Evidence that age-related changes in p38 MAP kinase contribute to the decreased steroid production by the adrenocortical cells from old rats

Aging Cell

Volumn 7, Issue 2, 2008, Pages 168-178

  Abidi, Parveen ^a   Leers Sucheta, Susan ^a,d   Cortez, Yuan ^a   Han, Jiahuai ^c   Azhar, Salman ^a,b  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d PFIZER INC   (United States)

Author keywords

Antioxidants; Corticosterone; MnTMPyP; NAC; Oxidative stress; Protein phosphorylation and cell signaling; Steroidogenesis

Indexed keywords

ACETYLCYSTEINE; LIPID; LIPID PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; STEROID; STRESS ACTIVATED PROTEIN KINASE 1; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ADRENAL CORTEX CELL; AGING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HORMONE INHIBITION; LIPID PEROXIDATION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; STEROIDOGENESIS; WESTERN BLOTTING;

ADRENAL CORTEX; ADRENAL CORTEX HORMONES; AGE FACTORS; AGING; ANIMALS; ENZYME ACTIVATION; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FREE RADICAL SCAVENGERS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPID PEROXIDATION; MALE; MAP KINASE SIGNALING SYSTEM; METALLOPORPHYRINS; OXIDANTS; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

ANIMALIA; RATTUS;

EID: 40549101870     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2007.00364.x     Document Type: Article

References (76)

1. Abidi P, Leers-Sucheta S, Azhar S (2004) Suppression of steroidogenesis and activator protein-a transcription factor activity in rat adrenals by vitamin E deficiency-induced oxidative stress. J. Nutr. Biochem. 15, 210-219.
2. Alessi DR, Cuenda A, Cohen P, Dudley DT, Saltiel AR (1995) PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270, 27489-27494.
3. Arlt W (2004) Dehydroepiandrosterone and ageing. Best Pract. Res. Clin. Endocrinol. Metab. 18, 363-380.
4. Azhar S, Wang H, Tsai H, Reaven E (1991) Okadaic acid interferes with lipoprotein-supported corticosterone production in adrenal cells. Biochem. Biophy. Res. Commun. 179, 726-733.
5. Azhar S, Cao L, Reaven E (1995) Alteration of the adrenal antioxidant system during aging in rats. J. Clin. Invest. 96, 1414-1424.
6. Belloni AS, Rebuffat P, Malendowicz LK, Mazzocchi G, Rocco S, Nussdorfer GG (1992) Age-related changes in the morphology and function of the zona glomerulosa of the rat adrenal cortex. Tissue Cell. 24, 835-842.
7. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W, Leisten JC, Motiwala A, Pierce S, Satoh Y, Bhagwat SP, Manning AM, Anderson DW (2001) SP600125, an anthrapyrazolone inhibitor of jun N -terminal kinase. Proc. Natl. Acad. Sci. USA 98, 13681-13686.
8. Bird RP, Draper HH (1984) Comparative studies on different methods of malonaldehyde determination. Methods Enzymol. 105, 299-416.
9. Burger HG, Dudley EC, Robertson DM, Dennerstein L (2002) Hormonal changes in the menopause transition. Recent Prog. Horm. Res. 57, 257-275.
10. Cao L, Leers-Sucheta S, Azhar S (2004) Aging alters the functional expression of enzymatic and non-enzymatic anti-oxidant defense system in testicular rat Leydig cells. J. Steroid Biochem. Molec. Biol. 88, 61-67.
11. Cheng B, Chou S-C, Abraham S, Kowal J (1998) Effects of prolonged ACTH-stimulation on adrenocortical cholesterol reserve and apolipoprotein E concentration in Young and aged Fischer 344 male rats. J. Steroid Biochem. Molec. Biol. 66, 335-345.
12. Cuenda A, Rouse J, Doza YN, Meier R, Cohen P, Gallagher TF, Young PR, Lee JC (1995) SB203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364, 229-233.
13. Culty M, Luo L, Yao Z-X, Chen H, Papadopoulos V, Zirkin BR (2002) Cholesterol transport, peripheral benzodiazepine receptor, and steroidogenesis in aging Leydig cells. J. Androl. 23, 439-447.
14. Davis T, Baird DM, Haughton MF, Jones CJ, Kipling D (2005) Prevention of accelerated cell aging in Warner Syndrome using a p38 mitogen-activated protein kinase inhibitor. J. Gerontol. (Biol. Sci.) 60A, 1386-1393.
15. Dharia S, Parker R (2004) Adrenal androgens and aging. Semin. Reprod. Med. 22, 361-368.
16. Diemer T, Allen JA, Hales KH, Hales DB (2003) Reactive oxygen disrupts mitochondria in MA-10 tumor Leydig cells and inhibits steroidogenic acute regulatory (StAR) protein and steroidogeneis. Endocrinology 144, 2882-2891.
17. Edmunds JW, Mahadevan LC (2004) MAP kinases as structural adaptors and enzymatic activators in transcription complexes. J. Cell Sci. 117, 3715-3723.
18. Favata MF, Horiuchi KY, Manos EJ, Dauleriot AJ, Stradley DA, Feeser WS, Van Dyk DE, Pitts WJ, Earl RA, Hobbs F, Copeland RA, Magolda RL, Scherle PA, Trazaskos JM (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273, 18623-18632.
19. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408, 239-247.
20. Frungieri MB, Gonzalez-Calvar SI, Parborell F, Albrecht M, Mayerhofer A, Calandra RS (2006) Cyclooxygenase-2 and prostaglandin F2α in Syrian hamster Leydig cells: Inhibitory role on luteinizing hormone/ human chronic gonadotropin-stimulated testosterone production. Endocrinology 147, 4476-4485.
21. Gay CA, Gebicki JM (2003) Measurement of protein and lipid hydroperoxides in biological systems by the ferric-xylenol orange method. Anal. Biochem. 315, 29-35.
22. 2 biosynthesis stimulated by interleukin-1β. J. Biol. Chem. 272, 8083-8089.
23. 2-terminal kinase and p38 MAPK signal pathways in rat renal mesangial cells. J. Biol. Chem. 273, 28670-28676.
24. Hanukoglu I (2006) Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metab. Rev. 38, 171-196.
25. Haq R, Brenton JD, Takahashi M, Finan D, Rottapel R, Zanke B (2002) Constitutive p38HOG mitogen-activated protein kinase activation induces permanent cell cycle arrest and senescence. Cancer Res. 62, 5076-5082.
26. Harman SM (2005) Testosterone in older men after the Institute of Medicine Report: Where do we go from here? Climacteric 8, 124-135.
27. Harper AJ, Buster JE, Casson PR (1999) Changes in adrenocortical function with aging and therapeutic implications. Semin. Reprod. Endocrinol. 17, 327-338.
28. Hendrickx N, Volanti C, Moens U, Seternes OM, de White P, Vandenheede JR, Piette J, Agostinis P (2003) Up-regulation of cyclooxygenase-2 and apoptosis resistance by p38 MAPK in hypericin-mediated photodynamic therapy of human cancer cells. J. Biol. Chem. 278, 52231-52239.
29. Hermes-Lima M, Willmore WG, Storey KB (1995) Quantification of lipid peroxidation in tissue extracts based on Fe(III) xylenol orange complex formation. Free Radic. Biol. Med. 19, 271-280.
30. Hsieh C-C, Papaconstantinou J (2006) Thioredoxin-ASK1 complex levels regulate ROS-mediated p38 MAPK pathway activity in livers of aged and long-lived Snell dwarf mice. FASEB J. 20, 259-268.
31. Ito K, Hirao A, Arai F, Takubo K, Matsuoka S, Miyamoto K, Ohmura M, Naka K, Hosokawa K, Ikeda Y, Suda T (2006) Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nature Med. 12, 446-251.
32. Ivell R, Balvers M, Anand RJK, Paust H-J, Mckinnell C, Sharpe R (2003) Differentiation-dependent expression of 17β-hydroxysteroid dehydrogenase, type 10, in the rodent testis: Effect of aging in Leydig cells. Endocrinology 144, 3130-3137.
33. Kang S, Jung M, Kim C-W, Shin D (2005) Inactivation of p38 kinase delays the onset of senescence in rabbit articular chondrocytes. Mech. Ageing Dev. 126, 591-597.
34. Kaufman JM, Vermeulen A (2005) The decline of androgen levels in elderly men and its clinical and therapeutic implications. Endocr. Rev. 26, 833-876.
35. Kelley L, Allan G, Azhar S (2004) High dietary fructose induces a hepatic stress response resulting in cholesterol and lipid dysregulation. Endocrinology 145, 548-555.
36. Kiritoshi S, Nishikawa T, Sonoda K, Kukidome D, Senokuchi T, Matsuo T, Matsumura T, Tokunaga H, Brownlee M, Araki E (2003) Reactive oxygen species from mitochondria induce cyclooxygenase-2 gene expression in human mesangial cells: Potential role in diabetic nephropathy. Diabetes 52, 2570-2577.
37. Kodaman PH, Aten RF, Behrman HR (1994) Lipid hydroperoxides evoke antigonadotropic and antisteroidogenic activity in rat luteal cells. Endocrinology 135, 2723-2730.
38. Kumagai T, Matsukawa N, Kaneko Y, Kusumi Y, Mitsumata M, Uchida K (2004) A lipid peroxidation-derived inflammatory mediator: Identifiaction of 4-hydroxy-2-nonenal as a potential inducer of cyclooxygenase-2 in macrophages. J. Boil. Chem. 279, 48389-48396.
39. Kyriakis JM, Avruch J (2001) Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81, 807-869.
40. Lamberts SWJ, van den Beld AW, van der Lely A-J (1997) The endocrinology of aging. Science 278, 419-424.
41. Lasa M, Mahtani KR, Finch A, Brewer G, Saklatvala J, Clark AR (2000) Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell. Biol. 20, 4265-4274.
42. Lee JC, Laydon JT, McDonnell PC, Gallagher TF, Kumar S, Green D, McNulty D, Blumenthal MJ, Heys JR, Landvatter SW, Strickler JE, McLaughlin MM, Siemens IR, Fisher SM, Livi GP, White JR, Adams JL, Young PR (1994) A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature (London) 372, 739-746.
43. Leers-Sucheta S, Stocco DM, Azhar S (1999) Down-regulation of steroidogenic acute regulatory (StAR) protein in rat Leydig cells: implications for regulation of testosterone production during aging. Mech. Ageing Dev. 107, 197-203.
44. Liao C, Reaven E, Azhar S (1993) Age-related decline in the steroidogenic capacity of isolated rat Rat Leydig cells: A defect in cholesterol mobilization and processing. J. Steroid Biochem. Molec. Biol. 64, 39-47.
45. Liu J, Li H, Padadopoulos V (2003) PAP7, a PBR/PKA-RIα-associated protein: A new element in the relay of the hormonal induction of steroidogenesis. J. Steroid Biochem. Mol. Biol. 85, 275-283.
46. Luo L, Chen H, Zirkin BR (2001) Leydig cell aging: Steroidogenic acute regulatory protein (StAR) and cholesterol side-chain cleavage enzyme. J. Androl. 22, 149-156.
47. Lykkesfeldt J (2007) Malondialdehyde as biomarker of oxidative damage to lipids caused by smoking. Clin. Chim. Acta 380, 50-58.
48. Manna PR, Stocco DM (2005) Regulation of steroidogenic acute regulatory protein expression: Functional and physiological consequences. Curr. Drug Targets Immune Endocr. Metabol. Disord. 5, 93-108.
49. Martindale JL, Holbrook NJ (2002) Cellular response to oxidative stress: Signaling for suicide and survival. J. Cell. Physiol. 192, 1-15.
50. Matsuzawa A, Ichijo H (2005) Stress-responsive protein kinases in redox-regulated apoptosis signaling. Antioxid. Redox Signal. 7, 472-481.
51. McCubrey JA, LaHair MM, Franklin RA (2006) Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid. Redox Signal. 8, 1775-1789.
52. McDermott EP, O'Neill LAJ (2002) Ras participates in the activation of p38 MAPK by interleukin-1 by associating with IRAK, IRAK2, TRAF6, and TAK-1. J. Biol. Chem. 277, 7808-7815.
53. Medicherla R, Leers-Sucheta S, Luo Y, Azhar S (2001) Impaired activation of AP-1 and altered expression of constitutive proteins in rat adrenal during aging. Mech. Ageing Dev. 122, 1169-1186.
54. Medicherla R, Leers-Sucheta S, Luo Y, Azhar S (2002) Age-dependent modulation of NF-kappaB expression in rat adrenal gland. Mech. Ageing Dev. 123, 1211-1227.
55. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
56. Musicki B, Aten RF, Behrman HR (1994) Inhibition of protein synthesis and hormone-sensitive steroidogenesis in response to hydrogen peroxide in rat luteal cells. Endocrinology 134, 588-595.
57. Nakamura T, Sakamoto K (2001) Reactive oxygen species up-regulates cyclooxygenase-2, 53, and Bax mRNA expression in bovine luteal cells. Biochem. Biophys. Res. Commun. 284, 203-210.
58. Natale DR, Paloga AJM, Beier F, D'Souza SJA, Watson AJ (2004) p38 MAPK signaling during murine preimplantation development. Dev. Biol. 268, 76-88.
59. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95, 351-358.
60. Page K, Li J, Hershenson MB (2001) p38 MAP kinase negatively regulates cyclin D1 expression in airway smooth muscle cells. Am. J. Physiol. Lung Cell Mol. Physiol. 280, L955-L964.
61. Pearson G, Robinson F, Gibson TB, Xu B, Karandikar M, Berman K, Cobb MH (2001) Mitogen-activated protein (MAP) kinase pathways: Regulation and physiological functions. Endocr. Rev. 22, 153-183.
62. Pimentel DR, Amin JK, Xiao L, Miller T, Viereck J, Oliver-krasinski J, Baliga R, Wang J, Siwik DA, Singh K, Pagano P, Colucci WS, Sawyer DB (2001) Reactive oxygen species mediate amplitude-dependent hypertrophic and apoptotic responses to mechanical stretch in cardiac myocytes. Circ. Res. 89, 453-460.
63. Popplewell PY, Azhar S (1987) Effects of aging on cholesterol content and cholesterol-metabolizing enzymes in the rat adrenal gland. Endocrinology 121, 64-73.
64. Popplewell PY, Tsubokawa M, Ramachandran J, Azhar S (1986) Differential effects of aging on adrenocorticotropin receptors, adenosine 3′5′-monophosphate response, and corticosterone secretion in adrenocortical cells from Sprague-Dawley rats. Endocrinology 119, 2206-2213.
65. Pramanik R, Qi X, Borowicz S, Choubey D, Schultz RM, Han J, Chen G (2003) p38 Isoforms have opposite effects on AP-1-dependent transcription through regulation of c-Jun: The determinant role of the isoforms in the MAPK signal specificity. J. Biol. Chem. 278, 4831-4839.
66. Pyles LA, Stejskal EJ, Einzig S (1993) Spectrophotometric measurement of plasma 2-thiobarbituric acid-reactive substances in the presence of hemoglobin and bilirubin interference. Proc. Soc. Exp. Biol. Med. 202, 407-419.
67. Reaven E, Kostrna M, Ramachandran J, Azhar S (1988) Structure and function changes in rat adrenal glands during aging. Am. J. Physiol. 255, E903-E911.
68. Shifren JL, Schiff I (2000) The aging ovary. J. Womens Health Gend. Based Med. 9 (Suppl. 1), S3-S7.
69. Uchida Y, Ohba K, Yoshioka T, Irie K, Muraki T, Maru Y (2004) Cellular carbonyl stress enhances the expression of plasminogen activator inhibitor-1 in rat white adipocytes via reactive oxygen species-dependent pathway. J. Biol. Chem. 279, 4075-4083.
70. Veldhuis JD, Veldhuis NJD, Keenan DM, Iranmanesh A (2005) Age diminishes the testicular steroidogenic response to repeated intravenous pulses of recombinant human LH during acute GnRH-receptor blockade in healthy men. Am. J. Physiol. Endocrinol. Metab. 288, E775-E781.
71. Wang X, Stocco DM (2005) The decline in testosterone biosynthesis during male aging: A consequence of multiple alterations. Mol. Cell. Endocrinol. 238, 1-7.
72. Wang X, Dyson MT, Jo Y, Stocco DM (2003) Inhibition of cyclooxygenase-2 activity enhances steroidogenesis and steroidogenic acute regulatory gene expression in MA-10 mouse Leydig cells. Endocrinology 144, 3368-3375.
73. Wu G, Fang Y-Z, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J. Nutr. 134, 489-492.
74. Yang T, Zhang A, Honeggar M, Kohn DE, Mizel D, Sanders K, Hoidal JR, Briggs JP, Schnermann JB (2005) Hypertonic induction of COX-2 in collecting duct cells by reactive oxygen species of mitochondrial origin. J. Biol. Chem. 280, 34966-34973.
75. Yang T, Zhang A, Pasumarthy A, Zhang L, Warnock Z, Schnermann JB (2006) Nitric oxide stimulates COX-2 expression in cultured collecting duct cells through MAP kinases and superoxide but not cGMP. Am. J. Physiol. Renal Physiol. 291, F891-F895.
76. Zirkin BR, Chen H (2000) Regulation of Leydig cell steroidogenic function during aging. Biol. Reprod. 63, 977-981.