Category Research project
  • Analytik
  • Toxikologie

Identification of the structure-dependent toxicity of hepatotoxic pyrrolizidine alkaloids

Project status
Completed
Project start
Jun 2017
Project end
May 2020
Department
Lebensmittelsicherheit

Description and Objective

Unsaturated pyrrolizidine alkaloids (PA) belong to the most toxic compounds; more than 400 PA have been described in a wide range of plants. They are also found in Senecio vulgaris L. PA are toxic to humans and animals. PA were detected in substantial amounts into honey and tea. Acute PA poisoning via food contamination causes severe damage to the liver; long-term, sub-lethal doses may cause cumulative damage or cancer. Animal studies revealed that PA are carcinogenic. Mutagenicity of PA was observed in several in vitro and in vivo test systems. The toxicity of these compounds is associated with enzymatic reactions by enzymes dominantly expressed in the liver and dependent on PA´s bioavailability. However, the modeModeTo glossary of action of PA to generate hepatotoxicity is not yet identified. Based on our results for bioavailability and the molecular mode of action of the structurally different PA echimidine, heliotrine, senecionine, and senkirkine we hypothesize that PA act in a structure-dependent manner. Therefore we aimed to group the PA structure- and toxicity-dependent within this project. For that purpose bioavailability shall be further studied in an in vitro model for the human intestinal barrier with a larger set of PA (22). As endpoint for grouping the ABCB1-dependent transport/detoxification shall be investigated for the structure-dependent mode of action of PA. Additionally, the molecular mechanism of PA hepatic toxicity shall be analyzed. We already showed in our transcriptomic study with the 4 structurally different PA differences in the induction of gene expression in the liver. Therefore, in vivo analysis of the induction of hepatotoxicity in mice in real time shall be analysed using two-photon excitation microscopy. The structure-dependent induction of toxicity shall be investigated using specific liver marker in wildtype mice and in further step in Abcb1 knockout mice.

Result

1,2-unsaturated pyrrolizidine alkaloids (PAs) are the most widespread natural toxins. Humans are directly exposed to these substances through the consumption of contaminated food. PA poisoning can lead to severe liver damage, such as hepatic veno-occlusive disease (VOD). PAs are not toxic per se. In the liver, their enzymatic activation occurs to form highly reactive metabolites that can form DNA and protein adducts. So far, little is known about the molecular mechanisms of action of PAs. This project aims to contribute to a better understanding of the molecular mode of action and, in particular, the structure-activity relationships of PAs in order to further elucidate the development of PA-induced toxicity in humans and to better assess a potential hazard to humans from PA ingestion. The aims of this project included elucidation of structure-dependent uptake across the intestinal epithelium in vitro (Caco-2/MDCKII cell model) and structure-dependent induction of liver toxic effects in vitro. Endpoints for analysis of liver toxicity included induction of cytotoxicity and apoptosis and disruption of bile acid homeostasis. The passage of structurally different PAs across the intestinal epithelium was studied using the Caco 2 and MDCKII cell models. In preliminary work for this project, it was hypothesized that PAs pass through the intestinal epithelium depending on their structure, which should be directly associated with ABCB1-dependent efflux. This hypothesis could not be confirmed as a result of this project. Potential ABCB-1-dependent efflux was shown to occur in all structure types regardless of necine base or degree of esterification. Nevertheless, we were able to show that PAs pass the intestinal epithelium to different degrees. Transferred to the in vivo situation, this implies that PAs enter the liver with portal blood. The structure-dependent induction of liver toxic effects was systematically investigated in the second part of this project. A transcriptome study in primary human hepatocytes treated with four structurally different PAs provided evidence for biological endpoints affected by PA. After establishing an appropriate liver cell model, induction of cytotoxicity, induction of apoptosis, and disruption of bile acid homeostasis were examined with a set of first 22, then 14 PAs in the human hepatoma cell line HepaRG. Our results clearly show strong grouping of PAs across all endpoints. The PA monoesters have no inducing effect on any of the end points studied, whereas cyclic PAs and open-chain diesters (especially of the heliotridine type) are particularly toxic. Also, the disturbance of bile acid homeostasis goes along with the grouping elaborated in the cytotoxicity studies. Thus, our studies in the liver show strong structure-dependent differences in the induction of toxic effects. This is possibly associated with different cellular uptake mechanisms and/or enzyme affinities for bioactivation.In a final part of the project, the induction of liver toxicity in vivo was investigated in mice using the PA senecionine as representative. This study demonstrated a time- and dose-dependent induction of severe liver injury associated with an increase in liver parameters ALT and AST. By using a reporter mouse with green-fluorescent endothelial cells, endothelial cells were specifically confirmed as a target of PA-induced liver toxicity. These effects were accompanied by pericentral hepatocellular necrosis, severe hemorrhage, and impaired bile acid secretion. In addition, infiltration of immune cells was observed. To investigate the metabolism¬dependency of this effect, Por-knockout mice that no longer exhibited CYP activity were used. In these mice, no liver toxic effects could be identified after senecionine treatment. Thus, we clearly demonstrated here that metabolic toxification by CYP must occur to form the potent liver toxic properties of senecionine.In summary, our results show that structure-dependent properties of PAs cannot be generalized. Although we identified a pattern in the liver, which could be reproduced in all levels of the studies, we could not find this grouping again with regard to passage across the intestinal epithelium, which, however, may also be associated with the chosen models. Thus, caution is advised to follow a uniform grouping; it is more important to consider the endpoints and questions separately.
Type of project

Third-party funded project

Research focus

Wirkungsbezogene Analytik und Risikofrüherkennung / Nachweis von Kontaminanten und zur Bewertung chemischer Risiken

Organisational units and partners

Lead specialist group: Risikobewertungsstrategien (RBS)
Contact persons: Prof. Dr. Dr. Alfonso Lampen, PDshort foroutside lecturer Dr. Stefanie Hessel-Pras
Involved BfR partners: Sicherheit in der Nahrungskette
External partner: Nederlands Kanker Instituut, Leibniz-Institut für Arbeitsforschung an der TU Dortmund, University of Dundee, Naturwissenschaftliches und Medizinisches Institut, Dr. Margarete Fischer-Bosch-Institut für Klinische Pharmakologie, Wallenberg laboratory, Sahlgrenska Hospital

Funding body and grant number

Deutsche Forschungsgemeinschaft e.V.
LA1177/12-1