Design patterns of biological cells

Andrews, Steven S.; Wiley, H. Steven; Sauro, Herbert M.

doi:10.1002/bies.202300188

Design patterns of biological cells

Journal Article · Sun Jan 21 00:00:00 EST 2024 · BioEssays

DOI:https://doi.org/10.1002/bies.202300188· OSTI ID:2376130

^[1]; ^[2]; ^[1]

Univ. of Washington, Seattle, WA (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Design patterns are generalized solutions to frequently recurring problems. They were initially developed by architects and computer scientists to create a higher level of abstraction for their designs. Here, we extend these concepts to cell biology to lend a new perspective on the evolved designs of cells' underlying reaction networks. We present a catalog of 21 design patterns divided into three categories: creational patterns describe processes that build the cell, structural patterns describe the layouts of reaction networks, and behavioral patterns describe reaction network function. Applying this pattern language to the E. coli central metabolic reaction network, the yeast pheromone response signaling network, and other examples lends new insights into these systems.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH)

Grant/Contract Number:: AC05-76RL01830; U01CA227544

OSTI ID:: 2376130

Report Number(s):: PNNL-SA-193524

Journal Information:: BioEssays, Vol. 46, Issue 3; ISSN 0265-9247

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (180)

Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system Batchelor, E.; Goulian, M. Proceedings of the National Academy of Sciences, Vol. 100, Issue 2 https://doi.org/10.1073/pnas.0234782100	journal	January 2003
Regulation of lipid stores and metabolism by lipophagy Liu, K.; Czaja, M. J. Cell Death & Differentiation, Vol. 20, Issue 1 https://doi.org/10.1038/cdd.2012.63	journal	May 2012
Modeling transcriptional regulatory networks Bolouri, Hamid; Davidson, Eric H. BioEssays, Vol. 24, Issue 12 https://doi.org/10.1002/bies.10189	journal	November 2002
YeastGPCRsignaling reflects the fraction of occupied receptors, not the number Bush, Alan; Vasen, Gustavo; Constantinou, Andreas Molecular Systems Biology, Vol. 12, Issue 12 https://doi.org/10.15252/msb.20166910	journal	December 2016
Hsp90 interacts with inducible NO synthase client protein in its heme‐free state and then drives heme insertion by an ATP‐dependent process Ghosh, Arnab; Chawla‐Sarkar, Mamta; Stuehr, Dennis J. The FASEB Journal, Vol. 25, Issue 6 https://doi.org/10.1096/fj.10-180554	journal	February 2011
A universal biomolecular integral feedback controller for robust perfect adaptation Aoki, Stephanie K.; Lillacci, Gabriele; Gupta, Ankit Nature, Vol. 570, Issue 7762 https://doi.org/10.1038/s41586-019-1321-1	journal	June 2019
Conformational spread in a ring of proteins: a stochastic approach to allostery Duke, T. A. J.; Le Novère, N.; Bray, D. Journal of Molecular Biology, Vol. 308, Issue 3 https://doi.org/10.1006/jmbi.2001.4610	journal	May 2001
The Hill equation: a review of its capabilities in pharmacological modelling Goutelle, Sylvain; Maurin, Michel; Rougier, Florent Fundamental & Clinical Pharmacology, Vol. 22, Issue 6 https://doi.org/10.1111/j.1472-8206.2008.00633.x	journal	December 2008
Saccharomyces cerevisiae Mpt5p interacts with Sst2p and plays roles in pheromone sensitivity and recovery from pheromone arrest. Chen, T.; Kurjan, J. Molecular and Cellular Biology, Vol. 17, Issue 6 https://doi.org/10.1128/MCB.17.6.3429	journal	June 1997
An engineering viewpoint on biological robustness Khammash, Mustafa BMC Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12915-016-0241-x	journal	March 2016
Tellurium: An extensible python-based modeling environment for systems and synthetic biology Choi, Kiri; Medley, J. Kyle; König, Matthias Biosystems, Vol. 171 https://doi.org/10.1016/j.biosystems.2018.07.006	journal	September 2018
Ultrasensitivity in the mitogen-activated protein kinase cascade. Huang, C. Y.; Ferrell, J. E. Proceedings of the National Academy of Sciences, Vol. 93, Issue 19 https://doi.org/10.1073/pnas.93.19.10078	journal	September 1996
A Whole-Cell Computational Model Predicts Phenotype from Genotype Karr, Jonathan R.; Sanghvi, Jayodita C.; Macklin, Derek N. Cell, Vol. 150, Issue 2 https://doi.org/10.1016/j.cell.2012.05.044	journal	July 2012
Ubiquitin, proteasomes, and the regulation of intracellular protein degradation Hochstrasser, Mark Current Opinion in Cell Biology, Vol. 7, Issue 2 https://doi.org/10.1016/0955-0674(95)80031-X	journal	January 1995
Dna Degradation in Development and Programmed cell Death Nagata, Shigekazu Annual Review of Immunology, Vol. 23, Issue 1 https://doi.org/10.1146/annurev.immunol.23.021704.115811	journal	April 2005
Analysis of network motifs in cellular regulation: Structural similarities, input–output relations and signal integration Straube, Ronny Biosystems, Vol. 162 https://doi.org/10.1016/j.biosystems.2017.10.012	journal	December 2017
Metabolic cycles as an underlying basis of biological oscillations Tu, Benjamin P.; McKnight, Steven L. Nature Reviews Molecular Cell Biology, Vol. 7, Issue 9 https://doi.org/10.1038/nrm1980	journal	July 2006
Modulation of Hsf1 activity by novobiocin and geldanamycin Conde, Renaud; Belak, Zachery R.; Nair, Manoj Biochemistry and Cell Biology, Vol. 87, Issue 6 https://doi.org/10.1139/O09-049	journal	December 2009
Kinetic and Thermodynamic Aspects of Enzyme Control and Regulation Rohwer, Johann M.; Hofmeyr, Jan-Hendrik S. The Journal of Physical Chemistry B, Vol. 114, Issue 49 https://doi.org/10.1021/jp108412s	journal	October 2010
Graded mode of transcriptional induction in yeast pheromone signalling revealed by single‐cell analysis Poritz, Mark A.; Malmstrom, Sharon; Kim, Marianne K. ‐H. Yeast, Vol. 18, Issue 14 https://doi.org/10.1002/yea.777	journal	August 2001
From molecular to modular cell biology Hartwell, Leland H.; Hopfield, John J.; Leibler, Stanislas Nature, Vol. 402, Issue S6761 https://doi.org/10.1038/35011540	journal	December 1999
Yeast Dynamically Modify Their Environment to Achieve Better Mating Efficiency Jin, M.; Errede, B.; Behar, M. Science Signaling, Vol. 4, Issue 186 https://doi.org/10.1126/scisignal.2001763	journal	August 2011
Target of Rapamycin (TOR) in Nutrient Signaling and Growth Control Loewith, Robbie; Hall, Michael N. Genetics, Vol. 189, Issue 4 https://doi.org/10.1534/genetics.111.133363	journal	December 2011
Autocrine, paracrine and juxtacrine signaling by EGFR ligands Singh, Amar B.; Harris, Raymond C. Cellular Signalling, Vol. 17, Issue 10 https://doi.org/10.1016/j.cellsig.2005.03.026	journal	October 2005
Input–output robustness in simple bacterial signaling systems Shinar, Guy; Milo, Ron; Martínez, María Rodríguez Proceedings of the National Academy of Sciences, Vol. 104, Issue 50 https://doi.org/10.1073/pnas.0706792104	journal	December 2007
Control theory meets synthetic biology Del Vecchio, Domitilla; Dy, Aaron J.; Qian, Yili Journal of The Royal Society Interface, Vol. 13, Issue 120 https://doi.org/10.1098/rsif.2016.0380	journal	July 2016
Rapid and sustained nuclear–cytoplasmic ERK oscillations induced by epidermal growth factor Shankaran, Harish; Ippolito, Danielle L.; Chrisler, William B. Molecular Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1038/msb.2009.90	journal	January 2009
Negative autoregulation linearizes the dose-response and suppresses the heterogeneity of gene expression Nevozhay, D.; Adams, R. M.; Murphy, K. F. Proceedings of the National Academy of Sciences, Vol. 106, Issue 13 https://doi.org/10.1073/pnas.0809901106	journal	March 2009
The essential tension: opposed reactions in bacterial two-component regulatory systems Russo, Frank D.; Silhavy, Thomas J. Trends in Microbiology, Vol. 1, Issue 8 https://doi.org/10.1016/0966-842X(93)90007-E	journal	November 1993
Proteolytic ectodomain shedding of membrane proteins in mammals—hardware, concepts, and recent developments Lichtenthaler, Stefan F.; Lemberg, Marius K.; Fluhrer, Regina The EMBO Journal, Vol. 37, Issue 15 https://doi.org/10.15252/embj.201899456	journal	May 2018
Assembly Dynamics of the Bacterial MinCDE System and Spatial Regulation of the Z Ring Lutkenhaus, Joe Annual Review of Biochemistry, Vol. 76, Issue 1 https://doi.org/10.1146/annurev.biochem.75.103004.142652	journal	June 2007
Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell Tyson, John J.; Chen, Katherine C.; Novak, Bela Current Opinion in Cell Biology, Vol. 15, Issue 2 https://doi.org/10.1016/S0955-0674(03)00017-6	journal	April 2003
Effects of sequestration on signal transduction cascades Bluthgen, Nils; Bruggeman, Frank J.; Legewie, Stefan FEBS Journal, Vol. 273, Issue 5 https://doi.org/10.1111/j.1742-4658.2006.05105.x	journal	March 2006
The reversible Hill equation: how to incorporate cooperative enzymes into metabolic models Hofmeyr, Jan-Hendrik S.; Cornish-Bowden, Hofmeyr Bioinformatics, Vol. 13, Issue 4 https://doi.org/10.1093/bioinformatics/13.4.377	journal	January 1997
Size and composition of membrane protein clusters predicted by Monte Carlo analysis Goldman, Jacki; Andrews, Steven; Bray, Dennis European Biophysics Journal, Vol. 33, Issue 6 https://doi.org/10.1007/s00249-004-0391-6	journal	March 2004
Signaling pathways as linear transmitters Nunns, Harry; Goentoro, Lea eLife, Vol. 7 https://doi.org/10.7554/eLife.33617	journal	September 2018
Proteolytic Processing Mechanisms in the Biosynthesis of Neuroendocrine Peptides: The Subtilisin-like Proprotein Convertases Rouillé, Yves; Duguay, Stephen J.; Lund, Kaare Frontiers in Neuroendocrinology, Vol. 16, Issue 4 https://doi.org/10.1006/frne.1995.1012	journal	October 1995
Ribosome-associated chaperones as key players in proteostasis Preissler, Steffen; Deuerling, Elke Trends in Biochemical Sciences, Vol. 37, Issue 7 https://doi.org/10.1016/j.tibs.2012.03.002	journal	July 2012
Push-Pull and Feedback Mechanisms Can Align Signaling System Outputs with Inputs Andrews, Steven S.; Peria, William J.; Yu, Richard C. Cell Systems, Vol. 3, Issue 5 https://doi.org/10.1016/j.cels.2016.10.002	journal	November 2016
The Coherent Feedforward Loop Serves as a Sign-sensitive Delay Element in Transcription Networks Mangan, S.; Zaslaver, A.; Alon, U. Journal of Molecular Biology, Vol. 334, Issue 2 https://doi.org/10.1016/j.jmb.2003.09.049	journal	November 2003
Regulation of Cell Signaling Dynamics by the Protein Kinase-Scaffold Ste5 Hao, Nan; Nayak, Sujata; Behar, Marcelo Molecular Cell, Vol. 30, Issue 5 https://doi.org/10.1016/j.molcel.2008.04.016	journal	June 2008
Autophagy as a Regulated Pathway of Cellular Degradation Klionsky, D. J. Science, Vol. 290, Issue 5497 https://doi.org/10.1126/science.290.5497.1717	journal	December 2000
Bow ties, metabolism and disease Csete, Marie; Doyle, John Trends in Biotechnology, Vol. 22, Issue 9 https://doi.org/10.1016/j.tibtech.2004.07.007	journal	September 2004
Ultradian oscillations and pulses: coordinating cellular responses and cell fate decisions Isomura, Akihiro; Kageyama, Ryoichiro Development, Vol. 141, Issue 19 https://doi.org/10.1242/dev.104497	journal	October 2014
A quantitative characterization of the yeast heterotrimeric G protein cycle Yi, T. -M.; Kitano, H.; Simon, M. I. Proceedings of the National Academy of Sciences, Vol. 100, Issue 19 https://doi.org/10.1073/pnas.1834247100	journal	September 2003
The topological requirements for robust perfect adaptation in networks of any size Araujo, Robyn P.; Liotta, Lance A. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04151-6	journal	May 2018
Ratiometric GPCR signaling enables directional sensing in yeast Henderson, Nicholas T.; Pablo, Michael; Ghose, Debraj PLOS Biology, Vol. 17, Issue 10 https://doi.org/10.1371/journal.pbio.3000484	journal	October 2019
Functional Roles of Pulsing in Genetic Circuits Levine, J. H.; Lin, Y.; Elowitz, M. B. Science, Vol. 342, Issue 6163 https://doi.org/10.1126/science.1239999	journal	December 2013
Toward a detailed computational model for the mammalian circadian clock Leloup, J. -C.; Goldbeter, A. Proceedings of the National Academy of Sciences, Vol. 100, Issue 12 https://doi.org/10.1073/pnas.1132112100	journal	May 2003
Pattern, Growth, and Control Lander, Arthur D. Cell, Vol. 144, Issue 6 https://doi.org/10.1016/j.cell.2011.03.009	journal	March 2011
Superfamilies of Evolved and Designed Networks Milo, R. Science, Vol. 303, Issue 5663 https://doi.org/10.1126/science.1089167	journal	March 2004
Germline P Granules Are Liquid Droplets That Localize by Controlled Dissolution/Condensation Brangwynne, C. P.; Eckmann, C. R.; Courson, D. S. Science, Vol. 324, Issue 5935 https://doi.org/10.1126/science.1172046	journal	May 2009
Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome Mann, Matthias; Ong, Shao-En; Grønborg, Mads Trends in Biotechnology, Vol. 20, Issue 6 https://doi.org/10.1016/S0167-7799(02)01944-3	journal	June 2002
Pheromone Response in Yeast Kurjan, Janet Annual Review of Biochemistry, Vol. 61, Issue 1 https://doi.org/10.1146/annurev.bi.61.070192.005313	journal	June 1992
Modulation of receptor dynamics by the regulator of G protein signaling Sst2 Venkatapurapu, Sai Phanindra; Kelley, Joshua B.; Dixit, Gauri Molecular Biology of the Cell, Vol. 26, Issue 22 https://doi.org/10.1091/mbc.E14-12-1635	journal	November 2015
The Shc adaptor protein is highly phosphorylated at conserved, twin tyrosine residues (Y239/240) that mediate protein–protein interactions van der Geer, Peter; Wiley, Sandra; Gish, Gerald D. Current Biology, Vol. 6, Issue 11 https://doi.org/10.1016/S0960-9822(96)00748-8	journal	November 1996
A synthetic oscillatory network of transcriptional regulators Elowitz, Michael B.; Leibler, Stanislas Nature, Vol. 403, Issue 6767 https://doi.org/10.1038/35002125	journal	January 2000
Modelling the dynamics of the yeast pheromone pathway Kofahl, Bente; Klipp, Edda Yeast, Vol. 21, Issue 10 https://doi.org/10.1002/yea.1122	journal	July 2004
Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous- growth signalling pathway Cook, Jeanette Gowen; Bardwell, Lee; Thorner, Jeremy Nature, Vol. 390, Issue 6655 https://doi.org/10.1038/36355	journal	November 1997
Signaling Motifs and Weber's Law Ferrell, James E. Molecular Cell, Vol. 36, Issue 5 https://doi.org/10.1016/j.molcel.2009.11.032	journal	December 2009
Intracellular Signaling: Spatial and Temporal Control Moraru, Ion I.; Loew, Leslie M. Physiology, Vol. 20, Issue 3 https://doi.org/10.1152/physiol.00052.2004	journal	June 2005
Ultrasensitivity part III: cascades, bistable switches, and oscillators Ferrell, James E.; Ha, Sang Hoon Trends in Biochemical Sciences, Vol. 39, Issue 12 https://doi.org/10.1016/j.tibs.2014.10.002	journal	December 2014
Cellular Noise Suppression by the Regulator of G Protein Signaling Sst2 Dixit, Gauri; Kelley, Joshua B.; Houser, John R. Molecular Cell, Vol. 55, Issue 1 https://doi.org/10.1016/j.molcel.2014.05.019	journal	July 2014
Receptor clustering as a cellular mechanism to control sensitivity Bray, Dennis; Levin, Matthew D.; Morton-Firth, Carl J. Nature, Vol. 393, Issue 6680 https://doi.org/10.1038/30018	journal	May 1998
Predicting Chemical Environments of Bacteria from Receptor Signaling Clausznitzer, Diana; Micali, Gabriele; Neumann, Silke PLoS Computational Biology, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pcbi.1003870	journal	October 2014
Transferring information without distortion Andrews, Steven S.; Brent, Roger; Balázsi, Gábor eLife, Vol. 7 https://doi.org/10.7554/eLife.41894	journal	October 2018
Historical review: the field of protein methylation Paik, Woon Ki; Paik, David C.; Kim, Sangduk Trends in Biochemical Sciences, Vol. 32, Issue 3 https://doi.org/10.1016/j.tibs.2007.01.006	journal	March 2007
A bistable autoregulatory module in the developing embryo commits cells to binary expression fates Zhao, Jiaxi; Perkins, Mindy Liu; Norstad, Matthew Current Biology, Vol. 33, Issue 14 https://doi.org/10.1016/j.cub.2023.06.060	journal	July 2023
Is Protein Folding a Thermodynamically Unfavorable, Active, Energy-Dependent Process? Sorokina, Irina; Mushegian, Arcady R.; Koonin, Eugene V. International Journal of Molecular Sciences, Vol. 23, Issue 1 https://doi.org/10.3390/ijms23010521	journal	January 2022
Construction of a genetic toggle switch in Escherichia coli Gardner, Timothy S.; Cantor, Charles R.; Collins, James J. Nature, Vol. 403, Issue 6767 https://doi.org/10.1038/35002131	journal	January 2000
Reverse Engineering of Biological Complexity Csete, M. E. Science, Vol. 295, Issue 5560 https://doi.org/10.1126/science.1069981	journal	March 2002
Covalent modification and metabolic control analysis Small, J. Rankin; Fell, David A. European Journal of Biochemistry, Vol. 191, Issue 2 https://doi.org/10.1111/j.1432-1033.1990.tb19136.x	journal	July 1990
Integrating fluctuating nitrate uptake and assimilation to robust homeostasis Huang, Yongshun; Drengstig, Tormod; Ruoff, Peter Plant, Cell & Environment, Vol. 35, Issue 5 https://doi.org/10.1111/j.1365-3040.2011.02462.x	journal	December 2011
Rapid Microtubule Self-Assembly Kinetics Gardner, Melissa K.; Charlebois, Blake D.; Jánosi, Imre M. Cell, Vol. 146, Issue 4 https://doi.org/10.1016/j.cell.2011.06.053	journal	August 2011
Control and regulation of pathways via negative feedback Sauro, Herbert M. Journal of The Royal Society Interface, Vol. 14, Issue 127 https://doi.org/10.1098/rsif.2016.0848	journal	February 2017
Regulation by proteolysis in bacterial cells Jenal, Urs; Hengge-Aronis, Regine Current Opinion in Microbiology, Vol. 6, Issue 2 https://doi.org/10.1016/S1369-5274(03)00029-8	journal	April 2003
The Biology of Chromatin Remodeling Complexes Clapier, Cedric R.; Cairns, Bradley R. Annual Review of Biochemistry, Vol. 78, Issue 1 https://doi.org/10.1146/annurev.biochem.77.062706.153223	journal	June 2009
Pheromone Signaling Mechanisms in Yeast: A Prototypical Sex Machine Wang, Y. Science, Vol. 306, Issue 5701 https://doi.org/10.1126/science.1104568	journal	November 2004
Spatial organization of intracellular communication: insights from imaging Dehmelt, Leif; Bastiaens, Philippe I. H. Nature Reviews Molecular Cell Biology, Vol. 11, Issue 6 https://doi.org/10.1038/nrm2903	journal	May 2010
Membrane Organization and Lipid Rafts Simons, K.; Sampaio, J. L. Cold Spring Harbor Perspectives in Biology, Vol. 3, Issue 10 https://doi.org/10.1101/cshperspect.a004697	journal	May 2011
The Biochemical Basis of an All-or-None Cell Fate Switch in Xenopus Oocytes Ferrell Jr., J. E. Science, Vol. 280, Issue 5365 https://doi.org/10.1126/science.280.5365.895	journal	May 1998
Can a biologist fix a radio?—Or, what I learned while studying apoptosis Lazebnik, Yuri Cancer Cell, Vol. 2, Issue 3 https://doi.org/10.1016/S1535-6108(02)00133-2	journal	September 2002
Modelling and analysis of gene regulatory networks Karlebach, Guy; Shamir, Ron Nature Reviews Molecular Cell Biology, Vol. 9, Issue 10 https://doi.org/10.1038/nrm2503	journal	September 2008
Protein Dimerization Generates Bistability in Positive Feedback Loops Hsu, Chieh; Jaquet, Vincent; Gencoglu, Mumun Cell Reports, Vol. 16, Issue 5 https://doi.org/10.1016/j.celrep.2016.06.072	journal	August 2016
The Utility of Paradoxical Components in Biological Circuits Hart, Yuval; Alon, Uri Molecular Cell, Vol. 49, Issue 2 https://doi.org/10.1016/j.molcel.2013.01.004	journal	January 2013
Ultrasensitivity part I: Michaelian responses and zero-order ultrasensitivity Ferrell, James E.; Ha, Sang Hoon Trends in Biochemical Sciences, Vol. 39, Issue 10 https://doi.org/10.1016/j.tibs.2014.08.003	journal	October 2014
Metabolic channeling: predictions, deductions, and evidence Pareek, Vidhi; Sha, Zhou; He, Jingxuan Molecular Cell, Vol. 81, Issue 18 https://doi.org/10.1016/j.molcel.2021.08.030	journal	September 2021
Fold Change of Nuclear NF-κB Determines TNF-Induced Transcription in Single Cells Lee, Robin E. C.; Walker, Sarah R.; Savery, Kate Molecular Cell, Vol. 53, Issue 6 https://doi.org/10.1016/j.molcel.2014.01.026	journal	March 2014
Regulating the cellular economy of supply and demand Hofmeyr, Jan-Hendrik S.; Cornish-Bowden, Athel FEBS Letters, Vol. 476, Issue 1-2 https://doi.org/10.1016/S0014-5793(00)01668-9	journal	June 2000
Robust perfect adaptation in bacterial chemotaxis through integral feedback control Yi, T. -M.; Huang, Y.; Simon, M. I. Proceedings of the National Academy of Sciences, Vol. 97, Issue 9 https://doi.org/10.1073/pnas.97.9.4649	journal	April 2000
Notch signaling: control of cell communication and cell fate Lai, E. C. Development, Vol. 131, Issue 5 https://doi.org/10.1242/dev.01074	journal	March 2004
An amplified sensitivity arising from covalent modification in biological systems. Goldbeter, A.; Koshland, D. E. Proceedings of the National Academy of Sciences, Vol. 78, Issue 11 https://doi.org/10.1073/pnas.78.11.6840	journal	November 1981
Role of proteolytic enzymes in biological regulation (a review). Neurath, H.; Walsh, K. A. Proceedings of the National Academy of Sciences, Vol. 73, Issue 11 https://doi.org/10.1073/pnas.73.11.3825	journal	November 1976
Bacterial chemotaxis Webre, Daniel J.; Wolanin, Peter M.; Stock, Jeffry B. Current Biology, Vol. 13, Issue 2 https://doi.org/10.1016/S0960-9822(02)01424-0	journal	January 2003
Oscillatory dynamics arising from competitive inhibition and multisite phosphorylation Chickarmane, Vijay; Kholodenko, Boris N.; Sauro, Herbert M. Journal of Theoretical Biology, Vol. 244, Issue 1 https://doi.org/10.1016/j.jtbi.2006.05.013	journal	January 2007
A Complete Pathway Model for Lipid A Biosynthesis in Escherichia coli Emiola, Akintunde; George, John; Andrews, Steven S. PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0121216	journal	April 2015
GAPDH is involved in the heme‐maturation of myoglobin and hemoglobin Tupta, Blair; Stuehr, Eric; Sumi, Mamta P. The FASEB Journal, Vol. 36, Issue 2 https://doi.org/10.1096/fj.202101237RR	journal	December 2021
Regulation by proteolysis: Developmental switches Gottesman, Susan Current Opinion in Microbiology, Vol. 2, Issue 2 https://doi.org/10.1016/S1369-5274(99)80025-3	journal	April 1999
Stochastic Gene Expression in a Single Cell Elowitz, M. B. Science, Vol. 297, Issue 5584 https://doi.org/10.1126/science.1070919	journal	August 2002
Ultrasensitivity part II: multisite phosphorylation, stoichiometric inhibitors, and positive feedback Ferrell, James E.; Ha, Sang Hoon Trends in Biochemical Sciences, Vol. 39, Issue 11 https://doi.org/10.1016/j.tibs.2014.09.003	journal	November 2014
Multisite and hierarchal protein phosphorylation Roach, P. J. Journal of Biological Chemistry, Vol. 266, Issue 22 https://doi.org/10.1016/S0021-9258(18)98653-9	journal	August 1991
Evidence that Fold-Change, and Not Absolute Level, of β-Catenin Dictates Wnt Signaling Goentoro, Lea; Kirschner, Marc W. Molecular Cell, Vol. 36, Issue 5 https://doi.org/10.1016/j.molcel.2009.11.017	journal	December 2009
The Incoherent Feedforward Loop Can Provide Fold-Change Detection in Gene Regulation Goentoro, Lea; Shoval, Oren; Kirschner, Marc W. Molecular Cell, Vol. 36, Issue 5 https://doi.org/10.1016/j.molcel.2009.11.018	journal	December 2009
Metabolic control and its analysis. Additional relationships between elasticities and control coefficients Fell, David A.; Sauro, Herbert M. European Journal of Biochemistry, Vol. 148, Issue 3 https://doi.org/10.1111/j.1432-1033.1985.tb08876.x	journal	May 1985
BioModels Database: a free, centralized database of curated, published, quantitative kinetic models of biochemical and cellular systems Le Novere, N. Nucleic Acids Research, Vol. 34, Issue 90001 https://doi.org/10.1093/nar/gkj092	journal	January 2006
An N-stage cascade of phosphorylation cycles as an insulation device for synthetic biological circuits Shah, Rushina; Del Vecchio, Domitilla 2016 European Control Conference (ECC) https://doi.org/10.1109/ECC.2016.7810557	conference	June 2016
Signalling scaffolds and local organization of cellular behaviour Langeberg, Lorene K.; Scott, John D. Nature Reviews Molecular Cell Biology, Vol. 16, Issue 4 https://doi.org/10.1038/nrm3966	journal	March 2015
Control, exploitation and tolerance of intracellular noise Rao, Christopher V.; Wolf, Denise M.; Arkin, Adam P. Nature, Vol. 420, Issue 6912 https://doi.org/10.1038/nature01258	journal	November 2002
Noise in biology Tsimring, Lev S. Reports on Progress in Physics, Vol. 77, Issue 2 https://doi.org/10.1088/0034-4885/77/2/026601	journal	January 2014
Integral Rein Control in Physiology Saunders, Peter T.; Koeslag, Johan H.; Wessels, Jabus A. Journal of Theoretical Biology, Vol. 194, Issue 2 https://doi.org/10.1006/jtbi.1998.0746	journal	September 1998
Information transfer in metabolic pathways Cornish‐Bowden, Athel; Cárdenas, María Luz European Journal of Biochemistry, Vol. 268, Issue 24 https://doi.org/10.1046/j.0014-2956.2001.02616.x	journal	December 2001
The Pattern of Streets Alexander, Christopher Journal of the American Institute of Planners, Vol. 32, Issue 5 https://doi.org/10.1080/01944366608978208	journal	September 1966
Defining Network Topologies that Can Achieve Biochemical Adaptation Ma, Wenzhe; Trusina, Ala; El-Samad, Hana Cell, Vol. 138, Issue 4 https://doi.org/10.1016/j.cell.2009.06.013	journal	August 2009
Kinetic Proofreading Boeger, Hinrich Annual Review of Biochemistry, Vol. 91, Issue 1 https://doi.org/10.1146/annurev-biochem-040320-103630	journal	June 2022
DNA Methylation and Its Basic Function Moore, Lisa D.; Le, Thuc; Fan, Guoping Neuropsychopharmacology, Vol. 38, Issue 1 https://doi.org/10.1038/npp.2012.112	journal	July 2012
Ultrasensitive response motifs: basic amplifiers in molecular signalling networks Zhang, Qiang; Bhattacharya, Sudin; Andersen, Melvin E. Open Biology, Vol. 3, Issue 4 https://doi.org/10.1098/rsob.130031	journal	April 2013
Direct observation of the enhancement of noncooperative protein self-assembly by macromolecular crowding: Indefinite linear self-association of bacterial cell division protein FtsZ Rivas, G.; Fernandez, J. A.; Minton, A. P. Proceedings of the National Academy of Sciences, Vol. 98, Issue 6 https://doi.org/10.1073/pnas.051634398	journal	March 2001
An Overview of Autophagy and Yeast Pseudohyphal Growth: Integration of Signaling Pathways during Nitrogen Stress Song, Qingxuan; Kumar, Anuj Cells, Vol. 1, Issue 3 https://doi.org/10.3390/cells1030263	journal	July 2012
Dynamics and Variability of ERK2 Response to EGF in Individual Living Cells Cohen-Saidon, Cellina; Cohen, Ariel A.; Sigal, Alex Molecular Cell, Vol. 36, Issue 5 https://doi.org/10.1016/j.molcel.2009.11.025	journal	December 2009
ExsB, an unusually highly phosphorylated protein required for the stable attachment of the exosporium of Bacillus anthracis: Phospho-ExsB required for B. anthracis exosporium attachment McPherson, Sylvia A.; Li, Mei; Kearney, John F. Molecular Microbiology, Vol. 76, Issue 6 https://doi.org/10.1111/j.1365-2958.2010.07182.x	journal	April 2010
Noise in protein expression scales with natural protein abundance Bar-Even, Arren; Paulsson, Johan; Maheshri, Narendra Nature Genetics, Vol. 38, Issue 6 https://doi.org/10.1038/ng1807	journal	May 2006
Appreciation of the Machinations of the Blind Watchmaker Arkin, Adam; Doyle, John IEEE Transactions on Automatic Control, Vol. 53, Issue Special Issue https://doi.org/10.1109/TAC.2007.913342	journal	January 2008
Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein phosphorylation. Goldbeter, A.; Dupont, G.; Berridge, M. J. Proceedings of the National Academy of Sciences, Vol. 87, Issue 4 https://doi.org/10.1073/pnas.87.4.1461	journal	February 1990
Molecular Mechanisms Controlling Actin Filament Dynamics in Nonmuscle Cells Pollard, Thomas D.; Blanchoin, Laurent; Mullins, R. Dyche Annual Review of Biophysics and Biomolecular Structure, Vol. 29, Issue 1 https://doi.org/10.1146/annurev.biophys.29.1.545	journal	June 2000
Design of insulating devices for in vitro synthetic circuits Franco, Elisa; Del Vecchio, Domitilla; Murray, Richard M. 2009 Joint 48th IEEE Conference on Decision and Control (CDC) and 28th Chinese Control Conference (CCC), Proceedings of the 48h IEEE Conference on Decision and Control (CDC) held jointly with 2009 28th Chinese Control Conference https://doi.org/10.1109/CDC.2009.5400523	conference	December 2009
Highly phosphorylated bacterial proteins Rosen, Ran; Becher, Dörte; Büttner, Knut PROTEOMICS, Vol. 4, Issue 10 https://doi.org/10.1002/pmic.200400890	journal	October 2004
Ion homeostasis, channels, and transporters: an update on cellular mechanisms Dubyak, George R. Advances in Physiology Education, Vol. 28, Issue 4 https://doi.org/10.1152/advan.00046.2004	journal	December 2004
Conformational Changes in Protein Loops and Helices Induced by Post-Translational Phosphorylation Groban, Eli S.; Narayanan, Arjun; Jacobson, Matthew P. PLoS Computational Biology, Vol. 2, Issue 4 https://doi.org/10.1371/journal.pcbi.0020032	journal	January 2006
Modeling the cell division cycle: cdc2 and cyclin interactions. Tyson, J. J. Proceedings of the National Academy of Sciences, Vol. 88, Issue 16 https://doi.org/10.1073/pnas.88.16.7328	journal	August 1991
Fold-change detection and scalar symmetry of sensory input fields Shoval, Oren; Goentoro, Lea; Hart, Yuval Proceedings of the National Academy of Sciences, Vol. 107, Issue 36 https://doi.org/10.1073/pnas.1002352107	journal	August 2010
Bistability by multiple phosphorylation of regulatory proteins Kapuy, Orsolya; Barik, Debashis; Domingo Sananes, Maria Rosa Progress in Biophysics and Molecular Biology, Vol. 100, Issue 1-3 https://doi.org/10.1016/j.pbiomolbio.2009.06.004	journal	September 2009
Modular cell biology: retroactivity and insulation Del Vecchio, Domitilla; Ninfa, Alexander J.; Sontag, Eduardo D. Molecular Systems Biology, Vol. 4, Issue 1 https://doi.org/10.1038/msb4100204	journal	January 2008
Network Motifs: Simple Building Blocks of Complex Networks Milo, R. Science, Vol. 298, Issue 5594 https://doi.org/10.1126/science.298.5594.824	journal	October 2002
Topology and Robustness in the Drosophila Segment Polarity Network Ingolia, Nicholas T. PLoS Biology, Vol. 2, Issue 6 https://doi.org/10.1371/journal.pbio.0020123	journal	June 2004
Principles that Govern the Folding of Protein Chains Anfinsen, C. B. Science, Vol. 181, Issue 4096 https://doi.org/10.1126/science.181.4096.223	journal	July 1973
Membrane curvature and mechanisms of dynamic cell membrane remodelling McMahon, Harvey T.; Gallop, Jennifer L. Nature, Vol. 438, Issue 7068 https://doi.org/10.1038/nature04396	journal	November 2005
Circuit simulation of genetic networks McAdams, H.; Shapiro, L. Science, Vol. 269, Issue 5224 https://doi.org/10.1126/science.7624793	journal	August 1995
Two Regulators of Ste12p Inhibit Pheromone-Responsive Transcription by Separate Mechanisms Olson, K. Amy; Nelson, Chris; Tai, Georgia Molecular and Cellular Biology, Vol. 20, Issue 12 https://doi.org/10.1128/MCB.20.12.4199-4209.2000	journal	June 2000
Quantitative analysis of signaling networks Sauro, Herbert M.; Kholodenko, Boris N. Progress in Biophysics and Molecular Biology, Vol. 86, Issue 1 https://doi.org/10.1016/j.pbiomolbio.2004.03.002	journal	September 2004
Antithetic Integral Feedback Ensures Robust Perfect Adaptation in Noisy Biomolecular Networks Briat, Corentin; Gupta, Ankit; Khammash, Mustafa Cell Systems, Vol. 2, Issue 1 https://doi.org/10.1016/j.cels.2016.01.004	journal	January 2016
A walk-through of the yeast mating pheromone response pathway Bardwell, Lee Peptides, Vol. 26, Issue 2 https://doi.org/10.1016/j.peptides.2004.10.002	journal	February 2005
Signaling properties of a covalent modification cycle are altered by a downstream target Ventura, Alejandra C.; Jiang, Peng; Van Wassenhove, Lauren Proceedings of the National Academy of Sciences, Vol. 107, Issue 22 https://doi.org/10.1073/pnas.0913815107	journal	May 2010
COMBINE archive and OMEX format: one file to share all information to reproduce a modeling project Bergmann, Frank T.; Adams, Richard; Moodie, Stuart BMC Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1186/s12859-014-0369-z	journal	December 2014
The power of two: protein dimerization in biology Marianayagam, Neelan J.; Sunde, Margaret; Matthews, Jacqueline M. Trends in Biochemical Sciences, Vol. 29, Issue 11 https://doi.org/10.1016/j.tibs.2004.09.006	journal	November 2004
Minimal Escherichia coli Cell for the Most Efficient Production of Ethanol from Hexoses and Pentoses Trinh, C. T.; Unrean, P.; Srienc, F. Applied and Environmental Microbiology, Vol. 74, Issue 12, p. 3634-3643 https://doi.org/10.1128/AEM.02708-07	journal	April 2008
Systems Biology: A Switch for Sex Andrews, Steven S.; Arkin, Adam P. Current Biology, Vol. 17, Issue 11 https://doi.org/10.1016/j.cub.2007.03.060	journal	June 2007
The evolutionary origins of modularity Clune, Jeff; Mouret, Jean-Baptiste; Lipson, Hod Proceedings of the Royal Society B: Biological Sciences, Vol. 280, Issue 1755 https://doi.org/10.1098/rspb.2012.2863	journal	March 2013
The Nuclear Pore Complex and Nuclear Transport Wente, S. R.; Rout, M. P. Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 10 https://doi.org/10.1101/cshperspect.a000562	journal	July 2010
The simulation experiment description markup language (SED-ML): language specification for level 1 version 4 Smith, Lucian P.; Bergmann, Frank T.; Garny, Alan Journal of Integrative Bioinformatics, Vol. 18, Issue 3 https://doi.org/10.1515/jib-2021-0021	journal	October 2021
Design Principles of Regulatory Networks: Searching for the Molecular Algorithms of the Cell Lim, Wendell A.; Lee, Connie M.; Tang, Chao Molecular Cell, Vol. 49, Issue 2 https://doi.org/10.1016/j.molcel.2012.12.020	journal	January 2013
An Integrated Model of Transcription Factor Diffusion Shows the Importance of Intersegmental Transfer and Quaternary Protein Structure for Target Site Finding Schmidt, Hugo G.; Sewitz, Sven; Andrews, Steven S. PLoS ONE, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pone.0108575	journal	October 2014
A Fluorescent α-Factor Analogue Exhibits Multiple Steps on Binding to Its G Protein Coupled Receptor in Yeast Bajaj, Anshika; Ćelić, Andjelka; Ding, Fa-Xiang Biochemistry, Vol. 43, Issue 42 https://doi.org/10.1021/bi0494018	journal	September 2004
Understanding complex signaling networks through models and metaphors Bhalla, Upinder S. Progress in Biophysics and Molecular Biology, Vol. 81, Issue 1 https://doi.org/10.1016/S0079-6107(02)00046-9	journal	January 2003
Understanding the regulation of aspartate metabolism using a model based on measured kinetic parameters Curien, Gilles; Bastien, Olivier; Robert‐Genthon, Mylène Molecular Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1038/msb.2009.29	journal	January 2009
The midnolin-proteasome pathway catches proteins for ubiquitination-independent degradation Gu, Xin; Nardone, Christopher; Kamitaki, Nolan Science, Vol. 381, Issue 6660 https://doi.org/10.1126/science.adh5021	journal	August 2023
Realizing ‘integral control’ in living cells: how to overcome leaky integration due to dilution? Qian, Yili; Del Vecchio, Domitilla Journal of The Royal Society Interface, Vol. 15, Issue 139 https://doi.org/10.1098/rsif.2017.0902	journal	February 2018
Design principles of biochemical oscillators Novák, Béla; Tyson, John J. Nature Reviews Molecular Cell Biology, Vol. 9, Issue 12 https://doi.org/10.1038/nrm2530	journal	October 2008
A Hidden Feedback in Signaling Cascades Is Revealed Ventura, Alejandra C.; Sepulchre, Jacques-A.; Merajver, Sofía D. PLoS Computational Biology, Vol. 4, Issue 3 https://doi.org/10.1371/journal.pcbi.1000041	journal	March 2008
Tuning the ribosome: The influence of rRNA modification on eukaryotic ribosome biogenesis and function Sloan, Katherine E.; Warda, Ahmed S.; Sharma, Sunny RNA Biology, Vol. 14, Issue 9 https://doi.org/10.1080/15476286.2016.1259781	journal	December 2016
Negative feedback that improves information transmission in yeast signalling Yu, Richard C.; Pesce, C. Gustavo; Colman-Lerner, Alejandro Nature, Vol. 456, Issue 7223 https://doi.org/10.1038/nature07513	journal	December 2008
Machines vs. Ensembles: Effective MAPK Signaling through Heterogeneous Sets of Protein Complexes Suderman, Ryan; Deeds, Eric J. PLoS Computational Biology, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pcbi.1003278	journal	October 2013
Modeling oscillations and waves of cAMP in Dictyostelium discoideum cells Halloy, José; Lauzeral, Jacques; Goldbeter, Albert Biophysical Chemistry, Vol. 72, Issue 1-2 https://doi.org/10.1016/S0301-4622(98)00119-7	journal	May 1998
Sst2, a Negative Regulator of Pheromone Signaling in the Yeast Saccharomyces cerevisiae: Expression, Localization, and Genetic Interaction and Physical Association with Gpa1 (the G-Protein α Subunit) Dohlman, Henrik G.; Song, Jianping; Ma, Doreen Molecular and Cellular Biology, Vol. 16, Issue 9 https://doi.org/10.1128/MCB.16.9.5194	journal	September 1996
Modularity defined Sauro, Herbert M. Molecular Systems Biology, Vol. 4, Issue 1 https://doi.org/10.1038/msb.2008.3	journal	January 2008
Conservation of protein abundance patterns reveals the regulatory architecture of the EGFR-MAPK pathway Shi, Tujin; Niepel, Mario; McDermott, Jason E. Science Signaling, Vol. 9, Issue 436 https://doi.org/10.1126/scisignal.aaf0891	journal	July 2016
A Systems-Level Analysis of Perfect Adaptation in Yeast Osmoregulation Muzzey, Dale; Gómez-Uribe, Carlos A.; Mettetal, Jerome T. Cell, Vol. 138, Issue 1 https://doi.org/10.1016/j.cell.2009.04.047	journal	July 2009
Comparing Apples and Oranges: Fold-Change Detection of Multiple Simultaneous Inputs Hart, Yuval; Mayo, Avraham E.; Shoval, Oren PLoS ONE, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pone.0057455	journal	March 2013
Protein sequestration generates a flexible ultrasensitive response in a genetic network Buchler, Nicolas E.; Cross, Frederick R. Molecular Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1038/msb.2009.30	journal	January 2009
Modeling the chemotactic response of Escherichia coli to time-varying stimuli Tu, Yuhai; Shimizu, Thomas S.; Berg, Howard C. Proceedings of the National Academy of Sciences, Vol. 105, Issue 39 https://doi.org/10.1073/pnas.0807569105	journal	September 2008
Binding of α-Factor Pheromone to Saccharomyces cerevisiae a Cells: Dissociation Constant and Number of Binding Sites Jenness, Duane D.; Burkholder, Anne C.; Hartwell, Leland H. Molecular and Cellular Biology, Vol. 6, Issue 1 https://doi.org/10.1128/mcb.6.1.318-320.1986	journal	January 1986
Kinetic Proofreading: A New Mechanism for Reducing Errors in Biosynthetic Processes Requiring High Specificity Hopfield, J. J. Proceedings of the National Academy of Sciences, Vol. 71, Issue 10 https://doi.org/10.1073/pnas.71.10.4135	journal	October 1974
Protein Clusters in Phosphotyrosine Signal Transduction Mayer, Bruce J.; Yu, Ji Journal of Molecular Biology, Vol. 430, Issue 22 https://doi.org/10.1016/j.jmb.2018.05.040	journal	October 2018
Receptor sensitivity in bacterial chemotaxis Sourjik, V.; Berg, H. C. Proceedings of the National Academy of Sciences, Vol. 99, Issue 1 https://doi.org/10.1073/pnas.011589998	journal	December 2001
Considerations for using integral feedback control to construct a perfectly adapting synthetic gene network Ang, Jordan; Bagh, Sangram; Ingalls, Brian P. Journal of Theoretical Biology, Vol. 266, Issue 4 https://doi.org/10.1016/j.jtbi.2010.07.034	journal	October 2010
Stochastic Kinetic Analysis of Developmental Pathway Bifurcation in Phage λ-Infected Escherichia coli Cells Arkin, Adam; Ross, John; McAdams, Harley H. Genetics, Vol. 149, Issue 4 https://doi.org/10.1093/genetics/149.4.1633	journal	August 1998
Perfect adaptation in biology Khammash, Mustafa H. Cell Systems, Vol. 12, Issue 6 https://doi.org/10.1016/j.cels.2021.05.020	journal	June 2021
Oscillations in NF- B Signaling Control the Dynamics of Gene Expression Nelson, D. E. Science, Vol. 306, Issue 5696 https://doi.org/10.1126/science.1099962	journal	October 2004
Purification and characterization of the S-adenosylmethionine:glutamyl methyltransferase that modifies membrane chemoreceptor proteins in bacteria. Simms, S. A.; Stock, A. M.; Stock, J. B. Journal of Biological Chemistry, Vol. 262, Issue 18 https://doi.org/10.1016/S0021-9258(18)47447-9	journal	June 1987
Functional cartography of complex metabolic networks Guimerà, Roger; Nunes Amaral, Luís A. Nature, Vol. 433, Issue 7028 https://doi.org/10.1038/nature03288	journal	February 2005
The midnolin-proteasome pathway catches proteins for ubiquitination-independent degradation Gu, Xin; Nardone, Christopher; Kamitaki, Nolan Dryad https://doi.org/10.5061/dryad.m905qfv6g	dataset	January 2023

Similar Records

Resilience Design Patterns: A Structured Approach to Resilience at Extreme Scale (V.2.0)

Technical Report · Fri Dec 16 00:00:00 EST 2022 · OSTI ID:1922296

Engelmann, Christian; Ashraf, Rizwan; Hukerikar, Saurabh; +2 more

Resilience Design Patterns - A Structured Approach to Resilience at Extreme Scale (version 1.2)

Technical Report · Tue Aug 01 00:00:00 EDT 2017 · OSTI ID:1436045

Hukerikar, Saurabh; Engelmann, Christian

"After the Genome 5, Conference to be held October 6-10, 1999, Jackson Hole, Wyoming"

Conference · Wed Oct 06 00:00:00 EDT 1999 · OSTI ID:803995

Brent, Roger

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
design principles
reaction network
cell biology
cell signaling
cell biology modeling
metabolism
systems biology

Design patterns of biological cells

Citation Formats

References (180)

Similar Records

Related Subjects