Skip to main content
Top
Published in: Gut Pathogens 1/2012

Open Access 01-12-2012 | Research

Serologic host response to Helicobacter pylori and Campylobacter jejuni in socially housed Rhesus macaques (Macaca mulatta)

Authors: Sabine Kienesberger, Guillermo I Perez-Perez, Juan L Rivera-Correa, Rafael Tosado-Acevedo, Huilin Li, Andre Dubois, Janis A Gonzalez-Martinez, Maria Gloria Dominguez-Bello, Martin J Blaser

Published in: Gut Pathogens | Issue 1/2012

Login to get access

Abstract

Background

Helicobacter pylori are successful colonizers of the human gastric mucosa. Colonization increases the risk of peptic ulcer disease and adenocarcinoma. However, potential benefits of H. pylori colonization include protection against early-onset asthma and against gastrointestinal infections. Campylobacter jejuni are a leading cause of bacterial diarrhea and complications include Guillain-Barré syndrome. Here, we describe the development of reliable serological assays to detect antibodies against those two bacteria in Rhesus macaques and investigated their distribution within a social group of monkeys.

Methods

Two cohorts of monkeys were analyzed. The first cohort consisted of 30 monkeys and was used to establish an enzyme-linked immunosorbent assay (ELISA) for H. pylori antibodies detection. To evaluate colonization of those macaques, stomach biopsies were collected and analyzed for the presence of H. pylori by histology and culture. C. jejuni ELISAs were established using human serum with known C. jejuni antibody status. Next, plasma samples of the 89 macaques (Cohort 2) were assayed for antibodies and then statistically analyzed.

Results

An H. pylori IgG ELISA, which was 100% specific and 93% sensitive, was established. In contrast, the IgA ELISA was only 82% specific and 61% sensitive. The CagA IgG assay was 100% sensitive and 61% of the macaques were positive. In cohort 2, 62% macaques were H. pylori sero-positive and 52% were CagA positive. The prevalence of H. pylori IgG and CagA IgG increased with monkey age as described for humans. Of the 89 macaques 52% showed IgG against C. jejuni but in contrast to H. pylori, the sero-prevalence was not associated with increasing age. However, there was a drop in the IgG (but not in IgA) mean values between infant and juvenile macaques, similar to trends described in humans.

Conclusions

Rhesus macaques have widespread exposure to H. pylori and C. jejuni, reflecting their social conditions and implying that Rhesus macaques might provide a model to study effects of these two important human mucosal bacteria on a population.
Appendix
Available only for authorised users
Literature
1.
go back to reference Perez-Perez GI, Salomaa A, Kosunen TU, Daverman B, Rautelin H, Aromaa A, Knekt P, Blaser MJ: Evidence that cagA(+) Helicobacter pylori strains are disappearing more rapidly than cagA(−) strains. Gut. 2002, 50: 295-298. 10.1136/gut.50.3.295.PubMedCentralCrossRefPubMed Perez-Perez GI, Salomaa A, Kosunen TU, Daverman B, Rautelin H, Aromaa A, Knekt P, Blaser MJ: Evidence that cagA(+) Helicobacter pylori strains are disappearing more rapidly than cagA(−) strains. Gut. 2002, 50: 295-298. 10.1136/gut.50.3.295.PubMedCentralCrossRefPubMed
2.
go back to reference Banatvala N, Mayo K, Megraud F, Jennings R, Deeks JJ, Feldman RA: The cohort effect and Helicobacter pylori. J Infect Dis. 1993, 168: 219-221. 10.1093/infdis/168.1.219.CrossRefPubMed Banatvala N, Mayo K, Megraud F, Jennings R, Deeks JJ, Feldman RA: The cohort effect and Helicobacter pylori. J Infect Dis. 1993, 168: 219-221. 10.1093/infdis/168.1.219.CrossRefPubMed
3.
go back to reference Mishra S, Singh V, Rao GR, Dixit VK, Gulati AK, Nath G: Prevalence of Helicobacter pylorin asymptomatic subjects–a nested PCR based study. Infect Genet Evol. 2008, 8: 815-819. 10.1016/j.meegid.2008.08.001.CrossRefPubMed Mishra S, Singh V, Rao GR, Dixit VK, Gulati AK, Nath G: Prevalence of Helicobacter pylorin asymptomatic subjects–a nested PCR based study. Infect Genet Evol. 2008, 8: 815-819. 10.1016/j.meegid.2008.08.001.CrossRefPubMed
4.
go back to reference Ahmed KS, Khan AA, Ahmed I, Tiwari SK, Habeeb A, Ahi JD, Abid Z, Ahmed N, Habibullah CM: Impact of household hygiene and water source on the prevalence and transmission of Helicobacter pylori: a South Indian perspective. Singapore Med J. 2007, 48: 543-549.PubMed Ahmed KS, Khan AA, Ahmed I, Tiwari SK, Habeeb A, Ahi JD, Abid Z, Ahmed N, Habibullah CM: Impact of household hygiene and water source on the prevalence and transmission of Helicobacter pylori: a South Indian perspective. Singapore Med J. 2007, 48: 543-549.PubMed
5.
go back to reference Kumagai T, Malaty HM, Graham DY, Hosogaya S, Misawa K, Furihata K, Ota H, Sei C, Tanaka E, Akamatsu T: Acquisition versus loss of Helicobacter pylori infection in Japan: results from an 8-year birth cohort study. J Infect Dis. 1998, 178: 717-721. 10.1086/515376.CrossRefPubMed Kumagai T, Malaty HM, Graham DY, Hosogaya S, Misawa K, Furihata K, Ota H, Sei C, Tanaka E, Akamatsu T: Acquisition versus loss of Helicobacter pylori infection in Japan: results from an 8-year birth cohort study. J Infect Dis. 1998, 178: 717-721. 10.1086/515376.CrossRefPubMed
6.
go back to reference Goodman KJ, Correa P, Tengana Aux HJ, Ramirez H, DeLany JP, Guerrero Pepinosa O, Lopez Quinones M, Collazos Parra T: Helicobacter pylori infection in the Colombian Andes: a population-based study of transmission pathways. Am J Epidemiol. 1996, 144: 290-299. 10.1093/oxfordjournals.aje.a008924.CrossRefPubMed Goodman KJ, Correa P, Tengana Aux HJ, Ramirez H, DeLany JP, Guerrero Pepinosa O, Lopez Quinones M, Collazos Parra T: Helicobacter pylori infection in the Colombian Andes: a population-based study of transmission pathways. Am J Epidemiol. 1996, 144: 290-299. 10.1093/oxfordjournals.aje.a008924.CrossRefPubMed
7.
go back to reference Ernst PB, Gold BD: The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu Rev Microbiol. 2000, 54: 615-640. 10.1146/annurev.micro.54.1.615.CrossRefPubMed Ernst PB, Gold BD: The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu Rev Microbiol. 2000, 54: 615-640. 10.1146/annurev.micro.54.1.615.CrossRefPubMed
8.
go back to reference Chen Y, Blaser MJ: Inverse associations of Helicobacter pylori with asthma and allergy. Arch Intern Med. 2007, 167: 821-827. 10.1001/archinte.167.8.821.CrossRefPubMed Chen Y, Blaser MJ: Inverse associations of Helicobacter pylori with asthma and allergy. Arch Intern Med. 2007, 167: 821-827. 10.1001/archinte.167.8.821.CrossRefPubMed
9.
10.
go back to reference Arnold IC, Dehzad N, Reuter S, Martin H, Becher B, Taube C, Muller A: Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells. J Clin Invest. 2011, 121: 3088-3093. 10.1172/JCI45041.PubMedCentralCrossRefPubMed Arnold IC, Dehzad N, Reuter S, Martin H, Becher B, Taube C, Muller A: Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells. J Clin Invest. 2011, 121: 3088-3093. 10.1172/JCI45041.PubMedCentralCrossRefPubMed
11.
go back to reference Higgins PD, Johnson LA, Luther J, Zhang M, Sauder KL, Blanco LP, Kao JY: Prior Helicobacter pylori infection ameliorates Salmonella typhimurium-induced colitis: Mucosal crosstalk between stomach and distal intestine. Inflamm Bowel Dis. 2011, 17: 1398-1408. 10.1002/ibd.21489.PubMedCentralCrossRefPubMed Higgins PD, Johnson LA, Luther J, Zhang M, Sauder KL, Blanco LP, Kao JY: Prior Helicobacter pylori infection ameliorates Salmonella typhimurium-induced colitis: Mucosal crosstalk between stomach and distal intestine. Inflamm Bowel Dis. 2011, 17: 1398-1408. 10.1002/ibd.21489.PubMedCentralCrossRefPubMed
12.
go back to reference Cohen D, Shoham O, Orr N, Muhsen K: An inverse and independent association between Helicobacter pylori infection and the ncidence of shigellosis and other diarrheal diseases. Clin Infect Dis. 2012, 54: e35-42. 10.1093/cid/cir916.CrossRefPubMed Cohen D, Shoham O, Orr N, Muhsen K: An inverse and independent association between Helicobacter pylori infection and the ncidence of shigellosis and other diarrheal diseases. Clin Infect Dis. 2012, 54: e35-42. 10.1093/cid/cir916.CrossRefPubMed
13.
go back to reference Dubois A, Fiala N, Heman-Ackah LM, Drazek ES, Tarnawski A, Fishbein WN, Perez-Perez GI, Blaser MJ: Natural gastric infection with Helicobacter pylori in monkeys: a model for spiral bacteria infection in humans. Gastroenterology. 1994, 106: 1405-1417.PubMed Dubois A, Fiala N, Heman-Ackah LM, Drazek ES, Tarnawski A, Fishbein WN, Perez-Perez GI, Blaser MJ: Natural gastric infection with Helicobacter pylori in monkeys: a model for spiral bacteria infection in humans. Gastroenterology. 1994, 106: 1405-1417.PubMed
14.
go back to reference Drazek ES, Dubois A, Holmes RK: Characterization and presumptive identification of Helicobacter pylori isolates from rhesus monkeys. J Clin Microbiol. 1994, 32: 1799-1804.PubMedCentralPubMed Drazek ES, Dubois A, Holmes RK: Characterization and presumptive identification of Helicobacter pylori isolates from rhesus monkeys. J Clin Microbiol. 1994, 32: 1799-1804.PubMedCentralPubMed
15.
go back to reference Allos BM: Campylobacter jejuni Infections: update on emerging issues and trends. Clin Infect Dis. 2001, 32: 1201-1206. 10.1086/319760.CrossRefPubMed Allos BM: Campylobacter jejuni Infections: update on emerging issues and trends. Clin Infect Dis. 2001, 32: 1201-1206. 10.1086/319760.CrossRefPubMed
16.
go back to reference Dingle KE, Van Den Braak N, Colles FM, Price LJ, Woodward DL, Rodgers FG, Endtz HP, Van Belkum A, Maiden MC: Sequence typing confirms that Campylobacter jejuni strains associated with Guillain-Barre and Miller-Fisher syndromes are of diverse genetic lineage, serotype, and flagella type. J Clin Microbiol. 2001, 39: 3346-3349. 10.1128/JCM.39.9.3346-3349.2001.PubMedCentralCrossRefPubMed Dingle KE, Van Den Braak N, Colles FM, Price LJ, Woodward DL, Rodgers FG, Endtz HP, Van Belkum A, Maiden MC: Sequence typing confirms that Campylobacter jejuni strains associated with Guillain-Barre and Miller-Fisher syndromes are of diverse genetic lineage, serotype, and flagella type. J Clin Microbiol. 2001, 39: 3346-3349. 10.1128/JCM.39.9.3346-3349.2001.PubMedCentralCrossRefPubMed
17.
go back to reference Yuki N, Tagawa Y, Irie F, Hirabayashi Y, Handa S: Close association of Guillain-Barre syndrome with antibodies to minor monosialogangliosides GM1b and GM1 alpha. J Neuroimmunol. 1997, 74: 30-34. 10.1016/S0165-5728(96)00201-9.CrossRefPubMed Yuki N, Tagawa Y, Irie F, Hirabayashi Y, Handa S: Close association of Guillain-Barre syndrome with antibodies to minor monosialogangliosides GM1b and GM1 alpha. J Neuroimmunol. 1997, 74: 30-34. 10.1016/S0165-5728(96)00201-9.CrossRefPubMed
18.
go back to reference Moran AP, Prendergast MM: Molecular mimicry in Campylobacter jejuni lipopolysaccharides and the development of Guillain-Barre syndrome. J Infect Dis. 1998, 178: 1549-1551. 10.1086/314462.CrossRefPubMed Moran AP, Prendergast MM: Molecular mimicry in Campylobacter jejuni lipopolysaccharides and the development of Guillain-Barre syndrome. J Infect Dis. 1998, 178: 1549-1551. 10.1086/314462.CrossRefPubMed
19.
go back to reference Andrade MC, Gabeira SC, Abreu-Lopes D, Esteves WT, Vilardo Mde C, Thome JD, Cabello PH, Lauria-Filgueiras AL: Circulation of Campylobacter spp. in rhesus monkeys (Macaca mulatta) held in captivity: a longitudinal study. Mem Inst Oswaldo Cruz. 2007, 102: 53-57. 10.1590/S0074-02762007000100008.CrossRefPubMed Andrade MC, Gabeira SC, Abreu-Lopes D, Esteves WT, Vilardo Mde C, Thome JD, Cabello PH, Lauria-Filgueiras AL: Circulation of Campylobacter spp. in rhesus monkeys (Macaca mulatta) held in captivity: a longitudinal study. Mem Inst Oswaldo Cruz. 2007, 102: 53-57. 10.1590/S0074-02762007000100008.CrossRefPubMed
20.
go back to reference Solnick JV, Chang K, Canfield DR, Parsonnet J: Natural acquisition of Helicobacter pylori infection in newborn rhesus macaques. J Clin Microbiol. 2003, 41: 5511-5516. 10.1128/JCM.41.12.5511-5516.2003.PubMedCentralCrossRefPubMed Solnick JV, Chang K, Canfield DR, Parsonnet J: Natural acquisition of Helicobacter pylori infection in newborn rhesus macaques. J Clin Microbiol. 2003, 41: 5511-5516. 10.1128/JCM.41.12.5511-5516.2003.PubMedCentralCrossRefPubMed
21.
go back to reference Boonjakuakul JK, Canfield DR, Solnick JV: Comparison of Helicobacter pylori virulence gene expression in vitro and in the Rhesus macaque. Infect Immun. 2005, 73: 4895-4904. 10.1128/IAI.73.8.4895-4904.2005.PubMedCentralCrossRefPubMed Boonjakuakul JK, Canfield DR, Solnick JV: Comparison of Helicobacter pylori virulence gene expression in vitro and in the Rhesus macaque. Infect Immun. 2005, 73: 4895-4904. 10.1128/IAI.73.8.4895-4904.2005.PubMedCentralCrossRefPubMed
22.
go back to reference Mattapallil JJ, Dandekar S, Canfield DR, Solnick JV: A predominant Th1 type of immune response is induced early during acute Helicobacter pylori infection in rhesus macaques. Gastroenterology. 2000, 118: 307-315. 10.1016/S0016-5085(00)70213-7.CrossRefPubMed Mattapallil JJ, Dandekar S, Canfield DR, Solnick JV: A predominant Th1 type of immune response is induced early during acute Helicobacter pylori infection in rhesus macaques. Gastroenterology. 2000, 118: 307-315. 10.1016/S0016-5085(00)70213-7.CrossRefPubMed
23.
go back to reference Solnick JV, Hansen LM, Salama NR, Boonjakuakul JK, Syvanen M: Modification of Helicobacter pylori outer membrane protein expression during experimental infection of rhesus macaques. Proc Natl Acad Sci U S A. 2004, 101: 2106-2111. 10.1073/pnas.0308573100.PubMedCentralCrossRefPubMed Solnick JV, Hansen LM, Salama NR, Boonjakuakul JK, Syvanen M: Modification of Helicobacter pylori outer membrane protein expression during experimental infection of rhesus macaques. Proc Natl Acad Sci U S A. 2004, 101: 2106-2111. 10.1073/pnas.0308573100.PubMedCentralCrossRefPubMed
24.
go back to reference Styer CM, Hansen LM, Cooke CL, Gundersen AM, Choi SS, Berg DE, Benghezal M, Marshall BJ, Peek RM, Boren T, Solnick JV: Expression of the BabA adhesin during experimental infection with Helicobacter pylori. Infect Immun. 2010, 78: 1593-1600. 10.1128/IAI.01297-09.PubMedCentralCrossRefPubMed Styer CM, Hansen LM, Cooke CL, Gundersen AM, Choi SS, Berg DE, Benghezal M, Marshall BJ, Peek RM, Boren T, Solnick JV: Expression of the BabA adhesin during experimental infection with Helicobacter pylori. Infect Immun. 2010, 78: 1593-1600. 10.1128/IAI.01297-09.PubMedCentralCrossRefPubMed
25.
go back to reference Dabiri H, Maleknejad P, Yamaoka Y, Feizabadi MM, Jafari F, Rezadehbashi M, Nakhjavani FA, Mirsalehian A, Zali MR: Distribution of Helicobacter pyloricagA, cagE, oipA and vacA in different major ethnic groups in Tehran, Iran. J Gastroenterol Hepatol. 2009, 24: 1380-1386. 10.1111/j.1440-1746.2009.05876.x.PubMedCentralCrossRefPubMed Dabiri H, Maleknejad P, Yamaoka Y, Feizabadi MM, Jafari F, Rezadehbashi M, Nakhjavani FA, Mirsalehian A, Zali MR: Distribution of Helicobacter pyloricagA, cagE, oipA and vacA in different major ethnic groups in Tehran, Iran. J Gastroenterol Hepatol. 2009, 24: 1380-1386. 10.1111/j.1440-1746.2009.05876.x.PubMedCentralCrossRefPubMed
26.
go back to reference Contreras M, Pujol FH, Perez-Perez GI, Marini E, Michelangeli FA, Ponce L, Dominguez-Bello MG: Helicobacter pylori seroprevalence in Amerindians from isolated locations. Am J Trop Med Hyg. 2008, 78: 574-576.PubMed Contreras M, Pujol FH, Perez-Perez GI, Marini E, Michelangeli FA, Ponce L, Dominguez-Bello MG: Helicobacter pylori seroprevalence in Amerindians from isolated locations. Am J Trop Med Hyg. 2008, 78: 574-576.PubMed
27.
go back to reference Torres J, Camorlinga-Ponce M, Perez-Perez G, Munoz L, Munoz O: Specific serum immunoglobulin G response to urease and CagA antigens of Helicobacter pylori in infected children and adults in a country with high prevalence of infection. Clin Diagn Lab Immunol. 2002, 9: 97-100.PubMedCentralPubMed Torres J, Camorlinga-Ponce M, Perez-Perez G, Munoz L, Munoz O: Specific serum immunoglobulin G response to urease and CagA antigens of Helicobacter pylori in infected children and adults in a country with high prevalence of infection. Clin Diagn Lab Immunol. 2002, 9: 97-100.PubMedCentralPubMed
28.
go back to reference Perez-Perez GI, Cohn DL, Guerrant RL, Patton CM, Reller LB, Blaser MJ: Clinical and immunologic significance of cholera-like toxin and cytotoxin production by Campylobacter species in patients with acute inflammatory diarrhea in the USA. J Infect Dis. 1989, 160: 460-468. 10.1093/infdis/160.3.460.CrossRefPubMed Perez-Perez GI, Cohn DL, Guerrant RL, Patton CM, Reller LB, Blaser MJ: Clinical and immunologic significance of cholera-like toxin and cytotoxin production by Campylobacter species in patients with acute inflammatory diarrhea in the USA. J Infect Dis. 1989, 160: 460-468. 10.1093/infdis/160.3.460.CrossRefPubMed
29.
go back to reference Blaser MJ, Black RE, Duncan DJ, Amer J: Campylobacter jejuni-specific serum antibodies are elevated in healthy Bangladeshi children. J Clin Microbiol. 1985, 21: 164-167.PubMedCentralPubMed Blaser MJ, Black RE, Duncan DJ, Amer J: Campylobacter jejuni-specific serum antibodies are elevated in healthy Bangladeshi children. J Clin Microbiol. 1985, 21: 164-167.PubMedCentralPubMed
30.
go back to reference Blaser MJ, Taylor DN, Echeverria P: Immune response to Campylobacter jejuni in a rural community in Thailand. J Infect Dis. 1986, 153: 249-254. 10.1093/infdis/153.2.249.CrossRefPubMed Blaser MJ, Taylor DN, Echeverria P: Immune response to Campylobacter jejuni in a rural community in Thailand. J Infect Dis. 1986, 153: 249-254. 10.1093/infdis/153.2.249.CrossRefPubMed
31.
go back to reference Timmins RJ, Richardson M, Chhangani A, Yongcheng L: Macaca mulatta. IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1. 2008, [www.iucnredlist.org]. Downloaded on 20 August 2012. Timmins RJ, Richardson M, Chhangani A, Yongcheng L: Macaca mulatta. IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1. 2008, [www.​iucnredlist.​org]. Downloaded on 20 August 2012.
32.
go back to reference Shedlock DJ, Silvestri G, Weiner DB: Monkeying around with HIV vaccines: using rhesus macaques to define 'gatekeepers' for clinical trials. Nat Rev Immunol. 2009, 9: 717-728. 10.1038/nri2636.PubMedCentralCrossRefPubMed Shedlock DJ, Silvestri G, Weiner DB: Monkeying around with HIV vaccines: using rhesus macaques to define 'gatekeepers' for clinical trials. Nat Rev Immunol. 2009, 9: 717-728. 10.1038/nri2636.PubMedCentralCrossRefPubMed
33.
go back to reference Edghill-Smith Y, Golding H, Manischewitz J, King LR, Scott D, Bray M, Nalca A, Hooper JW, Whitehouse CA, Schmitz JE: Smallpox vaccine-induced antibodies are necessary and sufficient for protection against monkeypox virus. Nat Med. 2005, 11: 740-747. 10.1038/nm1261.CrossRefPubMed Edghill-Smith Y, Golding H, Manischewitz J, King LR, Scott D, Bray M, Nalca A, Hooper JW, Whitehouse CA, Schmitz JE: Smallpox vaccine-induced antibodies are necessary and sufficient for protection against monkeypox virus. Nat Med. 2005, 11: 740-747. 10.1038/nm1261.CrossRefPubMed
34.
go back to reference Sparman M, Dighe V, Sritanaudomchai H, Ma H, Ramsey C, Pedersen D, Clepper L, Nighot P, Wolf D, Hennebold J, Mitalipov S: Epigenetic reprogramming by somatic cell nuclear transfer in primates. Stem Cells. 2009, 27: 1255-1264. 10.1002/stem.60.PubMedCentralCrossRefPubMed Sparman M, Dighe V, Sritanaudomchai H, Ma H, Ramsey C, Pedersen D, Clepper L, Nighot P, Wolf D, Hennebold J, Mitalipov S: Epigenetic reprogramming by somatic cell nuclear transfer in primates. Stem Cells. 2009, 27: 1255-1264. 10.1002/stem.60.PubMedCentralCrossRefPubMed
35.
go back to reference Byrne JA, Pedersen DA, Clepper LL, Nelson M, Sanger WG, Gokhale S, Wolf DP, Mitalipov SM: Producing primate embryonic stem cells by somatic cell nuclear transfer. Nature. 2007, 450: 497-502. 10.1038/nature06357.CrossRefPubMed Byrne JA, Pedersen DA, Clepper LL, Nelson M, Sanger WG, Gokhale S, Wolf DP, Mitalipov SM: Producing primate embryonic stem cells by somatic cell nuclear transfer. Nature. 2007, 450: 497-502. 10.1038/nature06357.CrossRefPubMed
36.
go back to reference Taylor DN, Echeverria P, Pitarangsi C, Seriwatana J, Bodhidatta L, Blaser MJ: Influence of strain characteristics and immunity on the epidemiology of Campylobacter infections in Thailand. J Clin Microbiol. 1988, 26: 863-868.PubMedCentralPubMed Taylor DN, Echeverria P, Pitarangsi C, Seriwatana J, Bodhidatta L, Blaser MJ: Influence of strain characteristics and immunity on the epidemiology of Campylobacter infections in Thailand. J Clin Microbiol. 1988, 26: 863-868.PubMedCentralPubMed
37.
go back to reference Perez-Perez GI, Blaser MJ: Conservation and diversity of Campylobacter pyloridis major antigens. Infect Immun. 1987, 55: 1256-1263.PubMedCentralPubMed Perez-Perez GI, Blaser MJ: Conservation and diversity of Campylobacter pyloridis major antigens. Infect Immun. 1987, 55: 1256-1263.PubMedCentralPubMed
38.
go back to reference Ng EK, Thompson SA, Perez-Perez GI, Kansau I, van der Ende A, Labigne A, Sung JJ, Chung SC, Blaser MJ: Helicobacter pylori heat shock protein A: serologic responses and genetic diversity. Clin Diagn Lab Immunol. 1999, 6: 377-382.PubMedCentralPubMed Ng EK, Thompson SA, Perez-Perez GI, Kansau I, van der Ende A, Labigne A, Sung JJ, Chung SC, Blaser MJ: Helicobacter pylori heat shock protein A: serologic responses and genetic diversity. Clin Diagn Lab Immunol. 1999, 6: 377-382.PubMedCentralPubMed
39.
go back to reference Gootz TD, Perez-Perez GI, Clancy J, Martin BA, Tait-Kamradt A, Blaser MJ: Immunological and molecular characterization of Helicobacter felis urease. Infect Immun. 1994, 62: 793-798.PubMedCentralPubMed Gootz TD, Perez-Perez GI, Clancy J, Martin BA, Tait-Kamradt A, Blaser MJ: Immunological and molecular characterization of Helicobacter felis urease. Infect Immun. 1994, 62: 793-798.PubMedCentralPubMed
40.
go back to reference Suerbaum S, Josenhans C, Sterzenbach T, Drescher B, Brandt P, Bell M, Droge M, Fartmann B, Fischer HP, Ge Z: The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc Natl Acad Sci U S A. 2003, 100: 7901-7906. 10.1073/pnas.1332093100.PubMedCentralCrossRefPubMed Suerbaum S, Josenhans C, Sterzenbach T, Drescher B, Brandt P, Bell M, Droge M, Fartmann B, Fischer HP, Ge Z: The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc Natl Acad Sci U S A. 2003, 100: 7901-7906. 10.1073/pnas.1332093100.PubMedCentralCrossRefPubMed
41.
go back to reference Perez-Perez GI, Dworkin BM, Chodos JE, Blaser MJ: Campylobacter pylori antibodies in humans. Ann Intern Med. 1988, 109: 11-17.CrossRefPubMed Perez-Perez GI, Dworkin BM, Chodos JE, Blaser MJ: Campylobacter pylori antibodies in humans. Ann Intern Med. 1988, 109: 11-17.CrossRefPubMed
42.
go back to reference Perez-Perez GI, Taylor DN, Bodhidatta L, Wongsrichanalai J, Baze WB, Dunn BE, Echeverria PD, Blaser MJ: Seroprevalence of Helicobacter pylori infections in Thailand. J Infect Dis. 1990, 161: 1237-1241. 10.1093/infdis/161.6.1237.CrossRefPubMed Perez-Perez GI, Taylor DN, Bodhidatta L, Wongsrichanalai J, Baze WB, Dunn BE, Echeverria PD, Blaser MJ: Seroprevalence of Helicobacter pylori infections in Thailand. J Infect Dis. 1990, 161: 1237-1241. 10.1093/infdis/161.6.1237.CrossRefPubMed
43.
go back to reference Faulde M, Putzker M, Mertes T, Sobe D: Evaluation of an immunofluorescence assay for specific detection of immunoglobulin G antibodies directed against Helicobacter pylori, and antigenic cross-reactivity between H. pylori and Campylobacter jejuni. J Clin Microbiol. 1991, 29: 323-327.PubMedCentralPubMed Faulde M, Putzker M, Mertes T, Sobe D: Evaluation of an immunofluorescence assay for specific detection of immunoglobulin G antibodies directed against Helicobacter pylori, and antigenic cross-reactivity between H. pylori and Campylobacter jejuni. J Clin Microbiol. 1991, 29: 323-327.PubMedCentralPubMed
44.
go back to reference Karvar S, Karch H, Frosch M, Burghardt W, Gross U: Use of serum-specific immunoglobulins A and G for detection of Helicobacter pylori infection in patients with chronic gastritis by immunoblot analysis. J Clin Microbiol. 1997, 35: 3058-3061.PubMedCentralPubMed Karvar S, Karch H, Frosch M, Burghardt W, Gross U: Use of serum-specific immunoglobulins A and G for detection of Helicobacter pylori infection in patients with chronic gastritis by immunoblot analysis. J Clin Microbiol. 1997, 35: 3058-3061.PubMedCentralPubMed
45.
go back to reference Vorobjova T, Nilsson I, Kull K, Maaroos HI, Covacci A, Wadstrom T, Uibo R: CagA protein seropositivity in a random sample of adult population and gastric cancer patients in Estonia. Eur J Gastroenterol Hepatol. 1998, 10: 41-46. 10.1097/00042737-199801000-00008.CrossRefPubMed Vorobjova T, Nilsson I, Kull K, Maaroos HI, Covacci A, Wadstrom T, Uibo R: CagA protein seropositivity in a random sample of adult population and gastric cancer patients in Estonia. Eur J Gastroenterol Hepatol. 1998, 10: 41-46. 10.1097/00042737-199801000-00008.CrossRefPubMed
46.
go back to reference Solnick JV, Fong J, Hansen LM, Chang K, Canfield DR, Parsonnet J: Acquisition of Helicobacter pylori infection in rhesus macaques is most consistent with oral-oral transmission. J Clin Microbiol. 2006, 44: 3799-3803. 10.1128/JCM.01482-06.PubMedCentralCrossRefPubMed Solnick JV, Fong J, Hansen LM, Chang K, Canfield DR, Parsonnet J: Acquisition of Helicobacter pylori infection in rhesus macaques is most consistent with oral-oral transmission. J Clin Microbiol. 2006, 44: 3799-3803. 10.1128/JCM.01482-06.PubMedCentralCrossRefPubMed
47.
go back to reference Dubois A, Berg DE, Incecik ET, Fiala N, Heman-Ackah LM, Perez-Perez GI, Blaser MJ: Transient and persistent experimental infection of nonhuman primates with Helicobacter pylori: implications for human disease. Infect Immun. 1996, 64: 2885-2891.PubMedCentralPubMed Dubois A, Berg DE, Incecik ET, Fiala N, Heman-Ackah LM, Perez-Perez GI, Blaser MJ: Transient and persistent experimental infection of nonhuman primates with Helicobacter pylori: implications for human disease. Infect Immun. 1996, 64: 2885-2891.PubMedCentralPubMed
48.
go back to reference Blaser MJ, Perez-Perez GI, Kleanthous H, Cover TL, Peek RM, Chyou PH, Stemmermann GN, Nomura A: Infection with Helicobacter pylori strains possessing CagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res. 1995, 55: 2111-2115.PubMed Blaser MJ, Perez-Perez GI, Kleanthous H, Cover TL, Peek RM, Chyou PH, Stemmermann GN, Nomura A: Infection with Helicobacter pylori strains possessing CagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res. 1995, 55: 2111-2115.PubMed
49.
go back to reference McCoy EC, Doyle D, Burda K, Corbeil LB, Winter AJ: Superficial antigens of Campylobacter (Vibrio) fetus: characterization of antiphagocytic component. Infect Immun. 1975, 11: 517-525.PubMedCentralPubMed McCoy EC, Doyle D, Burda K, Corbeil LB, Winter AJ: Superficial antigens of Campylobacter (Vibrio) fetus: characterization of antiphagocytic component. Infect Immun. 1975, 11: 517-525.PubMedCentralPubMed
50.
go back to reference Blaser MJ, Duncan DJ: Human serum antibody response to Campylobacter jejuni infection as measured in an enzyme-linked immunosorbent assay. Infect Immun. 1984, 44: 292-298.PubMedCentralPubMed Blaser MJ, Duncan DJ: Human serum antibody response to Campylobacter jejuni infection as measured in an enzyme-linked immunosorbent assay. Infect Immun. 1984, 44: 292-298.PubMedCentralPubMed
Metadata
Title
Serologic host response to Helicobacter pylori and Campylobacter jejuni in socially housed Rhesus macaques (Macaca mulatta)
Authors
Sabine Kienesberger
Guillermo I Perez-Perez
Juan L Rivera-Correa
Rafael Tosado-Acevedo
Huilin Li
Andre Dubois
Janis A Gonzalez-Martinez
Maria Gloria Dominguez-Bello
Martin J Blaser
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2012
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/1757-4749-4-9

Other articles of this Issue 1/2012

Gut Pathogens 1/2012 Go to the issue