Advertisement

Heat Shock Proteins and Diarrhea Causing Microorganisms: Emergence of Enteroaggregative Escherichia coli

  • Punit Kaur
  • Alexzander AseaEmail author
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 5)

Abstract:

Although a variety of bacterial species cause intestinal and extra-intestinal diseases in humans, the pathogenic Escherichia coli strains account for the majority of infections like typhoid, dysentery and diarrhea. These represent a notable burden particularly for children living in less developed regions of the world and are responsible for an estimated 780–900 million cases of diarrhea worldwide. These infections are benign and self-limiting, although young children are more prone than adults to severe complications from the disease. These diseases are usually acquired by ingesting food or water contaminated with human or animal feces and result in infection caused by bacteria, viruses, parasites, medications and food sensitivities. Enteroaggregative Escherichia coli (EAEC) infection, which generally presents with watery diarrhea and occasionally with blood and mucus is emerging as a particularly lethal pathogen responsible for acute and persistent diarrhea in both developing and developed countries. As pathogenicity becomes better elucidated and antigenic proteins or portions of proteins of the pathogens are identified, immunization becomes a feasible means of preventing diarrheal disease. Recently a great deal interest has been focused on the on 60-kDa (GroEL) and 70-kDa (DnaK) families since they represent major targets of the host’s immune response. This chapter briefly describes current the role of HSP in diarrhea causing microorganisms and the emergence of EAEC as a global threat

Keywords:

Diarrhea bacteria heat shock proteins 

Abbreviations

AA

aggregative adherence

AAF

aggregative adherence fimbriae

AR

acid resistance

ASP

acid stress proteins

ATR

acid tolerance response

DAEC

diffusely adherent Escherichia coli

E. coli

Escherichia coli

EAEC

enteroaggregative Escherichia coli

EHEC

enterohemorrhagic Escherichia coli

EIEC

enteroinvasive Escherichia coli

EPEC

enteropathogenic Escherichia coli

ETEC

enterotoxigenic Escherichia coli

GSH

glutathione

HA

haemaglutination

HIV

human immunodeficiency virus

Hsp

heat shock proteins

hsp

heat shock protein gene

HSP

heat shock protein family

ID

infectious dose

LPS

lipopolysaccharide

MRHA

mannose-resistant haemaglutination

OMP

outer membrane proteins

ORT

oral rehydration therapy

Notes

Acknowledgements

This work was supported in part by the National Institutes of Health grant RO1CA91889, institutional support from Scott & White Memorial Hospital and Clinic, Texas A&M University System Health Science Center College of Medicine, the Central Texas Veterans Health Administration and an Endowment from the Cain Foundation (to A. A).

References

  1. Abshire, K. Z. and Neidhardt, F. C. (1993) Analysis of proteins synthesized by Salmonella typhimurium during growth within a host macrophage. J Bacteriol 175, 3734–43.PubMedGoogle Scholar
  2. Adachi, J. A., Ericsson, C. D., Jiang, Z. D., DuPont, M. W., Pallegar, S. R. and DuPont, H. L. (2002) Natural history of enteroaggregative and enterotoxigenic Escherichia coli infection among US travelers to Guadalajara, Mexico. J Infect Dis 185, 1681–3.CrossRefPubMedGoogle Scholar
  3. Adachi, J. A., Jiang, Z. D., Mathewson, J. J., Verenkar, M. P., Thompson, S., Martinez-Sandoval, F., Steffen, R., Ericsson, C. D. and DuPont, H. L. (2001) Enteroaggregative Escherichia coli as a major etiologic agent in traveler’s diarrhea in 3 regions of the world. Clin Infect Dis 32, 1706–9.CrossRefPubMedGoogle Scholar
  4. Arnold, K. W. and Kaspar, C. W. (1995) Starvation- and stationary-phase-induced acid tolerance in Escherichia coli O157:H7. Appl Environ Microbiol 61, 2037–9.PubMedGoogle Scholar
  5. Bern, C., Martines, J., de Zoysa, I. and Glass, R. I. (1992) The magnitude of the global problem of diarrhoeal disease: a ten-year update. Bull World Health Organ 70, 705–14.PubMedGoogle Scholar
  6. Bey, R. F., Larson, M. E., Lowery, D. E., Lee, B. W., Knutson, K. S., Simonson, R. R. and King, V. L. (1995) Protection of C3H/He mice from experimental Borrelia burgdorferi infection by immunization with a 110-kilodalton fusion protein. Infect Immun 63, 3213–17.PubMedGoogle Scholar
  7. Bhan, M. K., Arora, N. K., Ghai, O. P., Ramachandran, K., Khoshoo, V. and Bhandari, N. (1986) Major factors in diarrhoea related mortality among rural children. Indian J Med Res 83, 9–12.PubMedGoogle Scholar
  8. Bhardwaj, R., Majumdar, S., Ganguly, N. K., Taneja, N., Dutta, S., Ramamurthy, T. and Chakraborti, A. (2006) Characterization of adhesin variants in Indian isolates of enteroaggregative Escherichia coli. FEMS Microbiol Lett 258, 274–83.CrossRefPubMedGoogle Scholar
  9. Booth, I. R. (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49, 359–78.PubMedGoogle Scholar
  10. Brandl, M. T. (2006) Fitness of human enteric pathogens on plants and implications for food safety. Annu Rev Phytopathol 44, 367–92.CrossRefPubMedGoogle Scholar
  11. Chiu, C. H., Su, L. H. and Chu, C. (2004) Salmonella enterica serotype Choleraesuis: epidemiology, pathogenesis, clinical disease, and treatment. Clin Microbiol Rev 17, 311–22.CrossRefPubMedGoogle Scholar
  12. Danilition, S. L., Maclean, I. W., Peeling, R., Winston, S. and Brunham, R. C. (1990) The 75-kilodalton protein of Chlamydia trachomatis: a member of the heat shock protein 70 family? Infect Immun 58, 189–96.PubMedGoogle Scholar
  13. Dunn, B. E., Blaser, M. J. and Snyder, E. L. (1987) Two-dimensional gel electrophoresis and immunoblotting of Campylobacter outer membrane proteins. Infect Immun 55, 1564–72.PubMedGoogle Scholar
  14. Durrer, P., Zbinden, R., Fleisch, F., Altwegg, M., Ledergerber, B., Karch, H. and Weber, R. (2000) Intestinal infection due to enteroaggregative Escherichia coli among human immunodeficiency virus-infected persons. J Infect Dis 182, 1540–4.CrossRefPubMedGoogle Scholar
  15. Emanuelsson, O. and von Heijne, G. (2001) Prediction of organellar targeting signals. Biochim Biophys Acta 1541, 114–9.CrossRefPubMedGoogle Scholar
  16. Gomez, H. F., Mathewson, J. J., Johnson, P. C. and DuPont, H. L. (1995) Intestinal immune response of volunteers ingesting a strain of enteroadherent (HEp-2 cell-adherent) Escherichia coli. Clin Diagn Lab Immunol 2, 10–3.PubMedGoogle Scholar
  17. Gorden, J. and Small, P. L. (1993) Acid resistance in enteric bacteria. Infect Immun 61, 364–7.PubMedGoogle Scholar
  18. Griffiths, P. L., Park, R. W. and Connerton, I. F. (1995) The gene for Campylobacter trigger factor: evidence for multiple transcription start sites and protein products. Microbiology 141 (Pt 6), 1359–67.CrossRefPubMedGoogle Scholar
  19. Hager, K. M., Striepen, B., Tilney, L. G. and Roos, D. S. (1999) The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J Cell Sci 112 (Pt 16), 2631–8.PubMedGoogle Scholar
  20. Henderson, I. R., Czeczulin, J., Eslava, C., Noriega, F. and Nataro, J. P. (1999a) Characterization of pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect Immun 67, 5587–96.PubMedGoogle Scholar
  21. Henderson, I. R., Hicks, S., Navarro-Garcia, F., Elias, W. P., Philips, A. D. and Nataro, J. P. (1999b) Involvement of the enteroaggregative Escherichia coli plasmid-encoded toxin in causing human intestinal damage. Infect Immun 67, 5338–44.PubMedGoogle Scholar
  22. Heyde, M. and Portalier, R. (1987) Regulation of major outer membrane porin proteins of Escherichia coli K 12 by pH. Mol Gen Genet 208, 511–7.CrossRefPubMedGoogle Scholar
  23. Hickey, E. W. and Hirshfield, I. N. (1990) Low-pH-induced effects on patterns of protein synthesis and on internal pH in Escherichia coli and Salmonella typhimurium. Appl Environ Microbiol 56, 1038–45.PubMedGoogle Scholar
  24. Huang, D. B. and Dupont, H. L. (2004) Enteroaggregative Escherichia coli: an emerging pathogen in children. Semin Pediatr Infect Dis 15, 266–71.CrossRefPubMedGoogle Scholar
  25. Itoh, Y., Nagano, I., Kunishima, M. and Ezaki, T. (1997) Laboratory investigation of enteroaggregative Escherichia coli O untypeable:H10 associated with a massive outbreak of gastrointestinal illness. J Clin Microbiol 35, 2546–50.PubMedGoogle Scholar
  26. Jordan, K. N., Oxford, L. and O’Byrne, C. P. (1999) Survival of low-pH stress by Escherichia coli O157:H7: correlation between alterations in the cell envelope and increased acid tolerance. Appl Environ Microbiol 65, 3048–55.PubMedGoogle Scholar
  27. Kahali, S., Sarkar, B., Chakraborty, S., Macaden, R., Deokule, J. S., Ballal, M., Nandy, R. K., Bhattacharya, S. K., Takeda, Y. and Ramamurthy, T. (2004a) Molecular epidemiology of diarrhoeagenic Escherichia coli associated with sporadic cases and outbreaks of diarrhoea between 2000 and 2001 in India. Eur J Epidemiol 19, 473–9.CrossRefPubMedGoogle Scholar
  28. Kahali, S., Sarkar, B., Rajendran, K., Khanam, J., Yamasaki, S., Nandy, R. K., Bhattacharya, S. K. and Ramamurthy, T. (2004b) Virulence characteristics and molecular epidemiology of enteroaggregative Escherichia coli isolates from hospitalized diarrheal patients in Kolkata, India. J Clin Microbiol 42, 4111–20.CrossRefPubMedGoogle Scholar
  29. Katoh, T., Ohmori, H., Murakami, T., Karasaki, Y., Higashi, K. and Muramatsu, M. (1991) Induction of glutathione-S-transferase and heat-shock proteins in rat liver after ethylene oxide exposure. Biochem Pharmacol 42, 1247–54.CrossRefPubMedGoogle Scholar
  30. Kaufmann, S. H. E. and Schoel, B. (1994) Heat shock proteins as antigens in immunity against infection and self. In The biology of heat shock proteins and molecular chaperones, Morimoto, R. I., Tissieres, A. and Georgopoulos, C. eds, pp. 495–531. Cold Spring Harbor Laboratory Press, Plainview, NY.Google Scholar
  31. Kaur, P. (2007) Molecular study of acid-induced proteins in a diarrheagenic enteroaggregative Escherichia coli. Ph.D. thesis, Department of Experimental Medicine and Biotechnology, Postgraduate Institute of Medical Education and Research, Chandrigarh, India. p. 150.Google Scholar
  32. Kaur, P. and Chakraborti, A. (2009) Acid stress augments expression of 41 and 48 kDa outer membrane proteins of diarreheagenic enteroaggative Escherichia coli (manuscript in preparation).Google Scholar
  33. Kiang, J. G. and Tsokos, G. C. (1998) Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol Ther 80, 183–201.CrossRefPubMedGoogle Scholar
  34. Knutton, S., Shaw, R., Phillips, A. D., Smith, H. R., Willshaw, G. A., Watson, P. and Price, E. (2001) Phenotypic and genetic analysis of diarrhea-associated Escherichia coli isolated from children in the United Kingdom. J Pediatr Gastroenterol Nutr 33, 32–40.CrossRefPubMedGoogle Scholar
  35. LaGier, M. J., Tachezy, J., Stejskal, F., Kutisova, K. and Keithly, J. S. (2003) Mitochondrial-type iron-sulfur cluster biosynthesis genes (IscS and IscU) in the apicomplexan Cryptosporidium parvum. Microbiology 149, 3519–30.CrossRefPubMedGoogle Scholar
  36. Lanata, C. F., Black, R. E., Gilman, R. H., Lazo, F. and Del Aguila, R. (1991) Epidemiologic, clinical, and laboratory characteristics of acute vs. persistent diarrhea in periurban Lima, Peru. J Pediatr Gastroenterol Nutr 12, 82–8.CrossRefPubMedGoogle Scholar
  37. Lee, I. S., Lin, J., Hall, H. K., Bearson, B. and Foster, J. W. (1995) The stationary-phase sigma factor sigma S (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium. Mol Microbiol 17, 155–67.CrossRefPubMedGoogle Scholar
  38. Lee, I. S., Slonczewski, J. L. and Foster, J. W. (1994) A low-pH-inducible, stationary-phase acid tolerance response in Salmonella typhimurium. J Bacteriol 176, 1422–6.PubMedGoogle Scholar
  39. Lin, J. and Ficht, T. A. (1995) Protein synthesis in Brucella abortus induced during macrophage infection. Infect Immun 63, 1409–14.PubMedGoogle Scholar
  40. Lin, J., Lee, I. S., Frey, J., Slonczewski, J. L. and Foster, J. W. (1995) Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J Bacteriol 177, 4097–104.PubMedGoogle Scholar
  41. Lin, J., Smith, M. P., Chapin, K. C., Baik, H. S., Bennett, G. N. and Foster, J. W. (1996) Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl Environ Microbiol 62, 3094–100.PubMedGoogle Scholar
  42. Lindquist, S. and Craig, E. A. (1988) The heat-shock proteins. Annu Rev Genet 22, 631–77.CrossRefPubMedGoogle Scholar
  43. Mahmoud, K. Z. and Edens, F. W. (2003) Influence of selenium sources on age-related and mild heat stress-related changes of blood and liver glutathione redox cycle in broiler chickens (Gallus domesticus). Comp Biochem Physiol B Biochem Mol Biol 136, 921–34.CrossRefPubMedGoogle Scholar
  44. Mayer, H. B. and Wanke, C. A. (1995) Enteroaggregative Escherichia coli as a possible cause of diarrhea in an HIV-infected patient. N Engl J Med 332, 273–4.CrossRefPubMedGoogle Scholar
  45. Miller, V. L., Taylor, R. K. and Mekalanos, J. J. (1987) Cholera toxin transcriptional activator toxR is a transmembrane DNA binding protein. Cell 48, 271–9.CrossRefPubMedGoogle Scholar
  46. Mitchell, J. B., Russo, A., Kinsella, T. J. and Glatstein, E. (1983) Glutathione elevation during thermotolerance induction and thermosensitization by glutathione depletion. Cancer Res 43, 987–91.PubMedGoogle Scholar
  47. Mobley, H. L. (1997) Helicobacter pylori factors associated with disease development. Gastroenterology 113, S21–8.PubMedGoogle Scholar
  48. Nataro, J. P. and Kaper, J. B. (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11, 142–201.PubMedGoogle Scholar
  49. Nishimura, H., Emoto, M., Kimura, K. and Yoshikai, Y. (1997) Hsp70 protects macrophages infected with Salmonella choleraesuis against TNF-alpha-induced cell death. Cell Stress Chaperones 2, 50–9.CrossRefPubMedGoogle Scholar
  50. O’Hagan, D. T. (1998) Recent advances in immunological adjuvants: the development of particulate antigen delivery systems. Expert Opin Investig Drugs 7, 349–59.CrossRefPubMedGoogle Scholar
  51. Pabst, W. L., Altwegg, M., Kind, C., Mirjanic, S., Hardegger, D. and Nadal, D. (2003) Prevalence of enteroaggregative Escherichia coli among children with and without diarrhea in Switzerland. J Clin Microbiol 41, 2289–93.CrossRefPubMedGoogle Scholar
  52. Pai, M., Kang, G., Ramakrishna, B. S., Venkataraman, A. and Muliyil, J. (1997) An epidemic of diarrhoea in south India caused by enteroaggregative Escherichia coli. Indian J Med Res 106, 7–12.PubMedGoogle Scholar
  53. Palade, G. (1975) Intracellular aspects of the process of protein synthesis. Science 189, 867.CrossRefPubMedGoogle Scholar
  54. Palmer, H. J. and Paulson, K. E. (1997) Reactive oxygen species and antioxidants in signal transduction and gene expression. Nutr Rev 55, 353–61.CrossRefPubMedGoogle Scholar
  55. Pei, Z. and Blaser, M. J. (1993) PEB1, the major cell-binding factor of Campylobacter jejuni, is a homolog of the binding component in gram-negative nutrient transport systems. J Biol Chem 268, 18717–25.PubMedGoogle Scholar
  56. Phan-Thanh, L. and Gormon, T. (1997) Stress proteins in Listeria monocytogenes. Electrophoresis 18, 1464–71.CrossRefPubMedGoogle Scholar
  57. Polla, B. S., Bachelet, M., Elia, G. and Santoro, M. G. (1998) Stress proteins in inflammation. Ann N Y Acad Sci 851, 75–85.CrossRefPubMedGoogle Scholar
  58. Presterl, E., Nadrchal, R., Wolf, D., Rotter, M. and Hirschl, A. M. (1999) Enteroaggregative and enterotoxigenic Escherichia coli among isolates from patients with diarrhea in Austria. Eur J Clin Microbiol Infect Dis 18, 209–12.CrossRefPubMedGoogle Scholar
  59. Prinz, T., Pfanner, N. and Truscott, K. N. (2002) Translocation of proteins into mitochondria. In Protein targeting, transport and translocation, Dalbey, R. E. and von Heijne, G. eds, pp. 214–239. Academic Press, Amsterdam, The Netherlands.CrossRefGoogle Scholar
  60. Qoronfleh, M. W., Bortner, C. A., Schwartzberg, P. and Wilkinson, B. J. (1998) Enhanced levels of Staphylococcus aureus stress protein GroEL and DnaK homologs early in infection of human epithelial cells. Infect Immun 66, 3024–7.PubMedGoogle Scholar
  61. Salmond, C. V., Kroll, R. G. and Booth, I. R. (1984) The effect of food preservatives on pH homeostasis in Escherichia coli. J Gen Microbiol 130, 2845–50.PubMedGoogle Scholar
  62. Samali, A. and Orrenius, S. (1998) Heat shock proteins: regulators of stress response and apoptosis. Cell Stress Chaperones 3, 228–36.CrossRefPubMedGoogle Scholar
  63. Sarantuya, J., Nishi, J., Wakimoto, N., Erdene, S., Nataro, J. P., Sheikh, J., Iwashita, M., Manago, K., Tokuda, K., Yoshinaga, M., Miyata, K. and Kawano, Y. (2004) Typical enteroaggregative Escherichia coli is the most prevalent pathotype among E. coli strains causing diarrhea in Mongolian children. J Clin Microbiol 42, 133–9.CrossRefPubMedGoogle Scholar
  64. Scotland, S. M., Willshaw, G. A., Cheasty, T., Rowe, B. and Hassall, J. E. (1994) Association of enteroaggregative Escherichia coli with travellers’ diarrhoea. J Infect 29, 115–6.CrossRefPubMedGoogle Scholar
  65. Sheikh, J., Czeczulin, J. R., Harrington, S., Hicks, S., Henderson, I. R., Le Bouguenec, C., Gounon, P., Phillips, A. and Nataro, J. P. (2002) A novel dispersin protein in enteroaggregative Escherichia coli. J Clin Invest 110, 1329–37.PubMedGoogle Scholar
  66. Sheikh, J., Hicks, S., Dall’Agnol, M., Phillips, A. D. and Nataro, J. P. (2001) Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol Microbiol 41, 983–97.CrossRefPubMedGoogle Scholar
  67. Skirrow, M. S. and Blaser, M. J. (1992) Clinical and epidemiological considerations. In Campylobacter jejuni: current status and future trends, Nachamkin, I., Blaser, M. J. and Tompkins, L. S. eds, pp. 3–8. American Society for Microbiology, Washington, DC.Google Scholar
  68. Smith, H. R., Cheasty, T. and Rowe, B. (1997) Enteroaggregative Escherichia coli and outbreaks of gastroenteritis in UK. Lancet 350, 814–5.CrossRefPubMedGoogle Scholar
  69. Smith, H. R., Scotland, S. M., Willshaw, G. A., Rowe, B., Cravioto, A. and Eslava, C. (1994) Isolates of Escherichia coli O44:H18 of diverse origin are enteroaggregative. J Infect Dis 170, 1610–3.PubMedGoogle Scholar
  70. Svennerholm, A. M. and Tobias, J. (2008) Vaccines against enterotoxigenic Escherichia coli. Expert Rev Vaccines 7, 795–804.CrossRefPubMedGoogle Scholar
  71. Triantafilou, M. and Triantafilou, K. (2002) Lipopolysaccharide recognition: CD14, TLRs and the LPS-activation cluster. Trends Immunol 23, 301–4.CrossRefPubMedGoogle Scholar
  72. Tzipori, S., Montanaro, J., Robins-Browne, R. M., Vial, P., Gibson, R. and Levine, M. M. (1992) Studies with enteroaggregative Escherichia coli in the gnotobiotic piglet gastroenteritis model. Infect Immun 60, 5302–6.PubMedGoogle Scholar
  73. Vila, J., Vargas, M., Henderson, I. R., Gascon, J. and Nataro, J. P. (2000) Enteroaggregative Escherichia coli virulence factors in traveler’s diarrhea strains. J Infect Dis 182, 1780–3.CrossRefPubMedGoogle Scholar
  74. Villaseca, J. M., Navarro-Garcia, F., Mendoza-Hernandez, G., Nataro, J. P., Cravioto, A. and Eslava, C. (2000) Pet toxin from enteroaggregative Escherichia coli produces cellular damage associated with fodrin disruption. Infect Immun 68, 5920–7.CrossRefPubMedGoogle Scholar
  75. Wai, S. N., Takade, A. and Amako, K. (1996) The hydrophobic surface protein layer of enteroaggregative Escherichia coli strains. FEMS Microbiol Lett 135, 17–22.CrossRefPubMedGoogle Scholar
  76. Walker, S. L., Sojka, M., Dibb-Fuller, M. and Woodward, M. J. (1999) Effect of pH, temperature and surface contact on the elaboration of fimbriae and flagella by Salmonella serotype Enteritidis. J Med Microbiol 48, 253–61.CrossRefPubMedGoogle Scholar
  77. Wallace-Gadsden, F. (2007) Enteroaggregative Escherichia coli related to uropathogenic clonal group A. Emerg Infect Dis 13, 757–60.PubMedGoogle Scholar
  78. Wang, S. and Edens, F. W. (1998) Heat conditioning induces heat shock proteins in broiler chickens and turkey poults. Poult Sci 77, 1636–45.PubMedGoogle Scholar
  79. Wizemann, T. M., Adamou, J. E. and Langermann, S. (1999) Adhesins as targets for vaccine development. Emerg Infect Dis 5, 395–403.CrossRefPubMedGoogle Scholar
  80. Wu, Y. L., Lee, L. H., Rollins, D. M. and Ching, W. M. (1994) Heat shock- and alkaline pH-induced proteins of Campylobacter jejuni: characterization and immunological properties. Infect Immun 62, 4256–60.PubMedGoogle Scholar
  81. Yamamoto, T., Wakisaka, N. and Nakae, T. (1997) A novel cryohemagglutinin associated with adherence of enteroaggregative Escherichia coli. Infect Immun 65, 3478–84.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Division of Investigative PathologyThe Texas A&M Health Science Center College of Medicine, Scott & White Memorial Hospital and ClinicTempleUSA
  2. 2.Division of Investigative PathologyThe Texas A&M Health Science Center College of Medicine, Scott & White Memorial Hospital and ClinicTempleUSA

Personalised recommendations