Androstenediol inhibits the trauma-hemorrhage-induced increase in caspase-3 by downregulating the inducible nitric oxide synthase pathway

Journal of Applied Physiology

Volumn 102, Issue 3, 2007, Pages 933-941

  Kiang, Juliann G ^a,b,c,e   Peckham, Russell M ^a   Duke, Leah E ^a   Shimizu, Tomoharu ^d   Chaudry, Irshad H ^d   Tsokos, George C ^a,c  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c Uniformed Services University of the Health Sciences and the Walter Reed National Military Medical Center   (United States)

^d Kentucky   (United States)

^e ARMED FORCES RADIOBIOLOGY RESEARCH INSTITUTE   (United States)

Author keywords

5 androstene 3 , 17 diol; Adiol; Caspase 9; Cytochrome c; Hemorrhage shock

Indexed keywords

ANDROSTENEDIOL; APOPTOSOME; CASPASE 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVITY; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LIVER DYSFUNCTION; LIVER PROTECTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOFT TISSUE INJURY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANDROSTENEDIOL; ANIMALS; APOPTOSIS; CASPASE 3; DOWN-REGULATION; LIVER; MALE; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; SHOCK, HEMORRHAGIC; TUMOR SUPPRESSOR PROTEIN P53; WOUNDS AND INJURIES;

EID: 33847699750     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00919.2006     Document Type: Article

References (60)

1. Adamus G. Autoantibody-induced apoptosis as a possible mechanism of autoimmune retinopathy. Autoimmun Rev 2: 63-68, 2003.
2. Angele MK, Fitzal F, Smail N, Knoferl MW, Schwacha MG, Ayala A, Wang P, Chaudry IH. L-Arginine attenuates trauma-hemorrhage-induced liver injury. Crit Care Med 28: 3242-3248, 2000.
3. Baue AE, Durham R, Faist E. Systemic inflammatory response syndrome (SIRS), multiple organ dysfunction syndrome (MODS), multiple organ failure (MOF): are we winning the battle? Shock 10: 79-89, 1998.
4. Blackwell TS, Blackwell TR, Holden EP, Christman BW, Christman JW. In vivo antioxidant treatment suppresses nuclear factor kB activation and neutrophilic lung inflammation. J Immunol 157: 1630-1637, 1996.
5. Carr DJ. Increased levels of IFN-gamma in the trigeminal ganglion correlate with protection against HSV-1-induced encephalitis following subcutaneous administration with androstenediol. J Neuroimmunol 89: 160-167, 1998.
6. Chang CG, Van Way CW III, Dhar A, Helling T Jr, Hahn Y. The use of insulin and glucose during resuscitation from hemorrhagic shock increases hepatic ATP. J Surg Res 92: 171-176, 2000.
7. Chaudry IH, Planer GJ, Sayeed MM, Baue AE. ATP depletion and replenishment in hemorrhagic shock. Surg Form 24: 77-79, 1973.
8. Chen T, Zamora R, Zuckerbraun B, Billiar TR. Role of nitric oxide in liver injury. Curr Mol Med 3: 519-526, 2003.
9. Cho NH, Lee JD, Cheong BS, Choi DY, Chang HK, Lee TH, Shin MC, Shin MS, Lee J, Kim CJ. Acupuncture suppresses intrastriatal hemorrhage-induced apoptotic neuronal cell death in rats. Neurosci Lett 362: 141-145, 2004.
10. Cho S, Liu D, Fairman D, Li P, Jenkins L, McGonigle P, Wood A. Spatiotemporal evidence of apoptosis-mediated ischemic injury in organotypic hippocampal slice cultures. Neurochem Int 45: 117-127, 2004.
11. Collins JL, Vodovotz Y, Hierholzer C, Villavicencio RT, Liu S, Alber S, Gallo D, Stolz DB, Watkins SC, Godfrey A, Gooding W, Kelly E, Peitzman AB, Billiar TR. Characterization of the expression of inducible nitric oxide synthase in rat and human liver during hemorrhagic shock. Shock 19: 117-122, 2003.
12. Eigel BN, Gursahani H, Hadley RW. The sodium-calcium exchanger plays a key role in inducing apoptosis following prolonged hypoxia in cultured guinea pig ventricular myocytes. Am J Physiol Heart Circ Physiol 287: H1466-H1475, 2004.
13. Ghosh DK, Rashid MB, Crane B, Taskar V, Mast M, Misukonis MA, Weinberg JB, Eissa NT. Characterization of key residues in the subdomain encoded by exon 8 and 9 of human inducible nitric oxide synthase: a critical role for Asp-280 in substrate binding and subunit interactions. Proc Natl Acad Sci USA 98: 10392-10397, 2001.
14. Head CC, Farrow MJ, Sheridan JF, Padgett DA. Androstenediol reduces the anti-inflammatory effects of restraint stress during wound healing. Brain Behav Immun 20: 590-596, 2006.
15. Hierholzer C, Harbracht B, Menezes JM, Kane J, MacMicking J, Nathan CF, Peitzman AB, Billiar TR, Tweardy DJ. Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock. J Exp Med 187: 917-928, 1998.
16. Hildebrand F, Hubbard WJ, Choudhry MA, Thobe BM, Pape HC, Chaudry IH. Effects of 17β-estradiol and flutamide on inflammatory response and distant organ damage following trauma-hemorrhage in metestrus females. J Leukoc Biol 80: 759-65, 2006.
17. Hill MM, Adrain C, Martin SJ. Portrait of a killer: the mitochondrial apoptosome emerges from the shadow. Mol Interv 3: 19-25, 2003.
18. Jiang X, Wang X. Cytochrome-c-mediated apoptosis. Annu Rev Biochem 73: 87-106, 2004.
19. Kiang JG. Inducible heat shock protein 70 kD and inducible nitric oxide synthase in hemorrhage/resuscitation-induced injury. Cell Res 14: 450-459, 2004.
20. Kiang JG, Bowman DP, Lu X, Li Y, Ding XZ, Zhao B, Juang YT, Atkins JL, Tsokos GC. Geldanmaycin treatment prevents hemorrhage-induced ATP loss by overexpressing HSP-70 and activating pyruvate dehydrogenase. Am J Physiol Gastrointest Liver Physiol 291: G117-G127, 2006.
21. Kiang JG, Bowman PD, Wu BW, Hampton N, Kiang AG, Zhao B, Juang YT, Atkins JL, Tsokos GC. Geldanamycin treatment inhibits hemorrhage-induced increases in KLF6 and iNOS expression in unresuscitated mouse organs: role of inducible HSP-70. J Appl Physiol 97: 564-569, 2004.
22. Kiang JG, Bowman PD, Wu BW, Hampton N, Kiang AG, Zhao B, Juang YT, Atkins JL, Tsokos GC. Geldanamycin inhibits hemorrhage-induced increases in caspase-3 activity, KLF6 and iNOS expression in unresuscitated organs of mice: Role of inducible HSP-70 (Abstract). FASEB J 18: A220-A221, 2004.
23. Kiang JG, Lu X, Tabaku LS, Bentley TB, Atkins JL, Tsokos GC. Resuscitation with lactated Ringer solution limits the expression of molecular events associated with lung injury after hemorrhage. J Appl Physiol 98: 550-556, 2005.
24. Kiang JG, Tsen KT. Biology of hypoxia. Chin J Physiol 49: 223-233, 2006.
25. Kiang JG, Warke VG, Tsokos GC. NaCN-induced chemical hypoxia is associated with altered gene expression. Mol Cell Biochem 245: 211-216, 2003.
26. Lee HH, Kim H, Lee MH, Chang HK, Lee TH, Jang MH, Shin MC, Lim BV, Shin MS, Kim YP, Yoon JH, Jeong IG, Kim CJ. Treadmill exercise decreases intrastriatal hemorrhage-induced neuronal cell death via suppression on caspase-3 expression in rats. Neurosci Lett 352: 33-36, 2003.
27. Liu LM, Ward JA, Dubick MA. Hemorrhage-induced vascular hyporeactivity to norepinephrine in select vasculatures of rats and the roles of nitric oxide and endothelin. Shock 19: 208-214, 2003.
28. Loria RM. Immune up-regulation and tumor apoptosis by androstene steroids. Steroids 67: 953-966, 2002.
29. Mauriz JL, Gonzalez P, Jorquera F, Olcoz JL, Gonzalez-Gallego J. Caspase inhibition does not protect against liver damage in hemorrhagic shock. Shock 19: 33-37, 2003.
30. McDonald M, Abdelrahman M, Cuzzocrea S, Thiemermann C. Tyrphostin reduced the organ injury in haemorrhagic shcok: role of inducible nitric oxide synthase. Resuscitation 58: 349-361, 2003.
31. Menezes JM, Hierholzer C, Watkins SC, Billiar TR, Peitzman AB, Harbrecht BG. The modulation of hepatic injury and heat shock expression by inhibition of inducible nitric oxide synthase after hemorrhagic shock. Shock 17: 13-18, 2002.
32. Mongan PD, Capacchione J, West S, Karaian J, Dubois D, Keneally R, Sharma P. Pyruvate improves redox status and decreases indicators of hepatic apoptosis during hemorrhagic shock in swine. Am J Physiol Heart Circ Physiol 283: H1634-H1644, 2002.
33. Murao Y, Hata M, Ohnishi K, Okuchi K, Nakajima Y, Hiasa Y, Junger WG, Hoyt DB, Ohnishi T. Hypertonic saline resuscitation reduces apoptosis and tissue damage of the small intestine in a mouse model of hemorrhagic shock. Shock 20: 23-28, 2003.
34. Nakada H, Kase Y, Matsunaga T, Komoda T, Iinuma T. Caspase 3 activation in nasal capillary in patients with epistaxis. Otolaryngol Head Neck Surg 128: 632-639, 2003.
35. Nathan BD, Padgett DA, Loria RM. Andreostenediol and dehydroepiandronsterone protect mice against lethal bacterial infections and lipopolysaccharide toxicity. J Med Microbiol 48: 425-431, 1999.
36. O'Mahoney ME, Logue S, Szegezdi E, Stenson-Cox C, Fitzgerald U, Samali A. Hypoxia and ischemia induce nuclear condensation and caspase activation in cardiomyocytes. Ann NY Acad Sci 1010: 728-732, 2003.
37. Pannen BH, Bauer M, Noldge-Schomburg GF, Zhang JX, Robotham JL, Clemens MG, Geiger KK. Regulation of hepatic blood flow during resuscitation from hemorrhagic shock: role of NO and endothelins. Am J Physiol Heart Circ Physiol 272: H2736-H2745, 1997.
38. Paxian M, Bauer I, Rensing H, Jaeschke H, Mautes AE, Kolb SA, Wolf B, Stockhausen A, Jeblick S, Bauer M. Recovery of hepatocellular ATP and "pericentral apoptosis" after hemorrhage and resuscitation. FASEB J 17: 993-1002, 2003.
39. Pelacho B, Natal C, Espana A, Sanchez-Carpintero I, Iraburu MJ, Lopez-Zabalza MJ. Pemphigus vulgaris autoantibodies induce apoptosis in HaCaT keratinocytes. FEBS Lett 566: 6-10, 2004.
40. Pittet JF, Lu LN, Geiser T, Lee H, Matthay A, Welch WJ. Stress preconditioning attenuates oxidative injury to the alveolar epithelium of the lung following haemorrhage in rats. J Physiol 538: 583-597, 2002.
41. Shenkar R, Schwartz MD, Terada LS, Repine JE, McCord J, Abraham E. Hemorrhage activates NF-κB in murine lung mononuclear cells in vivo. Am J Physiol Lung Cell Mol Physiol 270: L729-L735, 1996.
42. Shimizu T, Choudhry MA, Szalay L, Rue LW III, Bland KI, Chaudry IH. Salutary effects of androstenediol on cardiac function and splanchnic perfusion after trauma-hemorrhage. Am J Physiol Regul Integr Comp Physiol 287: R386-R390, 2004.
43. Shimizu T, Szalay L, Choudhry MA, Schwacha MG, Rue LW III, Bland KI, Chaudry IH. Mechanism of salutary effects of androstenediol on hepatic function following trauma-hemorrhage: the role of endothelin 1 and inducible nitric oxide synthase. Am J Physiol Gastrointest Liver Physiol 288: G244-G250, 2005.
44. Shimizu T, Szalay L, Hsieh YC, Choudhry MA, Bland KI, Chaudry IH. Salutary effects of androstenediol on hepatic function after trauma-hemorrhage are mediated via peroxisome proliferators-activated receptor gamma. Surgery 138: 204-211, 2005.
45. Shimizu T, Szalay L, Hsieh YC, Suzuki T, Choudhry MA, Bland KI, Chaudry IH. A role of PPAR-gamma in androstenediol-mediated salutary effects on cardiac function following trauma-hemorrhage. Ann Surg 244: 131-138, 2006.
46. Slomiany BL, Piotrowski J, Slomiany A. Induction of caspase-3 and nitric oxide synthase-2 during gastric mucosal inflammatory reaction to Helicobacter pylori lipopolysaccharide. Biochem Mol Biol Int 46: 1063-1070, 1998.
47. Szabo C, Billiar TR. Novel roles of nitric oxide in hemorrhagic shock. Shock 12: 1-9, 1999.
48. Taylor BS, Geller DA. Molecular regulation of the human inducible nitric oxide synthase (iNOS) gene. Shock 13: 413-424, 2000.
49. Toth B, Yokoyama Y, Kuebler JF, Schwacha MG, Rue LW III, Bland KI, Chaudry IH. Sex differences in hepatic heme oxygenase expression and activity following trauma and hemorrhagic shock. Arch Surg 138: 1375-1382, 2003.
50. Van Way CW III, Dhar A, Morrison DC, Longorio MA, Maxfield DM. Cellular energetics in hemorrhagic shock: restoring adenosine triphosphate to the cells. J Trauma 54, Suppl: S169-S176, 2003.
51. Wang P, Ba ZF, Burkhardt J, Chaudry IH. Measurement of hepatic blood flow after severe hemorrhage: lack of restoration despite adequate resuscitation. Am J Physiol Gastrointest Liver Physiol 262: G92-G98, 1992.
52. Wang X, Mori T, Sumii T, Lo EH. Hemoglobin-induced cytotoxicity in rat cerebral cortical neurons: caspase activation and oxidative stress. Stroke 33: 1882-1888, 2002.
53. Wang X, Zhu C, Wang X, Hagberg H, Korhonen L, Sandberg M, Lindholm D, Blomgren K. X-linked inhibitor of apoptosis (XIAP) protein protects against caspase activation and tissue loss after neonatal hypoxia-ischemia. Neurobiol Dis 16: 179-189, 2004.
54. Warke VG, Nambiar MP, Krishnan S, Tenbrock K, Geller DA, Koritschoner NP, Atkins JL, Farber DL, Tsokos GC. Transcriptional activation of the human inducible nitric-oxide synthase promoter by Kruppel-like factor 6. J Biol Chem 278: 14812-14819, 2003.
55. Whitnall MH, Villa V, Seed TM, Benjack J, Miner V, Lewbart ML, Dowding CA, Jackson WE III. Molecular specificity of 5-androstenediol as a systemic radioprotectant in mice. Immunopharmacol Immunotoxicol 27: 15-32, 2005.
56. Wong HR, Ryan M, Wispe JR. The heat shock response inhibits activation of inducible nitric oxide synthase gene expression by blocking I-kB degradation and NF-kB nuclear translocation. Biochem Biophys Res Commun 231: 257-263, 1997.
57. Yokoyama Y, Toth B, Kitchens WC, Schwacha MG, Bland KI, Chaudry IH. Role of thromboxane in producing portal hypertension following trauma-hemorrhage. Am J Physiol Gastrointest Liver Physiol 285: G1293-G1299, 2003.
58. Yokoyama Y, Toth B, Kitchens WC, Schwacha MG, Rue LW III, Bland KI, Chaudry IH. Estradiol's effect on portal response to endothelin-1 after trauma-hemorrahge. J Surg Res 121: 25-30, 2004.
59. Yu HP, Yang S, Choudhry MA, Hsieh YC, Bland KI, Chaudry IH. Mechanism responsible for the salutary effects of flutamide on cardiac performance after trauma-hemorrhagic shock: upregulation of cardiomyocyte estrogen receptors. Surgery 138: 85-92, 2005.
60. Zhou C, Yamaguchi M, Kusaka G, Schonholz C, Nanda A, Zhang JH. Caspase inhibitors prevent endothelial apoptosis and cerebral vasospasm in dog model of experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab 24: 419-431, 2004.