Revisiting summer infertility in the pig: could heat stress-induced sperm DNA damage negatively affect early embryo development?

Animal Production Science - Tập 57 Số 10 - Trang 1975 - 2017
Santiago T. Peña1,2,3, Bruce Gummow3,4, A. J. Parker5, Damien B.B.P. Paris2
1College of Veterinary Medicine, Visayas State University, Baybay City, Leyte, 6521-A, Philippines.
2Discipline of Biomedical Science, College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Qld 4811, Australia.
3Discipline of Veterinary Science, College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Qld 4811, Australia.
4Faculty of Veterinary Science, University of Pretoria, Onderstepoort 0110, South Africa
5College of Food, Agricultural and Environmental Sciences, Ohio State University, Wooster, OH 44691, USA.

Tóm tắt

Temperature is a crucial factor in mammalian spermatogenesis. The scrotum, pampiniform plexus, and cremaster and dartos muscles in mammals are specific adaptations to ensure sperm production in a regulated environment 4−6°C below internal body temperature. However, the limited endogenous antioxidant systems inherent in mammalian spermatozoa compounded by the loss of cytosolic repair mechanisms during spermatogenesis, make the DNA in these cells particularly vulnerable to oxidative damage. Boar sperm is likely to be more susceptible to the effects of heat stress and thus oxidative damage due to the relatively high unsaturated fatty acids in the plasma membrane, low antioxidant capacity in boar seminal plasma, and the boar’s non-pendulous scrotum. Heat stress has a significant negative impact on reproductive performance in piggeries, which manifests as summer infertility and results in productivity losses that amount to millions of dollars. This problem is particularly prevalent in tropical and subtropical regions where ambient temperatures rise beyond the animal’s zone of thermal comfort. Based on preliminary studies in the pig and other species, this article discusses whether heat stress could induce sufficient DNA damage in boar sperm to significantly contribute to the high rates of embryo loss and pregnancy failure observed in the sow during summer infertility. Heat stress-induced damage to sperm DNA can lead to disrupted expression of key developmental genes essential for the differentiation of early cell lineages, such as the trophectoderm, and can distort the timely formation of the blastocyst; resulting in a failure of implantation and ultimately pregnancy loss. Confirming such a link would prompt greater emphasis on boar management and strategies to mitigate summer infertility during periods of heat stress.

Từ khóa


Tài liệu tham khảo

Ahmad, 1995, Acta Theriologica, 40, 163, 10.4098/AT.arch.95-17

Ahmadi, 1999, The Journal of Experimental Zoology, 284, 696, 10.1002/(SICI)1097-010X(19991101)284:6<696::AID-JEZ11>3.0.CO;2-E

Aitken, 2010, Molecular Human Reproduction, 16, 3, 10.1093/molehr/gap059

Aitken, 2012, Reproduction in Domestic Animals, 47, 7, 10.1111/j.1439-0531.2012.02049.x

Anderson, 1978, The Anatomical Record, 190, 143, 10.1002/ar.1091900112

Ashikawa, 1987, Biochimica et Biophysica Acta – Gene Structure and Expression, 908, 263, 10.1016/0167-4781(87)90106-0

Auvigne, 2010, Theriogenology, 74, 60, 10.1016/j.theriogenology.2009.12.019

Barratt, 2010, Human Reproduction (Oxford, England), 25, 824, 10.1093/humrep/dep465

Bazer, 2014, Differentiation, 87, 52, 10.1016/j.diff.2013.11.005

Bazer, 1977, Prostaglandins, 14, 397, 10.1016/0090-6980(77)90185-X

Bettegowda, 2007, Frontiers in Bioscience, 12, 3713, 10.2741/2346

Bloemhof, 2008, Journal of Animal Science, 86, 3330, 10.2527/jas.2008-0862

Boe-Hansen, 2005, Theriogenology, 63, 2006, 10.1016/j.theriogenology.2004.09.006

Boe-Hansen, 2008, Theriogenology, 69, 728, 10.1016/j.theriogenology.2007.12.004

Boma, 2006, The Onderstepoort Journal of Veterinary Research, 73, 229

Britt, 1983, Theriogenology, 20, 133, 10.1016/0093-691X(83)90032-8

Bruce, 2010, Current Opinion in Genetics & Development, 20, 485, 10.1016/j.gde.2010.05.006

Cameron, 1980, Journal of Reproduction and Fertility, 59, 173, 10.1530/jrf.0.0590173

Casady, 1953, Journal of Dairy Science, 36, 14, 10.3168/jds.S0022-0302(53)91449-0

Chazaud, 2006, Developmental Cell, 10, 615, 10.1016/j.devcel.2006.02.020

Cockburn, 2010, The Journal of Clinical Investigation, 120, 995, 10.1172/JCI41229

Cohen, 2003, Science, 302, 1172, 10.1126/science.1088665

Didion, 2009, Journal of Andrology, 30, 655, 10.2164/jandrol.108.006254

Dostàlovà, 1994, Biochimica et Biophysica Acta – General Subjects, 1200, 48, 10.1016/0304-4165(94)90026-4

Dostalova, 1995, European Journal of Biochemistry, 230, 329, 10.1111/j.1432-1033.1995.tb20567.x

du Puy, 2011, Theriogenology, 75, 513, 10.1016/j.theriogenology.2010.09.019

Egbunike, 1980, International Journal of Biometeorology, 24, 129, 10.1007/BF02253800

Einarsson, 2008, Acta Veterinaria Scandinavica, 50, 48, 10.1186/1751-0147-50-48

Ekhlasi-Hundrieser, 2005, Biology of Reproduction, 73, 536, 10.1095/biolreprod.105.040824

Enciso, 2006, Theriogenology, 65, 308, 10.1016/j.theriogenology.2005.05.044

Evenson, 1999, Reproduction, Fertility and Development, 11, 1, 10.1071/RD98023

Evenson, 2006, Theriogenology, 65, 979, 10.1016/j.theriogenology.2005.09.011

Evenson, 1994, Theriogenology, 41, 637, 10.1016/0093-691X(94)90174-H

Evenson, 2009, Reproduction, Fertility and Development, 21, 212, 10.1071/RDv21n1Ab228

Fatehi, 2006, Journal of Andrology, 27, 176, 10.2164/jandrol.04152

Fernandes, 2008, Theriogenology, 70, 1560, 10.1016/j.theriogenology.2008.07.005

Flowers, 1997, Journal of Reproduction and Fertility. Supplement, 52, 67

Flowers, 2008, Theriogenology, 70, 1297, 10.1016/j.theriogenology.2008.06.016

Fortes, 2014, Andrology, 2, 370, 10.1111/j.2047-2927.2014.00196.x

Gandini, 2000, Human Reproduction (Oxford, England), 15, 830, 10.1093/humrep/15.4.830

Gasperowicz, 2011, Biology of Reproduction, 84, 621, 10.1095/biolreprod.110.085209

Geisert, 2002, Journal of Animal Science, 80, E54

Geisert, 1989, Journal of Reproduction and Fertility. Supplement, 40, 293

Gholami, 2011, International Journal of Fertility & Sterility, 4, 160

10.2527/2006.842360x

Hall, 2009, Developmental Dynamics, 238, 2014, 10.1002/dvdy.22027

Hammoud, 2009, Nature, 460, 473, 10.1038/nature08162

Heitman, 1984, Animal Science, 38, 129, 10.1017/S0003356100041441

Henkel, 2004, Fertility and Sterility, 81, 965, 10.1016/j.fertnstert.2003.09.044

Hennessy, 1984, Australian Veterinary Journal, 61, 212, 10.1111/j.1751-0813.1984.tb05991.x

Huang, 2000, Animal Reproduction Science, 63, 231, 10.1016/S0378-4320(00)00175-5

Ingram, 1964, Research in Veterinary Science, 5, 357, 10.1016/S0034-5288(18)34801-X

Ingram, 1965, Nature, 207, 415, 10.1038/207415a0

Jeanblanc, 2008, Gynecologie, Obstetrique & Fertilite, 36, 1126, 10.1016/j.gyobfe.2008.07.015

Johnson, 2009, Society of Reproduction and Fertility. Supplement, 66, 321

Karabinus, 1997, Journal of Andrology, 18, 549, 10.1002/j.1939-4640.1997.tb01971.x

Krawetz, 2005, Nature Reviews. Genetics, 6, 633, 10.1038/nrg1654

Kuijk, 2008, Developmental Dynamics, 237, 918, 10.1002/dvdy.21480

Kumar, 2013, Clinics, 68, 5, 10.6061/clinics/2013(Sup01)02

Latham, 2001, Frontiers in Bioscience, 6, D748, 10.2741/A639

10.2527/1996.74suppl_336x

Lewis, 2005, Cell and Tissue Research, 322, 33, 10.1007/s00441-005-1097-5

López Rodríguez, 2013, Systems Biology in Reproductive Medicine, 59, 5, 10.3109/19396368.2012.725120

Love, 1978, The Veterinary Record, 103, 443, 10.1136/vr.103.20.443

Love, 1981, The Veterinary Record, 109, 407, 10.1136/vr.109.18.407

Love, 1999, Biology of Reproduction, 60, 615, 10.1095/biolreprod60.3.615

Macklon, 2002, Human Reproduction Update, 8, 333, 10.1093/humupd/8.4.333

Malmgren, 1989, Journal of Veterinary Medicine Series A, 36, 411, 10.1111/j.1439-0442.1989.tb00748.x

McMichael, 2007, Lancet, 370, 1253, 10.1016/S0140-6736(07)61256-2

McNitt, 1970, International Journal of Biometeorology, 14, 373, 10.1007/BF01462914

Messerschmidt, 2010, Developments in Biologicals, 344, 129, 10.1016/j.ydbio.2010.04.020

Meyer, 1994, Experimental and Clinical Endocrinology, 102, 190, 10.1055/s-0029-1211281

Minami, 2007, The Journal of Reproduction and Development, 53, 707, 10.1262/jrd.19029

Moule, 1963, Journal of Reproduction and Fertility, 5, 433, 10.1530/jrf.0.0050433

Nakamura, 1987, Systems Biology in Reproductive Medicine, 19, 127

Novak, 2010, Journal of Andrology, 31, 188, 10.2164/jandrol.109.007583

Okazaki, 2012, Journal of Andrology, 33, 990, 10.2164/jandrol.111.015115

Oron, 2012, Physical Biology, 9, 045002, 10.1088/1478-3975/9/4/045002

Paterson, 1978, Australian Journal of Experimental Agriculture, 18, 698, 10.1071/EA9780698

Paul, 2008, Molecular Human Reproduction, 14, 1, 10.1093/molehr/gam089

Paul, 2008, Reproduction (Cambridge, England), 136, 73, 10.1530/REP-08-0036

Pérez-Crespo, 2008, Molecular Reproduction and Development, 75, 40, 10.1002/mrd.20759

Pérez-Llano, 2010, Animal Reproduction Science, 119, 235, 10.1016/j.anireprosci.2010.01.002

Perry, 1962, Journal of Reproduction and Fertility, 4, 175, 10.1530/jrf.0.0040175

Petrocelli, 2015, Revista Brasileira de Zootecnia, 44, 1, 10.1590/S1806-92902015000100001

Prunier, 1997, Livestock Production Science, 52, 123, 10.1016/S0301-6226(97)00137-1

Quesnel, 2005, Institut national de la recherche agronomique Production Animales, 18, 101, 10.20870/productions-animales.2005.18.2.3513

Ralston, 2005, Clinical Genetics, 68, 106, 10.1111/j.1399-0004.2005.00478.x

Ralston, 2010, Reproduction (Cambridge, England), 139, 35, 10.1530/REP-09-0024

Rockett, 2001, Biology of Reproduction, 65, 229, 10.1095/biolreprod65.1.229

Rosell, 2012, Animal Biodiversity and Conservation, 35, 209, 10.32800/abc.2012.35.0209

Schulte, 2010, Journal of Assisted Reproduction and Genetics, 27, 3, 10.1007/s10815-009-9359-x

Setchell, 2006, Animal Reproduction, 3, 81

Shi, 2009, Reproductive Biology and Endocrinology, 7, 59, 10.1186/1477-7827-7-59

Silva, 2006, Livestock Science, 105, 176, 10.1016/j.livsci.2006.06.007

Silva, 2009, Cell, 138, 722, 10.1016/j.cell.2009.07.039

Spencer, 2013, Animal frontiers, 3, 48, 10.2527/af.2013-0033

St-Pierre, 2003, Journal of Dairy Science, 86, E52, 10.3168/jds.S0022-0302(03)74040-5

Stefańczyk-Krzymowska, 1990, Animal Reproduction Science, 23, 223, 10.1016/0378-4320(90)90005-Z

Stone, 1981, Journal of Reproduction and Fertility, 63, 551, 10.1530/jrf.0.0630551

Stone, 1982, Animal Reproduction Science, 4, 283, 10.1016/0378-4320(82)90043-4

Stone, 1984, Animal Reproduction Science, 7, 391, 10.1016/0378-4320(84)90041-1

Suriyasomboon, 2004, Livestock Production Science, 89, 19, 10.1016/j.livprodsci.2003.12.008

Suriyasomboon, 2006, Theriogenology, 65, 606, 10.1016/j.theriogenology.2005.06.005

Sutovsky, 2015, Reproduction in Domestic Animals, 50, 11, 10.1111/rda.12554

Tramontano, 2000, Molecular Human Reproduction, 6, 575, 10.1093/molehr/6.7.575

Tsakmakidis, 2010, Journal of Veterinary Science (Suwon-si, Korea), 11, 151, 10.4142/jvs.2010.11.2.151

van Zelst, 1995, Reproduction, Fertility and Development, 7, 1117, 10.1071/RD9951117

Vega, 2010, Philippine Journal of Veterinary and Animal Science, 36, 63

Vernet, 1996, Biochemistry and Cell Biology, 74, 125, 10.1139/o96-014

Ward, 2010, Molecular Human Reproduction, 16, 30, 10.1093/molehr/gap080

Wettemann, 1985, Journal of Reproduction and Fertility. Supplement, 33, 199

Wettemann, 1979, Biology of Reproduction, 20, 235, 10.1095/biolreprod20.2.235

10.2527/jas1976.423664x

10.2527/jas1979.4961501x

Wolf, 2011, Developmental Dynamics, 240, 204, 10.1002/dvdy.22491

Wykes, 2003, The Journal of Biological Chemistry, 278, 29471, 10.1074/jbc.M304545200

Yamauchi, 2011, Asian Journal of Andrology, 13, 31, 10.1038/aja.2010.75

Zasiadczyk, 2015, Theriogenology, 83, 1287, 10.1016/j.theriogenology.2015.01.015

Zavy, 1980, Prostaglandins, 20, 837, 10.1016/0090-6980(80)90137-9

Zernicka-Goetz, 2009, Nature Reviews. Genetics, 10, 467, 10.1038/nrg2564

Thông tin
Thông tin xuất bản

Animal Production Science

Tập 57 Số 10

1975

Thông tin tác giả