Campylobacter jejuni cell lysates differently target mitochondria and lysosomes on HeLa cells

Apoptosis

Volumn 19, Issue 8, 2014, Pages 1225-1242

  Canonico, B ^a   Campana, R ^a   Luchetti, F ^a   Arcangeletti, M ^a   Betti, M ^a   Cesarini, E ^a   Ciacci, C ^a   Vittoria, E ^a   Galli, L ^a   Papa, S ^a   Baffone, W ^a  

^a UNIVERSITY OF URBINO   (Italy)

Author keywords

CCLys; CD54; Cell death; Lysosomes; Mitochondria; Modulation of CD59; P53

Indexed keywords

CARDIOLIPIN; CASPASE; CD59 ANTIGEN; CYTOLETHAL DISTENDING TOXIN; INTERCELLULAR ADHESION MOLECULE 1; PROTEIN BCL 2; PROTEIN P53; BACTERIAL TOXIN; CD63 ANTIGEN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1;

APOPTOSIS; ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; CAMPYLOBACTER ENTERITIS; CAMPYLOBACTER JEJUNI; CELL DEATH; CELL DEGENERATION; CELL LYSATE; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; DNA CONTENT; ENDOCYTOSIS; ENZYME ASSAY; ENZYME MECHANISM; FLOW CYTOMETRY; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INTERNALIZATION; LYSOSOME; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MONOLAYER CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; CYTOSOL; GENETICS; METABOLISM; MUTATION; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI;

ANTIGENS, CD63; APOPTOSIS; BACTERIAL TOXINS; CAMPYLOBACTER JEJUNI; CARDIOLIPINS; CASPASES; CYTOSOL; ENDOCYTOSIS; HELA CELLS; HUMANS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOMES; MITOCHONDRIA; MUTATION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84904268901     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-014-1005-0     Document Type: Article

References (73)

1. Sherman PM, Ossa JC, Wine E (2010) Bacterial infections: new and emerging enteric pathogens. Curr Opin Gastroenterol 26:1-4
2. Yabe S, Higuchi W, Iwao Y, Takano T, Razvina O, Reva I, Nishiyama A, Yamamoto T (2010) Molecular typing of Campylobacter jejuni and C. coli from chickens and patients with gastritis or Guillain-Barré syndrome based on multilocus sequence types and pulsed-field gel electrophoresis patterns. Microbiol Immunol 54:362-367
3. Kopecko DJ, Hu L, Zaal KJM (2001) Campylobacter jejuni - microtubule-dependent invasion. Trends Microbiol 9:389-396
4. Lindmark B, Rompikuntal PK, Vaitkevicius K, Song T, Mizunoe Y, Uhlin BE, Guerry P, Wai SN (2009) Outer membrane vesicle-mediated release of cytolethal distending toxin (CDT) from Campylobacter jejuni. BMC Microbiol 9:220-230
5. Pickett CL, Pesci EC, Cottle DL, Russell G, Erden AN, Zeytin H (1996) Prevalence of cytolethal distending toxin production in Campylobacter jejuni and relatedness Campylobacter sp. cdtB gene. Infect Immun 64:2070-2078 (Pubitemid 26165668)
6. Pickett CL, Whitehouse CA (1999) The cytolethal distending toxin family. Trends Microbiol 7:292-297 (Pubitemid 29304565)
7. Lara-Tejero M, Galán JE (2001) CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity. Infect Immun 69:4358-4365 (Pubitemid 32574433)
8. Mao X, DiRienzo JM (2002) Functional studies of the recombinant subunits of cytolethal distending holotoxin. Cell Microbiol 4:245-255 (Pubitemid 34413843)
9. Whitehouse CA, Balbo PB, Pesci EC, Cottle DL, Mirabito PM, Pickett CL (1998) Campylobacter jejuni cytolethal distending toxin causes a G2 phase cell cycle block. Infect Immun 66:1934-1940 (Pubitemid 28194085)
10. Shenker BJ, Hoffmaster RH, Zekavat A, Yamaguchi N, Lally ET, Demuth DR (2001) Induction of apoptosis in human T cells by Actinobacillus actinomycetemcomitans cytolethal distending toxin is a consequence of G2 arrest of the cell cycle. J Immunol 167:435-441 (Pubitemid 32567809)
11. Svensson LA, Tarkowski A, Thelestam M, Lagergård T (2001) The impact of Haemophilus ducrey cytolethal distending toxin on cells involved in the immune response. Microb Pathog 30:157-166 (Pubitemid 32564896)
12. Mathiasen IS, Jäättelä M (2002) Triggering caspase-independent cell death to combat cancer. Trends Mol Med 8:212-220 (Pubitemid 34493638)
13. Schmitt CA, Fridman JS, Yang M, Baranov E, Hoffman RM, Lowe SW (2002) Dissecting p53 tumor suppressor functions in vivo. Cancer Cell 1:289-298 (Pubitemid 41039153)
14. Owen-Schaub LB, Zhang W, Cusack JC, Angelo LS, Santee SM, Fujiwara T, Roth JA, Deisseroth AB, Zhang WW, Kruzel E, Radinsky R (1995) Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol Cell Biol 15:3032-3040
15. Müller M, Wilder S, Bannasch D, Israeli D, Lehlbach K, Li-Weber M, Friedman SL, Galle PR, Stremmel W, Oren M, Krammer PH (1998) p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J Exp Med 188:2033-2045
16. Miyashita T, Reed JC (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80:293-299
17. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, Tokino T, Taniguchi T, Tanaka N (2000) Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53- induced apoptosis. Science 288:1053-1058 (Pubitemid 30324238)
18. Schuler M, Bossy-Wetzel E, Goldstein JC, Fitzgerald P, Green DR (2000) p53 induces apoptosis by caspase activation through mitochondrial cytochrome c release. J Biol Chem 275:7337-7342 (Pubitemid 30146286)
19. Nalca A, Rangnekar VM (1998) The G1-phase growth arresting action of interleukin-1 is independent of p53 and p21/WAF1 function. J Biol Chem 273:30517-30523 (Pubitemid 28545527)
20. Gotlieb WH, Watson JM, Rezai A, Johnson M, Martínez-Maza O, Berek JS (1994) Cytokine-induced modulation of tumor suppressor gene expression in ovarian cancer cells: up-regulation of p53 gene expression and induction of apoptosis by tumor necrosis factor-alpha. Am J Obstet Gynecol 170:1121-1128
21. Ma W, Pobe JS (1998) Human endothelial cells effectively costimulate cytokine production by, but not differentiation of, naive CD4+ T cells. J Immunol 161:2158-2167 (Pubitemid 28397025)
22. Takami A, Zeng W, Wang H, Matsuda T, Nakao S (1999) Cytotoxicity against lymphoblastoid cells mediated by a T-cell clone from an aplastic anaemia patient: role of CD59 on target cells. Br J Haematol 107:791-796 (Pubitemid 30020152)
23. Liversidge J, Dawson R, Hoey S, McKay D, Grabowski P, Forrester JV (1996) CD59 and CD48 expressed by rat retinal pigment epithelial cells are major ligands for the CD2-mediated alternative pathway of T cell activation. J Immunol 156:3696-3703 (Pubitemid 26139941)
24. Sampaziotis F, Kokotas S, Gorgoulis VG (2002) p53 possibly upregulates the expression of CD58 (LFA-3) and CD59 (MIRL). Med Hypotheses 58:136-140 (Pubitemid 34174423)
25. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422:37-44 (Pubitemid 36323287)
26. Cossart P, Sansonetti PJ (2004) Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242-248 (Pubitemid 38452169)
27. Bang DD, Nielsen EM, Scheutz F, Pedersen K, Handberg K, Madsen M (2003) PCR detection of seven virulence and toxin genes of Campylobacter jejuni and Campylobacter coli isolates from Danish pigs and cattle and cytolethal distending toxin production of the isolates. J Appl Microbiol 94:1003-1014 (Pubitemid 36649021)
28. -immature human NK cell subset. Cytometry A 75:893-901
29. Brando B, Barnett D, Janossy G, Mandy F, Autran B, Rothe G, Scarpati B, D'Avanzo G, D'Hautcourt JL, Lenkei R, Schmitz G, Kunkl A, Chianese R, Papa S, Gratama JW (2000) Cytofluorometric methods for assessing absolute numbers of cell subsets in blood. European Working Group on Clinical Cell Analysis. Cytometry 42:327-346 (Pubitemid 32047563)
30. Gratama JW, Menéndez P, Kraan J, Orfao A (2000) Loss of CD34(+) hematopoietic progenitor cells due to washing can be reduced by the use of fixative-free erythrocyte lysing reagents. J Immunol Methods 239:13-23 (Pubitemid 30256014)
31. Luchetti F, Canonico B, Mannello F, Masoni C, D'Emilio A, Battistelli M, Papa S, Falcieri E (2007) Melatonin reduces early changes in intramitochondrial cardiolipin during apoptosis in U937 cell line. Toxicol In Vitro 21:293-301 (Pubitemid 46205074)
32. Luchetti F, Betti M, Canonico B, Arcangeletti M, Ferri P, Galli F, Papa S (2009) ERK MAPK activation mediates the antiapoptotic signaling of melatonin in UVB-stressed U937 cells. Free Radic Biol Med 46:339-351
33. Canonico B, Betti M, Luchetti F, Battistelli M, Falcieri E, Ferri P, Zamai L, Barnett D, Papa S (2010) Flow cytometric profiles, biomolecular and morphological aspects of transfixed leukocytes and red cells. Cytometry B Clin Cytom 78:267-278
34. Donev RM, Cole DS, Sivasankar B, Hughes TR, Morgan BP (2006) p53 regulates cellular resistance to complement lysis through enhanced expression of CD59. Cancer Res 66:2451-2458
35. Scott NE, Parker BL, Connolly AM, Paulech J, Edwards AV, Crossett B, Falconer L, Kolarich D, Djordjevic SP, Højrup P, Packer NH, Larsen MR, Cordwell SJ (2011) Simultaneous gly-can- peptide characterization using hydrophilic interaction chromatography and parallel fragmentation by CID, higher energy collisional dissociation, and electron transfer dissociation MS applied to the N-linked glycoproteome of Campylobacter jejuni. Mol Cell Proteomics 10:M000031-MCP201
36. Volokhov D, Chizhikov V, Chumakov K, Rasooly A (2003) Microarray-based identification of thermophilic Campylobacter jejuni, C. coli, C. lari, and C. upsaliensis. J Clin Microbiol 41:4071-4080 (Pubitemid 37099667)
37. Asakura M, Samosornsuk W, Hinenoya A, Misawa N, Nishimura K, Matsuhisa A, Yamasaki S (2008) Development of a cytolethal distending toxin (cdt) gene-based species-specific multiplex PCR assay for the detection and identification of Campylobacter jejuni, Campylobacter coli and Campylobacter fetus. FEMS Immunol Med Microbiol 52:260-266 (Pubitemid 351248431)
38. Nakajima T, Hirayama J, Tazumi A, Hayashi K, Tasaki E, Asakura M, Yamasaki S, Moore JE, Millar BC, Matsuda M (2012) Comparative analysis of Campylobacter lari cytolethal distending toxin (CDT) effect on HeLa cells. J Basic Microbiol 52:559-565
39. Karlyshev AV, Wren BW (2001) Detection and initial characterization of novel capsular polysaccharide among diverse Campylobacter jejuni strains using alcian blue dye. J Clin Microbiol 39:279-284 (Pubitemid 32059604)
40. Hickey TE, McVeigh AL, Scott DA, Michielutti RE, Bixby A, Carroll SA, Bourgeois AL, Guerry P (2000) Campylobacter jejuni cytolethal distending toxin mediates release of interleukin-8 from intestinal epithelial cells. Infect Immun 68:6535-6541 (Pubitemid 32463351)
41. Heywood W, Henderson B, Nair SP (2005) Cytolethal distending toxin: creating a gap in the cell cycle. J Med Microbiol 54:207-216 (Pubitemid 40879610)
42. McSweeney LA, Dreyfus LA (2004) Nuclear localization of the Escherichia coli cytolethal distending toxin CdtB subunit. Cell Microbiol 6:447-458 (Pubitemid 38488937)
43. Cortes-Bratti X, Karlsson C, Lagergård T, Thelestam M, Frisan T (2001) The Haemophilus ducreyi cytolethal distending toxin induces cell-cycle arrest and apoptosis via the DNA damage checkpoint pathways. J Biol Chem 276:5296-5302
44. Sugai M, Kawamoto T, Pérès SY, Ueno Y, Komatsuzawa H, Fujiwara T, Kurihara H, Suginaka H, Oswald E (1998) The cell cycle-specific growth-inhibitory factor produced by Actinobacillus actinomycetemcomitans is a cytolethal distending toxin. Infect Immun 66:5008-5019 (Pubitemid 28453114)
45. Sato T, Koseki T, Yamato K, Saiki K, Konishi K, Yoshikawa M, Ishikawa I, Nishihara T (2002) p53-independent expression of p21(CIP1/WAF1) in plasmacytic cells during G(2) cell cycle arrest induced by Actinobacillus actinomycetemcomitans cytolethal distending toxin. Infect Immun 70:528-534 (Pubitemid 34083810)
46. Deng K, Latimer JL, Lewis DA, Hansen EJ (2001) Investigation of the interaction among the components of the cytolethal distending toxin of Haemophilus ducreyi. Biochem Biophys Res Commun 285:609-615 (Pubitemid 32924814)
47. Ueno Y, Ohara M, Kawamoto T, Fujiwara T, Komatsuzawa H, Oswald E, Sugai M (2006) Biogenesis of the Actinobacillus actinomycetemcomitans cytolethal distending toxin holotoxin. Infect Immun 74:3480-3487 (Pubitemid 43794538)
48. Lindmark B, Rompikuntal PK, Vaitkevicius K, Song T, Mizunoe Y, Uhlin BE, Guerry P, Wai SN (2009) Outer membrane vesicle-mediated release of cytolethal distending toxin (CDT) from Campylobacter jejuni. BMC Microbiol 9:220-230
49. Elmi A, Watson E, Sandu P, Gundogdu O, Mills DC, Inglis NF, Manson E, Imrie L, Bajaj-Elliott M, Wren BW, Smith DGE, Dorrell N (2012) Campylobacter jejuni outer membrane vesicles play an important role in bacterial interactions with human intestinal epithelial cells. Infect Immun 80:4089-4098
50. Taylor RC, Cullen SP, Martin SJ (2008) Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 19:231-241 (Pubitemid 351301823)
51. Creagh EM, Conroy H, Martin SJ (2003) Caspase-activation pathways in apoptosis and immunity. Immunol Rev 193:10-21 (Pubitemid 36688035)
52. De Melo MA, Gabbiani G, Pechere JC (1989) Cellular events and intracellular survival of Campylobacter jejuni during infection of HEp-2 cells. Infect Immun 57:2214-2222 (Pubitemid 19186905)
53. Gao JX, Ma BL, Xie YL, Huang DS (1991) Electron microscopic appearance of the chronic Campylobacter jejuni enteritis of mice. Chin Med J (Engl) 104:1005-1010
54. Humphrey CD, Montag DM, Pittman FE (1986) Morphologic observations of experimental Campylobacter jejuni infection in the hamster intestinal tract. Am J Pathol 122:152-159 (Pubitemid 16108556)
55. Newell DG, Pearson A (1984) The invasion of epithelial cell lines and the intestinal epithelium of infant mice by Campylobacter jejuni/coli. J Diarrhoeal Dis Res 2:19-26
56. Blanke SR (2005) Micro-managing the executioner: pathogen targeting of mitochondria. Trends Microbiol 13:64-71
57. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479-489 (Pubitemid 27508237)
58. Brunk UT, Dalen H, Roberg K, Hellquist HB (1997) Photo-oxidative disruption of lysosomal membranes causes apoptosis of cultured human fibroblasts. Free Radic Biol Med 23:616-626 (Pubitemid 27287345)
59. Brunk UT, Svensson I (1999) Oxidative stress, growth factor starvation and Fas activation may all cause apoptosis through lysosomal leak. Redox Rep 4:3-11
60. Neuzil J, Svensson I, Weber T, Weber C, Brunk UT (1999) alpha-tocopheryl succinate-induced apoptosis in Jurkat T cells involves caspase-3 activation, and both lysosomal and mitochondrial destabilisation. FEBS Lett 445:295-300 (Pubitemid 29117231)
61. Li W, Yuan X, Nordgren G, Dalen H, Dubowchik GM, Firestone RA, Brunk UT (2000) Induction of cell death by the lysosomotropic detergent MSDH. FEBS Lett 470:35-39 (Pubitemid 30155619)
62. Yuan XM, Li W, Brunk UT, Dalen H, Chang YH, Sevanian A (2000) Lysosomal destabilization during macrophage damage induced by cholesterol oxidation products. Free Radic Biol Med 28:208-218 (Pubitemid 30084013)
63. Kågedal K, Zhao M, Svensson I, Brunk UT (2001) Sphingosine-induced apoptosis is dependent on lysosomal proteases. Biochem J 359:335-343 (Pubitemid 32999777)
64. 2 is a consequence of lysosomal rupture. Biochem J 356:549-555
65. Zdolsek JM, Olsson GM, Brunk UT (1990) Photooxidative damage to lysosomes of cultured macrophages by acridine orange. Photochem Photobiol 51:67-76
66. Brunk UT, Neuzil J, Eaton JW (2001) Lysosomal involvement in apoptosis. Redox Rep 6:91-97 (Pubitemid 32519816)
67. Zhao M, Brunk UT, Eaton JW (2001) Delayed oxidant-induced cell death involves activation of phospholipase A2. FEBS Lett 509:399-404 (Pubitemid 34031968)
68. Guicciardi ME, Deussing J, Miyoshi H, Bronk SF, Svingen PA, Peters C, Kaufmann SH, Gores GJ (2000) Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J Clin Invest 106:1127-1137
69. Stoka V, Turk B, Schendel SL, Kim TH, Cirman T, Snipas SJ, Ellerby LM, Bredesen D, Freeze H, Abrahamson M, Bromme D, Krajewski S, Reed JC, Yin XM, Turk V, Salvesen GS (2001) Lysosomal protease pathways to apoptosis. Cleavage of bid, not pro-caspases, is the most likely route. J Biol Chem 276:3149-3157
70. Gorgoulis VG, Zacharatos P, Kotsinas A, Kletsas D, Mariatos G, Zoumpourlis V, Ryan KM, Kittas C, Papavassiliou AG (2003) p53 activates ICAM-1 (CD54) expression in an NF-kappaB-independent manner. EMBO J 22:1567-1578 (Pubitemid 36417405)
71. Tamai R, Asai Y, Ogawa T (2005) Requirement for intercellular adhesion molecule 1 and caveolae in invasion of human oral epithelial cells by Porphyromonas gingivalis. Infect Immun 73:6290-6298 (Pubitemid 41368790)
72. Yakes FM, Wamil BD, Sun F, Yan HP, Carter CE, Hellerqvist CG (2000) CM101 treatment overrides tumor-induced immuno-privilege leading to apoptosis. Cancer Res 60:5740-5746
73. Amano A, Takeuchi H, Furuta N (2010) Outer membrane vesicles function as offensive weapons in hoste-parasite interactions. Microbes Infect 12:791-798