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Reciprocal Control of Thyroid Binding and the Pipecolate Pathway in the Brain

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An Erratum to this article was published on 16 March 2017

Abstract

Thyroid hormones have long been known to play an essential role in brain growth and development, with cytoplasmic thyroid hormone binding proteins (THBPs) playing a critical role in thyroid hormone bioavailability. A major mammalian THBP is μ-crystallin (CRYM), which was originally characterized by its ability to strongly bind thyroid hormones in an NADPH-dependent fashion. However, in 2011 it was discovered that CRYM is also an enzyme, namely ketimine reductase (KR), which catalyzes the NAD(P)H-dependent reduction of –C=N– (imine) double bonds of a number of cyclic ketimine substrates including sulfur-containing cyclic ketimines. The enzyme activity was also shown to be potently inhibited by thyroid hormones, thus suggesting a novel reciprocal relationship between enzyme catalysis and thyroid hormone bioavailability. KR is involved in a number of amino acid metabolic pathways. However, the best documented biological function of KR is its role as a ∆1-piperideine-2-carboxylate (P2C) reductase in the pipecolate pathway of lysine metabolism. The pipecolate pathway is the main l-lysine degradation pathway in the adult brain, whereas the saccharopine pathway predominates in extracerebral tissues and in infant brain, suggesting that KR has evolved to perform specific and important roles in neural development and function. The potent regulation of KR activity by thyroid hormones adds further weight to this suggestion. KR is also involved in l-ornithine/l-glutamate/l-proline metabolism as well as sulfur-containing amino acid metabolism. This review describes the pipecolate pathway and recent discoveries related to mammalian KR function, which have important implications in normal and pathological brain functions.

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Fig. 1
Fig. 2

Modified from [75]

Fig. 3
Fig. 4

Reproduced from [75] with permission

Fig. 5

From [75] with permission

Fig. 6

From [75] with permission

Fig. 7

From [75] with permission

Fig. 8

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Abbreviations

AAD:

α-Aminoadipate

AADT:

α-Aminoadipate transaminase (aminotransferase)

AAS:

α-Aminoadipate δ-semialdehyde

AASDH:

α-Aminoadipate δ-semialdehyde dehydrogenase

AECK:

Aminoethylcysteine ketimine

α-KG:

α-Ketoglutarate

AKA:

α-Ketoadipate

ALDH:

Aldehyde dehydrogenase

ALS:

Amyotrophic lateral sclerosis

CTBP:

Cytosolic thyroid hormone binding protein

CRYM:

μ-Crystallin

CysK:

Cystathionine ketimine

DAAO:

d-Amino acid oxidase

DTT:

Dithiothreitol

GAD:

Glutamate decarboxylase

GTL:

Glutamine transaminase L

KAC:

α-Keto-ε-aminocaproate

KATIII:

Kynurenine aminotransferase III

KR:

Ketimine reductase

Kyn:

l-Kynurenine

KynA:

Kynurenate

LK:

Lanthionine ketimine

IL4I1:

Interleukin-4–induced protein 1

LAAO:

l-Amino acid oxidase

LKR/SDH:

Lysine-α-ketoglutarate reductase/saccharopine dehydrogenase

P2C:

∆1-Piperideine-2-carboxylate

P6C:

∆1-Piperideine-6-carboxylate

PLP:

Pyridoxal 5′-phosphate

POX:

Pipecolate oxidase

Pyr2C:

∆1-Pyrroline-2-carboxylate

Pyr5C:

∆1-Pyrroline-5-carboxylate

rT3:

3,3′,5′-l-Triodothyronine; reverse T3

T2:

3,5-l-Diiodothyronine

3,3′-T2:

3,3′-l-Diiodothyronine

T3 :

3,5,3′-l-Triiodothyronine

T4 :

Thyroxine

T2C:

∆2-Thiazoline-2-carboxylate

THBP:

Thyroid binding protein

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Acknowledgments

Part of the cited work cited was supported Macquarie University Research Excellence Scholarship (to AH).

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  1. Department of Chemistry and Biomolecular Sciences, Macquarie University, Balaclava Road, North Ryde, Sydney, NSW, 2109, Australia

    André Hallen

  2. Department of Biochemistry and Molecular Biology, New York Medical College, Valhalla, New York, 10595, USA

    Arthur J. L. Cooper

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Special issue: in honor of Dr. Mary McKenna.

An erratum to this article is available at http://dx.doi.org/10.1007/s11064-017-2210-3.

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Hallen, A., Cooper, A.J.L. Reciprocal Control of Thyroid Binding and the Pipecolate Pathway in the Brain. Neurochem Res 42, 217–243 (2017). https://doi.org/10.1007/s11064-016-2015-9

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