated target gene regulation are identified.

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      An in vivo control map for the eukaryotic mRNA translation machinery

      Helena Firczuk, Shichina Kannambath, Jürgen Pahle, Amy Claydon, Robert Beynon, John Duncan, Hans Westerhoff, Pedro Mendes and John EG McCarthy

      Version of Record online: 22 JAN 2013 | DOI: 10.1038/msb.2012.73

      A new quantitative strategy has generated a comprehensive rate control map for protein synthesis in exponentially growing yeast cells. This analysis reveals the modularity of the system as well as highly non-stoichiometric relationships between components.

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      Accurate measurements of dynamics and reproducibility in small genetic networks

      Julien O Dubuis, Reba Samanta and Thomas Gregor

      Version of Record online: 22 JAN 2013 | DOI: 10.1038/msb.2012.72

      Precise analysis of systematic errors shows suitability of immunofluorescence protocols to quantify gene expression means, variances, and cross-correlations. Application to Drosophila gap genes enables reconstructing expression level dynamics and the progression of positional accuracy.

    4. You have full text access to this OnlineOpen article
      Autonomous bacterial localization and gene expression based on nearby cell receptor density

      Hsuan-Chen Wu, Chen-Yu Tsao, David N Quan, Yi Cheng, Matthew D Servinsky, Karen K Carter, Kathleen J Jee, Jessica L Terrell, Amin Zargar, Gary W Rubloff, Gregory F Payne, James J Valdes and William E Bentley

      Version of Record online: 22 JAN 2013 | DOI: 10.1038/msb.2012.71

      Escherichia coli were engineered to enable programmed motility, sensing and phenotypic response to the density of epidermal growth factor receptor expressed on the surface of cancer cells.

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      Shared control of gene expression in bacteria by transcription factors and global physiology of the cell

      Sara Berthoumieux, Hidde de Jong, Guillaume Baptist, Corinne Pinel, Caroline Ranquet, Delphine Ropers and Johannes Geiselmann

      Version of Record online: 22 JAN 2013 | DOI: 10.1038/msb.2012.70

      A simple, parameterless mathematical model, in combination with real-time monitoring of promoter activities, shows how control of gene expression in bacteria is shared between transcription factors and global physiological effects.

    6. You have full text access to this OnlineOpen article
      Systematic analysis of somatic mutations in phosphorylation signaling predicts novel cancer drivers

      Jüri Reimand and Gary D Bader

      Version of Record online: 22 JAN 2013 | DOI: 10.1038/msb.2012.68

      Phosphorylation sites of human proteins are frequently mutated in cancer. Statistical analysis of phosphorylation-associated single nucleotide variants (pSNVs) predicts novel cancer drivers and phospho-mutation mechanisms in known cancer genes.

      Corrected by:

      Corrigendum: Systematic analysis of somatic mutations in phosphorylation signaling predicts novel cancer drivers

      Vol. 10, Issue 8, Version of Record online: 28 AUG 2014

    7. You have full text access to this OnlineOpen article
      Widespread splicing changes in human brain development and aging

      Pavel Mazin, Jieyi Xiong, Xiling Liu, Zheng Yan, Xiaoyu Zhang, Mingshuang Li, Liu He, Mehmet Somel, Yuan Yuan, Yi-Ping Phoebe Chen, Na Li, Yuhui Hu, Ning Fu, Zhibin Ning, Rong Zeng, Hongyi Yang, Wei Chen, Mikhail Gelfand and Philipp Khaitovich

      Version of Record online: 22 JAN 2013 | DOI: 10.1038/msb.2012.67

      Human brain transcriptome analysis revealed widespread age-related splicing changes in the prefrontal cortex and cerebellum. While most of the splicing changes take place in development, approximately one-third of them extends into aging.

  33. Review

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      Genome-scale engineering for systems and synthetic biology

      Kevin M Esvelt and Harris H Wang

      Version of Record online: 22 JAN 2013 | DOI: 10.1038/msb.2012.66

      This review provides an overview of methodologies and technologies enabling genome-scale engineering, focusing on the design, construction, and testing of modified genomes in a variety of organisms. Future applications for systems and synthetic biology are discussed.

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      High-throughput sequencing for biology and medicine

      Wendy Weijia Soon, Manoj Hariharan and Michael P Snyder

      Version of Record online: 22 JAN 2013 | DOI: 10.1038/msb.2012.61

      Genome sequencing technologies have advanced rapidly, dramatically decreasing cost and increasing throughput. But beyond faster and cheaper, these advances have also stimulated the development of innovative new experimental approaches, and are opening new doors in human medicine and health.

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      An Oct4-Sall4-Nanog network controls developmental progression in the pre-implantation mouse embryo

      Meng How Tan, Kin Fai Au, Denise E Leong, Kira Foygel, Wing H Wong and Mylene WM Yao

      Version of Record online: 8 JAN 2013 | DOI: 10.1038/msb.2012.65

      Coordination of many biological processes is necessary for mammalian pre-implantation embryo development. The underlying regulatory network was mapped through mathematical modeling, gene-specific knockdowns, and profiling of pooled embryos, single embryos, and single cells.

    2. You have full text access to this OnlineOpen article
      Deconvolving the roles of Wnt ligands and receptors in sensing and amplification

      Rui Zhen Tan, Ni Ji, Remco A Mentink, Hendrik C Korswagen and Alexander van Oudenaarden

      Version of Record online: 8 JAN 2013 | DOI: 10.1038/msb.2012.64

      Establishment of cell polarity involves sensing of external cues followed by signal amplification. Analysis of Caenorhabditis elegans P-cell polarity in Wnt ligand and receptor mutants is used to separate the contribution of ligands and receptors to the sensing and amplification processes.

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