Characterization of Antimicrobial and Host-Defense Peptides by NMR Spectroscopy

  • Hans J. Vogel
  • Mauricio Arias
  • James M. Aramini
  • Subrata Paul
  • Zhihong Liu
  • Hiroaki Ishida
Reference work entry


The mammalian innate immune system relies on a series of cationic antimicrobial peptides and various host-defense proteins to ward of invasions by pathogenic bacteria. NMR spectroscopy has played a dominant role in identifying the amphipathic three-dimensional structures of antimicrobial peptides and gaining an understanding of their mechanism of action. Most studies to date have relied on regular proton NMR approaches, but multidimensional NMR studies of carbon-13 and nitrogen-15 isotope-labeled peptides, as well as fluorine-19 NMR, are now commonly used as well. While the majority of the cationic antimicrobial peptides can give rise to bacterial killing by selectively perturbing the negatively charged bacterial membranes, others enter the cell and act on intracellular protein targets or nucleic acids. Some host defense proteins create ‘nutritional immunity’, by binding essential metal ions, such as iron or zinc, while others can enzymatically degrade bacterial peptidoglycan in the cell envelope. In response, several pathogenic bacteria have developed various defense mechanisms, involving the alteration of their membrane surface charge, or expression of unique proteins that can intercept antimicrobial peptides or host defense proteins. NMR spectroscopy has also played a major role in characterizing the protein-protein or protein-peptide complexes that play a role in these processes. Finally, NMR metabolomics and MRI imaging approaches have been deployed to study the mode of action of antibiotics and antimicrobial peptides in animal models and hopefully in the future these techniques can be used to determine their efficacy in human patients.


Amphipathic structures Anticancer peptides Antimicrobial peptides Host-defense peptides Innate immunity Isotope labeling NMR structures Solvent perturbation 



Research on antimicrobial peptides and host-defense proteins in the authors’ laboratory was supported by a “Novel alternatives to antibiotics” operating team grant from the Canadian Institutes for Health Research and by a CRIO grant from Alberta Innovates Health Solutions.


  1. 1.
    Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States. 2013. Available from http//
  2. 2.
    World Health Organization (WHO). Antimicrobial resistance: global report on surveillance. 2014. Available from http//
  3. 3.
    Piddock LJV. The crisis of no new antibiotics-what is the way forward? Lancet Infect Dis. 2012;12:249–53.CrossRefGoogle Scholar
  4. 4.
    Bartlett JG, Gilbert DN, Spellberg B. Seven ways to preserve the miracle of antibiotics. Clin Infect Dis. 2013;56:1445–50.CrossRefGoogle Scholar
  5. 5.
    Bax R, Green S. Antibiotics: The changing regulatory and pharmaceutical industry paradigm. J Antimicrob Chemother. 2014;70:1281–4.CrossRefGoogle Scholar
  6. 6.
    Kostyanev T, Bonten MJM, O’Brien S, Steel H, Ross S, Francois B, et al. The innovative medicines initiative’s new drugs for bad bugs programme: European public-private partnerships for the development of new strategies to tackle antibiotic resistance. J Antimicrob Chemother. 2016;71:290–5.CrossRefGoogle Scholar
  7. 7.
    Hancock REW, Sahl H-G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol. 2006;24:1551–7.CrossRefGoogle Scholar
  8. 8.
    Wang G, Li X, Wang Z. APD3: The antimicrobial peptide database as a tool for research and education. Nucleic Acids Res. 2016;44:D1087–93.CrossRefGoogle Scholar
  9. 9.
    Arnold TM, Forrest GN, Messmer KJ. Polymyxin antibiotics for gram-negative infections. Am J Heal Pharm. 2007;64:819–26.CrossRefGoogle Scholar
  10. 10.
    Baltz RH, Miao V, Wrigley SK. Natural products to drugs: daptomycin and related lipopeptide antibiotics. Nat Prod Rep. 2005;22:717–41.CrossRefGoogle Scholar
  11. 11.
    Tam JP, Wang S, Wong KH, Tan WL. Antimicrobial peptides from plants. Pharmaceuticals. 2015;8:711–57.CrossRefGoogle Scholar
  12. 12.
    Henry BGD, Sykes BD. Methods to study membrane protein structure in solution. Methods Enzymol. 1994;239:515–35.CrossRefGoogle Scholar
  13. 13.
    Ramamoorthy A. Beyond NMR spectra of antimicrobial peptides: dynamical images at atomic resolution and functional insights. Solid State Nucl Magn Reson. 2009;35:201–7.CrossRefGoogle Scholar
  14. 14.
    Koch K, Afonin S, Ieronimo M, Berditsch M, Ulrich AS. Solid-state 19F-NMR of peptides in native membranes. Top Curr Chem. 2012;306:89–118.CrossRefGoogle Scholar
  15. 15.
    Fillion M, Ouellet M, Auger M. Solid-state NMR studies of the interactions and structure of antimicrobial peptides in model membranes. In: Webb GA, editor. Modern magnetic resonance. Dordrecht: Springer; 2016. p. 1–18.Google Scholar
  16. 16.
    Bechinger B, Salnikov ES. The membrane interactions of antimicrobial peptides revealed by solid-state NMR spectroscopy. Chem Phys Lipids. 2012;165:282–301.CrossRefGoogle Scholar
  17. 17.
    Hwang PM, Vogel HJ. Structure-function relationships of antimicrobial peptides. Biochem Cell Biol. 1998;76:235–46.CrossRefGoogle Scholar
  18. 18.
    Nguyen LT, Haney EF, Vogel HJ. The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol. 2011;29:464–72.CrossRefGoogle Scholar
  19. 19.
    Pletzer D, Coleman SR, Hancock REW. Anti-biofilm peptides as a new weapon in antimicrobial warfare. Curr Opin Microbiol. 2016;33:35–40.CrossRefGoogle Scholar
  20. 20.
    Hancock REW, Haney EF, Gill EE. The immunology of host defence peptides: beyond antimicrobial activity. Nat Rev Immunol. 2016;16:321–34.CrossRefGoogle Scholar
  21. 21.
    Rautenbach M, Troskie AM, Vosloo JA. Antifungal peptides: to be or not to be membrane active. Biochimie. 2016;130:132–45.CrossRefGoogle Scholar
  22. 22.
    Arias M, Hilchie A, Haney EF, Bolscher JG, Hyndman ME, Hancock REW, et al. Anticancer activities of bovine and human lactoferricin-derived peptides. Biochem Cell Biol. 2017;95:91–8.CrossRefGoogle Scholar
  23. 23.
    Gaspar D, Salomé Veiga A, Castanho MARB. From antimicrobial to anticancer peptides. A review. Front Microbiol. 2013;4:1–16.CrossRefGoogle Scholar
  24. 24.
    Wuthrich K. NMR of proteins and nucleic acids. New York: Wiley; 1986.Google Scholar
  25. 25.
    Wishart DS, Sykes BD, Richards FM. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J Mol Biol. 1991;222:311–33.CrossRefGoogle Scholar
  26. 26.
    Cordier F, Grzesiek S. Temperature-dependence of protein hydrogen bond properties as studied by high-resolution NMR. J Mol Biol. 2002;317:739–52.CrossRefGoogle Scholar
  27. 27.
    Baxter NJ, Williamson MP. Temperature dependence of 1H chemical shifts in proteins. J Biomol NMR. 1997;9:359–69.CrossRefGoogle Scholar
  28. 28.
    Haney EF, Vogel HJ. NMR of antimicrobial peptides. In: Webb G, editor. Annual reports on NMR spectroscopy. 1st ed. New York: Academic Press; 2009. p. 1–45.Google Scholar
  29. 29.
    Nishida M, Imura Y, Yamamoto M, Kobayashi S, Yano Y, Matsuzaki K. Interaction of a magainin−PGLa hybrid peptide with membranes: insight into the mechanism of synergism. Biochemistry. 2007;46:14284–90.CrossRefGoogle Scholar
  30. 30.
    Tencza SB, Creighton DJ, Yuan T, Vogel HJ, Montelaro RC, Mietzner TA. Lentivirus-derived antimicrobial peptides: increased potency by sequence engineering and dimerization. J Antimicrob Chemother. 1999;44:33–41.CrossRefGoogle Scholar
  31. 31.
    Haney EF, Hunter HN, Matsuzaki K, Vogel HJ. Solution NMR studies of amphibian antimicrobial peptides: linking structure to function? Biochim Biophys Acta. 2009;1788:1639–55.CrossRefGoogle Scholar
  32. 32.
    Kay LE. NMR methods for the study of protein structure and dynamics. Biochem Cell Biol. 1997;75:1–15.CrossRefGoogle Scholar
  33. 33.
    Ishida H, Nguyen LT, Ramamourthy G, Aizawa T, Vogel HJ. Overexpression of antimicrobial, anticancer, and transmembrane peptides in Escherichia coli through a calmodulin-peptide fusion system. J Am Chem Soc. 2016;138:11318–26.CrossRefGoogle Scholar
  34. 34.
    Kapust RB, Tözsér J, Fox JD, Anderson DE, Cherry S, Copeland TD, et al. Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency. Protein Eng Des Sel. 2001;14:993–1000.CrossRefGoogle Scholar
  35. 35.
    Sattler M, Fesik SW. Use of deuterium labeling in NMR: overcoming a sizeable problem. Structure. 1996;4:1245–9.CrossRefGoogle Scholar
  36. 36.
    Ruschak AM, Kay LE. Methyl groups as probes of supra-molecular structure, dynamics and function. J Biomol NMR. 2009;46:75.CrossRefGoogle Scholar
  37. 37.
    Weininger U, Diehl C, Akke M. 13C relaxation experiments for aromatic side chains employing longitudinal- and transverse-relaxation optimized NMR spectroscopy. J Biomol NMR. 2012;53:181–90.CrossRefGoogle Scholar
  38. 38.
    Frueh DP, Goodrich A, Mishra S, Nichols S. NMR methods for structural studies of large monomeric and multimeric proteins. Curr Opin Struct Biol. 2013;23:734–9.CrossRefGoogle Scholar
  39. 39.
    Tugarinov V, Hwang PM, Ollerenshaw JE, Kay LE. Cross-correlated relaxation enhanced 1H−13C NMR spectroscopy of methyl groups in very high molecular weight proteins and protein complexes. J Am Chem Soc. 2003;125:10420–8.CrossRefGoogle Scholar
  40. 40.
    Tzeng S-R, Pai M-T, Kalodimos CG. NMR studies of large protein systems. In: Shekhtman A, Burz DS, editors. Protein NMR techniques. Totowa: Humana Press; 2012. p. 133–40.CrossRefGoogle Scholar
  41. 41.
    Kitevski-LeBlanc JL, Prosser RS. Current applications of 19F NMR to studies of protein structure and dynamics. Prog Nucl Magn Reson Spectrosc. 2012;62:1–33.CrossRefGoogle Scholar
  42. 42.
    Marsh ENG, Suzuki Y. Using 19F NMR to probe biological interactions of proteins and peptides. ACS Chem Biol. 2014;9:1242–50.CrossRefGoogle Scholar
  43. 43.
    Arias M, Aramini JM, Vogel HJ. Recombinant expression of fluorinated analogs of the antimicrobial peptide Tritrpticin and biophysical studies by fluorine-19 NMR. Biochim Biophys Acta (Submitted for publication).Google Scholar
  44. 44.
    Arias M, Hoffarth ER, Ishida H, Aramini JM, Vogel HJ. Recombinant expression, antimicrobial activity and mechanism of action of tritrpticin analogs containing fluoro-tryptophan residues. Biochim Biophys Acta. 2016;1858:1012–23.CrossRefGoogle Scholar
  45. 45.
    Kim HW, Perez JA, Ferguson SJ, Campbell ID. The specific incorporation of labelled aromatic amino acids into proteins through growth of bacteria in the presence of glyphosate. Application to fluorotryptophan labelling to the H(+)-ATPase of Escherichia coli and NMR studies. FEBS Lett. 1990;272:34–6.CrossRefGoogle Scholar
  46. 46.
    Tkachenko AN, Mykhailiuk PK, Afonin S, Radchenko DS, Kubyshkin VS, Ulrich AS, et al. A 19F NMR label to substitute polar amino acids in peptides: A CF3-substituted analogue of serine and threonine. Angew Chem Int Ed. 2013;52:1486–9.CrossRefGoogle Scholar
  47. 47.
    Tkachenko AN, Mykhailiuk PK, Radchenko DS, Babii O, Afonin S, Ulrich AS, et al. Design and synthesis of a monofluoro-substituted aromatic amino acid as a conformationally restricted 19F NMR label for membrane-bound peptides. Eur J Org Chem. 2014;2014:3584–91.CrossRefGoogle Scholar
  48. 48.
    Kubyshkin V, Afonin S, Kara S, Budisa N, Mykhailiuk PK, Ulrich AS. γ-(S)-Trifluoromethyl proline: evaluation as a structural substitute of proline for solid state (19)F-NMR peptide studies. Org Biomol Chem. 2015;13:3171–81.CrossRefGoogle Scholar
  49. 49.
    Michurin OM, Afonin S, Berditsch M, Daniliuc CG, Ulrich AS, Komarov IV, et al. Delivering structural information on the polar face of membrane-active peptides: 19F-NMR labels with a cationic side chain. Angew Chem Int Ed. 2016;55:14595–9.CrossRefGoogle Scholar
  50. 50.
    Luchette PA, Prosser RS, Sanders CR. Oxygen as a paramagnetic probe of membrane protein structure by cysteine mutagenesis and 19F NMR spectroscopy. J Am Chem Soc. 2002;124:1778–81.CrossRefGoogle Scholar
  51. 51.
    Prosser RS, Evanics F, Kitevski JL, Patel S. The measurement of immersion depth and topology of membrane proteins by solution state NMR. Biochim Biophys Acta. 2007;1768:3044–51.CrossRefGoogle Scholar
  52. 52.
    Fleming A. On a remarkable bacteriolytic element found in tissues and secretions. Proc R Soc Lond Ser B Contain Pap Biol. 1922;93:306–17.CrossRefGoogle Scholar
  53. 53.
    Vogel HJ. Lactoferrin, a bird’s eye view. Biochem Cell Biol. 2012;90:233–44.CrossRefGoogle Scholar
  54. 54.
    Gifford JL, Hunter HN, Vogel HJ. Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cell Mol Life Sci. 2005;62:2588–98.CrossRefGoogle Scholar
  55. 55.
    Damo SM, Kehl-Fie TE, Sugitani N, Holt ME, Rathi S, Murphy WJ, et al. Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc Natl Acad Sci. 2013;110:3841–6.CrossRefGoogle Scholar
  56. 56.
    Zackular JP, Chazin WJ, Skaar EP. Nutritional immunity: S100 proteins at the host-pathogen interface. J Biol Chem. 2015;290:18991–8.CrossRefGoogle Scholar
  57. 57.
    Torrent M, Pulido D, Valle J, Nogués MV, Andreu D, Boix E. Ribonucleases as a host-defence family: evidence of evolutionarily conserved antimicrobial activity at the N-terminus. Biochem J. 2013;456:99–108.CrossRefGoogle Scholar
  58. 58.
    Koczera P, Martin L, Marx G, Schuerholz T. The ribonuclease a superfamily in humans: canonical RNases as the buttress of innate immunity. Int J Mol Sci. 2016;17:1278.CrossRefGoogle Scholar
  59. 59.
    Yang D, Chen Q, Hoover DM, Staley P, Tucker KD, Lubkowski J, et al. Many chemokines including CCL20/MIP-3α display antimicrobial activity. J Leukoc Biol. 2003;74:448–55.CrossRefGoogle Scholar
  60. 60.
    Nguyen LT, Vogel HJ. Structural perspectives on antimicrobial chemokines. Front Immunol. 2012;3:1–11.CrossRefGoogle Scholar
  61. 61.
    Chan DI, Hunter HN, Tack BF, Vogel HJ. Human macrophage inflammatory protein 3α: protein and peptide nuclear magnetic resonance solution structures, dimerization, dynamics, and anti-infective properties. Antimicrob Agents Chemother. 2008;52:883–94.CrossRefGoogle Scholar
  62. 62.
    Schibli DJ, Hunter HN, Aseyev V, Starner TD, Wiencek JM, McCray PB, et al. The solution structures of the human β-defensins lead to a better understanding of the potent bactericidal activity of HBD3 against Staphylococcus aureus. J Biol Chem. 2002;277:8279–89.CrossRefGoogle Scholar
  63. 63.
    Kwakman PHS, Krijgsveld J, de Boer L, Nguyen LT, Boszhard L, Vreede J, et al. Native thrombocidin-1 and unfolded thrombocidin-1 exert antimicrobial activity via distinct structural elements. J Biol Chem. 2011;286:43506–14.CrossRefGoogle Scholar
  64. 64.
    Haney EF, Nathoo S, Vogel HJ, Prenner EJ. Induction of non-lamellar lipid phases by antimicrobial peptides: a potential link to mode of action. Chem Phys Lipids. 2010;163:82–93.CrossRefGoogle Scholar
  65. 65.
    Hilpert K, McLeod B, Yu J, Elliott MR, Rautenbach M, Ruden S, et al. Short cationic antimicrobial peptides interact with ATP. Antimicrob Agents Chemother. 2010;54:4480–3.CrossRefGoogle Scholar
  66. 66.
    de la Fuente-Núñez C, Reffuveille F, Haney EF, Straus SK, Hancock REW. Broad-spectrum anti-biofilm peptide that targets a cellular stress response. PLoS Pathog. 2014;10:e1004152.CrossRefGoogle Scholar
  67. 67.
    Omardien S, Brul S, Zaat SAJ. Antimicrobial activity of cationic antimicrobial peptides against gram-positives: current progress made in understanding the mode of action and the response of cacteria. Front Cell Dev Biol. 2016;4:111.CrossRefGoogle Scholar
  68. 68.
    Chung M-C, Dean SN, van Hoek ML. Acyl carrier protein is a bacterial cytoplasmic target of cationic antimicrobial peptide LL-37. Biochem J. 2015;470:243–53.CrossRefGoogle Scholar
  69. 69.
    Joo H-S, Otto M. Mechanisms of resistance to antimicrobial peptides in staphylococci. Biochim Biophys Acta Biomembr. 2015;1848:3055–61.CrossRefGoogle Scholar
  70. 70.
    Bostanci N, Belibasakis GN. Porphyromonas gingivalis: an invasive and evasive opportunistic oral pathogen. FEMS Microbiol Lett. 2012;333:1–9.CrossRefGoogle Scholar
  71. 71.
    Braff MH, Jones AL, Skerrett SJ, Rubens CE. Staphylococcus aureus exploits cathelicidin antimicrobial peptides produced during early Pneumonia to promote staphylokinase-dependent fibrinolysis. J Infect Dis. 2007;195:1365–72.CrossRefGoogle Scholar
  72. 72.
    Jin T, Bokarewa M, Foster T, Mitchell J, Higgins J, Tarkowski A. Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J Immunol. 2004;172:1169–76.CrossRefGoogle Scholar
  73. 73.
    Nguyen LT, Vogel HJ. Staphylokinase has distinct modes of interaction with antimicrobial peptides, modulating its plasminogen-activation properties. Sci Report. 2016;6:31817.CrossRefGoogle Scholar
  74. 74.
    Abergel C, Monchois V, Byrne D, Chenivesse S, Lembo F, Lazzaroni J-C, et al. Structure and evolution of the Ivy protein family, unexpected lysozyme inhibitors in Gram-negative bacteria. Proc Natl Acad Sci. 2007;104:6394–9.CrossRefGoogle Scholar
  75. 75.
    Clarke CA, Scheurwater EM, Clarke AJ. The vertebrate lysozyme inhibitor Ivy functions to inhibit the activity of lytic transglycosylase. J Biol Chem. 2010;285:14843–7.CrossRefGoogle Scholar
  76. 76.
    Derbise A, Pierre F, Merchez M, Pradel E, Laouami S, Ricard I, et al. Inheritance of the lysozyme inhibitor Ivy was an important evolutionary step by Yersinia pestis to avoid the host innate immune response. J Infect Dis. 2013;207:1535–43.CrossRefGoogle Scholar
  77. 77.
    Dostal SM, Fang Y, Guerrette JC, Scanlon TC, Griswold KE. Genetically enhanced lysozyme evades a pathogen derived inhibitory protein. ACS Chem Biol. 2015;10:1110–7.CrossRefGoogle Scholar
  78. 78.
    Liu Z, García-Díaz B, Catacchio B, Chiancone E, Vogel HJ. Protecting gram-negative bacterial cell envelopes from human lysozyme: Interactions with Ivy inhibitor proteins from Escherichia coli and Pseudomonas aeruginosa. Biochim Biophys Acta Biomembr. 2015;1848:3032–46.CrossRefGoogle Scholar
  79. 79.
    Callewaert L, Van Herreweghe JM, Vanderkelen L, Leysen S, Voet A, Michiels CW. Guards of the great wall: bacterial lysozyme inhibitors. Trends Microbiol. 2012;20:501–10.CrossRefGoogle Scholar
  80. 80.
    Lindon JC. NMR-based metabolic phenotyping techniques and applications. In: Webb GA, editor. Modern magnetic resonance. Dordrecht: Springer; 2017. p. 1–25.Google Scholar
  81. 81.
    Nagana Gowda GA, Raftery D. Can NMR solve some significant challenges in metabolomics? J Magn Reson. 2015;260:144–60.CrossRefGoogle Scholar
  82. 82.
    Mickiewicz B, Vogel HJ, Wong HR, Winston BW. Metabolomics as a novel approach for early diagnosis of pediatric septic shock and its mortality. Am J Respir Crit Care Med. 2013;187:967–76.CrossRefGoogle Scholar
  83. 83.
    Mickiewicz B, Duggan GE, Winston BW, Doig C, Kubes P, Vogel HJ, et al. Metabolic profiling of serum samples by 1H nuclear magnetic resonance spectroscopy as a potential diagnostic approach for septic shock. Crit Care Med. 2014;42:1140–9.CrossRefGoogle Scholar
  84. 84.
    Mickiewicz B, Tam P, Jenne CN, Leger C, Wong J, Winston BW, et al. Integration of metabolic and inflammatory mediator profiles as a potential prognostic approach for septic shock in the intensive care unit. Crit Care. 2015;19:11.CrossRefGoogle Scholar
  85. 85.
    Mickiewicz B, Thompson GC, Blackwood J, Jenne CN, Winston BW, Vogel HJ, et al. Development of metabolic and inflammatory mediator biomarker phenotyping for early diagnosis and triage of pediatric sepsis. Crit Care. 2015;19:320.CrossRefGoogle Scholar
  86. 86.
    Adamko DJ, Saude E, Bear M, Regush S, Robinson JL. Urine metabolomic profiling of children with respiratory tract infections in the emergency department: a pilot study. BMC Infect Dis. 2016;16:439.CrossRefGoogle Scholar
  87. 87.
    Slupsky CM, Cheypesh A, Chao DV, Fu H, Rankin KN, Marrie TJ, et al. Streptococcus pneumoniae and Staphylococcus aureus Pneumonia induce distinct metabolic responses. J Proteome Res. 2009;8:3029–36.CrossRefGoogle Scholar
  88. 88.
    Hoerr V, Zbytnuik L, Leger C, Tam PPC, Kubes P, Vogel HJ. Gram-negative and Gram-positive bacterial infections give rise to a different metabolic response in a mouse model. J Proteome Res. 2012;11:3231–45.CrossRefGoogle Scholar
  89. 89.
    Dörries K, Schlueter R, Lalk M. Impact of antibiotics with various target sites on the metabolome of Staphylococcus aureus. Antimicrob Agents Chemother. 2014;58:7151–63.CrossRefGoogle Scholar
  90. 90.
    Hoerr V, Duggan GE, Zbytnuik L, Poon KKH, Große C, Neugebauer U, et al. Characterization and prediction of the mechanism of action of antibiotics through NMR metabolomics. BMC Microbiol. 2016;16:82.CrossRefGoogle Scholar
  91. 91.
    Halouska S, Fenton RJ, Barletta RG, Powers R. Predicting the in vivo mechanism of action for drug leads using NMR metabolomics. ACS Chem Biol. 2012;7:166–71.CrossRefGoogle Scholar
  92. 92.
    Hoerr V, Hoffmann K, Schollmayer C, Holzgrabe U, Haase A, Jakob P, et al. Assessment of inhibitory potency of antibiotics by MRI: apparent T2 as a marker of cell growth. Magn Reson Mater Physics, Biol Med. 2006;19:247–55.CrossRefGoogle Scholar
  93. 93.
    Hertlein T, Sturm V, Jakob P, Ohlsen K. 19F magnetic resonance imaging of perfluorocarbons for the evaluation of response to antibiotic therapy in a Staphylococcus aureus infection model. PLoS One. 2013;8:e64440.CrossRefGoogle Scholar
  94. 94.
    Ring J, Hoerr V, Tuchscherr L, Kuhlmann MT, Löffler B, Faber C. MRI visualization of Staphyloccocus aureus-induced infective endocarditis in mice. PLoS One. 2014;9:e107179.CrossRefGoogle Scholar
  95. 95.
    Hoerr V, Faber C. Magnetic resonance imaging characterization of microbial infections. J Pharm Biomed Anal. 2014;93:136–46.CrossRefGoogle Scholar
  96. 96.
    Nevins AM, Subramanian A, Tapia JL, Delgado DP, Tyler RC, Jensen DR, et al. A requirement for metamorphic interconversion in the antimicrobial activity of chemokine XCL1. Biochemistry. 2016;55:3784–93.CrossRefGoogle Scholar
  97. 97.
    Sim S, Wang P, Beyer BN, Cutrona KJ, Radhakrishnan ML, Elmore DE. Investigating the nucleic acid interactions of histone-derived antimicrobial peptides. FEBS Lett. 2017;591:706–17.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Hans J. Vogel
    • 1
  • Mauricio Arias
    • 1
  • James M. Aramini
    • 2
  • Subrata Paul
    • 1
  • Zhihong Liu
    • 1
  • Hiroaki Ishida
    • 1
  1. 1.Bio-NMR Centre, Department of Biological SciencesUniversity of CalgaryCalgaryCanada
  2. 2.Structural Biology InitiativeCity University of New YorkNew YorkUSA

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