Skip to main content

Helicobacter pylori Peptidyl Prolyl cis, trans Isomerase: A Modulator of the Host Immune Response

  • Chapter
  • First Online:

Part of the book series: Heat Shock Proteins ((HESP,volume 7))

Abstract

Helicobacter pylori is an intriguing bacterium because of its ability to survive at low pH in the stomach and its relationship with gastric inflammation and cancer. Among its armamentarium of virulence factors is HP0175, a peptidylprolyl isomerase (PPIase), which is secreted and is a major antigen in patients with H. pylori-induced pathology. This review summarizes the moonlighting functions of HP0175, revealing that this secreted protein-folding catalyst regulates cell signalling in gastric epithelial cells and in monocytic cells to modulate the inflammatory response and apoptosis during H. pylori infection. In addition, it elicits a Th17 response thereby modulating the adaptive immune response. These activities reveal the importance of protein moonlighting in the generation of H. pylori-induced disease states.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Acehan D, Jiang X, Morgan DG, Heuser JE, Wang X, Akey CW (2002) Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol Cell 9:423–432

    Article  PubMed  CAS  Google Scholar 

  • Alvi A, Ansari SA, Ehtesham NZ, Rizwan M, Devi S, Sechi LA, Qureshi IA, Hasnain SE, Ahmed N (2011) Concurrent proinflammatory and apoptotic activity of a Helicobacter pylori protein (HP986) points to its role in chronic persistence. PLoS One 6:e22530

    Article  PubMed  CAS  Google Scholar 

  • Amedei A, Munari F, Della Bella C, Niccolai E, Banagiano M, Bencini L, Cianchi F, Farsi M, Emmi G, Zanotti G, de Bernard M, Kundu M, D’Elios, MM (2012) Helicobacter pylori secreted peptidyl prolyl cis, trans-isomerase drives Th17 inflammation in gastric adenocarcinoma. Int Emerg Med. doi: 10.1007/s11739-012-0867-9

  • Amieva MR, Vogelmann R, Covacci A, Tompkins LS, Nelson WJ, Falkow S (2003) Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 300:1430–1434

    Article  PubMed  CAS  Google Scholar 

  • Ashktorab H, Neapolitano M, Bomma C, Allen C, Ahmed A, Dubois A, Naab T, Smoot DT (2002) In vivo and in vitro activation of caspase 8 and-3 associated with Helicobacter pylori infection. Microbes Infect 7:713–722

    Article  Google Scholar 

  • Atanassov C, Pezennec L, d’Alayer J, Grollier G, Picard B, Fauchère JL (2002) Novel antigens of Helicobacter pylori correspond to ulcer-related antibody pattern of sera from infected patients. J Clin Microbiol 40:547–552

    Article  PubMed  CAS  Google Scholar 

  • Atherton JC (2006) The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Annu Rev Pathol 1:63–96

    Article  PubMed  CAS  Google Scholar 

  • Backert S, Selbach M (2008) Role of type IV secretion in Helicobacter pylori pathogenesis. Cell Microbiol 10:1573–1581

    Article  PubMed  CAS  Google Scholar 

  • Basak C, Pathak SK, Bhattacharyya A, Pathak S, Basu J, Kundu M (2005) The secreted peptidyl prolyl cis, trans-isomerase HP0175 of Helicobacter pylori induces apoptosis of gastric epithelial cells in a TLR4- and apoptosis signal-regulating kinase 1-dependent manner. J Immunol 174:5672–5680

    PubMed  CAS  Google Scholar 

  • Basu S, Pathak SK, Chatterjee G, Pathak S, Basu J, Kundu M (2008) Helicobacter pylori protein HP0175 transactivates epidermal growth factor receptor through TLR4 in gastric epithelial cells. J Biol Chem 283:32369–32376

    Article  PubMed  CAS  Google Scholar 

  • Blanchard TG, Yu F, Hsieh CL, Redline RW (2003) Severe inflammation and reduced bacteria load in murine helicobacter infection caused by lack of phagocyte oxidase activity. J Infect Dis 187:1609–1615

    Article  PubMed  CAS  Google Scholar 

  • Blaser MJ, Parsonnet J (1994) Parasitism by the “slow” bacterium Helicobacter pylori leads to altered gastric homeostasis and neoplasia. J Clin Invest 94:4–8

    Article  PubMed  CAS  Google Scholar 

  • Bröker LE, Kruyt FA, Giaccone G (2005) Cell death independent of caspases: a review. Clin Cancer Res 11:3155–3162

    Article  PubMed  Google Scholar 

  • Bumann D, Aksu S, Wendland M, Janek K, Zimny-Arndt U, Sabarth N, Meyer TF, Jungblut PR (2002) Proteome analysis of secreted proteins of the gastric pathogen Helicobacter pylori. Infect Immun 70:3396–3403

    Article  PubMed  CAS  Google Scholar 

  • Cargnello M, Roux PR (2011) Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 75:50–83

    Article  PubMed  CAS  Google Scholar 

  • Caruso R, Fina D, Peluso I, Fantini MC, Tosti C et al (2007) IL-21 is highly produced in Helicobacter pylori-infected gastric mucosa and promotes gelatinase synthesis. J Immunol 178:5957–5965

    PubMed  CAS  Google Scholar 

  • Caruso R, Fina D, Paoluzi OA, Del Vecchio Blanco G, Stolfi C, Rizzo A, Caprioli F, Sarra M, Andrei F, Fantini MC, MacDonald TT, Pallone F, Monteleone G (2008) IL-23-mediated regulation of IL-17 production in Helicobacter pylori-infected gastric mucosa. Eur J Immunol 38:470–478

    Article  PubMed  CAS  Google Scholar 

  • Choi IJ, Kim JS, Kim JM, Jung HC, Song IS (2003) Effect of inhibition of extracellular signal-regulated kinase 1 and 2 pathway on apoptosis and bcl-2 expression in Helicobacter pylori-infected AGS cells. Infect Immun 71:830–837

    Article  PubMed  CAS  Google Scholar 

  • Correa P, Miller MJ (1998) Carcinogenesis, apoptosis and cell proliferation. Br Med Bull 54:151–162

    Article  PubMed  CAS  Google Scholar 

  • Cover TL, Krishna US, Israel DA, Peek RM Jr (2001) Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res 63:951–957

    Google Scholar 

  • D’Elios MM, Andersen LP (2009) Inflammation, immunity, and vaccines for H. pylori. Helicobacter 14(S1):21–28

    Article  PubMed  Google Scholar 

  • Eslick GD, Lim LL, Byles JE, Xia HH, Talley NJ (1999) Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis. Am J Gastroenterol 94:2373–2379

    Article  PubMed  CAS  Google Scholar 

  • Estaquier J, Vallette F, Vayssiere JL, Mignotte B (2012) The mitochondrial pathways of apoptosis. Adv Exp Med Biol 942:157–183

    Article  PubMed  CAS  Google Scholar 

  • Fan X, Gunasena H, Cheng Z, Espejo R, Crowe SE, Ernst PB, Reyes VE (2000) Helicobacter pylori urease binds to class II MHC on gastric epithelial cells and induces their apoptosis. J Immunol 165:1918–1924

    PubMed  CAS  Google Scholar 

  • Fanghänel J, Fischer G (2004) Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front Biosci 9:3453–3478

    Article  PubMed  Google Scholar 

  • Fischer G, Wittmann-Liebold B, Lang K, Kiefhaber T, Schmid FX (1989) Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337:476–478

    Article  PubMed  CAS  Google Scholar 

  • Fischer G, Bang H, Ludwig B, Mann K, Hacker J (1992) Mip protein of Legionella pneumophila exhibits peptidyl prolyl cis/trans isomerase (PPIase) activity. Mol Microbiol 6:1375–1383

    Article  PubMed  CAS  Google Scholar 

  • Fuchs Y, Steller H (2011) Programmed cell death in animal development and disease. Cell 47:742–758

    Article  Google Scholar 

  • Fujikawa A, Shirasaka D, Yamamoto S, Ota H, Yahiro K, Fukada M, Shintani T, Wada A, Aoyama N, Hirayama T, Fukamachi H, Noda M (2003) Mice deficient in protein tyrosine phosphatase receptor type Z are resistant to gastric ulcer induction by VacA of Helicobacter pylori. Nat Genet 33:375–381

    Article  PubMed  CAS  Google Scholar 

  • Hacker J, Fischer G (1993) Immunophilins: structure-function relationship and possible role in microbial pathogenecity. Mol Microbiol 10:445–456

    Article  PubMed  CAS  Google Scholar 

  • Harding MW, Galat A, Uehling DE, Schreiber SL (1989) A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature 341:758–760

    Article  PubMed  CAS  Google Scholar 

  • Hatakeyama M (2004) Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat Rev Cancer 4:688–694

    Article  PubMed  CAS  Google Scholar 

  • Hayano T, Takahashi N, Kato S, Maki N, Suzuki M (1991) Two distinct forms of peptidylprolyl-cis-trans-isomerase are expressed separately in periplasmic and cytoplasmic compartments of Escherichia coli. Biochemistry 30:3041–3048

    Article  PubMed  CAS  Google Scholar 

  • Heikkinen O, Seppala R, Tossavainen H, Heikkinen S, Koskela H, Permi P, Kilpeläinen I (2009) Solution structure of the parvulin-type PPIase domain of Staphylococcus aureus PrsA – implications for the catalytic mechanism of parvulins. BMC Struct Biol 9:17

    Article  PubMed  Google Scholar 

  • Hermans PW, Adrian PV, Albert C, Estevao S, Hoogenboezem T, Luijendijk IH, Kamphausen T, Hammerschmidt S (2006) The streptococcal lipoprotein rotamase A (SlrA) is a functional peptidyl-prolyl isomerase involved in pneumococcal colonization. J Biol Chem 281:968–976

    Article  PubMed  CAS  Google Scholar 

  • Huang JQ, Sridhar S, Chen Y, Hunt RH (1998) Meta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer. Gastroenterology 114:1169–1179

    Article  PubMed  CAS  Google Scholar 

  • Ichijo H (2004) The ASK1-MAP kinase cascades in mammalian stress response. J Biochem 136:261–265

    Article  PubMed  Google Scholar 

  • Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh S, Moriguchi T, Takagi M, Matsumoto K, Miyazono K, Gotoh Y (1997) Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275:90–94

    Article  PubMed  CAS  Google Scholar 

  • Ishihara S, Rumi MA, Kadowaki Y, Ortega-Cava CF, Yuki T, Yoshino N, Miyaoka Y, Kazumori H, Ishimura N, Amano Y, Kinoshita Y (2004) Essential role of MD-2 in TLR4-dependent signaling during Helicobacter pylori-associated gastritis. J Immunol 173:1406–1416

    PubMed  CAS  Google Scholar 

  • Ismail HF, Zhang J, Lynch RG, Wang Y, Berg DJ (2003) Role for complement in development of Helicobacter-induced gastritis in interleukin-10-deficient mice. Infect Immun 71:7140–7148

    Article  PubMed  CAS  Google Scholar 

  • Jones NL, Day AS, Jennings HA, Shermann 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 

  • Keates S, Keates AC, Warny M, Peek RM Jr, Murray PG, Kelly CP (1999) Differential activation of mitogen-activated protein kinases in AGS gastric epithelial cells by cag+ and cag- Helicobacter pylori. J Immunol 163:5552–5559

    PubMed  CAS  Google Scholar 

  • Kim N, Weeks DL, Shin JM, Scott DR, Young MK, Sachs G (2002) Proteins released by Helicobacter pylori in vitro. J Bacteriol 184:6155–66162

    Article  PubMed  CAS  Google Scholar 

  • Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer PH, Peter ME (1995) Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 14:5579–5588

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kusters JG, van Vliet AH, Kuipers EJ (2006) Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19:449–490

    Article  PubMed  CAS  Google Scholar 

  • Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of Bid by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491–501

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147–157

    Article  PubMed  CAS  Google Scholar 

  • Luzza F, Parrello T, Monteleone G, Sebkova L, Romano M, Zarrilli R, Imeneo M, Pallone F (2000) Up-regulation of IL-17 is associated with bioactive IL-8 expression in Helicobacter pylori-infected human gastric mucosa. J Immunol 165:5332–5337

    PubMed  CAS  Google Scholar 

  • Maity A, Pore N, Lee J, Solomon D, O’Rourke DM (2000) Epidermal growth factor receptor transcriptionally up-regulates vascular endothelial growth factor expression in human glioblastoma cells via a pathway involving phosphatidylinositol 3′-kinase and distinct from that induced by hypoxia. Cancer Res 60:5879–5886

    PubMed  CAS  Google Scholar 

  • Matsuzawa A, Ichijo H (2001) Molecular mechanisms of the decision between life and death: regulation of apoptosis by apoptosis signal-regulating kinase 1. J Biochem 130:1–8

    Article  PubMed  CAS  Google Scholar 

  • McAtee CP, Lim MY, Fung K, Velligan M, Fry K, Chow T, Berg DE (1998) Identification of potential diagnostic and vaccine candidates of Helicobacter pylori by two-dimensional gel electrophoresis, sequence analysis, and serum profiling. Clin Diagn Lab Immunol 5:537–542

    PubMed  CAS  Google Scholar 

  • Mimuro H, Suzuki T, Nagai S, Rieder G, Suzuki M, Nagai T, Fujita Y, Nagamatsu K, Ishijima N, Koyasu S, Haas R, Sasakawa C (2007) Helicobacter pylori dampens gut epithelial self-renewal by inhibiting apoptosis, a bacterial strategy to enhance colonization of the stomach. Cell Host Microbe 2:209–211

    Article  Google Scholar 

  • Muzio M, Salvesen GS, Dixit VM (1997) FLICE induced apoptosis in a cell-free system. Cleavage of caspase zymogens. J Biol Chem 272:2952–29556

    Article  PubMed  CAS  Google Scholar 

  • Nomura A, Stemmermann GN, Chyou PH, Perez-Perez GI, Blaser MJ (1994) Helicobacter pylori infection and the risk for duodenal and gastric ulceration. Ann Intern Med 120:977–981

    Article  PubMed  CAS  Google Scholar 

  • Oberst A, Bender C, Green DR (2008) Living with death: the evolution of the mitochondrial pathway of apoptosis in animals. Cell Death Differ 15:1139–1146

    Article  PubMed  CAS  Google Scholar 

  • Okada H, Suh WK, Jin J, Woo M, Du C, Elia A, Duncan GS, Wakeham A, Itie A, Lowe SW, Wang X, Mak TW (2002) Generation of Smac/Diablo-deficient mice. Mol Cell Biol 22:3509–3517

    Article  PubMed  CAS  Google Scholar 

  • Palframan SL, Kwok T, Gabriel K (2012) Vacuolating cytotoxin A (VacA), a key toxin for Helicobacter pylori pathogenesis. Front Cell Infect Microbiol 2:92

    Article  PubMed  Google Scholar 

  • Parsonnet J, Friedman GD, Vandersteen DP (1991) Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 325:1127–1131

    Article  PubMed  CAS  Google Scholar 

  • Pathak SK, Basu S, Bhattacharyya A, Pathak S, Banerjee A, Basu J, Kundu M (2006) TLR4-dependent NF-κB activation and mitogen- and stress-activated protein kinase 1-triggered phosphorylation events are central to Helicobacter pylori peptidyl prolyl cis-, trans-isomerase (HP0175)-mediated induction of IL-6 release from macrophages. J Immunol 177:7950–7958

    PubMed  CAS  Google Scholar 

  • Peek RM, Crabtree JE (2006) Helicobacter infection and gastric neoplasia. J Pathol 208:233–248

    Article  PubMed  CAS  Google Scholar 

  • Pereira PJ, Vega MC, Gonzalez-Rey E, Fernandez-Carazo R, Macedo-Ribeiro S, Gomis-Ruth FX, Gonzalez A, Coll M (2002) Trypanosoma cruzi macrophage infectivity potentiator has a rotamase core and a highly exposed α-helix. EMBO Rep 3:88–94

    Article  PubMed  CAS  Google Scholar 

  • Rahfeld JU, Rücknagel KP, Schelbert B, Ludwig B, Hacker J, Mann K, Fischer G (1994) Confirmation of the existence of a third family among peptidyl-prolyl cis/trans isomerases. Amino acid sequence and recombinant production of parvulin (1994). FEBS Lett 352:180–184

    Article  PubMed  CAS  Google Scholar 

  • Rieder G, Merchant JL, Haas R (2005) Helicobacter pylori cag-type IV secretion system facilitates corpus colonization to induce precancerous conditions in Mongolian gerbils. Gastroenterology 128:1229–1242

    Article  PubMed  CAS  Google Scholar 

  • Rudi J, Kuck D, Strand S, von Herbay A, Mariani SM, Krammer PH, Galle PR, Stremmel W (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

    Article  PubMed  CAS  Google Scholar 

  • Rulten S, Thorpe J, Kay J (1999) Identification of eukaryotic parvulin homologues: a new subfamily of peptidylprolyl cis-trans isomerases. Biochem Biophys Res Commun 259:557–562

    Article  PubMed  CAS  Google Scholar 

  • Salvesen GS, Dixit VM (1999) Caspase activation: the induced proximity model. Proc Natl Acad Sci U S A 96:10964–10967

    Article  PubMed  CAS  Google Scholar 

  • Shi Y, Liu XF, Zhuang Y, Zhang JY, Liu T et al (2010) Helicobacter pylori-induced Th17 responses modulate Th1 cell responses, benefit bacterial growth, and contribute to pathology in mice. J Immunol 184:5121–5129

    Article  PubMed  CAS  Google Scholar 

  • Shibayama K, Kamachi K, Nagata N, Yagi T, Nada T, Doi Y, Shibata N, Yokoyama K, Yamane K, Kato H, Iinuma Y, Arakawa Y (2003) A novel apoptosis-inducing protein from Helicobacter pylori. Mol Microbiol 47:443–451

    Article  PubMed  CAS  Google Scholar 

  • Spierings D, McStay G, Saleh M, Bender C, Chipuk J, Maurer U, Green DR (2005) Connected to death: the (unexpurgated) mitochondrial pathway of apoptosis. Science 310:66–67

    Article  PubMed  CAS  Google Scholar 

  • Srinivasula SM, Ahmad M, Fernandez-Alnemri T, Alnemri ES (1998) Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol Cell 1:949–957

    Article  PubMed  CAS  Google Scholar 

  • Stennicke HR, Jürgensmeier JM, Shin H, Deveraux Q, Wolf BB, Yang X, Zhou Q, Ellerby HM, Ellerby LM, Bredesen D, Green DR, Reed JC, Froelich CJ, Salvesen GS (1998) Pro-caspase-3 is a major physiologic target of caspase-8. J Biol Chem 273:27084–27090

    Article  PubMed  CAS  Google Scholar 

  • Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441–446

    Article  PubMed  CAS  Google Scholar 

  • Takahashi N, Hayano T, Suzuki M (1989) Peptidyl-prolyl cis-trans isomerase is the cyclosporine A-binding protein cyclophilin. Nature 337:473–475

    Article  PubMed  CAS  Google Scholar 

  • Thomson S, Clayton AL, Hazzalin CA, Rose S, Barratt MJ, Mahadevan LC (1999) The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase. EMBO J 18:4779–4793

    Article  PubMed  CAS  Google Scholar 

  • Tuccillo C, Cuomo A, Rocco A, Martinelli E, Staibano S, Mascolo M, Gravina AG, Nardone G, Ricci V, Ciardiello F, Del Vecchio Blanco C, Romano M (2005) Vascular endothelial growth factor and neo-angiogenesis in H. pylori gastritis in humans. J Pathol 207:277–284

    Article  PubMed  CAS  Google Scholar 

  • Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, Taniyama K, Sasaki N, Schlemper RJ (2001) Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 345:784–789

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Youle RJ (2009) The role of mitochondria in apoptosis. Annu Rev Genet 43:95–118

    Article  PubMed  CAS  Google Scholar 

  • Wroblewski LE, Peek RM, Wilson KT (2010) Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 23:713–739

    Article  PubMed  CAS  Google Scholar 

  • Xia HH, Talley NJ (2001) Apoptosis in gastric epithelium induced by Helicobacter pylori infection: implications in gastric carcinogenesis. Am J Gastroenterol 96:16–26

    Article  PubMed  CAS  Google Scholar 

  • Zhang JY, Liu T, Guo H, Liu XF, Zhuang Y, Yu S, Chen L, Wu C, Zhao Z, Tang B, Luo P, Mao XH, Guo G, Shi Y, Zou QM (2011) Induction of a Th17 cell response by Helicobacter pylori urease subunit B. J Immunol 216:803–810

    CAS  Google Scholar 

  • Zhong H, May MJ, Jimi E, Ghosh S (2002) The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1. Mol Cell 9:625–636

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Work from the author’s laboratory was supported by grants from the Indian Council of Medical Research and the Department of Atomic Energy, Government of India.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manikuntala Kundu .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Kundu, M. (2013). Helicobacter pylori Peptidyl Prolyl cis, trans Isomerase: A Modulator of the Host Immune Response. In: Henderson, B. (eds) Moonlighting Cell Stress Proteins in Microbial Infections. Heat Shock Proteins, vol 7. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6787-4_5

Download citation

Publish with us

Policies and ethics