Bone marrow-derived macrophages from BALB/c and C57BL/6 mice fundamentally differ in their respiratory chain complex proteins, lysosomal enzymes and components of antioxidant stress systems

Journal of Proteomics

Volumn 103, Issue , 2014, Pages 72-86

  Depke, Maren ^a   Breitbach, Katrin ^a   Dinh Hoang Dang, Khoa ^a   Brinkmann, Lars ^a   Salazar, Manuela Gesell ^a   Dhople, Vishnu Mukund ^a   Bast, Antje ^a   Steil, Leif ^a   Schmidt, Frank ^a   Steinmetz, Ivo ^a   Völker, Uwe ^a  

^a UNIVERSITY MEDICINE GREIFSWALD   (Germany)

Author keywords

BALB c; C57BL 6; IFN ; Macrophages; Proteome; Transcriptome

Indexed keywords

ANTIOXIDANT; GAMMA INTERFERON; PROTEOME; TRANSCRIPTOME;

ANIMAL; BAGG ALBINO MOUSE; BONE MARROW CELL; BURKHOLDERIA PSEUDOMALLEI; C57BL MOUSE; DRUG EFFECTS; ELECTRON TRANSPORT; MACROPHAGE; METABOLISM;

ANIMALS; ANTIOXIDANTS; BONE MARROW CELLS; BURKHOLDERIA PSEUDOMALLEI; ELECTRON TRANSPORT; INTERFERON-GAMMA; MACROPHAGES; MICE, INBRED BALB C; MICE, INBRED C57BL; PROTEOME; TRANSCRIPTOME;

EID: 84898811677     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.03.027     Document Type: Article

References (52)

1. de Veer M.J., Holko M., Frevel M., Walker E., Der S., Paranjape J.M., et al. Functional classification of interferon-stimulated genes identified using microarrays. J Leukoc Biol 2001, 69:912-920.
2. Nau G.J., Richmond J.F., Schlesinger A., Jennings E.G., Lander E.S., Young R.A. Human macrophage activation programs induced by bacterial pathogens. Proc Natl Acad Sci U S A 2002, 99:1503-1508.
3. Lacaze P., Raza S., Sing G., Page D., Forster T., Storm P., et al. Combined genome-wide expression profiling and targeted RNA interference in primary mouse macrophages reveals perturbation of transcriptional networks associated with interferon signalling. BMC Genomics 2009, 10:372.
4. Hancock G.E., Schaedler R.W., MacDonald T.T. Yersinia enterocolitica infection in resistant and susceptible strains of mice. Infect Immun 1986, 53:26-31.
5. Kohler J., Breitbach K., Renner C., Heitsch A.K., Bast A., van Rooijen N., et al. NADPH-oxidase but not inducible nitric oxide synthase contributes to resistance in a murine Staphylococcus aureus Newman pneumonia model. Microbes Infect 2011, 13:914-922.
6. Hoppe I., Brenneke B., Rohde M., Kreft A., Haussler S., Reganzerowski A., et al. Characterization of a murine model of melioidosis: comparison of different strains of mice. Infect Immun 1999, 67:2891-2900.
7. Heinzel F.P., Rerko R.M., Hujer A.M. Underproduction of interleukin-12 in susceptible mice during progressive leishmaniasis is due to decreased CD40 activity. Cell Immunol 1998, 184:129-142.
8. Tabel H., Kaushik R.S., Uzonna J.E. Susceptibility and resistance to Trypanosoma congolense infections. Microbes Infect 2000, 2:1619-1629.
9. Brenner G.J., Cohen N., Moynihan J.A. Similar immune response to nonlethal infection with herpes simplex virus-1 in sensitive (BALB/c) and resistant (C57BL/6) strains of mice. Cell Immunol 1994, 157:510-524.
10. Breitbach K., Klocke S., Tschernig T., van Rooijen N., Baumann U., Steinmetz I. Role of inducible nitric oxide synthase and NADPH oxidase in early control of Burkholderia pseudomallei infection in mice. Infect Immun 2006, 74:6300-6309.
11. Eske K., Breitbach K., Kohler J., Wongprompitak P., Steinmetz I. Generation of murine bone marrow derived macrophages in a standardised serum-free cell culture system. J Immunol Methods 2009, 342:13-19.
12. Breitbach K., Wongprompitak P., Steinmetz I. Distinct roles for nitric oxide in resistant C57BL/6 and susceptible BALB/c mice to control Burkholderia pseudomallei infection. BMC Immunol 2011, 12:20.
13. Mills C.D., Kincaid K., Alt J.M., Heilman M.J., Hill A.M. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 2000, 164:6166-6173.
14. Kaushik R.S., Uzonna J.E., Zhang Y., Gordon J.R., Tabel H. Innate resistance to experimental African trypanosomiasis: differences in cytokine (TNF-alpha, IL-6, IL-10 and IL-12) production by bone marrow-derived macrophages from resistant and susceptible mice. Cytokine 2000, 12:1024-1034.
15. Santos J.L., Andrade A.A., Dias A.A., Bonjardim C.A., Reis L.F., Teixeira S.M., et al. Differential sensitivity of C57BL/6 (M-1) and BALB/c (M-2) macrophages to the stimuli of IFN-gamma/LPS for the production of NO: correlation with iNOS mRNA and protein expression. J Interferon Cytokine Res 2006, 26:682-688.
16. Asare R., Santic M., Gobin I., Doric M., Suttles J., Graham J.E., et al. Genetic susceptibility and caspase activation in mouse and human macrophages are distinct for Legionella longbeachae and L. pneumophila. Infect Immun 2007, 75:1933-1945.
17. Flesch I.E., Kaufmann S.H. Effect of fetal calf serum on cytokine release by bone marrow-derived macrophages during infection with intracellular bacteria. Immunobiology 1999, 200:120-127.
18. Flesch I., Fruh A., Ferber E. Functional comparison of bone marrow-derived macrophages obtained by cultivation in serum-free or serum-supplemented medium. Immunobiology 1986, 173:72-81.
19. Thiele T., Steil L., Gebhard S., Scharf C., Hammer E., Brigulla M., et al. Profiling of alterations in platelet proteins during storage of platelet concentrates. Transfusion 2007, 47:1221-1233.
20. Eymann C., Dreisbach A., Albrecht D., Bernhardt J., Becher D., Gentner S., et al. A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics 2004, 4:2849-2876.
21. Eisen M.B., Spellman P.T., Brown P.O., Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 1998, 95:14863-14868.
22. Ehrt S., Schnappinger D., Bekiranov S., Drenkow J., Shi S., Gingeras T.R., et al. Reprogramming of the macrophage transcriptome in response to interferon-gamma and mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase. J Exp Med 2001, 194:1123-1140.
23. Jutras I., Houde M., Currier N., Boulais J., Duclos S., LaBoissiere S., et al. Modulation of the phagosome proteome by interferon-gamma. Mol Cell Proteomics 2008, 7:697-715.
24. Kitamura H., Ito M., Yuasa T., Kikuguchi C., Hijikata A., Takayama M., et al. Genome-wide identification and characterization of transcripts translationally regulated by bacterial lipopolysaccharide in macrophage-like J774.1 cells. Physiol Genomics 2008, 33:121-132.
25. Arnoult D., Soares F., Tattoli I., Girardin S.E. Mitochondria in innate immunity. EMBO Rep 2011, 12:901-910.
26. Arnoult D., Carneiro L., Tattoli I., Girardin S.E. The role of mitochondria in cellular defense against microbial infection. Semin Immunol 2009, 21:223-232.
27. Chen Y., Lu H., Liu Q., Huang G., Lim C.P., Zhang L., et al. Function of GRIM-19, a mitochondrial respiratory chain complex I protein, in innate immunity. J Biol Chem 2012, 287:27227-27235.
28. Tattoli I., Carneiro L.A., Jehanno M., Magalhaes J.G., Shu Y., Philpott D.J., et al. NLRX1 is a mitochondrial NOD-like receptor that amplifies NF-kappaB and JNK pathways by inducing reactive oxygen species production. EMBO Rep 2008, 9:293-300.
29. Arnoult D., Soares F., Tattoli I., Castanier C., Philpott D.J., Girardin S.E. An N-terminal addressing sequence targets NLRX1 to the mitochondrial matrix. J Cell Sci 2009, 122:3161-3168.
30. Castanier C., Arnoult D. Mitochondrial localization of viral proteins as a means to subvert host defense. Biochim Biophys Acta 1813, 2011:575-583.
31. Ebermann L., Wika S., Klumpe I., Hammer E., Klingel K., Lassner D., et al. The mitochondrial respiratory chain has a critical role in the antiviral process in Coxsackievirus B3-induced myocarditis. Lab Invest 2012, 92:125-134.
32. Tulone C., Tsang J., Prokopowicz Z., Grosvenor N., Chain B. Natural cathepsin E deficiency in the immune system of C57BL/6J mice. Immunogenetics 2007, 59:927-935.
33. Yamamoto K., Kawakubo T., Yasukochi A., Tsukuba T. Emerging roles of cathepsin E in host defense mechanisms. Biochim Biophys Acta 1824, 2012:105-112.
34. Katunuma N. Posttranslational processing and modification of cathepsins and cystatins. Journal Signal Transduct 2010, 2010:375345.
35. Sathiyaseelan J., Jiang X., Baldwin C.L. Growth of Brucella abortus in macrophages from resistant and susceptible mouse strains. Clin Exp Immunol 2000, 121:289-294.
36. Zamboni D.S. Genetic control of natural resistance of mouse macrophages to Coxiella burnetii infection in vitro: macrophages from restrictive strains control parasitophorous vacuole maturation. Infect Immun 2004, 72:2395-2399.
37. Kornfeld S., Mellman I. The biogenesis of lysosomes. Annu Rev Cell Biol 1989, 5:483-525.
38. Bast A., Erttmann S.F., Walther R., Steinmetz I. Influence of iNOS and COX on peroxiredoxin gene expression in primary macrophages. Free Radic Biol Med 2010, 49:1881-1891.
39. Culotta V.C., Yang M., O'Halloran T.V. Activation of superoxide dismutases: putting the metal to the pedal. Biochim Biophys Acta 2006, 1763:747-758.
40. Miao L., St Clair D.K. Regulation of superoxide dismutase genes: implications in disease. Free Radic Biol Med 2009, 47:344-356.
41. Li Y., Huang T.T., Carlson E.J., Melov S., Ursell P.C., Olson J.L., et al. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 1995, 11:376-381.
42. Lebovitz R.M., Zhang H., Vogel H., Cartwright J., Dionne L., Lu N., et al. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci U S A 1996, 93:9782-9787.
43. Wallace D.C. Mouse models for mitochondrial disease. Am J Med Genet 2001, 106:71-93.
44. Tyler D.D. Polarographic assay and intracellular distribution of superoxide dismutase in rat liver. Biochem J 1975, 147:493-504.
45. Shih D.M., Gu L., Xia Y.R., Navab M., Li W.F., Hama S., et al. Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature 1998, 394:284-287.
46. Ng C.J., Bourquard N., Grijalva V., Hama S., Shih D.M., Navab M., et al. Paraoxonase-2 deficiency aggravates atherosclerosis in mice despite lower apolipoprotein-B-containing lipoproteins: anti-atherogenic role for paraoxonase-2. J Biol Chem 2006, 281:29491-29500.
47. Shih D.M., Xia Y.R., Wang X.P., Wang S.S., Bourquard N., Fogelman A.M., et al. Decreased obesity and atherosclerosis in human paraoxonase 3 transgenic mice. Circ Res 2007, 100:1200-1207.
48. Altenhofer S., Witte I., Teiber J.F., Wilgenbus P., Pautz A., Li H., et al. One enzyme, two functions: PON2 prevents mitochondrial superoxide formation and apoptosis independent from its lactonase activity. J Biol Chem 2010, 285:24398-24403.
49. Shih D.M., Lusis A.J. The roles of PON1 and PON2 in cardiovascular disease and innate immunity. Curr Opin Lipidol 2009, 20:288-292.
50. Eberl L. Quorum sensing in the genus Burkholderia. Int J Med Microbiol 2006, 296:103-110.
51. Li Y.H., Tian X. Quorum sensing and bacterial social interactions in biofilms. Sensors (Basel) 2012, 12:2519-2538.
52. Jimenez P.N., Koch G., Thompson J.A., Xavier K.B., Cool R.H., Quax W.J. The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 2012, 76:46-65.