Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-16T09:20:17.341Z Has data issue: false hasContentIssue false

Innate immunity and metabolomic responses in dairy cows challenged intramammarily with lipopolysaccharide after subacute ruminal acidosis

Published online by Cambridge University Press:  13 March 2018

E. Humer
Affiliation:
Department for Farm Animals and Veterinary Public Health, Institute of Animal Nutrition and Functional Plant Compounds, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
S. Aditya
Affiliation:
Department for Farm Animals and Veterinary Public Health, Institute of Animal Nutrition and Functional Plant Compounds, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria Faculty of Veterinary Medicine, Brawijaya University, Jl. Mayjen Haryono No. 169, Malang 65145, East Java, Indonesia
Q. Zebeli*
Affiliation:
Department for Farm Animals and Veterinary Public Health, Institute of Animal Nutrition and Functional Plant Compounds, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
*
Get access

Abstract

Subacute ruminal acidosis (SARA) is a prevalent metabolic disorder in dairy cows known to elicit local and systemic immune responses. We recently showed that cows experiencing SARA and challenged intramammarily with lipopolysaccharide (LPS) experienced stronger metabolic disturbances compared with cows without SARA. Therefore, we hypothesized that cows experiencing SARA have a modulated innate immune response and impaired plasma metabolome compared with healthy cows when experiencing an acute mastitis challenge. A total of 18 Simmental cows were subjected either to a Control (CON, n=6) or SARA (n=12) feeding regimen, receiving either 40% or 60% concentrates for 30 days. Thereafter, six SARA (SARA-LPS) and the CON (CON-LPS) cows were intramammarily challenged with 50 µg LPS from Escherichia coli (O26 : B6), while the remaining six SARA cows (SARA-PLA) received a placebo. Blood and milk samples were analyzed for acute phase proteins and a targeted ESI-LC-MS/MS-based metabolomics approach was performed in blood samples 24 h after the LPS challenge. The LPS infusion caused a strong increase in immune response variables, with a higher concentration of milk amyloid A 48 h after the LPS challenge in SARA-LPS compared with CON-LPS cows. Cows receiving the LPS infusion had a lower plasma concentration of several amino acids and lysophosphatidylcholines but without differences in SARA cows and healthy cows. In conclusion, our results revealed that an intramammary LPS infusion increased acute phase proteins and modulated the blood metabolome. While no systemic differences between SARA and healthy cows were observed, cows experiencing SARA showed a higher concentration of an acute phase protein at the local level of the mammary gland. Further research is required to elucidate the underlying mechanisms and to evaluate its clinical significance for udder health.

Type
Research Article
Copyright
© The Animal Consortium 2018 

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.)

References

Aditya, S, Humer, E, Pourazad, P, Khiaosa-ard, R, Huber, J and Zebeli, Q 2017. Intramammary infusion of Escherichia coli lipopolysaccharide negatively affects feed intake, chewing behavior, milk and clinical parameters, but some effects are stronger in cows experiencing subacute rumen acidosis. Journal of Dairy Science 100, 13631377.Google Scholar
Aditya, S, Humer, E, Pourazad, P, Khiaosa-ard, R and Zebeli, Q 2018. Metabolic and stress responses in dairy cows fed concentrate-rich diet and submitted to intramammary lipopolysaccharide challenge. Animal 1–9, https://doi.org/10.1017/S1751731117002191.Google Scholar
Ceciliani, F, Geron, JJ, Eckersall, PD and Sauerwein, H 2012. Acute phase proteins in ruminants. Journal of Proteomics 75, 42074231.Google Scholar
del Bas, JM, Caimari, A, Rodriguez-Naranjo, MI, Childs, CE, Chavez, CP, West, AL, Miles, EA, Arola, L and Calder, PC 2016. Impairment of lysophospholipid metabolism in obesity: altered plasma profile and desensitization to the modulatory properties of n-3 polyunsaturated fatty acids in a randomized controlled trial. The American Journal of Clinical Nutrition 104, 266279.Google Scholar
Eckel, EF and Ametaj, BN 2016. Invited review: role of bacterial endotoxins in the etiopathogenesis of periparturient diseases of transition dairy cows. Journal of Dairy Science 99, 59675990.Google Scholar
Gerardi, G, Bernardini, D, Elia, CA, Ferrari, V, Iob, L and Segato, S 2009. Use of serum amyloid A and milk amyloid A in the diagnosis of subclinical mastitis in dairy cows. Journal of Dairy Research 76, 411417.Google Scholar
Grzelczyk, A and Gendaszewska-Darmach, E 2013. Novel bioactive glycerol-based lysophospholipids: new data – new insight into their function. Biochimie 95, 667679.Google Scholar
Grimble, RF 2001. Nutritional modulation of immune function. Proceedings of the Nutrition Society 60, 389397.Google Scholar
Hailemariam, D, Mandal, R, Saleem, F, Dunn, SM, Wishart, DS and Ametaj, BN 2014a. Identification of predictive biomarkers of disease state in transition dairy cows. Journal of Dairy Science 97, 26802693.Google Scholar
Hailemariam, D, Mandal, R, Saleem, F, Dunn, SM, Wishart, DS and Ametaj, BN 2014b. Metabolomics approach reveals altered plasma amino acid and sphingolipid profiles associated with pathological state in transition dairy cows. Current Metabolomics 2, 184195.Google Scholar
Humbledt, MF, Guyot, H, Boudry, B, Mbayahi, F, Hanzen, C, Rollin, R and Godeau, JM 2006. Relationship between haptoglobin, serum amyloid A, and clinical status in survey of dairy herds during a 6-month period. Veterinary Clinical Pathology 35, 188193.Google Scholar
Humer, E, Khol-Parisini, A, Metzler-Zebeli, BU, Gruber, L and Zebeli, Q 2016. Alterations of the lipid metabolome in dairy cows experiencing excessive lipolysis early postpartum. PLoS One 11, e0158633.Google Scholar
Hung, ND, Sok, D-E and Kim, MR 2012. Prevention of 1-palmitoyl lysophosphatidylcholine-induced inflammation by polyunsaturated acyl lysophosphatidylcholine. Inflammation Research 61, 473483.Google Scholar
Jain, S, Gautam, V and Naseem, S 2011. Acute-phase proteins: a diagnostic tool. Journal of Pharmacy and BioAllied Sciences 3, 118127.Google Scholar
Jia, YY, Wang, SQ, Ni, YD, Zhang, YS, Zhuang, S and Shen, XZ 2014. High concentrate-induced subacute ruminal acidosis (SARA) increases plasma acute phase protein and cortisol in goats. Animal 8, 14331438.Google Scholar
Jing, Q, Xin, SM, Zhang, WB, Wang, P, Qin, YW and Pei, G 2000. Lysophosphatidylcholine activates p38 and p42/44 mitogen-activated protein kinases in monocytic THP-1 cells, but only p38 activation is involved in its stimulated chemotaxis. Circulation Research 87, 5259.Google Scholar
Kabarowski, JH, Xu, Y and Witte, ON 2002. Lysophosphatidylcholine as a ligand for immunoregulation. Biochemical Pharmacology 64, 161167.Google Scholar
Karlstad, MD and Sayeed, MM 1987. Effect of endotoxic shock on skeletal muscle intracellular electrolytes and amino acid transport. American Journal of Physiology 252, 674680.Google Scholar
Khafipour, E, Krause, DO and Plaizier, JC 2009. A grain-based subacute ruminal acidosis challenge causes translocation of lipopolysaccharide and triggers inflammation. Journal of Dairy Science 92, 10601070.Google Scholar
Lüttgenau, J, Wellnitz, O, Kradolfer, D, Kalaitzakis, E, Ulbrich, SE, Bruckmaier, RM and Bollwein, H 2016. Intramammary lipopolysaccharide infusion alters gene expression but does not induce lysis of the bovine corpus luteum. Journal of Dairy Science 99, 114.Google Scholar
Murata, H, Shimada, N and Yoshioka, M 2004. Current research on acute phase proteins in veterinary diagnosis: an overview. The Veterinary Journal 168, 2840.Google Scholar
Newsholme, P 2001. Why is L-glutamine metabolism important to cells of the immune system in health, postinjury, surgery or infection? The Journal of Nutrition 131, 25152522.Google Scholar
Obled, C 2003. Amino acid requirements in inflammatory states. Canadian Journal of Animal Science 83, 365373.Google Scholar
Plaizier, JC, Khafipour, E, Li, S, Gozho, GN and Krause, DO 2012. Subacute ruminal acidosis (SARA), endotoxins, and health consequences. Animal Feed Science and Technology 172, 921.Google Scholar
Riederer, M, Ojala, PJ, Hrzenjak, A, Graier, WF, Malli, R, Tritscher, M, Hermansson, M, Watzer, B, Schweer, H, Desoye, G, Heinemann, A and Frank, S 2010. Acyl chain-dependent effect of lysophosphatidylcholine on endothelial prostacyclin production. Journal of Lipid Research 51, 29572966.Google Scholar
Suliman, ME, Qureshi, AR, Stenvinkel, P, Pecoits-Filho, R, Bárány, P, Heimbürger, O, Anderstam, B., Ayala, ER, Filho, JCD, Alverstrand, A and Lindholm, B 2005. Inflammation contributes to low plasma amino acid concentrations in patients with chronic kidney disease. The American Journal of Clinical Nutrition 82, 342439.Google Scholar
Taylor, LA, Arends, JA, Hodina, AK, Unger, C and Massing, U 2007. Plasma lyso-phosphatidylcholine concentration is decreased in cancer patients with weight loss and activated inflammatory status. Lipids in Health and Disease 6:17.Google Scholar
Vailati-Riboni, M, Zhou, Z, Jacometo, CB, Minuti, A, Trevisi, E, Luchini, DN and Loor, JJ 2017. Supplementation with rumen-protected methionine or choline during the transition period influences whole-blood immune response in periparturient dairy cows. Journal of Dairy Science 100, 39583968.Google Scholar
Vels, L, Røntved, CM, Bjerring, M and Ingvartsen, KL 2009. Cytokine and acute phase protein gene expression in repeated liver biopsies of dairy cows with a lipopolysaccharide-induced mastitis. Journal of Dairy Science 92, 922934.Google Scholar
Wu, G 1998. Intestinal mucosal amino acid catabolism. The Journal of Nutrition 128, 12491252.Google Scholar
Zebeli, Q and Metzler-Zebeli, BU 2012. Interplay between rumen digestive disorders and diet-induced inflammation in dairy cattle. Research in Veterinary Science 93, 10991108.Google Scholar
Zeng, R, Bequette, BJ, Vinyard, BT and Bannerman, DD 2009. Determination of milk and blood concentrations of lipopolysaccharide-binding protein in cows with naturally acquired subclinical and clinical mastitis. Journal of Dairy Science 92, 980989.Google Scholar
Zhou, Z, Loor, JJ, Piccioli-Cappelli, F, Librandi, F, Lobley, GE and Trevisi, E 2016. Circulating amino acids in blood plasma during the peripartal period in dairy cows with different liver functionality index. Journal of Dairy Science 99, 22572267.Google Scholar
Supplementary material: File

Humer et al. supplementary material

Tables S1-S2

Download Humer et al. supplementary material(File)
File 62.7 KB