Genetic Disruption of the Copulatory Plug in Mice Leads to Severely Reduced Fertility

PLoS Genetics

Volumn 9, Issue 1, 2013, Pages

  Dean, Matthew D ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREEDING; COITUS; CONTROLLED STUDY; DISEASE SEVERITY; EJACULATION; FEMALE; FEMALE GENITAL SYSTEM; FERTILIZATION; GENE; GENE DISRUPTION; GENE FUNCTION; GENE INACTIVATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MALE FERTILITY; MALE INFERTILITY; MOLECULAR MECHANICS; MOUSE; NONHUMAN; OOCYTE; REPRODUCTION; REPRODUCTIVE SUCCESS; SEMINAL PLASMA; SPERM; SPERMATOZOON COUNT; SPERMATOZOON MIGRATION; SPERMATOZOON MOTILITY; TGM4 GENE;

ANIMALS; COPULATION; EJACULATION; FEMALE; FERTILITY; MALE; MICE; MICE, KNOCKOUT; OOCYTES; REPRODUCTION; SEMEN; SPERM COUNT; SPERM MOTILITY; TRANSGLUTAMINASES;

EID: 84873511547     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003185     Document Type: Article

References (97)

1. Aigaki T, Fleischmann I, Chen PS, Kubli E, (1991) Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster. Neuron 7: 557-563.
2. Chen PS, Stumm-Zollinger E, Aigaki T, Balmer J, Bienz M, et al. (1988) A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell 54: 291-298.
3. Wolfner MF, (1997) Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect Biochem Mol Biol 27: 179-192.
4. Chapman T, Herndon LA, Heifetz Y, Partridge L, Wolfner MF, (2001) The Acp26Aa seminal fluid protein is a modulator of early egg hatchability in Drosophila melanogaster. Proc R Soc Lond B Biol Sci 268: 1647-1654.
5. Heifetz Y, Tram U, Wolfner MF, (2001) Male contributions to egg production: the role of accessory gland products and sperm in Drosophila melanogaster. Proc R Soc Lond B Biol Sci 268: 175-180.
6. Herndon LA, Wolfner MF, (1995) A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating. Proc Natl Acad Sci U S A 92: 10114-10118.
7. Robertson SA, (2007) Seminal fluid signaling in the female reproductive tract: lessons from rodents and pigs. J Anim Sci 85: E36-44.
8. Poiani A, (2006) Complexity of seminal fluid: a review. Behav Ecol Sociobiol 60: 289-310.
9. Rodríguez-Martínez H, Kvist U, Ernerudh J, Sanz L, Calvete JJ, (2011) Seminal plasma proteins: what role do they play? Am J Reprod Immunol 66: 11-22.
10. Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF, (2011) Insect seminal fluid proteins: identification and function. Annu Rev Entomol 56: 21-40.
11. Mann T, Lutwak-Mann C (1981) Male reproductive function and semen. New York, New York: Springer-Verlag. 495 p.
12. Wigby S, Sirot LK, Linklater JR, Buehner N, Calboli FCF, et al. (2009) Seminal fluid protein allocation and male reproductive success. Curr Biol 19: 751-757.
13. Harshman LG, Prout T, (1994) Sperm displacement without sperm transfer in Drosophila melanogaster. Evolution 48: 758-766.
14. Sirot LK, Wolfner MF, Wigby S, (2011) Protein-specific manipulation of ejaculate composition in response to female mating status in Drosophila melanogaster. Proc Natl Acad Sci U S A 108: 9922.
15. Barker DM, (1994) Copulatory plugs and paternity assurance in the nematode Caenorhabditis elegans. Anim Behav 48: 147-156.
16. Rogers DW, Baldini F, Battaglia F, Panico M, Dell A, et al. (2009) Transglutaminase-mediated semen coagulation controls sperm storage in the malaria mosquito. PLoS Biol 7: e1000272 doi:10.1371/journal.pbio.1000272.
17. Devine MC, (1975) Copulatory plugs in snakes: enforced chastity. Science 187: 844-845.
18. Price D, Williams-Ashman HG (1961) The accessory reproductive glands of mammals; Young WC, editor. Baltimore: Williams and Wilkins Inc. 366-448 p.
19. Leuckart R (1847) Zur morphologie und anatomie der geschlechtsorgane. Göttingen: Vandenhoeck und Ruprecht. 130 p.
20. Voss R, (1979) Male accessory glands and the evolution of copulatory plugs in rodents. Occas Pap Mus Zool Univ Mich 689: 1-27.
21. Hartung TG, Dewsbury DA, (1978) A comparative analysis of copulatory plugs in muroid rodents and their relationship to copulatory behavior. J Mammal 59: 717-723.
22. Dixson AF, Anderson MJ, (2002) Sexual selection, seminal coagulation and copulatory plug formation in primates. Folia Primatol 73: 63-69.
23. Camus L, Gley E, (1896) Action coagulante du liquide prostatique sur le contenu des vésicules séminales. Compt Rend Hebd Seances Acad Sci 123: 194-195.
24. Walker G, (1910) A special function discovered in a glandular structure hitherto supposed to form a part of the prostate gland in rats and guinea-pigs. Johns Hopkins Hosp Reports 21: 182-185.
25. Walker G, (1910) The nature of the secretion of the vesiculae seminales and of an adjacent glandular structure in the rat and guinea-pig, with special reference to the occurrence of histone in the former. Johns Hopkins Hosp Reports 21: 185-192.
26. Gotterer G, Ginsberg D, Schulman T, Banks J, Williams-Ashman HG, (1955) Enzymatic coagulation of semen. Nature 176: 1209-1211.
27. Notides AC, Williams-Ashman HG, (1967) The basic protein responsible for the clotting of guinea pig semen. Proc Natl Acad Sci U S A 58: 1991-1995.
28. Williams-Ashman HG, Notides AC, Pabalan SS, Lorand L, (1972) Transamidase reactions involved in the enzymic coagulation of semen: isolation of γ-glutamyl-ε-lysine dipeptide from clotted secretion protein of guinea pig seminal vesicle. Proc Natl Acad Sci U S A 69: 2322-2325.
29. Gentile V, Grant F, Porta R, (1995) Localization of the human prostate transglutaminase (type IV) gene (TGM4) to chromosome 3p21. 33-p22 by fluorescence in situ hybridization. Genomics 27: 219-220.
30. Grant FJ, Taylor DA, Sheppard PO, Mathewes SL, Lint W, et al. (1994) Molecular cloning and characterization of a novel transglutaminase cDNA from a human prostate cDNA library. Biochem Biophys Res Commun 203: 1117-1123.
31. Dubbink HJ, Verkaik NS, Faber PW, Trapman J, Schroder FH, et al. (1996) Tissue specific and androgen-regulated expression of human prostate-specific transglutaminase. Biochem J 315 (Pt 3):: 901-908.
32. Pilch B, Mann M, (2006) Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol 7: R40.
33. Dean MD, Findlay GD, Hoopmann MR, Wu CC, MacCoss MJ, et al. (2011) Identification of ejaculated proteins in the house mouse (Mus domesticus) via isotopic labeling. BMC Genomics 12: 306.
34. Tseng H-C, Tang J-B, Sudhakar Gandhi P, Luo C-W, Ou C-M, et al. (2011) Mutual adaptation between mouse transglutaminase 4 and its native substrates in the formation of copulatory plug. Amino Acids 42: 951-960.
35. Hart RG, Greenstein JS, (1968) A newly discovered role for Cowper's gland secretion in rodent semen coagulation. J Reprod Fertil 17: 87-94.
36. Hartman CG, (1924) Observations on the motility of the opossum genital tract and the vaginal plug. Anat Rec 27: 293-303.
37. Williams-Ashman HG, Beil RE, Wilson J, Hawkins M, Grayhack J, et al. (1980) Transglutaminases in mammalian reproductive tissues and fluids: relation to polyamine metabolism and semen coagulation. Adv Enzyme Regul 18: 239-246, IN213-IN214, 247-258.
38. Williams-Ashman HG, (1984) Transglutaminases and the clotting of mammalian seminal fluids. Mol Cell Biochem 58: 51-61.
39. Porta R, Esposito C, Metafora S, Malorni A, Pucci P, et al. (1991) Mass spectrometric identification of the amino donor and acceptor sites in a transglutaminase protein substrate secreted from rat seminal vesicles. Biochemistry 30: 3114-3120.
40. Walker G, (1911) The effect on breeding of the removal of the prostate gland or of the vesiculae seminales, or of both; together with observations on the condition of the testes after such operations on white rats. Johns Hopkins Hosp Reports 16: 223-255.
41. Blandau RJ, (1945) Is the copulation plug necessary for the en masse transport of spermatozoa into the uterine cornua of the albino rat? Anat Rec 91: 266-267.
42. Carballada R, Esponda P, (1992) Role of fluid from seminal vesicles and coagulating glands in sperm transport into the uterus and fertility in rats. J Reprod Fertil 95: 639-648.
43. Cukierski MA, Sina JL, Prahalada S, Robertson RT, (1991) Effects of seminal vesicle and coagulating gland ablation on fertility in rats. Reprod Toxicol 5: 347-352.
44. O W-S, Chen HQ, Chow PH, (1988) Effects of male accessory sex gland secretions on early embryonic development in the golden hamster. J Reprod Fertil 84: 341-344.
45. Queen K, Dhabuwala CB, Pierrepoint CG, (1981) The effect of the removal of the various accessory sex glands on the fertility of male rats. J Reprod Fertil 62: 423-426.
46. Peitz B, Olds-Clarke P, (1986) Effects of seminal vesicle removal on fertility and uterine sperm motility in the house mouse. Biol Reprod 35: 608-617.
47. Pang SF, Chow PH, Wong TM, (1979) The role of the seminal vesicles, coagulating glands and prostate glands on the fertility and fecundity of mice. J Reprod Fertil 56: 129-132.
48. Martan J, Shepherd BA, (1976) The role of the copulatory plug in reproduction of the guinea pig. J Exp Zool 196: 79-83.
49. Firman RC, Simmons LW, (2009) Experimental evolution of sperm quality via postcopulatory sexual selection in house mice. Evolution 64: 1245-1256.
50. Austin CP, Battey JF, Bradley A, Bucan M, Capecchi M, et al. (2004) The knockout mouse project. Nat Genet 36: 921-924.
51. Testa G, Schaft J, van der Hoeven F, Glaser S, Anastassiadis K, et al. (2004) A reliable lacZ expression reporter cassette for multipurpose, knockout-first alleles. Genesis 38: 151-158.
52. Blandau RJ, (1945) On the factors involved in sperm transport through the cervix uteri of the albino rat. Am J Anat 77: 253-272.
53. Toner JP, Attas AI, Adler NT, (1987) Transcervical sperm transport in the rat: the roles of pre-ejaculatory behavior and copulatory plug fit. Physiol Behav 39: 371-375.
54. Matthews MK Jr, Adler NT, (1978) Systematic interrelationship of mating, vaginal plug position, and sperm transport in the rat. Physiol Behav 20: 303-309.
55. Ball J, (1934) Demonstration of a quantitative relation between stimulus and response in pseudopregnancy in the rat. Am J Physiol 107: 698-703.
56. West JD, Frels WI, Papaioannou VE, Karr JP, Chapman VM, (1977) Development of interspecific hybrids of Mus. J Embryol Exp Morphol 41: 233-243.
57. Leckie PA, Watson JG, Chaykin S, (1973) An improved method for the artificial insemination of the mouse (Mus musculus). Biol Reprod 9: 420-425.
58. Engle ET, (1926) A morphological and experimental study of the proximal lobes of the prostate of the guinea-pig, cavia cobaya. Anat Rec 34: 75-90.
59. Dean MD, Clark NL, Findlay GD, Karn RC, Yi X, et al. (2009) Proteomics and comparative genomic investigations reveal heterogeneity in evolutionary rate of male reproductive proteins in mice (Mus domesticus). Mol Biol Evol 26: 1733-1743.
60. Dubbink HJ, de Waal L, van Haperen R, Verkaik NS, Trapman J, et al. (1998) The human prostate-specific transglutaminase gene (TGM4): genomic organization, tissue-specific expression, and promoter characterization. Genomics 51: 434-444.
61. Su AI, Cooke MP, Ching KA, Hakak Y, Walker JR, et al. (2002) Large-scale analysis of the human and mouse transcriptomes. Proc Natl Acad Sci U S A 99: 4465-4470.
62. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, et al. (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A 101: 6062-6067.
63. Paonessa G, Metafora S, Tajana G, Abrescia P, Santis AD, et al. (1984) Transglutaminase-mediated modifications of the rat sperm surface in vitro. Science 226: 852-855.
64. Mukherjee DC, Agrawal AK, Manjunath R, Mukherjee AB, (1983) Suppression of epididymal sperm antigenicity in the rabbit by uteroglobin and transglutaminase in vitro. Science 219: 989-991.
65. Dorus S, Wasbrough ER, Busby J, Wilkin EC, Karr TL, (2010) Sperm proteomics reveals intensified selection on mouse sperm membrane and acrosome genes. Mol Biol Evol 27: 1235-1246.
66. Baker MA, Reeves G, Hetherington L, Müller J, Baur I, et al. (2007) Identification of gene products present in Triton X-100 soluble and insoluble fractions of human spermatozoa lysates using LC-MS/MS analysis. Proteomics Clin Appl 1: 524-532.
67. Carnahan SJ, Jensen-Seaman MI, (2008) Hominoid seminal protein evolution and ancestral mating behavior. Am J Primatol 70: 939-948.
68. Parker GA, (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev Camb Philos Soc 45: 525-567.
69. Ramm SA, Parker GA, Stockley P, (2005) Sperm competition and the evolution of male reproductive anatomy in rodents. Proc Biol Sci 272: 949-955.
70. Kingan SB, Tatar M, Rand DM, (2003) Reduced polymorphism in the chimpanzee semen coagulating protein, semenogelin I. J Mol Evol 57: 159-169.
71. Jensen-Seaman MI, Li WH, (2003) Evolution of the hominoid semenogelin genes, the major proteins of ejaculated semen. J Mol Evol 57: 261-270.
72. Ramm SA, McDonald L, Hurst JL, Beynon RJ, Stockley P, (2009) Comparative proteomics reveals evidence for evolutionary diversification of rodent seminal fluid and its functional significance in sperm competition. Mol Biol Evol 26: 189-198.
73. Dorus S, Evans PD, Wyckoff GJ, Choi SS, Lahn BT, (2004) Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nat Genet 36: 1326-1329.
74. Murer V, Spetz JF, Hengst U, Altrogge LM, de Agostini A, et al. (2001) Male fertility defects in mice lacking the serine protease inhibitor protease nexin-1. Proc Natl Acad Sci U S A 98: 3029-3033.
75. Firman RC, Simmons LW, (2008) The frequency of multiple paternity predicts variation in testes size among island populations of house mice. J Evol Biol 21: 1524-1533.
76. Dean MD, Ardlie KG, Nachman MW, (2006) The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol Ecol 15: 4141-4151.
77. Koprowski JL, (1992) Removal of copulatory plugs by female tree squirrels. J Mammal 73: 572-576.
78. Parga JA, (2003) Copulatory plug displacement evidences sperm competition in Lemur catta. Int J Primatol 24: 889-899.
79. Parga JA, Maga M, Overdorff DJ, (2006) High-resolution X-ray computed tomography scanning of primate copulatory plugs. Am J Phys Anthropol 129: 567-576.
80. O'Hanlon JK, Sachs BD, (1986) Fertility of mating in rats (Rattus norvegicus): contributions of androgen-dependent morphology and actions of the penis. J Comp Psychol 100: 178-187.
81. Wallach SJR, Hart BL, (1983) The role of the striated penile muscles of the male rat in seminal plug dislodgement and deposition. Physiol Behav 31: 815-821.
82. Dewsbury DA, (1988) A test of the role of copulatory plugs in sperm competition in deer mice (Peromyscus maniculatus). J Mammal 69: 854-857.
83. Lanier DL, Estep DQ, Dewsbury DA, (1979) Role of prolonged copulatory behavior in facilitating reproductive success in a competitive mating situation in laboratory rats. J Comp Physiol Psychol 93: 781-792.
84. Oglesby JM, Lanier DL, Dewsbury DA, (1981) The role of prolonged copulatory behavior in facilitating reproductive success in male Syrian golden hamsters (Mesocricetus auratus) in a competitive mating situation. Behav Ecol Sociobiol 8: 47-54.
85. Huck UW, Tonias BA, Lisk RD, (1989) The effectiveness of competitive male inseminations in golden hamsters, Mesocricetus auratus, depends on an interaction of mating order, time delay between males, and the time of mating relative to ovulation. Anim Behav 37: 674-680.
86. Foltz DW, (1981) Genetic evidence for long-term monogamy in a small rodent, Peromyscus polionotus. Am Nat 117: 665-675.
87. Baumgardner DJ, Hartung TG, Sawrey DK, Webster DG, Dewsbury DA, (1982) Muroid copulatory plugs and female reproductive tracts: a comparative investigation. J Mammal 63: 110-117.
88. Asdell SA (1946) Patterns of mammalian reproduction. Ithaca, New York: Comstock Publishing Company. 437 p.
89. Huggins C, Neal W, (1942) Coagulation and liquefaction of semen. J Exp Med 76: 527.
90. Mikhailichenko VV, Esipov AS, (2005) Peculiarities of semen coagulation and liquefaction in males from infertile couples. Fertil Steril 84: 256-259.
91. Milardi D, Grande G, Vincenzoni F, Messana I, Pontecorvi A, et al. (2012) Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men. Fertil Steril 97: 67-73.
92. Snyder RL (1967) Fertility and reproductive performance of grouped male mice. In: Benirschke K, editor. Comparative aspects of reproductive failure. New York: Springer-Verlag. pp. 458-472.
93. Nagy A, Gertsenstein M, Vintersten K, Behringer R (2003) Manipulating the mouse embryo. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press. 764 p.
94. Dean MD, Nachman MW, (2009) Faster fertilization rate in conspecific versus heterospecific matings in house mice. Evolution 63: 20-28.
95. Good JM, Dean MD, Nachman MW, (2008) A complex genetic basis to X-linked hybrid male sterility between two species of house mice. Genetics 179: 2213-2228.
96. Good JM, Handel MA, Nachman MW, (2008) Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice. Evolution 62: 50-65.
97. Welch BL, (1947) The generalization of "Student's" problem when several different population variances are involved. Biometrika 34: 28-35.