Lactotransferrin in Asian Elephant (Elephas maximus) Seminal Plasma Correlates with Semen Quality

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Kiso, Wendy K ^a,b   Selvaraj, Vimal ^c   Nagashima, Jennifer ^c,d   Asano, Atsushi ^c   Brown, Janine L ^d   Schmitt, Dennis L ^e,f   Leszyk, John ^g   Travis, Alexander J ^c   Pukazhenthi, Budhan S ^d  

^a SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^b GEORGE MASON UNIVERSITY   (United States)

^c Department of Molecular Biology and Genetics   (United States)

^d SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^e MISSOURI STATE UNIVERSITY   (United States)

^f Ringling Bros Center for Elephant Conservation   (United States)

^g UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; CHLORIDE; CREATINE KINASE; GLUCOSE; LACTOFERRIN; MAGNESIUM; PHOSPHORUS; SODIUM;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CRYOPRESERVATION; ELEPHANT; ENDANGERED SPECIES; IMMUNOBLOTTING; MALE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; SEMEN ANALYSIS; SEMINAL PLASMA; SPERM PRESERVATION; SPERMATOZOON; SPERMATOZOON MOTILITY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; CRYOPRESERVATION; ELEPHANTS; ENDANGERED SPECIES; INSEMINATION, ARTIFICIAL; LACTOFERRIN; MALE; MASS SPECTROMETRY; SEMEN; SEMEN ANALYSIS; SEMEN PRESERVATION; SPECIMEN HANDLING; SPERM COUNT; SPERM MOTILITY; SPERMATOZOA;

EID: 84881577949     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071033     Document Type: Article

References (78)

1. Wiese RJ, (2000) Asian elephants are not self-sustaining in North America. Zoo Biol 19: 299-309.
2. Pukazhenthi BS, Wildt DE, (2004) Which reproductive technologies are most relevant to studying, managing and conserving wildlife? Reprod Fert Dev 16: 33-46.
3. Kiso WK, Brown JL, Siewerdt F, Schmitt DL, Olson D, et al. (2011) Liquid semen storage in elephants (Elephas maximus and Loxodonta africana): species differences and storage optimization. J Androl 32: 420-431.
4. Kiso WK, Asano A, Travis AJ, Schmitt DL, Brown JL, et al. (2012) Pretreatment of Asian elephant (Elephas maximus) spermatozoa with cholesterol-loaded cyclodextrins and glycerol addition at 4°C improves cryosurvival. Reprod Fertil Dev 24: 1134-1142.
5. Howard JG, Bush M, de Vos V, Wildt DE, (1984) Electroejaculation, semen characteristics and serum testosterone concentrations of free-ranging African elephants (Loxodonta africana). J Reprod Fertil 72: 187-195.
6. Jainudeen MR, Eisenberg JF, Jayasinghe JB, (1971) Semen of the Ceylon elephant. J Reprod Fertil 24: 213-217.
7. Kitiyanant Y, Schmidt MJ, Pavasuthipaisit K, (2000) Evaluation of sperm acrosome reaction in the Asiatic elephant. Theriogenology 53: 887-896.
8. Schmitt DL, Hildebrandt TB, (1998) Manual collection and characterization of semen from Asian elephants (Elephas maximus). Anim Reprod Sci 53: 309-314.
9. Thongtip N, Siakhun J, Mahasawangkul S, Komkaewrat K, Pongsopavijitr P, et al. (2008) Potential factors affecting semen quality in Asian Elephant (Elephas maximus). Reprod Biol Endocrinol 6: 1-19.
10. Hermes R, Behr B, Hildebrandt TB, Blottner S, Sieg B, et al. (2009) Sperm sex-sorting in the Asian elephant (Elephas maximus). Anim Reprod Sci 112: 390-396.
11. Portas TJ, Bryant BR, Goritz F, Hermes R, Keeley T, et al. (2007) Semen collection in an Asian elephant (Elephas maximus) under combined physical and chemical restraint. Aust Vet J 85: 425-427.
12. Schmitt D (2006) Reproductive System. In: Fowler ME, Mikota SK, editors. Biology, Medicine, and Surgery of Elephants. Ames: Blackwell Publishing Ltd. 347-355.
13. Kawano N, Yoshida K, Iwamoto T, Yoshida M, (2008) Ganglioside GM1 mediates decapacitation effects of SVS2 on murine spermatozoa. Biol Reprod 79: 1153-1159.
14. Howards S, Lechene C, Vigersky R (1979) The fluid environment of the maturing spermatozoon. In: Fawcett DW, Bedford JM, editors. The spermatozoon: maturation, motility, surface properties and comparative aspects. Baltimore: Urban & Schwarzenberg. 35-42.
15. Mann T, Lutwak-Mann C (1981) Male reproductive function and semen: themes and trends in physiology, biochemistry and investigative andrology. New York: Springer-Verlag. 495 p.
16. Oliva R, Martinez-Heredia M, (2008) Proteomics in the study of the sperm cell composition, differentiation, and function. Syst Biol Reprod Med 54: 23-36.
17. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
18. Morrissey JH, (1981) Silver stain for proteins in polyacrylamide gels - a modified procedure with enhanced uniform sensitivity. Anal Biochem 117: 307-310.
19. Travis AJ, Foster JA, Rosenbaum NA, Visconti PE, Gerton GL, et al. (1998) 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 Biol Cell 9: 263-276.
20. Mann T (1964) The Biochemistry of Semen and of the Male Reproductive Tract. Great Britain: Butler & Tanner Ltd. 493 p.
21. Jainudeen MR, Katongole CB, Short RV, (1972) Plasma testoterone levels in relation to musth and sexual activity in the male Asiatic elephant, Elephas maximus. J Reprod Fertil 29: 99-103.
22. O'Donnell L, Meachem SJ, Stanton PG, McLachlan RI (2006) Endocrine regulation of spermatogenesis. In: Neill JD, editor. Knobil and Neill's Physiology and Reproduction. 3rd ed. St. Louis: Elsevier Academic Press, Inc. 1017-1069.
23. Carr DW, Usselman MC, Acott TS, (1985) Effects of pH, lactate, and viscoelastic drag on sperm motility: a species comparison. Biol Reprod 33: 588-595.
24. Griggers S, Paccamonti DL, Thompson RA, Eilts BE, (2001) The effects of pH, osmolarity and urine contamination on equine spermatozoal motility. Theriogenology 56: 613-622.
25. Makler A, David R, Blumenfeld Z, Better OS, (1981) Factors affecting sperm motility. VII. Sperm viability as affected by change of pH and osmolarity of semen and urine specimens. Fertil Steril 36: 507-511.
26. Sivilaikul S, Jitprom A, Kularb A, Kornkaewrut K, Suthanmaphinuth P, et al. (2010) Relationship between seminal and serum calcium concentration with semen quality in the Asian elephant (Elephas maximus). Thai J Vet Med 40: 251-255.
27. Wirtu G, Pope CE, MacLean RA, Godke RA, Paccamonti DL, et al. (2008) Reversal of motility loss in bongo antelope (Tragelaphus eurycerus isaaci) spermatozoa contaminated with hyposmotic urine during electroejaculation. Anim Reprod Sci 103: 392-397.
28. Sirat MP, Sinha AK, Singh BK, Prasad RL, (1996) Effect of cryoprotectants on release of various enzymes from buck spermatozoa during freezing. Theriogenology 45: 405-416.
29. Gundogan M, Serteser M, (2005) Some reproductive parameters and biochemical properties in Akkaraman and Awassi rams. Turk J Vet Anim Sci 29: 595-599.
30. Yousef MI, Abdallah GA, Kamel KI, (2003) Effect of ascorbic acid and Vitamin E supplementation on semen quality and biochemical parameters of male rabbits. Anim Reprod Sci 76: 99-111.
31. Roth TL, Stoops MA, Robeck TR, Ball RL, Wolfe BA, et al. (2010) Alkaline phosphatase as an indicator of true ejaculation in the rhinoceros. Theriogenology 74: 1701-1706.
32. Stornelli A, Arauz M, Baschard H, de la Sota RL, (2003) Unilateral and bilateral vasectomy in the dog: alkaline phosphatase as an indicator of tubular patency. Reprod Domest Anim 38: 1-4.
33. Turner RMO, McDonnell SM, (2003) Alkaline phosphate in stallion semen: characterization and clinical applications. Theriogenology 60: 1-10.
34. Frenette G, Dube YJ, Tremblay RR, (1986) Origin of alkaline phosphatase of canine seminal plasma. Arch Androl 16: 235-241.
35. Kozdrowski R, Dubiel A, (2004) The effect of season on the properties of wild boar (Sus scofa L.) semen. Anim Reprod Sci 80: 281-289.
36. Kutzler MA, Solter PF, Hoffman WE, Volkmann DH, (2003) Characterization and localization of alkaline phosphatase in canine seminal plasma and gonadal tissues. Theriogenology 60: 299-306.
37. Pesch S, Bergmann M, Bostedt H, (2006) Determination of some enzymes and macro- and microelements in stallion seminal plasma and their correlations to semen quality. Theriogenology 66: 307-313.
38. O'Brien JK, Steinman KJ, Schmitt T, Robeck TR, (2008) Semen collection, characterisation and artificial insemination in the beluga (Delphinapterus leucas) using liquid-stored spermatozoa. Reprod Fertil Dev 20: 770-783.
39. Bessman SP, Carpenter CL, (1985) The creatine-creatine phosphate energy shuttle. Annu Rev Biochem 54: 831-862.
40. Darszon A, Trevino CL, Wood C, Galindo B, Rodriguez-Miranda E, et al. (2007) Ion channels in sperm motility and capacitation. Soc Reprod Fertil Suppl 65: 229-244.
41. Gusani PH, Skandhan KP, (1992) Sodium and potassium in normal and pathological seminal plasma. Acta Eur Fertil 23: 39-42.
42. Wong WY, Flik G, Groenen PMW, Swinkels DW, Thomas CMG, et al. (2001) The impact of calcium, magnesium, zinc and copper in blood and seminal plasma on semen parameters in men. Reprod Toxicol 15: 131-136.
43. Fakih H, Maclusky N, Decherney A, Wallimann T, Huszar G, (1986) Enhancement of human sperm motility and velocity in vitro: effects of calcium and creatine phosphate. Fertil Steril 46: 938-944.
44. Luconi M, Baldi E, (2003) How do sperm swim? Molecular mechanisms underlying sperm motility. Cell Mol Biol 49: 357-369.
45. Darszon A, Labarca P, Nishigaki T, Espinosa F, (1999) Ion channels in sperm physiology. Physiol Rev 79: 481-510.
46. Weissgerber P, Kriebs U, Tsvilovskyy V, Olausson J, Kretz O, et al. (2011) Male fertility depends on Ca2+ absorption by TRPV6 in epididymal epithelia. Sci Signal 4: 1-13.
47. Williams AC, Ford WC, (2001) The role of glucose in supporting motility and capacitation in human spermatozoa. J Androl 22: 680-695.
48. Truta Z, Garlovanu M, Lerintiu S, Micu R, (2010) A new method for human semen glucose concentration evaluation. Rom Biotech Lett 15: 5764-5772.
49. Mosaferi S, Niasari-Naslaji A, Abarghani A, Gharahdaghi AA, Gerami A, (2005) Biophysical and biochemical characteristics of bactrian camel semen collected by artificial vagina. Theriogenology 63: 92-101.
50. Gamboa S, Francisco M, Gomes P, Mendes C, Machado-Faria M, et al. (2011) Level of glycolyzable substrates in stallion semen: effect of ejaculation frequency on sperm survival after cool storage during the nonbreeding season. J Equine Vet Sci 31: 109-115.
51. Cevik M, Tuncer PB, Tasdemir U, Ozgurtas T, (2007) Comparison of spermatological characteristics and biochemical seminal plasma parameters of normozoospermic and oligoasthenozoospermic bulls of two breeds. Turk J Vet Anim Sci 31: 381-387.
52. Baronos S, (1971) Seminal carbohydrate in boar and stallion. J Reprod Fertil 24: 303-305.
53. Anand SR, (1973) The carbohydrates of buffalo and goat semen. J Reprod Fertil 32: 97-100.
54. Anderson R Jr, Reddy J, Oswald C, Zaneveld L, (1979) Enzymic determination of fructose in seminal plasma by initial rate analysis. Clin Chem 25: 1780-1782.
55. Brandt H, Acott TS, Johnson D, Hoskins DD, (1978) Evidence for an epididymal origin of bovine sperm forward motility protein. Biol Reprod 19: 830-835.
56. Eddy EM (2006) The Spermatozoon. In: Neill JD, editor. Knobil and Neill's Physiology of Reproduction. 3rd ed. St. Louis: Elsevier Academic Press, Inc. 3-54.
57. Killian GJ, Chapman DA, Rogowski LA, (1993) Fertility-associated proteins in Holstein bull seminal plasma. Biol Reprod 49: 1202-1207.
58. Minelli A, Moroni M, Castellini C, (2001) Isolation and purification of the IGF-I protein complex from rabbit seminal plasma: effects on sperm motility and viability. J Exp Zool 290: 279-290.
59. Brandon CI, Heusner GL, Caudle AB, Fayrer-Hosken RA, (1999) Two-dimensional polyacrylamide gel electrophoresis of equine seminal plasma proteins and their correlation with fertility. Theriogenology 52: 863-873.
60. Cancel AM, Chapman DA, Killian GJ, (1997) Osteopontin is the 55-kilodalton fertility-associated protein in Holstein bull seminal plasma. Biol Reprod 57: 1293-1301.
61. Gerena RL, Irikura D, Urade Y, Eguchi N, Chapman DA, et al. (1998) Identification of a fertility-associated protein in bull seminal plasma as lipocalin-type prostaglandin D synthase. Biol Reprod 58: 826-833.
62. Moura AA, (2006) Identification of proteins in the accessory sex gland fluid associated with fertility indexes of dairy bulls: a proteomic approach. J Androl 27: 201-211.
63. Novak S, Ruiz-Sanchez A, Dixon WT, Foxcroft GR, Dyck MK, (2010) Seminal plasma proteins as potential markers of relative fertility in boars. J Androl 31: 188-200.
64. Rajeev SK, Reddy KV, (2004) Sperm membrane protein profiles of fertile and infertile men: identification and characterization of fertility-associated sperm antigen. Hum Reprod 19: 234-242.
65. Favareto A, Rodello L, Taconeli CA, Bicudo SD, Klinefelter GR, et al. (2008) Identification of the SP22 sperm protein in Santa Ines and Dorper rams. Reprod Domest Anim 45: 323-330.
66. Levay PF, Viljoen M, (1995) Lactoferrin: a general review. Haematologica 80: 252-267.
67. Thaler CJ, Vanderpuye OA, McIntyre JA, Page Faulk W, (1990) Lactoferrin binding molecules in human seminal plasma. Biol Reprod 43: 712-717.
68. Kikuchi M, Takao Y, Tokuda N, Ohnami Y, Orino K, et al. (2003) Relationship between seminal plasma lactoferrin and gonadal function in horses. J Vet Med Sci 65: 1273-1274.
69. Pearl CA, Roser JF, (2008) Expression of lactoferrin in the boar epididymis: effects of reduced estrogen. Domest Anim Endocrin 34: 153-159.
70. Yu LC, Chen YH, (1993) The developmental profile of lactoferrin in mouse epididymis. Biochem J 296: 107-111.
71. Fouchecourt S, Metayer S, Locatelli A, Dacheux F, Dacheux JL, (2000) Stallion epididymal fluid proteome: qualitative and quantitative characterization; secretion and dynamic changes of major proteins. Biol Reprod 62: 1790-1803.
72. Wichmann L, Vaalasti A, Vaalasti T, Tuohimaa P, (1989) Localization of lactoferrin in the male reproductive tract. Int J Androl 12: 179-186.
73. Masson PL, Heremans JF, (1971) Lactoferrin in milk from different species. Comp Biochem Physiol B 39: 119-129.
74. Aitken RJ, Harkiss D, Buckingham D, (1993) Relationship between iron-catalysed lipid peroxidation potential and human sperm function. J Reprod Fertil 98: 257-265.
75. de Lamirande E, Jiang H, Zini A, Kodama H, Gagnon C, (1997) Reactive oxygen species and sperm physiology. Rev Reprod 2: 48-54.
76. Sanocka D, Kurpisz M, (2004) Reactive oxygen species and sperm cells. Reprod Biol Endocrinol 2: 12-18.
77. Brock JH, (2002) The physiology of lactoferrin. Biochem Cell Biol 80: 1-6.
78. Farnaud S, Evans RW, (2003) Lactoferrin-a multifunctional protein with antimicrobial properties. Mol Immunol 40: 395-405.