Mass spectrometry-based proteomic approaches to study pathogenic bacteria-host interactions

Abstract

Elucidation of molecular mechanisms underlying hostpathogen interactions is important for control and treatment of infectious diseases worldwide. Within the last decade, mass spectrometry (MS)-based proteomics has become a powerful and effective approach to better understand complex and dynamic host-pathogen interactions at the protein level. Herein we will review the recent progress in proteomic analyses towards bacterial infection of their mammalian host with a particular focus on enteric pathogens. Large-scale studies of dynamic proteomic alterations during infection will be discussed from the perspective of both pathogenic bacteria and host cells.

Key words： mass spectrometry; proteomics; bacterial infection; host-pathogen interactions

References

1 Adkins JN, Mottaz HM, Norbeck AD, Gustin JK, Rue J, Clauss TRW, Purvine SO, Rodland KD, Heffron F, Smith RD (2006) Analysis of the Salmonella Typhimurium proteome through environmental response toward infectious conditions. Mol Cell Proteomics5: 1450-1461

2 Albrethsen J, Agner J, Piersma SR, Hojrup P, Pham TV, Weldingh K, Jimenez CR, Andersen P, Rosenkrands I (2013) Proteomic profiling of Mycobacterium tuberculosis identifies nutrient-starvation-responsive toxin-antitoxin systems. Mol Cell Proteomics12: 1180-1191

3 Ansong C, Yoon H, Norbeck AD, Gustin JK, McDermott JE, Mottaz HM, Rue J, Adkins JN, Heffron F, Smith RD (2008) Proteomics analysis of the causative agent of typhoid fever. J Proteome Res7: 546-557

4 Ansong C, Yoon H, Porwollik S, Mottaz-Brewer H, Petritis BO, Jaitly N, Adkins JN, McClelland M, Heffron F, Smith RD (2009) Global systems-level analysis of Hfq and SmpB deletion mutants in Salmonella: implications for virulence and global protein translation. PLoS One4: e4809

5 Becker D, Selbach M, Rollenhagen C, Ballmaier M, Meyer TF, Mann M, Bumann D (2006) Robust Salmonella metabolism limits possibilities for new antimicrobials. Nature440: 303-307

6 Brown RN, Sanford JA, Park JH, Deatherage BL, Champion BL, Smith RD, Heffron F, Adkins JN (2012) A comprehensive subcellular proteomic survey of Salmonella grown under phagosome-mimicking versus standard laboratory conditions. Int J Proteomics2012: 123076

7 Bumann D (2009) System-level analysis of Salmonella metabolism during infection. Curr Opin Microbiol12: 559-567

8 Cash P (2011) Investigating pathogen biology at the level of the proteome. Proteomics11: 3190-3202

9 Cossart P, Sansonetti PJ (2004) Bacterial invasion: The paradigms of enteroinvasive pathogens. Science304: 242-248

10 Cravatt BF, Simon GM, Yates JR (2007) The biological impact of mass-spectrometry-based proteomics. Nature450: 991-1000

11 Cui J, Yao Q, Li S, Ding X, Lu Q, Mao H, Liu L, Zheng N, Chen S, Shao F (2010) Glutamine deamidation and dysfunction of ubiquitin/NEDD8 induced by a bacterial effector family. Science329: 1215-1218

12 Curreem SO, Watt RM, Lau SK, Woo PC (2012) Two-dimensional gel electrophoresis in bacterial proteomics. Protein Cell3: 346-363

13 Di Pasqua R, Mamone G, Ferranti P, Ercolini D, Mauriello G (2010) Changes in the proteome of Salmonella enterica serovar Thompson as stress adaptation to sublethal concentrations of thymol. Proteomics10: 1040-1049

14 Ding C, Jiang J, Wei J, Liu W, Zhang W, Liu M, Fu T, Lu T, Song L, Ying W (2013) A fast workflow for identification and quantification of proteomes. Mol Cell Proteomics12: 2370-2380

15 Engel P, Goepfert A, Stanger FV, Harms A, Schmidt A, Schirmer T, Dehio C (2012) Adenylylation control by intra- or intermolecular active-site obstruction in Fic proteins. Nature482: 107-110

16 Fernandez-Arenas E, Cabezon V, Bermejo C, Arroyo J, Nombela C, Diez-Orejas R, Gil C (2007) Intergrated proteomics and genomics strategies bring new insight into Candida albicans response upon macrophage interaction. Mol Cell Proteomics6: 460-478

17 Fields BS, Benson RF, Besser RE (2002) Legionella and Legionnaires’ disease: 25 years of investigation. Clin Microbiol Rev15: 506-526

18 Galan JE, Wolf-Watz H (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature444: 567-573

19 Geiger T, Wehner A, Schaab C, Cox J, Mann M (2012) Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins. Mol Cell Proteomics11(M111): 014050

20 Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R (1999) Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechol17: 994-999

21 Haraga A, Ohlson MB, Miller SI (2008) Salmonellae interplay with host cells. Nat Rev Microbiol6: 53-66

22 Hardwidge PR, Rodriguez-Escudero I, Goode D, Donohoe S, Eng J, Goodlett DR, Aebersold R, Finlay BB (2004) Proteomic analysis of the intestinal epithelial cell response to enteropathogenic Escherichia coli. J Biol Chem279: 20127-20136

23 Hartlova A, Krocova Z, Cerveny L, Stulik J (2011) A proteomic view of the host-pathogen interaction: the host perspective. Proteomics11: 3212-3220

24 Hoffmann C, Finsel I, Otto A, Pfaffinger G, Rothmeier E, Hecker M, Becher D, Hilbi H (2014) Functional analysis of novel Rab GTPase identified in the proteome of purified Legionella-containing vacuoles from macrophages. Cell Microbiol16: 1034-1052

25 Imami K, Bhavsar AP, Yu H, Brown NF, Rogers LD, Finlay BB, Foster LJ (2013) Global impact of Salmonella Pathogenicity Island 2-secreted effectors on the host phosphoproteome. Mol Cell Proteomics12: 1632-1643

26 Ingmundson A, Delprato A, Lambright DG, Roy CR (2007) Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature450: 365-369

27 Jafari M, Primo V, Smejkal GB, Moskovets EV, Kuo WP, Ivanov AR (2012) Comparison of in-gel protein separation techniques commonly used for fractionation in mass spectrometry-based proteomic profiling. Electrophoresis33: 2516-2526

28 Jenner RG, Young RA (2005) Insights into host responses against pathogens from transcriptional profiling. Nat Rev Microbiol 3: 281-294

29 Kaper JB, Nataro JP, Mobley HLT (2004) Pathogenic Escherichia coli. Nat Rev Microbiol2: 123-140

30 Khabbaz RF, Moseley RR, Steiner RJ, Levitt AM, Bell BP (2014) Challenges of infectious diseases in the USA. Lancet384: 53-63

31 Kim K, Yang E, Vu GP, Gong H, Su J, Liu F, Lu S (2010) Mass spectrometry-based quantitative proteomic analysis of Salmonella enterica serovar enteritidis protein expression upon exposure to hydrogen peroxide. BMC Microbiol10: 166

32 Kotloff KL, Winichoff JP, Ivanoff B, Clemens JD, Swerdlow DL, Sansonetti PJ, Adak GK, Levine MM (1999) Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull World Health Organ77: 651-666

33 Kuntumalla S, Zhang Q, Braisted JC, Fleischmann RD, Peterson SN, Donohue-Rolfe A, Tzipori S, Pieper R (2011) In vivo versus in vitro protein abundance analysis of Shigella dysenteriae type 1 reveals changes in the expression of proteins involved in virulence, stress and energy metabolism. BMC Microbiol11: 147

34 Li Q (2011) Phagosome proteomics: a powerful tool to assess bacteria-mediated immunomodulation. Bioeng Bugs2: 194-198

35 Li H, Xu H, Zhou Y, Zhang J, Long C, Li S, Chen S, Zhou J, Shao F (2007) The phosphothreonine lyase activity of a bacterial type III effector family. Science315: 1000-1003

36 Li S, Zhang L, Yao Q, Li L, Dong N, Rong J, Gao W, Ding X, Sun L, Chen X (2013) Pathogen blocks host death receptor signalling by arginine GlcNAcylation of death domains. Nature501: 242-246

37 Liu X, Gao B, Novik V, Galan JE (2012) Quantitative proteomics of intracellular Campylobacter jejuni reveals metabolic reprogramming. PLoS Pathog8: e1002562

38 Machner MP, Isberg RR (2007) A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science318: 974-977

39 Mukherjee S, Liu X, Arasaki K, McDonough J, Galan JE, Roy CR (2011) Modulation of Rab GTPase function by a protein phosphocholine transferase. Nature477: 103-106

40 Muller MP, Peters H, Bluemer J, Blankenfeldt W, Goody RS, Itzen A (2010) The Legionella effector protein DrrA AMPylates the membrane traffic regulator Rab1b. Science329: 946-949

41 Murata T, Delprato A, Ingmundson A, Toomre DK, Lambright DG, Roy CR (2006) The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor. Nat Cell Biol8: 971-977

42 Neunuebel MR, Chen Y, Gasper AH, Backlund PS Jr, Yergey A, Machner MP (2011) De-AMPylation of the small GTPase Rab1 by the pathogen Legionella pneumophila. Science333: 453-456

43 Ohl ME, Miller SI (2001) Salmonella: a model for bacterial pathogenesis. Annu Rev Med52: 259-274

44 Paape D, Lippuner C, Schmid M, Ackermann R, Barrios-Llerena ME, Zimny-Arndt U, Brinkmann V, Arndt B, Pleissner KP, Jungblut PR (2008) Transgenic, fluorescent Leishmania mexicana allow direct analysis of the proteome of intracellular amastigotes. Mol Cell Proteomics7: 1688-1701

45 Pieper R, Zhang Q, Parmar PP, Huang ST, Clark DJ, Alami H, Donohue-Rolfe A, Fleischmann RD, Peterson SN, Tzipori S (2009) The Shigella dysenteriae serotype 1 proteome, profiled in the host intestinal environment, reveals major metabolic modifications and increased expression of invasive proteins. Proteomics9: 5029-5045

46 Pieper R, Fisher CR, Suh MJ, Huang ST, Parmar P, Payne SM (2013) Analysis of the proteome of intracellular Shigella flexneri reveals pathways important for intracellular growth. Infect Immun81: 4635-4648

47 Rabilloud T, Chevallet M, Luche S, Lelong C (2010) Two-dimensional gel electrophoresis in proteomics: past, present and future. J Proteomics73: 2064-2077

48 Rogers LD, Brown NF, Fang Y, Pelech S, Foster LJ (2011) Phosphoproteomic Analysis of Salmonella-infected cells identifies key kinase regulators and SopB-dependent host phosphorylation events. Sci Signal4: 1-13

49 Salomon D, Orth K (2013) What pathogens have taught us about posttranslational modifications. Cell Host Microbe14: 269-279

50 Schmidt F, Volker U (2011) Proteome analysis of host-pathogen interactions: investigation of pathogen responses to the host cell environment. Proteomics11: 3203-3211

51 Schmutz C, Ahrne E, Kasper CA, Tschon T, Sorg I, Dreier RF, Schmidt A, Arrieumerlou C (2013) Systems-level overview of host protein phosphorylation during Shigella flexneri infection revealed by phosphoproteomics. Mol Cell Proteomics12: 2952-2968

52 Schoebel S, Oesterlin LK, Blankenfeldt W, Goody RS, Itzen A (2009) RabGDI displacement by DrrA from Legionella is a consequence of its guanine nucleotide exchange activity. Mol Cell36: 1060-1072

53 Sengupta N, Alam SI (2011) In vivo studies of Clostridium perfringens in mouse gas gangrene model. Curr Microbiol62: 999-1008

54 Sherwood RK, Roy CR (2013) A Rab-centric perspective of bacterial pathogen-occupied vacuoles. Cell Host Microbe14: 256-268

55 Shi L, Adkins JN, Coleman JR, Schepmoes AA, Dohnkova A, Mottaz HM, Norbeck AD, Purvine SO, Manes NP, Smallwood HS (2006) Proteomic analysis of Salmonella enterica serovar Typhimurium isolated from RAW 264.7 macrophages – Identification of a novel protein that contributes to the replication of serovar Typhimurium inside macrophages. J Biol Chem281: 29131-29140

56 Shi L, Ansong C, Smallwood H, Rommereim L, McDermott JE, Brewer HM, Norbeck AD, Taylor RC, Gustin JK, Heffron F (2009a) Proteome of Salmonella enterica serotype Typhimurium grown in a low Mg/pH medium. J Proteomics Bioinform2: 388-397

57 Shi L, Chowdhury SM, Smallwood HS, Yoon H, Mottaz-Brewer HM, Norbeck AD, McDermott JE, Clauss TRW, Heffron F, Smith RD (2009b) Proteomic investigation of the time course responses of RAW 264.7 macrophages to infection with Salmonella enterica. Infect Immun77: 3227-3233

58 Sonck KAJ, Kint G, Schoofs G, Vander Wauven C, Vanderleyden J, De Keersmaecker SCJ (2009) The proteome of Salmonella Typhimurium grown under in vivo-mimicking conditions. Proteomics9: 565-579

59 Stancik LM, Stancik DM, Schmidt B, Barnhart DM, Yoncheva YN, Slonczewski JL (2002) pH-dependent expression of periplasmic proteins and amino acid catabolism in Escherichia coli. J Bacteriol184: 4246-4258

60 Suh MJ, Kuntumalla S, Yu Y, Pieper R (2014) Proteomes of pathogenic Escherichia coli/Shigella group surveyed in their host environments. Expert Rev Proteomics11: 593-609

61 Tan Y, Luo Z (2011) Legionella pneumophila SidD is a deAMPylase that modifies Rab1. Nature475: 506-509

62 Tan Y, Arnold RJ, Luo Z (2011) Legionella pneumophila regulates the small GTPase Rab1 activity by reversible phosphorylcholination. Proc Natl Acad Sci USA108: 21212-21217

63 Thingholm TE, Jensen ON, Larsen MR (2009) Analytical strategies for phosphoproteomics. Proteomics9: 1451-1468

64 Twine SM, Mykytczuk NCS, Petit MD, Shen H, Sjostedt A, Conlan JW, Kelly JF (2006) In vivo proteomic analysis of the intracellular bacterial pathogen, Francisella tularensis, isolated from mouse spleen. Biochem Biophys Res Commun345: 1621-1633

65 Urwyler S, Nyfeler Y, Ragaz C, Lee H, Mueller LN, Aeversold R, Hilbi H (2009) Proteome analysis of Legiobella vacuoles purified by magnetic immunoseparation reveals secretory and endosomal GTPases. Traffic10: 76-87

66 Walduck A, Rudel T, Meyer TF (2004) Proteomic and gene profiling approaches to study host responses to bacterial infection. Curr Opin Microbiol7: 33-38

67 Weber A, Kogl SA, Jung K (2006) Time-dependent proteome alterations under osmotic stress during aerobic and anaerobic growth in Escherichia coli. J Bacteriol188: 7165-7175

68 Weekes MP, Tomasec P, Huttlin EL, Fielding CA, Nusinow D, Stanton RJ, Wang EC, Aicheler R, Murrell I, Wilkinson GW (2014) Quantitative temporal viromics: an approach to investigate host-pathogen interaction. Cell157: 1460-1472

69 Worby CA, Mattoo S, Kruger RP, Corbeil LB, Koller A, Mendez JC, Zekarias B, Lazar C, Dixon JE (2009) The fic domain: regulation of cell signaling by adenylylation. Mol Cell34: 93-103

70 Yarbrough ML, Li Y, Kinch LN, Grishin NV, Ball HL, Orth K (2009) AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science323: 269-272

71 Yohannes E, Barnhart DM, Slonczewski JL (2004) pH-dependent catabolic protein expression during anaerobic growth of Escherichia coli K-12. J Bacteriol186: 192-199

72 Yu J, Guo L (2011) Quantitative proteomic analysis of Salmonella enterica serovar Typhimurium under PhoP/PhoQ activation conditions. J Proteome Res10: 2992-3002

73 Zhang CG, Chromy BA, McCutchen-Maloney SL (2005) Hostpathogen interactions: a proteomic view. Expert Rev Proteomics2: 187-202

74 Zhang L, Ding X, Cui J, Xu H, Chen J, Gong Y, Hu L, Zhou Y, Ge J, Lu Q (2011) Cysteine methylation disrupts ubiquitin-chain sensing in NF-κB activation. Nature481: 204-208

75 Zhu L, Zhao G, Stein R, Zheng X, Hu W, Shang N, Bu X, Liu X, Wang J, Feng E (2010) The proteome of Shigella flexneri 2a 2457T grown at 30 and 37°. Mol Cell Proteomics9: 1209-1220