Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-18T16:42:17.158Z Has data issue: false hasContentIssue false

Acute exposure to ergot alkaloids from endophyte-infected tall fescue does not alter absorptive or barrier function of the isolated bovine ruminal epithelium*

Published online by Cambridge University Press:  18 June 2014

A. P. Foote
Affiliation:
Department of Animal and Food Sciences, University of Kentucky, Lexington, KY 40546-0215, USA
G. B. Penner
Affiliation:
Department of Animal and Poultry Science, University of Saskatchewan, Saskatoon, Canada, S7N 5A8
M. E. Walpole
Affiliation:
Department of Animal and Poultry Science, University of Saskatchewan, Saskatoon, Canada, S7N 5A8
J. L. Klotz
Affiliation:
USDA-ARS, Forage-Animal Production Research Unit, Lexington, KY 40546-0091, USA
K. R. Brown
Affiliation:
USDA-ARS, Forage-Animal Production Research Unit, Lexington, KY 40546-0091, USA
L. P. Bush
Affiliation:
Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546-0312, USA
D. L. Harmon*
Affiliation:
Department of Animal and Food Sciences, University of Kentucky, Lexington, KY 40546-0215, USA
*
Get access

Abstract

Ergot alkaloids in endophyte-infected (Neotyphodium coenophialum) tall fescue (Lolium arundinaceum) have been shown to cause a reduction in blood flow to the rumen epithelium as well as a decrease in volatile fatty acids (VFA) absorption from the washed rumen of steers. Previous data also indicates that incubating an extract of endophyte-infected tall fescue seed causes an increase in the amount of VFA absorbed per unit of blood flow, which could result from an alteration in the absorptive or barrier function of the rumen epithelium. An experiment was conducted to determine the acute effects of an endophyte-infected tall fescue seed extract (EXT) on total, passive or facilitated acetate and butyrate flux across the isolated bovine rumen as well as the barrier function measured by inulin flux and tissue conductance (Gt). Flux of ergovaline across the rumen epithelium was also evaluated. Rumen tissue from the caudal dorsal sac of Holstein steers (n=6), fed a common diet, was collected and isolated shortly after slaughter and mounted between two halves of Ussing chambers. In vitro treatments included vehicle control (80% methanol, 0.5% of total volume), Low EXT (50 ng ergovaline/ml) and High EXT (250 ng ergovaline/ml). Results indicate that there is no effect of acute exposure to ergot alkaloids on total, passive or facilitated flux of acetate or butyrate across the isolate bovine rumen epithelium (P>0.51). Inulin flux (P=0.16) and Gt (P>0.17) were not affected by EXT treatment, indicating no alteration in barrier function due to acute ergot alkaloid exposure. Ergovaline was detected in the serosal buffer of the High EXT treatment indicating that the flux rate is ~0.25 to 0.44 ng/cm2 per hour. Data indicate that specific pathways for VFA absorption and barrier function of the rumen epithelium are not affected by acute exposure to ergot alkaloids from tall fescue at the concentrations tested. Ergovaline has the potential to be absorbed from the rumen of cattle that could contribute to reduced blood flow and motility and lead to reduced growth rates of cattle.

Type
Full Paper
Copyright
© The Animal Consortium 2014 

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.)

Footnotes

*

Mention of trade name, proprietary product, or specified equipment does not constitute a guarantee or warranty by the USDA and does not imply approval to the exclusion of other products that may be available.

References

Aschenbach, JR, Bilk, S, Tadesse, G, Stumpff, F and Gabel, G 2009. Bicarbonate-dependent and bicarbonate-independent mechanisms contribute to nondiffusive uptake of acetate in the ruminal epithelium of sheep. American Journal of Physiology – Gastrointestinal and Liver Physiology 296, G1098G1107.CrossRefGoogle ScholarPubMed
Aschenbach, JR, Wehning, H, Kurze, M, Schaberg, E, Nieper, H, Burckhardt, G and Gäbel, G 2000. Functional and molecular biological evidence of SGLT-1 in the ruminal epithelium of sheep. American Journal of Physiology – Gastrointestinal and Liver Physiology 279, G20G27.Google Scholar
Ayers, AW, Hill, NS, Rottinghaus, GE, Stuedemann, JA, Thompson, FN, Purinton, PT, Seman, DH, Dawe, DL, Parks, AH and Ensley, D 2009. Ruminal metabolism and transport of tall fescue ergot alkaloids. Crop Science 49, 23092316.CrossRefGoogle Scholar
Clarke, LL 2009. A guide to Ussing chamber studies of mouse intestine. American Journal of Physiology – Gastrointestinal and Liver Physiology 296, G1151G1166.CrossRefGoogle ScholarPubMed
Foote, AP, Harmon, DL, Strickland, JR, Bush, LP and Klotz, JL 2011. Effect of ergot alkaloids on contractility of bovine right ruminal artery and vein. Journal of Animal Science 89, 29442949.CrossRefGoogle ScholarPubMed
Foote, AP, Harmon, DL, Brown, KR, Strickland, JR, McLeod, KR, Bush, LP and Klotz, JL 2012. Constriction of bovine vasculature caused by endophyte-infected tall fescue seed extract is similar to pure ergovaline. Journal of Animal Science 90, 16031609.Google Scholar
Foote, AP, Kristensen, NB, Klotz, JL, Kim, DH, Koontz, AF, McLeod, KR, Bush, LP, Schrick, FN and Harmon, DL 2013. Ergot alkaloids from endophyte-infected tall fescue decrease reticuloruminal epithelial blood flow and volatile fatty acid absorption from the washed reticulorumen. Journal of Animal Science 91, 53665378.CrossRefGoogle ScholarPubMed
Graham, C and Simmons, NL 2005. Functional organization of the bovine rumen epithelium. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 288, R173R181.Google Scholar
Harmon, DL, Gross, KL, Kreikemeier, KK, Coffey, KP, Avery, TB and Klindt, J 1991. Effects of feeding endophyte-infected fescue hay on portal and hepatic nutrient flux in steers. Journal of Animal Science 69, 12231231.Google Scholar
Hill, NS, Thompson, FN, Stuedemann, JA, Rottinghaus, GW, Ju, HJ, Dawe, DL and Hiatt, EE 2001. Ergot alkaloid transport across ruminant gastric tissues. Journal of Animal Science 79, 542549.CrossRefGoogle ScholarPubMed
Klotz, JL, Kirch, BH, Aiken, GE, Bush, LP and Strickland, JR 2010. Contractile response of fescue-naive bovine lateral saphenous veins to increasing concentrations of tall fescue alkaloids. Journal of Animal Science 88, 408415.CrossRefGoogle ScholarPubMed
Larson, BT, Samford, MD, Camden, JM, Piper, EL, Kerley, MS, Paterson, JA and Turner, JT 1995. Ergovaline binding and activation of D2 dopamine receptors in GH4ZR7 cells. Journal of Animal Science 73, 13961400.Google Scholar
Mulac, D, Hüwel, S, Galla, HJ and Humpf, HU 2012. Permeability of ergot alkaloids across the blood-brain barrier in vitro and influence on the barrier integrity. Molecular Nutrition and Food Research 56, 475485.Google Scholar
Penner, GB, Oba, M, Gäbel, G and Aschenbach, JR 2010. A single mild episode of subacute ruminal acidosis does not affect ruminal barrier function in the short term. Journal of Dairy Science 93, 48384845.Google Scholar
Penner, GB, Aschenbach, JR, Gabel, G, Rackwitz, R and Oba, M 2009. Epithelial capacity for apical uptake of short chain fatty acids is a key determinant for intraruminal pH and the susceptibility to subacute ruminal acidosis in sheep. Journal of Nutrition 139, 17141720.Google Scholar
Rhodes, MT, Paterson, JA, Kerley, MS, Garner, HE and Laughlin, MH 1991. Reduced blood flow to peripheral and core body tissues in sheep and cattle induced by endophyte-infected tall fescue. Journal of Animal Science 69, 20332043.Google Scholar
Schweigel, M, Freyer, M, Leclercq, S, Etschmann, B, Lodemann, U, Böttcher, A and Martens, H 2005. Luminal hyperosmolarity decreases Na transport and impairs barrier function of sheep rumen epithelium. Journal of Comparative Physiology B 175, 575591.Google Scholar
Sehested, J, Diernaes, L, Moller, PD and Skadhauge, E 1996a. Transport of sodium across the isolated bovine rumen epithelium: interaction with short-chain fatty acids, chloride and bicarbonate. Experimental Physiology 81, 7994.CrossRefGoogle ScholarPubMed
Sehested, J, Diernaes, L, Laverty, G, Møller, PD and Skadhauge, E 1996b. Methodological and functional aspects of the isolated bovine rumen epithelium in ussing chamber flux studies. Acta Agriculturae Scandinavica Section A, Animal Science 46, 7686.Google Scholar
Shappell, N and Smith, D 2005. Ergovaline movement across Caco-2 cells. In Vitro Cellular and Developmental Biology – Animal 41, 245251.Google Scholar
Strickland, JR, Looper, ML, Matthews, JC, Rosenkrans, CF Jr, Flythe, MD and Brown, KR 2011. Board-invited review: St. Anthony’s fire in livestock: causes, mechanisms, and potential solutions. Journal of Animal Science 89, 16031626.Google Scholar
Wilson, DJ, Mutsvangwa, T and Penner, GB 2012. Supplemental butyrate does not enhance the absorptive or barrier functions of the isolated ovine ruminal epithelia. Journal of Animal Science 90, 31533161.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Foote et al. supplementary material

Supplementary table S1

Download Foote et al. supplementary material(PDF)
PDF 169.7 KB