Lactate regulates rat male germ cell function through reactive oxygen species

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Galardo, María Noel ^a   Regueira, Mariana ^a   Riera, María Fernanda ^a   Pellizzari, Eliana Herminia ^a   Cigorraga, Selva Beatriz ^a   Meroni, Silvina Beatriz ^a  

^a Centro de Investigaciones Endocrinologicas   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME INHIBITOR; LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE INHIBITOR; LACTIC ACID; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCARBOXYLATE TRANSPORTER 2; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EXPOSURE; GENE EXPRESSION REGULATION; GERM CELL; MALE; NONHUMAN; NORTHERN BLOTTING; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; GENE EXPRESSION REGULATION; LACTIC ACID; MALE; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SERTOLI CELLS; SIGNAL TRANSDUCTION; SPERMATOZOA;

EID: 84900436669     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088024     Document Type: Article

References (44)

1. Jutte NH, Grootegoed JA, Rommerts FF, van der Molen HJ (1981) Exogenous lactate is essential for metabolic activities in isolated rat spermatocytes and spermatids. J Reprod Fertil 62: 399-405. (Pubitemid 11034886)
2. Jutte NH, Jansen R, Grootegoed JA, Rommerts FF, Clausen OP, et al. (1982) Regulation of survival of rat pachytene spermatocytes by lactate supply from Sertoli cells. J Reprod Fertil 65: 431-438. (Pubitemid 12013236)
3. Hashimoto T, Hussien R, Oommen S, Gohil K, Brooks GA (2007) Lactate sensitive transcription factor network in L6 cells: activation of MCT1 and mitochondrial biogenesis. FASEB J 21: 2602-2612. (Pubitemid 47230688)
4. Bassenge E, Sommer O, Schwemmer M, Bünger R (2000) Antioxidant pyruvate inhibits cardiac formation of reactive oxygen species through changes in redox state. Am J Physiol Heart Circ Physiol 279: 2431-2438.
5. Brooks GA (2009) Cell-cell and intracellular lactate shuttles. J Physiol 587: 5591-5600.
6. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, et al. (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39: 44-84. (Pubitemid 44566469)
7. Ji AR, Ku SY, Cho MS, Kim YY, Kim YJ, et al. (2010) Reactive oxygen species enhance differentiation of human embryonic stem cells into mesendodermal lineage. Exp Mol Med 42: 175-186.
8. Loh K, Deng H, Fukushima A, Cai X, Boivin B, et al. (2009) Reactive oxygen species enhance insulin sensitivity. Cell Metab 10: 260-272.
9. Tai P, Ascoli M (2011) Reactive Oxygen Species (ROS) play a critical role in the cAMP-induced activation of Ras and the phosphorylation of Erk1/2 in Leydig cells. Mol Endocrinol 25: 885-893.
10. Grootegoed JA, Jansen R, van der Molen HJ (1986) Effect of glucose on ATP dephosphorylation in rat spermatids. J Reprod Fertil 77: 99-107. (Pubitemid 16071721)
11. Mita M, Hall PF (1982) Metabolism of round spermatids from rats: lactate as the preferred substrate. Biol Reprod 26: 445-455. (Pubitemid 12084772)
12. Nakamura M, Okinaga S, Arai K (1984) Metabolism of round spermatids: evidence that lactate is preferred substrate. Am J Physiol 247: 234-242.
13. Schteingart HF, Rivarola MA, Cigorraga SB (1989) Hormonal and paracrine regulation of gamma-glutamyl transpeptidase in rat Sertoli cells. Mol Cell Endocrinol 67: 73-80. (Pubitemid 19262898)
14. Towler MC, Fogarty S, Hawley SA, Pan DA, Martin DM, et al. (2008) A novel short splice variant of the tumour suppressor LKB1 is required for spermiogenesis. Biochem J 416: 1-14.
15. Mihara M, Uchiyama M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86: 271-278. (Pubitemid 9050395)
16. Han KY, Yang D, Chang EJ, Lee Y, Huang H, et al. (2007) Inhibition of osteoclast differentiation and bone resorption by sauchinone. Biochem Pharmacol 74: 911-923. (Pubitemid 47212083)
17. Hu S, Sheng WS, Schachtele JS, Lokensgard JR (2011) Reactive oxygen species drive herpes simplex virus (HSV)-1-induced proinflammatory cytokine production by murine microglia. J Neuroinflammation 8: 123.
18. Bröer S, Bröer A, Schneider HP, Stegen C, Halestrap AP, et al. (1999) Characterization of the high-affinity monocarboxylate transporter MCT2 in Xenopus laevis oocytes. Biochem J 341: 529-535. (Pubitemid 29389181)
19. Dimmer KS, Friedrich B, Lang F, Deitmer JW, Bröer S (2000) The low-affinity monocarboxylate transporter MCT4 is adapted to the export of lactate in highly glycolytic cells. Biochem J 350: 219-227.
20. Miles MF, Hung P, Jungmann RA (1981) Cyclic AMP regulation of lactate dehydrogenase. Quantitation of lactate dehydrogenase M-subunit messenger RNA in isoproterenol-and N6,O29-dibutyryl cyclic AMP-stimulated rat C6 glioma cells by hybridization analysis using a cloned cDNA probe. J Biol Chem 256: 12545-12552. (Pubitemid 12141522)
21. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193: 265-275.
22. Courtens JL, Plöen L (1999) Improvement of spermatogenesis in adult cryptorchid rat testis by intratesticular infusion of lactate. Biol Reprod 61: 154-161. (Pubitemid 29295980)
23. Wasserman K (1984) The anaerobic threshold measurement to evaluate exercise performance. Am Rev Respir Dis 129: 35-40.
24. Bouzier-Sore AK, Merle M, Magistretti PJ, Pellerin L (2002) Feeding active neurons: (re)emergence of a nursing role for astrocytes. J Physiol Paris 96: 273-282. (Pubitemid 36090365)
25. Liu C, Wu J, Zhu J, Kuei C, Yu J, et al. (2009) Lactate inhibits lipolysis in fat cells through activation of an orphan G-protein-coupled receptor, GPR81. J Biol Chem 284: 2811-2822.
26. Végran F, Boidot R, Michiels C, Sonveaux P, Feron O (2011) Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-κB/IL-8 pathway that drives tumor angiogenesis. Cancer Res 71: 2550-2560.
27. Garcia CK, Brown MS, Pathak RK, Goldstein JL (1995) cDNA cloning of MCT2, a second monocarboxylate transporter expressed in different cells than MCT1. J Biol Chem 270: 1843-1849.
28. Pellerin L, Bergersen LH, Halestrap AP, Pierre K (2005) Cellular and subcellular distribution of monocarboxylate transporters in cultured brain cells and in the adult brain. J Neurosci Res 79: 55-64. (Pubitemid 40116418)
29. Brauchi S, Rauch MC, Alfaro IE, Cea C, Concha II, et al. (2005) Kinetics, molecular basis, and differentiation of L-lactate transport in spermatogenic cells. Am J Physiol Cell Physiol 288: 523-534.
30. Markert CL, Shaklee JB, Whitt GS (1975) Evolution of a gene. Multiple genes for LDH isozymes provide a model of the evolution of gene structure, function and regulation. Science 189: 102-114.
31. Battellino LJ, Jaime FR, Blanco A (1968) Kinetic properties of rabbit testicular lactate dehydrogenase isozyme. J Biol Chem 243: 5185-5192.
32. Cummings JH (1984) Colonic absorption: the importance of short chain fatty acids in man. Scand. J Gastroenterol Suppl 93: 89-99.
33. Cuff MA, Lambert DW, Shirazi-Beechey SP (2002) Substrate-induced regulation of the human colonic monocarboxylate transporter, MCT1. J Physiol 539: 361-371. (Pubitemid 35175393)
34. Thannickal VJ, Fanburg BL (2000) Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279: 1005-1028.
35. Chen K, Kirber MT, Xiao H, Yang Y, Keaney JF (2008) Regulation of ROS signal transduction by NADPH oxidase 4 localization. J Cell Biol 181: 1129-1139. (Pubitemid 351915488)
36. Cai TQ, Ren N, Jin L, Cheng K, Kash S, et al. (2008) Role of GPR81 in lactate-mediated reduction of adipose lipolysis. Biochem Biophys Res Commun 377: 987-991.
37. Oeckler RA, Arcuino E, Ahmad M, Olson SC, Wolin MS (2005) Cytosolic NADH redox and thiol oxidation regulate pulmonary arterial force through ERK MAP kinase. Am J Physiol Lung Cell Mol Physiol 288: 1017-1025.
38. Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313. (Pubitemid 46209993)
39. Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4: 181-189.
40. Cheng G, Cao Z, Xu X, van Meir EG, Lambeth JD (2001) Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269: 131-140. (Pubitemid 32488913)
41. Bánfi B, Malgrange B, Knisz J, Steger K, Dubois-Dauphin M, et al. (2004) NOX3, a superoxide-generating NADPH oxidase of the inner ear. J Biol Chem 279: 46065-46072. (Pubitemid 39491600)
42. Opitz N, Drummond GR, Selemidis S, Meurer S, Schmidt HH (2007) The 'A's and 'O's of NADPH oxidase regulation: a commentary on "Subcellular localization and function of alternatively spliced Noxo1 isoforms". Free Radic Biol Med 42: 175-179. (Pubitemid 44959749)
43. Serrander L, Cartier L, Bedard K, Banfi B, Lardy B, et al. (2007) NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem J 406: 105-114. (Pubitemid 47264740)
44. Meroni SB, Schteingart HF, Pellizzari EH, Cigorraga SB (1995) Possible involvement of microfilaments in the regulation of Sertoli cell aromatase activity. Mol Cell Endocrinol 112: 69-75.