Roles of Salmonella enterica serovar Typhimurium encoded Peptidase N during systemic infection of Ifnγ -/- mice

Immunobiology

Volumn 217, Issue 3, 2012, Pages 354-362

  Bhosale, Manoj ^a   Kadthur, Jayachandra C ^a   Nandi, Dipankar ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Cytokines; Host response; IFN ; Immunocompromised; Infection; Peptidase; S. typhimurium

Indexed keywords

AMINOPEPTIDASE; GAMMA INTERFERON; INTERLEUKIN 1BETA; PEPTIDASE N; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL SALMONELLOSIS; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; CATALYSIS; COLONY FORMING UNIT; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; ENZYME LOCALIZATION; HISTOLOGY; HOST SUSCEPTIBILITY; IMMUNE RESPONSE; LIVER INJURY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; SALMONELLA TYPHIMURIUM; SPLEEN INJURY; WILD TYPE;

AMINOPEPTIDASES; ANIMALS; CATALYSIS; CELL LINE; ENZYME ACTIVATION; HOT TEMPERATURE; INTERFERON-GAMMA; INTERLEUKIN-1BETA; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; PERITONITIS; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; STRESS, PHYSIOLOGICAL; SURVIVAL ANALYSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84856441968     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2011.07.010     Document Type: Article

References (58)

1. Acosta D., Cancela M., Piacenza L., Roche L., Carmona C., Tort J.F. Fasciola hepatica leucine aminopeptidase, a promising candidate for vaccination against ruminant fasciolosis. Mol. Biochem. Parasitol. 2008, 158:52-64.
2. Addlagatta A., Gay L., Matthews B.W. Structure of aminopeptidase N from Escherichia coli suggests a compartmentalized, gated active site. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:2449-2454.
3. Bao S., Beagley K.W., France M.P., Shen J., Husband A.J. Interferon-gamma plays a critical role in intestinal immunity against Salmonella typhimurium infection. Immunology 2000, 99:464-472.
4. Boddicker J.D., Jones B.D. Lon protease activity causes down-regulation of Salmonella pathogenicity island 1 invasion gene expression after infection of epithelial cells. Infect. Immun. 2004, 72:2002-2013.
5. Caprioglio D.R., Padilla C., Werner-Washburne M. Isolation and characterization of AAP1. A gene encoding an alanine/arginine aminopeptidase in yeast. J. Biol. Chem. 1993, 268:14310-14315.
6. Chandu D., Kumar A., Nandi D. PepN, the major Suc-LLVY-AMC-hydrolyzing enzyme in Escherichia coli, displays functional similarity with downstream processing enzymes in Archaea and eukarya. Implications in cytosolic protein degradation. J. Biol. Chem. 2003, 278:5548-5556.
7. Chandu D., Nandi D. PepN is the major aminopeptidase in Escherichia coli: insights on substrate specificity and role during sodium-salicylate-induced stress. Microbiology 2003, 149:3437-3447.
8. Contreras-Rodriguez A., Ramirez-Zavala B., Contreras A., Schurig G.G., Sriranganathan N., Lopez-Merino A. Purification and characterization of an immunogenic aminopeptidase of Brucella melitensis. Infect. Immun. 2003, 71:5238-5244.
9. Cooper A.M., Dalton D.K., Stewart T.A., Griffin J.P., Russell D.G., Orme I.M. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med. 1993, 178:2243-2247.
10. Darwin K.H., Ehrt S., Gutierrez-Ramos J.C., Weich N., Nathan C.F. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 2003, 302:1963-1966.
11. Dorman S.E., Holland S.M. Mutation in the signal-transducing chain of the interferon-gamma receptor and susceptibility to mycobacterial infection. J. Clin. Invest. 1998, 101:2364-2369.
12. Eriksson S., Lucchini S., Thompson A., Rhen M., Hinton J.C. Unraveling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol 2003, 47:103-118.
13. Everest P., Roberts M., Dougan G. Susceptibility to Salmonella typhimurium infection and effectiveness of vaccination in mice deficient in the tumor necrosis factor alpha p55 receptor. Infect Immun. 1998, 66:3355-3364.
14. Flynn J.L., Chan J., Triebold K.J., Dalton D.K., Stewart T.A., Bloom B.R. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 1993, 178:2249-2254.
15. Gamble M., Wilson I. The hematoxylin and eosin. Theory and Practice of Histological Techniques 2002, 125-138. Churchill Livingstone, London. 5th ed. J.D. Bancroft, M. Gamble (Eds.).
16. Gandotra S., Lebron M.B., Ehrt S. The Mycobacterium tuberculosis proteasome active site threonine is essential for persistence yet dispensable for replication and resistance to nitric oxide. PLoS Pathog. 2010, 6:e1001040.
17. Gardiner D.L., Trenholme K.R., Skinner-Adams T.S., Stack C.M., Dalton J.P. Over-expression of leucyl aminopeptidase in Plasmodium falciparum parasites: target for the anti-malarial activity of bestatin. J. Biol. Chem. 2006, 281:1741-1745.
18. Ge S., Danino V., He Q., Hinton J.C., Granfors K. Microarray analysis of response of Salmonella during infection of HLA-B27-transfected human macrophage-like U937 cells. BMC Genomics 2010, 11:456.
19. Gordon M.A., Jack D.L., Dockrell D.H., Lee M.E., Read R.C. Gamma interferon enhances internalization and early non oxidative killing of Salmonella enterica serovar Typhimurium by human macrophages and modifies cytokine responses. Infect. Immun. 2005, 73:3445-3452.
20. Gropp K., Schild L., Schindler S., Hube B., Zipfel P.F., Skerka C. The yeast Candida albicans evades human complement attack by secretion of aspartic proteases. Mol. Immunol. 2009, 47:465-475.
21. Harty J.T., Bevan M.J. Specific immunity to Listeria monocytogenes in the absence of IFN gamma. Immunity 1995, 3:109-117.
22. Kumagai Y., Yajima A., Konishi K. Peptidase activity of dipeptidyl aminopeptidase IV produced by Porphyromonas gingivalis is important but not sufficient for virulence. Microbiol. Immunol. 2003, 47:735-743.
23. Kumar A., Bhosale M., Reddy S., Srinivasan N., Nandi D. Importance of non-conserved distal carboxyl terminal amino acids in two peptidases belonging to the M1 family: Thermoplasma acidophilum Tricorn interacting factor F2 and Escherichia coli Peptidase N. Biochimie 2009, 91:1145-1155.
24. Kumar A., Nandi D. Characterization and role of peptidase N from Salmonella enterica serovar Typhimurium. Biochem. Biophys. Res. Commun. 2007, 353:706-712.
25. 4 biosynthesis. J. Biol. Chem. 2004, 279:50639-50642.
26. Haraga A., Ohlson M.B., Miller S.I. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 2008, 6:53-66.
27. Hautefort I., Thompson A., Eriksson-Ygberg S., Parker M.L., Lucchini V., et al. During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell. Microbiol. 2008, 10:958-984.
28. Ito K., Nakajima Y., Onohara Y., Takeo M., Nakashima K., Matsubara F., Ito T., Yoshimoto T. Crystal structure of aminopeptidase N (proteobacteria alanyl aminopeptidase) from Escherichia coli and conformational change of methionine 260 involved in substrate recognition. J. Biol. Chem. 2006, 281:33664-33676.
29. Lamichhane G., Raghunand T.R., Morrison N.E., Woolwine S.C., Tyagi S., Kandavelou K., Bishai W.R. Deletion of a Mycobacterium tuberculosis proteasomal ATPase homologue gene produces a slow-growing strain that persists in host tissues. J. Infect. Dis. 2006, 194:1233-1240.
30. Mizuno Y., Takada H., Nomura A., Jin C.H., Hattori H., Ihara K., Aoki T., Eguchi K., Hara T. Th1 and Th1-inducing cytokines in Salmonella infection. Clin. Exp. Immunol. 2003, 131:111-117.
31. Mo E., Peters S.E., Willers C., Maskell D.J., Charles I.G. Single, double and triple mutants of Salmonella enterica serovar Typhimurium degP (htrA), degQ (hhoA) and degS (hhoB) have diverse phenotypes on exposure to elevated temperature and their growth in vivo is attenuated to different extents. Microb. Pathog. 2006, 41:174-182.
32. Naglik J.R., Challacombe S.J., Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol. Mol. Biol. Rev. 2003, 67:400-428.
33. Naglik J.R., Moyes D., Makwana J., Kanzaria P., Tsichlaki E., Weindl G., et al. Quantitative expression of the Candida albicans secreted aspartyl proteinase gene family in human oral and vaginal candidiasis. Microbiology 2008, 154:3266-3280.
34. Nairz M., Fritsche G., Brunner P., Talasz H., Hantke K., Weiss G. Interferon-gamma limits the availability of iron for intramacrophage Salmonella typhimurium. Eur. J. Immunol. 2008, 38:1923-1936.
35. Patil V., Kumar A., Kuruppath S., Nandi D. Peptidase N encoded by Salmonella enterica serovar Typhimurium modulates systemic infection in mice. FEMS Immunol. Microbiol. 2007, 51:431-442.
36. Pie S., Truffa-Bachi P., Pla M., Nauciel C. Th1 response in Salmonella typhimurium-infected mice with a high or low rate of bacterial clearance. Infect. Immun. 1997, 65:4509-4514.
37. Pietrella D., Rachini A., Pandey N., Schild L., Netea M., Bistoni F., Hube B., Vecchiarelli A. The inflammatory response induced by aspartic proteases of Candida albicans is independent of proteolytic activity. Infect. Immun. 2010, 78:4754-4762.
38. Raupach B., Kurth N., Pfeffer K., Kaufmann S.H. Salmonella typhimurium strains carrying independent mutations display similar virulence phenotypes yet are controlled by distinct host defense mechanisms. J. Immunol. 2003, 170:6133-6140.
39. Raupach B., Peuschel S.K., Monack D.M., Zychlinsky A. Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection. Infect. Immun. 2006, 74:4922-4926.
40. Rhee S.J., Walker W.A., Cherayil B.J. Developmentally regulated intestinal expression of IFN-gamma and its target genes and the age-specific response to enteric Salmonella infection. J. Immunol. 2005, 175:1127-1136.
41. Rossier O., Dao J., Cianciotto N.P. The type II secretion system of Legionella pneumophila elaborates two aminopeptidases, as well as a metalloprotease that contributes to differential infection among protozoan hosts. Appl. Environ. Microbiol. 2008, 74:753-761.
42. Rottenberg M.E., Gigliotti Rothfuchs A., Gigliotti D., Ceausu M., Une C., Levitsky V., Wigzell H. Regulation and role of IFN-gamma in the innate resistance to infection with Chlamydia pneumoniae. J. Immunol. 2000, 164:4812-4818.
43. Ruepp A., Eckerskorn C., Bogyo M., Baumeister W. Proteasome function is dispensable under normal but not under heat shock conditions in Thermoplasma acidophilum. FEBS Lett. 1998, 425:87-90.
44. Rychlik I., Barrow P.A. Salmonella stress management and its relevance to behavior during intestinal colonization and infection. FEMS Microbiol. Rev. 2005, 29:1021-1040.
45. Saha B., Jyothi Prasanna S., Chandrasekar B., Nandi D. Gene modulation and immunoregulatory roles of interferon gamma. Cytokine 2010, 50:1-14.
46. Saveanu L., Carroll O., Lindo V., Del Val M., Lopez D., et al. Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nat. Immunol. 2005, 6:689-697.
47. Scharton-Kersten T.M., Wynn T.A., Denkers E.Y., Bala S., Grunvald E., Hieny S., Gazzinelli R.T., Sher A. In the absence of endogenous IFN-gamma, mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J. Immunol. 1996, 157:4045-4054.
48. 4H in limiting chronic pulmonary neutrophilic inflammation. Science 2010, 330:90-94.
49. Swenerton R.K., Zhang S., Sajid M., Medzihradszky K.F., Craik C.S., Kelly B.L., McKerrow J.H. The oligopeptidase B of Leishmania regulates parasite enolase and immune evasion. J. Biol. Chem. 2011, 286:429-440.
50. Takaya A., Kubota Y., Isogai E., Yamamoto T. Degradation of the HilC and HilD regulator proteins by ATP-dependent Lon protease leads to down regulation of Salmonella pathogenicity island 1 gene expression. Mol. Microbiol. 2005, 55:839-852.
51. Takaya A., Suzuki M., Matsui H., Tomoyasu T., Sashinami H., Nakane A., Yamamoto T. Lon, a stress-induced ATP-dependent protease, is critically important for systemic Salmonella enterica serovar Typhimurium infection of mice. Infect. Immun. 2003, 71:690-696.
52. Tamura N., Lottspeich F., Baumeister W., Tamura T. The role of tricorn protease and its aminopeptidase-interacting factors in cellular protein degradation. Cell 1998, 95:637-648.
53. Tierrez A., Garcia-del Portillo F. New concepts in Salmonella virulence: the importance of reducing the intracellular growth rate in the host. Cell. Microbiol. 2005, 7:901-909.
54. 4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 2010, 140:717-730.
55. Watanabe Y., Shibata K., Kikkawa F., Kajiyama H., Ino K., Hattori A., Tsujimoto M., Mizutani S. Adipocyte-derived leucine aminopeptidase suppresses angiogenesis in human endometrial carcinoma via renin-angiotensin system. Clin. Cancer. Res. 2003, 9:6497-6503.
56. Yagishita H., Kumagai Y., Konishi K., Takahashi Y., Aoba T., Yoshikawa M. Histopathological studies on virulence of dipeptidyl aminopeptidase IV (DPPIV) of Porphyromonas gingivalis in a mouse abscess model: use of a DPPIV-deficient mutant. Infect. Immun. 2001, 69:7159-7161.
57. Yamamoto T., Sashinami H., Takaya A., Tomoyasu T., Matsui H., Kikuchi Y., Hanawa T., Kamiya S., Nakane A. Disruption of the genes for ClpXP protease in Salmonella enterica serovar Typhimurium results in persistent infection in mice, and development of persistence requires endogenous gamma interferon and tumor necrosis factor alpha. Infect. Immun. 2001, 69:3164-3174.
58. Yan J., Parekh V.V., Mendez-Fernandez Y., Olivares-Villagómez D., et al. In vivo role of ER-associated peptidase activity in tailoring peptides for presentation by MHC class Ia and class Ib molecules. J. Exp. Med. 2006, 203:647-659.