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Title: Biogenesis of zinc storage granules in Drosophila melanogaster

Abstract

Membrane transporters and sequestration mechanisms concentrate metal ions differentially into discrete subcellular microenvironments for use in protein cofactors, signalling, storage or excretion. Here we identify zinc storage granules as the insect's major zinc reservoir in principal Malpighian tubule epithelial cells of Drosophila melanogaster. The concerted action of Adaptor Protein-3, Rab32, HOPS and BLOC complexes as well as of the white-scarlet (ABCG2-like) and ZnT35C (ZnT2/ZnT3/ZnT8-like) transporters is required for zinc storage granule biogenesis. Due to lysosome-related organelle defects caused by mutations in the homologous human genes, patients with Hermansky–Pudlak syndrome may lack zinc granules in beta pancreatic cells, intestinal paneth cells and presynaptic vesicles of hippocampal mossy fibers.

Authors:
; ORCiD logo; ; ; ; ; ORCiD logo
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1418066
Alternate Identifier(s):
OSTI ID: 1468689
Grant/Contract Number:  
AC02-76SF00515; P41GM103393
Resource Type:
Published Article
Journal Name:
Journal of Experimental Biology
Additional Journal Information:
Journal Name: Journal of Experimental Biology Journal Volume: 221 Journal Issue: 6; Journal ID: ISSN 0022-0949
Publisher:
The Company of Biologists
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; AP-3 complex; Eye color mutants; ICP-OES; Malpighian tubules; Synchrotron; Zincosomes

Citation Formats

Tejeda-Guzmán, Carlos, Rosas-Arellano, Abraham, Kroll, Thomas, Webb, Samuel M., Barajas-Aceves, Martha, Osorio, Beatriz, and Missirlis, Fanis. Biogenesis of zinc storage granules in Drosophila melanogaster. United Kingdom: N. p., 2018. Web. doi:10.1242/jeb.168419.
Tejeda-Guzmán, Carlos, Rosas-Arellano, Abraham, Kroll, Thomas, Webb, Samuel M., Barajas-Aceves, Martha, Osorio, Beatriz, & Missirlis, Fanis. Biogenesis of zinc storage granules in Drosophila melanogaster. United Kingdom. doi:10.1242/jeb.168419.
Tejeda-Guzmán, Carlos, Rosas-Arellano, Abraham, Kroll, Thomas, Webb, Samuel M., Barajas-Aceves, Martha, Osorio, Beatriz, and Missirlis, Fanis. Wed . "Biogenesis of zinc storage granules in Drosophila melanogaster". United Kingdom. doi:10.1242/jeb.168419.
@article{osti_1418066,
title = {Biogenesis of zinc storage granules in Drosophila melanogaster},
author = {Tejeda-Guzmán, Carlos and Rosas-Arellano, Abraham and Kroll, Thomas and Webb, Samuel M. and Barajas-Aceves, Martha and Osorio, Beatriz and Missirlis, Fanis},
abstractNote = {Membrane transporters and sequestration mechanisms concentrate metal ions differentially into discrete subcellular microenvironments for use in protein cofactors, signalling, storage or excretion. Here we identify zinc storage granules as the insect's major zinc reservoir in principal Malpighian tubule epithelial cells of Drosophila melanogaster. The concerted action of Adaptor Protein-3, Rab32, HOPS and BLOC complexes as well as of the white-scarlet (ABCG2-like) and ZnT35C (ZnT2/ZnT3/ZnT8-like) transporters is required for zinc storage granule biogenesis. Due to lysosome-related organelle defects caused by mutations in the homologous human genes, patients with Hermansky–Pudlak syndrome may lack zinc granules in beta pancreatic cells, intestinal paneth cells and presynaptic vesicles of hippocampal mossy fibers.},
doi = {10.1242/jeb.168419},
journal = {Journal of Experimental Biology},
number = 6,
volume = 221,
place = {United Kingdom},
year = {2018},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1242/jeb.168419

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Cited by: 4 works
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Works referenced in this record:

Genetic modifiers of abnormal organelle biogenesis in a Drosophila model of BLOC-1 deficiency
journal, December 2009

  • Cheli, Verónica T.; Daniels, Richard W.; Godoy, Ruth
  • Human Molecular Genetics, Vol. 19, Issue 5
  • DOI: 10.1093/hmg/ddp555

The multidrug transporter ABCG2: still more questions than answers
journal, June 2016

  • Horsey, Aaron J.; Cox, Megan H.; Sarwat, Sunehera
  • Biochemical Society Transactions, Vol. 44, Issue 3
  • DOI: 10.1042/BST20160014

Defective expression of the μ3 subunit of the AP-3 adaptor complex in the Drosophila pigmentation mutant carmine
journal, November 1999

  • Mullins, C.; Hartnell, L. M.; Wassarman, D. A.
  • Molecular and General Genetics MGG, Vol. 262, Issue 3
  • DOI: 10.1007/s004380051099

Zur Histochemie der Langerhansschen Inseln
journal, August 1958


Metal-metal interaction mediates the iron induction of Drosophila MtnB
journal, June 2017

  • Qiang, Wenjia; Huang, Yunpeng; Wan, Zhihui
  • Biochemical and Biophysical Research Communications, Vol. 487, Issue 3
  • DOI: 10.1016/j.bbrc.2017.04.109

The light gene of Drosophila melanogaster encodes a homologue of VPS41 , a yeast gene involved in cellular-protein trafficking
journal, April 1998

  • Warner, T. S.; Sinclair, Dar; Fitzpatrick, K. A.
  • Genome, Vol. 41, Issue 2
  • DOI: 10.1139/g98-017

Drosophila eye color mutants as therapeutic tools for Huntington disease
journal, April 2012

  • Green, Edward W.; Campesan, Susanna; Breda, Carlo
  • Fly, Vol. 6, Issue 2
  • DOI: 10.4161/fly.19999

Multidrug Transporter ABCG2/Breast Cancer Resistance Protein Secretes Riboflavin (Vitamin B2) into Milk
journal, December 2006

  • van Herwaarden, A. E.; Wagenaar, E.; Merino, G.
  • Molecular and Cellular Biology, Vol. 27, Issue 4
  • DOI: 10.1128/MCB.01621-06

Lysosome-Related Organelles in Intestinal Cells Are a Zinc Storage Site in C. elegans
journal, January 2012


Purine transport by Malpighian tubules of pteridine-deficient eye color mutants of Drosophila melanogaster
journal, June 1979

  • Sullivan, David T.; Bell, L. Anne; Paton, Duncan R.
  • Biochemical Genetics, Vol. 17, Issue 5-6
  • DOI: 10.1007/BF00498891

Znt7 ( Slc30a7 )-deficient Mice Display Reduced Body Zinc Status and Body Fat Accumulation
journal, October 2007

  • Huang, Liping; Yu, Yan Yiu; Kirschke, Catherine P.
  • Journal of Biological Chemistry, Vol. 282, Issue 51
  • DOI: 10.1074/jbc.M706631200

Biophysical and genetic analysis of iron partitioning and ferritin function in Drosophila melanogaster
journal, January 2013

  • Gutiérrez, Lucía; Zubow, Kristina; Nield, Jon
  • Metallomics, Vol. 5, Issue 8
  • DOI: 10.1039/c3mt00118k

The zinc sensing receptor, ZnR/GPR39, triggers metabotropic calcium signalling in colonocytes and regulates occludin recovery in experimental colitis
journal, August 2016

  • Sunuwar, Laxmi; Medini, Michal; Cohen, Limor
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 371, Issue 1700
  • DOI: 10.1098/rstb.2015.0420

The metal transporter ZIP13 supplies iron into the secretory pathway in Drosophila melanogaster
journal, July 2014


Development of Eye Colors in Drosophila: Fat Bodies and Malpighian Tubes as Sources of Diffusible Substances
journal, March 1937

  • Beadle, G. W.
  • Proceedings of the National Academy of Sciences, Vol. 23, Issue 3
  • DOI: 10.1073/pnas.23.3.146

The Manganese Superoxide Dismutase Gene of Drosophila : Structure, Expression, and Evidence for Regulation by MAP Kinase
journal, April 1997


Copper and Zinc Homeostasis: Lessons from Drosophila melanogaster
journal, December 2017


Ferritin Assembly in Enterocytes of Drosophila melanogaster
journal, February 2016

  • Rosas-Arellano, Abraham; Vásquez-Procopio, Johana; Gambis, Alexis
  • International Journal of Molecular Sciences, Vol. 17, Issue 2
  • DOI: 10.3390/ijms17020027

Transport defects as the physiological basis for eye color mutants of Drosophila melanogaster
journal, October 1975

  • Sullivan, David T.; Sullivan, Marie C.
  • Biochemical Genetics, Vol. 13, Issue 9-10
  • DOI: 10.1007/BF00484918

Molybdenum hydroxylases in Drosophila: II. Molybdenum cofactor in xanthine dehydrogenase, aldehyde oxidase and pyridoxal oxidase
journal, January 1981

  • Warner, Cynthia K.; Finnerty, Victoria
  • MGG Molecular & General Genetics, Vol. 184, Issue 1
  • DOI: 10.1007/BF00271201

Resonant Inelastic X-ray Scattering on Ferrous and Ferric Bis-imidazole Porphyrin and Cytochrome c : Nature and Role of the Axial Methionine–Fe Bond
journal, December 2014

  • Kroll, Thomas; Hadt, Ryan G.; Wilson, Samuel A.
  • Journal of the American Chemical Society, Vol. 136, Issue 52
  • DOI: 10.1021/ja5100367

Zinc transporter 2 interacts with vacuolar ATPase and is required for polarization, vesicle acidification, and secretion in mammary epithelial cells
journal, November 2017

  • Lee, Sooyeon; Rivera, Olivia C.; Kelleher, Shannon L.
  • Journal of Biological Chemistry, Vol. 292, Issue 52
  • DOI: 10.1074/jbc.M117.794461

RNAi-mediated suppression of the mitochondrial iron chaperone, frataxin, in Drosophila
journal, October 2005

  • Anderson, Peter R.; Kirby, Kim; Hilliker, Arthur J.
  • Human Molecular Genetics, Vol. 14, Issue 22
  • DOI: 10.1093/hmg/ddi367

Deletion of the mouse Slc30a8 gene encoding zinc transporter-8 results in impaired insulin secretion
journal, July 2009

  • Pound, Lynley D.; Sarkar, Suparna A.; Benninger, Richard K. P.
  • Biochemical Journal, Vol. 421, Issue 3
  • DOI: 10.1042/BJ20090530

Differential riboflavin deposition inwhite and variegatedwhite mutants ofDrosophila hydei
journal, January 1987


Functional studies of Drosophila zinc transporters reveal the mechanism for dietary zinc absorption and regulation
journal, January 2013


Iron regulatory proteins and their role in controlling iron metabolism
journal, January 2015


What can flies tell us about copper homeostasis?
journal, January 2013

  • Southon, Adam; Burke, Richard; Camakaris, James
  • Metallomics, Vol. 5, Issue 10
  • DOI: 10.1039/c3mt00105a

Mammalian metallothioneins: properties and functions
journal, January 2012

  • Babula, Petr; Masarik, Michal; Adam, Vojtech
  • Metallomics, Vol. 4, Issue 8
  • DOI: 10.1039/c2mt20081c

Moving and positioning the endolysosomal system
journal, August 2017


ZnT-1 extrudes zinc from mammalian cells functioning as a Zn 2+ /H + exchanger
journal, January 2014

  • Shusterman, Eden; Beharier, Ofer; Shiri, Levy
  • Metallomics, Vol. 6, Issue 9
  • DOI: 10.1039/C4MT00108G

The Drosophila Pigmentation Gene pink (p) Encodes a Homologue of Human Hermansky-Pudlak Syndrome 5 (HPS5)
journal, November 2006


The four aldehyde oxidases of Drosophila melanogaster have different gene expression patterns and enzyme substrate specificities
journal, April 2014

  • Marelja, Z.; Dambowsky, M.; Bolis, M.
  • Journal of Experimental Biology, Vol. 217, Issue 12
  • DOI: 10.1242/jeb.102129

Genes for iron metabolism influence circadian rhythms in Drosophila melanogaster
journal, January 2012

  • Mandilaras, Konstantinos; Missirlis, Fanis
  • Metallomics, Vol. 4, Issue 9
  • DOI: 10.1039/c2mt20065a

Synchrotron X-ray Fluorescence Reveals Abnormal Metal Distributions in Brain and Spinal Cord in Spinocerebellar Ataxia: A Case Report
journal, March 2009

  • Popescu, Bogdan F. Gh.; Robinson, Christopher A.; Chapman, L. Dean
  • The Cerebellum, Vol. 8, Issue 3
  • DOI: 10.1007/s12311-009-0102-z

Huntington disease arises from a combinatory toxicity of polyglutamine and copper binding
journal, August 2013

  • Xiao, G.; Fan, Q.; Wang, X.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 37
  • DOI: 10.1073/pnas.1308535110

Role of gut microbiota in aging-related health decline: insights from invertebrate models
journal, October 2017


The physiological functions of iron regulatory proteins in iron homeostasis - an update
journal, June 2014


Microbial influence on Drosophila biology
journal, August 2017


Distinct requirements for the AP-3 adaptor complex in pigment granule and synaptic vesicle biogenesis in Drosophila melanogaster
journal, August 2000

  • Mullins, C.; Hartnell, L. M.; Bonifacino, J. S.
  • MGG - Molecular and General Genetics, Vol. 263, Issue 6
  • DOI: 10.1007/PL00008688

Influence of the White Locus on the Courtship Behavior of Drosophila Males
journal, October 2013


Mutations in AP3D1 associated with immunodeficiency and seizures define a new type of Hermansky-Pudlak syndrome
journal, February 2016


Mitochondrial iron supply is required for the developmental pulse of ecdysone biosynthesis that initiates metamorphosis in Drosophila melanogaster
journal, October 2015

  • Llorens, Jose V.; Metzendorf, Christoph; Missirlis, Fanis
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 20, Issue 8
  • DOI: 10.1007/s00775-015-1302-2

The essential roles of metal ions in insect homeostasis and physiology
journal, October 2017


Genetic Diversity in Insect Metal Tolerance
journal, November 2017


Interstitial Lung Disease and Pulmonary Fibrosis in Hermansky-Pudlak Syndrome Type 2, an Adaptor Protein-3 Complex Disease
journal, October 2011

  • Gochuico, Bernadette R.; Huizing, Marjan; Golas, Gretchen A.
  • Molecular Medicine, Vol. 18, Issue 1
  • DOI: 10.2119/molmed.2011.00198

The pigment granules in the compound eyes of Drosophila
journal, February 1961


Ironing out Ferroportin
journal, November 2015


Molecular structure of human KATP in complex with ATP and ADP
journal, December 2017


cGMP transport by vesicles from human and mouse erythrocytes: cGMP transport by erythrocytes
journal, December 2006


A new role for a classical gene: White transports cyclic GMP
journal, March 2008

  • Evans, J. M.; Day, J. P.; Cabrero, P.
  • Journal of Experimental Biology, Vol. 211, Issue 6
  • DOI: 10.1242/jeb.014837

Zinc Transporter SLC39A7/ZIP7 Promotes Intestinal Epithelial Self-Renewal by Resolving ER Stress
journal, October 2016


Hypopigmentation in Hermansky-Pudlak syndrome
journal, May 2013


3D imaging of transition metals in the zebrafish embryo by X-ray fluorescence microtomography
journal, January 2014

  • Bourassa, Daisy; Gleber, Sophie-Charlotte; Vogt, Stefan
  • Metallomics, Vol. 6, Issue 9
  • DOI: 10.1039/C4MT00121D

Effect of Tryptophan Metabolites on Fluorescent Granules in the Malpighian Tubules of Eye Color Mutants of Drosophila melanogaster
journal, February 1996

  • Yagi, Shizuo; Ogawa, Hisamitsu
  • Zoological Science, Vol. 13, Issue 1
  • DOI: 10.2108/zsj.13.97

Epithelial septate junction assembly relies on melanotransferrin iron binding and endocytosis in Drosophila
journal, October 2010

  • Tiklová, Katarína; Senti, Kirsten-André; Wang, Shenqiu
  • Nature Cell Biology, Vol. 12, Issue 11
  • DOI: 10.1038/ncb2111

Inhibition of the PI3K-Akt signaling pathway disrupts ABCG2-rich extracellular vesicles and overcomes multidrug resistance in breast cancer cells
journal, May 2012

  • Goler-Baron, Vicky; Sladkevich, Irina; Assaraf, Yehuda G.
  • Biochemical Pharmacology, Vol. 83, Issue 10
  • DOI: 10.1016/j.bcp.2012.01.033

BLOC-3 Mutated in Hermansky-Pudlak Syndrome Is a Rab32/38 Guanine Nucleotide Exchange Factor
journal, November 2012


The Zn 2+ -sensing receptor, ZnR/GPR39, upregulates colonocytic Cl − absorption, via basolateral KCC1, and reduces fluid loss
journal, April 2017

  • Sunuwar, Laxmi; Asraf, Hila; Donowitz, Mark
  • Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1863, Issue 4
  • DOI: 10.1016/j.bbadis.2017.01.009

The pink gene encodes the Drosophila orthologue of the human Hermansky–Pudlak syndrome 5 ( HPS5 ) gene
journal, June 2007

  • Syrzycka, Monika; McEachern, Lori A.; Kinneard, Jennifer
  • Genome, Vol. 50, Issue 6
  • DOI: 10.1139/G07-032

A recessive X-linked mutation causes a threefold reduction of total body zinc accumulation in Drosophila melanogaster laboratory strains
journal, January 2013


Not just pretty eyes: Drosophila eye-colour mutations and lysosomal delivery
journal, December 1998


Dietary zinc absorption is mediated by ZnT1 in Drosophila melanogaster
journal, August 2009

  • Wang, Xiaoxi; Wu, Yuantai; Zhou, Bing
  • The FASEB Journal, Vol. 23, Issue 8
  • DOI: 10.1096/fj.08-126649

A genetic toolkit for tagging intronic MiMIC containing genes
journal, June 2015

  • Nagarkar-Jaiswal, Sonal; DeLuca, Steven Z.; Lee, Pei-Tseng
  • eLife, Vol. 4
  • DOI: 10.7554/eLife.08469

Autosomal-Recessive Mutations in AP3B2 , Adaptor-Related Protein Complex 3 Beta 2 Subunit, Cause an Early-Onset Epileptic Encephalopathy with Optic Atrophy
journal, December 2016

  • Assoum, Mirna; Philippe, Christophe; Isidor, Bertrand
  • The American Journal of Human Genetics, Vol. 99, Issue 6
  • DOI: 10.1016/j.ajhg.2016.10.009

Aconitase Causes Iron Toxicity in Drosophila pink1 Mutants
journal, April 2013


Cargo sorting to lysosome-related organelles regulates siRNA-mediated gene silencing
journal, July 2011

  • Harris, Dinari A.; Kim, Kevin; Nakahara, Kenji
  • The Journal of Cell Biology, Vol. 194, Issue 1
  • DOI: 10.1083/jcb.201102021

Molecular mechanism and functional significance of acid generation in the Drosophila midgut
journal, June 2016

  • Overend, Gayle; Luo, Yuan; Henderson, Louise
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep27242

Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene
journal, February 1999

  • Cole, T. B.; Wenzel, H. J.; Kafer, K. E.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 4
  • DOI: 10.1073/pnas.96.4.1716

The induction and distribution of an insect ferritin — A new function for the endoplasmic reticulum
journal, January 1984


Evidence for Metabolic Provisioning by a Common Invertebrate Endosymbiont, Wolbachia pipientis, during Periods of Nutritional Stress
journal, April 2009


Intracellular zinc in insulin secretion and action: a determinant of diabetes risk?
journal, September 2015

  • Rutter, Guy A.; Chabosseau, Pauline; Bellomo, Elisa A.
  • Proceedings of the Nutrition Society, Vol. 75, Issue 1
  • DOI: 10.1017/S0029665115003237

A Family Knockout of All Four Drosophila Metallothioneins Reveals a Central Role in Copper Homeostasis and Detoxification
journal, February 2006


Lysosome-related organelles
journal, July 2000


Drosophila Mitf regulates the V-ATPase and the lysosomal-autophagic pathway
journal, January 2016


Biosynthesis of drosopterins, the red eye pigments of Drosophila melanogaster
journal, February 2013

  • Kim, Heuijong; Kim, Kiyoung; Yim, Jeongbin
  • IUBMB Life, Vol. 65, Issue 4
  • DOI: 10.1002/iub.1145

Cellular sensing and transport of metal ions: implications in micronutrient homeostasis
journal, November 2015


Identification of the Zn 2+ Binding Site and Mode of Operation of a Mammalian Zn 2+ Transporter
journal, April 2009

  • Ohana, Ehud; Hoch, Eitan; Keasar, Chen
  • Journal of Biological Chemistry, Vol. 284, Issue 26
  • DOI: 10.1074/jbc.M109.007203

Red flag on the white reporter: a versatile insulator abuts the white gene in Drosophila and is omnipresent in mini-white constructs
journal, December 2007

  • Chetverina, Darya; Savitskaya, Ekaterina; Maksimenko, Oksana
  • Nucleic Acids Research, Vol. 36, Issue 3
  • DOI: 10.1093/nar/gkm992

Exploring interactions between pathogens and the Drosophila gut
journal, November 2016

  • Mistry, Rupal; Kounatidis, Ilias; Ligoxygakis, Petros
  • Developmental & Comparative Immunology, Vol. 64
  • DOI: 10.1016/j.dci.2016.01.016

Iron depletion in the intestines of Malvolio mutant flies does not occur in the absence of a multicopper oxidase
journal, February 2011

  • Bettedi, L.; Aslam, M. F.; Szular, J.
  • Journal of Experimental Biology, Vol. 214, Issue 6
  • DOI: 10.1242/jeb.051664

A role for dZIP89B in Drosophila dietary zinc uptake reveals additional complexity in the zinc absorption process
journal, December 2015

  • Richards, Christopher D.; Warr, Coral G.; Burke, Richard
  • The International Journal of Biochemistry & Cell Biology, Vol. 69
  • DOI: 10.1016/j.biocel.2015.10.004

Zinc in Pancreatic Islet Biology, Insulin Sensitivity, and Diabetes
journal, March 2017


Zinc accumulation in heterozygous mutants of fumble , the pantothenate kinase homologue of Drosophila
journal, May 2010


A Red Carpet for Iron Metabolism
journal, January 2017


Compartmentalized zinc deficiency and toxicities caused by ZnT and Zip gene over expression result in specific phenotypes in Drosophila
journal, March 2015

  • Dechen, Kesang; Richards, Christopher D.; Lye, Jessica C.
  • The International Journal of Biochemistry & Cell Biology, Vol. 60
  • DOI: 10.1016/j.biocel.2014.12.017

BLOC-2, AP-3, and AP-1 Proteins Function in Concert with Rab38 and Rab32 Proteins to Mediate Protein Trafficking to Lysosome-related Organelles
journal, April 2012

  • Bultema, Jarred J.; Ambrosio, Andrea L.; Burek, Carolyn L.
  • Journal of Biological Chemistry, Vol. 287, Issue 23
  • DOI: 10.1074/jbc.M112.351908

The Nuclear Receptor HIZR-1 Uses Zinc as a Ligand to Mediate Homeostasis in Response to High Zinc
journal, January 2017


Iron homeostasis in insects: Insights from Drosophila studies : Iron Homeostasis in Insects
journal, September 2013


Iron is a specific cofactor for distinct oxidation- and aggregation-dependent A  toxicity mechanisms in a Drosophila model
journal, April 2015

  • Ott, S.; Dziadulewicz, N.; Crowther, D. C.
  • Disease Models & Mechanisms, Vol. 8, Issue 7
  • DOI: 10.1242/dmm.019042

Instability of Superoxide Dismutase 1 of Drosophila in Mutants Deficient for Its Cognate Copper Chaperone
journal, October 2008

  • Kirby, Kim; Jensen, Laran T.; Binnington, Janet
  • Journal of Biological Chemistry, Vol. 283, Issue 51
  • DOI: 10.1074/jbc.M807131200

INTERACTION BETWEEN PTERIDINE SYNTHESIS AND RIBOFLAVIN ACCUMULATION IN DROSOPHILA MELANOGASTER
journal, March 1972

  • Nickla, Harry
  • Canadian Journal of Genetics and Cytology, Vol. 14, Issue 1
  • DOI: 10.1139/g72-013

Evidence for evolutionary constraints in Drosophila metal biology
journal, February 2011


Understanding the Contribution of Zinc Transporters in the Function of the Early Secretory Pathway
journal, October 2017

  • Kambe, Taiho; Matsunaga, Mayu; Takeda, Taka-aki
  • International Journal of Molecular Sciences, Vol. 18, Issue 10
  • DOI: 10.3390/ijms18102179

In vivo zinc toxicity phenotypes provide a sensitized background that suggests zinc transport activities for most of the Drosophila Zip and ZnT genes
journal, January 2013

  • Lye, Jessica C.; Richards, Christopher D.; Dechen, Kesang
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 18, Issue 3
  • DOI: 10.1007/s00775-013-0976-6

Single nucleotide in the MTF-1 binding site can determine metal-specific transcription activation
journal, September 2012

  • Sims, H. I.; Chirn, G. -W.; Marr, M. T.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 41
  • DOI: 10.1073/pnas.1207737109

Zinc-secreting Paneth Cells Studied by ZP Fluorescence
journal, March 2006

  • Giblin, Leonard J.; Chang, Christopher J.; Bentley, Anthony F.
  • Journal of Histochemistry & Cytochemistry, Vol. 54, Issue 3
  • DOI: 10.1369/jhc.5A6724.2005

AP-3-dependent trafficking and disease: the first decade
journal, August 2009


Effect of Kynurenic Acid on Development and Aging in Wild Type and Vermilion Mutants of Drosophila Melanogaster
journal, January 2016

  • Navrotskaya, Valeriya; Oxenkrug, Gregory
  • Pharmacology, Drug Development & Therapeutics, Vol. 1, Issue 1
  • DOI: 10.15761/PDDT.1000104

Conserved metallomics in two insect families evolving separately for a hundred million years
journal, October 2014


Multiple upstream regulatory elements control the expression of the Drosophila white gene.
journal, December 1985


Balancing Acts
journal, April 2004


A fly's eye view of zinc homeostasis: Novel insights into the genetic control of zinc metabolism from Drosophila
journal, December 2016


Iron Absorption in Drosophila melanogaster
journal, May 2013

  • Mandilaras, Konstantinos; Pathmanathan, Tharse; Missirlis, Fanis
  • Nutrients, Vol. 5, Issue 5
  • DOI: 10.3390/nu5051622

Drosophila melanogaster Models of Metal-Related Human Diseases and Metal Toxicity
journal, July 2017

  • Calap-Quintana, Pablo; González-Fernández, Javier; Sebastiá-Ortega, Noelia
  • International Journal of Molecular Sciences, Vol. 18, Issue 7
  • DOI: 10.3390/ijms18071456

Transcriptome response to heavy metal stress in Drosophila reveals a new zinc transporter that confers resistance to zinc
journal, September 2006

  • Yepiskoposyan, Hasmik; Egli, Dieter; Fergestad, Tim
  • Nucleic Acids Research, Vol. 34, Issue 17
  • DOI: 10.1093/nar/gkl606

Structure and Function of ABCG2-Rich Extracellular Vesicles Mediating Multidrug Resistance
journal, January 2011


Sorting Out Signals in Fly Endosomes: Sorting Out Signals in Fly Endosomes
journal, January 2002


Functional studies of Drosophila zinc transporters reveal the mechanism for zinc excretion in Malpighian tubules
journal, February 2017


ZnT2-Mediated Zinc Import Into Paneth Cell Granules Is Necessary for Coordinated Secretion and Paneth Cell Function in Mice
journal, May 2016

  • Podany, Abigail B.; Wright, Justin; Lamendella, Regina
  • Cellular and Molecular Gastroenterology and Hepatology, Vol. 2, Issue 3
  • DOI: 10.1016/j.jcmgh.2015.12.006

Terminal synthesis of xanthommatin in drosophila melanogaster. IV. Enzymatic and nonenzymatic catalysis
journal, December 1981

  • Wiley, Kathy; Forrest, H. S.
  • Biochemical Genetics, Vol. 19, Issue 11-12
  • DOI: 10.1007/BF00484574

The Insulin and the zinc Content of Normal and Diabetic Pancreas
journal, November 1938

  • Scott, D. A.; Fisher, A. M.
  • Journal of Clinical Investigation, Vol. 17, Issue 6
  • DOI: 10.1172/JCI101000

A Distinctive and Host-Restricted Gut Microbiota in Populations of a Cactophilic Drosophila Species
journal, September 2017

  • Martinson, Vincent G.; Carpinteyro-Ponce, Javier; Moran, Nancy A.
  • Applied and Environmental Microbiology, Vol. 83, Issue 23
  • DOI: 10.1128/AEM.01551-17

Drosophila Arginase Is Produced from a Nonvital Gene That Contains the elav Locus within Its Third Intron
journal, June 2000


The brown protein of Drosophila melanogaster is similar to the white protein and to components of active transport complexes.
journal, December 1988

  • Dreesen, T. D.; Johnson, D. H.; Henikoff, S.
  • Molecular and Cellular Biology, Vol. 8, Issue 12
  • DOI: 10.1128/MCB.8.12.5206

Dm1 -MMP, a Matrix Metalloproteinase from Drosophila with a Potential Role in Extracellular Matrix Remodeling during Neural Development
journal, August 2000

  • Llano, Elena; Pendás, Alberto M.; Aza-Blanc, Pedro
  • Journal of Biological Chemistry, Vol. 275, Issue 46
  • DOI: 10.1074/jbc.M006045200

Localizing organomercury uptake and accumulation in zebrafish larvae at the tissue and cellular level
journal, August 2008

  • Korbas, M.; Blechinger, S. R.; Krone, P. H.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 34
  • DOI: 10.1073/pnas.0803147105

Protein trafficking abnormalities in Drosophila tissues with impaired activity of the ZIP7 zinc transporter Catsup
journal, June 2013

  • Groth, C.; Sasamura, T.; Khanna, M. R.
  • Development, Vol. 140, Issue 14
  • DOI: 10.1242/dev.088336

Disruption of a putative Cys–zinc interaction eliminates the biological activity of the Krüppel finger protein
journal, March 1988

  • Redemann, Norbert; Gaul, Ulrike; Jäckle, Herbert
  • Nature, Vol. 332, Issue 6159
  • DOI: 10.1038/332090a0

The mutual control of iron and erythropoiesis
journal, May 2016

  • Camaschella, C.; Pagani, A.; Nai, A.
  • International Journal of Laboratory Hematology, Vol. 38
  • DOI: 10.1111/ijlh.12505

The Development of Pigment Granules in the eyes of wild type and Mutant Drosophila Melanogaster
journal, May 1966


The SLC39 family of zinc transporters
journal, April 2013


Characterization of MtnE, the fifth metallothionein member in Drosophila
journal, August 2011

  • Atanesyan, Lilit; Günther, Viola; Celniker, Susan E.
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 16, Issue 7
  • DOI: 10.1007/s00775-011-0825-4

Bombyx ortholog of the Drosophila eye color gene brown controls riboflavin transport in Malpighian tubules
journal, January 2018

  • Zhang, Haokun; Kiuchi, Takashi; Hirayama, Chikara
  • Insect Biochemistry and Molecular Biology, Vol. 92
  • DOI: 10.1016/j.ibmb.2017.11.012

Contrasting Influences of Drosophila white/mini-white on Ethanol Sensitivity in Two Different Behavioral Assays
journal, May 2014

  • Chan, Robin F.; Lewellyn, Lara; DeLoyht, Jacqueline M.
  • Alcoholism: Clinical and Experimental Research, Vol. 38, Issue 6
  • DOI: 10.1111/acer.12421

Elemental mapping of the entire intact Drosophila gastrointestinal tract
journal, July 2015

  • Jones, Michael W. M.; de Jonge, Martin D.; James, Simon A.
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 20, Issue 6
  • DOI: 10.1007/s00775-015-1281-3

What can flies tell us about zinc homeostasis?
journal, December 2016


Ferritin accumulation under iron scarcity in Drosophila iron cells
journal, October 2009


The zinc sensing receptor ZnR GPR39 in health and disease
journal, January 2017

  • Hershfinkel, Michal
  • Frontiers in Bioscience, Vol. 22, Issue 9
  • DOI: 10.2741/4554

A Drosophila Model Identifies a Critical Role for Zinc in Mineralization for Kidney Stone Disease
journal, May 2015


Ferritin Is Required in Multiple Tissues during Drosophila melanogaster Development
journal, July 2015


Tissue-specific interplay between copper uptake and efflux in Drosophila
journal, February 2010

  • Binks, Tim; Lye, Jessica Charlotte; Camakaris, James
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 15, Issue 4
  • DOI: 10.1007/s00775-010-0629-y

The taste of heavy metals: Gene regulation by MTF-1
journal, September 2012

  • Günther, Viola; Lindert, Uschi; Schaffner, Walter
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1823, Issue 9
  • DOI: 10.1016/j.bbamcr.2012.01.005

A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac
journal, February 2004

  • Thibault, Stephen T.; Singer, Matthew A.; Miyazaki, Wesley Y.
  • Nature Genetics, Vol. 36, Issue 3
  • DOI: 10.1038/ng1314

In Vivo Modeling of the Pathogenic Effect of Copper Transporter Mutations That Cause Menkes and Wilson Diseases, Motor Neuropathy, and Susceptibility to Alzheimer's Disease
journal, January 2017

  • Mercer, Stephen W.; Wang, Jianbin; Burke, Richard
  • Journal of Biological Chemistry, Vol. 292, Issue 10
  • DOI: 10.1074/jbc.M116.756163

The MicroAnalysis Toolkit: X-ray Fluorescence Image Processing Software
conference, January 2011

  • Webb, S. M.; McNulty, Ian; Eyberger, Catherine
  • THE 10TH INTERNATIONAL CONFERENCE ON X-RAY MICROSCOPY, AIP Conference Proceedings
  • DOI: 10.1063/1.3625338

The Zinc Transporter ZnT3 Interacts with AP-3 and It Is Preferentially Targeted to a Distinct Synaptic Vesicle Subpopulation
journal, February 2004

  • Salazar, Gloria; Love, Rachal; Werner, Erica
  • Molecular Biology of the Cell, Vol. 15, Issue 2
  • DOI: 10.1091/mbc.E03-06-0401

Sex Limited Inheritance in Drosophila
journal, July 1910


Volatile general anesthetics reveal a neurobiological role for thewhite andbrown genes ofDrosophila melanogaster
journal, January 2001

  • Campbell, Joseph L.; Nash, Howard A.
  • Journal of Neurobiology, Vol. 49, Issue 4
  • DOI: 10.1002/neu.10009

From pathogens to microbiota: How Drosophila intestinal stem cells react to gut microbes
journal, November 2016

  • Bonfini, Alessandro; Liu, Xi; Buchon, Nicolas
  • Developmental & Comparative Immunology, Vol. 64
  • DOI: 10.1016/j.dci.2016.02.008

The Functions of Metallothionein and ZIP and ZnT Transporters: An Overview and Perspective
journal, March 2016

  • Kimura, Tomoki; Kambe, Taiho
  • International Journal of Molecular Sciences, Vol. 17, Issue 3
  • DOI: 10.3390/ijms17030336

Drosophila ABC transporter mutants white, brown and scarlet have altered contents and distribution of biogenic amines in the brain
journal, November 2008

  • Borycz, J.; Borycz, J. A.; Kubow, A.
  • Journal of Experimental Biology, Vol. 211, Issue 21
  • DOI: 10.1242/jeb.021162

Drosophila melanogaster White Mutant w1118 Undergo Retinal Degeneration
journal, January 2018

  • Ferreiro, María José; Pérez, Coralia; Marchesano, Mariana
  • Frontiers in Neuroscience, Vol. 11
  • DOI: 10.3389/fnins.2017.00732

Zinc transporter 3 (ZnT3) and vesicular zinc in central nervous system function
journal, September 2017


Studies in Biochemical Genetics in Drosophila
journal, March 1948


Frataxin inactivation leads to steroid deficiency in flies and human ovarian cells
journal, January 2015

  • Palandri, Amandine; L'hôte, David; Cohen-Tannoudji, Joëlle
  • Human Molecular Genetics, Vol. 24, Issue 9
  • DOI: 10.1093/hmg/ddv024

The Essential Toxin: Impact of Zinc on Human Health
journal, March 2010

  • Plum, Laura M.; Rink, Lothar; Haase, Hajo
  • International Journal of Environmental Research and Public Health, Vol. 7, Issue 4
  • DOI: 10.3390/ijerph7041342

Carbonic anhydrase supports electrolyte transport in Drosophila Malpighian tubules. Evidence by X-ray microanalysis of cryosections
journal, February 1997


Timing of Locomotor Recovery from Anoxia Modulated by the white Gene in Drosophila
journal, March 2016


Regulation of Cation Balance in Saccharomyces cerevisiae
journal, March 2013


Lightoid and Claret: A rab GTPase and its putative guanine nucleotide exchange factor in biogenesis of Drosophila eye pigment granules
journal, August 2004

  • Ma, J.; Plesken, H.; Treisman, J. E.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 32
  • DOI: 10.1073/pnas.0401926101

Homeostatic Mechanisms for Iron Storage Revealed by Genetic Manipulations and Live Imaging of Drosophila Ferritin
journal, July 2007


Zinc Detoxification: A Functional Genomics and Transcriptomics Analysis in Drosophila melanogaster Cultured Cells
journal, December 2017

  • Mohr, Stephanie E.; Rudd, Kirstin; Hu, Yanhui
  • G3: Genes|Genomes|Genetics, Vol. 8, Issue 2
  • DOI: 10.1534/g3.117.300447

A role for the Drosophila zinc transporter Zip88E in protecting against dietary zinc toxicity
journal, July 2017


Tracing the evolutionary origins of insect renal function
journal, April 2015

  • Halberg, Kenneth A.; Terhzaz, Selim; Cabrero, Pablo
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7800

Structure of the human multidrug transporter ABCG2
journal, May 2017

  • Taylor, Nicholas M. I.; Manolaridis, Ioannis; Jackson, Scott M.
  • Nature, Vol. 546, Issue 7659
  • DOI: 10.1038/nature22345

Systematic functional characterization of putative zinc transport genes and identification of zinc toxicosis phenotypes in Drosophila melanogaster
journal, June 2012

  • Lye, J. C.; Richards, C. D.; Dechen, K.
  • Journal of Experimental Biology, Vol. 215, Issue 18
  • DOI: 10.1242/jeb.069260

Hermansky-Pudlak Syndrome: Health Care Throughout Life
journal, June 2013


Fine structure and X-ray microanalysis of mineralized concretions in the Malpighian tubules of the housefly, Musca domestica
journal, January 1976