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Helicobacter infection and phospholipase A2 enzymes: Effect of Helicobacter felis‐infection on the expression and activity of sPLA2 enzymes in mouse stomach

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Abstract

The murine gastric mucosa possesses very high secretory type phospholipase A2 activity. Northern and Western blots indicated that the pancreatic‐type, sPLA2‐IB represents the predominant form of sPLA2 enzymes present in the gastric mucosa. Both sPLA2‐IB mRNA and protein in the gastric mucosa exceeded levels found in the pancreas, and in contrast to the pancreatic enzyme it was present primarily in the active state. The sPLA2‐IB gene is not expressed in the murine small intestine and colon. Infection by the gastritis-inducing bacteria, Helicobacter felis (H. felis) dramatically and time dependently decreased the PLA2 activity in the glandular stomach of the mouse strain, C57BL/6, sensitive to the organism, which appeared to be related to a decrease in the percentage of sPLA2‐IB present in the active form. This bacterial-induced reduction in PLA2 activity was not observed in BALB/c mice that fail to develop gastritis in response to H. felis infection. C57BL/6 mice do not, while BALB/c mice express, the PLA2‐II enzyme. The H. felis‐induced reduction in sPLA2‐IB activity may weaken the gastric barrier by reducing the local concentration of arachidonic and linoleic acid, liberated from membrane phospholipids, the major precursors of ‘cytoprotective’ prostaglandins. Data presented here suggest that both sPLA2‐IB and sPLA2‐II enzymes may contribute to the gastric response to Helicobacter infection.

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References

  1. Blaser MJ, Parsonnet J: Parasitism by the ‘slow’ bacterium Helicobacter pylori leads to altered gastric homeostasis and neoplasia. J Clin Invest 94: 4–8, 1994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Stadnyk AW: Cytokine production by epithelial cells. FASEB J 8: 1041–1047, 1994

    CAS  PubMed  Google Scholar 

  3. Kagnoff MF, Eckmann L: Epithelial cells as sensors for microbial infection. J Clin Invest 100: 6–10, 1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Spychal RT, Goggin PM, Marrero JM, Saverymuttu SH, Yu CW, Corbishley CM, Maxwell JD, Norfield TC: Surface hydrophobicity of gastric mucosa in peptic ulcer disease. Relationship to gastritis and Campylobacter pylori infection. Gastroenterology 98: 1250–1254, 1990

    Article  CAS  PubMed  Google Scholar 

  5. Lichtenberger LM, Dial EJ, Ottlecz A, Romero JJ, Lechago J, Fox JG: Attenuation of hydrophobic phospholipid barrier is an early event in Helicobacter felis-induced gastritis in mice. Dig Dis Sci 44: 108–115, 1999

    Article  CAS  PubMed  Google Scholar 

  6. Fox JG, Blanco M, Murphy JC, Taylor NS, Lee A, Kabok Z, Pappo J: Local and systemic immune responses in murine Helicobacter felis active chronic gastritis. Infect Immun 61: 2309–2315, 1993

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Lee A, Fox JG, Otto G, Murphy JA: A small animal model of human Helicobacter pylori active chronic gastritis. Gastroenterology 99: 1315–1323, 1990

    Article  CAS  PubMed  Google Scholar 

  8. Dick-Hegedüs E, Lee A: Use of a mouse model to examine anti-Helicobacter pylori agents. Scand J Gastroenterol 26: 909–915, 1991

    Article  PubMed  Google Scholar 

  9. Fox JG, Li X, Cahill RJ, Andrutis K, Rustgi AK, Odze R, Wang TC: Hypertrophic gastropathy in Helicobacter felis-infected wild-type C57BL/6 mice and p53 hemizygous transgenic mice. Gastroenterology 110: 155–166, 1996

    Article  CAS  PubMed  Google Scholar 

  10. Sakagami T, Dixon M, O'Rouke J, Howlett R, Alderuccio F, Vella J, Shimoyama T, Lee A: Atrophic gastric changes in both Helicobacter felis and Helicobacter pylori infected mice are host dependent and separate from antral gastritis. Gut 39: 639–648, 1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Dietrich WF, Lander ES, Smith JS, Moser AR, Gould KA, Luongo C, Borenstein R, Dove W: Genetic identification of Mom-1, a major modifier locus affecting Min-induced intestinal neoplasia in the mouse. Cell 75: 631–639, 1993

    Article  CAS  PubMed  Google Scholar 

  12. MacPhee M, Chepenik KP, Liddell RA, Nelson KK, Siracusa LD, Buchberg AM: The secretory phospholipase A2 gene is a candidate for the Mom1 locus, a major modifier of ApcMin-induced intestinal neoplasia. Cell 81: 957–966, 1995

    Article  CAS  PubMed  Google Scholar 

  13. Kennedy BP, Payette P, Mudgett J, Vadas P, Pruzanski W, Kwan M, Tang C, Rancourt DE, Cromlish WA: A natural disruption of the secretory group II phospholipase A2 gene in inbred mouse strains. J Biol Chem 270: 22378–22385, 1995

    Article  CAS  PubMed  Google Scholar 

  14. Dennis EA: The growing phospholipase A2 superfamily of signal transduction enzymes. TIBS 22: 1–2, 1997

    CAS  PubMed  Google Scholar 

  15. Balsinde J, Balboa MA, Insel PA, Dennis EA: Regulation and inhibition of phospholipase A2. Annu Rev Pharmacol Toxicol 39: 175–189, 1999

    Article  CAS  PubMed  Google Scholar 

  16. Ottlecz A, Romero JJ, Hazell SL, Graham DY, Lichtenberger LM: Phospholipase activity of Helicobacter pylori and its inhibition by bismuth salts. Biochemical and biophysical studies. Digest Dis Sci 38: 2071–2080, 1993

    Article  CAS  PubMed  Google Scholar 

  17. Yang H-C, Mosior M, Johnson CA, Chen Y, Dennis EA: Group-specific assays that distinguish between the four major types of mammalian phospholipase A2. Anal Biochem 269: 278–288, 1999

    Article  CAS  PubMed  Google Scholar 

  18. Tojo H, Ono T, Okamoto M: A pancreatic-type phospholipase A2 in rat gastric mucosa. Biochem Biophys Res Commun 151: 1188–1193, 1988

    Article  CAS  PubMed  Google Scholar 

  19. Sakata T, Nakamura E, Tsuruta Y, Tamaki M, Teraoka H, Tojo H, Ono T, Okamoto M: Presence of pancreatic-type phospholipase A2 mRNA in rat gastric mucosa and lung. Biochim Biophys Acta 1007: 124–126, 1989

    Article  CAS  PubMed  Google Scholar 

  20. Wassef MK, Lin YN, Horowitz MI: Phospholipid-deacylating enzymes of rat stomach mucosa. Biochim Biophys Acta 528: 318–330, 1978

    Article  CAS  PubMed  Google Scholar 

  21. Yasuda T, Hirohara J, Okumara T, Saito K: Purification and characterization of phospholipase A2 from rat stomach. Biochim Biophys Acta 1046: 189–194, 1990

    Article  CAS  PubMed  Google Scholar 

  22. Dimberg J, Gustafson-Svard C, Westrom, B, Tagesson C, Soderkvist P: Group I phospholipase A2 mRNA expression in rat glandular stomach and pancreas. Ontogenic development and effects of cortisone acetate. Biochim Biophys Acta 1130: 47–51, 1992

    Article  CAS  PubMed  Google Scholar 

  23. Nagy L, Johnson BR, Hauschka P, Szabo S: Characterization of proteases and protease inhibitors in the rat stomach. Am J Physiol 272: G1151–G1158, 1997

    CAS  PubMed  Google Scholar 

  24. Wang TC. Goldenring JR, Dangler C, Ito S, Mueller A, Jeon WK, Koh TJ, Fox JG: Mice lacking secretory phospholipase A2 show altered apoptosis and differentiation with Helicobacter felis infection. Gastroenterology 114: 675–689, 1998

    Article  CAS  PubMed  Google Scholar 

  25. Seihamer JJ, Randall TL, Yamanaka M, Johnson LK: Pancreatic phospholipase A2: Isolation of the human gene and cDNAs from porcine pancreas and human lung. DNA 5: 519–527, 1986

    Article  Google Scholar 

  26. Tojo H, Ono T, Kuramitsu S, Okamoto M: A phospholipase A2 in the supernatant fraction of rat spleen. Its similarity to rat pancreatic phospholipase A2. J Biol Chem 263: 5724–5731, 1988

    CAS  PubMed  Google Scholar 

  27. Nomura K, Fujita H, Arita H: Gene expression of pancreatic-type phospholipase-A2 in rat ovaries: Stimulatory action on progesterone release. Endocrinology 135: 603–609, 1994

    CAS  PubMed  Google Scholar 

  28. Tasumi H, Tojo H, Senda T, Ono T, Fujita H, Okamoto M: Histochemistry 94: 135–140, 1990

    Article  CAS  PubMed  Google Scholar 

  29. Yasuda T, Hirohara J, Okumura T, Saiko K: Purification and characterization of phospholipase A2 from rat stomach. Biochim Biophys Acta 1046: 189–194, 1990

    Article  CAS  PubMed  Google Scholar 

  30. Grataroli R, Chabonnier M, Léonardi J, Grimaud J-C, Lafont H, Nalbone G: Phospholipase A2 activity of rat stomach. Arch Biochem Biophys 258: 77–84, 1987

    Article  CAS  PubMed  Google Scholar 

  31. Glaser KB, Mobilio D, Chang JY, Senko N: Phospholipase A2 enzymes: Regulation and inhibition. Trends Pharmacol Sci 14: 92–98, 1993

    Article  CAS  PubMed  Google Scholar 

  32. Mayer RJ, Marshall LA: New insights on mammalian phospholipase A2 (s); comparison of arachidonoyl-selective and-nonselective enzymes. FASEB J 7: 339–348, 1993

    CAS  PubMed  Google Scholar 

  33. Harwig SSL, Tan L, Qu XD, Cho Y, Eisenhauer PB, Lehrer RI: Bactericidal properties of murine intestinal phospholipase A2. J Clin Invest 95: 603–610, 1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Weinrauch Y, Elsbach P, Madsen LM, Foreman A, Weiss J: The potent anti-Staphylococcus aureus activity of a sterile rabbit inflammatory fluid is due to a 14-kD phospholipase A2. J Clin Invest 97: 250–257, 1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Integrative Biology and Pharmacology, The University of Texas Houston Medical School, Houston, TX, 77030, USA

    Anna Ottlecz, Jim J. Romero & Lenard M. Lichtenberger

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  1. Anna Ottlecz
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  2. Jim J. Romero
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  3. Lenard M. Lichtenberger
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Correspondence to Lenard M. Lichtenberger.

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Ottlecz, A., Romero, J.J. & Lichtenberger, L.M. Helicobacter infection and phospholipase A2 enzymes: Effect of Helicobacter felis‐infection on the expression and activity of sPLA2 enzymes in mouse stomach. Mol Cell Biochem 221, 71–77 (2001). https://doi.org/10.1023/A:1010971910866

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