Display options
Cite
Larsen J, Raisen CL, Ba X, et al. Emergence of methicillin resistance predates the clinical use of antibiotics. Nature. 2022;doi: 10.1038/s41586-021-04265-w.
Larsen, J., Raisen, C. L., Ba, X., Sadgrove, N. J., Padilla-González, G. F., Simmonds, M. S. J., Loncaric, I., Kerschner, H., Apfalter, P., Hartl, R., Deplano, A., Vandendriessche, S., Černá Bolfíková, B., Hulva, P., Arendrup, M. C., Hare, R. K., Barnadas, C., Stegger, M., Sieber, R. N., Skov, R. L., Petersen, A., Angen, �. �., Rasmussen, S. L., Espinosa-Gongora, C., Aarestrup, F. M., Lindholm, L. J., Nykäsenoja, S. M., Laurent, F., Becker, K., Walther, B., Kehrenberg, C., Cuny, C., Layer, F., Werner, G., Witte, W., Stamm, I., Moroni, P., Jørgensen, H. J., de Lencastre, H., Cercenado, E., García-Garrote, F., Börjesson, S., Hæggman, S., Perreten, V., Teale, C. J., Waller, A. S., Pichon, B., Curran, M. D., Ellington, M. J., Welch, J. J., Peacock, S. J., Seilly, D. J., Morgan, F. J. E., Parkhill, J., Hadjirin, N. F., Lindsay, J. A., Holden, M. T. G., Edwards, G. F., Foster, G., Paterson, G. K., Didelot, X., Holmes, M. A., Harrison, E. M., & Larsen, A. R. (2022). Emergence of methicillin resistance predates the clinical use of antibiotics. Nature, . https://doi.org/10.1038/s41586-021-04265-w
Larsen, Jesper, et al. "Emergence of methicillin resistance predates the clinical use of antibiotics." Nature vol. (2022). doi: https://doi.org/10.1038/s41586-021-04265-w
Larsen J, Raisen CL, Ba X, Sadgrove NJ, Padilla-González GF, Simmonds MSJ, Loncaric I, Kerschner H, Apfalter P, Hartl R, Deplano A, Vandendriessche S, Černá Bolfíková B, Hulva P, Arendrup MC, Hare RK, Barnadas C, Stegger M, Sieber RN, Skov RL, Petersen A, Angen Ø, Rasmussen SL, Espinosa-Gongora C, Aarestrup FM, Lindholm LJ, Nykäsenoja SM, Laurent F, Becker K, Walther B, Kehrenberg C, Cuny C, Layer F, Werner G, Witte W, Stamm I, Moroni P, Jørgensen HJ, de Lencastre H, Cercenado E, García-Garrote F, Börjesson S, Hæggman S, Perreten V, Teale CJ, Waller AS, Pichon B, Curran MD, Ellington MJ, Welch JJ, Peacock SJ, Seilly DJ, Morgan FJE, Parkhill J, Hadjirin NF, Lindsay JA, Holden MTG, Edwards GF, Foster G, Paterson GK, Didelot X, Holmes MA, Harrison EM, Larsen AR. Emergence of methicillin resistance predates the clinical use of antibiotics. Nature. 2022 Jan 05; doi: 10.1038/s41586-021-04265-w. Epub 2022 Jan 05. PMID: 34987223.
Copy Download .nbib Format: NLM
Share it on

Nature. 2022 Jan 05; doi: 10.1038/s41586-021-04265-w. Epub 2022 Jan 05.

Emergence of methicillin resistance predates the clinical use of antibiotics.

Nature

Jesper Larsen, Claire L Raisen, Xiaoliang Ba, Nicholas J Sadgrove, Guillermo F Padilla-González, Monique S J Simmonds, Igor Loncaric, Heidrun Kerschner, Petra Apfalter, Rainer Hartl, Ariane Deplano, Stien Vandendriessche, Barbora Černá Bolfíková, Pavel Hulva, Maiken C Arendrup, Rasmus K Hare, Céline Barnadas, Marc Stegger, Raphael N Sieber, Robert L Skov, Andreas Petersen, Øystein Angen, Sophie L Rasmussen, Carmen Espinosa-Gongora, Frank M Aarestrup, Laura J Lindholm, Suvi M Nykäsenoja, Frederic Laurent, Karsten Becker, Birgit Walther, Corinna Kehrenberg, Christiane Cuny, Franziska Layer, Guido Werner, Wolfgang Witte, Ivonne Stamm, Paolo Moroni, Hannah J Jørgensen, Hermínia de Lencastre, Emilia Cercenado, Fernando García-Garrote, Stefan Börjesson, Sara Hæggman, Vincent Perreten, Christopher J Teale, Andrew S Waller, Bruno Pichon, Martin D Curran, Matthew J Ellington, John J Welch, Sharon J Peacock, David J Seilly, Fiona J E Morgan, Julian Parkhill, Nazreen F Hadjirin, Jodi A Lindsay, Matthew T G Holden, Giles F Edwards, Geoffrey Foster, Gavin K Paterson, Xavier Didelot, Mark A Holmes, Ewan M Harrison, Anders R Larsen

Affiliations

  1. Department of Bacteria, Parasites & Fungi, Statens Serum Institut, Copenhagen, Denmark. [email protected].
  2. Department of Veterinary Medicine, University of Cambridge, Cambridge, UK.
  3. Royal Botanic Gardens, Kew, Richmond, UK.
  4. Institute of Microbiology, University of Veterinary Medicine, Vienna, Austria.
  5. National Reference Center for Antimicrobial Resistance and Nosocomial Infections, Institute for Hygiene, Microbiology and Tropical Medicine, Ordensklinikum Linz Elisabethinen, Linz, Austria.
  6. National Reference Centre-Staphylococcus aureus, Department of Microbiology, Hôpital Erasme, Université libre de Bruxelles, Brussels, Belgium.
  7. Laboratory for Medical Microbiology, Ghent University Hospital, Ghent, Belgium.
  8. Department of Animal Science and Food Processing, Faculty of Tropical AgriSciences, Czech University of Life Sciences Prague, Prague, Czech Republic.
  9. Department of Zoology, Charles University, Prague, Czech Republic.
  10. Department of Biology and Ecology, University of Ostrava, Ostrava, Czech Republic.
  11. Department of Bacteria, Parasites & Fungi, Statens Serum Institut, Copenhagen, Denmark.
  12. European Programme for Public Health Microbiology Training (EUPHEM), European Centre for Disease Prevention and Control (ECDC), Stockholm, Sweden.
  13. Infectious Disease Preparedness, Statens Serum Institut, Copenhagen, Denmark.
  14. Department of Chemistry and Bioscience, Aalborg University, Aalborg, Denmark.
  15. Wildlife Conservation Research Unit (WildCRU), Department of Zoology, University of Oxford, Tubney, UK.
  16. Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg, Denmark.
  17. National Food Institute, Technical University of Denmark, Kongens Lyngby, Denmark.
  18. Expert Microbiology Unit, Department of Health Security, Finnish Institute for Health and Welfare, Helsinki, Finland.
  19. Microbiology Unit, Finnish Food Authority, Helsinki, Finland.
  20. Bacteriology Department and French National Reference Center for Staphylococci, Hospices Civils de Lyon, University of Lyon, Lyon, France.
  21. Friedrich Loeffler-Institute of Medical Microbiology, University Medicine Greifswald, Greifswald, Germany.
  22. Institute of Microbiology and Epizootics, Veterinary Faculty, Freie Universität Berlin, Berlin, Germany.
  23. Advanced Light and Electron Microscopy (ZBS-4), Robert Koch Institute, Berlin, Germany.
  24. Institute for Veterinary Food Science, Justus-Liebig University Giessen, Giessen, Germany.
  25. National Reference Centre for Staphylococci and Enterococci, Division Nosocomial Pathogens and Antibiotic Resistances, Department of Infectious Diseases, Robert Koch Institute, Wernigerode, Germany.
  26. Vet Med Labor GmbH, Kornwestheim, Germany.
  27. Dipartimento di Medicina Veterinaria, Università degli Studi di Milano, Lodi, Italy.
  28. Quality Milk Production Services, Animal Health Diagnostic Center, Cornell University, Ithaca, NY, USA.
  29. Norwegian Veterinary Institute, Ås, Norway.
  30. Laboratory of Molecular Genetics, ITQB NOVA, Oeiras, Portugal.
  31. Laboratory of Microbiology and Infectious Diseases, The Rockefeller University, New York, NY, USA.
  32. Servicio de Microbiología, Hospital Universitario Lucus Augusti, Lugo, Spain.
  33. Servicio de Microbiología, Complejo Asistencial Universitario de Salamanca, Salamanca, Spain.
  34. Department of Animal Health and Antimicrobial Strategies, National Veterinary Institute (SVA), Uppsala, Sweden.
  35. Department of Microbiology, Public Health Agency of Sweden, Solna, Sweden.
  36. Institute of Veterinary Bacteriology, University of Bern, Bern, Switzerland.
  37. Department of Bacteriology, Animal and Plant Health Agency, Weybridge, UK.
  38. Animal Health Trust, Newmarket, UK.
  39. Intervacc AB, Stockholm, Stockholm, Sweden.
  40. Department of Biomedical Science and Veterinary Public Health, Swedish University of Agricultural Sciences, Uppsala, Sweden.
  41. Antimicrobial Resistance and Healthcare Associated Infections Reference Unit, UK Health Security Agency, London, UK.
  42. Clinical Microbiology and Public Health Laboratory, UK Health Security Agency, Addenbrooke's Hospital, Cambridge, UK.
  43. Department of Genetics, University of Cambridge, Cambridge, UK.
  44. Department of Medicine, University of Cambridge, Cambridge, UK.
  45. Department of Physiology, Development & Neuroscience, University of Cambridge, Cambridge, UK.
  46. Institute of Infection and Immunity, St George's, University of London, London, UK.
  47. School of Medicine, University of St Andrews, St Andrews, UK.
  48. Scottish MRSA Reference Laboratory, NHS Greater Glasgow and Clyde, Stobhill Hospital, Glasgow, UK.
  49. SRUC Veterinary Services, Inverness, UK.
  50. The Royal (Dick) School of Veterinary Studies and Roslin Institute, University of Edinburgh, Easter Bush, UK.
  51. School of Life Sciences and Department of Statistics, University of Warwick, Warwick, UK.
  52. Wellcome Sanger Institute, Hinxton, UK.
  53. Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.

PMID: 34987223 DOI: 10.1038/s41586-021-04265-w

Abstract

The discovery of antibiotics more than 80 years ago has led to considerable improvements in human and animal health. Although antibiotic resistance in environmental bacteria is ancient, resistance in human pathogens is thought to be a modern phenomenon that is driven by the clinical use of antibiotics

© 2022. The Author(s).

References

  1. Davies, J. & Davies, D. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74, 417–433 (2010). - PubMed
  2. European Centre for Disease Prevention and Control, European Medicines Agencies. The Bacterial Challenge: Time to React. A Call to Narrow the Gap Between Multidrug-Resistant Bacteria in the EU and the Development of New Antibacterial Agents https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/0909_TER_The_Bacterial_Challenge_Time_to_React.pdf (2009). - PubMed
  3. Jevons, M. P. “Celbenin”—resistant Staphylococci. Br. Med. J. 1, 124–125 (1961). - PubMed
  4. Harkins, C. P. et al. Methicillin-resistant Staphylococcus aureus emerged long before the introduction of methicillin into clinical practice. Genome Biol. 18, 130 (2017). - PubMed
  5. Chambers, H. F. & DeLeo, F. R. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 7, 629–641 (2009). - PubMed
  6. Price, L. B. et al. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 3, e00305-11 (2012). - PubMed
  7. Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics http://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf?ua=1 (WHO, 2017). - PubMed
  8. Rasmussen, S. L. et al. European hedgehogs (Erinaceus europaeus) as a natural reservoir of methicillin-resistant Staphylococcus aureus carrying mecC in Denmark. PLoS ONE 14, e0222031 (2019). - PubMed
  9. Bengtsson, B. et al. High occurrence of mecC-MRSA in wild hedgehogs (Erinaceus europaeus) in Sweden. Vet. Microbiol. 207, 103–107 (2017). - PubMed
  10. García-Álvarez, L. et al. Methicillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect. Dis. 11, 595–603 (2011). - PubMed
  11. Paterson, G. K., Harrison, E. M. & Holmes, M. A. The emergence of mecC methicillin-resistant Staphylococcus aureus. Trends Microbiol. 22, 42–47 (2014). - PubMed
  12. Marples, M. J. & Smith, J. M. B. The hedgehog as a source of human ringworm. Nature 188, 867–868 (1960). - PubMed
  13. English, M. P., Evans, C. D., Hewitt, M. & Warin, R. P. “Hedgehog ringworm”. Br. Med. J. 1, 149–151 (1962). - PubMed
  14. Smith, J. M. B. & Marples, M. J. A natural reservoir of penicillin-resistant strains of Staphylococcus aureus. Nature 201, 844 (1964). - PubMed
  15. Smith, J. M. B. & Marples, M. J. Dermatophyte lesions in the hedgehog as a reservoir of penicillin-resistant staphylococci. J. Hyg. 63, 293–303 (1965). - PubMed
  16. Smith, J. M. B. Staphylococcus aureus strains associated with the hedgehog Erinaceus europaeus. J. Hyg. Camb. 63, 293–303 (1965). - PubMed
  17. Morris, P. & English, M. P. Trichophyton mentagrophytes var. erinacei in British hedgehogs. Sabouraudia 7, 122–128 (1969). - PubMed
  18. Le Barzic, C. et al. Detection and control of dermatophytosis in wild European hedgehogs (Erinaceus europaeus) admitted to a French wildlife rehabilitation centre. J. Fungi 7, 74 (2021). - PubMed
  19. Dube, F., Söderlund, R., Salomonsson, M. L., Troell, K. & Börjesson, S. Benzylpenicillin-producing Trichophyton erinacei and methicillin resistant Staphylococcus aureus carrying the mecC gene on European hedgehogs: a pilot-study. BMC Microbiol. 21, 212 (2021). - PubMed
  20. Hewitt, G. The genetic legacy of the Quaternary ice ages. Nature 405, 907–913 (2000). - PubMed
  21. Brockie, R. E. Distribution and abundance of the hedgehog (Erinaceus europaeus) L. in New Zealand, 1869–1973. N. Z. J. Zool. 2, 445–462 (1975). - PubMed
  22. van den Berg, M. A. et al. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 26, 1161–1168 (2008). - PubMed
  23. Ullán, R. V., Campoy, S., Casqueiro, J., Fernández, F. J. & Martín, J. F. Deacetylcephalosporin C production in Penicillium chrysogenum by expression of the isopenicillin N epimerization, ring expansion, and acetylation genes. Chem. Biol. 14, 329–339 (2007). - PubMed
  24. Kitano, K. et al. A novel penicillin produced by strains of the genus Paecilomyces. J. Ferment. Technol. 54, 705–711 (1976). - PubMed
  25. Petersen, A. et al. Epidemiology of methicillin-resistant Staphylococcus aureus carrying the novel mecC gene in Denmark corroborates a zoonotic reservoir with transmission to humans. Clin. Microbiol. Infect. 19, E16–E22 (2013). - PubMed
  26. Richardson, E. J. et al. Gene exchange drives the ecological success of a multi-host bacterial pathogen. Nat. Ecol. Evol. 2, 1468–1478 (2018). - PubMed
  27. Holden, M. T. G. et al. A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic. Genome Res. 23, 653–664 (2013). - PubMed
  28. Strauß, L. et al. Origin, evolution, and global transmission of community-acquired Staphylococcus aureus ST8. Proc. Natl Acad. Sci. USA 114, E10596–E10604 (2017). - PubMed
  29. Nübel, U. et al. Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc. Natl Acad. Sci. USA 105, 14130–14135 (2008). - PubMed
  30. Rasmussen, S. L., Nielsen, J. L., Jones, O. R., Berg, T. B. & Pertoldi, C. Genetic structure of the European hedgehog (Erinaceus europaeus) in Denmark. PLoS ONE 15, e0227205 (2020). - PubMed
  31. Hansen, J. E. et al. LA-MRSA CC398 in dairy cattle and veal calf farms indicates spillover from pig production. Front. Microbiol. 10, 2733 (2019). - PubMed
  32. Eriksson, J. Espinosa-Gongora, C., Stamphøj, I., Larsen, A. R. & Guardabassi, L. Carriage frequency, diversity and methicillin resistance of in Danish small ruminants. Vet. Microbiol. 163, 110–115 (2013). - PubMed
  33. Danish Integrated Antimicrobial Resistance Monitoring and Research Programme. DANMAP 2019: Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria From Food Animals, Food, and Humans in DENMARK https://www.danmap.org/-/media/Sites/danmap/Downloads/Reports/2019/DANMAP_2019.ashx?la=da&hash=AA1939EB449203EF0684440AC1477FFCE2156BA5 (2020). - PubMed
  34. Veterinary Medicines Directorate. UK Veterinary Antibiotic Resistance and Sales Surveillance Report https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/950126/UK-VARSS_2019_Report__2020-TPaccessible.pdf (2020). - PubMed
  35. Harrison, E. M. et al. Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC. EMBO Mol. Med. 5, 509–515 (2013). - PubMed
  36. Loncaric, I. et al. Characterization of mecC gene-carrying coagulase-negative Staphylococcus spp. isolated from various animals. Vet. Microbiol. 230, 138–144 (2019). - PubMed
  37. Gómez, P. et al. Detection of MRSA ST3061-t843-mecC and ST398-t011-mecA in white stork nestlings exposed to human residues. J. Antimicrob. Chemother. 71, 53–57 (2016). - PubMed
  38. Kim, C. et al. Properties of a novel PBP2A protein homolog from Staphylococcus aureus strain LGA251 and its contribution to the β-lactam-resistant phenotype. J. Biol. Chem. 287, 36854–36863 (2012). - PubMed
  39. Tahlan, K. & Jensen, S. E. Origins of the β-lactam rings in natural products. J. Antibiot. 66, 401–419 (2013). - PubMed
  40. Pantůček, R. et al. Staphylococcus edaphicus sp. nov. isolated in Antarctica harbors the mecC gene and genomic islands with a suspected role in adaptation to extreme environment. Appl. Environ. Microbiol. 84, e01746-17 (2018). - PubMed
  41. D’Costa, V. M., et al. Antibiotic resistance is ancient. Nature 477, 457–461 (2011). - PubMed
  42. Allen, H. K., Moe, L. A., Rodbumrer, J., Gaarder, A. & Handelsman, J. Functional metagenomics reveals diverse beta-lactamases in a remote Alaskan soil. ISME J. 3, 243–251 (2009). - PubMed
  43. Forsberg, K. J. et al. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107–1111 (2012). - PubMed
  44. Forsberg, K. J. et al. Bacterial phylogeny structures soil resistomes across habitats. Nature 509, 612–616 (2014). - PubMed
  45. Coll, F. et al. Definition of a genetic relatedness cutoff to exclude recent transmission of meticillin-resistant Staphylococcus aureus: a genomic epidemiology analysis. Lancet Microbe 1, e328–e335 (2020). - PubMed
  46. Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its application to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012). - PubMed
  47. Enright, M. C., Day, N. P., Davies, C. E., Peacock, S. J., Spratt, B. G. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 38, 1008–1015 (2000). - PubMed
  48. Van Wamel, W. J., Rooijakkers, S. H., Ruyken, M. van Kessel, K. P. & Strijp, J. A. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J. Bacteriol. 188, 1310–1315 (2006). - PubMed
  49. Viana, D. et al. Adaptation of Staphylococcus aureus to ruminant and equine hosts involved SaPI-carried variants of von Willebrand factor-binding protein. Mol. Microbiol. 77, 1583–1594 (2010). - PubMed
  50. Rooijakkers, S. H. M. et al. Staphylococcal complement inhibitor: structure and active sites. J. Immunol. 179, 2989–2998 (2007). - PubMed
  51. Arndt, D. et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 44, W16–W21 (2016). - PubMed
  52. Bortolaia, V. et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J. Antimicrob. Chemother. 75, 3491–3500 (2020). - PubMed
  53. Clausen, P. T. L. C., Aarestrup, F. M. & Lund, O. Rapid and precise alignment of raw reads against redundant database with KMA. BMC Bioinform. 19, 397 (2018). - PubMed
  54. Sahl, J. W. et al. NASP: an accurate, rapid method for the identification of SNPs in WGS datasets that supports flexible input and output formats. Microb. Genom. 2, e000074 (2016). - PubMed
  55. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrow-Wheeler transform. Bioinformatics 25, 1754–1760 (2009). - PubMed
  56. McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010). - PubMed
  57. DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation sequencing data. Nat. Genet. 43, 491–498 (2011). - PubMed
  58. Delcher, A. L., Phillippy, A., Carlton, J. & Salzberg, S. L. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res. 30, 2478–2483 (2002). - PubMed
  59. Kurz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004). - PubMed
  60. Guindon, S. & Gasquel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003). - PubMed
  61. Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010). - PubMed
  62. Didelot, X. & Wilson, D. J. ClonalFrameML: efficient inference of recombination in whole bacterial genome. PLoS Comput. Biol. 11, e1004041 (2015). - PubMed
  63. Didelot, X. et al. Bayesian inference of ancestral dates on bacterial phylogenetic trees. Nucleic Acids Res. 46, e134 (2018). - PubMed
  64. Didelot, X., Siveroni, I. & Volz, E. M. Additive uncorrelated relaxed clock models for the dating of genomic epidemiology phylogenies. Mol. Biol. Evol. 38, 307–317 (2021). - PubMed
  65. Plummer, M., Best, N., Cowles, K. & Vines, K. CODA: convergence diagnosis and output analysis for MCMC. R News 6, 7–11 (2006). - PubMed
  66. Volz, E. M. & Frost, S. D. Scalable relaxed clock phylogenetic dating. Virus Evol. 3, vex025 (2017). - PubMed
  67. Wang, M. et al. Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nat. Biotechnol. 34, 828–837 (2016). - PubMed
  68. Adusumilli, R. & Mallick, P. Data conversion with ProteoWizard msConvert. Methods Mol. Biol. 1550, 339–368 (2017). - PubMed

Publication Types