Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-25T05:34:33.412Z Has data issue: false hasContentIssue false
  • English
  • Français

Mouse models for identifying genes modulating fertility parameters

Published online by Cambridge University Press:  01 January 2009

P. Laissue ,
D. L’Hôte ,
C. Serres  and
D. Vaiman
P. Laissue
Affiliation:
INSERM U567, Team21 ‘Genomics and Epigenetics of Placental Diseases’, Genetics and Development Department, Institute Cochin, 24 rue du Faubourg St-Jacques, 75014 Paris, France CNRS UMR8104, Institute Cochin, 24 rue du Faubourg St-Jacques, 75014 Paris, France Faculté de Médecine Cochin-Port-Royal, Université Paris Descartes, 24 rue du Faubourg St-Jacques, 75014 Paris, France
D. L’Hôte
Affiliation:
INSERM U567, Team21 ‘Genomics and Epigenetics of Placental Diseases’, Genetics and Development Department, Institute Cochin, 24 rue du Faubourg St-Jacques, 75014 Paris, France CNRS UMR8104, Institute Cochin, 24 rue du Faubourg St-Jacques, 75014 Paris, France
C. Serres
Affiliation:
INSERM U567, Team21 ‘Genomics and Epigenetics of Placental Diseases’, Genetics and Development Department, Institute Cochin, 24 rue du Faubourg St-Jacques, 75014 Paris, France CNRS UMR8104, Institute Cochin, 24 rue du Faubourg St-Jacques, 75014 Paris, France Faculté de Médecine Cochin-Port-Royal, Université Paris Descartes, 24 rue du Faubourg St-Jacques, 75014 Paris, France
D. Vaiman*
Affiliation:
INSERM U567, Team21 ‘Genomics and Epigenetics of Placental Diseases’, Genetics and Development Department, Institute Cochin, 24 rue du Faubourg St-Jacques, 75014 Paris, France CNRS UMR8104, Institute Cochin, 24 rue du Faubourg St-Jacques, 75014 Paris, France Faculté de Médecine Cochin-Port-Royal, Université Paris Descartes, 24 rue du Faubourg St-Jacques, 75014 Paris, France
*
E-mail: vaiman@cochin.inserm.fr
Get access

Abstract

Fertility can be defined as the natural capability of giving life. It is an important factor both for human medicine, where ~10% of the couples call for the services of assisted reproductive technologies, and for species of economic interest. In particular, in dairy cows, the recent years have seen a kind of competition between milk production and fertility, and genes improving fertility are now considered as parameters to be selected for. The study of fertility pathways is nevertheless made difficult by the strong impact of environmental factors on this parameter, as well as by the number of genes potentially involved (as shown by systematic transcriptome analysis studies in the recent years). One additional level of complexity is given by the fact that factors modulating fertility will probably be sex specific. The usage of mouse models has been one of the solutions exploited for tackling with these difficulties. Here, we review three different approaches using mice for identifying genes modulating fertility in mammals: gene invalidation, positional cloning and in vitro mutagenesis. These three approaches exploit specific characteristics of the mouse, such as the possibility of controlling precisely the environment, an excellent genetic characterization and the existence of genomic and molecular tools equalled only in humans. Many indications suggest that at least some of the results obtained in mice could be easily transposed to the species of interest.

Keywords

fertilitymicegametogenesiscattlehumans
Type
Full Paper
Information
animal , Volume 3 , Issue 1 , January 2009 , pp. 55 - 71
Copyright
Copyright © The Animal Consortium 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ashwell, MS, Heyen, DW, Sonstegard, TS, Van Tassell, CP, Da, Y, VanRaden, PM, Ron, M, Weller, JI, Lewin, HA 2004. Detection of quantitative trait loci affecting milk production, health, and reproductive traits in Holstein cattle. Journal of Dairy Science 87, 468–475.CrossRefGoogle ScholarPubMed
Atchison, FW, Capel, B, Means, AR 2003. Pin1 regulates the timing of mammalian primordial germ cell proliferation. Development (Cambridge, England) 130, 3579–3586.CrossRefGoogle ScholarPubMed
Ballow, D, Meistrich, ML, Matzuk, M, Rajkovic, A 2006. Sohlh1 is essential for spermatogonial differentiation. Developmental Biology 294, 161–167.CrossRefGoogle ScholarPubMed
Behringer, RR, Finegold, MJ, Cate, RL 1994. Mullerian-inhibiting substance function during mammalian sexual development. Cell 79, 415–425.CrossRefGoogle ScholarPubMed
Bergmann, JA, Hohenboken, WD 1992. Prediction of fertility from calfhood traits of Angus and Simmental heifers. Journal of Animal Science 70, 2611–2621.CrossRefGoogle ScholarPubMed
Beverdam, A, Koopman, P 2006. Expression profiling of purified mouse gonadal somatic cells during the critical time window of sex determination reveals novel candidate genes for human sexual dysgenesis syndromes. Human Molecular Genetics 15, 417–431.CrossRefGoogle ScholarPubMed
Boichard, D, Grohs, C, Bourgeois, F, Cerqueira, F, Faugeras, R, Neau, A, Rupp, R, Amigues, Y, Boscher, MY, Leveziel, H 2003. Detection of genes influencing economic traits in three French dairy cattle breeds. Genetics Selection Evolution 35, 77–101.CrossRefGoogle ScholarPubMed
Bolor, H, Wakasugi, N, Zhao, WD, Ishikawa, A 2006. Detection of quantitative trait loci causing abnormal spermatogenesis and reduced testis weight in the small testis (Smt) mutant mouse. Experimental Animals 55, 97–108.CrossRefGoogle ScholarPubMed
Bormann, JM, Totir, LR, Kachman, SD, Fernando, RL, Wilson, DE 2006. Pregnancy rate and first-service conception rate in Angus heifers. Journal of Animal Science 84, 2022–2025.CrossRefGoogle ScholarPubMed
Brockmann, GA, Bevova, MR 2002. Using mouse models to dissect the genetics of obesity. Trends in Genetics 18, 367–376.CrossRefGoogle ScholarPubMed
Buaas, FW, Kirsh, AL, Sharma, M, McLean, DJ, Morris, JL, Griswold, MD, de Rooij, DG, Braun, RE 2004. Plzf is required in adult male germ cells for stem cell self-renewal. Nature Genetics 36, 647–652.CrossRefGoogle ScholarPubMed
Burgio, G, Szatanik, M, Guenet, JL, Arnau, MR, Panthier, JJ, Montagutelli, X 2007. Interspecific recombinant congenic strains between C57BL/6 and mice of the Mus spretus species: a powerful tool to dissect genetic control of complex traits. Genetics 177, 2321–2333.CrossRefGoogle ScholarPubMed
Cederroth, CR, Pitetti, JL, Papaioannou, MD, Nef, S 2007. Genetic programs that regulate testicular and ovarian development. Molecular and Cellular Endocrinology 265–266, 3–9.CrossRefGoogle ScholarPubMed
Chang, C, Chen, YT, Yeh, SD, Xu, Q, Wang, RS, Guillou, F, Lardy, H, Yeh, S 2004. Infertility with defective spermatogenesis and hypotestosteronemia in male mice lacking the androgen receptor in Sertoli cells. Proceedings of the National Academy of Sciences USA 101, 6876–6881.CrossRefGoogle ScholarPubMed
Chang, H, Matzuk, MM 2001. Smad5 is required for mouse primordial germ cell development. Mechanisms of Development 104, 61–67.CrossRefGoogle ScholarPubMed
Chu, DS, Liu, H, Nix, P, Wu, TF, Ralston, EJ, Yates, JR III, Meyer, BJ 2006. Sperm chromatin proteomics identifies evolutionarily conserved fertility factors. Nature 443, 101–105.CrossRefGoogle ScholarPubMed
Chubb, C, Nolan, C 1987. Mouse hybrid sterility and testicular function. Biology of Reproduction 36, 1343–1348.CrossRefGoogle ScholarPubMed
Cram, DS, Ma, K, Bhasin, S, Arias, J, Pandjaitan, M, Chu, B, Audrins, MS, Saunders, D, Quinn, F, deKretser, D, McLachlan, R 2000. Y chromosome analysis of infertile men and their sons conceived through intracytoplasmic sperm injection: vertical transmission of deletions and rarity of de novo deletions. Fertility and Sterility 74, 909–915.CrossRefGoogle ScholarPubMed
De Gendt, K, Atanassova, N, Tan, KA, de Franca, LR, Parreira, GG, McKinnell, C, Sharpe, RM, Saunders, PT, Mason, JI, Hartung, S, Ivell, R, Denolet, E, Verhoeven, G 2005. Development and function of the adult generation of Leydig cells in mice with Sertoli cell-selective or total ablation of the androgen receptor. Endocrinology 146, 4117–4126.CrossRefGoogle ScholarPubMed
de Sousa Lopes, SM, Roelen, BA, Monteiro, RM, Emmens, R, Lin, HY, Li, E, Lawson, KA, Mummery, CL 2004. BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo. Genes and Development 18, 1838–1849.CrossRefGoogle ScholarPubMed
Dierich, A, Sairam, MR, Monaco, L, Fimia, GM, Gansmuller, A, LeMeur, M, Sassone-Corsi, P 1998. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proceedings of the National Academy of Sciences USA 95, 13612–13617.CrossRefGoogle ScholarPubMed
Dong, J, Albertini, DF, Nishimori, K, Kumar, TR, Lu, N, Matzuk, MM 1996. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531–535.CrossRefGoogle ScholarPubMed
Donovan, PJ, Reed, SI 2003. Germline exclusion of Cks1 in the mouse reveals a metaphase I role for Cks proteins in male and female meiosis. Cell Cycle 2, 275–276.CrossRefGoogle ScholarPubMed
Dupont, S, Krust, A, Gansmuller, A, Dierich, A, Chambon, P, Mark, M 2000. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development (Cambridge, England) 127, 4277–4291.CrossRefGoogle ScholarPubMed
Farini, D, Scaldaferri, ML, Iona, S, La Sala, G, De Felici, M 2005. Growth factors sustain primordial germ cell survival, proliferation and entering into meiosis in the absence of somatic cells. Developmental Biology 285, 49–56.CrossRefGoogle ScholarPubMed
Feng, HL 2003. Molecular biology of male infertility. Archives of Andrology 49, 19–27.CrossRefGoogle ScholarPubMed
Forbes, A, Lehmann, R 1998. Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development (Cambridge, England) 125, 679–690.CrossRefGoogle ScholarPubMed
Furnes, B, Schimenti, J 2007. Fast forward to new genes in mammalian reproduction. Journal of Physiology 578, 25–32.CrossRefGoogle ScholarPubMed
Galloway, SM, McNatty, KP, Cambridge, LM, Laitinen, MP, Juengel, JL, Jokiranta, TS, McLaren, RJ, Luiro, K, Dodds, KG, Montgomery, GW, Beattie, AE, Davis, GH, Ritvos, O 2000. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nature Genetics 25, 279–283.CrossRefGoogle Scholar
Garcia-Ispierto, I, Lopez-Gatius, F, Santolaria, P, Yaniz, JL, Nogareda, C, Lopez-Bejar, M 2007. Factors affecting the fertility of high producing dairy herds in northeastern Spain. Theriogenology 67, 632–638.CrossRefGoogle ScholarPubMed
Giudice, LC 2003. Elucidating endometrial function in the post-genomic era. Human Reproduction Update 9, 223–235.CrossRefGoogle ScholarPubMed
Guenet, JL, Bonhomme, F 2003. Wild mice: an ever-increasing contribution to a popular mammalian model. Trends in Genetics 19, 24–31.CrossRefGoogle ScholarPubMed
Guillaume, F, Gautier, M, Ben Jemaa, S, Fritz, S, Eggen, A, Boichard, D, Druet, T 2007. Refinement of two female fertility QTL using alternative phenotypes in French Holstein dairy cattle. Animal Genetics 38, 72–74.CrossRefGoogle ScholarPubMed
Hale, DW, Washburn, LL, Eicher, EM 1993. Meiotic abnormalities in hybrid mice of the C57BL/6J × Mus spretus cross suggest a cytogenetic basis for Haldane’s rule of hybrid sterility. Cytogenetics and Cell Genetics 63, 221–234.CrossRefGoogle ScholarPubMed
Holmberg, M, Andersson-Eklund, L 2006. Quantitative trait loci affecting fertility and calving traits in Swedish dairy cattle. Journal of Dairy Science 89, 3664–3671.CrossRefGoogle ScholarPubMed
Holmberg, M, Sahana, G, Andersson-Eklund, L 2007. Fine mapping of a quantitative trait locus on chromosome 9 affecting non-return rate in Swedish dairy cattle. Journal of Animal Breeding and Genetics 124, 257–263.CrossRefGoogle ScholarPubMed
Holt, JE, Jackson, A, Roman, SD, Aitken, RJ, Koopman, P, McLaughlin, EA 2006. CXCR4/SDF1 interaction inhibits the primordial to primary follicle transition in the neonatal mouse ovary. Developmental Biology 293, 449–460.CrossRefGoogle ScholarPubMed
Hu, YC, Wang, PH, Yeh, S, Wang, RS, Xie, C, Xu, Q, Zhou, X, Chao, HT, Tsai, MY, Chang, C 2004. Subfertility and defective folliculogenesis in female mice lacking androgen receptor. Proceedings of the National Academy of Sciences USA 101, 11209–11214.CrossRefGoogle ScholarPubMed
Jamin, SP, Arango, NA, Mishina, Y, Hanks, MC, Behringer, RR 2002. Requirement of Bmpr1a for Mullerian duct regression during male sexual development. Nature Genetics 32, 408–410.CrossRefGoogle ScholarPubMed
Jamrozik, J, Fatehi, J, Kistemaker, GJ, Schaeffer, LR 2005. Estimates of genetic parameters for Canadian Holstein female reproduction traits. Journal of Dairy Science 88, 2199–2208.CrossRefGoogle ScholarPubMed
Jin, J, Jin, N, Zheng, H, Ro, S, Tafolla, D, Sanders, KM, Yan, W 2007. Catsper3 and Catsper4 are essential for sperm hyperactivated motility and male fertility in the mouse. Biology of Reproduction 77, 37–44.CrossRefGoogle ScholarPubMed
Kirkpatrick, BW, Byla, BM, Gregory, KE 2000. Mapping quantitative trait loci for bovine ovulation rate. Mammalian Genome 11, 136–139.CrossRefGoogle ScholarPubMed
Koopman, P 1999. Sry and Sox9: mammalian testis-determining genes. Cellular and Molecular Life Science 55, 839–856.Google ScholarPubMed
Krewson, TD, Supelak, PJ, Hill, AE, Singer, JB, Lander, ES, Nadeau, JH, Palmert, MR 2004. Chromosomes 6 and 13 harbor genes that regulate pubertal timing in mouse chromosome substitution strains. Endocrinology 145, 4447–4451.CrossRefGoogle ScholarPubMed
Kumar, TR, Wang, Y, Lu, N, Matzuk, MM 1997. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nature Genetics 15, 201–204.CrossRefGoogle Scholar
L’Hote, D, Serres, C, Laissue, P, Oulmouden, A, Rogel-Gaillard, C, Montagutelli, X, Vaiman, D 2007. Centimorgan-range one-step mapping of fertility traits using interspecific recombinant congenic mice. Genetics 176, 1907–1921.CrossRefGoogle ScholarPubMed
Laissue, P, Burgio, G, L’Hôte, D, Renault, G, Marchiol-Fournigault, C, Fradelizi, D, Fellous, M, Serres, C, Montagutelli, X, Monget, P, Vaiman, D 2008. An in vivo approach of the embryonic development in an interspecific recombinant congenic mice model reveals QTL responsible for embryonic lethality and resorption. International Journal of Developmental Biology (in press).Google Scholar
Lawson, KA, Dunn, NR, Roelen, BA, Zeinstra, LM, Davis, AM, Wright, CV, Korving, JP, Hogan, BL 1999. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes and Development 13, 424–436.CrossRefGoogle ScholarPubMed
Le Roy, I, Tordjman, S, Migliore-Samour, D, Degrelle, H, Roubertoux, PL 2001. Genetic architecture of testis and seminal vesicle weights in mice. Genetics 158, 333–340.CrossRefGoogle ScholarPubMed
Lien, S, Karlsen, A, Klemetsdal, G, Vage, DI, Olsaker, I, Klungland, H, Aasland, M, Heringstad, B, Ruane, J, Gomez-Raya, L 2000. A primary screen of the bovine genome for quantitative trait loci affecting twinning rate. Mammalian Genome 11, 877–882.CrossRefGoogle ScholarPubMed
Liljander, M, Sallstrom, MA, Andersson, S, Wernhoff, P, Andersson, A, Holmdahl, R, Mattsson, R 2006. Identification of genetic regions of importance for reproductive performance in female mice. Genetics 173, 901–909.CrossRefGoogle ScholarPubMed
Lopez-Gatius, F, Garcia-Ispierto, I, Santolaria, P, Yaniz, J, Nogareda, C, Lopez-Bejar, M 2006. Screening for high fertility in high-producing dairy cows. Theriogenology 65, 1678–1689.CrossRefGoogle ScholarPubMed
Lubahn, DB, Moyer, JS, Golding, TS, Couse, JF, Korach, KS, Smithies, O 1993. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proceedings of the National Academy of Sciences USA 90, 11162–11166.CrossRefGoogle Scholar
Mason, AJ, Pitts, SL, Nikolics, K, Szonyi, E, Wilcox, JN, Seeburg, PH, Stewart, TA 1986. The hypogonadal mouse: reproductive functions restored by gene therapy. Science 234, 1372–1378.CrossRefGoogle ScholarPubMed
Matsuda, Y, Chapman, VM 1991. In situ analysis of centromeric satellite DNA segregating in Mus species crosses. Mammalian Genome 1, 71–77.CrossRefGoogle ScholarPubMed
Matsuda, Y, Moens, PB, Chapman, VM 1992. Deficiency of X and Y chromosomal pairing at meiotic prophase in spermatocytes of sterile interspecific hybrids between laboratory mice (Mus domesticus) and Mus spretus. Chromosoma 101, 483–492.CrossRefGoogle ScholarPubMed
Meschede, D, Lemcke, B, Behre, HM, De Geyter, C, Nieschlag, E, Horst, J 2000. Clustering of male infertility in the families of couples treated with intracytoplasmic sperm injection. Human Reproduction 15, 1604–1608.CrossRefGoogle ScholarPubMed
Molyneaux, KA, Zinszner, H, Kunwar, PS, Schaible, K, Stebler, J, Sunshine, MJ, O’Brien, W, Raz, E, Littman, D, Wylie, C, Lehmann, R 2003. The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development (Cambridge, England) 130, 4279–4286.CrossRefGoogle ScholarPubMed
Mulsant, P, Lecerf, F, Fabre, S, Schibler, L, Monget, P, Lanneluc, I, Pisselet, C, Riquet, J, Monniaux, D, Callebaut, I, Cribiu, E, Thimonier, J, Teyssier, J, Bodin, L, Cognie, Y, Chitour, N, Elsen, JM 2001. Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Merino ewes. Proceedings of the National Academy of Sciences USA 98, 5104–5109.CrossRefGoogle ScholarPubMed
Neesen, J, Kirschner, R, Ochs, M, Schmiedl, A, Habermann, B, Mueller, C, Holstein, AF, Nuesslein, T, Adham, I, Engel, W 2001. Disruption of an inner arm dynein heavy chain gene results in asthenozoospermia and reduced ciliary beat frequency. Human Molecular Genetics 10, 1117–1128.CrossRefGoogle ScholarPubMed
Nef, S, Schaad, O, Stallings, NR, Cederroth, CR, Pitetti, JL, Schaer, G, Malki, S, Dubois-Dauphin, M, Boizet-Bonhoure, B, Descombes, P, Parker, KL, Vassalli, JD 2005. Gene expression during sex determination reveals a robust female genetic program at the onset of ovarian development. Developmental Biology 287, 361–377.CrossRefGoogle ScholarPubMed
Niwa, H, Miyazaki, J, Smith, AG 2000. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics 24, 372–376.CrossRefGoogle ScholarPubMed
Oka, A, Mita, A, Sakurai-Yamatani, N, Yamamoto, H, Takagi, N, Takano-Shimizu, T, Toshimori, K, Moriwaki, K, Shiroishi, T 2004. Hybrid breakdown caused by substitution of the X chromosome between two mouse subspecies. Genetics 166, 913–924.CrossRefGoogle ScholarPubMed
Oka, A, Aoto, T, Totsuka, Y, Takahashi, R, Ueda, M, Mita, A, Sakurai-Yamatani, N, Yamamoto, H, Kuriki, S, Takagi, N, Moriwaki, K, Shiroishi, T 2007. Disruption of genetic interaction between two autosomal regions and the x chromosome causes reproductive isolation between mouse strains derived from different subspecies. Genetics 175, 185–197.CrossRefGoogle ScholarPubMed
Ottolenghi, C, Pelosi, E, Tran, J, Colombino, M, Douglass, E, Nedorezov, T, Cao, A, Forabosco, A, Schlessinger, D 2007. Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Human Molecular Genetics 16, 2795–2804.CrossRefGoogle ScholarPubMed
Paria, BC, Lim, H, Wang, XN, Liehr, J, Das, SK, Dey, SK 1998. Coordination of differential effects of primary estrogen and catecholestrogen on two distinct targets mediates embryo implantation in the mouse. Endocrinology 139, 5235–5246.CrossRefGoogle ScholarPubMed
Paria, BC, Song, H, Dey, SK 2001. Implantation: molecular basis of embryo-uterine dialogue. International Journal of Developmental Biology 45, 597–605.Google ScholarPubMed
Peripato, AC, De Brito, RA, Matioli, SR, Pletscher, LS, Vaughn, TT, Cheverud, JM 2004. Epistasis affecting litter size in mice. Journal of Evolution Biology 17, 593–602.CrossRefGoogle ScholarPubMed
Pilder, SH, Lu, J, Han, Y, Hui, L, Samant, SA, Olugbemiga, OO, Meyers, KW, Cheng, L, Vijayaraghavan, S 2007. The molecular basis of ‘curlicue’: a sperm motility abnormality linked to the sterility of t haplotype homozygous male mice. Soc Reproduction and Fertility Supplement 63, 123–133.Google Scholar
Quill, TA, Sugden, SA, Rossi, KL, Doolittle, LK, Hammer, RE, Garbers, DL 2003. Hyperactivated sperm motility driven by CatSper2 is required for fertilization. Proceedings of the National Academy of Sciences USA 100, 14869–14874.CrossRefGoogle ScholarPubMed
Rajkovic, A, Pangas, SA, Ballow, D, Suzumori, N, Matzuk, MM 2004. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305, 1157–1159.CrossRefGoogle ScholarPubMed
Ren, D, Navarro, B, Perez, G, Jackson, AC, Hsu, S, Shi, Q, Tilly, JL, Clapham, DE 2001. A sperm ion channel required for sperm motility and male fertility. Nature 413, 603–609.CrossRefGoogle ScholarPubMed
Rinchik, EM, Johnson, DK, Margolis, FL, Jackson, IJ, Russell, LB, Carpenter, DA 1991. Reverse genetics in the mouse and its application to the study of deafness. Annals of the New York Academy of Sciences 630, 80–92.CrossRefGoogle Scholar
Rocha, JL, Eisen, EJ, Siewerdt, F, Van Vleck, LD, Pomp, D 2004. A large-sample QTL study in mice: III. Reproduction. Mammalian Genome 15, 878–886.CrossRefGoogle ScholarPubMed
Roy, A, Matzuk, MM 2006. Deconstructing mammalian reproduction: using knockouts to define fertility pathways. Reproduction 131, 207–219.CrossRefGoogle ScholarPubMed
Russell, WL, Kelly, EM, Hunsicker, PR, Bangham, JW, Maddux, SC, Phipps, EL 1979. Specific-locus test shows ethylnitrosourea to be the most potent mutagen in the mouse. Proceedings of the National Academy of Sciences USA 76, 5818–5819.CrossRefGoogle ScholarPubMed
Saitou, M, Barton, SC, Surani, MA 2002. A molecular programme for the specification of germ cell fate in mice. Nature 418, 293–300.CrossRefGoogle ScholarPubMed
Samant, SA, Ogunkua, OO, Hui, L, Lu, J, Han, Y, Orth, JM, Pilder, SH 2005. The mouse t complex distorter/sterility candidate, Dnahc8, expresses a gamma-type axonemal dynein heavy chain isoform confined to the principal piece of the sperm tail. Developmental Biology 285, 57–69.CrossRefGoogle Scholar
Schnabel, RD, Sonstegard, TS, Taylor, JF, Ashwell, MS 2005. Whole-genome scan to detect QTL for milk production, conformation, fertility and functional traits in two US Holstein families. Animal Genetics 36, 408–416.CrossRefGoogle ScholarPubMed
Schulman, NF, Sahana, G, Lund, MS, Viitala, SM, Vilkki, JH 2008. Quantitative trait loci for fertility traits in Finnish Ayrshire cattle. Genetics Selection Evolution 40, 195–214.Google ScholarPubMed
Soyal, SM, Amleh, A, Dean, J 2000. FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. Development (Cambridge, England) 127, 4645–4654.CrossRefGoogle ScholarPubMed
Takeuchi, A, Mishina, Y, Miyaishi, O, Kojima, E, Hasegawa, T, Isobe, K 2003. Heterozygosity with respect to Zfp148 causes complete loss of fetal germ cells during mouse embryogenesis. Nature Genetics 33, 172–176.CrossRefGoogle ScholarPubMed
Talbi, S, Hamilton, AE, Vo, KC, Tulac, S, Overgaard, MT, Dosiou, C, Le Shay, N, Nezhat, CN, Kempson, R, Lessey, BA, Nayak, NR, Giudice, LC 2006. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 147, 1097–1121.CrossRefGoogle ScholarPubMed
Toure, A, Lhuillier, P, Gossen, JA, Kuil, CW, Lhote, D, Jegou, B, Escalier, D, Gacon, G 2007. The testis anion transporter 1 (Slc26a8) is required for sperm terminal differentiation and male fertility in the mouse. Human Molecular Genetics 16, 1783–1793.CrossRefGoogle ScholarPubMed
Tremblay, KD, Dunn, NR, Robertson, EJ 2001. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development (Cambridge, England) 128, 3609–3621.CrossRefGoogle ScholarPubMed
Vaiman, D 2002. Fertility, sex determination, and the X chromosome. Cytogenetics and Genome Research 99, 224–228.CrossRefGoogle ScholarPubMed
Vaiman, D 2003. Sexy transgenes: the impact of gene transfer and gene inactivation technologies on the understanding of mammalian sex determination. Transgenic Research 12, 255–269.CrossRefGoogle ScholarPubMed
Vaiman, D, Pailhoux, E 2000. Mammalian sex reversal and intersexuality: deciphering the sex-determination cascade. Trends in Genetics 16, 488–494.CrossRefGoogle ScholarPubMed
Vainio, S, Heikkilä, M, Kispert, A, Chin, N, McMahon, AP 1999. Female development in mammals is regulated by Wnt-4 signalling. Nature 397, 405–409.CrossRefGoogle ScholarPubMed
Valdar, W, Solberg, LC, Gauguier, D, Burnett, S, Klenerman, P, Cookson, WO, Taylor, MS, Rawlins, JN, Mott, R, Flint, J 2006. Genome-wide genetic association of complex traits in heterogeneous stock mice. Nature Genetics 38, 879–887.CrossRefGoogle ScholarPubMed
Vincent, SD, Dunn, NR, Sciammas, R, Shapiro-Shalef, M, Davis, MM, Calame, K, Bikoff, EK, Robertson, EJ 2005. The zinc finger transcriptional repressor Blimp1/Prdm1 is dispensable for early axis formation but is required for specification of primordial germ cells in the mouse. Development (Cambridge, England) 132, 1315–1325.CrossRefGoogle ScholarPubMed
Walters, KA, Allan, CM, Jimenez, M, Lim, PR, Davey, RA, Zajac, JD, Illingworth, P, Handelsman, DJ 2007. Female mice haploinsufficient for an inactivated androgen receptor (AR) exhibit age-dependent defects that resemble the AR null phenotype of dysfunctional late follicle development, ovulation, and fertility. Endocrinology 148, 3674–3684.CrossRefGoogle ScholarPubMed
Ying, Y, Zhao, GQ 2001. Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Developmental Biology 232, 484–492.CrossRefGoogle ScholarPubMed
Ying, Y, Liu, XM, Marble, A, Lawson, KA, Zhao, GQ 2000. Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Molecular Endocrinology 14, 1053–1063.CrossRefGoogle ScholarPubMed
Yoshinaga, K, Nishikawa, S, Ogawa, M, Hayashi, S, Kunisada, T, Fujimoto, T 1991. Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development (Cambridge, England) 113, 689–699.CrossRefGoogle ScholarPubMed
Zídek, V, Musilovà, A, Pintir, J, Simakova, M, Pravenec, M 1998. Genetic dissection of testicular weight in the mouse with the BXD recombinant inbred strains. Mammalian Genome 9, 503–505.Google ScholarPubMed