Sirtuin 4 Regulates Lipopolysaccharide Mediated Leydig Cell Dysfunction

Journal of Cellular Biochemistry

Volumn 117, Issue 4, 2016, Pages 904-916

  Ramatchandirin, Balamurugan ^a   Sadasivam, Mohanraj ^a   Kannan, Arun ^a   Prahalathan, Chidambaram ^a  

^a BHARATHIDASAN UNIVERSITY   (India)

Author keywords

APOPTOSIS; LEYDIG CELLS; LPS; SIRT4; STEROIDOGENESIS

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; 3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE TRIPHOSPHATE; BACTERIUM LIPOPOLYSACCHARIDE; CASPASE 3; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOOXYGENASE 2; INTERLEUKIN 6; LIVER RECEPTOR HOMOLOG 1; MESSENGER RNA; MITOCHONDRIAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BAX; RESVERATROL; SIRTUIN 1; SIRTUIN 2; SIRTUIN 3; SIRTUIN 4; SIRTUIN 5; SIRTUIN 6; SIRTUIN 7; STEROIDOGENIC ACUTE REGULATORY PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TESTOSTERONE 17BETA DEHYDROGENASE; TUMOR NECROSIS FACTOR ALPHA; 3 (OR 17)-BETA-HYDROXYSTEROID DEHYDROGENASE; ANTIOXIDANT; GLUTATHIONE; HYDROXYSTEROID DEHYDROGENASE; LIPOPOLYSACCHARIDE; SIRT5 PROTEIN, RAT; SIRTUIN; STILBENE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL FUNCTION; CELLULAR DISTRIBUTION; CLINICAL ASSESSMENT; COMPARATIVE STUDY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; ENZYME ACTIVATION; GENE EXPRESSION; GENE REPRESSION; LEYDIG CELL; LEYDIG CELL DYSFUNCTION; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEROIDOGENESIS; TESTIS DISEASE; TESTIS FUNCTION; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRION; SIGNAL TRANSDUCTION;

17-HYDROXYSTEROID DEHYDROGENASES; 3-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CELL LINE; CELL SURVIVAL; GENE EXPRESSION REGULATION; GLUTATHIONE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LEYDIG CELLS; LIPOPOLYSACCHARIDES; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; RATS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIRTUINS; STILBENES;

EID: 84958211715     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25374     Document Type: Article

References (45)

1. Aggarwal BB,. 2003. Signalling pathways of the TNF superfamily: A double-edged sword. Nat Rev Immunol 3: 745-756.
2. Aggarwal S, Dimitropoulou C, Lu Q, Black SM, Sharma S,. 2012. Glutathione supplementation attenuates lipopolysaccharide-induced mitochondrial dysfunction and apoptosis in a mouse model of acute lung injury. Front Physiol 28: 161.
3. Ahn SW, Gang GT, Tadi S, Nedumaran B, Kim YD, Park JH, Kweon GR, Koo SH, Lee K, Ahn RS, Yim YH, Lee CH, Harris RA, Choi HS,. 2012. Phosphoenolpyruvatecarboxykinase and glucose-6-phosphatase are required for steroidogenesis in testicular Leydig cells. J Biol Chem 7: 41875-41887.
4. Ahuja N, Schwer B, Carobbio S, Waltregny D, North BJ, Castronovo V, Maechler P, Verdin E,. 2007. Regulation of insulin secretion by SIRT4, a mitochondrial ADP-ribosyltransferase. J Biol Chem 16: 33583-33592.
5. Allen JA, Diemer T, Janus P, Hales KH, Hales DB,. 2004. Bacterial endotoxin lipopolysaccharide and reactive oxygen species inhibit Leydig cell steroidogenesis via perturbation of mitochondria. Endocrine 25: 265-275.
6. Allen JA, Shankara T, Janus P, Buck S, Diemer T, Hales KH, Hales DB,. 2006. Energized, polarized, and actively respiring mitochondria are required for acute Leydig cell steroidogenesis. Endocrinology 147: 3924-3935.
7. An H, Yu Y, Zhang M, Xu H, Qi R, Yan X, Liu S, Wang W, Guo Z, Guo J, Qin Z, Cao X,. 2002. Involvement of ERK, p38 and NF-kappaB signal transduction in regulation of TLR2, TLR4 and TLR9 gene expression induced by lipopolysaccharide in mouse dendritic cells. Immunology 106: 38-45.
8. Atmaca G,. 2004. Antioxidant effects of sulfur-containing amino acids. Yonsei Med J 45: 776-788.
9. Bergmeyer HU,. 1974. Steroid dehydrogenase. In:, Bergmeyer HU, editor. Methods of Enzymatic Analysis. New York: Academic Press. p 476.
10. Chen L, Daum G, Forough R, Clowes M, Walter U, Clowes AW,. 1998. Overexpression of human endothelial nitric oxide synthase in rat vascular smooth muscle cells and in balloon-injured carotid artery. Circ Res 82: 862-870.
11. Chen Y, Wang H, Luo G, Dai X,. 2014. SIRT4 inhibits cigarette smoke extracts-induced mononuclear cell adhesion to human pulmonary microvascular endothelial cells via regulating NF-κB activity. Toxicol Lett 2: 320-327.
12. Dali-Youcef N, Lagouge M, Froelich S, Koehl C, Schoonjans K, Auwerx J, Sirtuins,. 2007. The 'magnificent seven', function, metabolism and longevity. Ann Med 39: 335-345.
13. de Moura MB, Uppala R, Zhang Y, Van Houten B, Goetzman ES,. 2014. Overexpression of mitochondrial sirtuins alters glycolysis and mitochondrial function in HEK293 cells. PLoS One 9: e106028.
14. de Ronde W, de Jong FH,. 2011. Aromatase inhibitors in men: Effects and therapeuticoptions. Reprod Biol Endocrinol 21: 93.
15. 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 steroidogenesis. Endocrinology 144: 2882-2891.
16. Ellman GL,. 1959. Tissue sulfhydryl groups. Arch Biochem Biophys 82: 70-77.
17. Gautam DK, Misro MM, Chaki SP, Sehgal N,. 2006. H2O2 at physiological concentrations modulatesLeydig cell function inducing oxidative stress and apoptosis. Apoptosis 11: 39-46.
18. Hales DB, Diemer T, Hales KH,. 1999. Role of cytokines in testicular function. Endocrine 10: 201-217.
19. Ho L, Titus AS, Banerjee KK, George S, Lin W, Deota S, Saha AK, Nakamura K, Gut P, Verdin E, Kolthur-Seetharam U,. 2013. SIRT4 regulates ATP homeostasis and mediates a retrograde signaling via AMPK. Aging (Albany NY) 5: 835-849.
20. Jang JY, Choi Y, Jeon YK, Kim CW,. 2008. Suppression of adenine nucleotide translocase-2 by vector-based siRNA in human breast cancer cells induces apoptosis and inhibits tumor growth in vitro and in vivo. Breast Cancer Res 10: R11.
21. Jeong SM, Xiao C, Finley LW, Lahusen T, Souza AL, Pierce K, Li YH, Wang X, Laurent G, German NJ, Xu X, Li C, Wang RH, Lee J, Csibi A, Cerione R, Blenis J, Clish CB, Kimmelman A, Deng CX, Haigis MC,. 2013. SIRT4 has tumor-suppressive activity and regulates the cellular metabolic response to DNA damage by inhibiting mitochondrial glutamine metabolism. Cancer Cell 15: 450-463.
22. Kim HS, Je JH, Son TG, Park HR, Ji ST, Pokharel YR, Jeon HM, Kang KW, Kang HS, Chang SC, Kim HS, Chung HY, Lee J,. 2012. The hepatoprotective effects of adenine nucleotide translocator-2 against aging and oxidative stress. Free Radic Res 46: 21-29.
23. Kretova M, Sabova L, Hodny Z, Bartek J, Kollarovic G, Nelson BD, Hubackova S, Luciakova K,. 2014. TGF-β/NF1/Smad4-mediated suppression of ANT2 contributes to oxidative stress in cellular senescence. Cell Signal 26: 2903-2911.
24. LeBel CP, Ischiropoulos H, Bondy SC,. 1992. Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5: 227-231.
25. Li GC, Li LG, Liu YK, Mak JY, Chen LL, Lee WM,. 1991. Thermal response of rat fibroblasts stably transfected with the human 70-kDa heat shock protein-encoding gene. Proc Natl Acad Sci 88: 1681-1685.
26. Liu B, Che W, Xue J, Zheng C, Tang K, Zhang J, Wen J, Xu Y,. 2013. SIRT4 prevents hypoxia-induced apoptosis in H9c2 cardiomyoblast cells. Cell Physiol Biochem 32: 655-662.
27. Magata F, Horiuchi M, Echizenya R, Miura R, Chiba S, Matsui M, Miyamoto A, Kobayashi Y, Shimizu T,. 2014. Lipopolysaccharide in ovarian follicular fluid influencesthe steroid production in large follicles of dairy cows. Anim Reprod Sci 10: 6-13.
28. Metukuri MR, Reddy CM, Reddy PR, Reddanna P,. 2010. Bacterial LPS-mediated acute inflammation-induced spermatogenic failure in rats: Role of stress response proteins and mitochondrial dysfunction. Inflammation 33: 235-243.
29. Midzak AS, Chen H, Aon MA, Papadopoulos V, Zirkin BR,. 2011. ATP synthesis, mitochondrial function, and steroid biosynthesis in rodent primary and tumor Leydig cells. Biol Reprod 84: 976-985.
30. Mishra DP, Dhali A,. 2007. Endotoxin induces luteal cell apoptosis through the mitochondrial pathway. Prostaglandins Other Lipid Mediat 83: 75-88.
31. Mueller M, Cima I, Noti M, Fuhrer A, Jakob S, Dubuquoy L, Schoonjans K, Brunner T,. 2006. The nuclear receptor LRH-1 critically regulates extra-adrenal glucocorticoid synthesis in the intestine. J Exp Med 4: 2057-2062.
32. Nasrin N, Wu X, Fortier E, Feng Y, Bare' OC, Chen S, Ren X, Wu Z, Streeper RS, Bordone L,. 2010. SIRT4 regulates fatty acid oxidation and mitochondrial gene expression in liver and muscle cells. J Biol Chem 15: 31995-32002.
33. O'Bryan MK, Schlatt S, Phillips DJ, de Kretser DM, Hedger MP,. 2000. Bacterial lipopolysaccharide-induced inflammation compromises testicular function at multiple levels in vivo. Endocrinology 141: 238-246.
34. Reddy MM, Mahipal SV, Subhashini J, Reddy MC, Roy KR, Reddy GV, Reddy PR, Reddanna P,. 2006. Bacterial lipopolysaccharide-induced oxidative stress in the impairment of steroidogenesis and spermatogenesis in rats. Reprod Toxicol 22: 493-500.
35. Sadasivam M, Ramatchandirin B, Ayyanar A, Prahalathan C,. 2014. Bacterial lipopolysaccharide differently modulates steroidogenic enzymes gene expressions in the brain and testis in rats. Neurosci Res 83: 81-88.
36. Sadasivam M, Ramatchandirin B, Balakrishnan S, Prahalathan C,. 2015. TNF-α-mediatedsuppression of Leydig cell steroidogenesis involves DAX-1. Inflamm Res 64: 549-556.
37. Sharma AC, Bosmann HB, Motew SJ, Hales KH, Hales DB, Ferguson JL,. 1996. Steroid hormone alterations following induction of chronic intraperitoneal sepsis in male rats. Shock 6: 150-154.
38. Shivanandappa T, Venkatesh S,. 1997. A colorimetric assay method for 3beta-hydroxy-delta5-steroid dehydrogenase. Anal Biochem 254: 57-61.
39. Shoba B, Lwin ZM, Ling LS, Bay BH, Yip GW, Kumar SD,. 2009. Function of sirtuins in biological tissues. Anat Rec (Hoboken) 292: 536-543.
40. Stocco DM, Wang X, Jo Y, Manna PR,. 2005. Multiple signaling pathways regulating steroidogenesis and steroidogenic acute regulatory protein expression: More complicated than we thought. Mol Endocrinol 19: 2647-2659.
41. Tao Y, Huang C, Huang Y, Hong L, Wang H, Zhou Z, Qiu Y,. 2014. SIRT4 suppresses inflammatory responses in human umbilical vein endothelial cells. CardiovascToxicol 15: 217-223.
42. Venteclef N, Smith JC, Goodwin B, Delerive P,. 2006. Liver receptor homolog 1 is a negative regulator of the hepatic acute-phase response. Mol Cell Biol 26: 6799-6807.
43. Wallach D, Varfolomeev EE, Malinin NL, Goltsev YV, Kovalenko AV, Boldin MP,. 1999. Tumor necrosis factor receptor and Fas signaling mechanisms. Annu Rev Immunol 17: 331-367.
44. Wu L, Zhang A, Sun Y, Zhu X, Fan W, Lu X, Yang Q, Feng Y,. 2012. Sirt1 exerts anti-inflammatory effects and promotes steroidogenesis in Leydig cells. Fertil Steril 98: 194-199.
45. Yu W, Fu YC, Zhou XH, Chen CJ, Wang X, Lin RB, Wang W,. 2009. Effects of resveratrol on H(2)O(2)-induced apoptosis and expression of SIRTs in H9c2 cells. J Cell Biochem 1: 741-747.