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Article

Ginseng Extract Ameliorates the Negative Physiological Effects of Heat Stress by Supporting Heat Shock Response and Improving Intestinal Barrier Integrity: Evidence from Studies with Heat-Stressed Caco-2 Cells, C. elegans and Growing Broilers

by
Georg Sandner
1,†,
Andreas S. Mueller
2,*,
Xiaodan Zhou
2,†,
Verena Stadlbauer
1,3,
Bettina Schwarzinger
1,3,4,
Clemens Schwarzinger
4,
Uwe Wenzel
5,
Klaus Maenner
6,
Jan Dirk van der Klis
2,
Stefan Hirtenlehner
2,
Tobias Aumiller
2 and
Julian Weghuber
1,3,*
1
School of Engineering and Environmental Sciences, University of Applied Sciences Upper Austria, Stelzhamerstraße 23, Wels 4600, Austria
2
Delacon Biotechnik GmbH, Weissenwolffstraße 14, Steyregg 4221, Austria
3
FFoQSI GmbH-Austrian Competence Centre for Feed and Food Quality, Safety and Innovation, Technopark 1C, Tulln 3430, Austria
4
Johannes Kepler University, Institute for Chemical Technology of Organic Materials, Linz, Austria 4040
5
Molecular Nutrition Research, Interdisciplinary Research Centre, Justus-Liebig-University of Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany
6
Institute of Animal Nutrition of Free University Berlin, Königin-Luise-Str.49, 14195 Berlin, Germany
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Molecules 2020, 25(4), 835; https://doi.org/10.3390/molecules25040835
Submission received: 12 October 2019 / Revised: 11 February 2020 / Accepted: 13 February 2020 / Published: 14 February 2020
(This article belongs to the Special Issue Current Trends in Ginseng Research)
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Abstract

Climatic changes and heat stress have become a great challenge in the livestock industry, negatively affecting, in particular, poultry feed intake and intestinal barrier malfunction. Recently, phytogenic feed additives were applied to reduce heat stress effects on animal farming. Here, we investigated the effects of ginseng extract using various in vitro and in vivo experiments. Quantitative real-time PCR, transepithelial electrical resistance measurements and survival assays under heat stress conditions were carried out in various model systems, including Caco-2 cells, Caenorhabditis elegans and jejunum samples of broilers. Under heat stress conditions, ginseng treatment lowered the expression of HSPA1A (Caco-2) and the heat shock protein genes hsp-1 and hsp-16.2 (both in C. elegans), while all three of the tested genes encoding tight junction proteins, CLDN3, OCLN and CLDN1 (Caco-2), were upregulated. In addition, we observed prolonged survival under heat stress in Caenorhabditis elegans, and a better performance of growing ginseng-fed broilers by the increased gene expression of selected heat shock and tight junction proteins. The presence of ginseng extract resulted in a reduced decrease in transepithelial resistance under heat shock conditions. Finally, LC-MS analysis was performed to quantitate the most prominent ginsenosides in the extract used for this study, being Re, Rg1, Rc, Rb2 and Rd. In conclusion, ginseng extract was found to be a suitable feed additive in animal nutrition to reduce the negative physiological effects caused by heat stress.
Keywords: Ginseng extract; heat stress; intestinal barrier; broiler Ginseng extract; heat stress; intestinal barrier; broiler
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MDPI and ACS Style

Sandner, G.; Mueller, A.S.; Zhou, X.; Stadlbauer, V.; Schwarzinger, B.; Schwarzinger, C.; Wenzel, U.; Maenner, K.; van der Klis, J.D.; Hirtenlehner, S.; et al. Ginseng Extract Ameliorates the Negative Physiological Effects of Heat Stress by Supporting Heat Shock Response and Improving Intestinal Barrier Integrity: Evidence from Studies with Heat-Stressed Caco-2 Cells, C. elegans and Growing Broilers. Molecules 2020, 25, 835. https://doi.org/10.3390/molecules25040835

AMA Style

Sandner G, Mueller AS, Zhou X, Stadlbauer V, Schwarzinger B, Schwarzinger C, Wenzel U, Maenner K, van der Klis JD, Hirtenlehner S, et al. Ginseng Extract Ameliorates the Negative Physiological Effects of Heat Stress by Supporting Heat Shock Response and Improving Intestinal Barrier Integrity: Evidence from Studies with Heat-Stressed Caco-2 Cells, C. elegans and Growing Broilers. Molecules. 2020; 25(4):835. https://doi.org/10.3390/molecules25040835

Chicago/Turabian Style

Sandner, Georg, Andreas S. Mueller, Xiaodan Zhou, Verena Stadlbauer, Bettina Schwarzinger, Clemens Schwarzinger, Uwe Wenzel, Klaus Maenner, Jan Dirk van der Klis, Stefan Hirtenlehner, and et al. 2020. "Ginseng Extract Ameliorates the Negative Physiological Effects of Heat Stress by Supporting Heat Shock Response and Improving Intestinal Barrier Integrity: Evidence from Studies with Heat-Stressed Caco-2 Cells, C. elegans and Growing Broilers" Molecules 25, no. 4: 835. https://doi.org/10.3390/molecules25040835

APA Style

Sandner, G., Mueller, A. S., Zhou, X., Stadlbauer, V., Schwarzinger, B., Schwarzinger, C., Wenzel, U., Maenner, K., van der Klis, J. D., Hirtenlehner, S., Aumiller, T., & Weghuber, J. (2020). Ginseng Extract Ameliorates the Negative Physiological Effects of Heat Stress by Supporting Heat Shock Response and Improving Intestinal Barrier Integrity: Evidence from Studies with Heat-Stressed Caco-2 Cells, C. elegans and Growing Broilers. Molecules, 25(4), 835. https://doi.org/10.3390/molecules25040835

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