Correlation of heat shock protein expression to gender difference in development of stress-induced gastric mucosal injury in rats

Journal of Clinical Biochemistry and Nutrition

Volumn 47, Issue 1, 2010, Pages 64-73

  Takahashi, Taiji ^a   Otaka, Michiro ^a   Odashima, Masaru ^c   Tamaki, Kumiko ^a   Takada, Makiko ^a   Izumi, Yuko ^a   Shibuya, Tomoyoshi ^a   Sakamoto, Naoto ^a   Itoh, Hideaki ^b   Watanabe, Sumio ^a  

^a JUNTENDO UNIVERSITY   (Japan)

^b AKITA UNIVERSITY   (Japan)

^c Yokote Municipal Hospital   (Japan)

Author keywords

Estrogen; Gastric mucosal protection; Gender difference; Heat shock protein; Stress

Indexed keywords

ESTROGEN; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EXERCISE TEST; FEMALE; MALE; NONHUMAN; OVARIECTOMY; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; STOMACH INJURY; STOMACH MUCOSA; STOMACH PROTECTION; STRESS ULCER; WATER IMMERSION;

RATTUS;

EID: 77955598674     PISSN: 09120009     EISSN: None     Source Type: Journal    
DOI: 10.3164/jcbn.10-32     Document Type: Article

References (42)

1. Clark, D.H.: Peptic ulcer in women. Br. Med. J., 1, 1254-1257, 1953.
2. Sawrey, W.L. and Long, D.H.: Strain and sex differences in ulceration in the rat. J. Comp. Physiol. Psychol., 55, 603-605, 1962.
3. de Martel, C. and Personnet, J.: Helicobacter pylori infection and gender: a meta analysis of population-based prevalence surveys. Dig. Dis. Sci., 51, 2292-2301, 2006.
4. Kher, A., Wang, M., Tsai, B.M., Pitcher, J.M., Greenbaum, E.S., Nagy, R.D., Patel, K.M., Wairiuko, G.M., Markel, T.A., and Meldrum, D.R.: Sex differences in the myocardial inflammatory response to acute injury. Shock, 23, 1-10, 2005. (Pubitemid 40083021)
5. Feng, W., Cui, Y., Song, C., Zhan, H., Wang, X., Li, Q., Cui, W., Guo, K., Maki, M., Hisha, H., Mori, T., and Ikehara, S.: Prevention of osteoporosis and hypogonadism by allogeneic ovarian transplantation in conjunction with intra-bone marrow-bone marrow transplantation. Transplantation, 84, 1459-1466, 2007.
6. Kuiper, G.G., Shughrue, P.J., Merchenthaler, I., and Gustafsson, J.A.: The estrogen receptor beta subtype: a novel mediator of estrogen action in neuroendocrine systems. Front. Neuroendocrinol., 19, 253-286, 1998.
7. Shimozawa, N., Okajima, K., Harada, N., Arai, M., Ishida, Y., Shimada, S., Kurihara, H., and Nakagata, N.: Contribution of sensory neurons to sex difference in the development of stress-induced gastric mucosal injury in mice. Gastroenterology, 131, 1826-1834, 2006.
8. Machowska, A., Szlachcic, A., Pawlik, M., Brzozowski, T., Konturek, S.J., and Pawlik, W.W.: The role of female and male sex hormones in the healing process of preexisting lingual and gastric ulcerations. J. Physiol. Pharmacol., 55, 91-104, 2004.
9. Hightower, L.E.: Heat shock, stress proteins, chaperones, and proteotoxicity. Cell, 66, 191-197, 1991.
10. Otaka, M., Odashima, M., and Watanabe, S.: Role of heat shock proteins (molecular chaperones) in intestinal mucosal protection. Biochem. Biophys. Res. Commun., 348, 1-5, 2006.
11. Takagi, K. and Okabe, S.: The effects of drugs on the production and recovery processes of the stress ulcer. Jpn. J. Pharmacol., 18, 9-18, 1968.
12. Ohta, Y., Kaida, S., Chiba, S., Tada, M., Teruya, A., Imai, Y., and Kawanishi, M.: Involvement of oxidative stress in increases in the serum levels of various enzymes and components in rats with water-immersion restraint stress. J. Clin. Biochem. Nutr., 45, 347-354, 2009.
13. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685, 1970.
14. Otaka, M., Itoh, H., Kuwabara, T., Zeniya, A., Fujimori, S., Otani, S., Tashima, Y., and Masamune, O.: Induction of heat shock protein and prevention of caerulein-induced pancreatitis by water-immersion stress in rats. Int. J. Biochem., 26, 805-811, 1994.
15. Towbin, H., Staehelin, T., and Gordon, J.: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A., 76, 4350-4354, 1979.
16. Otaka, M., Itoh, H., Kuwabara, T., Zeniya, A., Fujimori, S., Tashima, Y., and Masamune, O.: Induction of a 60-kDa heat shock protein in rat pancreas by water-immersion stress. Int. J. Biochem., 25, 1769-1773, 1993.
17. Wakui, H., Itoh, H., Tashima, Y., Kobayashi, R., Nakamoto, Y., and Miura, A.B.: Specific antibodies against the stress-inducible 72-kDa protein, a member of the heat-shock protein hsp70, in healthy human subjects. Int. J. Biochem., 23, 975-978, 1991.
18. Itoh, H., Toyoshima, I., Mizunuma, H., Kobayashi, R., and Tashima, Y.: Three-step purification method and characterization of the bovine brain 90-kDa heat shock protein. Arch. Biochem. Biophys., 282, 290-296, 1990.
19. Otani, S., Otaka, M., Jin, M., Okuyama, A., Itoh, S., Iwabuchi, A., Sasahara, H., Itoh, H., Tashima, Y., and Masamune, O.: Effect of preinduction of heat shock proteins on acetic acid-induced colitis in rats. Dig. Dis. Sci., 42, 833-846, 1997.
20. Smith, A., Contreras, C., Ko, K.H., Chow, J., Dong, X., Tuo, B., Zhang, H.H., Chen, D.B., and Dong, H.: Gender-specific protection of estrogen against gastric acid-induced duodenal injury: stimulation of duodenal mucosal bicarbonate secretion. Endocrinology, 149, 4554-4566, 2008.
21. Izumi, Y., Otaka, M., Takahashi, T., Takada, M., Shimada, Y., Asaoka, D., Nagahara, A., Itoh, H., and Watanabe, S.: Specific induction of a 72-kDa heat shock protein protects esophageal mucosa from reflux esophagitis. Life Sci., 84, 517-522, 2009.
22. Zatloukal, K., Sohar, R., Lackinger, E., and Denk, H.: Induction of heat shock proteins in short-term cultured hepatocytes derived from normal and chronically griseofulvin-treated mice. Hepatology, 8, 607-612, 1988.
23. Emami, A., Schwartz, J.H., and Borkan, S.C.: Transient ischemia or heat stress induced a cytoprotectant protein in rat kidney. Am. J. Physiol., 260, F479-F485, 1991.
24. Li, G.C., Li, L., Liu, R.Y., Rehman, M., and Lee, W.M.: Heat shock protein hsp70 protects cells from thermal stress even after deletion of its APT-binding domain. Proc. Natl. Acad. Sci. U.S.A., 89, 2036-2040, 1992.
25. Higashi, T., Takechi, H., Uemura, Y., Kikuchi, H., and Nagata, K.: Differential induction of mRNA species encoding several classes of stress proteins following focal cerebral ischemia in rats. Brain Res., 650, 239-248, 1994.
26. Li, G.C., Meyer, J.L., Mak, J.Y., and Hahn, G.M.: Heat-induced protection of mice against thermal death. Cancer Res., 43, 5758-5760, 1983.
27. Nakamura, K., Rokutan, K., Marui, N., Aoike, A., and Kawai, K.: Induction of heat shock proteins and their implication in protection against ethanol-induced damage in cultured guinea pig gastric mucosal cells. Gastroenterology, 101, 161-166, 1991.
28. Wada, I., Otaka, M., Jin, M., Odashima, M., Komatsu, K., Konishi, N., Matsuhashi, T., Horikawa, Y., Ohba, R., Itoh, H., and Watanabe, S.: Expression of HSP72 in the gastric mucosa is regulated by gastric acid in rats-correlation of HSP72 expression with mucosal protection. Biochem. Biophys. Res. Commun., 349, 611-618, 2006.
29. Odashima, M., Otaka, M., Jin, M., Wada, I., Horikawa, Y., Matsuhashi, T., Ohba, R., Hatakeyama, N., Oyake, J., and Watanabe, S.: Zinc L-carnosine protects colonic mucosal injury through induction of heat shock protein 72 and suppression of NF-kappa B activation. Life Sci., 79, 2245-2250, 2006. (Pubitemid 44666062)
30. Hirata, I., Naito, Y., Handa, O., Hayashi, N., Mizushima, K., Adachi, S., Omatsu, T., Okayama, T., Kishimoto, E., Ichikawa, H., Takagi, T., Kokura, S., Otaka, M., and Yoshikawa, T.: Heat-shock protein 70-overexpressing gastric epithelial cells are resistant to indomethacin-induced apoptosis. Digestion, 79, 243-250, 2009.
31. Odashima, M., Otaka, M., Jin, M., Konishi, N., Sato, T., Kato, S., Matsuhashi, T., Nakamura, C., and Watanabe, S.: Induction of a 72-kDa heat-shock protein in cultured rat gastric mucosal cells and rat gastric mucosa by zinc L-carnosine. Dig. Dis. Sci., 47, 2799-2804, 2002.
32. Oh, T.Y., Ahn, B.O., Jang, E.J., Park, J.S., Park, S.J., Baik, H.W., and Hahm, K.-B.: Accelerated ulcer healing and resistance to ulcer recurrence with gastroprotectants in rat model of Acetic Acid-induced Gastric Ulcer. J. Clin. Biochem. Nutr., 42, 204-214, 2008.
33. Olazábal, U.E., Pfaff, D.W., and Mobbs, C.V.: Estrogenic regulation of heat shock protein 90 kDa in rat ventromedial hypothalamus and uterus. Mol. Cell. Endocrinol., 84, 175-183, 1992.
34. Paroo, Z., Dipchand, E.S., and Noble, E.G.: Estrogen attenuates postexercise HSP70 expression in skeletal muscle. Am. J. Physiol. Cell Physiol., 282, C245-C251, 2002.
35. Shinohara, T., Takahashi, N., Ooie, T., Ichinose, M., Hara, M., Yonemochi, H., Saikawa, T., and Yoshimatsu, H.: Estrogen inhibits hyperthermia-induced expression of heat-shock protein 72 and cardioprotection against ischemia/reperfusion injury in female rat heart. J. Mol. Cell Cardiol., 37, 1053-1061, 2004.
36. Suuronen, T., Ojala, J., Hyttinen, J.M., Kaarniranta, K., Thornell, A., Kyrylenko, S., and Salminen, A.: Regulation of ER alpha signaling pathway in neuronal HN10 cells: role of protein acetylation and Hsp90. Neurochem. Res., 33, 1768-1775, 2008.
37. Otaka, M., Okuyama, A., Otani, S., Jin, M., Itoh, S., Itoh, H., Iwabuchi, A., Sasahara, H., Odashima, M., Tashima, Y., and Masamune, O.: Differential induction of HSP60 and HSP72 by different stress situations in rats. Correlation with cerulein-induced pancreatitis. Dig. Dis. Sci., 42, 1473-1479, 1997.
38. Fujimori, S., Otaka, M., Itoh, H., Kuwabara, T., Zeniya, A., Otani, S., Tashima, Y., and Masamune, O.: Induction of a 60-kDa heat shock protein in rat gastric mucosa by restraint and water-immersion stress. J. Gastroenterol., 29, 544-546, 1994. (Pubitemid 24262728)
39. Picard, D., Khursheed, B., Garabedian, M.J., Fortin, M.G., Lindquist, S., and Yamamoto, K.R.: Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature, 348, 166-168, 1990.
40. Bharadwaj, S., Ali, A., and Ovsenek, N.: Multiple components of the HSP90 chaperone complex function in regulation of heat shock factor 1 in vivo. Mol. Cell. Biol., 19, 8033-8041, 1999.
41. Li, W., Li, Y., Guan, S., Fan, J., Cheng, C.F., Bright, A.M., Chinn, C., Chen, M., and Woodley, D.T.: Extracellular heat shock protein-90alpha: linking hypoxia to skin cell motility and wound healing. EMBO J., 26, 1221-1233, 2007.
42. Ramachandran, C., Catelli, M.G., Schneider, W., and Shyamala, G.: Estrogenic regulation of uterine 90-kilodalton heat shock protein. Endocrinology, 123, 956-961, 1988.