Skip to main content

Advertisement

SpringerLink
Log in

Oxidative stress by Helicobacter pylori causes apoptosis through mitochondrial pathway in gastric epithelial cells

  • Original Paper
  • Published:
Apoptosis Aims and scope Submit manuscript

Abstract

Helicobacter pylori is a gram negative bacterium that infects the human stomach of approximately half of the world’s population. It produces oxidative stress, and mitochondria are one of the possible targets and the major intracellular source of free radicals. The present study was aimed at determining mitochondrial alterations in H. pylori-infected gastric epithelial cells and its relationship with oxidative stress, one of the recognized causes of apoptotic processes. Cells were treated with a strain of H. pylori for 24 h. Cellular oxidative burst, antioxidant defense analysis, mitochondrial alterations and apoptosis-related processes were measured. Our data provide evidence on how superoxide acts on mitochondria to initiate apoptotic pathways, with these changes occurring in the presence of mitochondrial depolarization and other morphological and functional changes. Treatment of infected cells with Vitamin E prevented increases in intracellular ROS and mitochondrial damage consistent with H. pylori inducing a mitochondrial ROS mediated programmed cell death pathway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Allen LA (2000) Modulating phagocyte activation: the pros and cons of Helicobacter pylori virulence factors. J Exp Med 191:1451–1454. doi:10.1084/jem.191.9.1451

    Article  PubMed  CAS  Google Scholar 

  2. Montecucco C, Rappuoli R (2001) Living dangerously: how Helicobacter pylori survives in the human stomach. Nat Rev Mol Cell Biol 2:457–466. doi:10.1038/35073084

    Article  PubMed  CAS  Google Scholar 

  3. Willhite DC, Cover TL, Blanke SR (2003) Cellular vacuolation and mitochondrial cytochrome c release are independent outcomes of Helicobacter pylori vacuolating cytotoxin activity that are each dependent on membrane channel formation. J Biol Chem 278:48204–48209. doi:10.1074/jbc.M304131200

    Article  PubMed  CAS  Google Scholar 

  4. Peek RM Jr, Miller GG, Tham KT et al (1995) Heightened inflammatory response and cytokine expression in vivo to cagA+ Helicobacter pylori strains. Lab Invest 73:760–770

    PubMed  CAS  Google Scholar 

  5. Blaser MJ, Perez-Perez GI, Kleanthous H et al (1995) Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 55:2111–2115

    PubMed  CAS  Google Scholar 

  6. Oh TY, Yeo M, Han SU et al (2005) Synergism of Helicobacter pylori infection and stress on the augmentation of gastric mucosal damage and its prevention with alpha-tocopherol. Free Radic Biol Med 38:1447–1457. doi:10.1016/j.freeradbiomed.2005.02.005

    Article  PubMed  CAS  Google Scholar 

  7. Ding SZ, Minohara Y, Fan XJ et al (2007) Helicobacter pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect Immun 75:4030–4039. doi:10.1128/IAI.00172-07

    Article  PubMed  CAS  Google Scholar 

  8. Jones NL, Day AS, Jennings HA, Sherman PM (1999) Helicobacter pylori induces gastric epithelial cell apoptosis in association with increased Fas receptor expression. Infect Immun 67:4237–4242

    PubMed  CAS  Google Scholar 

  9. Ashktorab H, Frank S, Khaled AR, Durum SK, Kifle B, Smoot DT (2004) Bax translocation and mitochondrial fragmentation induced by Helicobacter pylori. Gut 53:805–813. doi:10.1136/gut.2003.024372

    Article  PubMed  CAS  Google Scholar 

  10. Kuck D, Kolmerer B, Iking-Konert C, Krammer PH, Stremmel W, Rudi J (2001) Vacuolating cytotoxin of Helicobacter pylori induces apoptosis in the human gastric epithelial cell line AGS. Infect Immun 69:5080–5087. doi:10.1128/IAI.69.8.5080-5087.2001

    Article  PubMed  CAS  Google Scholar 

  11. Peek RM Jr, Blaser MJ, Mays DJ et al (1999) Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle. Cancer Res 59:6124–6131

    PubMed  CAS  Google Scholar 

  12. Fan TJ, Han LH, Cong RS, Liang J (2005) Caspase family proteases and apoptosis. Acta Biochim Biophys Sin (Shanghai) 37:719–727. doi:10.1111/j.1745-7270.2005.00108.x

    Article  CAS  Google Scholar 

  13. Rudi J, Kuck D, Strand S et al (1998) Involvement of the CD95 (APO-1/Fas) receptor and ligand system in Helicobacter pylori-induced gastric epithelial apoptosis. J Clin Invest 102:1506–1514. doi:10.1172/JCI2808

    Article  PubMed  CAS  Google Scholar 

  14. Darzynkiewicz Z, Juan G, Li X, Gorczyca W, Murakami T, Traganos F (1997) Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry 27:1–20. doi :10.1002/(SICI)1097-0320(19970101)27:1<1::AID-CYTO2>3.0.CO;2-L

    Article  PubMed  CAS  Google Scholar 

  15. Palomba L, Sestili P, Columbaro M, Falcieri E, Cantoni O (1999) Apoptosis and necrosis following exposure of U937 cells to increasing concentrations of hydrogen peroxide: the effect of the poly(ADP-ribose)polymerase inhibitor 3-aminobenzamide. Biochem Pharmacol 58:1743–1750. doi:10.1016/S0006-2952(99)00271-3

    Article  PubMed  CAS  Google Scholar 

  16. Menaker RJ, Ceponis PJ, Jones NL (2004) Helicobacter pylori induces apoptosis of macrophages in association with alterations in the mitochondrial pathway. Infect Immun 72:2889–2898. doi:10.1128/IAI.72.5.2889-2898.2004

    Article  PubMed  CAS  Google Scholar 

  17. Maeda S, Yoshida H, Mitsuno Y et al (2002) Analysis of apoptotic and antiapoptotic signalling pathways induced by Helicobacter pylori. Mol Pathol 55:286–293. doi:10.1136/mp.55.5.286

    Article  PubMed  CAS  Google Scholar 

  18. Maeno E, Ishizaki Y, Kanaseki T, Hazama A, Okada Y (2000) Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci USA 97:9487–9492. doi:10.1073/pnas.140216197

    Article  PubMed  CAS  Google Scholar 

  19. Ormerod MG, Sun XM, Snowden RT, Davies R, Fearnhead H, Cohen GM (1993) Increased membrane permeability of apoptotic thymocytes: a flow cytometric study. Cytometry 14:595–602. doi:10.1002/cyto.990140603

    Article  PubMed  CAS  Google Scholar 

  20. Darzynkiewicz Z, Bruno S, Del Bino G et al (1992) Features of apoptotic cells measured by flow cytometry. Cytometry 13:795–808. doi:10.1002/cyto.990130802

    Article  PubMed  CAS  Google Scholar 

  21. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, van Oers MH (1994) Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84:1415–1420

    PubMed  CAS  Google Scholar 

  22. Zheng TS, Flavell RA (2000) Divinations and surprises: genetic analysis of caspase function in mice. Exp Cell Res 256:67–73. doi:10.1006/excr.2000.4841

    Article  PubMed  CAS  Google Scholar 

  23. Walker PR, LeBlanc J, Sikorska M (1997) Evidence that DNA fragmentation in apoptosis is initiated and propagated by single-strand breaks. Cell Death Differ 4:506–515. doi:10.1038/sj.cdd.4400273

    Article  PubMed  CAS  Google Scholar 

  24. Houghton J, Korah RM, Condon MR, Kim KH (1999) Apoptosis in Helicobacter pylori-associated gastric and duodenal ulcer disease is mediated via the Fas antigen pathway. Dig Dis Sci 44:465–478. doi:10.1023/A:1026628601284

    Article  PubMed  CAS  Google Scholar 

  25. Houghton J, Macera-Bloch LS, Harrison L, Kim KH, Korah RM (2000) Tumor necrosis factor alpha and interleukin 1beta up-regulate gastric mucosal Fas antigen expression in Helicobacter pylori infection. Infect Immun 68:1189–1195. doi:10.1128/IAI.68.3.1189-1195.2000

    Article  PubMed  CAS  Google Scholar 

  26. Zhang H, Fang DC, Lan CH, Luo YH (2007) Helicobacter pylori infection induces apoptosis in gastric cancer cells through the mitochondrial pathway. J Gastroenterol Hepatol 22:1051–1056. doi:10.1111/j.1440-1746.2007.04959.x

    Article  PubMed  CAS  Google Scholar 

  27. Kim KM, Lee SG, Park MG et al (2007) Gamma-glutamyltranspeptidase of Helicobacter pylori induces mitochondria-mediated apoptosis in AGS cells. Biochem Biophys Res Commun 355:562–567. doi:10.1016/j.bbrc.2007.02.021

    Article  PubMed  CAS  Google Scholar 

  28. Boya P, Roques B, Kroemer G (2001) New EMBO members’ review: viral and bacterial proteins regulating apoptosis at the mitochondrial level. EMBO J 20:4325–4331. doi:10.1093/emboj/20.16.4325

    Article  PubMed  CAS  Google Scholar 

  29. Yamasaki E, Wada A, Kumatori A et al (2006) Helicobacter pylori vacuolating cytotoxin induces activation of the proapoptotic proteins Bax and Bak, leading to cytochrome c release and cell death, independent of vacuolation. J Biol Chem 281:11250–11259. doi:10.1074/jbc.M509404200

    Article  PubMed  CAS  Google Scholar 

  30. Rajalingam K, Oswald M, Gottschalk K, Rudel T (2007) Smac/DIABLO is required for effector caspase activation during apoptosis in human cells. Apoptosis 12:1503–1510. doi:10.1007/s10495-007-0067-7

    Article  PubMed  CAS  Google Scholar 

  31. Shirin H, Sordillo EM, Oh SH et al (1999) Helicobacter pylori inhibits the G1 to S transition in AGS gastric epithelial cells. Cancer Res 59:2277–2281

    PubMed  CAS  Google Scholar 

  32. Bass DA, Parce JW, Dechatelet LR, Szejda P, Seeds MC, Thomas M (1983) Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. J Immunol 130:1910–1917

    PubMed  CAS  Google Scholar 

  33. Kosower NS, Kosower EM (1987) Thiol labeling with bromobimanes. Methods Enzymol 143:76–84. doi:10.1016/0076-6879(87)43015-2

    Article  PubMed  CAS  Google Scholar 

  34. Thorell B (1983) Flow-cytometric monitoring of intracellular flavins simultaneously with NAD(P)H levels. Cytometry 4:61–65. doi:10.1002/cyto.990040109

    Article  PubMed  CAS  Google Scholar 

  35. Poot M (2000) Multiparameter analysis of physiological changes in apoptosis. Curr Protoc Cytom 14(Suppl):9.15.11–17

    Google Scholar 

  36. Reers M, Smiley ST, Mottola-Hartshorn C, Chen A, Lin M, Chen LB (1995) Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol 260:406–417. doi:10.1016/0076-6879(95)60154-6

    Article  PubMed  CAS  Google Scholar 

  37. Mileykovskaya E, Dowhan W, Birke RL, Zheng D, Lutterodt L, Haines TH (2001) Cardiolipin binds nonyl acridine orange by aggregating the dye at exposed hydrophobic domains on bilayer surfaces. FEBS Lett 507:187–190. doi:10.1016/S0014-5793(01)02948-9

    Article  PubMed  CAS  Google Scholar 

  38. Lassus P, Opitz-Araya X, Lazebnik Y (2002) Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science 297:1352–1354. doi:10.1126/science.1074721

    Article  PubMed  CAS  Google Scholar 

  39. Pomorski T, Meyer TF, Naumann M (2001) Helicobacter pylori-induced prostaglandin E(2) synthesis involves activation of cytosolic phospholipase A(2) in epithelial cells. J Biol Chem 276:804–810. doi:10.1074/jbc.M003819200

    Article  PubMed  CAS  Google Scholar 

  40. Armstrong JS, Steinauer KK, Hornung B et al (2002) Role of glutathione depletion and reactive oxygen species generation in apoptotic signaling in a human B lymphoma cell line. Cell Death Differ 9:252–263. doi:10.1038/sj/cdd/4400959

    Article  PubMed  CAS  Google Scholar 

  41. Segal ED, Cha J, Lo J, Falkow S, Tompkins LS (1999) Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc Natl Acad Sci USA 96:14559–14564. doi:10.1073/pnas.96.25.14559

    Article  PubMed  CAS  Google Scholar 

  42. Bauer B, Moese S, Bartfeld S, Meyer TF, Selbach M (2005) Analysis of cell type-specific responses mediated by the type IV secretion system of Helicobacter pylori. Infect Immun 73:4643–4652. doi:10.1128/IAI.73.8.4643-4652.2005

    Article  PubMed  CAS  Google Scholar 

  43. Petrosillo G, Casanova G, Matera M, Ruggiero FM, Paradies G (2006) Interaction of peroxidized cardiolipin with rat-heart mitochondrial membranes: induction of permeability transition and cytochrome c release. FEBS Lett 580:6311–6316. doi:10.1016/j.febslet.2006.10.036

    Article  PubMed  CAS  Google Scholar 

  44. Gendron MC, Schrantz N, Metivier D et al (2001) Oxidation of pyridine nucleotides during Fas- and ceramide-induced apoptosis in Jurkat cells: correlation with changes in mitochondria, glutathione depletion, intracellular acidification and caspase 3 activation. Biochem J 353:357–367. doi:10.1042/0264-6021:3530357

    Article  PubMed  CAS  Google Scholar 

  45. Obst B, Wagner S, Sewing KF, Beil W (2000) Helicobacter pylori causes DNA damage in gastric epithelial cells. Carcinogenesis 21:1111–1115. doi:10.1093/carcin/21.6.1111

    Article  PubMed  CAS  Google Scholar 

  46. Smoot DT, Elliott TB, Verspaget HW et al (2000) Influence of Helicobacter pylori on reactive oxygen-induced gastric epithelial cell injury. Carcinogenesis 21:2091–2095. doi:10.1093/carcin/21.11.2091

    Article  PubMed  CAS  Google Scholar 

  47. Lim JW, Kim H, Kim JM, Kim JS, Jung HC, Kim KH (2004) Cellular stress-related protein expression in Helicobacter pylori-infected gastric epithelial AGS cells. Int J Biochem Cell Biol 36:1624–1634. doi:10.1016/j.biocel.2004.01.018

    Article  PubMed  CAS  Google Scholar 

  48. Bagchi D, McGinn TR, Ye X et al (2002) Helicobacter pylori-induced oxidative stress and DNA damage in a primary culture of human gastric mucosal cells. Dig Dis Sci 47:1405–1412. doi:10.1023/A:1015399204069

    Article  PubMed  CAS  Google Scholar 

  49. Teshima S, Rokutan K, Nikawa T, Kishi K (1998) Guinea pig gastric mucosal cells produce abundant superoxide anion through an NADPH oxidase-like system. Gastroenterology 115:1186–1196. doi:10.1016/S0016-5085(98)70090-3

    Article  PubMed  CAS  Google Scholar 

  50. Desouki MM, Kulawiec M, Bansal S, Das GM, Singh KK (2005) Cross talk between mitochondria and superoxide generating NADPH oxidase in breast and ovarian tumors. Cancer Biol Ther 4:1367–1373

    Article  PubMed  CAS  Google Scholar 

  51. Kudin AP, Bimpong-Buta NY, Vielhaber S, Elger CE, Kunz WS (2004) Characterization of superoxide-producing sites in isolated brain mitochondria. J Biol Chem 279:4127–4135. doi:10.1074/jbc.M310341200

    Article  PubMed  CAS  Google Scholar 

  52. Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552:335–344. doi:10.1113/jphysiol.2003.049478

    Article  PubMed  CAS  Google Scholar 

  53. Cadenas E, Davies KJ (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222–230. doi:10.1016/S0891-5849(00)00317-8

    Article  PubMed  CAS  Google Scholar 

  54. Zhang DX, Gutterman DD (2007) Mitochondrial reactive oxygen species-mediated signaling in endothelial cells. Am J Physiol Heart Circ Physiol 292:H2023–H2031. doi:10.1152/ajpheart.01283.2006

    Article  PubMed  CAS  Google Scholar 

  55. Correa P, Malcom G, Schmidt B et al (1998) Review article: antioxidant micronutrients and gastric cancer. Aliment Pharmacol Ther 12(Suppl 1):73–82. doi:10.1111/j.1365-2036.1998.00006.x

    Article  PubMed  CAS  Google Scholar 

  56. You WC, Zhang L, Gail MH et al (2000) Gastric dysplasia and gastric cancer: Helicobacter pylori, serum vitamin C, and other risk factors. J Natl Cancer Inst 92:1607–1612. doi:10.1093/jnci/92.19.1607

    Article  PubMed  CAS  Google Scholar 

  57. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12:913–922. doi:10.1007/s10495-007-0756-2

    Article  PubMed  CAS  Google Scholar 

  58. Paradies G, Petrosillo G, Pistolese M, Ruggiero FM (2002) Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene 286:135–141. doi:10.1016/S0378-1119(01)00814-9

    Article  PubMed  CAS  Google Scholar 

  59. Parone PA, Martinou JC (2006) Mitochondrial fission and apoptosis: an ongoing trial. Biochim Biophys Acta 1763:522–530. doi:10.1016/j.bbamcr.2006.04.005

    Article  PubMed  CAS  Google Scholar 

  60. Karbowski M, Youle RJ (2003) Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ 10:870–880. doi:10.1038/sj.cdd.4401260

    Article  PubMed  CAS  Google Scholar 

  61. Polyakov VY, Soukhomlinova MY, Fais D (2003) Fusion, fragmentation, and fission of mitochondria. Biochemistry (Mosc) 68:838–849. doi:10.1023/A:1025738712958

    Article  CAS  Google Scholar 

  62. Lee YJ, Jeong SY, Karbowski M, Smith CL, Youle RJ (2004) Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol Biol Cell 15:5001–5011. doi:10.1091/mbc.E04-04-0294

    Article  PubMed  CAS  Google Scholar 

  63. Perfettini JL, Roumier T, Kroemer G (2005) Mitochondrial fusion and fission in the control of apoptosis. Trends Cell Biol 15:179–183. doi:10.1016/j.tcb.2005.02.005

    Article  PubMed  CAS  Google Scholar 

  64. Rasola A, Bernardi P (2007) The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 12:815–833. doi:10.1007/s10495-007-0723-y

    Article  PubMed  CAS  Google Scholar 

  65. Isenberg JS, Klaunig JE (2000) Role of the mitochondrial membrane permeability transition (MPT) in rotenone-induced apoptosis in liver cells. Toxicol Sci 53:340–351. doi:10.1093/toxsci/53.2.340

    Article  PubMed  CAS  Google Scholar 

  66. Batandier C, Leverve X, Fontaine E (2004) Opening of the mitochondrial permeability transition pore induces reactive oxygen species production at the level of the respiratory chain complex I. J Biol Chem 279:17197–17204. doi:10.1074/jbc.M310329200

    Article  PubMed  CAS  Google Scholar 

  67. Cai J, Jones DP (1998) Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J Biol Chem 273:11401–11404. doi:10.1074/jbc.273.19.11401

    Article  PubMed  CAS  Google Scholar 

  68. Kim JS, He L, Lemasters JJ (2003) Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun 304:463–470. doi:10.1016/S0006-291X(03)00618-1

    Article  PubMed  CAS  Google Scholar 

  69. Justo P, Lorz C, Sanz A, Egido J, Ortiz A (2003) Intracellular mechanisms of cyclosporin A-induced tubular cell apoptosis. J Am Soc Nephrol 14:3072–3080. doi:10.1097/01.ASN.0000099383.57934.0E

    Article  PubMed  CAS  Google Scholar 

  70. Brenner C, Grimm S (2006) The permeability transition pore complex in cancer cell death. Oncogene 25:4744–4756. doi:10.1038/sj.onc.1209609

    Article  PubMed  CAS  Google Scholar 

  71. Grimm S, Brdiczka D (2007) The permeability transition pore in cell death. Apoptosis 12:841–855. doi:10.1007/s10495-007-0747-3

    Article  PubMed  CAS  Google Scholar 

  72. Kroemer G, Reed JC (2000) Mitochondrial control of cell death. Nat Med 6:513–519. doi:10.1038/74994

    Article  PubMed  CAS  Google Scholar 

  73. Xia T, Jiang C, Li L, Wu C, Chen Q, Liu SS (2002) A study on permeability transition pore opening and cytochrome c release from mitochondria, induced by caspase-3 in vitro. FEBS Lett 510:62–66. doi:10.1016/S0014-5793(01)03228-8

    Article  PubMed  CAS  Google Scholar 

  74. Ashktorab H, Neapolitano M, Bomma C et al (2002) In vivo and in vitro activation of caspase-8 and -3 associated with Helicobacter pylori infection. Microbes Infect 4:713–722. doi:10.1016/S1286-4579(02)01591-5

    Article  PubMed  CAS  Google Scholar 

  75. Zago EB, Castilho RF, Vercesi AE (2000) The redox state of endogenous pyridine nucleotides can determine both the degree of mitochondrial oxidative stress and the solute selectivity of the permeability transition pore. FEBS Lett 478:29–33. doi:10.1016/S0014-5793(00)01815-9

    Article  PubMed  CAS  Google Scholar 

  76. Aronis A, Komarnitsky R, Shilo S, Tirosh O (2002) Membrane depolarization of isolated rat liver mitochondria attenuates permeability transition pore opening and oxidant production. Antioxid Redox Signal 4:647–654. doi:10.1089/15230860260220157

    Article  PubMed  CAS  Google Scholar 

  77. Takeda K, Akira S (2003) Toll receptors and pathogen resistance. Cell Microbiol 5:143–153. doi:10.1046/j.1462-5822.2003.00264.x

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported in part by a grant 04062-00 from “Instituto de Ciencias de la Salud” J.C.C.M-Spain. M. Calvino was supported by a "Ayuda para incorporación de Jóvenes Investigadores a grupos de investigación de Castilla La Mancha" (JI05000) from J.C.C.M. and by a "Contrato de apoyo a la investigación en el SNS" from Instituto de Salud Carlos III (CA07/00157), Spain. S. Benito was supported by a "Ayuda para incorporación de Jóvenes Investigadores a grupos de investigación de Castilla La Mancha" (MV2007JI/18) from FISCAM-Spain.

Author information

Authors and Affiliations

  1. Hospital Universitario de Guadalajara, Unidad de Investigación, C/Donante de Sangre s/n19002, Guadalajara, Spain

    Miryam Calvino-Fernández, Selma Benito-Martínez & Trinidad Parra-Cid

Authors
  1. Miryam Calvino-Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Selma Benito-Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Trinidad Parra-Cid
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Miryam Calvino-Fernández.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Calvino-Fernández, M., Benito-Martínez, S. & Parra-Cid, T. Oxidative stress by Helicobacter pylori causes apoptosis through mitochondrial pathway in gastric epithelial cells. Apoptosis 13, 1267–1280 (2008). https://doi.org/10.1007/s10495-008-0255-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10495-008-0255-0

Keywords

Search

Navigation