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Fumonisins: oxidative stress-mediated toxicity and metabolism in vivo and in vitro

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Abstract

Fumonisins (FBs) are widespread Fusarium toxins commonly found as corn contaminants. FBs could cause a variety of diseases in animals and humans, such as hepatotoxic, nephrotoxic, hepatocarcinogenic and cytotoxic effects in mammals. To date, almost no review has addressed the toxicity of FBs in relation to oxidative stress and their metabolism. The focus of this article is primarily intended to summarize the progress in research associated with oxidative stress as a plausible mechanism for FB-induced toxicity as well as the metabolism. The present review showed that studies have been carried out over the last three decades to elucidate the production of reactive oxygen species (ROS) and oxidative stress as a result of FBs treatment and have correlated them with various types of FBs toxicity, indicating that oxidative stress plays critical roles in the toxicity of FBs. The major metabolic pathways of FBs are hydrolysis, acylation and transamination. Ceramide synthase, carboxylesterase FumD and aminotransferase FumI could degrade FB1 and FB2. The cecal microbiota of pigs and alkaline processing such as nixtamalization can also transform FB1 into metabolites. Most of the metabolites of FB1 were less toxic than FB1, except its partial (pHFB1) metabolites. Further understanding of the role of oxidative stress in FB-induced toxicity will throw new light on the use of antioxidants, scavengers of ROS, as well as on the blind spots of metabolism and the metabolizing enzymes of FBs. The present review might contribute to reveal the toxicity of FBs and help to protect against their oxidative damage.

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Abbreviations

8-OH-dG:

8-Hydroxydeoxyguanosine

ALAT:

Alanine aminotransferase

aminopolyols:

Hydrolyzed fumonisins

ASAT:

Aspartate aminotransferase

CAT:

Catalase

CBMN:

Cytokinesis-block micronucleus assay

CHL:

Sodium copper chlorophyllin

CoQ10:

Coenzyme Q10

CYP1A1:

O-deethylation of ethoxyresorufin

CYP3A1:

N-demethylation of erythromycin

DPPH:

2,2-Diphenyl-1-picrylhydrazyl

DON:

Deoxynivalenol

ERK:

Extracellular signal-regulated kinase

FB:

Fumonisin

FL:

Fluorescence detection

GE:

Ginseng extract

GPx:

Glutathione peroxidase

GR:

Glutathione reductase

GSH:

Glutathione

GST:

Glutathione S-transferases

H2O2 :

Hydrogen peroxide

HFB1/2:

Hydrolyzed fumonisin B1 and/or B2

HPBLs:

Human peripheral blood lymphocytes

HPLC:

High-performance liquid chromatography

HO· :

Hydroxyl radical

HOO− :

Perhydroxy radical

Hsps:

Heat shock proteins

HT29:

Human colonic cell line

IARC:

The International Agency for Research on Cancer

IHKE cells:

Human proximal tubule-derived cells

iNOS:

Inducible nitric oxide synthase

i.p.:

Intraperitoneally

JNK:

c-Jun N-terminal kinase

LAB:

Lactic acid bacteria

MAPKs:

Mitogen-activated protein kinases

MDA:

Malondialdehyde

MEF:

Mouse embryonic fibroblasts

Mn-PCEs:

Micronucleated polychromatic erythrocytes

MTA:

Methylthioadenosine

NCEs:

Normochromatic erythrocytes

NDF:

N-(1-deoxy-d-fructos-1-yl) fumonisin1

N-Pal-HFB1 (PAP1):

N-palmitoyl-hydrolyzed fumonisin1, NTD, neural tube defects

O ·−2 :

Superoxide anion

OTA:

Ochratoxin A

OTM:

Olive tail moment

PBMC:

Peripheral blood mononuclear cells

PCEs:

Polychromatic erythrocytes

PCs:

Protein carbonyls

PGE:

Panax ginseng extract

pHFB1:

Partially hydrolyzed FB1

RJ:

Royal jelly

RNS:

Reactive nitrogen species

ROM:

Reactive oxygen metabolites

ROS:

Reactive oxygen species

SAM:

S-adenosylmethionine

SCGE:

Alkaline comet assay

SMC:

Spleen mononuclear cells

SOD:

Superoxide dismutase

TBARS:

Thiobarbituric acid-reacting substances

U-118MG:

Human U-118MG glioblastoma

ZEN:

Zearalenone

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Acknowledgments

This work was supported by Grants from 948 of the Ministry of Agriculture Project (2014-S12), International Cooperation Project (4002-122002), National Basic Research Program of China (2009C118800), Project of Excellence FIM UHK and Project Ref. S2013/ABI-2728 (ALIBIRD-CM Program) from Comunidad de Madrid, Spain.

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Authors and Affiliations

  1. National Reference Laboratory of Veterinary Drug Residues (HZAU) and MAO Key Laboratory for Detection of Veterinary Drug Residues, Huazhong Agricultural University, Wuhan, 430070, Hubei, China

    Xu Wang & Zonghui Yuan

  2. MOA Laboratory for Risk Assessment of Quality and Safety of Livestock and Poultry Products, Huazhong Agricultural University, Wuhan, 430070, Hubei, China

    Dan Wan, Qianying Liu, Dongmei Chen & Zonghui Yuan

  3. Hubei Collaborative Innovation Center for Animal Nutrition and Feed Safety, Wuhan, Hubei, China

    Zhenli Liu & Zonghui Yuan

  4. Departamento de Toxicología y Farmacología, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040, Madrid, Spain

    Xu Wang, María Rosa Martínez-Larrañaga, María Aránzazu Martínez & Arturo Anadón

  5. College of Life Science, Yangtze University, Jingzhou, China

    Qinghua Wu

  6. Center for Basic and Applied Research, Faculty of Informatics and Management, University of Hradec Kralove, Hradec Kralove, Czech Republic

    Qinghua Wu

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  1. Xu Wang
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  2. Qinghua Wu
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  3. Dan Wan
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Correspondence to Arturo Anadón or Zonghui Yuan.

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Wang, X., Wu, Q., Wan, D. et al. Fumonisins: oxidative stress-mediated toxicity and metabolism in vivo and in vitro. Arch Toxicol 90, 81–101 (2016). https://doi.org/10.1007/s00204-015-1604-8

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