Tryptophan regulates <i>Drosophila</i> zinc stores

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Significance

Zinc deficiency in the human population, a major public health concern, can also be a consequence of nutritional deficiency in protein uptake. The discovery that tryptophan metabolites 3-hydroxykynurenine and xanthurenic acid are major zinc-binding ligands in insect cells establishes the kynurenine pathway as a regulator of systemic zinc homeostasis. Many biological processes influenced by zinc and the kynurenine pathway, including the regulation of innate and acquired immune responses to viral infections, have not been studied in light of the direct molecular links revealed in this study.

Abstract

Zinc deficiency is commonly attributed to inadequate absorption of the metal. Instead, we show that body zinc stores in Drosophila melanogaster depend on tryptophan consumption. Hence, a dietary amino acid regulates zinc status of the whole insect—a finding consistent with the widespread requirement of zinc as a protein cofactor. Specifically, the tryptophan metabolite kynurenine is released from insect fat bodies and induces the formation of zinc storage granules in Malpighian tubules, where 3-hydroxykynurenine and xanthurenic acid act as endogenous zinc chelators. Kynurenine functions as a peripheral zinc-regulating hormone and is converted into a 3-hydroxykynurenine–zinc–chloride complex, precipitating within the storage granules. Thus, zinc and the kynurenine pathway—well-known modulators of immunity, blood pressure, aging, and neurodegeneration—are physiologically connected.

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Stefan Grimme, Jens Antony, Stephan Ehrlich … (2010)

The method of dispersion correction as an add-on to standard Kohn-Sham density functional theory (DFT-D) has been refined regarding higher accuracy, broader range of applicability, and less empiricism. The main new ingredients are atom-pairwise specific dispersion coefficients and cutoff radii that are both computed from first principles. The coefficients for new eighth-order dispersion terms are computed using established recursion relations. System (geometry) dependent information is used for the first time in a DFT-D type approach by employing the new concept of fractional coordination numbers (CN). They are used to interpolate between dispersion coefficients of atoms in different chemical environments. The method only requires adjustment of two global parameters for each density functional, is asymptotically exact for a gas of weakly interacting neutral atoms, and easily allows the computation of atomic forces. Three-body nonadditivity terms are considered. The method has been assessed on standard benchmark sets for inter- and intramolecular noncovalent interactions with a particular emphasis on a consistent description of light and heavy element systems. The mean absolute deviations for the S22 benchmark set of noncovalent interactions for 11 standard density functionals decrease by 15%-40% compared to the previous (already accurate) DFT-D version. Spectacular improvements are found for a tripeptide-folding model and all tested metallic systems. The rectification of the long-range behavior and the use of more accurate C(6) coefficients also lead to a much better description of large (infinite) systems as shown for graphene sheets and the adsorption of benzene on an Ag(111) surface. For graphene it is found that the inclusion of three-body terms substantially (by about 10%) weakens the interlayer binding. We propose the revised DFT-D method as a general tool for the computation of the dispersion energy in molecules and solids of any kind with DFT and related (low-cost) electronic structure methods for large systems.

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Author and article information

Journal

Journal ID (nlm-ta): Proc Natl Acad Sci U S A

Journal ID (iso-abbrev): Proc Natl Acad Sci U S A

Journal ID (hwp): pnas

Journal ID (publisher-id): PNAS

Title: Proceedings of the National Academy of Sciences of the United States of America

Publisher: National Academy of Sciences

ISSN (Print): 0027-8424

ISSN (Electronic): 1091-6490

Publication date (Electronic): 11 April 2022

Publication date (Print): 19 April 2022

Publication date PMC-release: 11 October 2022

Volume: 119

Issue: 16

Electronic Location Identifier: e2117807119

Affiliations

[1] ^aDepartment of Physiology, Biophysics and Neuroscience, Cinvestav , 07360 Mexico City, Mexico;

[2] ^bDepartment of Chemistry, Cinvestav , 07360 Mexico City, Mexico;

[3] ^cDepartment of Chemistry, University of Bari Aldo Moro , 70125 Bari, Italy;

[4] ^dPaul Scherrer Institute , CH-5232 Villigen, Switzerland;

[5] ^eDepartment of Physics, Freie Universität Berlin , 14195 Berlin, Germany

Author notes

²To whom correspondence may be addressed. Email: fabio.arnesano@ 123456uniba.it , lilianaq@ 123456cinvestav.mx , or fanis@ 123456fisio.cinvestav.mx .

Edited by Amy Rosenzweig, Northwestern University, Evanston, IL; received September 29, 2021; accepted March 3, 2022

Author contributions: E.G., N.S., A.B., C.T.-G., A.V., F.A., L.Q., and F.M. designed research; E.G., N.S., A.B., C.T.-G., D.V., B.O., A.H.C., M.N., A.V., L.Q., and F.M. performed research; E.G., N.S., A.B., C.T.-G., D.V., A.H.C., M.N., M.H., H.D., A.V., F.A., L.Q., and F.M. analyzed data; and E.G., N.S., A.B., A.V., F.A., L.Q., and F.M. wrote the paper.

¹E.G. and N.S. contributed equally to this work.