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Effect of Ergot Alkaloids on Contractility of Bovine Right Ruminal Artery and Vein A

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Effect of Ergot Alkaloids on Contractility of Bovine Right Ruminal Artery and Vein A Effect of ergot alkaloids on contractility of bovine right ruminal artery and vein A. P. Foote, D. L. Harmon, J. R. Strickland, L. P. Bush and J. L. Klotz J ANIM SCI 2011, 89:2944-2949. doi: 10.2527/jas.2010-3626 originally published online April 21, 2011 The online version of this article, along with updated information and services, is located on the World Wide Web at: http://jas.fass.org/content/89/9/2944 www.asas.org Downloaded from jas.fass.org at USDA Natl Agricultural Library on October 6, 2011 Effect of ergot alkaloids on contractility of bovine right ruminal artery and vein1,2 A. P. Foote,* D. L. Harmon,* J. R. Strickland,† L. P. Bush,‡ and J. L. Klotz†3 *Department of Animal and Food Sciences, University of Kentucky, Lexington 40546-0215; †USDA-ARS, Forage-Animal Production Research Unit, Lexington, KY 40546-0091; and ‡Department of Plant and Soil Sciences, University of Kentucky, Lexington 40546-0312 ABSTRACT: Ergot alkaloids produced by the en- ized as a percentage of the contractile response induced dophyte (Neotyphodium coenophialum) associated with by KCl. Alkaloid (P < 0.0001), concentration (P < tall fescue (Lolium arundinaceum) are implicated in the 0.0001), and vessel type (artery or vein; P = 0.004) af- clinical signs of fescue toxicosis. These compounds were fected contractility. No arterial response was observed hypothesized to correspondingly affect foregut vascu- until 10−6 M for ergovaline and ergotamine; 10−5 M for lature. The objective of this study was to determine ergocryptine, ergocornine, and ergonovine; and 10−4 M vasoconstrictive potentials of ergovaline, ergotamine, for ergocristine. Lysergic acid did not induce a contrac- ergocryptine, ergocristine, ergonovine, ergocornine, tile response in the ruminal artery. No venous contrac- and lysergic acid on right ruminal artery and vein. Seg- tile response was observed until concentrations of 10−6 ments of right ruminal artery and vein were collected M for ergovaline, 10−5 M for ergotamine, and 10−4 M from the ventral coronary groove of predominantly An- for ergocryptine and ergocristine were achieved. Lyser- gus heifers (n = 10) shortly after slaughter and placed gic acid, ergonovine, and ergocornine did not induce a in a modified Krebs-Henseleit buffer on ice. Vessels contractile response in the ruminal vein. A greater ar- were cleaned of excess connective tissue and fat, sliced terial maximal response was observed for ergovaline (P into 2- to 3-mm segments, and suspended in a multi- < 0.0001), whereas the arterial and venous responses myograph chamber with 5 mL of continuously oxygen- were not different for ergotamine (P = 0.16), ergocryp- ated Krebs-Henseleit buffer (95%O2/5% CO2; pH 7.4; tine (P = 0.218), and ergocristine (P = 0.425). These 37°C). Arteries and veins were equilibrated to 1.0 and results indicate that ergot alkaloids associated with 0.5 g, respectively, for 90 min followed by the reference toxic endophyte-infected tall fescue are vasoactive and addition of 120 mM KCl. Increasing concentrations of can potentially alter arterial blood supply and venous each alkaloid were added to the respective chamber ev- drainage from the bovine foregut. ery 15 min after buffer replacement. Data were normal- Key words: bovine, ergot alkaloid, fescue toxicosis, ruminal artery and vein, vasoconstriction ©2011 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2011. 89:2944–2949 doi:10.2527/jas.2010-3626 INTRODUCTION Ergot alkaloids have been implicated in causing vaso- constriction, which is a source of clinical symptoms of The association of Neotyphodium coenophialum with the fescue toxicosis syndrome (Strickland et al., 2011). tall fescue (Lolium arundinaceum) results in produc- Prior research has mainly focused on constriction of tion of numerous ergot alkaloids (Lyons et al., 1986). peripheral vasculature like the caudal artery (Aiken et al., 2007), saphenous vein (Klotz et al., 2006), and the dorsal pedal vein (Solomons et al., 1989). There is a paucity of data addressing the effects of ergot alkaloids 1 Mention of a trade name, proprietary product, or specified equip- ment does not constitute a guarantee or warranty by the USDA and on vasculature supporting core body tissues. Rhodes does not imply approval to the exclusion of other products that may et al. (1991) is the only study that has addressed this. be available. Using labeled microspheres, they reported a reduction 2 The authors gratefully acknowledge Adam J. Barnes of the For- in blood flow to the duodenum, colon, and kidney of age-Animal Production Research Unit for his hard work in monitor- cattle consuming endophyte-infected tall fescue at high ing the myograph. 3 Corresponding author: [email protected] ambient temperatures. Received October 22, 2010. Westendorf et al. (1992), Moyer et al. (1993), and Accepted April 12, 2011. DeLorme et al. (2007) all assert that the rumen is the 2944 Downloaded from jas.fass.org at USDA Natl Agricultural Library on October 6, 2011 Foregut vasculature response to ergot alkaloids 2945 primary site of alkaloid liberation, degradation, and possibly absorption. Bovine ruminal tissue has been shown to have a capacity to absorb ergot alkaloids (Ayers et al., 2009). Using sheep, Westendorf et al. (1993) demonstrated that only 50 to 60% of ingest- ed alkaloids are recovered in abomasal contents. The fraction of alkaloids disappearing in the reticulorumen likely represents both microbial degradation and ab- sorption. It is hypothesized that absorption of ergot alkaloids combined with the tendency of ergopeptine alkaloids to bioaccumulate in vascular tissue (Klotz et al., 2009) could result in vasoconstriction and a con- comitant reduction in blood flow. Klotz et al. (2011) recently developed a ruminal artery and vein bioassay designed to evaluate the response different toxicants elicit. Therefore, the objective of this study was to de- termine if ergoline and ergopeptine alkaloids (Figure 1) would elicit a vasoactive response in bovine ruminal artery and vein preparations in vitro. MATERIALS AND METHODS Methods used with live animals in this study were approved by the University of Kentucky Institutional Animal Care and Use Committee. Animals and Tissues Predominantly Angus-bred heifers (n = 10; BW = 498 ± 9 kg) were utilized in this study. Heifers were fed a basal diet consisting of cotton seed hulls, soybean hulls, corn, and soybean meal (41.9, 31.4, 21.45, and 5.25% of diet on an as-fed basis, respectively). The nu- trient composition of the diet was 9.9% CP and 58.0% NDF on a DM basis. Heifers were fed this diet for a minimum of 232 d. Sections of right ruminal artery and vein were col- lected from the ventral coronary groove of the rumen shortly after each animal was stunned by captive bolt, exsanguinated, and eviscerated at the University of Kentucky abattoir. Tissues were immersed in a modi- fied Krebs-Henseleit oxygenated buffer (95% O2 + 5% CO2; pH = 7.4; mM composition = d-glucose, 11.1; MgSO4, 1.2; KH2PO4, 1.2; KCl, 4.7; NaCl, 118.1; CaCl2, 3.4; and NaHCO3, 24.9; Sigma Chemical Co., St. Louis, MO) and placed on ice for transport to the laboratory. Artery and vein were separated, cleaned of excessive Figure 1. Chemical structure of A) d-lysergic acid and B) ergo- fat and connective tissue, sliced into 2- to 3-mm cross novine, which are both examples of ergoline alkaloids present in Neo- sections, and examined under a dissecting microscope typhodium coenophialum infected tall fescue (Lolium arundinaceum). (Stemi 2000-C, Carl Zeiss Inc., Oberkochen, Germany) C) Generalized structure of ergopeptine alkaloids indicating the vari- able R1 and R2 sites. Common R1 groups are methyl (ergotamine, at 12.5× magnification to ensure structural integrity ergovaline, and α-ergosine) and isopropyl (ergocristine, ergocornine, of the vessel. Dimensions of the blood vessels were re- and α-ergocryptine). Common R2 groups are isopropyl (ergovaline and ergocornine), isobutyl (α-ergosine and α-ergocryptine), and methyl corded (Axiovision, version 20, Carl Zeiss Inc.) to en- benzyl (ergotamine and ergocristine). sure the segment size was consistent. Vessel segments were then mounted on luminal supports in a tissue bath (DMT610M Multichamber myograph, Danish Myo was further modified for tissue incubation by adding Technologies, Atlanta, GA) containing 5 mL of con- desipramine (3 × 10−5 M; D3900 Sigma Chemical Co.) −6 tinuously gassed (95% O2 + 5% CO2) modified Krebs- and propranolol (1 × 10 M; P0844, Sigma Chemical Henseleit buffer at 37°C. The buffer used for transport Co.) to inactivate neuronal reuptake of catecholamines Downloaded from jas.fass.org at USDA Natl Agricultural Library on October 6, 2011 2946 Foote et al. and to block β-adrenergic receptors, respectively. Tis- sue samples were equilibrated to a resting tension of 1.0 g for ruminal artery and 0.5 g for ruminal vein for 90 min with buffer replacement at 15-min intervals, as validated by Klotz et al. (2011). Vessels were then exposed to KCl (120 mM) to ensure tissue viability and to provide a reference for normalization of contractile responses. Concentration Responses of Ergot Alkaloids Stock standards of ergovaline tartrate (≥93% purity, supplied by F. T. Smith, Auburn University, Auburn, AL), ergotamine d-tartrate (≥97% purity, #45510, Fluka, Sigma Chemical Co.), α-ergocryptine (99% purity, E5625, Sigma Chemical Co.), and ergocristine (05-9034-17, Research Plus Inc., Barnegat, NJ) were prepared in 100% methanol. d-Lysergic acid hydrate (95% purity, Acros Organics, Geel, Belgium) was pre- pared in 80% (vol/vol) methanol that contained 1.2 × 10−4 M acetic acid. Ergonovine maleate (100% purity, E6500, Sigma Chemical Co.) was prepared in H2O. Er- gocornine (>95% purity, E131, Sigma Chemical Co.) was prepared in dimethyl sulfoxide. Standards were prepared in a concentration of 2 × 10−2 M and added in 25-µL aliquots to achieve a concentration of 1 × 10−4 M in the tissue bath.
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