Helicobacter pylori perturbs iron trafficking in the epithelium to grow on the cell surface
Open accessAbstract
Helicobacter pylori (Hp) injects the CagA effector protein into host epithelial cells and induces growth factor-like signaling, perturbs cell-cell junctions, and alters host cell polarity. This enables Hp to grow as microcolonies adhered to the host cell surface even in conditions that do not support growth of free-swimming bacteria. We hypothesized that CagA alters host cell physiology to allow Hp to obtain specific nutrients from or across the epithelial barrier. Using a polarized epithelium model system, we find that isogenic ΔcagA mutants are defective in cell surface microcolony formation, but exogenous addition of iron to the apical medium partially rescues this defect, suggesting that one of CagA's effects on host cells is to facilitate iron acquisition from the host. Hp adhered to the apical epithelial surface increase basolateral uptake of transferrin and induce its transcytosis in a CagA-dependent manner. Both CagA and VacA contribute to the perturbation of transferrin recycling, since VacA is involved in apical mislocalization of the transferrin receptor to sites of bacterial attachment. To determine if the transferrin recycling pathway is involved in Hp colonization of the cell surface, we silenced transferrin receptor expression during infection. This resulted in a reduced ability of Hp to colonize the polarized epithelium. To test whether CagA is important in promoting iron acquisition in vivo, we compared colonization of Hp in iron-replete vs. iron-deficient Mongolian gerbils. While wild type Hp and ΔcagA mutants colonized iron-replete gerbils at similar levels, ΔcagA mutants are markedly impaired in colonizing iron-deficient gerbils. Our study indicates that CagA and VacA act in concert to usurp the polarized process of host cell iron uptake, allowing Hp to use the cell surface as a replicative niche.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
H. pylori alters host iron metabolism when iron is scarce, aiding its survival in the stomach.
“H. pylori subsequently acquires iron from transferrin and reveals how H. pylori manipulates host iron metabolism under iron-deplete conditions to promote survival in the stomach.”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Tan et al., 2011
CagA drives the relocation of transferrin receptors to the apical surface, where H. pylori resides, from their normal basolateral position.
“CagA causes the mislocalization of transferrin receptors from the basolateral membrane to the apical surface where the pathogen is located (Tan et al., 2011).”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Tan et al., 2011
H. pylori obtains iron from transferrin.
“H. pylori subsequently acquires iron from transferrin”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Tan et al., 2011
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Malfertheiner, P., Mégraud, F., O'Morain, C. A., Bazzoli, F., El-Omar, E. M., Graham, D., Hunt, R. H., Rokkas, T., Vakil, N. B., Kuipers, E. J., et al. (2006) · Gut · doi:10.1136/gut.2006.101634 · Cited by 2,242 · see citing works
Mosaicism in Vacuolating Cytotoxin Alleles of Helicobacter pylori
Atherton, J. C., Cao, P., Peek, R. M., Tummuru, M. K. R., Blaser, M. J., & Cover, T. L. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.30.17771 · Cited by 1,564 · see citing works
Self-citationHelicobacter pylori Adhesin Binding Fucosylated Histo-Blood Group Antigens Revealed by Retagging
Ilver, D., Arnqvist, A., Ögren, J., Frick, I.-M., Kersulyte, D., Incecik, E. T., Berg, D. E., Covacci, A., Engstrand, L. G., & Borén, T. (1998) · Science · doi:10.1126/science.279.5349.373 · Cited by 1,225 · see citing works
SHP-2 Tyrosine Phosphatase as an Intracellular Target of Helicobacter pylori CagA Protein
Higashi, H., Tsutsumi, R., Muto, S., Sugiyama, T., Azuma, T., Asaka, M., & Hatakeyama, M. (2002) · Science · doi:10.1126/science.1067147 · Cited by 1,028 · see citing works
Helicobacter pylori SabA Adhesin in Persistent Infection and Chronic Inflammation
Mahdavi, J., Sondén, B., Hurtig, M., Olfat, F. O., Forsberg, L., Roche, N., Ångström, J., Larsson, T. P., Teneberg, S., Karlsson, K., et al. (2002) · Science · doi:10.1126/science.1069076 · Cited by 935 · see citing works
Lactoferrin: structure, function and applications
González‐Chávez, S. A., Arévalo‐Gallegos, S., & Rascón-Cruz, Q. (2008) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2008.07.020 · Cited by 759 · see citing works
Disruption of the Epithelial Apical-Junctional Complex by Helicobacter pylori CagA
Amieva, M. R., Vogelmann, R., Covacci, A., Tompkins, L. S., Nelson, W. J., & Falkow, S. (2003) · Science · doi:10.1126/science.1081919 · Cited by 739 · see citing works
Self-citationOrganization of vesicular trafficking in epithelia
Rodriguez-Boulan, E., Kreitzer, G., & Müsch, A. (2005) · Nature reviews. Molecular cell biology · doi:10.1038/nrm1593 · Cited by 644 · see citing works
The serine protease TMPRSS6 is required to sense iron deficiency
Du, X., She, E., Gelbart, T., Truksa, J., Lee, P., Xia, Y., Khovananth, K., Mudd, S., Mann, N., Moresco, E. M. Y., et al. (2008) · Science · doi:10.1126/science.1157121 · Cited by 578 · see citing works
Helicobacter pylori VacA, a paradigm for toxin multifunctionality
Cover, T. L., & Blanke, S. R. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1095 · Cited by 569 · see citing works
Receptor-mediated endocytosis of transferrin in K562 cells.
Klausner, R. D., van Renswoude, J., Ashwell, G., Kempf, C., Schechter, A. N., Dean, A., & Bridges, K. R. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)32481-5 · Cited by 563 · see citing works
Ernst, P. B., & Gold, B. D. (2000) · Annual Review of Microbiology · doi:10.1146/annurev.micro.54.1.615 · Cited by 554 · see citing works
Coordinated protein sorting, targeting and distribution in polarized cells
Mellman, I., & Nelson, W. J. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2525 · Cited by 521 · see citing works
Iron availability and infection
Weinberg, E. D. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2008.07.002 · Cited by 516 · see citing works
Gumbiner, B. M., & Simons, K. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.102.2.457 · Cited by 509 · see citing works
Helicobacter pylori CagA targets PAR1/MARK kinase to disrupt epithelial cell polarity
Saadat, I., Higashi, H., Obuse, C., Umeda, M., Murata‐Kamiya, N., Saito, Y., Lu, H., Ohnishi, N., Azuma, T., Suzuki, A., et al. (2007) · Nature · doi:10.1038/nature05765 · Cited by 501 · see citing works
Activation of β-catenin by carcinogenic Helicobacter pylori
Franco, A. T., Israel, D. A., Washington, M. K., Krishna, U. S., Fox, J. G., Rogers, A. B., Neish, A. S., Collier-Hyams, L. S., Perez-Perez, G. I., Hatakeyama, M., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504927102 · Cited by 479 · see citing works
Self-citationNatural history and epidemiology of Helicobacter pylori infection
Go, M. F. (2002) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.2002.0160s1003.x · Cited by 440 · see citing works
Stein, M., Bagnoli, F., Halenbeck, R., Rappuoli, R., Fantl, W. J., & Covacci, A. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.02781.x · Cited by 439 · see citing works
Src Is the Kinase of the Helicobacter pylori CagA Protein in Vitro and in Vivo
Selbach, M., Moese, S., Hauck, C. R., Meyer, T. F., & Backert, S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c100754200 · Cited by 414 · see citing works
Grb2 Is a Key Mediator of Helicobacter pylori CagA Protein Activities
Mimuro, H., Suzuki, T., Tanaka, J., Asahi, M., Haas, R., & Sasakawa, C. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00681-0 · Cited by 367 · see citing works
Churin, Y., Al-Ghoul, L., Kepp, O., Meyer, T. F., Birchmeier, W., & Naumann, M. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200208039 · Cited by 354 · see citing works
Israel, D. A., Salama, N. R., Arnold, C. N., Moss, S. F., Ando, T., Wirth, H.-P., Tham, K. T., Camorlinga, M., Blaser, M. J., Falkow, S., et al. (2001) · Journal of Clinical Investigation · doi:10.1172/jci11450 · Cited by 334 · see citing works
Self-citationThe spatial orientation of Helicobacter pylori in the gastric mucus
Schreiber, S., Konradt, M., Groll, C., Scheid, P., Hanauer, G., Werling, H. O., Josenhans, C., & Suerbaum, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308386101 · Cited by 330 · see citing works
Bacterial adhesion and disease activity in Helicobacter associated chronic gastritis.
Hessey, S. J., Spencer, J., Wyatt, J. I., Sobala, G. M., Rathbone, B. J., Axon, A. T. R., & Dixon, M. F. (1990) · Gut · doi:10.1136/gut.31.2.134 · Cited by 301 · see citing works
Cholesterol glucosylation promotes immune evasion by Helicobacter pylori
Wunder, C., Churin, Y., Winau, F., Warnecke, D. C., Vieth, M. W., Lindner, B., Zähringer, U., Mollenkopf, H., Heinz, E., & Meyer, T. F. (2006) · Nature Medicine · doi:10.1038/nm1480 · Cited by 291 · see citing works
Regulation of Gastric Carcinogenesis by Helicobacter pylori Virulence Factors
Franco, A. T., Johnston, E., Krishna, U. S., Yamaoka, Y., Israel, D. A., Nagy, T. A., Wroblewski, L. E., Piazuelo, M. B., Correa, P., & Peek, R. M. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-0824 · Cited by 278 · see citing works
Self-citationP HYSIOLOGY AND M OLECULAR B IOLOGY OF D IETARY I RON A BSORPTION
Miret, S., Simpson, R. J., & McKie, A. T. (2003) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.23.011702.073139 · Cited by 269 · see citing works
Helicobacter pylori CagA induces a transition from polarized to invasive phenotypes in MDCK cells
Bagnoli, F., Buti, L., Tompkins, L. S., Covacci, A., & Amieva, M. R. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502598102 · Cited by 267 · see citing works
Self-citationMeguro, R., Asano, Y., Odagiri, S., Li, C., Iwatsuki, H., & Shoumura, K. (2007) · Archivum histologicum japonicum · doi:10.1679/aohc.70.1 · Cited by 261 · see citing works
Iron acquisition in microbial pathogenesis
Payne, S. M. (1993) · Trends in Microbiology · doi:10.1016/0966-842x(93)90036-q · Cited by 257 · see citing works
Papini, E., Satin, B., Norais, N., de Bernard, M., Telford, J. L., Rappuoli, R., & Montecucco, C. (1998) · Journal of Clinical Investigation · doi:10.1172/jci2764 · Cited by 248 · see citing works
Sargiacomo, M., Lisanti, M. P., Graeve, L., Bivic, A. L., & Rodriguez-Boulan, E. J. (1989) · The Journal of Membrane Biology · doi:10.1007/bf01871942 · Cited by 230 · see citing works
The Versatility of Helicobacter pylori CagA Effector Protein Functions: The Master Key Hypothesis
Backert, S., Tegtmeyer, N., & Selbach, M. (2010) · Helicobacter · doi:10.1111/j.1523-5378.2010.00759.x · Cited by 227 · see citing works
Iron-Deficiency Anemia and Helicobacter pylori Infection: A Review of the Evidence
DuBois, S., & Kearney, D. J. (2005) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2005.30252.x · Cited by 226 · see citing works
Tammer, I., Brandt, S., Hartig, R., König, W., & Backert, S. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.01.050 · Cited by 219 · see citing works
Listeria monocytogenes Invades the Epithelial Junctions at Sites of Cell Extrusion
Pentecost, M., Otto, G. M., Theriot, J. A., & Amieva, M. R. (2006) · PLoS Pathogens · doi:10.1371/journal.ppat.0020003 · Cited by 215 · see citing works
Self-citationMimuro, H., Suzuki, T., Nagai, S., Rieder, G., Suzuki, M., Nagai, T., Fujita, Y., Nagamatsu, K., Ishijima, N., Koyasu, S., et al. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2007.09.005 · Cited by 212 · see citing works
Annibale, B., Marignani, M., Monarca, B., Antonelli, G., Marcheggiano, A., Martino, G., Mandelli, F., Caprilli, R., & Fave, G. D. (1999) · Annals of Internal Medicine · doi:10.7326/0003-4819-131-9-199911020-00006 · Cited by 197 · see citing works
Helicobacter pylorienter and survive within multivesicular vacuoles of epithelial cells
Amieva, M. R., Salama, N. R., Tompkins, L. S., & Falkow, S. (2002) · Cellular Microbiology · doi:10.1046/j.1462-5822.2002.00222.x · Cited by 194 · see citing works
Self-citationGrifantini, R., Sebastian, S., Frigimelica, E., Draghi, M., Bartolini, E., Muzzi, A., Rappuoli, R., Grandi, G., & Genco, C. A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1033001100 · Cited by 187 · see citing works
Two distinct modes of myosin assembly and dynamics during epithelial wound closure
Tamada, M., Perez, T. D., Nelson, W. J., & Sheetz, M. P. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200609116 · Cited by 179 · see citing works
Elemental and Redox Analysis of Single Bacterial Cells by X-ray Microbeam Analysis
Kemner, K., Kelly, S. D., Lai, B. C. H., Maser, J., O’Loughlin, E. J., Sholto-Douglas, D., Cai, Z., Schneegurt, M. A., Kulpa, C. F., & Nealson, K. H. (2004) · Science · doi:10.1126/science.1103524 · Cited by 177 · see citing works
The Versatility of Helicobacter pylori CagA Effector Protein Functions: the Master Key Hypothesis
Backert, S., Tegtmeyer, N., & Selbach, M. (2010) · Helicobacter · doi:10.1111/j.1523-5378.2010.00797.x · Cited by 177 · see citing works
The effect of the iron saturation of transferrin on its binding and uptake by rabbit reticulocytes
Young, S. P., Bomford, A. B., & Williams, R. J. R. (1984) · Biochemical Journal · doi:10.1042/bj2190505 · Cited by 176 · see citing works
Schmitt, M. P., & Holmes, R. K. (1991) · Infection and Immunity · doi:10.1128/iai.59.6.1899-1904.1991 · Cited by 172 · see citing works
Iron nutrition and tumor growth: decreased tumor growth in iron-deficient mice.
Hann, H. W., Stahlhut, M. W., & Blumberg, B. S. (1988) · PubMed · Cited by 157 · see citing works
Chalker, A. F., Minehart, H. W., Hughes, N. J., Koretke, K. K., Lonetto, M. A., Brinkman, K. K., Warren, P. V., Lupas, A. N., Stanhope, M. J., Brown, J. R., et al. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.4.1259-1268.2001 · Cited by 157 · see citing works
Wenzhen, Y., Li, Y., Kehu, Y., Ma, B., Quanlin, G., Donghai, W., & Lijuan, Y. (2010) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365521003663670 · Cited by 155 · see citing works
Helicobacter pylori Usurps Cell Polarity to Turn the Cell Surface into a Replicative Niche
Tan, S., Tompkins, L. S., & Amieva, M. R. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000407 · Cited by 152 · see citing works
Self-citationGrowth Phase-Dependent Response of<i>Helicobacter pylori</i>to Iron Starvation
Merrell, D. S., Thompson, L. J., Kim, C. C., Mitchell, H., Tompkins, L. S., Lee, A., & Falkow, S. (2003) · Infection and Immunity · doi:10.1128/iai.71.11.6510-6525.2003 · Cited by 149 · see citing works
Helicobacter pylori VacA-induced Inhibition of GSK3 through the PI3K/Akt Signaling Pathway
Nakayama, M., Hisatsune, J., Yamasaki, E., Isomoto, H., Kurazono, H., Hatakeyama, M., Azuma, T., Yamaoka, Y., Yahiro, K., Moss, J., et al. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m806981200 · Cited by 142 · see citing works
Oldani, A., Cormont, M., Hofman, V., Chiozzi, V., Oregioni, O., Canonici, A., Sciullo, A. D., Sommi, P., Fabbri, A., Ricci, V., et al. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000603 · Cited by 137 · see citing works
Yokoyama, K., Higashi, H., Ishikawa, S., Fujii, Y., Kondo, S., Kato, H., Azuma, T., Wada, A., Hirayama, T., Aburatani, H., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502529102 · Cited by 136 · see citing works
Odorizzi, G., Pearse, A., Domingo, D., Trowbridge, I. S., & Hopkins, C. R. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.135.1.139 · Cited by 133 · see citing works
Kierbel, A., Gassama‐Diagne, A., Mostov, K. E., & Engel, J. N. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-08-0717 · Cited by 131 · see citing works
The Helicobacter pylori Homologue of the Ferric Uptake Regulator Is Involved in Acid Resistance
Bijlsma, J. J. E., Waidner, B., van Vliet, A. H. M., Hughes, N. J., Häg, S., Bereswill, S., Kelly, D. J., Vandenbroucke‐Grauls, C. M. J. E., Kist, M., & Kusters, J. G. (2002) · Infection and Immunity · doi:10.1128/iai.70.2.606-611.2002 · Cited by 125 · see citing works
Gancz, H., Censini, S., & Merrell, D. S. (2005) · Infection and Immunity · doi:10.1128/iai.74.1.602-614.2006 · Cited by 125 · see citing works
Nagy, T. A., Frey, M. R., Yan, F., Israel, D. A., Polk, D. B., & Peek, R. M. (2009) · The Journal of Infectious Diseases · doi:10.1086/596660 · Cited by 120 · see citing works
Self-citationPentecost, M., Kumaran, J., Ghosh, P., & Amieva, M. R. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000900 · Cited by 118 · see citing works
Self-citationSatin, B., Norais, N., Rappuoli, R., Telford, J., Murgia, M., Montecucco, C., & Papini, E. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.40.25022 · Cited by 117 · see citing works
Functional association between the Helicobacter pylori virulence factors VacA and CagA
Argent, R. H., Thomas, R. J., Letley, D. P., Rittig, M. G., Hardie, K. R., & Atherton, J. C. (2008) · Journal of Medical Microbiology · doi:10.1099/jmm.0.47465-0 · Cited by 117 · see citing works
The Helicobacter pylori VacA toxin is a urea permease that promotes urea diffusion across epithelia
Tombola, F., Morbiato, L., Giudice, G. D., Rappuoli, R., Zoratti, M., & Papini, E. (2001) · Journal of Clinical Investigation · doi:10.1172/jci13045 · Cited by 113 · see citing works
Tegtmeyer, N., Zabler, D., Schmidt, D., Hartig, R., Brandt, S., & Backert, S. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01269.x · Cited by 103 · see citing works
Interaction of Helicobacter pylori with host cells: function of secreted and translocated molecules
Rieder, G., Fischer, W. H., & Haas, R. (2005) · Current Opinion in Microbiology · doi:10.1016/j.mib.2004.12.004 · Cited by 102 · see citing works
Davis, R. J., & Czech, M. (1986) · The EMBO Journal · doi:10.1002/j.1460-2075.1986.tb04263.x · Cited by 101 · see citing works
Muza–Moons, M. M., Koutsouris, A., & Hecht, G. A. (2003) · Infection and Immunity · doi:10.1128/iai.71.12.7069-7078.2003 · Cited by 99 · see citing works
Kierbel, A., Gassama‐Diagne, A., Rocha, C. L., Radoshevich, L., Olson, J. C., Mostov, K. E., & Engel, J. N. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200605142 · Cited by 98 · see citing works
Wollner, D. A., Krzeminski, K. A., & Nelson, W. J. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.116.4.889 · Cited by 97 · see citing works
Koerper, M. A., & Dallman, P. R. (1977) · The Journal of Pediatrics · doi:10.1016/s0022-3476(77)80879-2 · Cited by 92 · see citing works
Zeaiter, Z., Cohen, D., Müsch, A., Bagnoli, F., Covacci, A., & Stein, M. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2007.01084.x · Cited by 90 · see citing works
Siderophore-mediated iron acquisition in the staphylococci
Beasley, F. C., & Heinrichs, D. E. (2010) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2009.09.011 · Cited by 90 · see citing works
Genes ofHelicobacter pyloriRegulated by Attachment to AGS Cells
Kim, N., Marcus, E. A., Wen, Y., Weeks, D. L., Scott, D. R., Jung, H. C., Song, I. S., & Sachs, G. M. (2004) · Infection and Immunity · doi:10.1128/iai.72.4.2358-2368.2004 · Cited by 77 · see citing works
Botham, C. M., Wandler, A. M., & Guillemin, K. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000064 · Cited by 76 · see citing works
Hatakeyama, M. (2008) · Oncogene · doi:10.1038/onc.2008.353 · Cited by 75 · see citing works
Transferrin saturation, plasma iron turnover, and transferrin uptake in normal humans
Cazzola, M., Huebers, H., Sayers, M., MacPhail, A. P., Eng, M., & Finch, C. (1985) · Blood · doi:10.1182/blood.v66.4.935.935 · Cited by 74 · see citing works
Helicobacter pylori toxin VacA is transferred to host cells via a novel contact-dependent mechanism
Ilver, D., Barone, S., Mercati, D., Lupetti, P., & Telford, J. L. (2004) · Cellular Microbiology · doi:10.1046/j.1462-5822.2003.00349.x · Cited by 71 · see citing works
Senkovich, O., Ceaser, S., McGee, D. J., & Testerman, T. L. (2010) · Infection and Immunity · doi:10.1128/iai.01258-09 · Cited by 70 · see citing works
Testerman, T. L., Conn, P. B., Mobley, H. L. T., & McGee, D. J. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.44.5.1650-1658.2006 · Cited by 69 · see citing works
The Role of Uvomorulin in the Formation of Epithelial Occluding Junctions
Gumbiner, B. M., & Simons, K. (2007) · Novartis Foundation symposium · doi:10.1002/9780470513408.ch11 · Cited by 66 · see citing works
Structural and functional diversity in the PAR1b/MARK2‐binding region of Helicobacter pylori CagA
Lu, H., Saito, Y., Umeda, M., Murata‐Kamiya, N., Zhang, H., Higashi, H., & Hatakeyama, M. (2008) · Cancer Science · doi:10.1111/j.1349-7006.2008.00950.x · Cited by 64 · see citing works
Fields, I. C., King, S. M., Shteyn, E., Kang, R. S.-O., & Fölsch, H. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-01-0036 · Cited by 50 · see citing works
Duque, X., Morán, S., Mera, R. M., Medina, M., Martı́nez, H., Mendoza, E., Torres, J., & Correa, P. (2010) · Archives of Medical Research · doi:10.1016/j.arcmed.2009.11.006 · Cited by 46 · see citing works
Zak, O., Ikuta, K., & Aisen, P. (2002) · Biochemistry · doi:10.1021/bi0160258 · Cited by 39 · see citing works
Dhur, A., Galan, P., Preziosi, P., & Herçberg, S. (1991) · Journal of Nutrition · doi:10.1093/jn/121.9.1418 · Cited by 37 · see citing works
Helicobacter pylori CagA inhibits endocytosis of cytotoxin VacA in host cells
Akada, J. K., Aoki, H., Torigoe, Y., Kitagawa, T., Kurazono, H., Hoshida, H., Nishikawa, J., Terai, S., Matsuzaki, M., Hirayama, T., et al. (2010) · Disease Models & Mechanisms · doi:10.1242/dmm.004879 · Cited by 36 · see citing works
van Vliet, A. H. M., Bereswill, S., & Kusters, J. G. (2014) · ASM Press eBooks · doi:10.1128/9781555818005.ch17 · Cited by 35 · see citing works
Enns, C. A., Rutledge, E. A., & Williams, A. M. (1996) · Biomembranes · doi:10.1016/s1874-5342(96)80012-2 · Cited by 31 · see citing works
Membrane Dynamics and the Regulation of Epithelial Cell Polarity
van der Wouden, J. M., Maier, O., van IJzendoorn, S. C. D., & Hoekstra, D. (2003) · International review of cytology · doi:10.1016/s0074-7696(03)01003-9 · Cited by 31 · see citing works
Chapter 4 Protein Trafficking in Polarized Cells
Duffield, A. S., Caplan, M. J., & Muth, T. R. (2008) · International review of cytology · doi:10.1016/s1937-6448(08)01404-4 · Cited by 29 · see citing works
Motility of Urease-Deficient Derivatives of Helicobacter pylori
Tan, S., & Berg, D. E. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.3.885-888.2004 · Cited by 28 · see citing works
Self-citationSzczebara, F. M., Dhaenens, L., Armand, S., & Husson, M. O. (1999) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1999.tb13615.x · Cited by 26 · see citing works
A Possible Role of Iron Deficiency in Gastric Cancer in Colombia
Broitman, S. A., Vélez, H., & Vitale, J. J. (1981) · Springer eBooks · doi:10.1007/978-1-4615-9200-6_9 · Cited by 20 · see citing works
Iron binding of gastric mucins
Bella, A., & Kim, Y. S. (1973) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(73)90280-8 · Cited by 18 · see citing works
Davis, R. J., Kuck, L., Faucher, M., & Czech, M. (1986) · Federation Proceedings · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Pathobiology of Helicobacter pylori–Induced Gastric Cancer
Amieva, M. R., & Peek, R. M. (2015) · Gastroenterology · doi:10.1053/j.gastro.2015.09.004 · Cited by 907 · see citing works
Self-citationLife in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori
Salama, N. R., Hartung, M. L., & Mueller, A. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro3016 · Cited by 668 · see citing works
Helicobacter pylori CagA and Gastric Cancer: A Paradigm for Hit-and-Run Carcinogenesis
Hatakeyama, M. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.02.008 · Cited by 557 · see citing works
Helicobacter pylori and gastric cancer: mechanisms and new perspectives
Duan, Y., Xu, Y., Dou, Y., & Xu, D. (2025) · Journal of Hematology & Oncology · doi:10.1186/s13045-024-01654-2 · Cited by 311 · see citing works
Gastrointestinal biofilms in health and disease
Motta, J., Wallace, J. L., Buret, A. G., Deraison, C., & Vergnolle, N. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-020-00397-y · Cited by 271 · see citing works
HATAKEYAMA, M. (2017) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.93.013 · Cited by 261 · see citing works
Sigal, M. J., Rothenberg, M. E., Logan, C. Y., Lee, J. Y., Honaker, R. W., Cooper, R. L., Passarelli, B., Camorlinga, M., Bouley, D. M., Cabrera-Álvarez, G., et al. (2015) · Gastroenterology · doi:10.1053/j.gastro.2015.02.049 · Cited by 244 · see citing works
Self-citationAn Overview of Helicobacter pylori VacA Toxin Biology
Foegeding, N. J., Caston, R. R., McClain, M. S., Ohi, M. D., & Cover, T. L. (2016) · Toxins · doi:10.3390/toxins8060173 · Cited by 244 · see citing works
Helicobacter pylori Diversity and Gastric Cancer Risk
Cover, T. L. (2016) · mBio · doi:10.1128/mbio.01869-15 · Cited by 217 · see citing works
High Dietary Salt Intake Exacerbates Helicobacter pylori-Induced Gastric Carcinogenesis
Gaddy, J. A., Radin, J. N., Loh, J. T., Zhang, F., Washington, M. K., Peek, R. M., Algood, H. M. S., & Cover, T. L. (2013) · Infection and Immunity · doi:10.1128/iai.01271-12 · Cited by 209 · see citing works
Self-citationBackert, S., Tegtmeyer, N., & Fischer, W. H. (2015) · Future Microbiology · doi:10.2217/fmb.15.32 · Cited by 194 · see citing works
The Impact of Dietary Transition Metals on Host-Bacterial Interactions
Lopez, C. A., & Skaar, E. P. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.05.008 · Cited by 190 · see citing works
Iron deficiency accelerates Helicobacter pylori–induced carcinogenesis in rodents and humans
Noto, J. M., Gaddy, J. A., Lee, J. Y., Piazuelo, M. B., Friedman, D. B., Colvin, D. C., Romero-Gallo, J., Suarez, G., Loh, J., Slaughter, J. C., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci64373 · Cited by 178 · see citing works
Self-citationChemodetection and Destruction of Host Urea Allows Helicobacter pylori to Locate the Epithelium
Huang, J. Y., Sweeney, E. G., Sigal, M. J., Zhang, H. C., Remington, S. J., Cantrell, M. A., Kuo, C. J., Guillemin, K. J., & Amieva, M. R. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.07.002 · Cited by 176 · see citing works
Self-citationBackert, S., Clyne, M., & Tegtmeyer, N. (2011) · Cell Communication and Signaling · doi:10.1186/1478-811x-9-28 · Cited by 174 · see citing works
Helicobacter pylori Vacuolating Toxin and Gastric Cancer
McClain, M. S., Beckett, A. C., & Cover, T. L. (2017) · Toxins · doi:10.3390/toxins9100316 · Cited by 148 · see citing works
Functional Plasticity in the Type IV Secretion System of Helicobacter pylori
Barrozo, R. M., Cooke, C. L., Hansen, L. M., Lam, A. M., Gaddy, J. A., Johnson, E., Cariaga, T. A., Suárez, G., Peek, R. M., Cover, T. L., et al. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003189 · Cited by 145 · see citing works
Self-citationThe Helicobacter pylori Cag Type IV Secretion System
Cover, T. L., Lacy, D. B., & Ohi, M. D. (2020) · Trends in Microbiology · doi:10.1016/j.tim.2020.02.004 · Cited by 144 · see citing works
Wroblewski, L. E., Piazuelo, M. B., Chaturvedi, R., Schumacher, M., Aihara, E., Feng, R., Noto, J. M., Delgado, A., Israel, D. A., Zavros, Y., et al. (2015) · Gut · doi:10.1136/gutjnl-2014-307650 · Cited by 143 · see citing works
Self-citationStein, S. C., Faber, E., Bats, S. H., Murillo, T., Speidel, Y., Coombs, N., & Josenhans, C. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006514 · Cited by 131 · see citing works
Helicobacter pylori in Gastric Carcinogenesis
Wroblewski, L. E., & Peek, R. M. (2013) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2013.01.006 · Cited by 126 · see citing works
Self-citationIntoxication strategy of Helicobacter pylori VacA toxin
Boquet, P., & Ricci, V. (2012) · Trends in Microbiology · doi:10.1016/j.tim.2012.01.008 · Cited by 120 · see citing works
Chemorepulsion from the Quorum Signal Autoinducer-2 Promotes Helicobacter pylori Biofilm Dispersal
Anderson, J. K., Huang, J. Y., Wreden, C. C., Sweeney, E. G., Goers, J. W. F., Remington, S. J., & Guillemin, K. J. (2015) · mBio · doi:10.1128/mbio.00379-15 · Cited by 118 · see citing works
Structural Insights into Polymorphic ABO Glycan Binding by Helicobacter pylori
Moonens, K., Gideonsson, P., Subedi, S., Bugaytsova, J. A., Romão, E., Méndez, M., Nordén, J., Fallah, M., Rakhimova, L., Shevtsova, A. A., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2015.12.004 · Cited by 113 · see citing works
Subversion of host kinases: a key network in cellular signaling hijacked by Helicobacter pylori CagA
Tegtmeyer, N., Neddermann, M., Asche, C. I., & Backert, S. (2017) · Molecular Microbiology · doi:10.1111/mmi.13707 · Cited by 111 · see citing works
Diet, microbial virulence, and Helicobacter pylori -induced gastric cancer
Cover, T. L., & Peek, R. M. (2013) · Gut Microbes · doi:10.4161/gmic.26262 · Cited by 109 · see citing works
Self-citationKim, I.-J., & Blanke, S. R. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00037 · Cited by 102 · see citing works
Fung, C., Tan, S., Nakajima, M., Skoog, E. C., Camarillo-Guerrero, L. F., Klein, J. A., Lawley, T. D., Solnick, J. V., Fukami, T., & Amieva, M. R. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000231 · Cited by 101 · see citing works
Self-citationMultiple Acid Sensors Control Helicobacter pylori Colonization of the Stomach
Huang, J. Y., Sweeney, E. G., Guillemin, K. J., & Amieva, M. R. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006118 · Cited by 91 · see citing works
Self-citationEpidemiology and role of Helicobacter pylori virulence factors in gastric cancer carcinogenesis
Sukri, A., Hanafiah, A., Zin, N. M., & Kosai, N. R. (2020) · Apmis · doi:10.1111/apm.13034 · Cited by 90 · see citing works
Polymorphism in the Helicobacter pylori CagA and VacA toxins and disease
Bridge, D. R., & Merrell, D. S. (2013) · Gut Microbes · doi:10.4161/gmic.23797 · Cited by 92 · see citing works
CagY Is an Immune-Sensitive Regulator of the Helicobacter pylori Type IV Secretion System
Barrozo, R. M., Hansen, L. M., Lam, A. M., Skoog, E. C., Martín, M. E., Cai, L. P., Lin, Y., Latoscha, A., Suerbaum, S., Canfield, D. R., et al. (2016) · Gastroenterology · doi:10.1053/j.gastro.2016.08.014 · Cited by 85 · see citing works
Commensal inter-bacterial interactions shaping the microbiota
Kern, L., Abdeen, S. K., Kolodziejczyk, A. A., & Elinav, E. (2021) · Current Opinion in Microbiology · doi:10.1016/j.mib.2021.07.011 · Cited by 79 · see citing works
Rizzato, C., Torres, J., Kasamatsu, E., Camorlinga‐Ponce, M., Bravo, M. M., Canzian, F., & Kato, I. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00846 · Cited by 81 · see citing works
Immunological Perspective: Helicobacter pylori Infection and Gastritis
Yang, H., & Hu, B. (2022) · Mediators of Inflammation · doi:10.1155/2022/2944156 · Cited by 85 · see citing works
The Helicobacter pylori cag pathogenicity island as a determinant of gastric cancer risk
Tran, S. C., Bryant, K. N., & Cover, T. L. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2314201 · Cited by 80 · see citing works
Morgenthau, A., Pogoutse, A., Adamiak, P., Moraes, T. F., & Schryvers, A. B. (2013) · Future Microbiology · doi:10.2217/fmb.13.125 · Cited by 78 · see citing works
The adherens junctions control susceptibility to Staphylococcus aureus α-toxin
Popov, L. M., Marceau, C. D., Starkl, P. M., Lumb, J. H., Shah, J., Guerrera, D., Cooper, R. L., Merakou, C., Bouley, D. M., Meng, W., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1510265112 · Cited by 78 · see citing works
Self-citationWizenty, J., & Sigal, M. J. (2025) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-025-01042-2 · Cited by 86 · see citing works
Haley, K. P., Delgado, A. G., Piazuelo, M. B., Mortensen, B. L., Correa, P., Damo, S. M., Chazin, W. J., Skaar, E. P., & Gaddy, J. A. (2015) · Infection and Immunity · doi:10.1128/iai.00544-15 · Cited by 68 · see citing works
Structure of the Helicobacter pylori CagA oncoprotein bound to the human tumor suppressor ASPP2
Nes̆ić, D., Buti, L., Lü, X., & Stebbins, C. E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320631111 · Cited by 67 · see citing works
Helicobacter pylori senses bleach (HOCl) as a chemoattractant using a cytosolic chemoreceptor
Perkins, A., Tudorica, D. A., Amieva, M. R., Remington, S. J., & Guillemin, K. J. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000395 · Cited by 61 · see citing works
Self-citationHelicobacter pylori in the Oral Cavity: Current Evidence and Potential Survival Strategies
Zhang, L., Chen, X., Ren, B., Zhou, X., & Cheng, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113646 · Cited by 65 · see citing works
Pich, Ò. Q., & Merrell, D. S. (2013) · Future Microbiology · doi:10.2217/fmb.13.43 · Cited by 64 · see citing works
Hathroubi, S., Hu, S., & Ottemann, K. M. (2020) · npj Biofilms and Microbiomes · doi:10.1038/s41522-020-00167-3 · Cited by 60 · see citing works
Helicobacter pylori shows tropism to gastric differentiated pit cells dependent on urea chemotaxis
Aguilar, C., Paužuolis, M., Pompaiah, M., Vafadarnejad, E., Arampatzi, P., Fischer, M., Narres, D., Neyazi, M., Kayisoglu, Ö., Sell, T., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33165-4 · Cited by 54 · see citing works
Pathogenesis of H elicobacter pylori Infection
Delahay, R. M., & Rugge, M. (2012) · Helicobacter · doi:10.1111/j.1523-5378.2012.00976.x · Cited by 53 · see citing works
Unintended consequences of Helicobacter pylori infection in children in developing countries
Queiroz, D. M. M., Rocha, A. M., & Crabtree, J. E. (2013) · Gut Microbes · doi:10.4161/gmic.26277 · Cited by 53 · see citing works
Pich, Ò. Q., Carpenter, B. M., Gilbreath, J. J., & Merrell, D. S. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.08066.x · Cited by 47 · see citing works
Targeting the Mucosal Barrier: How Pathogens Modulate the Cellular Polarity NetworkPreprint
Ruch, T. R., & Engel, J. N. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a027953 · Cited by 47 · see citing works
Helicobacter and Salmonella Persistent Infection StrategiesPreprint
Monack, D. M. (2013) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a010348 · Cited by 44 · see citing works
Jones, T. A., Hernandez, D. Z., Wong, Z. C., Wandler, A. M., & Guillemin, K. J. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006631 · Cited by 44 · see citing works
Natural History of Helicobacter pylori Infection in Mexican Schoolchildren
Duque, X., Vilchis‐Gil, J., Mera, R. M., Valdivia, B. T., Goodman, K. J., Mendoza, E., Navarro, F., Roque-Evangelista, V., Morán, S., Torres, J., et al. (2012) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e318248877f · Cited by 42 · see citing works
Helicobacter pylori-associated hypochlorhydria in children, and development of iron deficiency
Harris, P. R., Serrano, C. A., Villagrán, A., Walker, M. M., Thomson, M. J., Duarte, I., Windle, H. J., & Crabtree, J. E. (2012) · Journal of Clinical Pathology · doi:10.1136/jclinpath-2012-201243 · Cited by 42 · see citing works
Extracellular vesicles promote transkingdom nutrient transfer during viral-bacterial co-infection
Hendricks, M. R., Lane, S., Melvin, J. A., Ouyang, Y., Stolz, D. B., Williams, J. V., Sadovsky, Y., & Bomberger, J. M. (2021) · Cell Reports · doi:10.1016/j.celrep.2020.108672 · Cited by 41 · see citing works
The CagA toxin of Helicobacter pylori: abundant production but relatively low amount translocated
Soto, L. F. J., & Haas, R. (2016) · Scientific Reports · doi:10.1038/srep23227 · Cited by 39 · see citing works
Iron trafficking system in Helicobacter pylori
Ge, R., & Sun, X. (2011) · BioMetals · doi:10.1007/s10534-011-9512-8 · Cited by 39 · see citing works
Gastric Helicobacter Infection Induces Iron Deficiency in the INS-GAS Mouse
Thomson, M. J., Pritchard, D. M., Boxall, S., Abuderman, A. A., Williams, J. M., Varró, A., & Crabtree, J. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050194 · Cited by 38 · see citing works
Metalloregulation of Helicobacter pylori physiology and pathogenesis
Haley, K. P., & Gaddy, J. A. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00911 · Cited by 37 · see citing works
A Repeat-Associated Small RNA Controls the Major Virulence Factors of Helicobacter pylori
Eisenbart, S. K., Alzheimer, M., Pernitzsch, S. R., Dietrich, S., Stahl, S., & Sharma, C. M. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.09.009 · Cited by 37 · see citing works
Raghwan, & Chowdhury, R. (2013) · Helicobacter · doi:10.1111/hel.12087 · Cited by 37 · see citing works
Burns, M. A., Muthupalani, S., Ge, Z., Wang, T. C., Bakthavatchalu, V., Cunningham, C. J., Ennis, K., Georgieff, M., & Fox, J. G. (2015) · PLoS ONE · doi:10.1371/journal.pone.0142630 · Cited by 37 · see citing works
Haley, K. P., & Gaddy, J. A. (2016) · Gastroenterology Research and Practice · doi:10.1155/2016/3019362 · Cited by 35 · see citing works
Behrens, W., Schweinitzer, T., Bal, J., Dorsch, M. M., Bleich, A., Kops, F., Brenneke, B., Didelot, X., Suerbaum, S., & Josenhans, C. (2013) · Infection and Immunity · doi:10.1128/iai.00750-13 · Cited by 34 · see citing works
Kersulyte, D., Rossi, M., & Berg, D. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083177 · Cited by 33 · see citing works
Skoog, E. C., Morikis, V. A., Martín, M. E., Foster, G. A., Cai, L. P., Hansen, L. M., Li, B., Gaddy, J. A., Simon, S. I., & Solnick, J. V. (2018) · mBio · doi:10.1128/mbio.00717-18 · Cited by 33 · see citing works
Activity and Functional Importance of Helicobacter pylori Virulence Factors
Sgouras, D. N., Tegtmeyer, N., & Weßler, S. (2019) · Advances in experimental medicine and biology · doi:10.1007/5584_2019_358 · Cited by 32 · see citing works
New Advances in Nano-Drug Delivery Systems: Helicobacter pylori and Gastric Cancer
Zhu, X. Y., Su, T., Wang, S., Zhou, H.-Q., & Shi, W. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.834934 · Cited by 31 · see citing works
Yokota, S., Toita, N., Yamamoto, S., Fujii, N., & Konno, M. (2012) · Helicobacter · doi:10.1111/hel.12011 · Cited by 31 · see citing works
Avilés‐Jiménez, F., Reyes-León, A., Nieto-Patlán, E., Hansen, L. M., Burgueño, J. A., Ramos, I., Camorlinga‐Ponce, M., Bermúdez, H., Blancas, J. M., Cabrera, L., et al. (2011) · Infection and Immunity · doi:10.1128/iai.05845-11 · Cited by 32 · see citing works
Alterations in Helicobacter pylori Triggered by Contact with Gastric Epithelial Cells
Johnson, E., Gaddy, J. A., & Cover, T. L. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00017 · Cited by 30 · see citing works
Saberi, S., Douraghi, M., Azadmanesh, K., Shokrgozar, M. A., Zeraati, H., Hosseini, M. E., Mohagheghi, M. A., Parsaeian, M., & Mohammadi, M. (2012) · Helicobacter · doi:10.1111/j.1523-5378.2012.00954.x · Cited by 30 · see citing works
Hansen, L. M., Gideonsson, P., Canfield, D. R., Borén, T., & Solnick, J. V. (2017) · Infection and Immunity · doi:10.1128/iai.00094-17 · Cited by 30 · see citing works
Kronsteiner, B., Bassaganya-Riera, J., Philipson, N., & Hontecillas, R. (2014) · Gut Microbes · doi:10.4161/gmic.28899 · Cited by 29 · see citing works
The Mongolian Gerbil: A Robust Model of Helicobacter pylori-Induced Gastric Inflammation and Cancer
Noto, J. M., Romero–Gallo, J., Piazuelo, M. B., & Peek, R. M. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3603-8_24 · Cited by 29 · see citing works
Self-citationMechanisms and Regulation of Intestinal Iron Transport
Collins, J. F., Flores, S. R., Wang, X., & Anderson, G. J. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809954-4.00060-8 · Cited by 30 · see citing works
Nishikawa, H., Hayashi, T., Arisaka, F., Senda, T., & Hatakeyama, M. (2016) · Scientific Reports · doi:10.1038/srep30031 · Cited by 29 · see citing works
Helicobacter pylori infection perturbs iron homeostasis in gastric epithelial cells
Flores, S. E., Aitchison, A., Day, A. S., & Keenan, J. I. (2017) · PLoS ONE · doi:10.1371/journal.pone.0184026 · Cited by 28 · see citing works
Regulation ofHelicobacter pyloriVirulence Within the Context of Iron Deficiency
Noto, J. M., Lee, J. Y., Gaddy, J. A., Cover, T. L., Amieva, M. R., & Peek, R. M. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu805 · Cited by 27 · see citing works
Self-citationBacterial cyclomodulins: types and roles in carcinogenesis
Morgan, R. N., Saleh, S. E., Farrag, H. A., & Aboulwafa, M. (2021) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2021.1944052 · Cited by 27 · see citing works
Mohammadzadeh, R., Menbari, S., Pishdadian, A., & Farsiani, H. (2023) · Expert Reviews in Molecular Medicine · doi:10.1017/erm.2023.17 · Cited by 28 · see citing works
Donczew, R., Makowski, Ł., Jaworski, P., Bezulska‐Ditkowska, M., Nowaczyk, M., Zakrzewska‐Czerwińska, J., & Zawilak-Pawlik, A. M. (2014) · Molecular Microbiology · doi:10.1111/mmi.12866 · Cited by 27 · see citing works
The Human Stomach in Health and Disease: Infection Strategies by Helicobacter pylori
Robinson, K., Letley, D. P., & Kaneko, K. (2017) · Current topics in microbiology and immunology · doi:10.1007/978-3-319-50520-6_1 · Cited by 27 · see citing works
Genetic Manipulation of Helicobacter pylori Virulence Function by Host Carcinogenic Phenotypes
Suárez, G., Romero–Gallo, J., Sierra, J. C., Piazuelo, M. B., Krishna, U. S., Zuleta, M. A. G., Wilson, K. T., & Peek, R. M. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-2922 · Cited by 27 · see citing works
Self-citationThe Role of Adhesion in Helicobacter pylori Persistent Colonization
Yang, H., Wang, L., Zhang, M., & Hu, B. (2023) · Current Microbiology · doi:10.1007/s00284-023-03264-6 · Cited by 26 · see citing works
Lin, A. S., McClain, M. S., Beckett, A. C., Caston, R. R., Harvey, M. L., Dixon, B. R. E. A., Campbell, A. M., Shuman, J. H. B., Sawhney, N., Delgado, A. G., et al. (2020) · mBio · doi:10.1128/mbio.01296-20 · Cited by 25 · see citing works
Jang, S., Hansen, L. M., Su, H., Solnick, J. V., & Cha, J. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2044721 · Cited by 25 · see citing works
Helicobacter pylori: Genomic Insight into the Host-Pathogen Interaction
Haley, K. P., & Gaddy, J. A. (2015) · International Journal of Genomics · doi:10.1155/2015/386905 · Cited by 24 · see citing works
Dyer, V., Brüggemann, H., Soerensen, M., Kühl, A. A., Hoffman, K., Brinkmann, V., Reinés, M., Zimmerman, S., Meyer, T. F., & Koch, M. (2018) · Molecular Microbiology · doi:10.1111/mmi.14123 · Cited by 23 · see citing works
Kassa, E. G., Zlotkin‐Rivkin, E., Friedman, G., Ramachandran, R. P., Melamed‐Book, N., Weiss, A. M., Belenky, M. A., Reichmann, D., Breuer, W. V., Pal, R. R., et al. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1007851 · Cited by 23 · see citing works
Pirzadeh, M., Khalili, N., & Rezaei, N. (2020) · International Reviews of Immunology · doi:10.1080/08830185.2020.1851371 · Cited by 20 · see citing works
Targeting bacterial transferrin and lactoferrin receptors for vaccines
Schryvers, A. B. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2022.01.017 · Cited by 20 · see citing works
Measurement of total iron in Helicobacter pylori-infected gastric epithelial cells
Flores, S. E., Day, A. S., & Keenan, J. I. (2014) · BioMetals · doi:10.1007/s10534-014-9810-z · Cited by 20 · see citing works
Responses of gastric epithelial stem cells and their niche to Helicobacter pylori infection
Wizenty, J., Tacke, F., & Sigal, M. J. (2020) · Annals of Translational Medicine · doi:10.21037/atm.2020.02.178 · Cited by 20 · see citing works
Estibariz, I., Ailloud, F., Woltemate, S., Bunk, B., Spröer, C., Overmann, J., Aebischer, T., Meyer, T. F., Josenhans, C., & Suerbaum, S. (2020) · mBio · doi:10.1128/mbio.01803-20 · Cited by 20 · see citing works
Asl, D. H., Farivar, T. N., Rahmani, B., Hajmanoochehri, F., Razavi, À. E., Jahanbin, B., Dodaran, M. S., & Peymani, A. (2018) · Microbial Pathogenesis · doi:10.1016/j.micpath.2018.10.039 · Cited by 18 · see citing works
Burns, M. A., Amaya, A., Winn, C. B., Ge, Z., Bakthavatchalu, V., Ennis, K., Wang, T. C., Georgieff, M., & Fox, J. G. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173108 · Cited by 17 · see citing works
Identification of genetic modifiers of CagA-induced epithelial disruption in Drosophila
Reid, D. W., Muyskens, J. B., Neal, J. T., Gaddini, G. W., Cho, L. Y., Wandler, A. M., Botham, C. M., & Guillemin, K. (2012) · Front. Cell. Inf. Microbio. · doi:10.3389/fcimb.2012.00024 · Cited by 14 · see citing works
Lettl, C., Haas, R., & Fischer, W. H. (2021) · Molecular Microbiology · doi:10.1111/mmi.14772 · Cited by 16 · see citing works
Pu, S., Zhuang, Z., Liu, N., Luo, Q., & Zhang, D. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1552630 · Cited by 15 · see citing works
- Authors
- Tan, S., Noto, J. M., Romero-Gallo, J., Peek, R. M., & Amieva, M. R.
- Affiliations
- Stanford University (US)
- Vanderbilt University (US)
- Corresponding author
- Amieva, Manuel R.
- Venue
- PLoS Pathogens
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-05-12
- Volume
- 7
- Issue
- 5
- Pages
- e1002050
- ISSN
- 1553-7366 (ISSN-L)
- 1553-7374
- PMC
- PMC3093365
- OpenAlex
- W2079054594
- Cited by
- 175
- References
- 95
- Citations by year
- 2026: 8 · 2025: 8 · 2024: 4 · 2023: 6 · 2022: 9 · 2021: 14 · 2020: 15 · 2019: 8 · 2018: 8 · 2017: 15 · 2016: 17 · 2015: 17 · 2014: 12 · 2013: 18 · 2012: 13
- FWCI
- 15.07
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Pathogens (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Institutes of Health (CA-77955)
- National Cancer Institute (R29CA077955, CA 92229, CA-77955, CA116837, R01CA092229, R01CA077955)
- National Institute of Allergy and Infectious Diseases (R01AI038459, AI038459)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK058587, DK-58587)
- Topics
- Health Sciences › Medicine › Surgery › Helicobacter pylori-related gastroenterology studies
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
- Keywords
- Helicobacter pylori, CagA, VacA, iron acquisition, transferrin, transferrin receptor, transcytosis, iron trafficking, host-pathogen interaction, iron deficiency, Mongolian gerbil, bacterial effector proteins
- MeSH terms
- Adaptation, Physiological, Animals, Antigens, Bacterial, Bacterial Adhesion, Bacterial Proteins, Cell Line, Cell Membrane, Dogs, Epithelium, Gastric Mucosa, Gerbillinae, Humans, Intercellular Junctions, Iron, Receptors, Transferrin, Transferrin, Signal Transduction, Down-Regulation, Helicobacter pylori, Helicobacter Infections, Cell Polarity, Sequence Deletion, Caco-2 Cells, Transcytosis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
