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A review of species differences in the control of, and response to, chemical-induced thyroid hormone perturbations leading to thyroid cancer

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Abstract

This review summarises the current state of knowledge regarding the physiology and control of production of thyroid hormones, the effects of chemicals in perturbing their synthesis and release that result in thyroid cancer. It does not consider the potential neurodevelopmental consequences of low thyroid hormones. There are a number of known molecular initiating events (MIEs) that affect thyroid hormone synthesis in mammals and many chemicals are able to activate multiple MIEs simultaneously. AOP analysis of chemical-induced thyroid cancer in rodents has defined the key events that predispose to the development of rodent cancer and many of these will operate in humans under appropriate conditions, if they were exposed to high enough concentrations of the affecting chemicals. There are conditions however that, at the very least, would indicate significant quantitative differences in the sensitivity of humans to these effects, with rodents being considerably more sensitive to thyroid effects by virtue of differences in the biology, transport and control of thyroid hormones in these species as opposed to humans where turnover is appreciably lower and where serum transport of T4/T3 is different to that operating in rodents. There is heated debate around claimed qualitative differences between the rodent and human thyroid physiology, and significant reservations, both scientific and regulatory, still exist in terms of the potential neurodevelopmental consequences of low thyroid hormone levels at critical windows of time. In contrast, the situation for the chemical induction of thyroid cancer, through effects on thyroid hormone production and release, is less ambiguous with both theoretical, and actual data, showing clear dose-related thresholds for the key events predisposing to chemically induced thyroid cancer in rodents. In addition, qualitative differences in transport, and quantitative differences in half life, catabolism and turnover of thyroid hormones, exist that would not operate under normal situations in humans.

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Fig. 1

Redrawn from https://courses.lumenlearning.com/ap2/chapter/the-thyroid-gland/

Fig. 2
Fig. 3
Fig. 4
Fig. 5

Derived from Crofton (2008) and Noyes et al (2019)

Fig. 6
Fig. 7
Fig. 8

Adapted from Visser et al. (2016)

Fig. 9

Redrawn from Fig. 8 from Yu et al. (2002)

Fig. 10
Fig. 11
Fig. 12
Fig. 13

Data taken from York et al. (2003)

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Abbreviations

T4:

Thyroxine

T3:

Tri-iodothyronine

DIT:

Di-iodothyronine

MIT:

Mono-iodothyronine

TSH:

Thyrotropin or thyroid stimulating hormone

UDPGT:

Uridine diphosphate glucuronyltransferase

SULT:

Sulfotransferase

NIS:

Sodium-iodide symporter

TPO:

Thyroperoxidase

AOP:

Adverse outcome pathway

KE:

Key events

MIE:

Molecular initiating event

MoA:

Mode of action

Ph II:

Phase 2 metabolism

TTR:

Transthyretin

TBG:

Thyroxine binding globulin

NIS:

Sodium iodide symporter

rT3:

Reverse T3

T3S:

Sulphated T3

TRE:

Thyroid response elements

PPAR:

Peroxisome proliferator activated receptor

RXR:

Retinoid X receptor

CAR:

Constitutive androstane receptor

IGF:

Insulin like growth factor

PCB:

Polychlorinated biphenyl

PBB:

Polybrominated biphenyl

TCDD:

Tetrachlorodibenzo-p-dioxin

PTU:

6-Propylthiouracil

CSF:

Cerebrospinal fluid

MCT:

Monocarboxylate transporter

OATP:

Organic anion transporter protein

NOAEL:

No observable adverse effect level

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Acknowledgements

The author acknowledges the financial support of the European Crop Protection Agency in financially supporting the preparation of this manuscript.

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The preparation of this manuscript was funded by the European Crop Protection Association.

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  1. Regulatory Science Associates, Kip Marina, Inverkip, Renfrewshire, PA16 0AS, UK

    John R. Foster

  2. Bayer SAS, 16 Rue Jean-Marie Leclair, 69009, Lyon, France

    Helen Tinwell

  3. BASF SE, APD/ET-Li 444, Speyerer Str. 2, 67117, Limburgerhof, Germany

    Stephanie Melching-Kollmuss

  4. Regulatory Science Associates, 1 Troutbeck Avenue, Congleton, CH, CW12 4JA, UK

    John R. Foster

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Foster, J.R., Tinwell, H. & Melching-Kollmuss, S. A review of species differences in the control of, and response to, chemical-induced thyroid hormone perturbations leading to thyroid cancer. Arch Toxicol 95, 807–836 (2021). https://doi.org/10.1007/s00204-020-02961-6

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