A systems biology approach to study the phagosomal proteome modulated by mycobacterial infections

International Journal of Clinical and Experimental Medicine

Volumn 2, Issue 3, 2009, Pages 233-247

  Rao, Prahlad K ^a   Singh, Christoher R ^b   Jagannath, Chinnaswamy ^b   Li, Qingbo ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Macrophage; Mycobacterium tuberculosis; Phagosome; Proteomics; Systems biology

Indexed keywords

BACTERIAL PROTEIN;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; CELL MATURATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOCYTOSIS; PHAGOSOME; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

MYCOBACTERIUM TUBERCULOSIS;

EID: 74549224346     PISSN: None     EISSN: 19405901     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, Haddix PL, Collins HL, Fok AK, Allen RD, Gluck SL, Heuser J and Russell DG. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 1994; 263: 678-681.
2. Philips JA. Mycobacterial manipulation of vacuolar sorting. Cell Microbiol 2008; 10: 2408-2415.
3. Stuart LM and Ezekowitz RA. Phagocytosis: elegant complexity. Immunity 2005; 22: 539-550.
4. Gotthardt D, Warnatz HJ, Henschel O, Bruckert F, Schleicher M and Soldati T. High-resolution dissection of phagosome maturation reveals distinct membrane trafficking phases. Mol Biol Cell 2002; 13: 3508-3520.
5. Underhill DM and Ozinsky A. Phagocytosis of microbes: complexity in action. Annu Rev Immunol 2002; 20: 825-852.
6. Stuart LM, Boulais J, Charriere GM, Hennessy EJ, Brunet S, Jutras I, Goyette G, Rondeau C, Letarte S, Huang H, Ye P, Morales F, Kocks C, Bader JS, Desjardins M and Ezekowitz RA. A systems biology analysis of the Drosophila phagosome. Nature 2007; 445: 95-101.
7. Desjardins M and Griffiths G. Phagocytosis: latex leads the way. Curr Opin Cell Biol 2003; 15: 498-503.
8. Rogers LD and Foster LJ. The dynamic phagosomal proteome and the contribution of the endoplasmic reticulum. Proc Natl Acad Sci U S A 2007; 104: 18520-18525.
9. Shui W, Sheu L, Liu J, Smart B, Petzold CJ, Hsieh TY, Pitcher A, Keasling JD and Bertozzi CR. Membrane proteomics of phagosomes suggests a connection to autophagy. Proc Natl Acad Sci U S A 2008; 105: 16952-16957.
10. Jutras I, Houde M, Currier N, Boulais J, Duclos S, LaBoissiere S, Bonneil E, Kearney P, Thibault P, Paramithiotis E, Hugo P and Desjardins M. Modulation of the phagosome proteome by interferon-gamma. Mol Cell Proteomics 2008; 7: 697-715.
11. Robinson N, Kolter T, Wolke M, Rybniker J, Hartmann P and Plum G. Mycobacterial phenolic glycolipid inhibits phagosome maturation and subverts the pro-inflammatory cytokine response. Traffic 2008; 9: 1936-1947.
12. Garin J, Diez R, Kieffer S, Dermine JF, Duclos S, Gagnon E, Sadoul R, Rondeau C and Desjardins M. The phagosome proteome: insight into phagosome functions. J Cell Biol 2001; 152: 165-180.
13. Trost M, English L, Lemieux S, Courcelles M, Desjardins M and Thibault P. The phagosomal proteome in interferon-gamma-activated macrophages. Immunity 2009; 30: 143-154.
14. Gotthardt D, Blancheteau V, Bosserhoff A, Ruppert T, Delorenzi M and Soldati T. Proteomics fingerprinting of phagosome maturation and evidence for the role of a Galpha during uptake. Mol Cell Proteomics 2006; 5: 2228-2243.
15. Marion S, Laurent C and Guillen N. Signalization and cytoskeleton activity through myosin IB during the early steps of phagocytosis in Entamoeba histolytica: a proteomic approach. Cell Microbiol 2005; 7: 1504-1518.
16. Kovarova H, Halada P, Man P, Golovliov I, Krocova Z, Spacek J, Porkertova S and Necasova R. Proteome study of Francisella tularensis live vaccine strain-containing phagosome in Bcg/Nramp1 congenic macrophages: resistant allele contributes to permissive environment and susceptibility to infection. Proteomics 2002; 2: 85-93.
17. Sturgill-Koszycki S, Haddix PL and Russell DG. The interaction between Mycobacterium and the macrophage analyzed by two-dimensional polyacrylamide gel electrophoresis. Electrophoresis 1997; 18: 2558-2565.
18. Mills SD and Finlay BB. Isolation and characterization of Salmonella typhimurium and Yersinia pseudotuberculosis-containing phagosomes from infected mouse macrophages: Y. pseudotuberculosis traffics to terminal lysosomes where they are degraded. Eur J Cell Biol 1998; 77: 35-47.
19. Luhrmann A and Haas A. A method to purify bacteria-containing phagosomes from infected macrophages. Methods Cell Sci 2000; 22: 329-341.
20. Fernandez-Mora E, Polidori M, Luhrmann A, Schaible UE and Haas A. Maturation of Rhodococcus equi-containing vacuoles is arrested after completion of the early endosome stage. Traffic 2005; 6: 635-653.
21. Kima PE and Dunn W. Exploiting calnexin expression on phagosomes to isolate Leishmania parasitophorous vacuoles. Microb Pathog 2005; 38: 139-145.
22. Urwyler S, Nyfeler Y, Ragaz C, Lee H, Mueller LN, Aebersold R and Hilbi H. Proteome analysis of Legionella vacuoles purified by magnetic immunoseparation reveals secretory and endosomal GTPases. Traffic 2009; 10: 76-87.
23. Shevchuk O, Batzilla C, Hagele S, Kusch H, Engelmann S, Hecker M, Haas A, Heuner K, Glockner G and Steinert M. Proteomic analysis of Legionella- containing phagosomes isolated from Dictyostelium. Int J Med Microbiol 2009;
24. Fratti RA, Vergne I, Chua J, Skidmore J and Deretic V. Regulators of membrane trafficking and Mycobacterium tuberculosis phagosome maturation block. Electrophoresis 2000; 21: 3378-3385.
25. Rupper A and Cardelli J. Large-scale purification of latex bead phagosomes from mouse macrophage cell lines and subsequent preparation for high-throughput quantitative proteomics. Methods Mol Biol 2008; 445: 339-351.
26. Copenhaver RH, Sepulveda E, Armitige LY, Actor JK, Wanger A, Norris SJ, Hunter RL and Jagannath C. A mutant of Mycobacterium tuberculosis H37Rv that lacks expression of antigen 85A is attenuated in mice but retains vaccinogenic potential. Infect Immun 2004; 72: 7084-7095.
27. Katti MK, Dai G, Armitige LY, Rivera Marrero C, Daniel S, Singh CR, Lindsey DR, Dhandayuthapani S, Hunter RL and Jagannath C. The Delta fbpA mutant derived from Mycobacterium tuberculosis H37Rv has an enhanced susceptibility to intracellular antimicrobial oxidative mechanisms, undergoes limited phagosome maturation and activates macrophages and dendritic cells. Cell Microbiol 2008; 10: 1286-1303.
28. Rao PK, Rodriguez GM, Smith I and Li Q. Protein dynamics in iron-starved Mycobacterium tuberculosis revealed by turnover and abundance measurement using hybrid-linear ion trap-fourier transform mass spectrometry. Anal Chem 2008; 80: 6860-6869.
29. Li Q and Roxas BA. An assessment of false discovery rates and statistical significance in label-free quantitative proteomics with combined filters. BMC Bioinformatics 2009; 10: 43.
30. Rao P and Li Q. Principal Component Analysis of Proteome Dynamics in Iron-Starved Mycobacterium Tuberculosis. Journal of Proteomics and Bioinformatics 2009; 2: 19-31.
31. Choi H, Ghosh D and Nesvizhskii AI. Statistical validation of peptide identifications in large-scale proteomics using the target-decoy database search strategy and flexible mixture modeling. J Proteome Res 2008; 7: 286-292.
32. http://tools.proteomecenter.org/wiki/index.p hp?title=Software:TPP.
33. Rao PK, Roxas BA and Li Q. Determination of global protein turnover in stressed mycobacterium cells using hybrid-linear ion trap-fourier transform mass spectrometry. Anal Chem 2008; 80: 396-406.
34. Andreev VP, Li L, Cao L, Gu Y, Rejtar T, Wu SL and Karger BL. A new algorithm using cross-assignment for label-free quantitation with LCLTQ-FT MS. J Proteome Res 2007; 6: 2186-2194.
35. Finney GL, Blackler AR, Hoopmann MR, Canterbury JD, Wu CC and MacCoss MJ. Label-free comparative analysis of proteomics mixtures using chromatographic alignment of high-resolution muLC-MS data. Anal Chem 2008; 80: 961-971.
36. Apraiz I, Mi J and Cristobal S. Identification of proteomic signatures of exposure to marine pollutants in mussels (Mytilus edulis). Mol Cell Proteomics 2006; 5: 1274-1285.
37. Ivosev G, Burton L and Bonner R. Dimensionality reduction and visualization in principal component analysis. Anal Chem 2008; 80: 4933-4944.
38. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM and Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000; 25: 25-29.
39. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B and Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003; 13: 2498-2504.
40. von Mering C, Jensen LJ, Kuhn M, Chaffron S, Doerks T, Kruger B, Snel B and Bork P. STRING 7--recent developments in the integration and prediction of protein interactions. Nucleic Acids Res 2007; 35: D358-362.
41. http://string.embl.de/.
42. http://www.genome.jp/kegg/.
43. Mollenkopf HJ, Jungblut PR, Raupach B, Mattow J, Lamer S, Zimny-Arndt U, Schaible UE and Kaufmann SH. A dynamic two-dimensional polyacrylamide gel electrophoresis database: the mycobacterial proteome via Internet. Electrophoresis 1999; 20: 2172-2180.
44. Rosenkrands I, King A, Weldingh K, Moniatte M, Moertz E and Andersen P. Towards the proteome of Mycobacterium tuberculosis. Electrophoresis 2000; 21: 3740-3756.
45. Monahan IM, Betts J, Banerjee DK and Butcher PD. Differential expression of mycobacterial proteins following phagocytosis by macrophages. Microbiology 2001; 147: 459-471.
46. Wong DK, Lee BY, Horwitz MA and Gibson BW. Identification of fur, aconitase, and other proteins expressed by Mycobacterium tuberculosis under conditions of low and high concentrations of iron by combined two-dimensional gel electrophoresis and mass spectrometry. Infect Immun 1999; 67: 327-336.
47. Sassetti CM, Boyd DH and Rubin EJ. Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 2003; 48: 77-84.
48. Gagnon E, Duclos S, Rondeau C, Chevet E, Cameron PH, Steele-Mortimer O, Paiement J, Bergeron JJ and Desjardins M. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 2002; 110: 119-131.
49. Harriff MJ, Danelishvili L, Wu M, Wilder C, McNamara M, Kent ML and Bermudez LE. Mycobacterium avium genes MAV-5138 and MAV-3679 are transcriptional regulators that play a role in invasion of epithelial cells, in part by their regulation of CipA, a putative surface protein interacting with host cell signaling pathways. J Bacteriol 2009; 191: 1132-1142.
50. Zhao H, Ettala O and Vaananen HK. Intracellular membrane trafficking pathways in bone-resorbing osteoclasts revealed by cloning and subcellular localization studies of small GTP-binding rab proteins. Biochem Biophys Res Commun 2002; 293: 1060-1065.
51. Jutras I, Laplante A, Boulais J, Brunet S, Thinakaran G and Desjardins M. Gamma-secretase is a functional component of phagosomes. J Biol Chem 2005; 280: 36310-36317.