NutriPhysioGenomics applications to identify adaptations of cattle to consumption of ergot alkaloids and inorganic versus organic forms of selenium: altered nutritional, physiological and health states?
J. C. Matthews A B and P. J. Bridges AA Department of Animal and Food Sciences, University of Kentucky, Lexington, Kentucky 40546-0215, USA.
B Corresponding author. Email: jmatthew@uky.edu
Animal Production Science 54(10) 1594-1604 https://doi.org/10.1071/AN14274
Submitted: 13 March 2014 Accepted: 30 June 2014 Published: 19 August 2014
Abstract
NutriPhysioGenomics (NPG) seeks to measure nutrition-responsive genome expression during specific physiological states, thus defining how a given challenge alters the ‘basal’ transcriptome. Application of NGS regimens (transcriptome and bioinformatics analyses) in combination with targeted-gene approaches has revealed cellular mechanisms putatively responsible for complex, whole-animal, metabolic syndromes such as heat stress and subacute ruminal acidosis. Using similar approaches, our laboratory sought to understand how the basal physiology of developing cattle adapted to two prevalent health challenges of forage-based beef cattle production in south-eastern USA: fescue toxicosis and selenium (Se) deficiency. In Model 1, pituitary and hepatic genomic expression profiles of growing beef steers grazing high (E+, n = 9) versus low (E–, n = 10) endophyte-infected tall fescue pastures for 85 days, and consuming sodium selenite (ISe) as a free-choice Se supplement, were compared by a combination of microarray, bioinformatic, and targeted-gene/protein (real-time reverse transcription–PCR, Nanostring, immunoblot) analyses. In Model 2, hepatic genomic expression profiles of growing beef heifers (0.5 kg gain/day) fed a cotton seed hull-based diet and different sources (n = 9) of dietary Se (3 mg/day) supplements (no supplement, Control; inorganic Se, sodium selenite, ISe; organic Se, Sel-Plex; OSe), or a 1.5 mg : 1.5 mg blend of ISe and OSe, MIX) were compared after 168 days of supplementation, as described for Model 1. The results for Model 1 showed, that in the pituitary of E+ steers, expression of genes for prolactin signalling; redox capacity; regulation of lactotroph, gonadotroph, and thyrotroph proliferation; gonadotropin-releasing hormone-mediated signalling; and Se-based metabolism was impaired. Concomitantly, the livers of E+ steers had an increased level of expression of genes encoding proteins responsible for shunting of amino acid carbons into pyruvate and ATP synthesis capacity (oxidative phosphorylation pathway, mitochondrial mass), increased serine and proline biosynthesis, and reduced selenoprotein-mediated metabolism. Result for Model 2 showed that, overall, there were clear differences in the profiles of differentially expressed genes (DEG) among the four Se treatment groups, with the form of Se administered being more reflective of DEG profiles than the total amount of Se assimilated. Moreover, hepatic transcriptomes profiles of MIX heifers revealed an increased potential for selenoprotein synthesis and selenoprotein-mediated metabolism. In addition, several genes involved with increased redox capacity were upregulated in MIX versus ISe heifers. Taken together, our NGS approach characterised adaptation to physiological challenges and, serendipitously, identified suppression of several metabolic pathways by consumption of ergot alkaloid consumption that have the potential to be increased with supplementation of the MIX form of Se.
Additional keywords: gene expression, liver, pituitary, testis.
References
Aiken GE, Strickland JR, Looper ML, Bush LP, Schrick FN (2009) Hemodynamics are altered in the caudal artery of beef heifers fed different ergot alkaloid concentrations. Journal of Animal Science 87, 2142–2150.| Hemodynamics are altered in the caudal artery of beef heifers fed different ergot alkaloid concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1eis7w%3D&md5=c0515c37c9e3090d8b0f6d0a7233aa37CAS | 19251925PubMed |
Ammerman CB, Miller SM (1975) Selenium in ruminant nutrition: a review. Journal of Dairy Science 58, 1561–1577.
| Selenium in ruminant nutrition: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXlslOjt7c%3D&md5=e6db39e4c3b142140dcd3981d45d8462CAS | 1102575PubMed |
Ayers S, Switnicki MP, Angajala A, Lammel J, Arumanayagam AS, Webb P (2014) Genome-wide binding patterns of thyroid hormone receptor Beta. PLoS ONE 9, e81186
| Genome-wide binding patterns of thyroid hormone receptor Beta.Crossref | GoogleScholarGoogle Scholar | 24558356PubMed |
Beardwell C, Robertson GL (1981) ‘The pituitary.’ (Butterworths: London)
Bhusari S, Hearne LB, Spiers DE, Lamberson WR, Antoniou E (2006) Effect of fescue toxicosis on hepatic gene expression in mice. Journal of Animal Science 84, 1600–1612.
Brennan KM, Burris WR, Boling JA, Matthews JC (2011) Selenium content in blood fractions and liver of beef heifers is greater with a mix of inorganic/organic or organic versus inorganic supplemental selenium but the time required for maximal assimilation is tissue-specific. Biological Trace Element Research 144, 504–516.
| Selenium content in blood fractions and liver of beef heifers is greater with a mix of inorganic/organic or organic versus inorganic supplemental selenium but the time required for maximal assimilation is tissue-specific.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1emu7vO&md5=191bb4834da16a78069a8bc922995f5fCAS | 21562759PubMed |
Brown KR, Anderson GA, Son K, Rentfrow G, Bush LP, Klotz JL, Strickland JR, Boling JA, Matthews JC (2009) Growing steers grazing high versus low endophyte (Neotyphodium coenophialum)-infected tall fescue have reduced serum enzymes, increased hepatic glucogenic enzymes, and reduced liver and carcass mass. Journal of Animal Science 87, 748–760.
| Growing steers grazing high versus low endophyte (Neotyphodium coenophialum)-infected tall fescue have reduced serum enzymes, increased hepatic glucogenic enzymes, and reduced liver and carcass mass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFGnsLs%3D&md5=4c078fcd318f967309abeba73106c20bCAS | 18952729PubMed |
Browning R, Thompson FN, Sartin JL, Leite-Browning ML (1997) Plasma concentrations of prolactin, growth hormone, and luteinizing hormone in steers administered ergotamine or ergonovine. Journal of Animal Science 75, 796–802.
Browning R, Schrick FN, Thompson FN, Wakefield T (1998) Reproductive hormonal responses to ergotamine and ergonovine in cows during the luteal phase of the estrous cycle. Journal of Animal Science 76, 1448–1454.
Carabelli J, Burgueno AL, Rosselli MS, Gianotti TF, Lago NR, Pirola CJ, Sookoian S (2011) High fat diet-induced liver steatosis promotes an increase in liver mitochondrial biogenesis in response to hypoxia. Journal of Cellular and Molecular Medicine 15, 1329–1338.
| High fat diet-induced liver steatosis promotes an increase in liver mitochondrial biogenesis in response to hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFelsrg%3D&md5=acb8a5700799629c098c075e6d32c241CAS | 20629985PubMed |
Chestnut AB, Anderson PD, Cochran MA, Fribourg HA, Gwinn KD (1992) Effects of hydrated sodium calcium aluminosilicate on fescue toxicosis and mineral absorption. Journal of Animal Science 70, 2838–2846.
Cox LA, Glenn JP, Spradling KD, Nijland MJ, Garcia R, Nathanielsz PW, Ford SP (2012) A genome resource to address mechanisms of developmental programming: determination of the fetal sheep heart transcriptome. The Journal of Physiology 590, 2873–2884.
| A genome resource to address mechanisms of developmental programming: determination of the fetal sheep heart transcriptome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFehtLjJ&md5=acb622fce092899d92a3e8d694fc0519CAS | 22508961PubMed |
Dargatz DA, Ross PF (1996) Blood selenium concentrations in cows and heifers on 253 cow-calf operations in 18 states. Journal of Animal Science 74, 2891–2895.
Deshmukh RS, Ostrup O, Ostrup E, Vejlsted M, Niemann H, Lucas-Hahn A, Petersen B, Li J, Callesen H, Hyttel P (2011) DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation and somatic cell nuclear transfer. Epigenetics 6, 177–187.
| DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation and somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs12ksLY%3D&md5=04eeffce516fe0fe2a086eb37925c533CAS | 20935454PubMed |
Dyer DC (1993) Evidence that ergovaline acts on serotonin receptors. Life Sciences 53, PL223–PL228.
| Evidence that ergovaline acts on serotonin receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmtF2ntb0%3D&md5=c5ad07d1d929970f539d28cd0f315852CAS | 8371626PubMed |
Fischer A, Pallauf J, Gohil K, Weber SU, Packer L, Rimbach G (2001) Effect of selenium and vitamin E deficiency on differential gene expression in rat liver. Biochemical and Biophysical Research Communications 285, 470–475.
| Effect of selenium and vitamin E deficiency on differential gene expression in rat liver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvFOqsr0%3D&md5=78683968a2c2bb7cf2b06d7438874de2CAS | 11444866PubMed |
Fitzgerald P, Dinan TG (2008) Prolactin and dopamine: what is the connection? A review article. Journal of Psychopharmacology (Oxford, England) 22, 12–19.
| Prolactin and dopamine: what is the connection? A review article.Crossref | GoogleScholarGoogle Scholar |
Food and Drug Administration (1987) Food additives permitted in feed and drinking water of animals: selenium. Federal Register 52: 10668.
Fry RS, Spears JW, Lloyd KE, O’Nan AT, Ashwell MS (2013) Effect of dietary copper and breed on gene products involved in copper acquisition, distribution, and use in Angus and Simmental cows and fetuses. Journal of Animal Science 91, 861–871.
| Effect of dietary copper and breed on gene products involved in copper acquisition, distribution, and use in Angus and Simmental cows and fetuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvVKmsrc%3D&md5=f7c358674dd1a945b6bab4b0dd73ac17CAS | 23148247PubMed |
Gao Y, Jammes H, Rasmussen MA, Oestrup O, Beaujean N, Hall V, Hyttel P (2011) Epigenetic regulation of gene expression in porcine epiblast, hypoblast, trophectoderm and epiblast-derived neural progenitor cells. Epigenetics 6, 1149–1161.
| Epigenetic regulation of gene expression in porcine epiblast, hypoblast, trophectoderm and epiblast-derived neural progenitor cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitlGks74%3D&md5=3260940476910a5131b93c994ab8c248CAS | 21975513PubMed |
Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL, Fell HP, Ferree S, George RD, Grogan T, James JJ, Maysuria M, Mitton JD, Oliveri P, Osborn JL, Peng T, Ratcliffe AL, Webster PJ, Davidson EH, Hood L, Dimitrov K (2008) Direct multiplexed measurement of gene expression with color-coded probe pairs. Nature Biotechnology 26, 317–325.
| Direct multiplexed measurement of gene expression with color-coded probe pairs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVGit7w%3D&md5=f8ef84b4369d2022d92fb2ca3e593e20CAS | 18278033PubMed |
Harrison GA, Tricarico JM, Elliot SA (2005) Effect of Sel-Plex supplementation on milk production, composition and somatic cell count of lactating dairy cows in commercial dairy herds: herd and individual cow responses. Journal of Dairy Science 88, 60
Hemken RW, Boling JA, Bull LS, Hatton RH, Buckner RC, Bush LP (1981) Interaction of environmental temperature and anti-quality factors on the severity of summer fescue toxicosis. Journal of Animal Science 52, 710–714.
Huang JQ, Li DL, Zhao H, Sun LH, Xia XJ, Wang KN, Luo X, Lei XG (2011) The selenium deficiency disease exudative diathesis in chicks is associated with downregulation of seven common selenoprotein genes in liver and muscle. The Journal of Nutrition 141, 1605–1610.
| The selenium deficiency disease exudative diathesis in chicks is associated with downregulation of seven common selenoprotein genes in liver and muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFais7fF&md5=77e886763c0b8f3a6a041677d561d218CAS | 21795426PubMed |
Jiang ST, Chiou YY, Wang E, Lin HK, Lee SP, Lu HY, Wang CK, Tang MJ, Li H (2008) Targeted disruption of Nphp1 causes male infertility due to defects in the later steps of sperm morphogenesis in mice. Human Molecular Genetics 17, 3368–3379.
| Targeted disruption of Nphp1 causes male infertility due to defects in the later steps of sperm morphogenesis in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1entrvO&md5=2f8fdfc5e92cc512a9be65c6b0fad5f7CAS | 18684731PubMed |
Judson GJ, Reuter DJ (1999) Selenium. In ‘Soil analysis: an interpretation manual’. (Eds KI Peverill, LA Sparrow, DJ Reuter) pp. 325–329. (CSIRO Publishing: Melbourne)
Juniper DT, Phipps RH, Ramos-Morales E, Bertin G (2008) Effect of dietary supplementation with selenium-enriched yeast or sodium selenite on selenium tissue distribution and meat quality in beef cattle. Journal of Animal Science 86, 3100–3109.
| Effect of dietary supplementation with selenium-enriched yeast or sodium selenite on selenium tissue distribution and meat quality in beef cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlCnsbzO&md5=bfe0876dc7d5fb718c1c313cdde3d263CAS | 18567732PubMed |
Klotz JL, Brown KR, Xue Y, Matthews JC, Boling JA, Burris WR, Bush LP, Strickland JR (2012) Alterations in serotonin receptor-induced contractility of bovine lateral saphenous vein in cattle grazing endophyte-infected tall fescue. Journal of Animal Science 90, 682–693.
| Alterations in serotonin receptor-induced contractility of bovine lateral saphenous vein in cattle grazing endophyte-infected tall fescue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitVeltbg%3D&md5=bd1c4e2761efb74b633c77e3bf806bf5CAS | 22274863PubMed |
Kohda T, Ishino F (2013) Embryo manipulation via assisted reproductive technology and epigenetic asymmetry in mammalian early development. Philosophical Tranactions of the Royal Society of London:B Biological Sciences 368, 20120353
| Embryo manipulation via assisted reproductive technology and epigenetic asymmetry in mammalian early development.Crossref | GoogleScholarGoogle Scholar |
Korhola M, Vainio A, Edelmann K (1986) Selenium yeast. Annals of Clinical Research 18, 65–68.
Larson BT, Harmon DL, Piper EL, Griffis LM, Bush LP (1999) Alkaloid binding and activation of D2 dopamine receptors in cell culture. Journal of Animal Science 77, 942–947.
Liao SF, Brown KR, Stromberg AJ, Burris WR, Boling JA, Matthews JC (2011) Dietary supplementation of selenium in inorganic and organic forms differentially and commonly alters blood and liver selenium concentrations and liver gene expression profiles of growing beef heifers. Biological Trace Element Research 140, 151–169.
| Dietary supplementation of selenium in inorganic and organic forms differentially and commonly alters blood and liver selenium concentrations and liver gene expression profiles of growing beef heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktVOitr0%3D&md5=cb85049642317f5edf0d264aae8e5e42CAS | 20387001PubMed |
Matthews JC, Zhang Z, Patterson JD, Bridges PJ, Stromberg AJ, Boling JA (2014) Hepatic transcriptome profiles differ among maturing beef heifers supplemented with inorganic, organic, or a mixed (50% inorganic:50% organic) forms of dietary selenium. Biological Trace Element Research
| Hepatic transcriptome profiles differ among maturing beef heifers supplemented with inorganic, organic, or a mixed (50% inorganic:50% organic) forms of dietary selenium.Crossref | GoogleScholarGoogle Scholar | 24996959PubMed |
McIntosh GH, Royle PJ (2002) Supplementation of cows with organic selenium and the identification of selenium-rich protein fractions in milk. In ‘Nutritional biotechnology in the feed and food industries. Proceedings of Alltech’s 18th annual symposium’. (Eds TP Lyons, KA Jacques) pp. 233–238. (Nottingham University Press: Nottingham, UK)
Mehla K, Magotra A, Choudhary J, Singh AK, Mohanty AK, Upadhyay RC, Srinivasan S, Gupta P, Choudhary N, Antony B, Khan F (2014) Genome-wide analysis of the heat stress response in Zebu (Sahiwal) cattle. Gene 533, 500–507.
| Genome-wide analysis of the heat stress response in Zebu (Sahiwal) cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsF2ns7zP&md5=b74931a5400e23e846c92432f0cf19b9CAS | 24080481PubMed |
Miles ED, Xue Y, Strickland JR, Boling JA, Matthews JC (2011) Ergopeptines bromocriptine and ergovaline and the dopamine type-2 receptor inhibitor domperidone inhibit bovine equilibrative nucleoside transporter 1-like activity. Journal of Agricultural and Food Chemistry 59, 9691–9699.
| Ergopeptines bromocriptine and ergovaline and the dopamine type-2 receptor inhibitor domperidone inhibit bovine equilibrative nucleoside transporter 1-like activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpslyisb8%3D&md5=f468cf767b6e64e1b45a0700ba296ebeCAS | 21790119PubMed |
Mutiara S, Kanasaki H, Harada T, Miyazaki K (2006) Dopamine D(2) receptor expression and regulation of gonadotropin alpha-subunit gene in clonal gonadotroph LbetaT2 cells. Molecular and Cellular Endocrinology 259, 22–29.
| Dopamine D(2) receptor expression and regulation of gonadotropin alpha-subunit gene in clonal gonadotroph LbetaT2 cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvV2qsb8%3D&md5=dc5ce6bedf283c5b2fe11667936e8d0cCAS | 16959402PubMed |
National Research Council (1996) Minerals. In ‘Nutrient requirements of beef cattle’. 7th revised edn. 2001 update. pp. 54–74. (National Academy Press: Washington, DC).
Oliver JW, Schultze AE, Rohrbach BW, Fribourg HA, Ingle T, Waller JC (2000) Alterations in hemograms and serum biochemical analytes of steers after prolonged consumption of endophyte-infected tall fescue. Journal of Animal Science 78, 1029–1035.
Patterson JD, Burris WR, Boling JA, Matthews JC (2013) Individual intake of free-choice mineral mix by grazing beef cows may be less than typical formulation assumptions and form of selenium in mineral mix affects blood Se concentrations of cows and their suckling calves. Biological Trace Element Research 155, 38–48.
| Individual intake of free-choice mineral mix by grazing beef cows may be less than typical formulation assumptions and form of selenium in mineral mix affects blood Se concentrations of cows and their suckling calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1eksb%2FL&md5=0fd79e0799ca9578f86979acc31dd1caCAS | 23928729PubMed |
Qin S, Gao J, Huang K (2007) Effects of different selenium sources on tissue selenium concentrations, blood GSH-Px activities and plasma interleukin levels in finishing lambs. Biological Trace Element Research 116, 91–102.
| Effects of different selenium sources on tissue selenium concentrations, blood GSH-Px activities and plasma interleukin levels in finishing lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmslyqtb0%3D&md5=8e209fdd9d070bc482a7d647e02187c3CAS | 17634631PubMed |
Revollo JR, Cidlowski JA (2009) Mechanisms generating diversity in glucocorticoid receptor signaling. Annals of the New York Academy of Sciences 1179, 167–178.
| Mechanisms generating diversity in glucocorticoid receptor signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFChtL3F&md5=7f5decaa9eb7eb565b19cfa859b62f7bCAS | 19906239PubMed |
Settivari RS, Bhusari S, Evans T, Eichen PA, Hearne LB, Antoniou E, Spiers DE (2006) Genomic analysis of the impact of fescue toxicosis on hepatic function. Journal of Animal Science 84, 1279–1294.
Sigel MR, Bush LP (1994) Importance of Endophytes in forage grasses, a statement of problems and selection of endophytes. In ‘Biotechnology of endophytic fungi of grasses’. (Eds CW Bacon, JF White Jr) pp. 135–150. (CRC Press: Boca Raton, FL)
Steele MA, Croom J, Kahler M, AlZahal O, Hook SE, Plaizier K, McBride BW (2011) Bovine rumen epithelium undergoes rapid structural adaptations during grain-induced subacute ruminal acidosis. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 300, R1515–R1523.
| Bovine rumen epithelium undergoes rapid structural adaptations during grain-induced subacute ruminal acidosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXot1Grtro%3D&md5=88b528db4a907ca0b5e91a8e92fe48c4CAS | 21451145PubMed |
Strickland JR, Looper ML, Matthews JC, Rosenkrans CF, Flythe MD, Brown KR (2011) Board-invited review: St Anthony’s Fire in livestock: causes, mechanisms, and potential solutions. Journal of Animal Science 89, 1603–1626.
| Board-invited review: St Anthony’s Fire in livestock: causes, mechanisms, and potential solutions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXls1Ohsrk%3D&md5=b738734ab874b6fcf82988982df41bf7CAS | 21521821PubMed |
Sun B, Wang R, Li J, Jiang Z, Xu S (2011) Dietary selenium affects selenoprotein W gene expression in the liver of chicken. Biological Trace Element Research 143, 1516–1523.
| Dietary selenium affects selenoprotein W gene expression in the liver of chicken.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFSis7nN&md5=35d53d7edb9feeb79f8c0307c3ed0f90CAS | 21331563PubMed |
Tong MH, Christenson LK, Song WC (2004) Aberrant cholesterol transport and impaired steroidogenesis in Leydig cells lacking estrogen sulfotransferase. Endocrinology 145, 2487–2497.
| Aberrant cholesterol transport and impaired steroidogenesis in Leydig cells lacking estrogen sulfotransferase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsV2jsLk%3D&md5=8fe9ed3680d8402ef7aee7b5e6315c3eCAS | 14749355PubMed |
Tortonese DJ, Brooks J, Ingleton PM, McNeilly AS (1998) Detection of prolactin receptor gene expression in the sheep pituitary gland and visualization of the specific translation of the signal in gonadotrophs. Endocrinology 139, 5215–5223.
| Detection of prolactin receptor gene expression in the sheep pituitary gland and visualization of the specific translation of the signal in gonadotrophs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXns1ehurw%3D&md5=7c1e0838ac060f1b71bfac60791eb5dfCAS | 9832462PubMed |
Xue Y, Liao SF, Strickland JR, Boling JA, Matthews JC (2011) Bovine neuronal vesicular glutamate transporter activity is inhibited by ergovaline and other ergopeptines. Journal of Dairy Science 94, 3331–3341.
| Bovine neuronal vesicular glutamate transporter activity is inhibited by ergovaline and other ergopeptines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFahsro%3D&md5=bf1145e240d08f2a666c8bad81dd0ef6CAS | 21700019PubMed |