Measurement of Yersinia Translocon Pore Formation in Erythrocytes

  • Tiago R. D. Costa
  • Monika K. Francis
  • Salah I. Farag
  • Tomas Edgren
  • Matthew S. FrancisEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 2010)


Many Gram-negative pathogens produce a type III secretion system capable of intoxicating eukaryotic cells with immune-modulating effector proteins. Fundamental to this injection process is the prior secretion of two translocator proteins destined for injectisome translocon pore assembly within the host cell plasma membrane. It is through this pore that effectors are believed to travel to gain access to the host cell interior. Yersinia species especially pathogenic to humans and animals assemble this translocon pore utilizing two hydrophobic translocator proteins—YopB and YopD. Although a full molecular understanding of the biogenesis, function and regulation of this translocon pore and subsequent effector delivery into host cells remains elusive, some of what we know about these processes can be attributed to studies of bacterial infections of erythrocytes. Herein we describe the methodology of erythrocyte infections by Yersinia, and how analysis of the resultant contact-dependent hemolysis can serve as a relative measurement of YopB- and YopD-dependent translocon pore formation.

Key words

Contact-dependent hemolysis Type III translocon pore complex Biogenesis Function and regulation Membrane integration Effector recognition and intracellular delivery Host immune response 



This work was performed within the framework of the Umeå Centre for Microbial Research at Umeå University. MSF acknowledges financial support from the Swedish Research Council grant 2014–2105, the Medical Research Foundation of Umeå University, and the Faculty of Science and Technology at Umeå University.


  1. 1.
    Buttner D (2012) Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol Mol Biol Rev 76(2):262–310PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Deng W, Marshall NC, Rowland JL, McCoy JM, Worrall LJ, Santos AS, Strynadka NCJ, Finlay BB (2017) Assembly, structure, function and regulation of type III secretion systems. Nat Rev Microbiol 15(6):323–337. Scholar
  3. 3.
    Pallen MJ, Beatson SA, Bailey CM (2005) Bioinformatics, genomics and evolution of non-flagellar type-III secretion systems: a Darwinian perpective. FEMS Microbiol Rev 29(2):201–229PubMedCrossRefGoogle Scholar
  4. 4.
    Erhardt M, Namba K, Hughes KT (2010) Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb Perspect Biol 2(11):a000299PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Diepold A, Armitage JP (2015) Type III secretion systems: the bacterial flagellum and the injectisome. Philos Trans R Soc Lond B Biol Sci 370(1679):pii: 20150020. Scholar
  6. 6.
    Hu B, Lara-Tejero M, Kong Q, Galan JE, Liu J (2017) In situ molecular architecture of the Salmonella type III secretion machine. Cell 168(6):1065–1074.e1010. Scholar
  7. 7.
    Worrall LJ, Hong C, Vuckovic M, Deng W, Bergeron JR, Majewski DD, Huang RK, Spreter T, Finlay BB, Yu Z, Strynadka NC (2016) Near-atomic-resolution cryo-EM analysis of the Salmonella T3S injectisome basal body. Nature 540:597. Scholar
  8. 8.
    Nans A, Kudryashev M, Saibil HR, Hayward RD (2015) Structure of a bacterial type III secretion system in contact with a host membrane in situ. Nat Commun 6:10114. Scholar
  9. 9.
    Radics J, Konigsmaier L, Marlovits TC (2014) Structure of a pathogenic type 3 secretion system in action. Nat Struct Mol Biol 21(1):82–87. Scholar
  10. 10.
    Dohlich K, Zumsteg AB, Goosmann C, Kolbe M (2014) A substrate-fusion protein is trapped inside the type III secretion system channel in Shigella flexneri. PLoS Pathog 10(1):e1003881. Scholar
  11. 11.
    Akeda Y, Galan JE (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 437(7060):911–915PubMedCrossRefGoogle Scholar
  12. 12.
    Lee PC, Rietsch A (2015) Fueling type III secretion. Trends Microbiol 23(5):296–300. Scholar
  13. 13.
    Erhardt M, Mertens ME, Fabiani FD, Hughes KT (2014) ATPase-independent type-III protein secretion in Salmonella enterica. PLoS Genet 10(11):e1004800. Scholar
  14. 14.
    Wilharm G, Dittmann S, Schmid A, Heesemann J (2007) On the role of specific chaperones, the specific ATPase, and the proton motive force in type III secretion. Int J Med Microbiol 297(1):27–36PubMedCrossRefGoogle Scholar
  15. 15.
    Mahdavi A, Szychowski J, Ngo JT, Sweredoski MJ, Graham RL, Hess S, Schneewind O, Mazmanian SK, Tirrell DA (2014) Identification of secreted bacterial proteins by noncanonical amino acid tagging. Proc Natl Acad Sci U S A 111(1):433–438. Scholar
  16. 16.
    Barison N, Gupta R, Kolbe M (2013) A sophisticated multi-step secretion mechanism: how the type 3 secretion system is regulated. Cell Microbiol 15(11):1809–1817. Scholar
  17. 17.
    Dewoody RS, Merritt PM, Marketon MM (2013) Regulation of the Yersinia type III secretion system: traffic control. Front Cell Infect Microbiol 3:4PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Galan JE (2009) Common themes in the design and function of bacterial effectors. Cell Host Microbe 5(6):571–579PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Dean P (2011) Functional domains and motifs of bacterial type III effector proteins and their roles in infection. FEMS Microbiol Rev 35(6):1100–1125PubMedCrossRefGoogle Scholar
  20. 20.
    Grabowski B, Schmidt MA, Ruter C (2017) Immunomodulatory Yersinia outer proteins (Yops)-useful tools for bacteria and humans alike. Virulence 8(7):1124–1147. Scholar
  21. 21.
    Mattei PJ, Faudry E, Job V, Izore T, Attree I, Dessen A (2011) Membrane targeting and pore formation by the type III secretion system translocon. FEBS J 278(3):414–426PubMedCrossRefGoogle Scholar
  22. 22.
    Mueller CA, Broz P, Cornelis GR (2008) The type III secretion system tip complex and translocon. Mol Microbiol 68(5):1085–1095PubMedCrossRefGoogle Scholar
  23. 23.
    Tejeda-Dominguez F, Huerta-Cantillo J, Chavez-Duenas L, Navarro-Garcia F (2017) A novel mechanism for protein delivery by the type 3 secretion system for extracellularly secreted proteins. MBio 8(2):pii: e00184-17. Scholar
  24. 24.
    Akopyan K, Edgren T, Wang-Edgren H, Rosqvist R, Fahlgren A, Wolf-Watz H, Fallman M (2011) Translocation of surface-localized effectors in type III secretion. Proc Natl Acad Sci U S A 108(4):1639–1644PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Russo BC, Stamm LM, Raaben M, Kim CM, Kahoud E, Robinson LR, Bose S, Queiroz AL, Herrera BB, Baxt LA, Mor-Vaknin N, Fu Y, Molina G, Markovitz DM, Whelan SP, Goldberg MB (2016) Intermediate filaments enable pathogen docking to trigger type 3 effector translocation. Nat Microbiol 1:16025. Scholar
  26. 26.
    Armentrout EI, Rietsch A (2016) The type III secretion translocation pore senses host cell contact. PLoS Pathog 12(3):e1005530. Scholar
  27. 27.
    Ji H, Dong H (2015) Key steps in type III secretion system (T3SS) towards translocon assembly with potential sensor at plant plasma membrane. Mol Plant Pathol 16(7):762–773. Scholar
  28. 28.
    Sheahan KL, Isberg RR (2015) Identification of mammalian proteins that collaborate with type III secretion system function: involvement of a chemokine receptor in supporting translocon activity. MBio 6(1):e02023-02014. Scholar
  29. 29.
    Viala JP, Prima V, Puppo R, Agrebi R, Canestrari MJ, Lignon S, Chauvin N, Meresse S, Mignot T, Lebrun R, Bouveret E (2017) Acylation of the type 3 secretion system translocon using a dedicated acyl carrier protein. PLoS Genet 13(1):e1006556. Scholar
  30. 30.
    Dortet L, Lombardi C, Cretin F, Dessen A, Filloux A (2018) Pore-forming activity of the Pseudomonas aeruginosa type III secretion system translocon alters the host epigenome. Nat Microbiol 3(3):378–386. Scholar
  31. 31.
    Francis MS, Wolf-Watz H (1998) YopD of Yersinia pseudotuberculosis is translocated into the cytosol of HeLa epithelial cells: evidence of a structural domain necessary for translocation. Mol Microbiol 29(3):799–813PubMedCrossRefGoogle Scholar
  32. 32.
    Neyt C, Cornelis GR (1999) Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol Microbiol 33(5):971–981PubMedCrossRefGoogle Scholar
  33. 33.
    Marenne MN, Journet L, Mota LJ, Cornelis GR (2003) Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb Pathog 35(6):243–258PubMedCrossRefGoogle Scholar
  34. 34.
    Montagner C, Arquint C, Cornelis GR (2011) Translocators YopB and YopD from Yersinia form a multimeric integral membrane complex in eukaryotic cell membranes. J Bacteriol 193(24):6923–6928PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Håkansson S, Schesser K, Persson C, Galyov EE, Rosqvist R, Homble F, Wolf-Watz H (1996) The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J 15(21):5812–5823PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Tardy F, Homble F, Neyt C, Wattiez R, Cornelis GR, Ruysschaert JM, Cabiaux V (1999) Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J 18(23):6793–6799PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Håkansson S, Bergman T, Vanooteghem JC, Cornelis G, Wolf-Watz H (1993) YopB and YopD constitute a novel class of Yersinia Yop proteins. Infect Immun 61(1):71–80PubMedPubMedCentralGoogle Scholar
  38. 38.
    Mueller CA, Broz P, Muller SA, Ringler P, Erne-Brand F, Sorg I, Kuhn M, Engel A, Cornelis GR (2005) The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 310(5748):674–676PubMedCrossRefGoogle Scholar
  39. 39.
    Broz P, Mueller CA, Muller SA, Philippsen A, Sorg I, Engel A, Cornelis GR (2007) Function and molecular architecture of the Yersinia injectisome tip complex. Mol Microbiol 65(5):1311–1320PubMedCrossRefGoogle Scholar
  40. 40.
    Goure J, Broz P, Attree O, Cornelis GR, Attree I (2005) Protective anti-V antibodies inhibit Pseudomonas and Yersinia translocon assembly within host membranes. J Infect Dis 192(2):218–225PubMedCrossRefGoogle Scholar
  41. 41.
    Ligtenberg KG, Miller NC, Mitchell A, Plano GV, Schneewind O (2013) LcrV mutants that abolish Yersinia type III injectisome function. J Bacteriol 195(4):777–787. Scholar
  42. 42.
    Ekestubbe S, Broms JE, Edgren T, Fallman M, Francis MS, Forsberg A (2016) The amino-terminal part of the needle-tip translocator LcrV of Yersinia pseudotuberculosis is required for early targeting of YopH and in vivo virulence. Front Cell Infect Microbiol 6:175. Scholar
  43. 43.
    Dewoody R, Merritt PM, Marketon MM (2013) YopK controls both rate and fidelity of Yop translocation. Mol Microbiol 87(2):301–317PubMedCrossRefGoogle Scholar
  44. 44.
    Holmström A, Pettersson J, Rosqvist R, Håkansson S, Tafazoli F, Fällman M, Magnusson KE, Wolf-Watz H, Forsberg Å (1997) YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membrane. Mol Microbiol 24(1):73–91PubMedCrossRefGoogle Scholar
  45. 45.
    Thorslund SE, Edgren T, Pettersson J, Nordfelth R, Sellin ME, Ivanova E, Francis MS, Isaksson EL, Wolf-Watz H, Fallman M (2011) The RACK1 signaling scaffold protein selectively interacts with Yersinia pseudotuberculosis virulence function. PLoS One 6(2):e16784PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Dewoody R, Merritt PM, Houppert AS, Marketon MM (2011) YopK regulates the Yersinia pestis type III secretion system from within host cells. Mol Microbiol 79(6):1445–1461PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Costa TR, Edqvist PJ, Broms JE, Ahlund MK, Forsberg A, Francis MS (2010) YopD self-assembly and binding to LcrV facilitate type III secretion activity by Yersinia pseudotuberculosis. J Biol Chem 285(33):25269–25284PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Brodsky IE, Palm NW, Sadanand S, Ryndak MB, Sutterwala FS, Flavell RA, Bliska JB, Medzhitov R (2010) A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell Host Microbe 7(5):376–387PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Boyd AP, Grosdent N, Totemeyer S, Geuijen C, Bleves S, Iriarte M, Lambermont I, Octave JN, Cornelis GR (2000) Yersinia enterocolitica can deliver Yop proteins into a wide range of cell types: development of a delivery system for heterologous proteins. Eur J Cell Biol 79(10):659–671PubMedCrossRefGoogle Scholar
  50. 50.
    Durand EA, Maldonado-Arocho FJ, Castillo C, Walsh RL, Mecsas J (2010) The presence of professional phagocytes dictates the number of host cells targeted for Yop translocation during infection. Cell Microbiol 12(8):1064–1082PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Koberle M, Klein-Gunther A, Schutz M, Fritz M, Berchtold S, Tolosa E, Autenrieth IB, Bohn E (2009) Yersinia enterocolitica targets cells of the innate and adaptive immune system by injection of Yops in a mouse infection model. PLoS Pathog 5(8):e1000551PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Marketon MM, DePaolo RW, DeBord KL, Jabri B, Schneewind O (2005) Plague bacteria target immune cells during infection. Science 309(5741):1739–1741PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Ashton N (2013) Physiology of red and white blood cells. Anaesth Intens Care Med 14(6):261–266. Scholar
  54. 54.
    Gordon-Smith T (2013) Structure and function of red and white blood cells. Medicine 41(4):193–199. Scholar
  55. 55.
    Bain BJ (2017) Structure and function of red and white blood cells. Medicine 45(4):187–193. Scholar
  56. 56.
    Diez-Silva M, Dao M, Han J, Lim CT, Suresh S (2010) Shape and biomechanical characteristics of human red blood cells in health and disease. MRS Bull 35(5):382–388PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Viallat A, Abkarian M (2014) Red blood cell: from its mechanics to its motion in shear flow. Int J Lab Hematol 36(3):237–243. Scholar
  58. 58.
    SEt L (2016) Anatomy of the red cell membrane skeleton: unanswered questions. Blood 127(2):187–199. Scholar
  59. 59.
    Kaestner L, Minetti G (2017) The potential of erythrocytes as cellular aging models. Cell Death Differ 24(9):1475–1477. Scholar
  60. 60.
    Kay MM, Goodman J (2003) Immunoregulation of cellular lifespan: physiologic autoantibodies and their peptide antigens. Cell Mol Biol (Noisy-le-Grand) 49(2):217–243Google Scholar
  61. 61.
    Pretorius E, du Plooy JN, Bester J (2016) A comprehensive review on eryptosis. Cell Physiol Biochem 39(5):1977–2000. Scholar
  62. 62.
    Bernheimer AW (1988) Assay of hemolytic toxins. Methods Enzymol 165:213–217. Scholar
  63. 63.
    Rowe GE, Welch RA (1994) Assays of hemolytic toxins. Methods Enzymol 235:657–667PubMedCrossRefGoogle Scholar
  64. 64.
    Clerc P, Baudry B (1985) Sansonetti PJ (1986) Plasmid-mediated contact haemolytic activity in Shigella species: correlation with penetration into HeLa cells. Ann Inst Pasteur Microbiol 137A(3):267–278Google Scholar
  65. 65.
    Dacheux D, Goure J, Chabert J, Usson Y, Attree I (2001) Pore-forming activity of type III system-secreted proteins leads to oncosis of Pseudomonas aeruginosa-infected macrophages. Mol Microbiol 40(1):76–85PubMedCrossRefGoogle Scholar
  66. 66.
    Warawa J, Finlay BB, Kenny B (1999) Type III secretion-dependent hemolytic activity of enteropathogenic Escherichia coli. Infect Immun 67(10):5538–5540PubMedPubMedCentralGoogle Scholar
  67. 67.
    Kwuan L, Adams W, Auerbuch V (2013) Impact of host membrane pore formation by the Yersinia pseudotuberculosis type III secretion system on the macrophage innate immune response. Infect Immun 81(3):905–914. Scholar
  68. 68.
    Olsson J, Edqvist PJ, Bröms JE, Forsberg Å, Wolf-Watz H, Francis MS (2004) The YopD translocator of Yersinia pseudotuberculosis is a multifunctional protein comprised of discrete domains. J Bacteriol 186(13):4110–4123PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Costa TR, Amer AA, Farag SI, Wolf-Watz H, Fallman M, Fahlgren A, Edgren T, Francis MS (2013) Type III secretion translocon assemblies that attenuate Yersinia virulence. Cell Microbiol 15(7):1088–1110PubMedCrossRefGoogle Scholar
  70. 70.
    Holmström A, Olsson J, Cherepanov P, Maier E, Nordfelth R, Pettersson J, Benz R, Wolf-Watz H, Forsberg Å (2001) LcrV is a channel size-determining component of the Yop effector translocon of Yersinia. Mol Microbiol 39(3):620–632PubMedCrossRefGoogle Scholar
  71. 71.
    Bröms JE, Sundin C, Francis MS, Forsberg Å (2003) Comparative analysis of type III effector translocation by Yersinia pseudotuberculosis expressing native LcrV or PcrV from Pseudomonas aeruginosa. J Infect Dis 188(2):239–249PubMedCrossRefGoogle Scholar
  72. 72.
    Zwack EE, Snyder AG, Wynosky-Dolfi MA, Ruthel G, Philip NH, Marketon MM, Francis MS, Bliska JB, Brodsky IE (2015) Inflammasome activation in response to the Yersinia type III secretion system requires hyperinjection of translocon proteins YopB and YopD. MBio 6(1):e02095-02014. Scholar
  73. 73.
    Edqvist PJ, Aili M, Liu J, Francis MS (2007) Minimal YopB and YopD translocator secretion by Yersinia is sufficient for Yop-effector delivery into target cells. Microbes Infect 9(2):224–233PubMedCrossRefGoogle Scholar
  74. 74.
    Auerbuch V, Golenbock DT, Isberg RR (2009) Innate immune recognition of Yersinia pseudotuberculosis type III secretion. PLoS Pathog 5(12):e1000686. Scholar
  75. 75.
    Viboud GI, So SS, Ryndak MB, Bliska JB (2003) Proinflammatory signalling stimulated by the type III translocation factor YopB is counteracted by multiple effectors in epithelial cells infected with Yersinia pseudotuberculosis. Mol Microbiol 47(5):1305–1315PubMedCrossRefGoogle Scholar
  76. 76.
    Viboud GI, Bliska JB (2001) A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J 20(19):5373–5382PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Shaw RK, Daniell S, Frankel G, Knutton S (2002) Enteropathogenic Escherichia coli translocate Tir and form an intimin-Tir intimate attachment to red blood cell membranes. Microbiology 148(Pt 5):1355–1365PubMedCrossRefGoogle Scholar
  78. 78.
    Ciana A, Achilli C, Minetti G (2017) Spectrin and other membrane-skeletal components in human red blood cells of different age. Cell Physiol Biochem 42(3):1139–1152. Scholar
  79. 79.
    Romero M, Keyel M, Shi G, Bhattacharjee P, Roth R, Heuser JE, Keyel PA (2017) Intrinsic repair protects cells from pore-forming toxins by microvesicle shedding. Cell Death Differ 24(5):798–808. Scholar
  80. 80.
    Blocker A, Gounon P, Larquet E, Niebuhr K, Cabiaux V, Parsot C, Sansonetti P (1999) The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol 147(3):683–693PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Mejia E, Bliska JB, Viboud GI (2008) Yersinia controls type III effector delivery into host cells by modulating Rho activity. PLoS Pathog 4(1):e3. Scholar
  82. 82.
    Solomon R, Zhang W, McCrann G, Bliska JB, Viboud GI (2015) Random mutagenesis identifies a C-terminal region of YopD important for Yersinia type III secretion function. PLoS One 10(3):e0120471. Scholar
  83. 83.
    Shin H, Cornelis GR (2007) Type III secretion translocation pores of Yersinia enterocolitica trigger maturation and release of pro-inflammatory IL-1beta. Cell Microbiol 9(12):2893–2902. Scholar
  84. 84.
    Adams W, Morgan J, Kwuan L, Auerbuch V (2015) Yersinia pseudotuberculosis YopD mutants that genetically separate effector protein translocation from host membrane disruption. Mol Microbiol 96(4):764–778. Scholar
  85. 85.
    Aili M, Isaksson EL, Carlsson SE, Wolf-Watz H, Rosqvist R, Francis MS (2008) Regulation of Yersinia Yop-effector delivery by translocated YopE. Int J Med Microbiol 298(3-4):183–192PubMedCrossRefGoogle Scholar
  86. 86.
    Coleman MA, Cappuccio JA, Blanchette CD, Gao T, Arroyo ES, Hinz AK, Bourguet FA, Segelke B, Hoeprich PD, Huser T, Laurence TA, Motin VL, Chromy BA (2016) Expression and association of the Yersinia pestis translocon proteins, YopB and YopD, are facilitated by nanolipoprotein particles. PLoS One 11(3):e0150166. Scholar
  87. 87.
    Hur J, Kim K, Lee S, Park H, Park Y (2017) Melittin-induced alterations in morphology and deformability of human red blood cells using quantitative phase imaging techniques. Sci Rep 7(1):9306. Scholar
  88. 88.
    Francis MS, Amer AA, Milton DL, Costa TR (2017) Site-directed mutagenesis and its application in studying the interactions of T3S components. Methods Mol Biol 1531:11–31. Scholar
  89. 89.
    Bogdanova A, Kaestner L (2018) The red blood cells on the move! Front Physiol 9:474. Scholar
  90. 90.
    Bertani G (2004) Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J Bacteriol 186(3):595–600PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Lobo AL, Welch RA (1994) Identification and assay of RTX family of cytolysins. Methods Enzymol 235:667–678. Scholar
  92. 92.
    Shaw RK, Daniell S, Ebel F, Frankel G, Knutton S (2001) EspA filament-mediated protein translocation into red blood cells. Cell Microbiol 3(4):213–222PubMedCrossRefGoogle Scholar
  93. 93.
    Kotlarz A, Tukaj S, Krzewski K, Brycka E, Lipinska B (2013) Human Hsp40 proteins, DNAJA1 and DNAJA2, as potential targets of the immune response triggered by bacterial DnaJ in rheumatoid arthritis. Cell Stress Chaperones 18(5):653–659. Scholar
  94. 94.
    Tang Y, Romano FB, Brena M, Heuck AP (2018) The Pseudomonas aeruginosa type III secretion translocator PopB assists the insertion of the PopD translocator into host cell membranes. J Biol Chem 293:8982. Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Tiago R. D. Costa
    • 1
    • 2
    • 3
  • Monika K. Francis
    • 1
    • 2
  • Salah I. Farag
    • 1
    • 2
  • Tomas Edgren
    • 1
    • 2
    • 4
  • Matthew S. Francis
    • 1
    • 2
    Email author
  1. 1.Department of Molecular BiologyUmeå UniversityUmeåSweden
  2. 2.Umeå Centre for Microbial ResearchUmeå UniversityUmeåSweden
  3. 3.Department of Life Sciences, MRC Centre for Molecular Bacteriology and InfectionImperial CollegeLondonUK
  4. 4.Department of Medical Biochemistry and Microbiology, Uppsala Biomedical CenterUppsala UniversityUppsalaSweden

Personalised recommendations