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Annual Review of Chemical and Biomolecular Engineering

Volume 12, 2021

Phagosome–Bacteria Interactions from the Bottom Up

Abstract

When attempting to propagate infections, bacterial pathogens encounter phagocytes that encase them in vacuoles called phagosomes. Within phagosomes, bacteria are bombarded with a plethora of stresses that often lead to their demise. However, pathogens have evolved numerous strategies to counter those host defenses and facilitate survival. Given the importance of phagosome–bacteria interactions to infection outcomes, they represent a collection of targets that are of interest for next-generation antibacterials. To facilitate such therapies, different approaches can be employed to increase understanding of phagosome–bacteria interactions, and these can be classified broadly as top down (starting from intact systems and breaking down the importance of different parts) or bottom up (developing a knowledge base on simplified systems and progressively increasing complexity). Here we review knowledge of phagosomal compositions and bacterial survival tactics useful for bottom-up approaches, which are particularly relevant for the application of reaction engineering to quantify and predict the time evolution of biochemical species in these death-dealing vacuoles. Further, we highlight how understanding in this area can be built up through the combination of immunology, microbiology, and engineering.

Keyword(s): antimicrobial, antivirulence, innate immunity, macrophage, neutrophil, phagocytosis
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/content/journals/10.1146/annurev-chembioeng-090920-015024
2021-06-07
2024-04-19
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Literature Cited

  1. 1. 
    Flannagan RS, Cosio G, Grinstein S. 2009. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 7:355–66
     [Google Scholar]
  2. 2. 
    Lim JJ, Grinstein S, Roth Z. 2017. Diversity and versatility of phagocytosis: roles in innate immunity, tissue remodeling, and homeostasis. Front. . Cell. Infect. Microbiol. 7:191
     [Google Scholar]
  3. 3. 
    Rabinovitch M. 1995. Professional and non-professional phagocytes: an introduction. Trends Cell Biol 5:85–87
     [Google Scholar]
  4. 4. 
    Savina A, Amigorena S. 2007. Phagocytosis and antigen presentation in dendritic cells. Immunol. Rev. 219:143–56
     [Google Scholar]
  5. 5. 
    Sompayrac L. 2016. How the Immune System Works Chichester, UK: John Wiley & Sons
  6. 6. 
    Foote JR, Patel AA, Yona S, Segal AW. 2019. Variations in the phagosomal environment of human neutrophils and mononuclear phagocyte subsets. Front. Immunol. 10:188
     [Google Scholar]
  7. 7. 
    Levin R, Grinstein S, Canton J. 2016. The life cycle of phagosomes: formation, maturation, and resolution. Immunol. Rev. 273:156–79
     [Google Scholar]
  8. 8. 
    Haas A. 2007. The phagosome: compartment with a license to kill. Traffic 8:311–30
     [Google Scholar]
  9. 9. 
    Nordenfelt P, Tapper H. 2011. Phagosome dynamics during phagocytosis by neutrophils. J. Leukoc. Biol. 90:271–84
     [Google Scholar]
  10. 10. 
    Helaine S, Cheverton AM, Watson KG, Faure LM, Matthews SA, Holden DW. 2014. Internalization of Salmonella by macrophages induces formation of nonreplicating persisters. Science 343:204–8
     [Google Scholar]
  11. 11. 
    Stapels DAC, Hill PWS, Westermann AJ, Fisher RA, Thurston TL et al. 2018. Salmonella persisters undermine host immune defenses during antibiotic treatment. Science 362:1156–60
     [Google Scholar]
  12. 12. 
    Vazquez-Torres A, Jones-Carson J, Mastroeni P, Ischiropoulos H, Fang FC. 2000. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects on microbial killing by activated peritoneal macrophages in vitro. J. Exp. Med. 192:227–36
     [Google Scholar]
  13. 13. 
    Vazquez-Torres A, Xu Y, Jones-Carson J, Holden DW, Lucia SM et al. 2000. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287:1655–58
     [Google Scholar]
  14. 14. 
    Morales EH, Calderón IL, Collao B, Gil F, Porwollik S et al. 2012. Hypochlorous acid and hydrogen peroxide-induced negative regulation of Salmonella enterica serovar Typhimurium ompW by the response regulator ArcA. BMC Microbiol 12:63
     [Google Scholar]
  15. 15. 
    Lutz DA, Chen XM, McLaughlin BJ. 1993. Isolation of the phagocytic compartment from macrophages using a paramagnetic, particulate ligand. Anal. Biochem. 214:205–11
     [Google Scholar]
  16. 16. 
    Steinberg BE, Grinstein S. 2009. Analysis of macrophage phagocytosis: quantitative assays of phagosome formation and maturation using high-throughput fluorescence microscopy. Methods Mol. Biol. 531:45–56
     [Google Scholar]
  17. 17. 
    Hebrard M, Viala JP, Meresse S, Barras F, Aussel L. 2009. Redundant hydrogen peroxide scavengers contribute to Salmonella virulence and oxidative stress resistance. J. Bacteriol. 191:4605–14
     [Google Scholar]
  18. 18. 
    Henard CA, Bourret TJ, Song M, Vázquez-Torres A. 2010. Control of redox balance by the stringent response regulatory protein promotes antioxidant defenses of Salmonella. J. Biol. Chem. 285:36785–93
     [Google Scholar]
  19. 19. 
    Gordon S. 2016. Phagocytosis: an immunobiologic process. Immunity 44:463–75
     [Google Scholar]
  20. 20. 
    Weiss G, Schaible UE. 2015. Macrophage defense mechanisms against intracellular bacteria. Immunol. Rev. 264:182–203
     [Google Scholar]
  21. 21. 
    Pauwels A-M, Trost M, Beyaert R, Hoffmann E. 2017. Patterns, receptors, and signals: regulation of phagosome maturation. Trends Immunol 38:407–22
     [Google Scholar]
  22. 22. 
    Flannagan RS, Jaumouillé V, Grinstein S. 2012. The cell biology of phagocytosis. Annu. Rev. Pathol. Mech. Dis. 7:61–98
     [Google Scholar]
  23. 23. 
    Castellano F, Chavrier P, Caron E 2001. Actin dynamics during phagocytosis. Semin. Immunol. 13:347–55
     [Google Scholar]
  24. 24. 
    May RC, Machesky LM. 2001. Phagocytosis and the actin cytoskeleton. J. Cell Sci. 114:1061–77
     [Google Scholar]
  25. 25. 
    Netea MG, Brown GD, Kullberg BJ, Gow NA. 2008. An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 6:67–78
     [Google Scholar]
  26. 26. 
    Gutierrez MG. 2013. Functional role(s) of phagosomal Rab GTPases. Small GTPases 4:148–58
     [Google Scholar]
  27. 27. 
    Duclos S, Diez R, Garin J, Papadopoulou B, Descoteaux A et al. 2000. Rab5 regulates the kiss and run fusion between phagosomes and endosomes and the acquisition of phagosome leishmanicidal properties in RAW 264.7 macrophages. J. Cell Sci. 113:193531–41
     [Google Scholar]
  28. 28. 
    Vieira OV, Bucci C, Harrison RE, Trimble WS, Lanzetti L et al. 2003. Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase. Mol. Cell. Biol. 23:2501–14
     [Google Scholar]
  29. 29. 
    Kanai F, Liu H, Field SJ, Akbary H, Matsuo T et al. 2001. The PX domains of p47phox and p40phox bind to lipid products of PI(3)K. Nat. Cell Biol. 3:675–78
     [Google Scholar]
  30. 30. 
    Bréchard S, Plançon S, Tschirhart EJ. 2013. New insights into the regulation of neutrophil NADPH oxidase activity in the phagosome: a focus on the role of lipid and Ca2+ signaling. Antioxid. Redox Signal. 18:661–76
     [Google Scholar]
  31. 31. 
    Bagaitkar J, Barbu EA, Perez-Zapata LJ, Austin A, Huang G et al. 2017. PI(3)P-p40phox binding regulates NADPH oxidase activation in mouse macrophages and magnitude of inflammatory responses in vivo. J. Leukoc. Biol. 101:449–57
     [Google Scholar]
  32. 32. 
    Panday A, Sahoo MK, Osorio D, Batra S. 2015. NADPH oxidases: an overview from structure to innate immunity-associated pathologies. Cell. Mol. Immunol. 12:5–23
     [Google Scholar]
  33. 33. 
    Liochev SI, Fridovich I. 1999. Superoxide and iron: partners in crime. IUBMB Life 48:157–61
     [Google Scholar]
  34. 34. 
    Miller RA, Britigan BE. 1997. Role of oxidants in microbial pathophysiology. Clin. Microbiol. Rev. 10:1–18
     [Google Scholar]
  35. 35. 
    Imlay JA. 2003. Pathways of oxidative damage. Annu. Rev. Microbiol. 57:395–418
     [Google Scholar]
  36. 36. 
    Robinson JM. 2008. Reactive oxygen species in phagocytic leukocytes. Histochem. Cell Biol. 130:281–97
     [Google Scholar]
  37. 37. 
    Robinson JL, Adolfsen KJ, Brynildsen MP. 2014. Deciphering nitric oxide stress in bacteria with quantitative modeling. Curr. Opin. Microbiol. 19:16–24
     [Google Scholar]
  38. 38. 
    Shepherd VL. 1986. The role of the respiratory burst of phagocytes in host defense. Semin. Respir. Infect. 1:99–106
     [Google Scholar]
  39. 39. 
    Winterbourn CC, Hampton MB, Livesey JH, Kettle AJ. 2006. Modeling the reactions of superoxide and myeloperoxidase in the neutrophil phagosome: implications for microbial killing. J. Biol. Chem. 281:39860–69
     [Google Scholar]
  40. 40. 
    Arnold DE, Heimall JR. 2017. A review of chronic granulomatous disease. Adv. Ther. 34:2543–57
     [Google Scholar]
  41. 41. 
    Marciano BE, Spalding C, Fitzgerald A, Mann D, Brown T et al. 2015. Common severe infections in chronic granulomatous disease. Clin. Infect. Dis. 60:1176–83
     [Google Scholar]
  42. 42. 
    Kinchen JM, Ravichandran KS. 2008. Phagosome maturation: going through the acid test. Nat. Rev. Mol. Cell Biol. 9:781–95
     [Google Scholar]
  43. 43. 
    Beyenbach KW, Wieczorek H. 2006. The V-type H+ ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol. 209:577–89
     [Google Scholar]
  44. 44. 
    Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, Haddix PL, Collins HL et al. 1994. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263:678–81
     [Google Scholar]
  45. 45. 
    Huynh KK, Grinstein S. 2007. Regulation of vacuolar pH and its modulation by some microbial species. Microbiol. . Mol. Biol. Rev. 71:452–62
     [Google Scholar]
  46. 46. 
    Pethe K, Swenson DL, Alonso S, Anderson J, Wang C, Russell DG 2004. Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. PNAS 101:13642–47
     [Google Scholar]
  47. 47. 
    Ehrt S, Schnappinger D. 2009. Mycobacterial survival strategies in the phagosome: defence against host stresses. Cell Microbiol 11:1170–78
     [Google Scholar]
  48. 48. 
    Xu L, Shen X, Bryan A, Banga S, Swanson MS, Luo ZQ. 2010. Inhibition of host vacuolar H+-ATPase activity by a Legionella pneumophila effector. PLOS Pathog 6:e1000822
     [Google Scholar]
  49. 49. 
    Nevo Y, Nelson N. 2006. The NRAMP family of metal-ion transporters. Biochim. Biophys. Acta 1763:609–20
     [Google Scholar]
  50. 50. 
    Ip WK, Sokolovska A, Charriere GM, Boyer L, Dejardin S et al. 2010. Phagocytosis and phagosome acidification are required for pathogen processing and MyD88-dependent responses to Staphylococcus aureus. J. Immunol. 184:7071–81
     [Google Scholar]
  51. 51. 
    DeCoursey TE. 2010. Voltage-gated proton channels find their dream job managing the respiratory burst in phagocytes. Physiology 25:27–40
     [Google Scholar]
  52. 52. 
    Bogdan C. 2001. Nitric oxide and the immune response. Nat. Immunol. 2:907–16
     [Google Scholar]
  53. 53. 
    Lowenstein CJ, Padalko E. 2004. iNOS (NOS2) at a glance. J. Cell Sci. 117:2865–67
     [Google Scholar]
  54. 54. 
    Fang FC. 2004. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2:820–32
     [Google Scholar]
  55. 55. 
    Webb JL, Harvey MW, Holden DW, Evans TJ. 2001. Macrophage nitric oxide synthase associates with cortical actin but is not recruited to phagosomes. Infect. Immun. 69:6391–400
     [Google Scholar]
  56. 56. 
    Thomas DD, Ridnour LA, Isenberg JS, Flores-Santana W, Switzer CH et al. 2008. The chemical biology of nitric oxide: implications in cellular signaling. Free Radic. . Biol. Med. 45:18–31
     [Google Scholar]
  57. 57. 
    Radi R. 2018. Oxygen radicals, nitric oxide, and peroxynitrite: redox pathways in molecular medicine. PNAS 115:5839–48
     [Google Scholar]
  58. 58. 
    Reiter TA. 2006. NO* chemistry: a diversity of targets in the cell. Redox Rep 11:194–206
     [Google Scholar]
  59. 59. 
    Bowman LA, McLean S, Poole RK, Fukuto JM. 2011. The diversity of microbial responses to nitric oxide and agents of nitrosative stress: close cousins but not identical twins. Adv. Microb. Physiol. 59:135–219
     [Google Scholar]
  60. 60. 
    Vandal OH, Nathan CF, Ehrt S. 2009. Acid resistance in Mycobacterium tuberculosis. J. Bacteriol. 191:4714–21
     [Google Scholar]
  61. 61. 
    Appelberg R. 2006. Macrophage nutriprive antimicrobial mechanisms. J. Leukoc. Biol. 79:1117–28
     [Google Scholar]
  62. 62. 
    Soares MP, Hamza I. 2016. Macrophages and iron metabolism. Immunity 44:492–504
     [Google Scholar]
  63. 63. 
    Hood MI, Skaar EP. 2012. Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10:525–37
     [Google Scholar]
  64. 64. 
    Palmer LD, Skaar EP. 2016. Transition metals and virulence in bacteria. Annu. Rev. Genet. 50:67–91
     [Google Scholar]
  65. 65. 
    Forbes JR, Gros P. 2001. Divalent-metal transport by NRAMP proteins at the interface of host-pathogen interactions. Trends Microbiol 9:397–403
     [Google Scholar]
  66. 66. 
    White C, Yuan X, Schmidt PJ, Bresciani E, Samuel TK et al. 2013. HRG1 is essential for heme transport from the phagolysosome of macrophages during erythrophagocytosis. Cell Metab 17:261–70
     [Google Scholar]
  67. 67. 
    Knutson MD, Oukka M, Koss LM, Aydemir F, Wessling-Resnick M 2005. Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin. PNAS 102:1324–28
     [Google Scholar]
  68. 68. 
    Soares MP, Weiss G. 2015. The Iron age of host-microbe interactions. EMBO Rep 16:1482–500
     [Google Scholar]
  69. 69. 
    Kehl-Fie TE, Skaar EP 2010. Nutritional immunity beyond iron: a role for manganese and zinc. Curr. Opin. Chem. Biol. 14:218–24
     [Google Scholar]
  70. 70. 
    Ladomersky E, Petris MJ. 2015. Copper tolerance and virulence in bacteria. Metallomics 7:957–64
     [Google Scholar]
  71. 71. 
    Fields PI, Swanson RV, Haidaris CG, Heffron F 1986. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. PNAS 83:5189–93
     [Google Scholar]
  72. 72. 
    Leung KY, Finlay BB 1991. Intracellular replication is essential for the virulence of Salmonella typhimurium. PNAS 88:11470–74
     [Google Scholar]
  73. 73. 
    Klose KE, Mekalanos JJ. 1997. Simultaneous prevention of glutamine synthesis and high-affinity transport attenuates Salmonella typhimurium virulence. Infect. Immun. 65:587–96
     [Google Scholar]
  74. 74. 
    Hondalus MK, Bardarov S, Russell R, Chan J, Jacobs WR, Bloom BR. 2000. Attenuation of and protection induced by a leucine auxotroph of Mycobacterium tuberculosis. Infect. Immun. 68:2888–98
     [Google Scholar]
  75. 75. 
    Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA et al. 2003. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J. Exp. Med. 198:693–704
     [Google Scholar]
  76. 76. 
    McKinney JD, Höner zu Bentrup K, Muñoz-Elías EJ, Miczak A, Chen B et al. 2000. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406:735–38
     [Google Scholar]
  77. 77. 
    Uribe-Querol E, Rosales C. 2017. Control of phagocytosis by microbial pathogens. Front. Immunol. 8:1368
     [Google Scholar]
  78. 78. 
    Schröder BA, Wrocklage C, Hasilik A, Saftig P. 2010. The proteome of lysosomes. Proteomics 10:4053–76
     [Google Scholar]
  79. 79. 
    Ragland SA, Criss AK. 2017. From bacterial killing to immune modulation: recent insights into the functions of lysozyme. PLOS Pathog 13:e1006512
     [Google Scholar]
  80. 80. 
    Yount NY, Yeaman MR. 2013. Peptide antimicrobials: cell wall as a bacterial target. Ann. N.Y. Acad. Sci. 1277:127–38
     [Google Scholar]
  81. 81. 
    Zhang LJ, Gallo RL. 2016. Antimicrobial peptides. Curr. Biol. 26:R14–19
     [Google Scholar]
  82. 82. 
    Ganz T. 2003. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3:710–20
     [Google Scholar]
  83. 83. 
    Delamarre L, Pack M, Chang H, Mellman I, Trombetta ES. 2005. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307:1630–34
     [Google Scholar]
  84. 84. 
    Lennon-Duménil AM, Bakker AH, Maehr R, Fiebiger E, Overkleeft HS et al. 2002. Analysis of protease activity in live antigen-presenting cells shows regulation of the phagosomal proteolytic contents during dendritic cell activation. J. Exp. Med. 196:529–40
     [Google Scholar]
  85. 85. 
    Segal AW, Dorling J, Coade S. 1980. Kinetics of fusion of the cytoplasmic granules with phagocytic vacuoles in human polymorphonuclear leukocytes. Biochemical and morphological studies. J. Cell Biol. 85:42–59
     [Google Scholar]
  86. 86. 
    Paul D, Achouri S, Yoon Y-Z, Herre J, Bryant CE, Cicuta P. 2013. Phagocytosis dynamics depends on target shape. Biophys. J. 105:1143–50
     [Google Scholar]
  87. 87. 
    Lee WL, Harrison RE, Grinstein S. 2003. Phagocytosis by neutrophils. Microbes Infect 5:1299–306
     [Google Scholar]
  88. 88. 
    Tapper H, Grinstein S. 1997. Fc receptor-triggered insertion of secretory granules into the plasma membrane of human neutrophils: selective retrieval during phagocytosis. J. Immunol. 159:409–18
     [Google Scholar]
  89. 89. 
    Borregaard N, Lollike K, Kjeldsen L, Sengeløv H, Bastholm L et al. 1993. Human neutrophil granules and secretory vesicles. Eur. J. Haematol. 51:187–98
     [Google Scholar]
  90. 90. 
    Oren A, Taylor JM 1995. The subcellular localization of defensins and myeloperoxidase in human neutrophils: immunocytochemical evidence for azurophil granule heterogeneity. J. Lab. Clin. Med. 125:340–47
     [Google Scholar]
  91. 91. 
    Karlsson A, Dahlgren C. 2002. Assembly and activation of the neutrophil NADPH oxidase in granule membranes. Antioxid. Redox Signal. 4:49–60
     [Google Scholar]
  92. 92. 
    Nguyen GT, Green ER, Mecsas J. 2017. Neutrophils to the ROScue: mechanisms of NADPH oxidase activation and bacterial resistance. Front. Cell Infect. Microbiol. 7:373
     [Google Scholar]
  93. 93. 
    Kaufmann SHE, Dorhoi A. 2016. Molecular determinants in phagocyte-bacteria interactions. Immunity 44:476–91
     [Google Scholar]
  94. 94. 
    Thi EP, Lambertz U, Reiner NE. 2012. Sleeping with the enemy: how intracellular pathogens cope with a macrophage lifestyle. PLOS Pathog 8:e1002551
     [Google Scholar]
  95. 95. 
    Smith EJ, Visai L, Kerrigan SW, Speziale P, Foster TJ. 2011. The Sbi protein is a multifunctional immune evasion factor of Staphylococcus aureus. Infect. Immun. 79:3801–9
     [Google Scholar]
  96. 96. 
    Kobayashi SD, DeLeo FR. 2013.. Staphylococcus aureus protein A promotes immune suppression. mBio 4:e00764–13
     [Google Scholar]
  97. 97. 
    Ko YP, Kuipers A, Freitag CM, Jongerius I, Medina E et al. 2013. Phagocytosis escape by a Staphylococcus aureus protein that connects complement and coagulation proteins at the bacterial surface. PLOS Pathog 9:e1003816
     [Google Scholar]
  98. 98. 
    Spaan AN, van Strijp JAG, Torres VJ. 2017. Leukocidins: staphylococcal bi-component pore-forming toxins find their receptors. Nat. Rev. Microbiol. 15:435–47
     [Google Scholar]
  99. 99. 
    Alonzo F, Torres VJ. 2014. The bicomponent pore-forming leucocidins of Staphylococcus aureus. Microbiol. . Mol. Biol. Rev. 78:199–230
     [Google Scholar]
  100. 100. 
    Mao Y, Finnemann SC. 2015. Regulation of phagocytosis by Rho GTPases. Small GTPases 6:89–99
     [Google Scholar]
  101. 101. 
    Jank T, Giesemann T, Aktories K. 2007. Rho-glucosylating Clostridium difficile toxins A and B: new insights into structure and function. Glycobiology 17:15R–22R
     [Google Scholar]
  102. 102. 
    Krall R, Sun J, Pederson KJ, Barbieri JT. 2002. In vivo rho GTPase-activating protein activity of Pseudomonas aeruginosa cytotoxin ExoS. Infect. Immun. 70:360–67
     [Google Scholar]
  103. 103. 
    Singaravelu P, Lee WL, Wee S, Ghoshdastider U, Ding K et al. 2017. Yersinia effector protein (YopO)-mediated phosphorylation of host gelsolin causes calcium-independent activation leading to disruption of actin dynamics. J. Biol. Chem. 292:8092–100
     [Google Scholar]
  104. 104. 
    Haas A. 1998. Reprogramming the phagocytic pathway—intracellular pathogens and their vacuoles (review). Mol. Membr. Biol. 15:103–21
     [Google Scholar]
  105. 105. 
    Wong D, Bach H, Sun J, Hmama Z, Av-Gay Y 2011. Mycobacterium tuberculosis protein tyrosine phosphatase (PtpA) excludes host vacuolar-H+-ATPase to inhibit phagosome acidification. PNAS 108:19371–76
     [Google Scholar]
  106. 106. 
    Binker MG, Cosen-Binker LI, Terebiznik MR, Mallo GV, McCaw SE et al. 2007. Arrested maturation of Neisseria-containing phagosomes in the absence of the lysosome-associated membrane proteins, LAMP-1 and LAMP-2. Cell Microbiol 9:2153–66
     [Google Scholar]
  107. 107. 
    Hertzén E, Johansson L, Wallin R, Schmidt H, Kroll M et al. 2010. M1 protein-dependent intracellular trafficking promotes persistence and replication of Streptococcus pyogenes in macrophages. J. Innate Immun. 2:534–45
     [Google Scholar]
  108. 108. 
    Chou WK, Brynildsen MP. 2016. A biochemical engineering view of the quest for immune-potentiating anti-infectives. Curr. Opin. Chem. Eng. 14:82–92
     [Google Scholar]
  109. 109. 
    De Groote MA, Ochsner UA, Shiloh MU, Nathan C, McCord JM et al. 1997. Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. PNAS 94:13997–4001
     [Google Scholar]
  110. 110. 
    Poole RK, Hughes MN. 2000. New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol. Microbiol. 36:775–83
     [Google Scholar]
  111. 111. 
    Gardner PR. 2005. Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J. Inorg. Biochem. 99:247–66
     [Google Scholar]
  112. 112. 
    Stevanin TM, Poole RK, Demoncheaux EAG, Read RC. 2002. Flavohemoglobin Hmp protects Salmonella enterica serovar Typhimurium from nitric oxide-related killing by human macrophages. Infect. Immun. 70:4399–405
     [Google Scholar]
  113. 113. 
    Shiro Y. 2012. Structure and function of bacterial nitric oxide reductases: nitric oxide reductase, anaerobic enzymes. Biochim. Biophys. Acta 1817:1907–13
     [Google Scholar]
  114. 114. 
    Zumft WG. 2005. Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme-copper oxidase type. J. Inorg. Biochem. 99:194–215
     [Google Scholar]
  115. 115. 
    Hendriks J, Oubrie A, Castresana J, Urbani A, Gemeinhardt S, Saraste M. 2000. Nitric oxide reductases in bacteria. Biochim. Biophys. Acta 1459:266–73
     [Google Scholar]
  116. 116. 
    Nguyen Y, Sperandio V. 2012. Enterohemorrhagic E. coli (EHEC) pathogenesis. Front. . Cell Infect. Microbiol. 2:90
     [Google Scholar]
  117. 117. 
    Shimizu T, Tsutsuki H, Matsumoto A, Nakaya H, Noda M. 2012. The nitric oxide reductase of enterohaemorrhagic Escherichia coli plays an important role for the survival within macrophages. Mol. Microbiol. 85:492–512
     [Google Scholar]
  118. 118. 
    Beasley FC, Vinés ED, Grigg JC, Zheng Q, Liu S et al. 2009. Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Mol. Microbiol. 72:947–63
     [Google Scholar]
  119. 119. 
    Cheung J, Beasley FC, Liu S, Lajoie GA, Heinrichs DE. 2009. Molecular characterization of staphyloferrin B biosynthesis in Staphylococcus aureus. Mol. Microbiol. 74:594–608
     [Google Scholar]
  120. 120. 
    Sritharan M. 2016. Iron homeostasis in Mycobacterium tuberculosis: mechanistic insights into siderophore-mediated iron uptake. J. Bacteriol. 198:2399–409
     [Google Scholar]
  121. 121. 
    Zaharik ML, Cullen VL, Fung AM, Libby SJ, Kujat Choy SL et al. 2004. The Salmonella enterica serovar Typhimurium divalent cation transport systems MntH and SitABCD are essential for virulence in an Nramp1G169 murine typhoid model. Infect. Immun. 72:5522–25
     [Google Scholar]
  122. 122. 
    Kim S, Watanabe K, Shirahata T, Watarai M. 2004. Zinc uptake system (znuA locus) of Brucella abortus is essential for intracellular survival and virulence in mice. J. Vet. Med. Sci. 66:1059–63
     [Google Scholar]
  123. 123. 
    Osman D, Waldron KJ, Denton H, Taylor CM, Grant AJ et al. 2010. Copper homeostasis in Salmonella is atypical and copper-CueP is a major periplasmic metal complex. J. Biol. Chem. 285:25259–68
     [Google Scholar]
  124. 124. 
    Joo H-S, Fu C-I, Otto M 2016. Bacterial strategies of resistance to antimicrobial peptides. Philos. Trans. R. Soc. B Biol. Sci. 371:20150292
     [Google Scholar]
  125. 125. 
    Cole JN, Nizet V. 2016. Bacterial evasion of host antimicrobial peptide defenses. Microbiol. Spectr 4: https://doi.org/10.1128/microbiolspec.VMBF-0006-2015
    [Crossref] [Google Scholar]
  126. 126. 
    Stumpe S, Schmid R, Stephens DL, Georgiou G, Bakker EP. 1998. Identification of OmpT as the protease that hydrolyzes the antimicrobial peptide protamine before it enters growing cells of Escherichia coli. J. Bacteriol. 180:4002–6
     [Google Scholar]
  127. 127. 
    Guina T, Yi EC, Wang H, Hackett M, Miller SI. 2000. A PhoP-regulated outer membrane protease of Salmonella enterica serovar Typhimurium promotes resistance to alpha-helical antimicrobial peptides. J. Bacteriol. 182:4077–86
     [Google Scholar]
  128. 128. 
    Galván EM, Lasaro MA, Schifferli DM. 2008. Capsular antigen fraction 1 and Pla modulate the susceptibility of Yersinia pestis to pulmonary antimicrobial peptides such as cathelicidin. Infect. Immun. 76:1456–64
     [Google Scholar]
  129. 129. 
    Wang X, Preston JF, Romeo T. 2004. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J. Bacteriol. 186:2724–34
     [Google Scholar]
  130. 130. 
    Vuong C, Voyich JM, Fischer ER, Braughton KR, Whitney AR et al. 2004. Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell Microbiol 6:269–75
     [Google Scholar]
  131. 131. 
    Münch D, Sahl HG. 2015. Structural variations of the cell wall precursor lipid II in Gram-positive bacteria—impact on binding and efficacy of antimicrobial peptides. Biochim. Biophys. Acta 1848:3062–71
     [Google Scholar]
  132. 132. 
    Malanovic N, Lohner K. 2016. Antimicrobial peptides targeting Gram-positive bacteria. Pharmaceuticals 9:59
     [Google Scholar]
  133. 133. 
    Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, Götz F 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274:8405–10
     [Google Scholar]
  134. 134. 
    Fernando DM, Kumar A. 2013. Resistance-nodulation-division multidrug efflux pumps in Gram-negative bacteria: role in virulence. Antibiotics 2:163–81
     [Google Scholar]
  135. 135. 
    Shafer WM, Qu X, Waring AJ, Lehrer RI 1998. Modulation of Neisseria gonorrhoeae susceptibility to vertebrate antibacterial peptides due to a member of the resistance/nodulation/division efflux pump family. PNAS 95:1829–33
     [Google Scholar]
  136. 136. 
    Padilla E, Llobet E, Doménech-Sánchez A, Martínez-Martínez L, Bengoechea JA, Albertí S 2010. Klebsiella pneumoniae AcrAB efflux pump contributes to antimicrobial resistance and virulence. Antimicrob. Agents Chemother. 54:177–83
     [Google Scholar]
  137. 137. 
    Hurst JK. 2012. What really happens in the neutrophil phagosome? Free Radic. . Biol. Med. 53:508–20
     [Google Scholar]
  138. 138. 
    Mosser DM, Edwards JP. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8:958–69
     [Google Scholar]
  139. 139. 
    Anjem A, Imlay JA. 2012. Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. J. Biol. Chem. 287:15544–56
     [Google Scholar]
  140. 140. 
    Mishra S, Imlay JA. 2013. An anaerobic bacterium, Bacteroides thetaiotaomicron, uses a consortium of enzymes to scavenge hydrogen peroxide. Mol. Microbiol. 90:1356–71
     [Google Scholar]
  141. 141. 
    VanderWal AR, Makthal N, Pinochet-Barros A, Helmann JD, Olsen RJ, Kumaraswami M. 2017. Iron efflux by PmtA is critical for oxidative stress resistance and contributes significantly to group A Streptococcus virulence. Infect. Immun. 85:e00091–17
     [Google Scholar]
  142. 142. 
    Adolfsen KJ, Brynildsen MP. 2015. A kinetic platform to determine the fate of hydrogen peroxide in Escherichia coli. PLOS Comput. Biol. 11:e1004562
     [Google Scholar]
  143. 143. 
    Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, Storz G. 2001. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183:4562–70
     [Google Scholar]
  144. 144. 
    Staudinger BJ, Oberdoerster MA, Lewis PJ, Rosen H. 2002. mRNA expression profiles for Escherichia coli ingested by normal and phagocyte oxidase-deficient human neutrophils. J. Clin. Investig. 110:1151–63
     [Google Scholar]
  145. 145. 
    Ricci S, Janulczyk R, Björck L. 2002. The regulator PerR is involved in oxidative stress response and iron homeostasis and is necessary for full virulence of Streptococcus pyogenes. Infect. Immun. 70:4968–76
     [Google Scholar]
  146. 146. 
    Gryllos I, Grifantini R, Colaprico A, Cary ME, Hakansson A et al. 2008. PerR confers phagocytic killing resistance and allows pharyngeal colonization by group A Streptococcus. PLOS Pathog 4:e1000145
     [Google Scholar]
  147. 147. 
    Vandal OH, Pierini LM, Schnappinger D, Nathan CF, Ehrt S. 2008. A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat. Med. 14:849–54
     [Google Scholar]
  148. 148. 
    Raynaud C, Papavinasasundaram KG, Speight RA, Springer B, Sander P et al. 2002. The functions of OmpATb, a pore-forming protein of Mycobacterium tuberculosis. Mol. Microbiol. 46:191–201
     [Google Scholar]
  149. 149. 
    Gardner AM, Gardner PR. 2002. Flavohemoglobin detoxifies nitric oxide in aerobic, but not anaerobic, Escherichia coli. Evidence for a novel inducible anaerobic nitric oxide-scavenging activity. J. Biol. Chem. 277:8166–71
     [Google Scholar]
  150. 150. 
    Bang I-S, Liu L, Vazquez-Torres A, Crouch M-L, Stamler JS, Fang FC. 2006. Maintenance of nitric oxide and redox homeostasis by the Salmonella flavohemoglobin Hmp. J. Biol. Chem. 281:28039–47
     [Google Scholar]
  151. 151. 
    Kakishima K, Shiratsuchi A, Taoka A, Nakanishi Y, Fukumori Y. 2007. Participation of nitric oxide reductase in survival of Pseudomonas aeruginosa in LPS-activated macrophages. Biochem. Biophys. Res. Commun. 355:587–91
     [Google Scholar]
  152. 152. 
    Harrington JC, Wong SM, Rosadini CV, Garifulin O, Boyartchuk V, Akerley BJ. 2009. Resistance of Haemophilus influenzae to reactive nitrogen donors and gamma interferon-stimulated macrophages requires the formate-dependent nitrite reductase regulator-activated ytfE gene. Infect. Immun. 77:1945–58
     [Google Scholar]
  153. 153. 
    Henard CA, Vázquez-Torres A. 2012. DksA-dependent resistance of Salmonella enterica serovar Typhimurium against the antimicrobial activity of inducible nitric oxide synthase. Infect. Immun. 80:1373–80
     [Google Scholar]
  154. 154. 
    Chou WK, Brynildsen MP. 2019. Loss of DksA leads to multi-faceted impairment of nitric oxide detoxification by Escherichia coli. Free Radic. . Biol. Med. 130:288–96
     [Google Scholar]
  155. 155. 
    Pope CD, O'Connell W, Cianciotto NP. 1996. Legionella pneumophila mutants that are defective for iron acquisition and assimilation and intracellular infection. Infect. Immunity 64:629–36
     [Google Scholar]
  156. 156. 
    De Voss JJ, Rutter K, Schroeder BG, Su H, Zhu Y, Barry CE 2000. The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. PNAS 97:1252–57
     [Google Scholar]
  157. 157. 
    Kristian SA, Dürr M, Van Strijp JA, Neumeister B, Peschel A. 2003. MprF-mediated lysinylation of phospholipids in Staphylococcus aureus leads to protection against oxygen-independent neutrophil killing. Infect. Immun. 71:546–49
     [Google Scholar]
  158. 158. 
    Poyart C, Pellegrini E, Marceau M, Baptista M, Jaubert F et al. 2003. Attenuated virulence of Streptococcus agalactiae deficient in D-alanyl-lipoteichoic acid is due to an increased susceptibility to defensins and phagocytic cells. Mol. Microbiol. 49:1615–25
     [Google Scholar]
  159. 159. 
    Jackett PS, Aber VR, Lowrie DB. 1978. Virulence and resistance to superoxide, low pH and hydrogen peroxide among strains of Mycobacterium tuberculosis. J. Gen. Microbiol. 104:37–45
     [Google Scholar]
  160. 160. 
    Brener D, DeVoe IW, Holbein BE. 1981. Increased virulence of Neisseria meningitidis after in vitro iron-limited growth at low pH. Infect. Immun. 33:59–66
     [Google Scholar]
  161. 161. 
    Adolfsen KJ, Chou WK, Brynildsen MP. 2019. Transcriptional regulation contributes to prioritized detoxification of hydrogen peroxide over nitric oxide. J. Bacteriol. 201:e00081–19
     [Google Scholar]
  162. 162. 
    Yadav R, Samuni Y, Abramson A, Zeltser R, Casap N et al. 2014. Pro-oxidative synergic bactericidal effect of NO: kinetics and inhibition by nitroxides. Free Radic. . Biol. Med. 67:248–54
     [Google Scholar]
  163. 163. 
    Gusarov I, Nudler E 2005. NO-mediated cytoprotection: instant adaptation to oxidative stress in bacteria. PNAS 102:13855–60
     [Google Scholar]
  164. 164. 
    Gold B, Warrier T, Nathan C. 2015. A multi-stress model for high throughput screening against non-replicating Mycobacterium tuberculosis. Methods Mol. Biol. 1285:293–315
     [Google Scholar]
  165. 165. 
    Gold B, Pingle M, Brickner SJ, Shah N, Roberts J et al. 2012. Nonsteroidal anti-inflammatory drug sensitizes Mycobacterium tuberculosis to endogenous and exogenous antimicrobials. PNAS 109:16004–11
     [Google Scholar]
  166. 166. 
    Zheng P, Somersan-Karakaya S, Lu S, Roberts J, Pingle M et al. 2014. Synthetic calanolides with bactericidal activity against replicating and nonreplicating Mycobacterium tuberculosis. J. Med. Chem. 57:3755–72
     [Google Scholar]
  167. 167. 
    Robinson JL, Brynildsen MP. 2013. A kinetic platform to determine the fate of nitric oxide in Escherichia coli. PLOS Comput. Biol. 9:e1003049
     [Google Scholar]
  168. 168. 
    Robinson JL, Miller RV, Brynildsen MP. 2014. Model-driven identification of dosing regimens that maximize the antimicrobial activity of nitric oxide. Metab. Eng. Commun. 1:12–18
     [Google Scholar]
  169. 169. 
    Robinson JL, Brynildsen MP. 2015. An ensemble-guided approach identifies ClpP as a major regulator of transcript levels in nitric oxide-stressed Escherichia coli. Metab. Eng. 31:22–34
     [Google Scholar]
  170. 170. 
    Robinson JL, Brynildsen MP 2016. Discovery and dissection of metabolic oscillations in the microaerobic nitric oxide response network of Escherichia coli. . PNAS 113:E1757–66
     [Google Scholar]
  171. 171. 
    Sivaloganathan DM, Brynildsen MP. 2020. Quantitative modeling extends the antibacterial activity of nitric oxide. Front. Physiol. 11:330
     [Google Scholar]
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Phagosome–Bacteria Interactions from the Bottom Up
Annual Review of Chemical and Biomolecular Engineering 12, 309 (2021); https://doi.org/10.1146/annurev-chembioeng-090920-015024
/content/journals/10.1146/annurev-chembioeng-090920-015024
/content/journals/10.1146/annurev-chembioeng-090920-015024
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