Glycolytic enzyme activity is essential for domestic cat (Felis catus) and cheetah (Acinonyx jubatus) sperm motility and viability in a sugar-free medium

Biology of Reproduction

Volumn 84, Issue 6, 2011, Pages 1198-1206

  Terrell, Kimberly A ^a,b   Wildt, David E ^a   Anthony, Nicola M ^b   Bavister, Barry D ^c   Leibo, S P ^b   Penfold, Linda M ^d   Marker, Laurie L ^e   Crosier, Adrienne E ^a  

^a SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^b University of New Orleans   (United States)

^c UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^d WHITE OAK CONSERVATION CENTER   (United States)

^e CHEETAH CONSERVATION FUND   (Namibia)

Author keywords

chlorohydrin; Assisted reproductive technology; Endogenous substrates; Gamete biology; Glycerol; Glycogen; Glycolysis; Lactate; Male sexual function; Metabolic inhibition; Oxidative metabolism; Sodium oxamate; Sperm metabolism; Sperm motility and transport; Spermatozoa

Indexed keywords

ALPHA CHLOROHYDRIN; GLUCOSE; LACTATE DEHYDROGENASE; PYRUVIC ACID;

ACINONYX JUBATUS; ANIMAL CELL; ARTICLE; CAT; CHEETAH; CONTROLLED STUDY; ENERGY YIELD; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SYNTHESIS; FELIS CATUS; GLYCOLYSIS; MALE; NONHUMAN; PRIORITY JOURNAL; SEMEN ANALYSIS; SPECIES COMPARISON; SPERM RETRIEVAL; SPERMATOZOON MOTILITY;

ACINONYX; ANIMALS; CATS; CULTURE MEDIA; GLUCOSE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE (PHOSPHORYLATING); L-LACTATE DEHYDROGENASE; MALE; SEMEN PRESERVATION; SPERM MOTILITY;

ACINONYX JUBATUS; FELIDAE; FELIS CATUS;

EID: 79958235655     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.090225     Document Type: Article

References (65)

1. Mukai C, Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod 2004; 71:540-547
2. Turner R. Tales from the tail: what do we really know about sperm motility? J Androl 2003; 24:790-803
3. 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
4. Ford WCL, Rees JM. The bioenergetics of mammalian sperm motility. In: Gagnon C (ed.), Controls of Sperm Motility: Biological and Clinical Aspects. Boca Raton, FL: CRC Press; 1990:175-202
5. Williams AC, Ford WC. The role of glucose in supporting motility and capacitation in human spermatozoa. J Androl 2001; 22:680-695
6. Albarracín JL, Fernández-Novell JP, Ballester J, Rauch MC, Quintero- Moreno A, Peña A, Mogas T, Rigau T, Yañez A, Guinovart JJ, Slebe JC, Concha II, et al. Gluconeogenesis-linked glycogen metabolism is important in the achievement of in vitro capacitation of dog spermatozoa in a medium without glucose. Biol Reprod 2004; 71:1437-1445
7. Leese HJ, Astley NR, Lambert D. Glucose and fructose utilization by rat spermatozoa within the uterine lumen. J Reprod Fertil 1981; 61:435-437
8. Lardy HA, Phillips PH. Inhibition of sperm respiration and reversibility of the effects of metabolic inhibitors. J Biol Chem 1943; 148:333-341
9. Storey B. Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol 2008; 52:427-437
10. Lardy HA, Winchester B, Phillips PH. The respiratory metabolism of ram spermatozoa. Arch Biochem 1945; 6:33-40
11. 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
12. Macleod J. The effect of glycolysis inhibitors and of certain substrates on the metabolism and motility of human spermatozoa. Endocrinology 1941; 29:583-591
13. Hung P, 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
14. MacLeod J. The metabolism of human spermatozoa. Am J Physiol 1941; 132:193-201
15. Rigau T, Farré M, Ballester J, Mogas T, Peña A, Rodríguez-Gil JE. Effects of glucose and fructose on motility patterns of dog spermatozoa from fresh ejaculates. Theriogenology 2001; 56:801-815.
16. Rigau T, Rivera M, Palomo MJ, Fernández-Novell JM, Mogas T, Ballester J, Peña A, Otaegui PJ, Guinovart JJ, Rodríguez-Gil JE. Differential effects of glucose and fructose on hexose metabolism in dog spermatozoa. Reproduction 2002; 123:579-591.
17. Voet D, Voet JG. Glycolysis. In: Harris D, Fitzgerald P (eds.), Biochemistry, 3rd ed. Hoboken, NJ: John Wiley & Sons; 2004:581-624. 18
18. Westhoff D, Kamp G. Glyceraldehyde 3-phosphate dehydrogenase is bound to the fibrous sheath of mammalian spermatozoa. J Cell Sci 1997; 110:1821-1829.
19. Travis AJ, Foster JA, Rosenbaum NA, Visconti PE, Gerton GL, Kopf GS, Moss SB. Targeting of a germ cell-specific type 1 hexokinase lacking a porin-binding domain to the mitochondria as well as to the head and fibrous sheath of murine spermatozoa. Mol Cell Biol 1998; 9:263-276
20. Storey B, Kayne FJ. Energy metabolism of spermatozoa. V. The Embden-Meyerhof pathway of glycolysis: activities of the pathway enzymes in hypertonically treated rabbit epididymal spermatozoa. Fertil Steril 1975; 26:1257-1265
21. Bradley M, Geelan A, Leitch V, Goldberg E. Cloning sequencing and characterization of LDH-C-4 from a fox testis cDNA library. Mol Reprod Dev 1996; 44:452-459
22. Fraser LR, Herod JE. Expression of capacitation-dependent changes in chlorotetracycline fluorescence patterns in mouse spermatozoa requires a suitable glycolysable substrate. J Reprod Fertil 1990; 88:611-621
23. Hoppe PC. Glucose requirement for mouse sperm capacitation in vitro. Biol Reprod 1976; 15:39-45
24. Cooper T. The onset and maintenance of hyperactivated motility of spermatozoa from the mouse. Gamete Res 1984; 9:55-74
25. Fraser L, Quinn P. A glycolytic product is obligatory for initiation of thesperm acrosome reaction and whiplash motility required for fertilization in the mouse. J Reprod Fertil 1981; 61:25-35
26. Travis AJ, Tutuncu L, Jorgez C, Ord T, Jones B, Kopf GS, Williams C. Requirements for glucose beyond sperm capacitation during in vitro fertilization in the mouse. Biol Reprod 2004; 71:139-145
27. Terrell KA, Wildt DE, Anthony NM, Bavister BD, Leibo SP, Penfold LM, Marker LL, Crosier AE. Evidence for compromised metabolic function and limited glucose uptake in spermatozoa from the teratospermic domestic cat (Felis catus) and cheetah (Acinonyx jubatus). Biol Reprod 2010; 83:833-841
28. Long JA, Wildt DE, Wolfe BA, Crister JK, DeRossi RV, Howard JG. Sperm capacitation and the acrosome reaction are compromised in teratospermic domestic cats. Biol Reprod 1996; 54:638-646
29. Pukazhenthi BS, Wildt DE, Ottinger MA, Howard JG. Compromised sperm protein phosphorylation after capacitation, swim-up, and zona pellucida exposure in teratospermic domestic cats. J Androl 1996; 17:409-419
30. Pukazhenthi BS, Long JA, Wildt DE, Ottinger MA, Armstrong DL, Howard JG. Regulation of sperm function by protein tyrosine phosphorylation in diverse wild felid species. J Androl 1998; 19:675-685
31. Howard JG, Donoghue AM, Johnston LA, Wildt DE. Zona pellucida filtration of structurally abnormal spermatozoa and reduced fertilization in teratospermic cats. Biol Reprod 1993; 49:131-139
32. Ballester J, Fernández-Novell JP, Rutllant J, García-Rocha M, Palomo MJ, Mogas T, Peña A, Rigau T, Guinovart JJ, Rodríguez-Gil JE. Evidence for a functional glycogen metabolism in mature mammalian spermatozoa. Mol Reprod Dev 2000; 56:207-219.
33. Carey JE, Oldsclarke P, Storey BT. Oxidative metabolism of spermatozoa from inbred and random bred mice. J Exp Zool 1981; 216:285-292
34. Lardy HA, Phillips PH. Phospholipids as a source of energy for motility of bull spermatozoa. Am J Physiol 1941; 134:542-548
35. Jones AR, Milmlow D. Endogenous energy production by mature boar spermatozoa. J Reprod Fertil 1997; 111:285-290
36. Cooper TG, Noonan E, von Eckardstein S, Auger J, Gordon Baker HW, Behre HM, Haugen TB, Kruger T, Wang C, Mbizvo MT, Vogelsong KM. World Health Organization reference values for human semen characteristics. Hum Reprod Update 2010; 16:231-245
37. Pukazhenthi BS, Wildt DE, Howard JG. The phenomenon and significance of teratospermia in felids. J Reprod Fertil Suppl 2001; 57:423-433
38. Wildt DE, Bush M, Howard JG, O'Brien SJ, Meltzer D, van Dyk A, Ebedes H, Brand DJ. Unique seminal quality in the South African cheetah and a comparative evaluation in the domestic cat. Biol Reprod 1983; 29:1019-1025
39. Crosier AE, Marker L, Howard JG, Pukazhenthi BS, Henghali JN, Wildt DE. Ejaculate traits in the Namibian cheetah (Acinonyx jubatus): influence of age, season, and captivity. Reprod Fertil Dev 2007; 19:370-382
40. Howard JG, Brown JL, Bush M, Wildt DE. Teratospermic and normospermic domestic cats: ejaculate traits, pituitary-gonadal hormones and improvement of spermatozoal motility and morphology after swim-up processing. J Androl 1990; 11:204-215
41. Pukazhenthi BS, Neubauer K, Jewgenow K, Howard JG, Wildt DE. The impact and potential etiology of teratospermia in the domestic cat and its wild relatives. Theriogenology 2006; 66:112-121
42. Crosier AE, Pukazhenthi BS, Henghali JN, Howard JG, Dickman AJ, Marker L, Wildt DE. Cryopreservation of spermatozoa from wild-born Namibian cheetahs (Acinonyx jubatus) and influence of glycerol on cryosurvival. Cryobiology 2006; 52:169-181
43. Penfold LM, Jost L, Evenson DP, Wildt DE. Normospermic versus teratospermic domestic cat sperm chromatin integrity evaluated by flow cytometry and intracytoplasmic injection. Biol Reprod 2003; 69:1730-1735
44. Crosier A, Henghali J, Howard JG, Pukazhenthi BS, Terrell KA, MarkerLL, Wildt DE. Improved quality of cryopreserved cheetah (Acinonyx jubatus) spermatozoa after centrifugation through Accudenz. J Androl 2009; 30:298-308
45. Howard JG. Semen collection and analysis in carnivores. In: Fowler ME (ed.), Zoo and Wild Animal Medicine: Current Therapy III. Philadelphia: WB Saunders; 1993:390-399
46. Pukazhenthi BS, Noiles E, Pelican K, Donoghue AM, Wildt DE, Howard JG. Osmotic effects on feline spermatozoa from normospermic versus teratospermic donors. Cryobiology 2000; 40:139-150
47. Gardner DK, Leese HJ. Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro. J Reprod Fertil 1990; 88:361-368
48. Bavister BD. Substitution of a synthetic polymer for protein in a mammalian gamete culture system. J Exp Zool 1981; 217:45-51
49. Shah D, Naciri M, Clee P, Al-Rubeai M. NucleoCounter: an efficient technique for the determination of cell number and viability in animal cell culture processes. Cytotechnology 2006; 51:39-44
50. Ford S, Jones AR. The effect of alpha-chlorohydrin on the oxidation of fructose by rabbit spermatozoa in vitro. Contraception 1983; 28:565-573
51. Ford WCL. Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round? Hum Reprod Update 2006; 12:269-274
52. Ford W, Harrison A. The concerted effect of alpha-chlorohydrin and glucose on the ATP concentration in spermatozoa is associated with the accumulation of glycolytic intermediates. J Reprod Fertil 1986; 77:537-545
53. Larson JL, Miller DJ. Simple histochemical stain for acrosomes on sperm from several species. Mol Reprod Dev 1999; 52:445-449
54. Passonneau JV, Lowry OH. Enzymatic Analysis: A Practical Guide. Totowa, NJ: Humana Press; 1993
55. SAS. SAS/STAT User's Guide: Statistics, Version 9.1. Cary, NC: Statistical Analysis System Institute, Inc; 2002
56. Voet D, Voet JG. Lipid metabolism. In: Harris D, Fitzgerald P (eds.), Biochemistry, 3rd ed. Hoboken, NJ: John Wiley & Sons; 2004:909-984
57. Voet D, Voet JG. Electron transport and oxidative phosphorylation. In: Harris D, Fitzgerald P (eds.), Biochemistry, 3rd ed. Hoboken, NJ: John Wiley & Sons; 2004:797-842
58. Ford W, Harrison A. The presence of glucose increases the lethal effect of a-chlorohydrin on ram and boar spermatozoa in vitro. J Reprod Fertil 1985; 73:197-206
59. Jones AR, Chantrill LA. Oxidative metabolic activity of boar spermatozoa: a system for assessing anti-glycolytic activity of potential inhibitors in vitro. Reprod Fert Dev 1989; 1:357-367
60. Tash J, Mann T. Adenosine 3′,5′-cyclic monophosphate in relation to motility and senescence of spermatozoa. Proc R Soc Lond B Biol Sci 1973; 184:109-114
61. Hoskins D, Patterson D. Metabolism of rhesus monkey spermatozoa. J Reprod Fertil 1968; 16:183-195
62. Pukazhenthi B, Pelican K, Wildt D, Howard JG. Sensitivity of domestic cat (Felis catus) sperm from normospermic versus teratospermic donors to cold-induced acrosome damage. Biol Reprod 1999; 61:135-141
63. Wildt DE, Comizzoli P, Pukazhenthi B, Songsasen N. Lessons from biodiversity-the value of nontraditional species to advance reproductive science, conservation and human health. Mol Reprod Dev 2010; 77:397- 409
64. Stachecki JJ, Ginsburg KA, Armant DR. Stimulation of cryopreserved epididymal spermatozoa of the domestic cat using the motility stimulants caffeine, pentoxifylline, and 2′-deoxyadenosine. J Androl 1994; 15:157- 164
65. Herrick JR, Campbell M, Levens G, Moore T, Benson K, D'Agostino J, West G, Okeson DM, Coke R, Portacio SC, Leiske K, Kreider C, et al. In vitro fertilization and sperm cryopreservation in the black-footed cat (Felis nigripes) and sand cat (Felis margarita). Biol Reprod 2010; 82:552-562.