Small Proteins Can No Longer Be Ignored
Open accessAbstract
Small proteins, here defined as proteins of 50 amino acids or fewer in the absence of processing, have traditionally been overlooked due to challenges in their annotation and biochemical detection. In the past several years, however, increasing numbers of small proteins have been identified either through the realization that mutations in intergenic regions are actually within unannotated small protein genes or through the discovery that some small, regulatory RNAs encode small proteins. These insights, together with comparative sequence analysis, indicate that tens if not hundreds of small proteins are synthesized in a given organism. This review summarizes what has been learned about the functions of several of these bacterial small proteins, most of which act at the membrane, illustrating the astonishing range of processes in which these small proteins act and suggesting several general conclusions. Important questions for future studies of these overlooked proteins are also discussed.
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Growing experimental evidence in mycobacteria and other prokaryotes has shown that many sproteins are functional, requiring a rethinking of gene definitions.
“However, growing experimental evidence in mycobacteria and other prokaryotes has shown that many sproteins are functional, requiring a rethinking of gene definitions (71–75).”
From Mycobacterium smegmatis: The Vanguard of Mycobacterial Research (2023) · cites this paper as [71]
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Cites
Regulation by Small RNAs in Bacteria: Expanding Frontiers
Storz, G., Vogel, J., & Wassarman, K. M. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.08.022 · Cited by 1,181 · see citing works
Self-citationSTRUCTURE AND FUNCTION OF PHOTOSYSTEMS I AND II
Nelson, N., & Yocum, C. F. (2006) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.57.032905.105350 · Cited by 1,039 · see citing works
Some like it hot: the structure and function of small heat-shock proteins
Haslbeck, M., Franzmann, T. M., Weinfurtner, D., & Büchner, J. (2005) · Nature Structural & Molecular Biology · doi:10.1038/nsmb993 · Cited by 830 · see citing works
Mathematical models of infectious disease transmission
Grassly, N. C., & Fraser, C. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1845 · Cited by 739 · see citing works
Robinson, N. J., & Winge, D. R. (2010) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-030409-143539 · Cited by 708 · see citing works
Phenotypic Landscape of a Bacterial Cell
Nichols, R. J., Sen, Ś., Choo, Y. J., Beltrão, P., Zietek, M., Chaba, R., Lee, S., Kazmierczak, K. M., Lee, K. J., Wong, A., et al. (2010) · Cell · doi:10.1016/j.cell.2010.11.052 · Cited by 702 · see citing works
Proto-genes and de novo gene birth
Carvunis, A.-R., Rolland, T., Wapinski, I., Calderwood, M. A., Yildirim, M. A., Simonis, N., Charloteaux, B., Hidalgo, C. A., Barbette, J., Santhanam, B., et al. (2012) · Nature · doi:10.1038/nature11184 · Cited by 669 · see citing works
MOLECULAR GENETICS OF SPORULATION IN BACILLUS SUBTILIS
Stragier, P., & Losick, R. M. (1996) · Annual Review of Genetics · doi:10.1146/annurev.genet.30.1.297 · Cited by 647 · see citing works
FtsZ in Bacterial Cytokinesis: Cytoskeleton and Force Generator All in One
Erickson, H., Anderson, D. E., & Osawa, M. (2010) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00021-10 · Cited by 641 · see citing works
The anti-Shine–Dalgarno sequence drives translational pausing and codon choice in bacteria
Li, G., Oh, E., & Weissman, J. S. (2012) · Nature · doi:10.1038/nature10965 · Cited by 640 · see citing works
Emerging evidence for functional peptides encoded by short open reading frames
Andrews, S. J., & Rothnagel, J. A. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3520 · Cited by 547 · see citing works
I will survive: DNA protection in bacterial spores
Setlow, P. (2007) · Trends in Microbiology · doi:10.1016/j.tim.2007.02.004 · Cited by 466 · see citing works
Basis of Virulence in Community-Associated Methicillin-Resistant <i>Staphylococcus aureus</i>
Otto, M. (2010) · Annual Review of Microbiology · doi:10.1146/annurev.micro.112408.134309 · Cited by 457 · see citing works
Conserved Regulation of Cardiac Calcium Uptake by Peptides Encoded in Small Open Reading Frames
Magny, E. G., Pueyo, J. I., Pearl, F. M. G., Céspedes, M. A., Niven, J. E., Bishop, S. A., & Couso, J. P. (2013) · Science · doi:10.1126/science.1238802 · Cited by 368 · see citing works
Peptides Encoded by Short ORFs Control Development and Define a New Eukaryotic Gene Family
Galindo, M. I., Pueyo, J. I., Fouix, S., Bishop, S. A., & Couso, J. P. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050106 · Cited by 357 · see citing works
Vanderpool, C. K., & Gottesman, S. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04348.x · Cited by 353 · see citing works
Small Peptides Switch the Transcriptional Activity of Shavenbaby During Drosophila Embryogenesis
Kondo, T., Plaza, S., Zanet, J., Benrabah, E., Valenti, P., Hashimoto, Y., Kobayashi, S., Payre, F., & Kageyama, Y. (2010) · Science · doi:10.1126/science.1188158 · Cited by 348 · see citing works
Identification of FtsW as a transporter of lipid‐linked cell wall precursors across the membrane
Mohammadi, T., van Dam, V., Sijbrandi, R., Vernet, T., Zapun, A., Bouhss, A., Bruin, M. D.-D., Nguyen‐Distèche, M., KRUIJFF, B. D., & Breukink, E. J. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.61 · Cited by 314 · see citing works
Wadler, C. S., & Vanderpool, C. K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708102104 · Cited by 313 · see citing works
Ben‐Yehuda, S., & Losick, R. M. (2002) · Cell · doi:10.1016/s0092-8674(02)00698-0 · Cited by 291 · see citing works
Fozo, E. M., Makarova, K. S., Shabalina, S. A., Yutin, N., Koonin, E. V., & Storz, G. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq054 · Cited by 281 · see citing works
Self-citationGalperin, M. Y., Mekhedov, S., Puigbò, P., Smirnov, S. V., Wolf, Y. I., & Rigden, D. J. (2012) · Environmental Microbiology · doi:10.1111/j.1462-2920.2012.02841.x · Cited by 263 · see citing works
Self-citationSmall Toxic Proteins and the Antisense RNAs That Repress Them
Fozo, E. M., Hemm, M. R., & Storz, G. (2008) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00025-08 · Cited by 263 · see citing works
Self-citationBacterial cytokinesis: From Z ring to divisome
Lutkenhaus, J., Pichoff, S., & Du, S. (2012) · Cytoskeleton · doi:10.1002/cm.21054 · Cited by 261 · see citing works
Small peptide regulators of actin-based cell morphogenesis encoded by a polycistronic mRNA
Kondo, T., Hashimoto, Y. K., Kato, K., Inagaki, S., Hayashi, S., & Kageyama, Y. (2007) · Nature Cell Biology · doi:10.1038/ncb1595 · Cited by 260 · see citing works
Levin, P. A., & Losick, R. M. (1996) · Genes & Development · doi:10.1101/gad.10.4.478 · Cited by 260 · see citing works
Phylogenomics of Prokaryotic Ribosomal Proteins
Yutin, N., Puigbò, P., Koonin, E. V., & Wolf, Y. I. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036972 · Cited by 253 · see citing works
Self-citationWhy and How Bacteria Localize Proteins
Shapiro, L., McAdams, H. H., & Losick, R. M. (2009) · Science · doi:10.1126/science.1175685 · Cited by 251 · see citing works
Global analysis of the <i>Bacillus subtilis</i> Fur regulon and the iron starvation stimulon
Baichoo, N., Wang, T., Ye, R., & Helmann, J. D. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.03113.x · Cited by 250 · see citing works
Small Open Reading Frames: Beautiful Needles in the HaystackPreprint
Basrai, M. A., Hieter, P., & Boeke, J. D. (1997) · Genome Research · doi:10.1101/gr.7.8.768 · Cited by 240 · see citing works
Feedback Inhibition in the PhoQ/PhoP Signaling System by a Membrane Peptide
Lippa, A. M., & Goulian, M. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000788 · Cited by 240 · see citing works
Plasmid-Encoded ComI Inhibits Competence in the Ancestral 3610 Strain of Bacillus subtilis
Konkol, M. A., Blair, K. M., & Kearns, D. B. (2013) · Journal of Bacteriology · doi:10.1128/jb.00696-13 · Cited by 233 · see citing works
Gaballa, A., Antelmann, H., Aguilar, C., Khakh, S. K., Song, K.-B., Smaldone, G. T., & Helmann, J. D. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711752105 · Cited by 232 · see citing works
Small membrane proteins found by comparative genomics and ribosome binding site models
Hemm, M. R., Paul, B. J., Schneider, T. D., Storz, G., & Rudd, K. E. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06495.x · Cited by 223 · see citing works
Self-citationA question of size: the eukaryotic proteome and the problems in defining it
Harrison, P. M. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.5.1083 · Cited by 222 · see citing works
Hobbs, E. C., Yin, X., Paul, B. J., Astarita, J. L., & Storz, G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210093109 · Cited by 220 · see citing works
Self-citationGeometric Cue for Protein Localization in a Bacterium
Ramamurthi, K. S., Lecuyer, S., Stone, H. A., & Losick, R. M. (2009) · Science · doi:10.1126/science.1169218 · Cited by 204 · see citing works
Self-citationReplication Initiation Proteins Regulate a Developmental Checkpoint in Bacillus subtilis
Burkholder, W. F., Kurtser, I., & Grossman, A. D. (2001) · Cell · doi:10.1016/s0092-8674(01)00211-2 · Cited by 200 · see citing works
On the total number of genes and their length distribution in complete microbial genomes
Skovgaard, M., Jensen, L. J., Brunak, S., Ussery, D. W., & Krogh, A. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(01)02372-1 · Cited by 194 · see citing works
Small open reading frames associated with morphogenesis are hidden in plant genomes
Hanada, K., Higuchi‐Takeuchi, M., Okamoto, M., Yoshizumi, T., Shimizu, M., Nakaminami, K., Nishi, R., Ohashi, C., Iida, K., Tanaka, M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1213958110 · Cited by 188 · see citing works
Characterization of spoIVA, a sporulation gene involved in coat morphogenesis in Bacillus subtilis
Roels, S. M., Driks, A., & Losick, R. M. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.2.575-585.1992 · Cited by 186 · see citing works
The low molecular mass subunits of the photosynthetic supracomplex, photosystem II
Shi, L.-X., & Schröder, W. P. (2004) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2003.12.004 · Cited by 179 · see citing works
A PhoQ/P‐regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides
Moon, K., & Gottesman, S. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06944.x · Cited by 178 · see citing works
Herrera, C. M., Hankins, J. V., & Trent, M. S. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07150.x · Cited by 170 · see citing works
Programmed drug‐dependent ribosome stalling
Ramu, H., Mankin, A. S., & Vázquez‐Laslop, N. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06576.x · Cited by 165 · see citing works
Waters, L. S., Sandoval, M., & Storz, G. (2011) · Journal of Bacteriology · doi:10.1128/jb.05872-11 · Cited by 157 · see citing works
Self-citationLee, E., Pontes, M. H., & Groisman, E. A. (2013) · Cell · doi:10.1016/j.cell.2013.06.004 · Cited by 155 · see citing works
SpoIVA and SipL Are Clostridium difficile Spore Morphogenetic Proteins
Putnam, E. E., Nock, A. M., Lawley, T. D., & Shen, A. (2013) · Journal of Bacteriology · doi:10.1128/jb.02181-12 · Cited by 144 · see citing works
Sandman, K., Losick, R. M., & Youngman, P. J. (1987) · Genetics · doi:10.1093/genetics/117.4.603 · Cited by 140 · see citing works
SulA inhibits assembly of FtsZ by a simple sequestration mechanism
Chen, Y.-D., Milam, S. L., & Erickson, H. (2012) · Biochemistry · doi:10.1021/bi201669d · Cited by 135 · see citing works
Coote, J. G. (1972) · Journal of General Microbiology · doi:10.1099/00221287-71-1-1 · Cited by 135 · see citing works
Modell, J. W., Hopkins, A. C., & Laub, M. T. (2011) · Genes & Development · doi:10.1101/gad.2038911 · Cited by 134 · see citing works
Rowland, S., Burkholder, W. F., Cunningham, K. A., Maciejewski, M. W., Grossman, A. D., & King, G. F. (2004) · Molecular Cell · doi:10.1016/s1097-2765(04)00084-x · Cited by 128 · see citing works
Chen, L., James, L. P., & Helmann, J. D. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.17.5428-5437.1993 · Cited by 127 · see citing works
Eguchi, Y., Itou, J., Yamane, M., Demizu, R., Yamato, F., Okada, A., Mori, H., Kato, A., & Utsumi, R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705768104 · Cited by 126 · see citing works
Peptide‐assisted degradation of the Salmonella MgtC virulence factor
Alix, E., & Blanc‐Potard, A. (2008) · The EMBO Journal · doi:10.1038/sj.emboj.7601983 · Cited by 124 · see citing works
High-resolution view of bacteriophage lambda gene expression by ribosome profiling
Liu, X., Jiang, H., Gu, Z., & Roberts, J. W. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1309739110 · Cited by 120 · see citing works
Gaßel, M., Möllenkamp, T., Puppe, W., & Altendorf, K. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.53.37901 · Cited by 118 · see citing works
Peptide inhibitor of cytokinesis during sporulation in Bacillus subtilis
Handler, A. A., Lim, J. E., & Losick, R. M. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06173.x · Cited by 116 · see citing works
Hobbs, E. C., Astarita, J. L., & Storz, G. (2009) · Journal of Bacteriology · doi:10.1128/jb.00873-09 · Cited by 108 · see citing works
Self-citationVanOrsdel, C. E., Bhatt, S., Allen, R. J., Brenner, E. P., Hobson, J. J., Jamil, A., Haynes, B. M., Genson, A. M., & Hemm, M. R. (2013) · Journal of Bacteriology · doi:10.1128/jb.00324-13 · Cited by 107 · see citing works
An unusually small gene required for sporulation by Bacillus subtilis
Levin, P. A., Fan, N. C., Ricca, E., Driks, A., Losick, R. M., & Cutting, S. M. (1993) · Molecular Microbiology · doi:10.1111/j.1365-2958.1993.tb01736.x · Cited by 105 · see citing works
Peptide anchoring spore coat assembly to the outer forespore membrane in Bacillus subtilis
Ramamurthi, K. S., Clapham, K. R., & Losick, R. M. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05468.x · Cited by 101 · see citing works
Self-citationInserting proteins into the bacterial cytoplasmic membrane using the Sec and YidC translocases
Xie, K., & Dalbey, R. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro3595 · Cited by 98 · see citing works
Kato, A., Chen, H. D., Latifi, T. N., & Groisman, E. A. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.07.017 · Cited by 97 · see citing works
Crystal Structure of AcrB in Complex with a Single Transmembrane Subunit Reveals Another Twist
Törnroth‐Horsefield, S., Gourdon, P. E., Horsefield, R., Brive, L., Yamamoto, N., Mori, H., Snijder, A., & Neutze, R. (2007) · Structure · doi:10.1016/j.str.2007.09.023 · Cited by 97 · see citing works
Xie, K., & Dalbey, R. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.160 · Cited by 92 · see citing works
The Novel Transcription Factor SgrR Coordinates the Response to Glucose-Phosphate Stress
Vanderpool, C. K., & Gottesman, S. (2007) · Journal of Bacteriology · doi:10.1128/jb.01689-06 · Cited by 90 · see citing works
Whitten, A. E., Jacques, D. A., Hammouda, B., Hanley, T. L., King, G. F., Guss, J. M., Trewhella, J., & Langley, D. B. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.01.064 · Cited by 88 · see citing works
Status of genome projects for nonpathogenic bacteria and archaea
Nelson, K. E., Paulsen, I. T., Heidelberg, J. F., & Fraser, C. M. (2000) · Nature Biotechnology · doi:10.1038/80235 · Cited by 87 · see citing works
Insertion of short transmembrane helices by the Sec61 translocon
Jaud, S., Fernández-Vidal, M., Nilsson, I., Meindl‐Beinker, N. M., Hübner, N. C., Tobias, D. J., von HEIJNE, G., & White, S. H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900638106 · Cited by 87 · see citing works
Hydrophobic peptides: novel regulators within bacterial membrane
Alix, E., & Blanc‐Potard, A. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06626.x · Cited by 85 · see citing works
ATP-Driven Self-Assembly of a Morphogenetic Protein in Bacillus subtilis
Ramamurthi, K. S., & Losick, R. M. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.05.030 · Cited by 82 · see citing works
Self-citationA genome-wide survey of short coding sequences in streptococci
Ibrahim, M., Nicolas, P., Bessières, P., Bolotin, A., Monnet, V., & Gardan, R. (2007) · Microbiology · doi:10.1099/mic.0.2007/006205-0 · Cited by 81 · see citing works
Membrane Localization of Small Proteins in Escherichia coli
Fontaine, F., Fuchs, R. T., & Storz, G. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.245696 · Cited by 80 · see citing works
Self-citationHorler, R. S. P., & Vanderpool, C. K. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp501 · Cited by 80 · see citing works
Cutting, S. M., Anderson, M., Lysenko, E., Page, A., Tomoyasu, T., Tatematsu, K., Tatsuta, T., Kroos, L., & Ogura, T. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.17.5534-5542.1997 · Cited by 78 · see citing works
Yepes, A., Schneider, J., Mielich‐Süss, B., Koch, G., García-Betancur, J. C., Ramamurthi, K. S., Vlamakis, H. C., & López, D. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.08205.x · Cited by 77 · see citing works
Self-citationMagnesium and the Role of mgtC in Growth of Salmonella typhimurium
Moncrief, M. B. C., & Maguire, M. E. (1998) · Infection and Immunity · doi:10.1128/iai.66.8.3802-3809.1998 · Cited by 77 · see citing works
CtrA mediates a DNA replication checkpoint that prevents cell division in Caulobacter crescentus
Wortinger, M. A., Sackett, M. J., & Brun, Y. V. (2000) · The EMBO Journal · doi:10.1093/emboj/19.17.4503 · Cited by 74 · see citing works
Karimova, G., Robichon, C., & Ladant, D. (2008) · Journal of Bacteriology · doi:10.1128/jb.00331-08 · Cited by 71 · see citing works
Small Genes under Sporulation Control in the Bacillus subtilis genome
Schmalisch, M. H., Maiques, E., Nikolov, L. A., Camp, A. H., Chevreux, B., Muffler, A., Rodriguez, S. C., Perkins, J. B., & Losick, R. M. (2010) · Journal of Bacteriology · doi:10.1128/jb.00534-10 · Cited by 71 · see citing works
Smaldone, G. T., Antelmann, H., Gaballa, A., & Helmann, J. D. (2012) · Journal of Bacteriology · doi:10.1128/jb.05567-11 · Cited by 67 · see citing works
Bick, M. J., Lamour, V., Rajashankar, K. R., Gordiyenko, Y., Robinson, C. V., & Darst, S. A. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.12.006 · Cited by 66 · see citing works
The small protein CydX is required for function of cytochrome bd oxidase in Brucella abortus
Sun, Y.-H., de Jong, M. F., den Hartigh, A. B., Roux, C. M., Rolán, H. G., & Tsolis, R. M. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00047 · Cited by 60 · see citing works
Subcellular Localization of a Small Sporulation Protein inBacillus subtilis
van Ooij, C., & Losick, R. M. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.4.1391-1398.2003 · Cited by 60 · see citing works
Lippa, A. M., & Goulian, M. (2012) · Journal of Bacteriology · doi:10.1128/jb.06055-11 · Cited by 58 · see citing works
Schneider, D., Volkmer, T., & Rögner, M. (2006) · Research in Microbiology · doi:10.1016/j.resmic.2006.10.002 · Cited by 54 · see citing works
Stimulus-dependent differential regulation in the Escherichia coli PhoQ–PhoP system
Miyashiro, T., & Goulian, M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700025104 · Cited by 51 · see citing works
Small proteins link coat and cortex assembly during sporulation in Bacillus subtilis
Ebmeier, S., Tan, I. S., Clapham, K. R., & Ramamurthi, K. S. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.08052.x · Cited by 51 · see citing works
Self-citationPhage Lambda CIII: A Protease Inhibitor Regulating the Lysis-Lysogeny Decision
Kobiler, O., Rokney, A., & Oppenheim, A. B. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000363 · Cited by 48 · see citing works
Castaing, J.-P., Nagy, A., Anantharaman, V., Aravind, L., & Ramamurthi, K. S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210554110 · Cited by 44 · see citing works
Self-citationCunningham, K. A., & Burkholder, W. F. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06554.x · Cited by 43 · see citing works
Kirkpatrick, C. L., & Viollier, P. H. (2011) · Current Opinion in Microbiology · doi:10.1016/j.mib.2011.09.011 · Cited by 43 · see citing works
Structural and functional studies on an FtsH inhibitor from Bacillus subtilis
Prajapati, R. S., Ogura, T., & Cutting, S. M. (2000) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(00)00089-1 · Cited by 41 · see citing works
Choi, E., Lee, K., & Shin, D. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.11.107 · Cited by 40 · see citing works
Identification of prokaryotic small proteins using a comparative genomic approach
Samayoa, J. A., Yildiz, F. H., & Karplus, K. J. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr275 · Cited by 39 · see citing works
Karimova, G., Davi, M., & Ladant, D. (2012) · Journal of Bacteriology · doi:10.1128/jb.00774-12 · Cited by 39 · see citing works
Balasubramanian, D., & Vanderpool, C. K. (2013) · Journal of Bacteriology · doi:10.1128/jb.00586-13 · Cited by 38 · see citing works
Reduction of Turgor Is Not the Stimulus for the Sensor Kinase KdpD ofEscherichia coli
Hamann, K., Zimmann, P., & Altendorf, K. (2008) · Journal of Bacteriology · doi:10.1128/jb.01635-07 · Cited by 37 · see citing works
TorI, a response regulator inhibitor of phage origin in Escherichia coli
Ansaldi, M., Théraulaz, L., & Méjean, V. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401927101 · Cited by 33 · see citing works
The Spo0E phosphatase of Bacillus subtilis is a substrate of the FtsH metalloprotease
Le, A. T. T., & Schumann, W. (2009) · Microbiology · doi:10.1099/mic.0.024182-0 · Cited by 28 · see citing works
Kosfeld, A., & Jahreis, K. (2012) · Metabolites · doi:10.3390/metabo2040756 · Cited by 26 · see citing works
Gannoun-Zaki, L., Alibaud, L., Carrère‐Kremer, S., Kremer, L., & Blanc‐Potard, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060379 · Cited by 25 · see citing works
Wong, R. S. Y., McMurry, L. M., & Levy, S. B. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01998.x · Cited by 23 · see citing works
Cardenal‐Muñoz, E., & Ramos‐Morales, F. (2013) · Journal of Bacteriology · doi:10.1128/jb.00110-13 · Cited by 16 · see citing works
Jacques, D. A., Streamer, M., Rowland, S., King, G. F., Guss, J. M., Trewhella, J., & Langley, D. B. (2009) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s090744490901169x · Cited by 13 · see citing works
Halder, S., Banerjee, S., & Parrack, P. (2008) · FEBS Journal · doi:10.1111/j.1742-4658.2008.06610.x · Cited by 10 · see citing works
Guan, Z., Wang, X., & Raetz, C. R. H. (2010) · Analytical Biochemistry · doi:10.1016/j.ab.2010.10.035 · Cited by 9 · see citing works
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- [3]National Center for Biotechnology What Kind of Data Can be Submitted to GenBank? The GenBank Submissions Handbook 2011 Bethesda, MD http://www.ncbi.nlm.nih.gov/books/NBK53707/
Cited by
Sorted by citations
Schwengers, O., Jelonek, L., Dieckmann, M. A., Beyvers, S., Blom, J., & Goesmann, A. (2021) · Microbial Genomics · doi:10.1099/mgen.0.000685 · Cited by 1,469 · see citing works
Multidrug efflux pumps: structure, function and regulation
Du, D., Wang‐Kan, X., Neuberger, A., van Veen, H. W., Pos, K. M., Piddock, L. J. V., & Luisi, B. F. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0048-6 · Cited by 1,063 · see citing works
A Peptide Encoded by a Putative lncRNA HOXB-AS3 Suppresses Colon Cancer Growth
Huang, J., Chen, M., Chen, D., Gao, X.-C., Zhu, S., Huang, H., Hu, M., Zhu, H., & Yan, G. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.09.015 · Cited by 711 · see citing works
Discovery of antimicrobial peptides in the global microbiome with machine learning
Júnior, C. D. S., Torres, M. D. T., Duan, Y., del Río, Á. R., Schmidt, T., Chong, H., Fullam, A., Kuhn, M., Zhu, C., Houseman, A., et al. (2024) · Cell · doi:10.1016/j.cell.2024.05.013 · Cited by 435 · see citing works
Alternative ORFs and small ORFs: shedding light on the dark proteome
Orr, M. W., Mao, Y., Storz, G., & Qian, S. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz734 · Cited by 320 · see citing works
Self-citationA human microprotein that interacts with the mRNA decapping complex
D’Lima, N. G., Ma, J., Winkler, L., Chu, Q., Loh, K. H., Corpuz, E. O., Budnik, B., Lykke‐Andersen, J., Saghatelian, A., & Slavoff, S. A. (2016) · Nature Chemical Biology · doi:10.1038/nchembio.2249 · Cited by 302 · see citing works
Shell, S. S., Wang, J., Lapierre, P., Mir, M., Chase, M. R., Pyle, M. M., Gawande, R., Ahmad, R., Sarracino, D. A., Ioerger, T. R., et al. (2015) · PLOS Genetics · doi:10.1371/journal.pgen.1005641 · Cited by 238 · see citing works
Large-Scale Analyses of Human Microbiomes Reveal Thousands of Small, Novel Genes
Sberro, H., Fremin, B. J., Zlitni, S., Edfors, F., Greenfield, N., Snyder, M. P., Pavlopoulos, G. A., Kyrpides, N. C., & Bhatt, A. S. (2019) · Cell · doi:10.1016/j.cell.2019.07.016 · Cited by 237 · see citing works
Greene, N. P., Kaplan, E., Crow, A., & Koronakis, V. E. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00950 · Cited by 229 · see citing works
Redefining the Translational Status of 80S Monosomes
Heyer, E. E., & Moore, M. J. (2016) · Cell · doi:10.1016/j.cell.2016.01.003 · Cited by 202 · see citing works
Identifying Small Proteins by Ribosome Profiling with Stalled Initiation Complexes
Weaver, J., Mohammad, F., Buskirk, A. R., & Storz, G. (2019) · mBio · doi:10.1128/mbio.02819-18 · Cited by 180 · see citing works
Self-citationBacterial RNA Biology on a Genome Scale
Hör, J., Gorski, S. A., & Vogel, J. (2018) · Molecular Cell · doi:10.1016/j.molcel.2017.12.023 · Cited by 186 · see citing works
Retapamulin-Assisted Ribosome Profiling Reveals the Alternative Bacterial Proteome
Meydan, S., Marks, J., Klepacki, D., Sharma, V., Baranov, P. V., Firth, A. E., Margus, T., Kefi, A., Vázquez-Laslop, N., & Mankin, A. S. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.02.017 · Cited by 184 · see citing works
McLysaght, A., & Guerzoni, D. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0332 · Cited by 159 · see citing works
Mycobacterium smegmatis: The Vanguard of Mycobacterial Research
Sparks, I. L., Derbyshire, K. M., Jacobs, W. R., & Morita, Y. S. (2023) · Journal of Bacteriology · doi:10.1128/jb.00337-22 · Cited by 149 · see citing works
Babski, J., Haas, K. A., NäTher-Schindler, D., Pfeiffer, F., Förstner, K. U., Hammelmann, M., Hilker, R., Becker, A., Sharma, C. M., Marchfelder, A., et al. (2016) · BMC Genomics · doi:10.1186/s12864-016-2920-y · Cited by 140 · see citing works
Cross-species RNA-seq for deciphering host–microbe interactions
Westermann, A. J., & Vogel, J. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-021-00326-y · Cited by 136 · see citing works
Unraveling the hidden universe of small proteins in bacterial genomes
Miravet‐Verde, S., Ferrar, T. S., Espadas, G., Mazzolini, R., Gharrab, A., Sabidó, E., Serrano, L. G., & Lluch‐Senar, M. (2019) · Molecular Systems Biology · doi:10.15252/msb.20188290 · Cited by 127 · see citing works
In Search of Lost Small Peptides
Plaza, S., Menschaert, G., & Payre, F. (2017) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100616-060516 · Cited by 122 · see citing works
Application of targeted mass spectrometry in bottom-up proteomics for systems biology research
Manes, N. P., & Nita‐Lazar, A. (2018) · Journal of Proteomics · doi:10.1016/j.jprot.2018.02.008 · Cited by 124 · see citing works
Characterization of a second open reading frame in genome segment 10 of bluetongue virus
Stewart, M. E., Hardy, A., Barry, G., Pinto, R. M., Caporale, M., Melzi, E., Hughes, J., Taggart, A., Janowicz, A., Varela, M., et al. (2015) · Journal of General Virology · doi:10.1099/jgv.0.000267 · Cited by 113 · see citing works
Revisiting sORFs: overcoming challenges to identify and characterize functional microproteins
Schlesinger, D., & Elsässer, S. J. (2021) · FEBS Journal · doi:10.1111/febs.15769 · Cited by 111 · see citing works
Fiebig, M., Kelly, S. L., & Gluenz, E. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005186 · Cited by 110 · see citing works
Ultrasensitive Label-Free Nanosensing and High-Speed Tracking of Single Proteins
Liebel, M., Hugall, J. T., & van Hulst, N. F. (2017) · Nano Letters · doi:10.1021/acs.nanolett.6b05040 · Cited by 108 · see citing works
Li, X. L., Pongor, L. S., Tang, W., Das, S., Muys, B. R., Jones, M. F., Lazar, S. B., Dangelmaier, E. A., Hartford, C. C. R., Grammatikakis, I., et al. (2020) · eLife · doi:10.7554/elife.53734 · Cited by 105 · see citing works
A metabolic pathway for catabolizing levulinic acid in bacteria
Rand, J. M., Pisithkul, T., Clark, R. L., Thiede, J. M., Mehrer, C. R., Agnew, D. E., Campbell, C. E., Markley, A. L., Price, M. N., Ray, J., et al. (2017) · Nature Microbiology · doi:10.1038/s41564-017-0028-z · Cited by 104 · see citing works
A Practical Guide to Small Protein Discovery and Characterization Using Mass Spectrometry
Ahrens, C. H., Wade, J. T., Champion, M. M., & Langer, J. D. (2021) · Journal of Bacteriology · doi:10.1128/jb.00353-21 · Cited by 97 · see citing works
De novo birth of functional microproteins in the human lineage
Vakirlis, N., Vance, Z., Duggan, K. M., & McLysaght, A. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111808 · Cited by 97 · see citing works
Impens, F., Rolhion, N., Radoshevich, L., Bécavin, C., Duval, M., Mellin, J. R., del Portillo, F. G., Pucciarelli, M. G., Williams, A. H., & Cossart, P. (2017) · Nature Microbiology · doi:10.1038/nmicrobiol.2017.5 · Cited by 93 · see citing works
<i>Escherichia coli</i> Small Proteome
Hemm, M. R., Weaver, J., & Storz, G. (2020) · EcoSal Plus · doi:10.1128/ecosalplus.esp-0031-2019 · Cited by 91 · see citing works
Self-citationWidespread Antisense Transcription in Prokaryotes
Georg, J., & Hess, W. R. (2018) · Microbiology Spectrum · doi:10.1128/microbiolspec.rwr-0029-2018 · Cited by 88 · see citing works
Oswald, J., Njenga, R., Natriashvili, A., Sarmah, P., & Koch, H.-G. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.664241 · Cited by 88 · see citing works
Small open reading frames and cellular stress responses
Khitun, A., Ness, T. J., & Slavoff, S. A. (2019) · Molecular Omics · doi:10.1039/c8mo00283e · Cited by 85 · see citing works
Regulatory RNAs in photosynthetic cyanobacteria
Kopf, M., & Hess, W. R. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv017 · Cited by 84 · see citing works
Gelsinger, D. R., Dallon, E., Reddy, R., Mohammad, F., Buskirk, A. R., & DiRuggiero, J. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa304 · Cited by 77 · see citing works
Miranda-CasoLuengo, A. A., Staunton, P. M., Dinan, A. M., Lohan, A. J., & Loftus, B. J. (2016) · BMC Genomics · doi:10.1186/s12864-016-2868-y · Cited by 81 · see citing works
Co-translational protein targeting in bacteria.
Steinberg, R., Knüpffer, L., Origi, A., Asti, R., & Koch, H.-G. (2018) · FEMS Microbiology Letters · doi:10.1093/femsle/fny095 · Cited by 81 · see citing works
Increasing intracellular magnesium levels with the 31-amino acid MgtS protein
Wang, H., Yin, X., Orr, M. W., Dambach, M., Curtis, R., & Storz, G. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1703415114 · Cited by 80 · see citing works
Self-citationRyan, D., Jenniches, L., Reichardt, S., Barquist, L., & Westermann, A. J. (2020) · Nature Communications · doi:10.1038/s41467-020-17348-5 · Cited by 81 · see citing works
Diversity in Sensing and Signaling of Bacterial Sensor Histidine Kinases
Ishii, E., & Eguchi, Y. (2021) · Biomolecules · doi:10.3390/biom11101524 · Cited by 81 · see citing works
Omasits, U., Varadarajan, A. R., Schmid, M., Götze, S., Melidis, D. P., Bourqui, M., Nikolayeva, O., Québatte, M., Patrignani, A., Dehio, C., et al. (2017) · Genome Research · doi:10.1101/gr.218255.116 · Cited by 79 · see citing works
Cassidy, L., Kaulich, P. T., Maaß, S., Bartel, J., Becher, D., & Tholey, A. (2021) · Proteomics · doi:10.1002/pmic.202100008 · Cited by 61 · see citing works
Small bacterial and phagic proteins: an updated view on a rapidly moving field
Duval, M., & Cossart, P. (2017) · Current Opinion in Microbiology · doi:10.1016/j.mib.2017.09.010 · Cited by 78 · see citing works
Du, D., Neuberger, A., Orr, M. W., Newman, C. E., Hsu, P., Samsudin, F., Harris, A., Ramos, L. M., Debela, M., Khalid, S., et al. (2020) · Structure · doi:10.1016/j.str.2020.03.013 · Cited by 77 · see citing works
Self-citationOvchinnikova, O. G., Treat, L. P., Teelucksingh, T., Clarke, B. R., Miner, T. A., Whitfield, C., Walker, K. A., & Miller, V. L. (2023) · mBio · doi:10.1128/mbio.00800-23 · Cited by 73 · see citing works
ANNOgesic: a Swiss army knife for the RNA-seq based annotation of bacterial/archaeal genomes
Yu, S., Vogel, J., & Förstner, K. U. (2018) · GigaScience · doi:10.1093/gigascience/giy096 · Cited by 73 · see citing works
Pervasive translation in Mycobacterium tuberculosis
Smith, C., Canestrari, J. G., Wang, A. J., Champion, M. M., Derbyshire, K. M., Gray, T. A., & Wade, J. T. (2022) · eLife · doi:10.7554/elife.73980 · Cited by 71 · see citing works
The largely unexplored biology of small proteins in pro‐ and eukaryotes
Steinberg, R., & Koch, H. (2021) · FEBS Journal · doi:10.1111/febs.15845 · Cited by 71 · see citing works
Brunet, M. A., Levesque, S. A., Hunting, D. J., Cohen, A. A., & Roucou, X. (2018) · Genome Research · doi:10.1101/gr.230938.117 · Cited by 69 · see citing works
Delcourt, V., Staskevicius, A., Salzet, M., Fournier, I., & Roucou, X. (2017) · PROTEOMICS · doi:10.1002/pmic.201700058 · Cited by 68 · see citing works
Regulation of Resistance in Vancomycin-Resistant Enterococci: The VanRS Two-Component System
Guffey, A. A., & Loll, P. J. (2021) · Microorganisms · doi:10.3390/microorganisms9102026 · Cited by 70 · see citing works
A large-scale proteogenomic atlas of pear
Wang, P., Wu, X. B., Shi, Z., Tao, S., Liu, Z., Qi, K., Xie, Z., Qiao, X., Gu, C., Yin, H., et al. (2023) · Molecular Plant · doi:10.1016/j.molp.2023.01.011 · Cited by 67 · see citing works
Salazar, M. E., Podgornaia, A., & Laub, M. T. (2016) · Molecular Microbiology · doi:10.1111/mmi.13471 · Cited by 66 · see citing works
Liu, J., & Rozovsky, S. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2015.6388 · Cited by 65 · see citing works
Fuchs, M., Lamm‐Schmidt, V., Sulzer, J., Ponath, F., Jenniches, L., Kirk, J. A., Fagan, R. P., Barquist, L., Vogel, J., & Faber, F. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2103579118 · Cited by 65 · see citing works
Yang, H., Li, Q., Stroup, E. K., Wang, S., & Ji, Z. (2024) · Nature Communications · doi:10.1038/s41467-024-46240-9 · Cited by 65 · see citing works
Raina, M., King, A., Bianco, C. M., & Vanderpool, C. K. (2018) · Microbiology Spectrum · doi:10.1128/microbiolspec.rwr-0032-2018 · Cited by 62 · see citing works
van der Meulen, S. B., de Jong, A., & Kok, J. (2016) · RNA Biology · doi:10.1080/15476286.2016.1146855 · Cited by 64 · see citing works
Delcourt, V., Brunelle, M., Roy, A. V., Jacques, J., Salzet, M., Fournier, I., & Roucou, X. (2018) · Molecular & Cellular Proteomics · doi:10.1074/mcp.ra118.000593 · Cited by 65 · see citing works
Identification of Unannotated Small Genes in Salmonella
Baek, J., Lee, J., Yoon, K., & Lee, H.-W. (2017) · G3 Genes Genomes Genetics · doi:10.1534/g3.116.036939 · Cited by 63 · see citing works
Cao, X., Khitun, A., Na, Z., Dumitrescu, D. G., Kubica, M., Olatunji, E., & Slavoff, S. A. (2020) · Journal of Proteome Research · doi:10.1021/acs.jproteome.0c00254 · Cited by 63 · see citing works
Identifying New Small Proteins in Escherichia coli
VanOrsdel, C. E., Kelly, J. P., Burke, B. N., Lein, C. D., Oufiero, C. E., Sanchez, J. F., Wimmers, L. E., Hearn, D. J., Abuikhdair, F. J., Barnhart, K. R., et al. (2018) · PROTEOMICS · doi:10.1002/pmic.201700064 · Cited by 61 · see citing works
Venturini, E., Svensson, S. L., Maaß, S., Gelhausen, R., Eggenhofer, F., Li, L., Cain, A. K., Parkhill, J., Becher, D., Backofen, R., et al. (2020) · microLife · doi:10.1093/femsml/uqaa002 · Cited by 57 · see citing works
Automated Prediction and Annotation of Small Open Reading Frames in Microbial Genomes
Durrant, M. G., & Bhatt, A. S. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.11.002 · Cited by 59 · see citing works
Nhu, N. T. K., Phan, M., Peters, K. M., Lo, A. W. H., Forde, B. M., Chong, T. M., Yin, W., Chan, K., Chromek, M., Brauner, A., et al. (2018) · mBio · doi:10.1128/mbio.01462-18 · Cited by 56 · see citing works
Kaulich, P. T., Cassidy, L., Bartel, J., Schmitz, R. A., & Tholey, A. (2021) · Journal of Proteome Research · doi:10.1021/acs.jproteome.1c00115 · Cited by 55 · see citing works
Cai, T., Zhang, Q., Wu, B., Wang, J., Li, N., Zhang, T., Wang, Z., Luo, J., Guo, X., Ding, X. D., et al. (2021) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12123 · Cited by 55 · see citing works
Structural basis for the tryptophan sensitivity of TnaC-mediated ribosome stalling
van der Stel, A., Gordon, E. R., Sengupta, A., Martínez, A. K., Klepacki, D., Perry, T. N., del Valle, A. H., Vázquez‐Laslop, N., Sachs, M. S., Cruz-Vera, L. R., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25663-8 · Cited by 55 · see citing works
Reconsidering proteomic diversity with functional investigation of small ORFs and alternative ORFs
Brunet, M. A., Leblanc, S., & Roucou, X. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.112057 · Cited by 54 · see citing works
Dimonaco, N. J., Aubrey, W., Kenobi, K., Clare, A. J., & Creevey, C. J. (2021) · Bioinformatics · doi:10.1093/bioinformatics/btab827 · Cited by 54 · see citing works
Cassidy, L., Prasse, D., Linke, D., Schmitz, R. A., & Tholey, A. (2016) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00569 · Cited by 52 · see citing works
Genome-wide discovery of structured noncoding RNAs in bacteria
Stav, S., Atilho, R. M., Arachchilage, G. M., Nguyen, G., Higgs, G., & Breaker, R. R. (2019) · BMC Microbiology · doi:10.1186/s12866-019-1433-7 · Cited by 54 · see citing works
Varadarajan, A. R., Allan, R. N., Valentin, J. D. P., Ocampo, O. E. C., Somerville, V., Pietsch, F., Buhmann, M. T., West, J. J., Skipp, P. J. S., van der Mei, H. C., et al. (2020) · npj Biofilms and Microbiomes · doi:10.1038/s41522-020-00154-8 · Cited by 55 · see citing works
RNA landscape of the emerging cancer-associated microbe Fusobacterium nucleatum
Ponath, F., Tawk, C., Zhu, Y., Barquist, L., Faber, F., & Vogel, J. (2021) · Nature Microbiology · doi:10.1038/s41564-021-00927-7 · Cited by 54 · see citing works
Towards functional characterization of archaeal genomic dark matter
Makarova, K. S., Wolf, Y. I., & Koonin, E. V. (2019) · Biochemical Society Transactions · doi:10.1042/bst20180560 · Cited by 51 · see citing works
Self-citationDe Novo Emergence of Peptides That Confer Antibiotic Resistance
Knopp, M. R., Guðmundsdóttir, J. S., Nilsson, T., König, F., Warsi, O., Rajer, F., Ädelroth, P., & Andersson, D. I. (2019) · mBio · doi:10.1128/mbio.00837-19 · Cited by 53 · see citing works
Thousands of small, novel genes predicted in global phage genomes
Fremin, B. J., Bhatt, A. S., Kyrpides, N. C., Sengupta, A., Sczyrba, A., da Silva, A. M., Buchan, A., Gaudin, A. C. M., Brune, A., Hirsch, A. M., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110984 · Cited by 51 · see citing works
Microproteins—Discovery, structure, and function
Mohsen, J. J., Martel, A. A., & Slavoff, S. A. (2023) · PROTEOMICS · doi:10.1002/pmic.202100211 · Cited by 51 · see citing works
Proteomic Detection and Validation of Translated Small Open Reading Frames
Khitun, A., & Slavoff, S. A. (2019) · Current Protocols in Chemical Biology · doi:10.1002/cpch.77 · Cited by 49 · see citing works
Garai, P., & Blanc‐Potard, A. (2020) · Molecular Microbiology · doi:10.1111/mmi.14564 · Cited by 51 · see citing works
Discovery of novel community-relevant small proteins in a simplified human intestinal microbiome
Petruschke, H., Schori, C., Canzler, S., Riesbeck, S., Poehlein, A., Daniel, R., Frei, D., Segessemann, T., Zimmerman, J., Μαρίνος, Γ., et al. (2021) · Microbiome · doi:10.1186/s40168-020-00981-z · Cited by 49 · see citing works
TWS1, a Novel Small Protein, Regulates Various Aspects of Seed and Plant Development
Fiume, E., Guyon, V., Remoué, C., Magnani, E., Miquel, M., Grain, D., & Lepiniec, L. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.00915 · Cited by 49 · see citing works
Diversity and complexity of flavodiiron NO/O2 reductases
Folgosa, F., Martins, M. C., & Teixeira, M. S. (2017) · FEMS Microbiology Letters · doi:10.1093/femsle/fnx267 · Cited by 49 · see citing works
Yin, X., Orr, M. W., Wang, H., Hobbs, E. C., Shabalina, S. A., & Storz, G. (2018) · Molecular Microbiology · doi:10.1111/mmi.14143 · Cited by 49 · see citing works
Self-citationLago, M., Monteil, V., Douché, T., Guglielmini, J., Criscuolo, A., Maufrais, C., Matondo, M., & Norel, F. (2017) · Scientific Reports · doi:10.1038/s41598-017-02362-3 · Cited by 48 · see citing works
He, C., Jia, C., Zhang, Y., & Xu, P. (2018) · Journal of Proteome Research · doi:10.1021/acs.jproteome.8b00032 · Cited by 48 · see citing works
Bacterial Small Membrane Proteins: the Swiss Army Knife of Regulators at the Lipid Bilayer
Yadavalli, S. S., & Yuan, J. (2021) · Journal of Bacteriology · doi:10.1128/jb.00344-21 · Cited by 49 · see citing works
Functional Determinants of a Small Protein Controlling a Broadly Conserved Bacterial Sensor Kinase
Yadavalli, S. S., Goh, T., Carey, J. N., Malengo, G., Vellappan, S., Nickels, B. E., Sourjik, V., Goulian, M., & Yuan, J. (2020) · Journal of Bacteriology · doi:10.1128/jb.00305-20 · Cited by 42 · see citing works
Yeom, J., Shao, Y., & Groisman, E. A. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2006116117 · Cited by 44 · see citing works
Enrichment and identification of small proteins in a simplified human gut microbiome
Petruschke, H., Anders, J., Stadler, P. F., Jehmlich, N., & von Bergen, M. (2020) · Journal of Proteomics · doi:10.1016/j.jprot.2019.103604 · Cited by 43 · see citing works
Shining in the dark: the big world of small peptides in plants
Feng, Y., Zhu, Q., Xue, J., Chen, P. C., & Yu, Y. (2023) · aBIOTECH · doi:10.1007/s42994-023-00100-0 · Cited by 44 · see citing works
Allen, R. J., Brenner, E. P., VanOrsdel, C. E., Hobson, J. J., Hearn, D. J., & Hemm, M. R. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-946 · Cited by 43 · see citing works
Stringer, A. M., Smith, C., Mangano, K., & Wade, J. T. (2021) · Journal of Bacteriology · doi:10.1128/jb.00352-21 · Cited by 42 · see citing works
Understanding small ORF diversity through a comprehensive transcription feature classification
Guerra-Almeida, D., Tschoeke, D. A., & Nunes-da-Fonseca, R. (2021) · DNA Research · doi:10.1093/dnares/dsab007 · Cited by 40 · see citing works
Small RNA-Based Regulation of Bacterial Quorum Sensing and Biofilm Formation
Svenningsen, S. L. (2018) · Microbiology Spectrum · doi:10.1128/microbiolspec.rwr-0017-2018 · Cited by 40 · see citing works
Fuchs, S., Kucklick, M., Lehmann, E., Beckmann, A., Wilkens, M., Kolte, B. S., Mustafayeva, A., Ludwig, T., Diwo, M., Wissing, J. B., et al. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009585 · Cited by 41 · see citing works
The hidden bacterial microproteome
Fesenko, I. A., Sahakyan, H., Dhyani, R., Shabalina, S. A., Storz, G., & Koonin, E. V. (2025) · Molecular Cell · doi:10.1016/j.molcel.2025.01.025 · Cited by 41 · see citing works
Self-citationOptimized Proteomics Workflow for the Detection of Small Proteins
Bartel, J., Varadarajan, A. R., Sura, T., Ahrens, C. H., Maaß, S., & Becher, D. (2020) · Journal of Proteome Research · doi:10.1021/acs.jproteome.0c00286 · Cited by 39 · see citing works
Cornet, L., Cleenwerck, I., Praet, J., Léonard, R. R., Vereecken, N. J., Michez, D., Smagghe, G. J., Baurain, D., & Vandamme, P. A. R. (2022) · mSystems · doi:10.1128/msystems.01500-21 · Cited by 40 · see citing works
Zhao, L., Svetec, N., & Begun, D. J. (2024) · Annual Review of Genetics · doi:10.1146/annurev-genet-111523-102413 · Cited by 38 · see citing works
- Authors
- Storz, G., Wolf, Y. I., & Ramamurthi, K. S.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Storz, Gisela
- Ramamurthi, Kumaran S.
- Venue
- Annual Review of Biochemistry
- Publisher
- Annual Reviews
- Published
- 2014-06-02
- Volume
- 83
- Issue
- 1
- Pages
- 753-777
- ISSN
- 0066-4154 (ISSN-L)
- 1545-4509
- PMC
- PMC4166647
- OpenAlex
- W2121350645
- Cited by
- 359
- References
- 108
- Citations by year
- 2026: 19 · 2025: 27 · 2024: 32 · 2023: 37 · 2022: 22 · 2021: 46 · 2020: 41 · 2019: 29 · 2018: 38 · 2017: 28 · 2016: 24 · 2015: 11 · 2014: 4
- FWCI
- 2.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Annual Review of Biochemistry (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (Z99 LM999999)
- National Cancer Institute (ZIABC011211)
- National Institute of Child Health and Human Development
- U.S. National Library of Medicine
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (ZIAHD008855)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
- Keywords
- small proteins, small regulatory RNAs, protein annotation, membrane proteins, sequence comparison, protein function
- MeSH terms
- Amino Acids, Animals, Bacillus subtilis, Bacterial Proteins, Bacteriophages, Cell Division, Codon, Drosophila, Escherichia coli, Protein Kinases, Proteins, Ribosomes, RNA, Signal Transduction, Open Reading Frames, Computational Biology
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