Cleavage of disulfide bonds in mouse spermatogenic cell-specific type 1 hexokinase isozyme is associated with increased hexokinase activity and initiation of sperm motility

Biology of Reproduction

Volumn 79, Issue 3, 2008, Pages 537-545

  Nakamura, Noriko ^a   Miranda Vizuete, Antonio ^b   Miki, Kiyoshi ^c   Mori, Chisato ^d   Eddy, Edward M ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b Universidad Pablo de Olavide   (Spain)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d CHIBA UNIVERSITY   (Japan)

Author keywords

Disulfide bond reduction; Epididymis; Fibrous sheath; Glycolysis; Sperm; Sperm activation; Sperm capacitation; Sperm maturation; Sperm motility and transport

Indexed keywords

DIAMIDE; ENZYME ANTIBODY; HEXOKINASE; HEXOKINASE TYPE 1; PHOSPHOTYROSINE; THIOREDOXIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVITY; EPIDIDYMIS TAIL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPERMATOZOON; SPERMATOZOON MOTILITY;

ADENOSINE TRIPHOSPHATE; ANIMALS; DIMERIZATION; DISULFIDES; ENZYME ACTIVATION; HEXOKINASE; ISOENZYMES; MALE; MICE; MODELS, BIOLOGICAL; ORGAN SPECIFICITY; OXIDATION-REDUCTION; PHOSPHORYLATION; PHOSPHOTYROSINE; SPERM CAPACITATION; SPERM MOTILITY; SPERMATOZOA; SULFHYDRYL COMPOUNDS;

EID: 50849130574     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.108.067561     Document Type: Article

References (50)

1. Yanagimachi R. Mammalian fertilization. In: Knobil E, Neill JD (eds.), The Physiology of Reproduction, 2nd ed. New York: Raven Press; 1994:189-317.
2. Inaba K. Molecular architecture of the sperm flagella: molecules for motility and signaling. Zool Sci 2003; 20:1043-1056.
3. Urner F, Sakkas D. Protein phosphorylation in mammalian spermatozoa. Reproduction 2003; 125:17-26.
4. McCarrey JR, Thomas K. Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 1987; 326:501-505.
5. Sakai I, Sharief FS, Li SSL. Molecular cloning and nucleotide sequence of the cDNA for sperm-specific lactate dehydrogenase-C from mouse. Biochem J 1987; 242:619-622.
6. Welch JE, Schatte EC, O'Brien DA, Eddy EM. Expression of a glyceraldehyde 3-phosphatase dehydrogenase gene specific to mouse spermatogenic cells. Biol Reprod 1992; 46:869-878.
7. Mori C, Welch JE, Fulcher KD, O'Brien DA, Eddy EM. Unique hexokinase messenger ribonucleic acids lacking the porin-binding domain are developmentally expressed in mouse spermatogenic cells. Biol Reprod 1993; 49:191-203.
8. Storey BT, Kayne FJ. Energy metabolism of spermatozoa. V. The Embden-Myerhof pathway of glycolysis: activities of pathway enzymes in hypotonically treated rabbit epididymal spermatozoa. Fertil Steril 1975; 26:1257-1265.
9. Miki K, Qu W, Goulding EH, Willis WD, Bunch DO, Strader LF, Perreault SD, Eddy EM, O'Brien DA. Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc Natl Acad Sci U S A 2004; 101:16501-16506.
10. Mori C, Nakamura N, Welch JE, Gotoh H, Goulding EH, Fujioka M, Eddy EM. Mouse spermatogenic cell-specific type 1 hexokinase mHk1-s transcripts are expressed by alternative splicing from the mHk1 gene and the HK1-S protein is localized mainly in the sperm tail. Mol Reprod Dev 1998; 49:374-385.
11. Nakamura N, Shibata H, O'Brien DA, Mori C, Eddy EM. Spermatogenic cell-specific type 1 hexokinase is the predominant hexokinase in sperm. Mol Reprod Dev 2008; 75:632-640.
12. Kalab P, Visconti P, Leclerc P, Kopf GS. p95, the major phosphotyrosine-containing protein in mouse spermatozoa, is a hexokinase with unique properties. J Biol Chem 1994; 269:3810-3817.
13. Visconti PE, Olds-Clarke P, Moss SB, Kalab P, Travis AJ, de las Heras M, Kopf GS. Properties and localization of a tyrosine phosphorylated form of hexokinase in mouse sperm. Mol Reprod Dev 1996; 43:82-93.
14. Wilson JE. Hexokinase. Rev Physiol Biochem Pharmacol 1995; 126:65-198.
15. Travis AJ, Jorgez CJ, Merdiushev T, Jones BH, Dess DM, Diaz-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.
16. Shalgi R, Seligman J, Kosower NS. Dynamics of the thiol status of rat spermatozoa during maturation: analysis with the fluorescent labeling agent monobromobimane. Biol Reprod 1989; 40:1037-1045.
17. Seligman J, Newton GL, Fahey RC, Shalgi R, Kosower NS. Nonprotein thiols and disulfides in rat epididymal spermatozoa and epididymal fluid: role of gamma-glutamyl-transpeptidase in sperm maturation. J Androl 2005; 26:629-637.
18. Joshi MD, Jagannathan V. Hexokinase I. Brain. Methods Enzymol 1966; 9:371-376.
19. Tsao T-S, Burcelin R, Charron MJ. Regulation of hexokinase II gene expression by glucose flux in skeletal muscle. J Biol Chem 1996; 271:14959-14963.
20. Kaneko T, Whittingham DG, Overstreet JW, Yanagimachi R. Tolerance of the mouse sperm nuclei to freeze-drying depends on their disulfide status. Biol Reprod 2003; 69:1859-1862.
21. Wollman EE, Auriol L, Rimsky L, Shaw A, Jacquot J-P, Wingfield P, Graber P, Dessarps F, Robin P, Galibert F, Bertoglio J, Fradeliz D. Cloning and expression of cDNA for human thioredoxin. J Biol Chem 1988; 263:15506-15512.
22. Mukai C, Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod 2004; 71:540-547.
23. Seligman J, Kosower NS, Weissberg R, Shalgi R. Thiol-disulfide states of human sperm proteins. J Reprod Fertil 1994; 101:435-443.
24. 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.
25. Narisawa S, Hecht NB, Goldberg E, Boatright KM, Reed JC, Millán JL. Testis-specific cytochrome c-null mice produce functional sperm but undergo early testicular atrophy. Mol Cell Biol 2002; 22:5554-5562.
26. Hoppe PC. Glucose requirement for mouse sperm capacitation in vitro. Biol Reprod 1976; 15:39-45.
27. 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.
28. Urner F, Sakkas D. Glucose participates in sperm-oocyte fusion in the mouse. Biol Reprod 1996; 55:917-922.
29. Williams AC, Ford WC. The role of glucose in supporting motility and capacitation in human spermatozoa. J Androl 2001; 22:680-695.
30. Rapoport S. Regulation of metabolism in red cells. Bibl Haematol 1968; 29:133-145.
31. Lowry OH, Passonneau JV. The relationships between substrates and enzymes of glycolysis in brain. J Biol Chem 1964; 239:31-42.
32. Sebastian S, Kenkare UW. Stimulation of brain hexokinase gene expression by recombinant brain insulin-like growth factor in C6 glial cells. Exp Cell Res 1999; 246:243-247.
33. Aleshin AE, Zeng C, Bourenkov GP, Bartunik HD, Fromm HJ, Honzatko RB. The mechanism of regulation of hexokinase: new insights from the crystal structure of recombinant human brain hexokinase complexed with glucose and glucose and glucose-6-phosphate. Structure 1998; 15:39-50.
34. Aleshin AE, Fromm HJ, Honzatko RB. Multiple crystal forms of hexokinase I: new insights regarding conformational dynamics, subunit interactions, and membrane association. FEBS Lett 1998; 434:42-46.
35. Aleshin AE, Zeng C, Bartunik HD, Fromm HJ, Honzatko RB. Regulation of hexokinase I: crystal structure of recombinant human brain hexokinase complexed with glucose and phosphate. J Mol Biol 1998; 282:345-347.
36. Tsai HJ, Wilson JE. Functional organization of mammalian hexokinases: characterization of chimeric hexokinases constructed from the N- and C-terminal domains of the rat type I and type II isozymes. Arch Biochem Biophys 1995; 316:206-214.
37. Mulichak AM, Wilson JE, Padmanabhan K, Garavito RM. The structure of mammalian hexokinase-1. Nat Struct Biol 1998; 5:555-560.
38. Luther MA, Gilbert HF, Lee JC. Self-association of rabbit muscle phosphofructokinase: role of subunit interaction in regulation of enzymatic activity. Biochemistry 1983; 22:5494-5500.
39. Tosic J, Walton A. Metabolism of spermatozoa. The formation and elimination of hydrogen peroxide by spermatozoa and effects on motility and survival. Biochem J 1950; 47:199-212.
40. Holland MK, Storey BT. Oxygen metabolism of mammalian spermatozoa. Generation of hydrogen peroxide by rabbit epididymal spermatozoa. Biochem J 1981; 198:273-280.
41. Aitken RJ, Clarkson JS. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil 1987; 81:459-469.
42. de Lamirande E, O'Flaherty C. Sperm activation: role of reactive species and kinases. Biochim Biophys Acta 2008; 1784:106-115.
43. Cornwall GA, Smyth TB, Vindivich D, Harter C, Robinson J, Chang TSK. Induction and enhancement of progress motility in hamster caput epidydimal spermatozoa. Biol Reprod 1986; 35:1065-1074.
44. Rietsch A, Beckwith J. The genetics of disulfide bond metabolism. Annu Rev Genet 1998; 32:163-184.
45. Arner ES, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 2000; 267:6102-6109.
46. Miranda-Vizuete A, Ljung J, Damdimopoulos AE, Gustafsson JA, Oko R, Pelto-Huikko M, Spyrou G. Characterization of Sptrx, a novel member of the thioredoxun family specifically expressed in human spermatozoa. J Biol Chem 2001; 276:31567-31574.
47. Alvarez JG, Storey BT. Lipid peroxidation and the reactions of superoxide and hydrogen peroxide in mouse spermatozoa. Biol Reprod 1984; 30:833-841.
48. Miranda-Vizuete A, Tsang K, Yu Y, Jiménez A, Pelto-Huikko M, Flickinger CJ, Sutovsky P, Oko R. Cloning and developmental analysis of murid spermatid-specific thioredoxin-2 (SPTRX-2), a novel sperm fibrous sheath protein and autoantigen. J Biol Chem 2003; 278:44874-44885.
49. Jimenez A, Zu W, Rawe VY, Pelto-Huikko M, Flickinger CJ, Sutovsky P, Gustafsson JA, Oko R, Miranda-Vizuete A. Spermatocyte/spermatid-specific thioredoxin-3, a novel Golgi apparatus-associated thioredoxin, is a specific marker of aberrant spermatogenesis. J Biol Chem 2004; 279:34971-34982.
50. Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P, Kopf GS. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 1995; 121:1129-1137.