N-terminal region of Mannheimia haemolytica leukotoxin serves as a mitochondrial targeting signal in mammalian cells

Cellular Microbiology

Volumn 12, Issue 7, 2010, Pages 976-987

  Kisiela, Dagmara I ^a,b   Aulik, Nicole A ^a   Atapattu, Dhammika N ^a   Czuprynski, Charles J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; CARRIER PROTEIN; CYTOCHROME C; EXOTOXIN; GREEN FLUORESCENT PROTEIN; HEMOLYSIN; HYBRID PROTEIN; LEUKOTOXIN; MANNHEIMIA HAEMOLYTICA LEUKOTOXIN; MITOCHONDRIAL TARGETING SIGNAL TOXIN; UNCLASSIFIED DRUG;

ACTINOBACILLUS PLEUROPNEUMONIAE; AGGREGATIBACTER ACTINOMYCETEMCOMITANS; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; ESCHERICHIA COLI; IMMUNOPRECIPITATION; MAMMAL CELL; MANNHEIMIA HAEMOLYTICA; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ANIMALS; BACTERIAL TOXINS; CATTLE; CELL LINE; CERCOPITHECUS AETHIOPS; COMPUTATIONAL BIOLOGY; COS CELLS; IMMUNOPRECIPITATION; MANNHEIMIA HAEMOLYTICA; MICROSCOPY, CONFOCAL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROTEIN BINDING;

ACTINOBACILLUS PLEUROPNEUMONIAE; ESCHERICHIA COLI; MAMMALIA; MANNHEIMIA HAEMOLYTICA;

EID: 77954431690     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01445.x     Document Type: Article

References (61)

1. Ambagala TC, Ambagala AP, Srikumaran S. The leukotoxin of Pasteurella haemolytica binds to beta(2) integrins on bovine leukocytes. FEMS Microbiol Lett 1999, 179:161-167.
2. Atapattu DN, Czuprynski CJ. Mannheimia haemolytica leukotoxin induces apoptosis of bovine lymphoblastoid cells (BL-3) via a caspase-9-dependent mitochondrial pathway. Infect Immun 2005, 73:5504-5513.
3. Atapattu DN, Czuprynski CJ. Mannheimia haemolytica leukotoxin binds to lipid rafts in bovine lymphoblastoid cells and is internalized in a dynamin-2- and clathrin-dependent manner. Infect Immun 2007, 75:4719-4727.
4. Atapattu DN, Albrecht RM, McClenahan DJ, Czuprynski CJ. Dynamin-2-dependent targeting of Mannheimia haemolytica leukotoxin to mitochondrial cyclophilin D in bovine lymphoblastoid cells. Infect Immun 2008, 76:5357-5365.
5. Bauer ME, Welch RA. Characterization of an RTX toxin from enterohemorrhagic Escherichia coli O157:H7. Infect Immun 1996, 64:167-175.
6. Becker T, Vogtle FN, Stojanovski D, Meisinger C. Sorting and assembly of mitochondrial outer membrane proteins. Biochim Biophys Acta 2008, 1777:557-563.
7. Bellot G, Cartron PF, Er E, Oliver L, Juin P, Armstrong LC. TOM22, a core component of the mitochondria outer membrane protein translocation pore, is a mitochondrial receptor for the proapoptotic protein Bax. Cell Death Differ 2007, 14:785-794.
8. Blanke SR. Micro-managing the executioner: pathogen targeting of mitochondria. Trends Microbiol 2005, 13:64-71.
9. Braun JS, Hoffmann O, Schickhaus M, Freyer D, Dagand E, Bermpohl D. Pneumolysin causes neuronal cell death through mitochondrial damage. Infect Immun 2007, 75:4245-4254.
10. Bryson K, McGuffin LJ, Marsden RL, Ward JJ, Sodhi JS, Jones DT. Protein structure prediction servers at University College London. Nucleic Acids Res 2005, 33:W36-W38.
11. Cartron PF, Bellot G, Oliver L, Grandier-Vazeille X, Manon S, Vallette FM. Bax inserts into the mitochondrial outer membrane by different mechanisms. FEBS Lett 2008, 582:3045-3051.
12. Chang YF, Young R, Struck DK. Cloning and characterization of a hemolysin gene from Actinobacillus (Haemophilus) pleuropneumoniae. DNA 1989, 8:635-647.
13. Chang YF, Shi J, Ma DP, Shin SJ, Lein DH. Molecular analysis of the Actinobacillus pleuropneumoniae RTX toxin-III gene cluster. DNA Cell Biol 1993, 12:351-362.
14. Choi CH, Lee EY, Lee YC, Park TI, Kim HJ, Hyun SH. Outer membrane protein 38 of Acinetobacter baumannii localizes to the mitochondria and induces apoptosis of epithelial cells. Cell Microbiol 2005, 7:1127-1138.
15. Claros MG, Vincens P. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 1996, 241:779-786.
16. Clinkenbeard KD, Mosier DA, Confer AW. Transmembrane pore size and role of cell swelling in cytotoxicity caused by Pasteurella haemolytica leukotoxin. Infect Immun 1989, 57:420-425.
17. Cudd LA, Ownby CL, Clarke CR, Sun Y, Clinkenbeard KD. Effects of Mannheimia haemolytica leukotoxin on apoptosis and oncosis of bovine neutrophils. Am J Vet Res 2001, 62:136-141.
18. Czuprynski CJ, Noel EJ, Ortiz-Carranza O, Srikumaran S. Activation of bovine neutrophils by partially purified Pasteurella haemolytica leukotoxin. Infect Immun 1991, 59:3126-3133.
19. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 2004, 116:205-219.
20. Felmlee T, Pellett S, Welch RA. Nucleotide sequence of an Escherichia coli chromosomal hemolysin. J Bacteriol 1985, 163:94-105.
21. Frank GH, Smith PC. Prevalence of Pasteurella haemolytica in transported calves. Am J Vet Res 1983, 44:981-985.
22. Frey J, Deillon JB, Gygi D, Nicolet J. Identification and partial characterization of the hemolysin (HlyII) of Actinobacillus pleuropneumoniae serotype 2. Vet Microbiol 1991, 28:303-312.
23. Galmiche A, Rassow J, Doye A, Cagnol S, Chambard JC, Contamin S. The N-terminal 34 kDa fragment of Helicobacter pylori vacuolating cytotoxin targets mitochondria and induces cytochrome c release. EMBO J 2000, 19:6361-6370.
24. Glaser P, Sakamoto H, Bellalou J, Ullmann A, Danchin A. Secretion of cyclolysin, the calmodulin-sensitive adenylate cyclase-haemolysin bifunctional protein of Bordetella pertussis. EMBO J 1988, 7:3997-4004.
25. He D, Hagen SJ, Pothoulakis C, Chen M, Medina ND, Warny M, LaMont JT. Clostridium difficile toxin A causes early damage to mitochondria in cultured cells. Gastroenterology 2000, 119:139-150.
26. von Heijne G. Mitochondrial targeting sequences may form amphiphilic helices. EMBO J 1986, 5:1335-1342.
27. Jansen R, Briaire J, Kamp EM, Gielkens AL, Smits MA. Cloning and characterization of the Actinobacillus pleuropneumoniae-RTX-toxin III (ApxIII) gene. Infect Immun 1993, 61:947-954.
28. Jones DT. Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 1999, 292:195-202.
29. Kenny B. Mechanism of action of EPEC type III effector molecules. Int J Med Microbiol 2002, 291:469-477.
30. Kenny B, Jepson M. Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell Microbiol 2000, 2:579-590.
31. Khalimonchuk O, Rodel G. Biogenesis of cytochrome c oxidase. Mitochondrion 2005, 5:363-388.
32. Kozjak-Pavlovic V, Ross K, Rudel T. Import of bacterial pathogenicity factors into mitochondria. Curr Opin Microbiol 2008, 11:9-14.
33. Kunkele KP, Heins S, Dembowski M, Nargang FE, Benz R, Thieffry M. The preprotein translocation channel of the outer membrane of mitochondria. Cell 1998, 93:1009-1019.
34. Lalier L, Cartron PF, Juin P, Nedelkina S, Manon S, Bechinger B, Vallette FM. Bax activation and mitochondrial insertion during apoptosis. Apoptosis 2007, 12:887-896.
35. Lally ET, Golub EE, Kieba IR, Taichman NS, Rosenbloom J, Rosenbloom JC. Analysis of the Actinobacillus actinomycetemcomitans leukotoxin gene. Delineation of unique features and comparison to homologous toxins. J Biol Chem 1989, 264:15451-15456.
36. Lawrence PK, Nelson WR, Liu W, Knowles DP, Foreyt WJ, Srikumaran S. beta(2) Integrin Mac-1 is a receptor for Mannheimia haemolytica leukotoxin on bovine and ovine leukocytes. Vet Immunol Immunopathol 2008, 122:285-294.
37. Leung AW, Halestrap AP. Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore. Biochim Biophys Acta 2008, 1777:946-952.
38. Lin W, Fullner KJ, Clayton R, Sexton JA, Rogers MB, Calia KE. Identification of a Vibrio cholerae RTX toxin gene cluster that is tightly linked to the cholera toxin prophage. Proc Natl Acad Sci USA 1999, 96:1071-1076.
39. Lucattini R, Likic VA, Lithgow T. Bacterial proteins predisposed for targeting to mitochondria. Mol Biol Evol 2004, 21:652-658.
40. Maheswaran SK, Weiss DJ, Kannan MS, Townsend EL, Reddy KR, Whiteley LO, Srikumaran S. Effects of Pasteurella haemolytica A1 leukotoxin on bovine neutrophils: degranulation and generation of oxygen-derived free radicals. Vet Immunol Immunopathol 1992, 33:51-68.
41. Matarrese P, Falzano L, Fabbri A, Gambardella L, Frank C, Geny B. Clostridium difficile toxin B causes apoptosis in epithelial cells by thrilling mitochondria. Involvement of ATP-sensitive mitochondrial potassium channels. J Biol Chem 2007, 282:9029-9041.
42. Matouschek A, Rospert S, Schmid K, Glick BS, Schatz G. Cyclophilin catalyzes protein folding in yeast mitochondria. Proc Natl Acad Sci USA 1995, 92:6319-6323.
43. Meisinger C, Brix J, Model K, Pfanner N, Ryan MT. The preprotein translocase of the outer mitochondrial membrane: receptors and a general import pore. Cell Mol Life Sci 1999, 56:817-824.
44. Muller A, Gunther D, Brinkmann V, Hurwitz R, Meyer TF, Rudel T. Targeting of the pro-apoptotic VDAC-like porin (PorB) of Neisseria gonorrhoeae to mitochondria of infected cells. EMBO J 2000, 19:5332-5343.
45. Nagai T, Abe A, Sasakawa C. Targeting of enteropathogenic Escherichia coli EspF to host mitochondria is essential for bacterial pathogenesis: critical role of the 16th leucine residue in EspF. J Biol Chem 2005, 280:2998-3011.
46. Nakamura Y, Suzuki H, Sakaguchi M, Mihara K. Targeting and assembly of rat mitochondrial translocase of outer membrane 22 (TOM22) into the TOM complex. J Biol Chem 2004, 279:21223-21232.
47. Nougayrede JP, Donnenberg MS. Enteropathogenic Escherichia coli EspF is targeted to mitochondria and is required to initiate the mitochondrial death pathway. Cell Microbiol 2004, 6:1097-1111.
48. Papatheodorou P, Domanska G, Oxle M, Mathieu J, Selchow O, Kenny B, Rassow J. The enteropathogenic Escherichia coli (EPEC) Map effector is imported into the mitochondrial matrix by the TOM/Hsp70 system and alters organelle morphology. Cell Microbiol 2006, 8:677-689.
49. Rapaport D. Finding the right organelle. Targeting signals in mitochondrial outer-membrane proteins. EMBO Rep 2003, 4:948-952.
50. Rapaport D, Neupert W, Lill R. Mitochondrial protein import. Tom40 plays a major role in targeting and translocation of preproteins by forming a specific binding site for the presequence. J Biol Chem 1997, 272:18725-18731.
51. Rassow J, Mohrs K, Koidl S, Barthelmess IB, Pfanner N, Tropschug M. Cyclophilin 20 is involved in mitochondrial protein folding in cooperation with molecular chaperones Hsp70 and Hsp60. Mol Cell Biol 1995, 15:2654-2662.
52. Reid GA, Walker ME. Mitochondrial protein targeting signals. Biochem Soc Trans 1988, 16:709-710.
53. Saier MH, Yamada M, Suda K, Erni B, Rak B, Lengeler J. Bacterial proteins with N-terminal leader sequences resembling mitochondrial targeting sequences of eukaryotes. Biochimie 1988, 70:1743-1748.
54. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual 2001, New York, Cold Spring Harbor Laboratory Press
55. Shanthalingham S, Srikumaran S. Intact signal peptide of CD18, the beta subunit of β2 integrins, renders ruminants susceptible to Mannheimia haemolytica leukotoxin. Proc Natl Acad Sci USA 2009, 106:15448-15453.
56. Shewen PE, Wilkie BN. Cytotoxin of Pasteurella haemolytica acting on bovine leukocytes. Infect Immun 1982, 35:91-94.
57. Stins MF, Prasadarao NV, Zhou J, Arditi M, Kim KS. Bovine brain microvascular endothelial cells transfected with SV40-large T antigen: development of an immortalized cell line to study pathophysiology of CNS disease. In Vitro Cell Dev Biol Anim 1997, 33:243-247.
58. Tsujimoto Y, Shimizu S. Role of the mitochondrial membrane permeability transition in cell death. Apoptosis 2007, 12:835-840.
59. Welch RA. RTX toxin structure and function: a story of numerous anomalies and few analogies in toxin biology. Curr Top Microbiol Immunol 2001, 257:85-111.
60. Welch RA, Bauer ME, Kent AD, Leeds JA, Moayeri M, Regassa LB, Swenson DL. Battling against host phagocytes: the wherefore of the RTX family of toxins? Infect Agents Dis 1995, 4:254-272.
61. Zaharik ML, Gruenheid S, Perrin AJ, Finlay BB. Delivery of dangerous goods: type III secretion in enteric pathogens. Int J Med Microbiol 2002, 291:593-603.