Reproduction in Domestic Animals

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370 JP Kastelic and JC Thundathilsperm–oocyte interactions. Following capacitation,sperm interact with the zona pellucida (ZP). For thisinteraction, galactosyl transferase (Larson and Miller2000), p47 (Ensslin et al. 1998), sp56 (Cheng et al. 1994)and zonadhesin (Hardy and Garbers 1995) are apparentlysperm receptors, whereas zona glycoprotein (ZP3)is the ligand (Yanagimachi 1994). This interaction leadsto an acrosome reaction (Yanagimachi 1994); the inneracrosomal membrane interacts with a second glycoprotein,ZP2, facilitating the secondary binding of sperm tothe zona matrix during penetration (Yanagimachi 1994;Aitken 2006).There are several reports regarding the associationbetween sperm–zona binding and fertility. There weredifferences among bulls (with known fertility) in therelative number of sperm bound to bovine oocytes(Fazeli et al. 1993). However, large numbers of oocytesare needed and differences among bulls are detectableonly if they exceed differences among oocytes (Zhanget al. 1995). Alternatively, a hemizona assay (Fazeliet al. 1997) uses both halves of a ZP to compare bindingability of control sperm (known fertility) and test sperm(unknown fertility). Zona binding and hemizona bindingassays and non-return rates were significantlycorrelated. In vitro zona penetration assays have beenused to predict in vivo fertility (Puglisi et al. 2004).However, sperm penetration varies according to sperm–oocyte ratio, duration of incubation and heparin concentration,limiting the value of this test.Sperm Oolemma Fusion and Sperm DNADecondensationHenault et al. (1995) used a homologous zona-freeoocyte penetration assay to demonstrate the effects ofaccessory gland fluid from low- vs high-fertility bulls.Moreover, competitive penetration of zona-free bovineoocytes by fluorochrome-labelled bull sperm was relatedto in vivo fertility (Henault and Killian 1995) andevaluated the ability of sperm to undergo chromatindecondensation and pronucleus formation. In theabsence of a ZP, there is an equal opportunity for allsperm to fuse with the oocyte membrane, undergo DNAdecondensation and pronuclei formation (Thundathilet al. 2001a).Sperm chromatin integrity is an important determinantof the ability of sperm to form normal pronuclei.Sperm DNA is associated with histone nucleoproteinsand organized into classical nucleosome core particlesduring early spermatogenesis. However, these histonenucleoproteins are replaced by transition proteins,which are subsequently replaced by protamines (Yanagimachi1994). Ultimately, chromatin of mature spermhas a compact toroidal structure that resists denaturation.Lewis and Aitken (2005) suggested oxidativestress was a major cause of sperm DNA damage, withreduced pre-implantation embryo development andpregnancy rates. Increased testicular temperature reducedthe stability of sperm DNA (Karabinus et al.1997) and impaired the ability of these sperm to undergoDNA decondensation and pronuclei formation (Walterset al. 2006). However, links among elevated testiculartemperature, oxidative stress and sperm DNA damagein bulls remain unclear. The sperm cell structure assay(SCSA) uses flow cytometry to determine chromatinintegrity, based on resistance to acid denaturation.Sperm are exposed to low pH and stained with acridineorange, which emits green or red fluorescence when itbinds to double- (intact) or single-stranded DNA(denatured), respectively. The ratio of red to (red + -green) fluorescence measures chromatin denaturation,which is significantly correlated with fertility (Ballacheyet al. 1987, 1988; Januskauskas et al. 2001; Waterhouseet al. 2006). In brief, flow cytometry-based approachesprovide a quantitative measure of the structural integrityof sperm chromatin, based on a large number ofsperm, whereas IVF-based tests evaluate the ability ofsperm to undergo DNA decondensation and pronuclearformation during fertilization.Association Between In Vitro Fertilization andFertilityMarquant-Le Guienne et al. (1990) reported that pronuclearformation can be used to predict field fertility ofbulls. Zhang et al. (1997) reported that fertilizationbased on cleavage rate was highly correlated with nonreturnrates, but blastocyst production varied amongtest dates. However, fertility predictions were moreaccurate when based on several laboratory assays vs asingle assay (Truelson et al. 1996). In this regard, aseven-variable model (post-thaw total motility, postthawsperm with a linear motile pattern, sperm concentration,concentration of motile sperm after swim-up,sperm ZP-binding, cleavage rate of total oocytes andblastocyst rate of total oocytes) accounted for 84.6% ofthe variation in non-return rates (Zhang et al. 1999).However, this approach may not be sensitive enough todiscriminate among highly fertile bulls. Similarly, amodel with 30 post-thaw sperm characteristics (includingcleavage rate) accurately predicted fertility (based onconception and non-return rates) of both high- and lowfertilitybulls (Phillips et al. 2004).Future DirectionsThe cell biology approaches described earlier may serveas supplementary tests to a standard breeding soundnessevaluation and improve the reliability of fertility predictions.However, a better understanding of the regulationof sperm function and its contributions to earlyembryo development at the molecular level may lead toreliable molecular markers of fertility, with implicationsfor predicting fertility variations in bulls used for AI.As DNA is transcriptionally inactive in ejaculatedsperm, physiological functions are regulated by structuraland functional proteins and identifying theseproteins may have implications for predicting fertility.The role of heat-shock proteins in sperm capacitation(Kamaruddin et al. 2004) and their potential role insperm–oocyte binding have been reported (Matweeet al. 2001). Specific sperm proteins involved in theinteraction between sperm and ZP (Larson and Miller2000; Inoue et al. 2005) and sperm–oocyte adhesion andegg activation (Evans and Florman 2002) have beenidentified, and the role of angiotensin converting enzymeÓ 2008 The Authors. Journal compilation Ó 2008 Blackwell Verlag
Breeding Soundness and Semen Analysis in Bulls 371(ACE) in fertilization (Kondoh et al. 2005) has beendescribed. In addition, PAWP, a sperm-specific WWdomain-binding protein, promotes meiotic resumptionand pronuclear development during fertilization (Wuet al. 2007).We recently used scrotal insulation to induce abnormalspermatogenesis (unpublished) and identified spermproteins associated with abnormal spermatogenesis as aresult of elevated testicular temperature. There wasdifferential expression (between normal and abnormalsperm of the same bull) of the alpha 4 subunit ofNa + ⁄ K + ATPase, tissue inhibitor of metalloproteinase-2 (TIMP-2), ACE and hexokinase-1. Further studies areneeded to elucidate the specific role of these spermproteins in fertilization and early development.Although the sperm proteins described earlier areassociated with the regulation of specific sperm functions,proteins with changes in expression patterns inresponse to variations in fertility remain unknown, buthave great potential as fertility markers. In this regard,heparin-binding proteins (24–31 kDa) were proposed asa genetic marker for fertility differences in bullsproducing normal semen (Bellin et al. 1998; McCauleyet al. 1999). Furthermore, there are associations betweenspecific seminal plasma proteins and fertility(Killian et al. 1993; Moura et al. 2006). Sperm proteinsfrom low- vs high-fertility Nelore bulls with acceptablesemen had differential expression (two-dimensional gelelectrophoresis) of sperm membrane proteins (Roncolettaet al. 2006). Similarly, accessory gland fluids fromhigh-fertility Holstein bulls had more bovine seminalplasma protein (BSP) 30 kDa and phospholipase A2,whereas osteopontin appeared to improve the ability ofepididymal sperm (from low-fertility bulls) to penetrateoocytes in vitro (Moura et al. 2007). Therefore, identifyingfertility-associated sperm or seminal plasma proteinsby comparing low- vs high-fertility bulls, andinvestigating the role of these proteins in the regulationof sperm function, fertilization or embryo development,may identify markers that predict fertility.Morphologically abnormal sperm failed during gameteinteraction or pre-implantation development (Thundathilet al. 2000, 2001b; Walters et al. 2005). Inaddition, embryos resulting from the fertilization ofoocytes by morphologically normal sperm, coexisting inthe ejaculate along with abnormal sperm, had reduceddevelopmental competence, suggesting that these spermwere functionally impaired. Therefore, increasing theinsemination dose to compensate for infertility as aresult of compensable factors (Saacke et al. 2000)requires further investigation. Data from commercialembryo production units suggested that bulls differ intheir ability to produce pre-implantation embryos in vivo(Thundathil and Mapletoft, unpublished data). In thisregard, damage to sperm DNA because of oxidativestress, chromosome anomalies and environmental effects,including elevated testicular temperature, time ofAI relative to oestrus, duration of semen storage,duration of sperm–oocyte interaction, age of malesand infectious agents in semen influence quality ofembryos (reviewed by Chenoweth 2007). However, morestudies are needed to elucidate the effects of paternalgenes (Browing and Strome 1996), sperm RNA(Krawetz 2005; Miller et al. 2005; Miller and Ostermeier2006; Boerke et al. 2007), specific sperm and seminalplasma proteins (Cancel et al. 1997; McCauley et al.2001; Roncoletta et al. 2006) and evolutionarily conservedfactors associated with sperm DNA (Wu andChu 2008) on fertilization and early embryo development.As fertility is affected by numerous factors, thesearch for fertility markers should include the wholeanimallevel. Bovine testes must be 4–5°C below bodycoretemperature (38°C) for normal spermatogenesis(Setchell 1978). Assessment of scrotal surface temperatureswith infrared thermography (scrotal thermogram)provided detailed information regarding a bull’sability to regulate testicular temperature (Coulter 1988;Kastelic et al. 2000). Beef bulls with abnormal scrotalthermograms had lower fertility to natural service(Lunstra and Coulter 1997). Furthermore, ultrasonographicevaluations of the testicular vascular cone andits fat cover were indicative of thermoregulatorycapability, and associated with semen productionpotential and semen quality (Kastelic et al. 2001;Arteaga et al. 2005).ConclusionA traditional breeding soundness examination willusually identify bulls that are grossly abnormal. However,a comprehensive approach, including assessingsperm function and fertility at the molecular, cellularand whole-animal levels, is needed to predict fertility ofbulls that are producing apparently normal sperm.ReferencesAitken RJ, 2006: Sperm function tests and fertility. Int JAndrol 29, 69–75.Anzar M, He L, Buhr MM, Kroetsch TG, Pauls KP, 2002:Sperm apoptosis in fresh and cryopreserved bull semendetected by flow cytometry and its relationship with fertility.Biol Reprod 66, 354–360.Arteaga AA, Barth AD, Brito LF, 2005: Relationship betweensemen quality and pixel-intensity of testicular ultrasonogramsafter scrotal insulation in beef bulls. Theriogenology64, 408–415.Ballachey BE, Hohenboken WD, Evenson DP, 1987: Heterogeneityof sperm nuclear chromatin structure and itsrelationship to bull fertility. Biol Reprod 36, 915–925.Ballachey BE, Evenson DP, Saacke RG, 1988: The spermchromatin structure assay. Relationship with alternate testsof semen quality and heterospermic performance of bulls.J Androl 9, 109–115.Barth AD, 2007: Evaluation of potential breeding soundnessof the bull. in: Youngquist RS, Threlfall WR (eds), CurrentTherapy in Large Animal Theriogenology 2. SaundersElsevier, Philadelphia, pp. 228–240.Bellin ME, Oyarzo JN, Hawkins HE, Zhang H, Smith RG,Forrest DW, Sprott LR, Ax RL, 1998: Fertility-associatedantigen on bull sperm indicates fertility potential. J Anim Sci76, 2032–2039.Boerke A, Dieleman SJ, Gadella BM, 2007: A possible role forsperm RNA in early embryo development. Theriogenology68(Suppl. 1), S147–S155.Boilard M, Bailey J, Collin S, Dufour M, Sirard M-A, 2002:Effect of bovine oviduct epithelial cell apical plasmaÓ 2008 The Authors. Journal compilation Ó 2008 Blackwell Verlag
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Embryo Biotechnologies in Farm Anim
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Ethical Models for Studying Reprodu
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Dietary Pollutants as Risk Factors
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Factors Influencing Reproduction in
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GH and IGF-I in Cattle and Pigs 35h
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GH and IGF-I in Cattle and Pigs 37B
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GH and IGF-I in Cattle and Pigs 39R
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Seasonality of Reproduction in Mamm
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Dominant Follicle Selection in Cows
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Regulation of Luteal Function 59and
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Regulation of Luteal Function 61bov
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Captive Breeding of Cheetahs in Sou
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Non-invasive Monitoring of Hormones
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Genetic Improvement of Dairy Cow Re
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Reproductive Status Assessed by Mil
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Genetic Aspects of Reproduction in
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Developmental Capabilities of Prepu
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Reproductive Physiology, Pathology
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Canine Anoestrus, Oestrous Inductio
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The Ethics and Role of AI in Dogs 1
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Control of Fertility in Females by
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Controlling Animal Populations Usin
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Recombinant Gonadotropins in Assist
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Farm Animals Embryonic Stem Cells 1
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Postpartum Ovarian Activity in Sout
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Reproduction Augmentation in Yak an
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Follicles and Mares 2251982). Simil
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Follicles and Mares 227Studies invo
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Proteins in Early Equine Conceptuse
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Fertilization in the Porcine Fallop
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Mastitis in Post-Partum Dairy Cows
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Death Ligand and Receptor Pig Ovari
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Death Ligand and Receptor Pig Ovari
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Lactocrine Programming of Uterine D
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278 FF Bartol, AA Wiley and CA Bagn
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282 KC Caires, JA Schmidt, AP Olive
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Page 418 and 419: 410 B ObackReprogramming Ability of
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