Lipopolysaccharide directly stimulates aldosterone production via toll-like receptor 2 and toll-like receptor 4 related PI3K/Akt pathway in rat adrenal zona glomerulosa cells

Journal of Cellular Biochemistry

Volumn 111, Issue 4, 2010, Pages 872-880

  Huang, Hsin Lei ^a   Chiang, Ming Fu ^b   Lin, Chia Wen ^a   Pu, Hsiao Fung ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Akt; Aldosterone; LPS; SR B1; StAR; Toll like receptor

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ALDOSTERONE; CYTOCHROME P450; ENDOTOXIN; LIPOPOLYSACCHARIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SCAVENGER RECEPTOR BI; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ADRENAL GLAND; ALDOSTERONE BLOOD LEVEL; ALDOSTERONE RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; DISEASE SEVERITY; ENZYME PHOSPHORYLATION; GLOMERULOSA CELL; HORMONE SYNTHESIS; INFLAMMATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STEROIDOGENESIS; STRESS; ZONA GLOMERULOSA;

ALDOSTERONE; ANIMALS; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; LIPOPOLYSACCHARIDES; MALE; MODELS, BIOLOGICAL; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SCAVENGER RECEPTORS, CLASS B; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; ZONA GLOMERULOSA;

RATTUS;

EID: 78049242013     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22774     Document Type: Article

References (57)

1. Akashi K, Richie LI, Miyamoto T, Carr WH, Weissman IL. 2000. B lymphopoiesis in the thymus. J Immunol 164: 5221-5226.
2. Andersen JM, Dietschy JM. 1978. Relative importance of high and low density lipoproteins in the regulation of cholesterol synthesis in the adrenal gland, ovary, and testis of the rat. J Biol Chem 253: 9024-9032.
3. Asehnoune K, Strassheim D, Mitra S, Kim JY, Abraham E. 2004. Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-kappa B. J Immunol 172: 2522-2529.
4. Banno Y, Takuwa Y, Yamada M, Takuwa N, Ohguchi K, Hara A, Nozawa Y. 2003. Involvement of phospholipase D in insulin-like growth factor-I-induced activation of extracellular signal-regulated kinase, but not phosphoinositide 3-kinase or Akt, in Chinese hamster ovary cells. Biochem J 369: 363-368.
5. Beishuizen A, Thijs LG. 2003. Endotoxin and the hypothalamo-pituitary-adrenal (HPA) axis. J Endotoxin Res 9: 3-24.
6. Berg KK, Madsen HO, Garred P, Wiseth R, Gunnes S, Videm V. 2009. The additive contribution from inflammatory genetic markers on the severity of cardiovascular disease. Scand J Immunol 69: 36-42.
7. Bommhardt U, Chang KC, Swanson PE, Wagner TH, Tinsley KW, Karl IE, Hotchkiss RS. 2004. Akt decreases lymphocyte apoptosis and improves survival in sepsis. J Immunol 172: 7583-7591.
8. Bornstein SR, Schumann RR, Rettori V, McCann SM, Zacharowski K. 2004a. Toll-like receptor 2 and Toll-like receptor 4 expression in human adrenals. Horm Metab Res 36: 470-473.
9. Bornstein SR, Zacharowski P, Schumann RR, Barthel A, Tran N, Papewalis C, Rettori V, McCann SM, Schulze-Osthoff K, Scherbaum WA, Tarnow J, Zacharowski K. 2004b. Impaired adrenal stress response in Toll-like receptor 2-deficient mice. Proc Natl Acad Sci USA 101: 16695-16700.
10. Bornstein SR, Ziegler CG, Krug AW, Kanczkowski W, Rettori V, McCann SM, Wirth M, Zacharowski K. 2006. The role of toll-like receptors in the immune-adrenal crosstalk. Ann NY Acad Sci 1088: 307-318.
11. Burstein S, Gut M. 1976. Intermediates in the conversion of cholesterol to pregnenolone: Kinetics and mechanism. Steroids 28: 115-131.
12. Campbell S, Otis M, Cote M, Gallo-Payet N, Payet MD. 2003. Connection between integrins and cell activation in rat adrenal glomerulosa cells: A role for Arg-Gly-Asp peptide in the activation of the p42/p44(mapk) pathway and intracellular calcium. Endocrinology 144: 1486-1495.
13. Chang LL, Wun WS, Wang PS. 2008. Effects of dehydroepiandrosterone on aldosterone release in rat zona glomerulosa cells. J Biomed Sci 15: 463-470.
14. Christenson LK, Strauss JF. 2000. Steroidogenic acute regulatory protein (StAR) and the intramitochondrial translocation of cholesterol. Biochim Biophys Acta 1529: 175-187.
15. Dijk PC, Jager KJ, de Charro F, Collart F, Cornet R, Dekker FW, Gronhagen-Riska C, Kramar R, Leivestad T, Simpson K, Briggs JD. 2001. Renal replacement therapy in Europe: The results of a collaborative effort by the ERA-EDTA registry and six national or regional registries. Nephrol Dial Transplant 16: 1120-1129.
16. Enriquez de Salamanca A, Garcia R. 2003. Rat glomerulosa cells in primary culture and E. coli lipopolysaccharide action. J Steroid Biochem Mol Biol 85: 81-88.
17. Fukao T, Koyasu S. 2003. PI3K and negative regulation of TLR signaling. Trends Immunol 24: 358-363.
18. Garcia R, Abarca S, Municio AM. 1990. Adrenal gland function in reversible endotoxic shock. Circ Shock 30: 365-374.
19. Givalois L, Dornand J, Mekaouche M, Solier MD, Bristow AF, Ixart G, Siaud P, Assenmacher I, Barbanel G. 1994. Temporal cascade of plasma level surges in ACTH, corticosterone, and cytokines in endotoxin-challenged rats. Am J Physiol 267: R164-R170.
20. Griendling KK, Sorescu D, Lassegue B, Ushio-Fukai M. 2000. Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler Thromb Vasc Biol 20: 2175-2183.
21. Gwynne JT, Strauss JF. 1982. The role of lipoproteins in steroidogenesis and cholesterol metabolism in steroidogenic glands. Endocr Rev 3: 299-329.
22. Hajjar AM, O'Mahony DS, Ozinsky A, Underhill DM, Aderem A, Klebanoff SJ, Wilson CB. 2001. Cutting edge: Functional interactions between toll-like receptor (TLR) 2 and TLR1 or TLR6 in response to phenol-soluble modulin. J Immunol 166: 15-19.
23. 2 and nitric oxide in inducible nitric oxide synthase expression in macrophages. Nitric Oxide 5: 504-513.
24. Hirschfeld M, Ma Y, Weis JH, Vogel SN, Weis JJ. 2000. Cutting edge: Repurification of lipopolysaccharide eliminates signaling through both human and murine toll-like receptor 2. J Immunol 165: 618-622.
25. Jang SI, Kim HJ, Kim YJ, Jeong SI, You YO. 2006. Tanshinone IIA inhibits LPS-induced NF-kappaB activation in RAW 264.7 cells: Possible involvement of the NIK-IKK, ERK1/2, p38 and JNK pathways. Eur J Pharmacol 542: 1-7.
26. Kanczkowski W, Ziegler CG, Zacharowski K, Bornstein SR. 2008. Toll-like receptors in endocrine disease and diabetes. Neuroimmunomodulation 15: 54-60.
27. Kanczkowski W, Zacharowski K, Wirth MP, Ehrhart-Bornstein M, Bornstein SR. 2009. Differential expression and action of Toll-like receptors in human adrenocortical cells. Mol Cell Endocrinol 300: 57-65.
28. Kiechl S, Lorenz E, Reindl M, Wiedermann CJ, Oberhollenzer F, Bonora E, Willeit J, Schwartz DA. 2002. Toll-like receptor 4 polymorphisms and atherogenesis. N Engl J Med 347: 185-192.
29. Kim I, Oh JL, Ryu YS, So JN, Sessa WC, Walsh K, Koh GY. 2002. Angiopoietin-1 negatively regulates expression and activity of tissue factor in endothelial cells. FASEB J 16: 126-128.
30. 2 in NF-kappaB activation. Free Radic Biol Med 45: 885-896.
31. Kim JH, Na HJ, Kim CK, Kim JY, Ha KS, Lee H, Chung HT, Kwon HJ, Kwon YG, Kim YM. 2008b. The non-provitamin A carotenoid, lutein, inhibits NF-kappaB-dependent gene expression through redox-based regulation of the phosphatidylinositol 3-kinase/PTEN/Akt and NF-kappaB-inducing kinase pathways: Role of H(2)O(2) in NF-kappaB activation. Free Radic Biol Med 45: 885-896.
32. Kraemer FB. 2007. Adrenal cholesterol utilization. Mol Cell Endocrinol 265-266: 42-45.
33. Li Q, Engelhardt JF. 2006. Interleukin-1beta induction of NFkappaB is partially regulated by H2O2-mediated activation of NFkappaB-inducing kinase. J Biol Chem 281: 1495-1505.
34. Liu SF, Malik AB. 2006. NF-kappa B activation as a pathological mechanism of septic shock and inflammation. Am J Physiol Lung Cell Mol Physiol 290: L622-L645.
35. Liu SL, Lin X, Shi DY, Cheng J, Wu CQ, Zhang YD. 2002. Reactive oxygen species stimulated human hepatoma cell proliferation via cross-talk between PI3-K/PKB and JNK signaling pathways. Arch Biochem Biophys 406: 173-182.
36. Machida K, Tsukamoto H, Mkrtchyan H, Duan L, Dynnyk A, Liu HM, Asahina K, Govindarajan S, Ray R, Ou JH, Seki E, Deshaies R, Miyake K, Lai MM. 2009. Toll-like receptor 4 mediates synergism between alcohol and HCV in hepatic oncogenesis involving stem cell marker Nanog. Proc Natl Acad Sci USA 106: 1548-1553.
37. Meng G, Rutz M, Schiemann M, Metzger J, Grabiec A, Schwandner R, Luppa PB, Ebel F, Busch DH, Bauer S, Wagner H, Kirschning CJ. 2004. Antagonistic antibody prevents toll-like receptor 2-driven lethal shock-like syndromes. J Clin Invest 113: 1473-1481.
38. Meroni SB, Riera MF, Pellizzari EH, Cigorraga SB. 2002. Regulation of rat Sertoli cell function by FSH: Possible role of phosphatidylinositol 3-kinase/protein kinase B pathway. J Endocrinol 174: 195-204.
39. Ozes ON, Mayo LD, Gustin JA, Pfeffer SR, Pfeffer LM, Donner DB. 1999. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401: 82-85.
40. Palsson OS, Heymen S, Whitehead WE. 2004. Biofeedback treatment for functional anorectal disorders: A comprehensive efficacy review. Appl Psychophysiol Biofeedback 29: 153-174.
41. Path G, Bornstein SR, Ehrhart-Bornstein M, Scherbaum WA. 1997. Interleukin-6 and the interleukin-6 receptor in the human adrenal gland: Expression and effects on steroidogenesis. J Clin Endocrinol Metab 82: 2343-2349.
42. Rigotti A, Trigatti BL, Penman M, Rayburn H, Herz J, Krieger M. 1997. A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism. Proc Natl Acad Sci USA 94: 12610-12615.
43. Rocha R, Chander PN, Zuckerman A, Stier CT. 1999. Role of aldosterone in renal vascular injury in stroke-prone hypertensive rats. Hypertension 33: 232-237.
44. Rossi G, Boscaro M, Ronconi V, Funder JW. 2005. Aldosterone as a cardiovascular risk factor. Trends Endocrinol Metab 16: 104-107.
45. Sanchez-Lemus E, Murakami Y, Larrayoz-Roldan IM, Moughamian AJ, Pavel J, Nishioku T, Saavedra JM. 2008. Angiotensin II AT1 receptor blockade decreases lipopolysaccharide-induced inflammation in the rat adrenal gland. Endocrinology 149: 5177-5188.
46. Shah BH, Baukal AJ, Shah FB, Catt KJ. 2005. Mechanisms of extracellularly regulated kinases 1/2 activation in adrenal glomerulosa cells by lysophosphatidic acid and epidermal growth factor. Mol Endocrinol 19: 2535-2548.
47. + concentration. Mol Cell Endocrinol 217: 23-26.
48. Stier CT, Chander PN, Rocha R. 2002. Aldosterone as a mediator in cardiovascular injury. Cardiol Rev 10: 97-107.
49. Szeto CC, Kwan BC, Chow KM, Lai KB, Chung KY, Leung CB, Li PK. 2008. Endotoxemia is related to systemic inflammation and atherosclerosis in peritoneal dialysis patients. Clin J Am Soc Nephrol 3: 431-436.
50. Temel RE, Trigatti B, DeMattos RB, Azhar S, Krieger M, Williams DL. 1997. Scavenger receptor class B, type I (SR-BI) is the major route for the delivery of high density lipoprotein cholesterol to the steroidogenic pathway in cultured mouse adrenocortical cells. Proc Natl Acad Sci USA 94: 13600-13605.
51. Vakharia K, Hinson JP. 2005. Lipopolysaccharide directly stimulates cortisol secretion by human adrenal cells by a cyclooxygenase-dependent mechanism. Endocrinology 146: 1398-1402.
52. Vakharia K, Renshaw D, Hinson JP. 2002. Bacterial lipopolysaccharide directly stimulates cortisol secretion in human adrenal cells. Endocr Res 28: 357-361.
53. Wang X, McCullough KD, Franke TF, Holbrook NJ. 2000. Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J Biol Chem 275: 14624-14631.
54. Weber KT. 2001. Aldosterone in congestive heart failure. N Engl J Med 345: 1689-1697.
55. Zacharowski K, Zacharowski PA, Koch A, Baban A, Tran N, Berkels R, Papewalis C, Schulze-Osthoff K, Knuefermann P, Zahringer U, Schumann RR, Rettori V, McCann SM, Bornstein SR. 2006. Toll-like receptor 4 plays a crucial role in the immune-adrenal response to systemic inflammatory response syndrome. Proc Natl Acad Sci USA 103: 6392-6397.
56. Zhang WJ, Wei H, Hagen T, Frei B. 2007. Alpha-lipoic acid attenuates LPS-induced inflammatory responses by activating the phosphoinositide 3-kinase/Akt signaling pathway. Proc Natl Acad Sci USA 104: 4077-4082.
57. Zor T, Selinger Z. 1996. Linearization of the Bradford protein assay increases its sensitivity: Theoretical and experimental studies. Anal Biochem 236: 302-308.