History of protein–protein interactions: From egg‐white to complex networks

Today, it is widely appreciated that protein–protein interactions play a fundamental role in biological processes. This was not always the case. The study of protein interactions started slowly and evolved considerably, together with conceptual and technological progress in different areas of research through the late 19th and the 20th centuries. In this review, we present some of the key experiments that have introduced major conceptual advances in biochemistry and molecular biology, and review technological breakthroughs that have paved the way for today's systems‐wide approaches to protein–protein interaction analysis.

[1]  P. Braun Interactome mapping for analysis of complex phenotypes: Insights from benchmarking binary interaction assays , 2012, Proteomics.

[2]  Yves Pommier,et al.  Interfacial inhibitors: targeting macromolecular complexes , 2012, Nature Reviews Drug Discovery.

[3]  A. Barabasi,et al.  The network takeover , 2011, Nature Physics.

[4]  Caroline C Friedel,et al.  Virus-host interactomes and global models of virus-infected cells. , 2011, Trends in microbiology.

[5]  Jian Wang,et al.  Insight into Bacterial Virulence Mechanisms against Host Immune Response via the Yersinia pestis-Human Protein-Protein Interaction Network , 2011, Infection and Immunity.

[6]  Y. J. Kim,et al.  A Network-Based Approach to Prioritize Results from Genome-Wide Association Studies , 2011, PloS one.

[7]  Jonathan D. G. Jones,et al.  Evidence for Network Evolution in an Arabidopsis Interactome Map , 2011, Science.

[8]  M. S. Mukhtar,et al.  Independently Evolved Virulence Effectors Converge onto Hubs in a Plant Immune System Network , 2011, Science.

[9]  Igor Stagljar,et al.  Using yeast as a model to study membrane proteins , 2011, Current opinion in nephrology and hypertension.

[10]  K. Colwill,et al.  A roadmap to generate renewable protein binders to the human proteome , 2011, Nature Methods.

[11]  Thomas M Green,et al.  A public genome-scale lentiviral expression library of human ORFs , 2011, Nature Methods.

[12]  D. Chan,et al.  Analysis of the Human Endogenous Coregulator Complexome , 2011, Cell.

[13]  A. Barabasi,et al.  Interactome Networks and Human Disease , 2011, Cell.

[14]  P. Aloy,et al.  Interactome mapping suggests new mechanistic details underlying Alzheimer's disease. , 2011, Genome research.

[15]  Mathieu Blanchette,et al.  Modeling contaminants in AP-MS/MS experiments. , 2011, Journal of proteome research.

[16]  Gary D. Bader,et al.  Protein Complexes are Central in the Yeast Genetic Landscape , 2011, PLoS Comput. Biol..

[17]  M. Daly,et al.  Proteins Encoded in Genomic Regions Associated with Immune-Mediated Disease Physically Interact and Suggest Underlying Biology , 2011, PLoS genetics.

[18]  Hyungwon Choi,et al.  SAINT: Probabilistic Scoring of Affinity Purification - Mass Spectrometry Data , 2010, Nature Methods.

[19]  S. Celniker,et al.  Development of expression-ready constructs for generation of proteomic libraries. , 2011, Methods in molecular biology.

[20]  Vincent Lotteau,et al.  When the human viral infectome and diseasome networks collide: towards a systems biology platform for the aetiology of human diseases , 2011, BMC Systems Biology.

[21]  Nicolas Thierry-Mieg,et al.  New insights into protein-protein interaction data lead to increased estimates of the S. cerevisiae interactome size , 2010, BMC Bioinformatics.

[22]  M. Matsuoka,et al.  A Rice gid1 Suppressor Mutant Reveals That Gibberellin Is Not Always Required for Interaction between Its Receptor, GID1, and DELLA Proteins[W][OA] , 2010, Plant Cell.

[23]  T. Ideker,et al.  A decade of systems biology. , 2010, Annual review of cell and developmental biology.

[24]  Jan Tavernier,et al.  Large-scale protein interactome mapping: strategies and opportunities , 2010, Expert review of proteomics.

[25]  D. Altshuler,et al.  A map of human genome variation from population-scale sequencing , 2010, Nature.

[26]  Peter Uetz,et al.  Exhaustive benchmarking of the yeast two-hybrid system , 2010, Nature Methods.

[27]  Guillaume Pilot,et al.  A Membrane Protein/Signaling Protein Interaction Network for Arabidopsis Version AMPv2 , 2010, Front. Physio..

[28]  Zhaohui S. Qin,et al.  A Global Protein Kinase and Phosphatase Interaction Network in Yeast , 2010, Science.

[29]  A. Hyman,et al.  Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions , 2010, The Journal of cell biology.

[30]  E. Fischer Phosphorylase and the origin of reversible protein phosphorylation , 2010, Biological chemistry.

[31]  Gary D Bader,et al.  The Genetic Landscape of a Cell , 2010, Science.

[32]  J. Changeux Allosteric receptors: from electric organ to cognition. , 2010, Annual review of pharmacology and toxicology.

[33]  Daniel A. Fletcher,et al.  Cell mechanics and the cytoskeleton , 2010, Nature.

[34]  J. Schlessinger,et al.  Cell Signaling by Receptor Tyrosine Kinases , 2000, Cell.

[35]  Susan S. Taylor,et al.  cAMP-Dependent Protein Kinase , 2010 .

[36]  C. Landry,et al.  A toolkit of protein-fragment complementation assays for studying and dissecting large-scale and dynamic protein-protein interactions in living cells. , 2010, Methods in enzymology.

[37]  A. Barabasi,et al.  Network medicine : a network-based approach to human disease , 2010 .

[38]  Richard M. Karp,et al.  Genome-Wide Association Data Reveal a Global Map of Genetic Interactions among Protein Complexes , 2009, PLoS genetics.

[39]  M. Vidal,et al.  Edgetic perturbation models of human inherited disorders , 2009, Molecular systems biology.

[40]  M. Vidal,et al.  Edgetic perturbation of a C. elegans BCL2 ortholog , 2009, Nature Methods.

[41]  S. Gygi,et al.  Defining the Human Deubiquitinating Enzyme Interaction Landscape , 2009, Cell.

[42]  P. Aloy,et al.  A network medicine approach to human disease , 2009, FEBS letters.

[43]  David Warde-Farley,et al.  Dynamic modularity in protein interaction networks predicts breast cancer outcome , 2009, Nature Biotechnology.

[44]  Julie M. Sahalie,et al.  An experimentally derived confidence score for binary protein-protein interactions , 2008, Nature Methods.

[45]  A. Barabasi,et al.  An empirical framework for binary interactome mapping , 2008, Nature Methods.

[46]  Christian von Mering,et al.  STRING 8—a global view on proteins and their functional interactions in 630 organisms , 2008, Nucleic Acids Res..

[47]  K. Gunsalus,et al.  Empirically controlled mapping of the Caenorhabditis elegans protein-protein interactome network , 2009, Nature Methods.

[48]  Janice M Reichert,et al.  Monoclonal antibodies as innovative therapeutics. , 2008, Current pharmaceutical biotechnology.

[49]  A. Barabasi,et al.  High-Quality Binary Protein Interaction Map of the Yeast Interactome Network , 2008, Science.

[50]  R. Shamir,et al.  From E-MAPs to module maps: dissecting quantitative genetic interactions using physical interactions , 2008, Molecular Systems Biology.

[51]  C. Landry,et al.  An in Vivo Map of the Yeast Protein Interactome , 2008, Science.

[52]  Hyeong Jun An,et al.  Estimating the size of the human interactome , 2008, Proceedings of the National Academy of Sciences.

[53]  Trey Ideker,et al.  Functional Maps of Protein Complexes from Quantitative Genetic Interaction Data , 2008, PLoS Comput. Biol..

[54]  Mihaela E. Sardiu,et al.  Probabilistic assembly of human protein interaction networks from label-free quantitative proteomics , 2008, Proceedings of the National Academy of Sciences.

[55]  Yanhui Hu,et al.  A Biomedically Enriched Collection of 7000 Human ORF Clones , 2008, PloS one.

[56]  Yasukazu Nakamura,et al.  A Large Scale Analysis of Protein–Protein Interactions in the Nitrogen-fixing Bacterium Mesorhizobium loti , 2008, DNA research : an international journal for rapid publication of reports on genes and genomes.

[57]  César A. Hidalgo,et al.  Scale-free networks , 2008, Scholarpedia.

[58]  N. Horowitz George Wells Beadle (1903–1989) , 1989, Journal of Genetics.

[59]  Mark R Player,et al.  Small-molecule inhibitors of the p53-HDM2 interaction for the treatment of cancer. , 2008, Expert opinion on investigational drugs.

[60]  Christopher L. McClendon,et al.  Reaching for high-hanging fruit in drug discovery at protein–protein interfaces , 2007, Nature.

[61]  Yasukazu Nakamura,et al.  A Large-scale Protein–protein Interaction Analysis in Synechocystis sp. PCC6803 , 2007, DNA research : an international journal for rapid publication of reports on genes and genomes.

[62]  K. Gunsalus,et al.  Network modeling links breast cancer susceptibility and centrosome dysfunction. , 2007, Nature genetics.

[63]  T. Ideker,et al.  Network-based classification of breast cancer metastasis , 2007, Molecular systems biology.

[64]  S. Bradberry Ricin and abrin , 2007 .

[65]  A. Nanji,et al.  Functional Characterization of Pathogenic Human MSH2 Missense Mutations in Saccharomyces cerevisiae , 2007, Genetics.

[66]  A. Barabasi,et al.  The human disease network , 2007, Proceedings of the National Academy of Sciences.

[67]  A. Vazquez,et al.  Epstein–Barr virus and virus human protein interaction maps , 2007, Proceedings of the National Academy of Sciences.

[68]  J. Rogers,et al.  hORFeome v3.1: A resource of human open reading frames representing over 10,000 human genes , 2007, Genomics.

[69]  Pall I. Olason,et al.  A human phenome-interactome network of protein complexes implicated in genetic disorders , 2007, Nature Biotechnology.

[70]  A. Matera,et al.  Faculty Opinions recommendation of Repo-Man recruits PP1 gamma to chromatin and is essential for cell viability. , 2007 .

[71]  David E. Gloriam,et al.  ProteomeBinders: planning a European resource of affinity reagents for analysis of the human proteome , 2007, Nature Methods.

[72]  M. Mann,et al.  Protein interaction screening by quantitative immunoprecipitation combined with knockdown (QUICK) , 2006, Nature Methods.

[73]  John D. Scott,et al.  Anchored cAMP signaling: onward and upward - a short history of compartmentalized cAMP signal transduction. , 2006, European journal of cell biology.

[74]  Sophia Hober,et al.  A human protein atlas based on antibody proteomics. , 2006, Current opinion in molecular therapeutics.

[75]  A. Barabasi,et al.  A Protein–Protein Interaction Network for Human Inherited Ataxias and Disorders of Purkinje Cell Degeneration , 2006, Cell.

[76]  P. Bork,et al.  Proteome survey reveals modularity of the yeast cell machinery , 2006, Nature.

[77]  Sean R. Collins,et al.  Global landscape of protein complexes in the yeast Saccharomyces cerevisiae , 2006, Nature.

[78]  M. Philips,et al.  Compartmentalized Ras/MAPK signaling. , 2006, Annual review of immunology.

[79]  Tony Pawson,et al.  Modification of the Creator recombination system for proteomics applications – improved expression by addition of splice sites , 2006, BMC biotechnology.

[80]  P. Hilson Cloned sequence repertoires for small- and large-scale biology. , 2006, Trends in plant science.

[81]  Matthias Mann,et al.  Repo-Man recruits PP1γ to chromatin and is essential for cell viability , 2006, The Journal of cell biology.

[82]  G. Milligan,et al.  Heterotrimeric G‐proteins: a short history , 2006, British journal of pharmacology.

[83]  H. Rang The receptor concept: pharmacology's big idea , 2006, British journal of pharmacology.

[84]  Erik K. Malm,et al.  A Human Protein Atlas for Normal and Cancer Tissues Based on Antibody Proteomics* , 2005, Molecular & Cellular Proteomics.

[85]  M. Gerstein,et al.  Global analysis of protein phosphorylation in yeast , 2005, Nature.

[86]  S. L. Wong,et al.  Towards a proteome-scale map of the human protein–protein interaction network , 2005, Nature.

[87]  H. Lehrach,et al.  A Human Protein-Protein Interaction Network: A Resource for Annotating the Proteome , 2005, Cell.

[88]  Janice M Reichert,et al.  Monoclonal antibody successes in the clinic , 2005, Nature Biotechnology.

[89]  William Stafford Noble,et al.  Large-scale identification of yeast integral membrane protein interactions. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[90]  Christian von Mering,et al.  STRING: known and predicted protein–protein associations, integrated and transferred across organisms , 2004, Nucleic Acids Res..

[91]  R. Lefkowitz Historical review: a brief history and personal retrospective of seven-transmembrane receptors. , 2004, Trends in pharmacological sciences.

[92]  R. Aebersold,et al.  Identification of TFB5, a new component of general transcription and DNA repair factor IIH , 2004, Nature Genetics.

[93]  A. Szent-Györgyi,et al.  The Early History of the Biochemistry of Muscle Contraction , 2004, The Journal of general physiology.

[94]  Michelle R. Arkin,et al.  Small-molecule inhibitors of protein–protein interactions: progressing towards the dream , 2004, Nature Reviews Drug Discovery.

[95]  Patrick A. Curmi,et al.  Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain , 2004, Nature.

[96]  Gary D Bader,et al.  Global Mapping of the Yeast Genetic Interaction Network , 2004, Science.

[97]  A. Barabasi,et al.  Network biology: understanding the cell's functional organization , 2004, Nature Reviews Genetics.

[98]  S. L. Wong,et al.  A Map of the Interactome Network of the Metazoan C. elegans , 2004, Science.

[99]  J. Hayles,et al.  The fission yeast cell cycle control gene cdc2: structure of the cdc2 region , 1985, Molecular and General Genetics MGG.

[100]  P. Thuriaux,et al.  Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe , 1976, Molecular and General Genetics MGG.

[101]  James R. Knight,et al.  A Protein Interaction Map of Drosophila melanogaster , 2003, Science.

[102]  Joseph M. Dale,et al.  Empirical Analysis of Transcriptional Activity in the Arabidopsis Genome , 2003, Science.

[103]  M. Gerstein,et al.  A Bayesian Networks Approach for Predicting Protein-Protein Interactions from Genomic Data , 2003, Science.

[104]  E. O’Shea,et al.  Global analysis of protein expression in yeast , 2003, Nature.

[105]  E. O’Shea,et al.  Global analysis of protein localization in budding yeast , 2003, Nature.

[106]  J. Hudson,et al.  C. elegans ORFeome version 1.1: experimental verification of the genome annotation and resource for proteome-scale protein expression , 2003, Nature Genetics.

[107]  R. Aebersold,et al.  Mass spectrometry-based proteomics , 2003, Nature.

[108]  K. V. van Holde Reflections on a century of protein chemistry. , 2003, Biophysical chemistry.

[109]  Ronald W. Davis,et al.  Functional profiling of the Saccharomyces cerevisiae genome , 2002, Nature.

[110]  Gary D Bader,et al.  Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry , 2002, Nature.

[111]  P. Bork,et al.  Functional organization of the yeast proteome by systematic analysis of protein complexes , 2002, Nature.

[112]  G. Church,et al.  Correlation between transcriptome and interactome mapping data from Saccharomyces cerevisiae , 2001, Nature Genetics.

[113]  L. Nyholm,et al.  Evaluations of the stability of sheathless electrospray ionization mass spectrometry emitters using electrochemical techniques. , 2001, Analytical chemistry.

[114]  B. Séraphin,et al.  The tandem affinity purification (TAP) method: a general procedure of protein complex purification. , 2001, Methods.

[115]  R. Ozawa,et al.  A comprehensive two-hybrid analysis to explore the yeast protein interactome , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[116]  E Marshall,et al.  A History of the Human Genome Project , 2001, Science.

[117]  B. Schwikowski,et al.  A network of protein–protein interactions in yeast , 2000, Nature Biotechnology.

[118]  M. Gerstein,et al.  Analysis of yeast protein kinases using protein chips , 2000, Nature Genetics.

[119]  J. Schlessinger Cell Signaling by Receptor Tyrosine Kinases , 2000, Cell.

[120]  T. Pawson Protein Modules and Signaling Networks , 2000 .

[121]  A. Barabasi,et al.  Error and attack tolerance of complex networks , 2000, Nature.

[122]  James R. Knight,et al.  A comprehensive analysis of protein–protein interactions in Saccharomyces cerevisiae , 2000, Nature.

[123]  T. Ito,et al.  Toward a protein-protein interaction map of the budding yeast: A comprehensive system to examine two-hybrid interactions in all possible combinations between the yeast proteins. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[124]  M. Vidal,et al.  Protein interaction mapping in C. elegans using proteins involved in vulval development. , 2000, Science.

[125]  M. Vidal,et al.  GATEWAY recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes. , 2000, Methods in enzymology.

[126]  B. Séraphin,et al.  A generic protein purification method for protein complex characterization and proteome exploration , 1999, Nature Biotechnology.

[127]  Ronald W. Davis,et al.  Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. , 1999, Science.

[128]  M. Colledge,et al.  AKAPs: from structure to function. , 1999, Trends in cell biology.

[129]  R. Wagner,et al.  Anecdotal, historical and critical commentaries on genetics. Rudolph Virchow and the genetic basis of somatic ecology. , 1999 .

[130]  M. Vidal,et al.  Yeast forward and reverse 'n'-hybrid systems. , 1999, Nucleic acids research.

[131]  G. V. Vande Woude,et al.  Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes * , 1998, Biology of the cell.

[132]  Yoshio Masui,et al.  Understanding the cell cycle , 1998, Nature Medicine.

[133]  M. Uhlén,et al.  Affinity fusion strategies for detection, purification, and immobilization of recombinant proteins. , 1997, Protein expression and purification.

[134]  M. Vidal,et al.  Genetic characterization of a mammalian protein-protein interaction domain by using a yeast reverse two-hybrid system. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[135]  Stanley Fields,et al.  A protein linkage map of Escherichia coli bacteriophage T7 , 1996, Nature Genetics.

[136]  K. Manchester Louis Pasteur (1822-1895)--chance and the prepared mind. , 1995, Trends in biotechnology.

[137]  Tony Pawson,et al.  Protein modules and signalling networks , 1995, Nature.

[138]  Christian Rosenmund,et al.  Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons , 1994, Nature.

[139]  S. Korsmeyer,et al.  Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programed cell death , 1993, Cell.

[140]  Jonathan A. Cooper,et al.  Mammalian Ras interacts directly with the serine/threonine kinase raf , 1993, Cell.

[141]  P. Cohen,et al.  On target with a new mechanism for the regulation of protein phosphorylation. , 1993, Trends in biochemical sciences.

[142]  L. Johnson,et al.  Structural mechanism for glycogen phosphorylase control by phosphorylation and AMP. , 1992, Journal of molecular biology.

[143]  M. Moran,et al.  Binding of SH2 domains of phospholipase C gamma 1, GAP, and Src to activated growth factor receptors. , 1990, Science.

[144]  H. Hauptman History of X-ray crystallography , 1990 .

[145]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[146]  Jeremy Minshull,et al.  Cyclin is a component of maturation-promoting factor from Xenopus , 1990, Cell.

[147]  Susan S. Taylor,et al.  cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. , 1990, Annual review of biochemistry.

[148]  M. Mann,et al.  Electrospray ionization for mass spectrometry of large biomolecules. , 1989, Science.

[149]  Tony Hunter,et al.  Isolation of a human cyclin cDNA: Evidence for cyclin mRNA and protein regulation in the cell cycle and for interaction with p34cdc2 , 1989, Cell.

[150]  S. Fields,et al.  A novel genetic system to detect protein–protein interactions , 1989, Nature.

[151]  B Hammarberg,et al.  Dual affinity fusion approach and its use to express recombinant human insulin-like growth factor II. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[152]  Susan S. Taylor,et al.  cAMP-dependent protein kinase. Model for an enzyme family. , 1989, The Journal of biological chemistry.

[153]  D. Ledbetter,et al.  Chromosome 17 deletions and p53 gene mutations in colorectal carcinomas. , 1989, Science.

[154]  D. Bregman,et al.  High affinity binding protein for the regulatory subunit of cAMP-dependent protein kinase II-B. Cloning, characterization, and expression of cDNAs for rat brain P150. , 1989, The Journal of biological chemistry.

[155]  F. B. Straub Note on the work concerning ‘Adenosine triphosphate. The functional group of actin’ by F.B. Straub and G. Feuer Biochim. Biophys. Acta 4 (1950) 455–470 , 1989 .

[156]  F. B. Straub Note on the work of F. Bruno Straub concerning 'Adenosine Triphosphate. The Functional Group of Actin'. , 1989, Biochimica et biophysica acta.

[157]  M. Karas,et al.  Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons. , 1988, Analytical chemistry.

[158]  J. Labbé,et al.  Activation at M-phase of a protein kinase encoded by a starfish homologue of the cell cycle control gene cdc2+ , 1988, Nature.

[159]  Jean Gautier,et al.  Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene cdc2 + , 1988, Cell.

[160]  D. Smith,et al.  Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. , 1988, Gene.

[161]  Stephen H. Friend,et al.  Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product , 1988, Nature.

[162]  K. Mullis,et al.  Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. , 1988, Science.

[163]  T. Hunt,et al.  Molecular cloning and characterization of the mRNA for cyclin from sea urchin eggs. , 1987, The EMBO journal.

[164]  A. D. McLachlan,et al.  Profile analysis: detection of distantly related proteins. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[165]  P. Nurse,et al.  Complementation used to clone a human homologue of the fission yeast cell cycle control gene cdc2 , 1987, Nature.

[166]  T Pawson,et al.  A noncatalytic domain conserved among cytoplasmic protein-tyrosine kinases modifies the kinase function and transforming activity of Fujinami sarcoma virus P130gag-fps , 1986, Molecular and cellular biology.

[167]  P. Nurse,et al.  The cell cycle control gene cdc2 + of fission yeast encodes a protein kinase potentially regulated by phosphorylation , 1986, Cell.

[168]  R. Cooks,et al.  New scan modes accessed with a hybrid mass spectrometer , 1985 .

[169]  T. Førland On the mechanism of muscular contraction. , 1985, Biophysical journal.

[170]  D. Bastia,et al.  Rapid purification of a cloned gene product by genetic fusion and site-specific proteolysis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[171]  Susan M. Watanabe,et al.  An alteration of the human c-abl protein in K562 leukemia cells unmasks associated tyrosine kinase activity , 1984, Cell.

[172]  B. Hoffman,et al.  A simple and very efficient method for generating cDNA libraries. , 1983, Gene.

[173]  L. Brunton,et al.  Compartments of cyclic AMP and protein kinase in mammalian cardiomyocytes. , 1983, The Journal of biological chemistry.

[174]  R. Lerner,et al.  Generation of protein-reactive antibodies by short peptides is an event of high frequency: implications for the structural basis of immune recognition. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[175]  Eric T. Rosenthal,et al.  Cyclin: A protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division , 1983, Cell.

[176]  H. Okayama,et al.  High-efficiency cloning of full-length cDNA , 1982, Molecular and cellular biology.

[177]  S. Cohen,et al.  Identification of phosphotyrosine as a product of epidermal growth factor-activated protein kinase in A-431 cell membranes. , 1980, The Journal of biological chemistry.

[178]  J. Beckwith,et al.  Labeling of proteins with beta-galactosidase by gene fusion. Identification of a cytoplasmic membrane component of the Escherichia coli maltose transport system. , 1980, The Journal of biological chemistry.

[179]  D. Lane,et al.  Characterization of the complex between SV40 large T antigen and the 53K host protein in transformed mouse cells. , 1980, Cold Spring Harbor symposia on quantitative biology.

[180]  T. Hunter,et al.  An activity phosphorylating tyrosine in polyoma T antigen immunoprecipitates , 1979, Cell.

[181]  D. Lane,et al.  T antigen is bound to a host protein in SY40-transformed cells , 1979, Nature.

[182]  H. Varmus,et al.  Evidence that the transforming gene of avian sarcoma virus encodes a protein kinase associated with a phosphoprotein , 1978, Cell.

[183]  R. Erikson,et al.  Protein kinase activity associated with the avian sarcoma virus src gene product. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[184]  F. Jacob,et al.  Délétions fusionnant l'Opéron Lactose et un Opéron Purine chez Escherichia coli , 1978 .

[185]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[186]  J. Brugge,et al.  Identification of a transformation-specific antigen induced by an avian sarcoma virus , 1977, Nature.

[187]  G. Carpenter,et al.  125I-labeled human epidermal growth factor. Binding, internalization, and degradation in human fibroblasts , 1976, The Journal of cell biology.

[188]  Y. Masui,et al.  A cytoplasmic factor promoting oocyte maturation: its extraction and preliminary characterization. , 1976, Science.

[189]  E. Southern Detection of specific sequences among DNA fragments separated by gel electrophoresis. , 1975, Journal of molecular biology.

[190]  H. Brandt,et al.  Purification and properties of rabbit liver phosphorylase phosphatase. , 1975, The Journal of biological chemistry.

[191]  C. Milstein,et al.  Continuous cultures of fused cells secreting antibody of predefined specificity , 1975, Nature.

[192]  E. Krebs,et al.  Mechanisms of control for cAMP-dependent protein kinase from skeletal muscle. , 1975, Advances in cyclic nucleotide research.

[193]  T. Soderling,et al.  Hormonal regulation of adenosine 3',5'-monophosphate-dependent protein kinase. , 1975, Advances in cyclic nucleotide research.

[194]  A. Fersht,et al.  Influence of globin structure on the state of the heme. II. Allosteric transitions in methemoglobin. , 1974, Biochemistry.

[195]  F. Crick,et al.  Molecular Structure of Nucleic Acids: A Structure for Deoxyribose Nucleic Acid , 1974, Nature.

[196]  L. Hartwell,et al.  Genetic control of the cell division cycle in yeast. , 1974, Science.

[197]  F. Hucho Molecular weight and quaternary structure of the cholinergic receptor protein extracted by detergents from Electrophorus electricus electric tissue , 1973, FEBS letters.

[198]  J. Changeux,et al.  Immunological characterisation of the cholinergic receptor protein from Electrophorus electricus. , 1973, FEBS letters.

[199]  J. Patrick,et al.  Autoimmune Response to Acetylcholine Receptor , 1973, Science.

[200]  H. C. Hartzell,et al.  Acetylcholine Receptors: Number and Distribution at Neuromuscular Junctions in Rat Diaphragm , 1972, Science.

[201]  P. Cuatrecasas Insulin--receptor interactions in adipose tissue cells: direct measurement and properties. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[202]  R. Miledi,et al.  Biological Sciences: Isolation of the Cholinergic Receptor Protein of Torpedo Electric Tissue , 1971, Nature.

[203]  R. Miledi,et al.  Isolation of the cholinergic receptor protein of Torpedo electric tissue. , 1971, Nature.

[204]  Carl Frieden Protein-protein interaction and enzymatic activity. , 1971, Annual review of biochemistry.

[205]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[206]  D. Pette,et al.  Binding of aldolase and triosephosphate dehydrogenase to F-actin and modification of catalytic properties of aldolase. , 1970, European journal of biochemistry.

[207]  I. Pastan,et al.  ACTH receptors in the adrenal: specific binding of ACTH-125I and its relation to adenyl cyclase. , 1970, Proceedings of the National Academy of Sciences of the United States of America.

[208]  G. Robison,et al.  The Role of Cyclic AMP in the Control of Carbohydrate Metabolism , 1969, Diabetes.

[209]  S. McGavin Interallelic complementation and allostery. , 1968, Journal of molecular biology.

[210]  E. Krebs,et al.  An adenosine 3',5'-monophosphate-dependant protein kinase from rabbit skeletal muscle. , 1968, The Journal of biological chemistry.

[211]  M. Meselson,et al.  DNA Restriction Enzyme from E. coli , 1968, Nature.

[212]  P. Edman,et al.  A protein sequenator. , 1967, European journal of biochemistry.

[213]  F. Jacob,et al.  Délétions fusionnant ľopéron lactose et un opéron purine chez Escherichia coli , 1965 .

[214]  J. Changeux,et al.  ON THE NATURE OF ALLOSTERIC TRANSITIONS: A PLAUSIBLE MODEL. , 1965, Journal of molecular biology.

[215]  S. Ide,et al.  Isolation and properties of pyruvate and α-ketoglutarate dehydrogenation complexes from pig heart muscle , 1964 .

[216]  F. Crick,et al.  THE THEORY OF INTER-ALLELIC COMPLEMENTATION. , 1964, Journal of molecular biology.

[217]  E. Sutherland,et al.  THE EFFECT OF L-EPINEPHRINE AND OTHER AGENTS ON THE SYNTHESIS AND RELEASE OF ADENOSINE 3',5'-PHOSPHATE BY WHOLE PIGEON ERYTHROCYTES. , 1963, The Journal of biological chemistry.

[218]  G. Hein The Liebig-Pasteur controversy: Vitality without vitalism , 1961 .

[219]  M. Perutz,et al.  Structure of hemoglobin. , 1960, Brookhaven symposia in biology.

[220]  L. Reed,et al.  alpha-Keto acid dehydrogenation complexes. I. Purification and properties of pyruvate and alpha-ketoglutarate dehydrogenation complexes of Escherichia coli. , 1960, The Journal of biological chemistry.

[221]  E. Krebs,et al.  Specificity studies on muscle phosphorylase phosphatase. , 1960, The Journal of biological chemistry.

[222]  Structure and function in myoglobin and other proteins. , 1959 .

[223]  Structure and function in myoglobin and other proteins. , 1959, Federation proceedings.

[224]  E. Sutherland,et al.  Formation of a cyclic adenine ribonucleotide by tissue particles. , 1958, The Journal of biological chemistry.

[225]  M. DePamphilis,et al.  HUMAN DISEASE , 1957, The Ulster Medical Journal.

[226]  M. Florkin [Discovery of pepsin by Theodor Schwann]. , 1957, Revue medicale de Liege.

[227]  E. Krebs,et al.  The phosphorylase b to a converting enzyme of rabbit skeletal muscle. , 1956, Biochimica et biophysica acta.

[228]  E. Krebs,et al.  Conversion of phosphorylase b to phosphorylase a in muscle extracts. , 1955, The Journal of biological chemistry.

[229]  R. Dulbecco,et al.  PLAQUE FORMATION AND ISOLATION OF PURE LINES WITH POLIOMYELITIS VIRUSES , 1954, The Journal of experimental medicine.

[230]  Y. Tonomura,et al.  MECHANISM OF MUSCULAR CONTRACTION , 1953 .

[231]  F. Sanger,et al.  The amino-acid sequence in the glycyl chain of insulin. II. The investigation of peptides from enzymic hydrolysates. , 1951, The Biochemical journal.

[232]  F. Sanger,et al.  The amino-acid sequence in the glycyl chain of insulin. I. The identification of lower peptides from partial hydrolysates. , 1953, The Biochemical journal.

[233]  F. Sanger,et al.  The amino-acid sequence in the glycyl chain of insulin. , 1952, The Biochemical journal.

[234]  J. Littlefield,et al.  Studies on alpha-ketoglutaric oxidase. II. Purification and properties. , 1952, The Journal of biological chemistry.

[235]  F. Sanger,et al.  The arrangement of amino acids in proteins. , 1952, Advances in protein chemistry.

[236]  J. Telleria [Mechanism of muscular contraction]. , 1951, Medicina.

[237]  F. Sanger,et al.  The amino-acid sequence in the phenylalanyl chain of insulin. I. The identification of lower peptides from partial hydrolysates. , 1951, The Biochemical journal.

[238]  H. Hartley Origin of the Word ‘Protein’ , 1951, Nature.

[239]  F. Sanger,et al.  The amino-acid sequence in the phenylalanyl chain of insulin. 2. The investigation of peptides from enzymic hydrolysates. , 1951, The Biochemical journal.

[240]  F. Sanger Some chemical investigations on the structure of insulin. , 1950, Cold Spring Harbor symposia on quantitative biology.

[241]  F. B. Straub,et al.  [Adenosine triphosphate, the functional group of actin]. , 1950, Kiserletes orvostudomany.

[242]  T. Szilágyi,et al.  Antigenic Activity of Myosin and Actin , 1949, Nature.

[243]  F. Sanger Some Peptides from Insulin , 1948, Nature.

[244]  M. A. Jakus,et al.  Studies of actin and myosin. , 1947, The Journal of biological chemistry.

[245]  A. Tiselius Adsorption analysis of amino acid mixtures. , 1947, Advances in protein chemistry.

[246]  C. Cori,et al.  THE ENZYMATIC CONVERSION OF PHOSPHORYLASE a TO b , 1945 .

[247]  J. Needham,et al.  STUDIES ON THE ANOMALOUS VISCOSITY AND FLOW-BIREFRINGENCE OF PROTEIN SOLUTIONS , 1944, The Journal of general physiology.

[248]  A. J. Martin,et al.  Qualitative analysis of proteins: a partition chromatographic method using paper. , 1944, The Biochemical journal.

[249]  G. T. Cori,et al.  CRYSTALLINE MUSCLE PHOSPHORYLASE II. PROSTHETIC GROUP , 1943 .

[250]  D. Needham,et al.  The adenosinetriphosphatase activity of myosin preparations. , 1942, The Biochemical journal.

[251]  K. Bailey,et al.  Myosin and adenosinetriphosphatase. , 1942, The Biochemical journal.

[252]  C. Cori,et al.  CRYSTALLINE MUSCLE PHOSPHORYLASE , 1942 .

[253]  G. Beadle,et al.  Genetic Control of Biochemical Reactions in Neurospora , 1941 .

[254]  W. Engelhardt,et al.  Myosine and Adenosinetriphosphatase , 1939, Nature.

[255]  M. Bergmann The Structure of Proteins in Relation to Biological Problems. , 1938 .

[256]  Aristotle,et al.  Parts of Animals. Movement of Animals. Progression of Animals , 1937 .

[257]  Arne Tiselius,et al.  A new apparatus for electrophoretic analysis of colloidal mixtures , 1937 .

[258]  Inga-Britta,et al.  THE MOLECULAR WEIGHTS AND PH-STABILITY REGIONS OF THE HEMOCYANINS , 1936 .

[259]  J. Sumner THE CHEMICAL NATURE OF ENZYMES. , 1933, Science.

[260]  J. Edsall,et al.  Double refraction of myosin and its relation to the structure of the muscle fibre , 1930 .

[261]  THE. SVEDBERG,et al.  Mass and Size of Protein Molecules , 1929, Nature.

[262]  Eugen Chirnoaga THE MOLECULAR WEIGHT OF HEMOCYANIN , 1928 .

[263]  J. Sumner THE ISOLATION AND CRYSTALLIZATION OF THE ENZYME UREASE PRELIMINARY PAPER , 1926 .

[264]  J. Northrop THE INACTIVATION OF TRYPSIN : II. THE EQUILIBRIUM BETWEEN TRYPSIN AND THE INHIBITING SUBSTANCE FORMED BY ITS ACTION ON PROTEINS. , 1922 .

[265]  Rokuro Umemura The Relation Between the Absorption of Antibodies and the Isolated Protein Bodies , 1921 .

[266]  J. Loeb THE PROTEINS AND COLLOID CHEMISTRY. , 1920, Science.

[267]  R. M. Pearce CHANCE AND THE PREPARED MIND. , 1912, Science.

[268]  S. Hedin Trypsin and Antitrypsin. , 1906, The Biochemical journal.

[269]  J. H. Kastle ON THE VITAL ACTIVITY OF THE ENZYMES. , 1901, Science.

[270]  P. Ehrlich,et al.  Experimentelle Untersuchungen über Immunität. II. Ueber Abrin , 1891 .

[271]  R. Norris Researches on Muscular Irritability and the Relations which exist between Muscle, Nerve and Blood. , 1867, Journal of anatomy and physiology.