RahU: An inducible and functionally pleiotropic protein in Pseudomonas aeruginosa modulates innate immunity and inflammation in host cells

Cellular Immunology

Volumn 270, Issue 2, 2011, Pages 103-113

  Rao, Jayasimha ^a   Elliott, Michael R ^b,c   Leitinger, Norbert ^b   Jensen, Roderick V ^d   Goldberg, Joanna B ^b   Amin, Ashok R ^a,e,f  

^a VIRGINIA TECH CARILION SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^c UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^d VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^e EDWARD VIA COLLEGE OF OSTEOPATHIC MEDICINE   (United States)

^f WAKE FOREST UNIVERSITY   (United States)

Author keywords

Chemotaxis; Inflammation; Inflammation resolution; Innate immunity; Nitric oxide

Indexed keywords

BACTERIAL PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; N(G) METHYLARGININE; NITRIC OXIDE; PREDNISONE; PROTEINASE K; RAHU PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MIGRATION; CELL VIABILITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME INHIBITION; FLOW CYTOMETRY; HOST CELL; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; INFLAMMATION; MACROPHAGE; MONOCYTE MACROPHAGE PRECURSOR CELL; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLEIOTROPY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN PURIFICATION; PSEUDOMONAS AERUGINOSA; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UNINDEXED SEQUENCE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BACTERIAL PROTEINS; BASE SEQUENCE; CELL LINE; CELL SURVIVAL; DNA, BACTERIAL; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; MACROPHAGES; MICE; NITRIC OXIDE; PSEUDOMONAS AERUGINOSA; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); MURINAE; PSEUDOMONAS AERUGINOSA;

EID: 80051667277     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2011.05.012     Document Type: Article

References (74)

1. Berne S., Lah L., Sepcic K. Aegerolysins: structure, function, and putative biological role. Protein Sci. 2009, 18:694-706.
2. Berne S., Krizaj I., Pohleven F., Turk T., Macek P., Sepcic K. Pleurotus and Agrocybe hemolysins, new proteins hypothetically involved in fungal fruiting. Biochim. Biophys. Acta 2002, 1570(3):153-159.
3. Ebina K., Sakagami H., Yokota K., Kondo H. Cloning and nucleotide sequence of cDNA encoding Asp-hemolysin from Aspergillus fumigatus. Biochim. Biophys. Acta 1994, 1219(1):148-150.
4. Kumagai T., Kudo Y., Fukuchi Y., Ebina K., Yokota K. Expression of a synthetic gene encoding the Asp-hemolysin from Aspergillus fumigatus in Escherichia coli. Biol. Pharm. Bull. 2002, 25(1):115-117.
5. Fernandez Espinar M.T., Labarere J. Cloning and sequencing of the Aa-Pri1 gene specifically expressed during fruiting initiation in the edible mushroom Agrocybe aegerita, and analysis of the predicted amino-acid sequence. Curr. Genet. 1997, 32(6):420-424.
6. Pires A.B., Gramacho K.P., Silva D.C., Goes-Neto A., Silva M.M., Muniz-Sobrinho J.S., Porto R.F., Villela-Dias C., Brendel M., Cascardo J.C., Pereira G.A. Early development of Moniliophthora perniciosa basidiomata and developmentally regulated genes. BMC Microbiol. 2009, 9:158.
7. Sakaguchi O., Yokota K., Kamaguchi A. Studies on the toxin of Aspergillus fumigatus. VIII. Biological properties of Asp-hemolysin, Nippon Saikingaku Zasshi. Jpn. J. Bacteriol. 1977, 32(6):821-828.
8. Nayak A.P., Blachere F.M., Hettick J.M., Lukomski S., Schmechel D., Beezhold D.H. Characterization of recombinant Terrelysin, a Hemolysin of Aspergillus terreus. Mycopathologia 2011, 171(1):23-34.
9. Vesper S.J., Vesper M.J. Possible role of fungal hemolysins in sick building syndrome. Adv. Appl. Microbiol. 2004, 55:191-213.
10. Rao J., DiGiandomenico A., Unger J., Bao Y., Polanowska-Grabowska R.K., Goldberg J.B. A novel oxidized low-density lipoprotein-binding protein from Pseudomonas aeruginosa. Microbiology 2008, 154:654-665.
11. Beutler B.A. TLRs and innate immunity. Blood 2009, 113:1399-1407.
12. Bogdan C. Nitric oxide and the immune response. Nat. Immunol. 2001, 2:907-916.
13. McClellan S.A., Huang X., Barrett R.P., Van R.N., Hazlett L.D. Macrophages restrict Pseudomonas aeruginosa growth, regulate polymorphonuclear neutrophil influx, and balance pro- and anti-inflammatory cytokines in BALB/c mice. J. Immunol. 2003, 170:5219-5227.
14. Murray T.S., Egan M., Kazmierczak B.I. Pseudomonas aeruginosa chronic colonization in cystic fibrosis patients. Curr. Opin. Pediatr. 2007, 19:83-88.
15. Wagner V.E., Iglewski B.H. P. aeruginosa biofilms in CF Infection. Clin. Rev. Allergy Immunol. 2008, 35:124-134.
16. Pruitt J., McManus A.T., Kim S.H., Goodwin C.W. Burn wound infections. Current Status World J. Surg. 1998, 22:135-145.
17. Bielecki P., Glik J., Kawecki M., Martins D.S. V, Towards understanding Pseudomonas aeruginosa burn wound infections by profiling gene expression. Biotechnol. Lett. 2008, 30:777-790.
18. Sadikot R.T., Blackwell T.S., Christman J.W., Prince A.S. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am. J. Respir. Crit. Care Med. 2005, 171:1209-1223.
19. Campodonico V.L., Gadjeva M., Paradis-Bleau C., Uluer A., Pier G.B. Airway epithelial control of Pseudomonas aeruginosa infection in cystic fibrosis. Trends Mol. Med. 2008, 14:120-133.
20. Cheminay C., Chakravortty D., Hensel M. Role of neutrophils in murine salmonellosis. Infect. Immun. 2004, 72:468-477.
21. Husain M., Bourret T.J., McCollister B.D., Jones-Carson J., Laughlin J., Vazquez-Torres A. Nitric oxide evokes an adaptive response to oxidative stress by arresting respiration. J. Biol. Chem. 2008, 283:7682-7689.
22. 2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol. 2007, 145:890-904.
23. Vishwanath S., Ramphal R., Guay C.M., DesJardins D., Pier G.B. Respiratory-mucin inhibition of the opsonophagocytic killing of Pseudomonas aeruginosa. Infect. Immun. 1988, 56:2218-2222.
24. MacMicking J., Xie Q.W., Nathan C. Nitric oxide and macrophage function. Annu. Rev. Immunol. 1997, 15:323-350.
25. Kooguchi K., Hashimoto S., Kobayashi A., Kitamura Y., Kudoh I., Wiener-Kronish J., Sawa T. Role of alveolar macrophages in initiation and regulation of inflammation in Pseudomonas aeruginosa pneumonia. Infect. Immun. 1998, 66:3164-3169.
26. Escotte S., Al A.D., Le N.R., Puchelle E., Guenounou M., Gangloff S.C. T cell chemotaxis and chemokine release after Staphylococcus aureus interaction with polarized airway epithelium. Am. J. Respir. Cell. Mol. Biol. 2006, 34:348-354.
27. Griess P. Bemerkungen zu der abhandlung der H.H. Weselsky und Benedikt. Ueber einige azoverbindungen. Ber. 1879, 12:426-428.
28. Lauber K., Bohn E., Krober S.M., Xiao Y.J., Blumenthal S.G., Lindemann R.K., Marini P., Wiedig C., Zobywalski A., Baksh S., Xu Y., Autenrieth I.B., Schulze-Osthoff K., Belka C., Stuhler G., Wesselborg S. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 2003, 113:717-730.
29. Petty R.D., Sutherland L.A., Hunter E.M., Cree I.A. Comparison of MTT and ATP-based assays for the measurement of viable cell number. J. Biolumin. Chemilumin. 1995, 10:29-34.
30. Beissbarth T., Speed T.P. GOstat: find statistically overrepresented gene ontologies within a group of genes. Bioinformatics 2004, 20:1464-1465.
31. J. Rao, A. DiGiandomenico, M. Artamonov, N. Leitinger, A.R. Amin, J.B. Goldberg, Host derived inflammatory phospholipids regulate rahU (PA0122) Gene, Protein, and Biofilm Formation in Pseudomonas aeruginosa, Cell Immunol. (2011), doi:10.1016/j.cellimm.2011.04.011.
32. An H., Xu H., Yu Y., Zhang M., Qi R., Yan X., Liu S., Wang W., Guo Z., Qin Z., Cao X. Up-regulation of TLR9 gene expression by LPS in mouse macrophages via activation of NF-[kappa]B, ERK and p38 MAPK signal pathways. Immunol. Lett. 2002, 81:165-169.
33. Zhu X., Chang M.S., Hsueh R.C., Taussig R., Smith K.D., Simon M.I., Choi S. Dual ligand stimulation of RAW 264.7 cells uncovers feedback mechanisms that regulate TLR-mediated gene expression. J. Immunol. 2006, 177:4299-4310.
34. Gao J.J., Diesl V., Wittmann T., Morrison D.C., Ryan J.L., Vogel S.N., Follettie M.T. Bacterial LPS and CpG DNA differentially induce gene expression profiles in mouse macrophages. J. Endotoxin Res. 2003, 9:237-243.
35. Sutterwala F.S., Mijares L.A., Li L., Ogura Y., Kazmierczak B.I., Flavell R.A. Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J. Exp. Med. 2007, 204:3235-3245.
36. Sutterwala F.S., Ogura Y., Flavell R.A. The inflammasome in pathogen recognition and inflammation. J. Leukoc. Biol. 2007, 82:259-264.
37. Barnes P.J. How corticosteroids control inflammation: Quintiles Prize Lecture 2005. Br. J. Pharmacol. 2006, 148:245-254.
38. Schneeweiss S., Setoguchi S., Weinblatt M.E., Katz J.N., Avorn J., Sax P.E., Levin R., Solomon D.H. Anti-tumor necrosis factor alpha therapy and the risk of serious bacterial infections in elderly patients with rheumatoid arthritis. Arthritis Rheum. 2007, 56:1754-1764.
39. Attur M.G., Patel R.N., Patel P.D., Abramson S.B., Amin A.R. Tetracycline up-regulates COX-2 expression and prostaglandin E2 production independent of its effect on nitric oxide. J. Immunol. 1999, 162:3160-3167.
40. Kota R.S., Rutledge J.C., Gohil K., Kumar A., Enelow R.I., Ramana C.V. Regulation of gene expression in RAW 264.7 macrophage cell line by interferon-gamma. Biochem. Biophys. Res. Commun. 2006, 342:1137-1146.
41. Ogura Y., Sutterwala F.S., Flavell R.A. The inflammasome: first line of the immune response to cell stress. Cell 2006, 126:659-662.
42. Pedra J.H., Cassel S.L., Sutterwala F.S. Sensing pathogens and danger signals by the inflammasome. Curr. Opin. Immunol. 2009, 21(1):10-16.
43. Hein T.W., Liao J.C., Kuo L. OxLDL specifically impairs endothelium-dependent, NO-mediated dilation of coronary arterioles. Am. J. Physiol. Heart Circul. Physiol. 2000, 278:H175-H183.
44. Chakravortty D., Hensel M. Inducible nitric oxide synthase and control of intracellular bacterial pathogens. Microbes. Infect. 2003, 5:621-627.
45. Chan J., Flynn J. Nitric Oxide in Mycobacterium tuberculosis, Infection. Nitric Oxide and Infection 1999, 281-307. Kluwer Academic/Plenum, New York. Fang (Ed.).
46. Karupiah G., Xie Q.W., Buller R.M., Nathan C., Duarte C., MacMicking J.D. Inhibition of viral replication by interferon-gamma-induced nitric oxide synthase. Science 1993, 261:1445-1448.
47. Clancy R.M., Amin A.R., Abramson S.B. The role of nitric oxide in inflammation and immunity. Arthritis Rheum. 1998, 41:1141-1151.
48. Nathan C., Xie Q.W. Nitric oxide synthases: roles, tolls, and controls. Cell 1994, 78:915-918.
49. Patel R.N., Attur M.G., Dave M.N., Patel I.V., Stuchin S.A., Abramson S.B., Amin A.R. A novel mechanism of action of chemically modified tetracyclines: inhibition of COX-2-mediated prostaglandin E2 production. J. Immunol. 1999, 163:3459-3467.
50. Patel R., Attur M.G., Dave M., Abramson S.B., Amin A.R. Regulation of cytosolic COX-2 and prostaglandin E2 production by nitric oxide in activated murine macrophages. J. Immunol. 1999, 162:4191-4197.
51. Winter C., Herbold W., Maus R., Langer F., Briles D.E., Paton J.C., Welte T., Maus U.A. Important role for C-C chemokine ligand 2-dependent lung mononuclear phagocyte recruitment to inhibit sepsis in mice infected with Streptococcus pneumoniae. J. Immunol. 2009, 182:4931-4937.
52. Elliott M.R., Chekeni F.B., Trampont P.C., Lazarowski E.R., Kadl A., Walk S.F., Park D., Woodson R.I., Ostankovich M., Sharma P., Lysiak J.J., Harden T.K., Leitinger N., Ravichandran K.S. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009, 461:282-286.
53. Truman L.A., Ford C.A., Pasikowska M., Pound J.D., Wilkinson S.J., Dumitriu I.E., Melville L., Melrose L.A., Ogden C.A., Nibbs R., Graham G., Combadiere C., Gregory C.D. CX3CL1/fractalkine is released from apoptotic lymphocytes to stimulate macrophage chemotaxis. Blood 2008, 112:5026-5036.
54. Zuzek M.C., Macek P., Sepcic K., Cestnik V., Frangez R. Toxic and lethal effects of ostreolysin, a cytolytic protein from edible oyster mushroom (Pleurotus ostreatus), in rodents. Toxicon 2006, 48:264-271.
55. Juarez-Perez V., Delecluse A. The cry toxins and the putative hemolysins of Clostridium bifermentans ser. malaysia are not involved in mosquitocidal activity. J. Invertebr. Pathol. 2001, 78:57-58.
56. Wei B., Huang T., Dalwadi H., Sutton C.L., Bruckner D., Braun J. Pseudomonas fluorescens encodes the Crohn's disease-associated I2 sequence and T-cell superantigen. Infect. Immun. 2002, 70:6567-6575.
57. Barbier M., Oliver A., Rao J., Hanna S.L., Goldberg J.B., Alberti S. Novel phosphorylcholine-containing protein of Pseudomonas aeruginosa chronic infection isolates interacts with airway epithelial cells. J. Infect. Dis. 2008, 197:465-473.
58. K. Takeda, S. Akira, Toll-like receptors, Curr. Protoc. Immunol. Chapter 14, (2007) Unit 14.12.
59. Chung J., Choi M.J., Jeong S.Y., Oh J.S., Kim H.K. Chemokines gene expression of RAW 264.7 cells by Actinobacillus actinomycetemcomitans lipopolysaccharide using microarray and RT-PCR analysis. Mol. Cells 2009, 27:257-261.
60. Diaz M.H., Shaver C.M., King J.D., Musunuri S., Kazzaz J.A., Hauser A.R. Pseudomonas aeruginosa induces localized immunosuppression during Pneumonia. Infect. Immun. 2008, 76:4414-4421.
61. Nathan C., Xie Q.W. Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 1994, 269:13725-13728.
62. Miller B.H., Fratti R.A., Poschet J.F., Timmins G.S., Master S.S., Burgos M., Marletta M.A., Deretic V. Mycobacteria inhibit nitric oxide synthase recruitment to phagosomes during macrophage infection. Infect. Immun. 2004, 72:2872-2878.
63. Mills P.C., Richardson D.J., Hinton J.C., Spiro S. Detoxification of nitric oxide by the flavorubredoxin of Salmonella enterica serovar Typhimurium. Biochem. Soc. Trans. 2005, 33:198-199.
64. Lavon I., Goldberg I., Amit S., Landsman L., Jung S., Tsuberi B.Z., Barshack I., Kopolovic J., Galun E., Bujard H., Ben Neriah Y. High susceptibility to bacterial infection, but no liver dysfunction, in mice compromised for hepatocyte NF-kappaB activation. Nat. Med. 2000, 6:573-577.
65. Matsumura M., Kakishita H., Suzuki M., Banba N., Hattori Y. Dexamethasone suppresses iNOS gene expression by inhibiting NF-kappaB in vascular smooth muscle cells. Life Sci. 2001, 69:1067-1077.
66. Serhan C.N., Yang R., Martinod K., Kasuga K., Pillai P.S., Porter T.F., Oh S.F., Spite M. Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions. J. Exp. Med. 2009, 206:15-23.
67. Nakano Y., Kasahara T., Mukaida N., Ko Y.C., Nakano M., Matsushima K. Protection against lethal bacterial infection in mice by monocyte-chemotactic and -activating factor. Infect. Immun. 1994, 62:377-383.
68. Kooguchi K., Hashimoto S., Kobayashi A., Kitamura Y., Kudoh I., Wiener-Kronish J., Sawa T. Role of alveolar macrophages in initiation and regulation of inflammation in Pseudomonas aeruginosa Pneumonia. Infect. Immun. 1998, 66:3164-3169.
69. Lyczak J.B., Cannon C.L., Pier G.B. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2000, 2:1051-1060.
70. Gouwy M., Struyf S., Noppen S., Schutyser E., Springael J.Y., Parmentier M., Proost P., Van Damme J. Synergy between coproduced C-C and C-X-C chemokines in monocyte chemotaxis through receptor-mediated events. Mol. Pharmacol. 2008, 74:485-495.
71. Luscinskas F.W., Gerszten R.E., Garcia-Zepeda E.A., Lim Y.C., Yoshida M., Ding H.A., Gimbrone M.A., Luster A.D., Rosenzweig A. C-C and C-X-C chemokines trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Ann. N Y. Acad. Sci. 2000, 902:288-293.
72. Bignold L.P., Rogers S.D., Siaw T.M., Bahnisch J. Inhibition of chemotaxis of neutrophil leukocytes to interleukin-8 by endotoxins of various bacteria. Infect. Immun. 1991, 59:4255-4258.
73. Frascaroli G., Varani S., Moepps B., Sinzger C., Landini M.P., Mertens T. Human cytomegalovirus subverts the functions of monocytes, impairing chemokine-mediated migration and leukocyte recruitment. J. Virol. 2006, 80:7578-7589.
74. Rinehart J.J., Balcerzak S.P., Sagone A.L., LoBuglio A.F. Effects of corticosteroids on human monocyte function. J. Clin. Invest. 1974, 54:1337-1343.