Mechanism of estrogen-mediated attenuation of hepatic injury following trauma-hemorrhage: Akt-dependent HO-1 up-regulation

Journal of Leukocyte Biology

Volumn 82, Issue 4, 2007, Pages 1019-1026

  Hsu, Jun Te ^a,b   Kan, Wen Hong ^a   Hsieh, Chi Hsun ^a,c   Choudhry, Mashkoor A ^a   Schwacha, Martin G ^a   Bland, Kirby I ^a   Chaudry, Irshad H ^a,d  

^a Kentucky   (United States)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

CINC 1; MIP 2; MPO; Protein kinase B

Indexed keywords

CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; ESTROGEN; ESTROGEN RECEPTOR; FULVESTRANT; GLUTATHIONE TRANSFERASE ALPHA; HEME OXYGENASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; MYELOPEROXIDASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; TUMOR NECROSIS FACTOR ALPHA; WORTMANNIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FLUID RESUSCITATION; INFLAMMATION; LIVER HEMORRHAGE; LIVER INJURY; MALE; MEAN ARTERIAL PRESSURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANDROSTADIENES; ANIMALS; BLOOD PRESSURE; CHEMOKINE CXCL1; CHEMOKINE CXCL2; ESTRADIOL; ESTROGEN ANTAGONISTS; ESTROGENS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTATHIONE TRANSFERASE; HEME OXYGENASE-1; HEMORRHAGE; INTERCELLULAR ADHESION MOLECULE-1; INTERLEUKIN-6; LIVER; MALE; PEROXIDASE; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ESTROGEN; RESUSCITATION; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; WOUNDS AND INJURIES;

RATTUS;

EID: 34848856657     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0607355     Document Type: Article

References (49)

1. Yokoyama, Y., Toth, B., Kitchens, W. C., Schwacha, M. G., Bland, K. I., Chaudry, I. H. (2003) Role of thromboxane in producing portal hypertension following trauma-hemorrhage. Am. J. Physiol. Gastrointest. Liver Physiol. 285, G1293-G1299.
2. Meng, X., Ao, L., Song, Y., Raeburn, C. D., Fullerton, D. A., Harken, A. H. (2005) Signaling for myocardial depression in hemorrhagic shock: roles of Toll-like receptor 4 and p55 TNF-α receptor. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R600-R606.
3. Shen, X. D., Ke, B., Zhai, Y., Gao, F., Busuttil, R. W., Cheng, G., Kupiec-Weglinski, J. W. (2005) Toll-like receptor and heme oxygenase-1 signaling in hepatic ischemia/reperfusion injury. Am. J. Transplant. 5, 1793-1800.
4. Prince, J. M., Ming, M. J., Levy, R. M., Liu, S., Pinsky, D. J., Vodovotz, Y., Billiar, T. R. (2007) Early growth response 1 mediates the systemic and hepatic inflammatory response initiated by hemorrhagic shock. Shock 27, 157-164.
5. Murphy, T. J., Paterson, H. M., Mannick, J. A., Lederer, J. A. (2004) Injury, sepsis, and the regulation of Toll-like receptor responses. J. Leukoc. Biol. 75, 400-407.
6. 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., Meldrum, D. R. (2005) Sex differences in the myocardial inflammatory response to acute injury. Shock 23, 1-10.
7. Terrell, A. M., Crisostomo, P. R., Wairiuko, G. M., Wang, M., Morrell, E. D., Meldrum, D. R. (2006) Jak/STAT/SOCS signaling circuits and associated cytokine-mediated inflammation and hypertrophy in the heart. Shock 26, 226-234.
8. Tsai, B. M., Patel, K., Wang, M., Morrell, E. D., Crisostomo, P. R., Meldrum, D. R. (2007) Selective protein kinase C inhibition attenuates pulmonary artery cytokine expression without affecting hypoxic pulmonary vasoconstriction. Shock 27, 36-39.
9. Fukao, T., Koyasu, S. (2003) PI3K and negative regulation of TLR signaling. Trends Immunol. 24, 358-363.
10. Williams, D. L., Ozment-Skelton, T., Li, C. (2006) Modulation of the phosphoinositide 3-kinase signaling pathway alters host response to sepsis, inflammation, and ischemia/reperfusion injury. Shock 25, 432-439.
11. Schabbauer, G., Tencati, M., Pedersen, B., Pawlinski, R., Mackman, N. (2004) PI3K-Akt pathway suppresses coagulation and inflammation in endotoxemic mice. Arterioscler. Thromb. Vasc. Biol. 24, 1963-1969.
12. Malech, H. L., Gallin, J. I. (1987) Current concepts: immunology. Neutrophils in human diseases. N. Engl. J. Med. 317, 687-694.
13. Vaday, G. G., Franitza, S., Schor, H., Hecht, I., Brill, A., Cahalon, L., Hershkoviz, R., Lider, O. (2001) Combinatorial signals by inflammatory cytokines and chemokines mediate leukocyte interactions with extracellular matrix. J. Leukoc. Biol. 69, 885-892.
14. Angle, N., Hoyt, D. B., Coimbra, R., Liu, F., Herdon-Remelius, C., Loomis, W., Junger, W. G. (1998) Hypertonic saline resuscitation diminishes lung injury by suppressing neutrophil activation after hemorrhagic shock. Shock 9, 164-170.
15. Yu, H. P., Shimizu, T., Hsieh, Y. C., Suzuki, T., Choudhry, M. A., Schwacha, M. G., Chaudry, I. H. (2006) Tissue-specific expression of estrogen receptors and their role in the regulation of neutrophil infiltration in various organs following trauma-hemorrhage. J. Leukoc. Biol. 79, 963-970.
16. Guo, R. F., Ward, P. A. (2002) Mediators and regulation of neutrophil accumulation in inflammatory responses in lung: insights from the IgG immune complex model. Free Radic. Biol. Med. 33, 303-310.
17. Dayal, S. D., Hasko, G., Lu, Q., Xu, D. Z., Caruso, J. M., Sambol, J. T., Deitch, E. A. (2002) Trauma/hemorrhagic shock mesenteric lymph upregulates adhesion molecule expression and IL-6 production in human umbilical vein endothelial cells. Shock 17, 491-495.
18. Yu, H. P., Choudhry, M. A., Shimizu, T., Hsieh, Y. C., Schwacha, M. G., Yang, S., Chaudry, I. H. (2006) Mechanism of the salutary effects of flutamide on intestinal myeloperoxidase activity following trauma-hemorrhage: up-regulation of estrogen receptor-{β}-dependent HO-1. J. Leukoc. Biol. 79, 277-284.
19. Jaeschke, H. (2006) Mechanisms of liver injury. II. Mechanisms of neutrophil-induced liver cell injury during hepatic ischemia-reperfusion and other acute inflammatory conditions. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G1083-G1088.
20. Wanner, G. A., Muller, P. E., Ertel, W., Bauer, M., Menger, M. D., Messmer, K. (1999) Differential effect of anti-TNF-α antibody on proinflammatory cytokine release by Kupffer cells following liver ischemia and reperfusion. Shock 11, 391-395.
21. Maier, M., Strobele, H., Voges, J., Bauer, C., Marzi, I. (2003) Attenuation of leukocyte adhesion by recombinant TNF-binding protein after hemorrhagic shock in the rat. Shock 19, 457-461.
22. Guo, R. F., Riedemann, N. C., Laudes, I. J., Sarma, V. J., Kunkel, R. G., Dilley, K. A., Paulauskis, J. D., Ward, P. A. (2002) Altered neutrophil trafficking during sepsis. J. Immunol. 169, 307-314.
23. Han, X. B., Liu, X., Hsueh, W., De Plaen, I. G. (2004) Macrophage inflammatory protein-2 mediates the bowel injury induced by platelet-activating factor. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G1220-G1226.
24. Shanley, T. P., Schmal, H., Warner, R. L., Schmid, E., Friedl, H. P., Ward, P. A. (1997) Requirement for C-X-C chemokines (macrophage inflammatory protein-2 and cytokine-induced neutrophil chemoattractant) in IgG immune complex-induced lung injury. J. Immunol. 158, 3439-3448.
25. Martin, D., Rojo, A. I., Salinas, M., Diaz, R., Gallardo, G., Alam, J., De Galarreta, C. M., Cuadrado, A. (2004) Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol. J. Biol. Chem. 279, 8919-8929.
26. Salinas, M., Wang, J., Rosa de Sagarra, M., Martin, D., Rojo, A. I., Martin-Perez, J., Ortiz de Montellano, P. R., Cuadrado, A. (2004) Protein kinase Akt/PKB phosphorylates heme oxygenase-1 in vitro and in vivo. FEBS Lett. 578, 90-94.
27. Wijayanti, N., Kietzmann, T., Immenschuh, S. (2005) Heme oxygenase-1 gene activation by the NAD(P)H oxidase inhibitor 4-(2-aminoethyl) benzenesulfonyl fluoride via a protein kinase B, p38-dependent signaling pathway in monocytes. J. Biol. Chem. 280, 21820-21829.
28. Szalay, L., Shimizu, T., Schwacha, M. G., Choudhry, M. A., Rue III, L. W., Bland, K. I., Chaudry, I. H. (2005) Mechanism of salutary effects of estradiol on organ function after trauma-hemorrhage: upregulation of heme oxygenase. Am. J. Physiol. Heart Circ. Physiol. 289, H92-H98.
29. Szalay, L., Shimizu, T., Suzuki, T., Yu, H. P., Choudhry, M. A., Schwacha, M. G., Rue III, L. W., Bland, K. I., Chaudry, I. H. (2006) Estradiol improves cardiac and hepatic function after trauma-hemorrhage: role of enhanced heat shock protein expression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R812-R818.
30. Man, K., Ng, K. T., Lee, T. K., Lo, C. M., Sun, C. K., Li, X. L., Zhao, Y., Ho, J. W., Fan, S. T. (2005) FTY720 attenuates hepatic ischemia-reperfusion injury in normal and cirrhotic livers. Am. J. Transplant. 5, 40-49.
31. Hsu, J. T., Hsieh, Y. C., Kan, W. H., Chen, J. G., Choudhry, M. A., Schwacha, M. G., Bland, K. I., Chaudry, I. H. (2007) Role of p38 mitogen-activated protein kinase pathway in estrogen-mediated cardioprotection following trauma-hemorrhage. Am. J. Physiol. Heart Circ. Physiol. 292, H2982-H2987.
32. Bauer, I., Rensing, H., Florax, A., Ulrich, C., Pistorius, G., Redl, H., Bauer, M. (2003) Expression pattern and regulation of heme oxygenase-1/heat shock protein 32 in human liver cells. Shock 20, 116-122.
33. Rensing, H., Bauer, I., Datene, V., Patau, C., Pannen, B. H., Bauer, M. (1999) Differential expression pattern of heme oxygenase-1/heat shock protein 32 and nitric oxide synthase-II and their impact on liver injury in a rat model of hemorrhage and resuscitation. Crit. Care Med. 27, 2766-2775.
34. Morita, T., Perrella, M. A., Lee, M. E., Kourembanas, S. (1995) Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc. Natl. Acad. Sci. USA 92, 1475-1479.
35. Wang, R., Wu, L., Wang, Z. (1997) The direct effect of carbon monoxide on KCa channels in vascular smooth muscle cells. Pflugers Arch. 434, 285-291.
36. Soares, M. P., Seldon, M. P., Gregoire, I. P., Vassilevskaia, T., Berberat, P. O., Yu, J., Tsui, T. Y., Bach, F. H. (2004) Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J. Immunol. 172, 3553-3563.
37. Hartsfield, C. L., Alam, J., Cook, J. L., Choi, A. M. (1997) Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. Am. J. Physiol. 273, L980-L988.
38. Baranano, D. E., Rao, M., Ferris, C. D., Snyder, S. H. (2002) Biliverdin reductase: a major physiologic cytoprotectant. Proc. Natl. Acad. Sci. USA 99, 16093-16098.
39. Nakao, A., Otterbein, L. E., Overhaus, M., Sarady, J. K., Tsung, A., Kimizuka, K., Nalesnik, M. A., Kaizu, T., Uchiyama, T., Liu, F., Murase, N., Bauer, A. J., Bach, F. H. (2004) Biliverdin protects the functional integrity of a transplanted syngeneic small bowel. Gastroenterology 127, 595-606.
40. Bornman, L., Steinmann, C. M., Gericke, G. S., Polla, B. S. (1998) In vivo heat shock protects rat myocardial mitochondria. Biochem. Biophys. Res. Commun. 246, 836-840.
41. Camper-Kirby, D., Welch, S., Walker, A., Shiraishi, I., Setchell, K. D., Schaefer, E., Kajstura, J., Anversa, P., Sussman, M. A. (2001) Myocardial Akt activation and gender: increased nuclear activity in females versus males. Circ. Res. 88, 1020-1027.
42. Hisamoto, K., Ohmichi, M., Kurachi, H., Hayakawa, J., Kanda, Y., Nishio, Y., Adachi, K., Tasaka, K., Miyoshi, E., Fujiwara, N., Taniguchi, N., Murata, Y. (2001) Estrogen induces the Akt-dependent activation of endothelial nitric-oxide synthase in vascular endothelial cells. J. Biol. Chem. 276, 3459-3467.
43. Honda, K., Sawada, H., Kihara, T., Urushitani, M., Nakamizo, T., Akaike, A., Shimohama, S. (2000) Phosphatidylinositol 3-kinase mediates neuroprotection by estrogen in cultured cortical neurons. J. Neurosci. Res. 60, 321-327.
44. Simoncini, T., Hafezi-Moghadam, A., Brazil, D. P., Ley, K., Chin, W. W., Liao, J. K. (2000) Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407, 538-541.
45. Song, G., Ouyang, G., Bao, S. (2005) The activation of Akt/PKB signaling pathway and cell survival. J. Cell. Mol. Med. 9, 59-71.
46. Shimizu, T., Yu, H. P., Hsieh, Y. C., Choudhry, M. A., Suzuki, T., Bland, K. I., Chaudry, I. H. (2007) Flutamide attenuates pro-inflammatory cytokine production and hepatic injury following trauma-hemorrhage via estrogen receptor-related pathway. Ann. Surg. 245, 297-304.
47. Hsieh, Y. C., Yu, H. P., Frink, M., Suzuki, T., Choudhry, M. A., Schwacha, M. G., Chaudry, I. H. (2007) G protein-coupled receptor 30-dependent protein kinase A pathway is critical in nongenomic effects of estrogen in attenuating liver injury after trauma-hemorrhage. Am. J. Pathol. 170, 1210-1218.
48. Hsieh, Y. C., Yang, S., Choudhry, M. A., Yu, H. P., Bland, K. I., Schwacha, M. G., Chaudry, I. H. (2006) Flutamide restores cardiac function after trauma-hemorrhage via an estrogen-dependent pathway through upregulation of PGC-1. Am. J. Physiol. Heart Circ. Physiol. 290, H416-H423.
49. Yu, H. P., Hsieh, Y. C., Suzuki, T., Choudhry, M. A., Schwacha, M. G., Bland, K. I., Chaudry, I. H. (2007) The PI3K/Akt pathway mediates the nongenomic cardioprotective effects of estrogen following trauma-hemorrhage. Ann. Surg. 245, 971-977.