Exogenous pyruvate accelerates glycolysis and promotes capacitation in human spermatozoa

Human Reproduction

Volumn 26, Issue 12, 2011, Pages 3249-3263

  Hereng, T H ^a   Elgstoen K B P ^b   Cederkvist, F H ^c,d   Eide, L ^b,d   Jahnsen, T ^a,d   Sklhegg, B S ^a,d   Rosendal, K R ^a  

^a Spermatech AS   (Norway)

^b Department of Medical Biochemistry ^*  (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d UNIVERSITY OF OSLO   (Norway)

Author keywords

capacitation; glycolysis; human spermatozoa; pyruvate; sperm metabolism

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALBUMIN; BICARBONATE; CARBON 13; GLUCOSE; LACTIC ACID; METHYLENE BLUE; OXAMIC ACID; PYRUVIC ACID; SODIUM CYANIDE;

ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; GLUCOSE METABOLISM; GLYCOLYSIS; HUMAN; HUMAN CELL; MALE; MALE FERTILITY; MITOCHONDRIAL RESPIRATION; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PROTEIN PHOSPHORYLATION; RESPIRATORY CHAIN; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY;

MAMMALIA;

EID: 81055132901     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/der317     Document Type: Article

References (64)

1. Adam DE, Wei J. Mass transport of ATP within the motile sperm. J Theor Biol 1975;49:125-145.
2. Adams MJ, Buehner M, Chandrasekhar K, Ford GC, Hackert ML, Liljas A, Rossmann MG, Smiley IE, Allison WS, Everse J et al. Structure-function relationships in lactate dehydrogenase. Proc Natl Acad Sci USA 1973; 70:1968-1972.
3. Andrae U, Singh J, Ziegler-Skylakakis K. Pyruvate and related alpha-ketoacids protect mammalian cells in culture against hydrogen peroxide-induced cytotoxicity. Toxicol Lett 1985;28:93-98.
4. Angulo C, Rauch MC, Droppelmann A, Reyes AM, Slebe JC, Delgado-Lopez F, Guaiquil VH, Vera JC, Concha II. Hexose transporter expression and function in mammalian spermatozoa: cellular localization and transport of hexoses and vitamin C. J Cell Biochem 1998;71:189-203.
5. Baker MA, Hetherington L, Aitken RJ. Identification of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa. J Cell Sci 2006;119:3182-3192.
6. Barbonetti A, Vassallo MR, Fortunato D, Francavilla S, Maccarrone M, Francavilla F. Energetic metabolism and human sperm motility: impact of CB1 receptor activation. Endocrinology 2010;151:5882-5892.
7. Blanco A, Zinkham WH. Lactate dehydrogenases in human testes. Science 1963;139:601-602.
8. Brand KA, Hermfisse U. Aerobic glycolysis by proliferating cells: a protective strategy against reactive oxygen species. FASEB J 1997; 11:388-395.
9. Burant CF, Takeda J, Brot-Laroche E, Bell GI, Davidson NO. Fructose transporter in human spermatozoa and small intestine is GLUT5. J Biol Chem 1992;267:14523-14526.
10. Burkman LJ. Discrimination between nonhyperactivated and classical hyperactivated motility patterns in human spermatozoa using computerized analysis. Fertil Steril 1991;55:363-371.
11. Calvin J, Tubbs PK. Mitochondrial transport processes and oxidation of NADH by hypotonically-treated boar spermatozoa. Eur J Biochem 1978;89:315-320.
12. Cao W, Aghajanian HK, Haig-Ladewig LA, Gerton GL. Sorbitol can fuel mouse sperm motility and protein tyrosine phosphorylation via sorbitol dehydrogenase. Biol Reprod 2009;80:124-133.
13. Carey JE, Olds-Clarke P, Storey BT. Oxidative metabolism of spermatozoa from inbred and random bred mice. J Exp Zool 1981;216:285-292.
14. Clausen J, Ovlisen B. Lactate dehydrogenase isoenzymes of human semen. Biochem J 1965;97:513-517.
15. Coronel CE, Burgos C, Gerez de Burgos NM, Rovai LE, Blanco A. Catalytic properties of the sperm-specific lactate dehydrogenase (LDH X or C4) from different species. J Exp Zool 1983;225:379-385.
16. Cummins JM, Woodall PF. On mammalian sperm dimensions. J Reprod Fertil 1985;75:153-175.
17. de Lamirande E, Gagnon C. Reactive oxygen species and human spermatozoa. II. Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility. J Androl 1992; 13:379-386.
18. Demott RP, Suarez SS. Hyperactivated sperm progress in the mouse oviduct. Biol Reprod 1992;46:779-785.
19. Dickens CJ, Maguiness SD, Comer MT, Palmer A, Rutherford AJ, Leese HJ. Human tubal fluid: formation and composition during vascular perfusion of the fallopian tube. Hum Reprod 1995;10:505-508.
20. Ford WC. Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round. Hum Reprod Update 2006;12:269-274.
21. Ford WC, Harrison A. The role of oxidative phosphorylation in the generation of ATP in human spermatozoa. J Reprod Fertil 1981; 63:271-278.
22. Fraser LR, Quinn PJ. A glycolytic product is obligatory for initiation of the sperm acrosome reaction and whiplash motility required for fertilization in the mouse. J Reprod Fertil 1981;61:25-35.
23. Gardner DK, Lane M, Calderon I, Leeton J. Environment of the preimplantation human embryo in vivo: metabolite analysis of oviduct and uterine fluids and metabolism of cumulus cells. Fertil Steril 1996; 65:349-353.
24. Goldberg E. Lactic and malic dehydrogenases in human spermatozoa. Science 1963;139:602-603.
25. Haber RS, Weinstein SP, O'Boyle E, Morgello S. Tissue distribution of the human GLUT3 glucose transporter. Endocrinology 1993; 132:2538-2543.
26. Halangk W, Bohnensack R. Quantification of sperm motility by a turbidimetric assay. Correlation to cellular respiration. Biomed Biochim Acta 1986;45:331-341.
27. Halangk W, Bohnensack R, Frank K, Kunz W. Effect of various substrates on mitochondrial and cellular energy state of intact spermatozoa. Biomed Biochim Acta 1985;44:411-420.
28. Ho HC, Granish KA, Suarez SS. Hyperactivated motility of bull sperm is triggered at the axoneme by Ca2+ and not cAMP. Dev Biol 2002; 250:208-217.
29. Hoshi K, Tsukikawa S, Sato A. Importance of Ca2+, K+ and glucose in the medium for sperm penetration through the human zona pellucida. Tohoku J Exp Med 1991;165:99-104.
30. Hung PH, Miller MG, Meyers SA, Vandevoort CA. Sperm mitochondrial integrity is not required for hyperactivated motility, zona binding, or acrosome reaction in the rhesus macaque. Biol Reprod 2008; 79:367-375.
31. Hutson SM, Van DC, Lardy HA. Mitochondrial metabolism of pyruvate in bovine spermatozoa. J Biol Chem 1977;252:1309-1315.
32. Jones AR, Chantrill LA, Cokinakis A. Metabolism of glycerol by mature boar spermatozoa. J Reprod Fertil 1992;94:129-134.
33. Kim YH, Haidl G, Schaefer M, Egner U, Mandal A, Herr JC. Compartmentalization of a unique ADP/ATP carrier protein SFEC (Sperm Flagellar Energy Carrier, AAC4) with glycolytic enzymes in the fibrous sheath of the human sperm flagellar principal piece. Dev Biol 2007;302:463-476.
34. Krisfalusi M, Miki K, Magyar PL, O'Brien DA. Multiple glycolytic enzymes are tightly bound to the fibrous sheath of mouse spermatozoa. Biol Reprod 2006;75:270-278.
35. LeVan KM, Goldberg E. Properties of human testis-specific lactate dehydrogenase expressed from Escherichia coli. Biochem J 1991; 273(Pt 3):587-592.
36. Mahadevan MM, Miller MM, Moutos DM. Absence of glucose decreases human fertilization and sperm movement characteristics in vitro. Hum Reprod 1997;12:119-123.
37. Mukai C, Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod 2004;71:540-547.
38. Mukai C, Bergkvist M, Nelson JL, Travis AJ. Sequential reactions of surface-tethered glycolytic enzymes. Chem Biol 2009;16:1013-1020.
39. Murdoch RN, White IG. Studies of the metabolism of human spermatozoa. J Reprod Fertil 1968;16:351-361.
40. Nascimento JM, Shi LZ, Tam J, Chandsawangbhuwana C, Durrant B, Botvinick EL, Berns MW. Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers, and real-time automated tracking and trapping. J Cell Physiol 2008; 217:745-751.
41. Nevo AC, Rikmenspoel R. Diffusion of ATP in sperm flagella. J Theor Biol 1970;26:11-18.
42. Nolan MA, Babcock DF, Wennemuth G, Brown W, Burton KA, McKnight GS. Sperm-specific protein kinase A catalytic subunit Calpha2 orchestrates cAMP signaling for male fertility. Proc Natl Acad Sci USA 2004;101:13483-13488.
43. Odet F, Duan C, Willis WD, Goulding EH, Kung A, Eddy EM, Goldberg E. Expression of the gene for mouse lactate dehydrogenase C (Ldhc) is required for male fertility. Biol Reprod 2008;79:26-34.
44. Odet F, Gabel SA, Williams J, London RE, Goldberg E, Eddy EM. Lactate dehydrogenase C (LDHC) and energy metabolism in mouse sperm. Biol Reprod 2011;85:556-564.
45. Rigau T, Farre M, Ballester J, Mogas T, Pena A, Rodriguez-Gil JE. Effects of glucose and fructose on motility patterns of dog spermatozoa from fresh ejaculates. Theriogenology 2001;56:801-815.
46. Rodriguez-Paez L, Guzman-Ibarra R, cuna-Gonzalez C, Santillan-Baez A, Moreno-Rodriguez R, Wong C. The study of N-isopropyl oxamate on sperm motility and fertility, in mice. Proc West Pharmacol Soc 2002; 45:171-173.
47. Rogers BJ, Perreault SD. Importance of glycolysable substrates for in vitro capacitation of human spermatozoa. Biol Reprod 1990;43: 1064-1069.
48. Ruiz-Pesini E, Lapena AC, Diez-Sanchez C, Perez-Martos A, Montoya J, Alvarez E, Diaz M, Urries A, Montoro L, Lopez-Perez MJ et al. Human mtDNA haplogroups associated with high or reduced spermatozoa motility. Am J Hum Genet 2000;67:682-696.
49. Ruiz-Pesini E, ez-Sanchez C, Lopez-Perez MJ, Enriquez JA. The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is this a purely glycolytic process? Curr Top Dev Biol 2007;77:3-19.
50. Sevcik P, Dunford HB. Kinetics of the oxidation of NADH by methylene-blue in a closed system. J Phys Chem 1991;95:2411-2415.
51. Sevcik P, Dunford B. The rate-constant for aerial oxidation of NADH by methylene-blue. Int J Chem Kinet 1995;27:925-928.
52. Stauss CR, Votta TJ, Suarez SS. Sperm motility hyperactivation facilitates penetration of the hamster zona pellucida. Biol Reprod 1995; 53:1280-1285.
53. Storey BT. Effect of ionophores and inhibitors and uncouplers of oxidative phosphorylation on sperm respiration. Arch Androl 1978;1:169-177.
54. Storey BT. Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol 2008;52:427-437.
55. Storey BT, Kayne FJ. Energy metabolism of spermatozoa. VI. Direct intramitochondrial lactate oxidation by rabbit sperm mitochondria. Biol Reprod 1977;16:549-556.
56. Sukcharoen N, Keith J, Irvine DS, Aitken RJ. Definition of the optimal criteria for identifying hyperactivated human spermatozoa at 25 Hz using in-vitro fertilization as a functional end-point. Hum Reprod 1995; 10:2928-2937.
57. Tay JI, Rutherford AJ, Killick SR, Maguiness SD, Partridge RJ, Leese HJ. Human tubal fluid: production, nutrient composition and response to adrenergic agents. Hum Reprod 1997;12:2451-2456.
58. Travis AJ, Jorgez CJ, Merdiushev T, Jones BH, Dess DM, az-Cueto L, Storey BT, Kopf GS, Moss SB. Functional relationships between capacitation-dependent cell signaling and compartmentalized metabolic pathways in murine spermatozoa. J Biol Chem 2001; 276:7630-7636.
59. Turner RM. Tales from the tail: what do we really know about sperm motility? J Androl 2003;24:790-803.
60. Van DC, Hutson SM, Lardy HA. Pyruvate metabolism in bovine epididymal spermatozoa. J Biol Chem 1977;252:1303-1308.
61. Way JL. Cyanide intoxication and its mechanism of antagonism. Annu Rev Pharmacol Toxicol 1984;24:451-481.
62. Williams AC, Ford WC. The role of glucose in supporting motility and capacitation in human spermatozoa. J Androl 2001;22:680-695.
63. Wong C, Rodriguez-Paez L, Nogueda B, Perez A, Baeza I. Selective inhibition of the sperm-specific lactate dehydrogenase isozyme-C4 by N-isopropyl oxamate. Biochim Biophys Acta 1997; 1343:16-22.
64. Zinkham WH, Blanco A, Clowry LJ Jr. An unusual isozyme of lactate dehydrogenase in mature testis: localization, ontogeny, and kinetic properties. Ann NY Acad Sci 1964;121: 571-588.