Temporal candidate gene expression in the sow placenta and embryo during early gestation and effect of maternal Progenos supplementation on embryonic and placental development
S. Novak A , F. Paradis A , J. L. Patterson A , J. A. Pasternak A , K. Oxtoby A , H. S. Moore A , M. Hahn A , M. K. Dyck A , W. T. Dixon A and G. R. Foxcroft A B
+ Author Affiliations
- Author Affiliations
A Swine Reproduction–Development Program, Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, T6G 2P5, Canada.
B Corresponding author. Email: george.foxcroft@ualberta.ca
Reproduction, Fertility and Development 24(4) 550-558 https://doi.org/10.1071/RD10312
Submitted: 22 November 2010 Accepted: 20 September 2011 Published: 17 November 2011
Abstract
The present study characterised gene expression associated with embryonic muscle development and placental vascularisation during early gestation in the pig and examined effects of Progenos supplementation in early pregnancy. Tissues were collected from commercial multiparous sows (n = 48) from Days 16 to 49 of gestation. In the placenta, qPCR revealed that vascular endothelial growth factor (VEGFA) expression did not change from Day 17 to 49 of gestation; however, KDR receptor and angiopoietin-1 and -2 expression were differentially regulated, with periods of high expression corresponding to two critical phases of angiogenesis in the pig. In the embryo, the pattern of myogenesis-related gene expression was consistent with available literature. A commercially available nutritional supplement Progenos (20 g day–1 l-arginine) added to the diet of sows from either Day 15 to 29 (P15–29; n = 33), Day 30 to 44 (n = 29) or from Day 15 to 44 (n = 76) of gestation tended to increase (P = 0.058) embryonic growth rate compared with non-supplemented controls (n = 79) and angiogenin expression was higher (P = 0.028) at Day 30 of gestation in placentae from sows on the P15–29 Progenos treatment. These results are consistent with proposed beneficial effects of l-arginine on early embryonic development and placental vascularisation.
Additional keywords: angiogenesis; myogenesis, nutrition, pig, pregnancy.
References
Buckingham, M., Bajard, L., Chang, T., Daubas, P., Hadchouel, J., Meilhac, S., Montarras, D., Rocancourt, D., and Relaix, F. (2003). The formation of skeletal muscle: from somite to limb. J. Anat. 202, 59–68.| The formation of skeletal muscle: from somite to limb.Crossref | GoogleScholarGoogle Scholar | 12587921PubMed |
Dwyer, C. M., Stickland, N. C., and Fletcher, J. M. (1994). The influence of maternal nutrition on muscle fiber number development in the porcine fetus and on subsequent postnatal growth. J. Anim. Sci. 72, 911–917.
| 1:STN:280:DyaK2c3osVahsA%3D%3D&md5=287192f5f04aa546976e61e2c14df92bCAS | 8014156PubMed |
Dwyer, C. M., Madgwick, A. J., Ward, S. S., and Stickland, N. C. (1995). Effect of maternal undernutrition in early gestation on the development of fetal myofibres in the guinea-pig. Reprod. Fertil. Dev. 7, 1285–1292.
| Effect of maternal undernutrition in early gestation on the development of fetal myofibres in the guinea-pig.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK283kvFegtg%3D%3D&md5=5ef862deea449184ad877b053d762f2fCAS | 8848601PubMed |
Foxcroft, G. R., Dixon, W. T., Dyck, M. K., Novak, S., Harding, J. C., and Almeida, F. C. (2009). Prenatal programming of postnatal development in the pig. Soc. Reprod. Fertil. Suppl. 66, 213–231.
| 1:STN:280:DC%2BD1MjgvFaksA%3D%3D&md5=69bc35aa765776318c99aa04cf881568CAS | 19848290PubMed |
Hahn, M., Town, S, Smit, M., Patterson,, J., Pasternak, A., Wellen, A., Guggenbiller, D., Smits, C., Ramaekers, P., Dyck, M., and Foxcroft, G. R. (2008). Effects of sow parity and l-arginine treatment during early gestation on litter size and birth weight. J. Anim. Sci. 86, 89..
Hazeleger, W., Ramaekers, P., Smits, C., and Kemp, B. (2007) Influence of nutritional factors on placental growth and piglet imprinting. In ‘Paradigms in Pig Science’. (Eds J. Wiseman, M. A. Varley, S. McOrist and B. Kemp.) pp. 309–328. (Nottingham Univ. Press: Nottingham.)
Li, X., Bazer, F. W., Johnson, G. A., Burghardt, R. C., Erikson, D. W., Frank, J. W., Spencer, T. E., Shinzato, I., and Wu, G. (2010). Dietary supplementation with 0.8% l-arginine between Days 0 and 25 of gestation reduces litter size in gilts. J. Nutr. 140, 1111–1116.
| Dietary supplementation with 0.8% l-arginine between Days 0 and 25 of gestation reduces litter size in gilts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVChsro%3D&md5=65c74ac34459601bede3a80389092f43CAS | 20392885PubMed |
Mateo, R. D., Wu, G., Bazer, F. W., Park, J. C., Shinzato, I., and Kim, S. W. (2007). Dietary l-arginine supplementation enhances the reproductive performance of gilts. J. Nutr. 137, 652–656.
| 1:CAS:528:DC%2BD2sXisVygs7c%3D&md5=b0cd3f0fa40b4a3bd3cff11ee2bd0619CAS | 17311955PubMed |
McDermott, A., Gustafsson, M., Elsam, T., Hui, C. C., Emerson, C. P., , and Borycki, A. G. (2005). Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation. Development 132, 345–357.
| Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1Wgt70%3D&md5=900a251c29f02de7fef8e423dd2cd003CAS | 15604102PubMed |
Milkiewicz, M., Ispanovic, E., Doyle, J. L., and Haas, T. L. (2006). Regulators of angiogenesis and strategies for their therapeutic manipulation. Int. J. Biochem. Cell Biol. 38, 333–357.
| Regulators of angiogenesis and strategies for their therapeutic manipulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCrtr3M&md5=ca53453728c6293342f42534744dde44CAS | 16309946PubMed |
Oliver, G., Novak, S., Patterson, J. L., Pasternak, J. A., Paradis, F., Norrby, M., Oxtoby, K., Dyck, M. K., Dixon, W. T., and Foxcroft, G. R. (2011). Restricted feed intake in lactating primiparous sows: II. Effects on subsequent litter sex ratio and embryonic gene expression. Reprod. Fertil. Dev. 23, 899–911.
| Restricted feed intake in lactating primiparous sows: II. Effects on subsequent litter sex ratio and embryonic gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOrtLfF&md5=c2f58214670d6403cead8af93665ff10CAS | 21871209PubMed |
Quigley, S. P., Kleemann, D. O., Kakar, M. A., Owens, J. A., Nattrass, G. S., Maddocks, S., and Walker, S. K. (2005). Myogenesis in sheep is altered by maternal feed intake during the peri-conception period. Anim. Reprod. Sci. 87, 241–251.
| Myogenesis in sheep is altered by maternal feed intake during the peri-conception period.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MzhvFyrsA%3D%3D&md5=8efbd86754d1ccd0a4858ffed81be805CAS | 15911174PubMed |
Rehfeldt, C., and Kuhn, G. (2006). Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J. Anim. Sci. 84, E113–E123.
| 16582082PubMed |
Reynolds, L. P., and Redmer, D. A. (2001). Angiogenesis in the placenta. Biol. Reprod. 64, 1033–1040.
| Angiogenesis in the placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1artbk%3D&md5=2e7718efc3b5e4a1ef1c663967251c13CAS | 11259247PubMed |
Rudnicki, M. A., Schnegelsberg, P. N., Stead, R. H., Braun, T., Arnold, H. H., and Jaenisch, R. (1993). MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351–1359.
| MyoD or Myf-5 is required for the formation of skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhtVaqtbk%3D&md5=62b2a8a37f797a735573ea43a17846faCAS | 8269513PubMed |
Tajbakhsh, S., Rocancourt, D., Cossu, G., and Buckingham, M. (1997). Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89, 127–138.
| Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXisVyks7s%3D&md5=93c17bb898dd5db99d18f03fa62f6a5dCAS | 9094721PubMed |
Tayade, C., Fang, Y., and Croy, B. A. (2007). A review of gene expression in porcine endometrial lymphocytes, endothelium and trophoblast during pregnancy success and failure. J. Reprod. Dev. 53, 455–463.
| A review of gene expression in porcine endometrial lymphocytes, endothelium and trophoblast during pregnancy success and failure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosVyls74%3D&md5=607a48541ffbd7452d3db1b85cfa03ebCAS | 17617733PubMed |
Town, S. C., Putman, C. T., Turchinsky, N. J., Dixon, W. T., and Foxcroft, G. R. (2004). Number of conceptuses in utero affects porcine fetal muscle development. Reproduction 128, 443–454.
| Number of conceptuses in utero affects porcine fetal muscle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptlGjsLs%3D&md5=a75fda122d48057a06ca120cc0d1e837CAS | 15454639PubMed |
Tse, W. Y., Town, S. C., Murdoch, G. K., Novak, S., Dyck, M. K., Putman, C. T., Foxcroft, G. R., and Dixon, W. T. (2008). Uterine crowding in the sow affects litter sex ratio, placental development and embryonic myogenin expression in early gestation. Reprod. Fertil. Dev. 20, 497–504.
| Uterine crowding in the sow affects litter sex ratio, placental development and embryonic myogenin expression in early gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFagsrw%3D&md5=9728afa7df50db42ddc9ea44f648a65dCAS | 18462612PubMed |
Vallet, J. L., Miles, J. R., and Freking, B. A. (2010). Effect of fetal size on fetal placental hyaluronan and hyaluronoglucosaminidases throughout gestation in the pig. Anim. Reprod. Sci. 118, 297–309.
| Effect of fetal size on fetal placental hyaluronan and hyaluronoglucosaminidases throughout gestation in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGlurY%3D&md5=0bc05c2661d84e05b409f8e212d31580CAS | 19647381PubMed |
van der Lende, T., and van Rens, B. T. (2003). Critical periods for foetal mortality in gilts identified by analysing the length distribution of mummified foetuses and frequency of non-fresh stillborn piglets. Anim. Reprod. Sci. 75, 141–150.
| Critical periods for foetal mortality in gilts identified by analysing the length distribution of mummified foetuses and frequency of non-fresh stillborn piglets.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s%2FislOnuw%3D%3D&md5=ea0fea79e623efe9b4df8f8d50a6afddCAS | 12535589PubMed |
Vonnahme, K. A., Wilson, M. E., and Ford, S. P. (2001). Relationship between placental vascular endothelial growth factor expression and placental–endometrial vascularity in the pig. Biol. Reprod. 64, 1821–1825.
| Relationship between placental vascular endothelial growth factor expression and placental–endometrial vascularity in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFGgtLo%3D&md5=1f7f6fe0388aa2a6ea02622732c909e4CAS | 11369614PubMed |
Wu, G., Bazer, F. W., Davis, T. A., Kim, S. W., Li, P., Marc Rhoads, J., Carey Satterfield, M., Smith, S. B., Spencer, T. E., and Yin, Y. (2009). Arginine metabolism and nutrition in growth, health and disease. Amino Acids 37, 153–168.
| Arginine metabolism and nutrition in growth, health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltlemtL0%3D&md5=bcbeb7d78aa359955cae3f2c3d37af48CAS | 19030957PubMed |
Yancopoulos, G. D., Davis, S., Gale, N. W., Rudge, J. S., Wiegand, S. J., and Holash, J. (2000). Vascular-specific growth factors and blood vessel formation. Nature 407, 242–248.
| Vascular-specific growth factors and blood vessel formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmvVSlsrY%3D&md5=0caee2e2bba73f63891389f72e0aeca9CAS | 11001067PubMed |
