Haem-responsive gene transporter enables mobilization of host haem in ticks

. 2021 Sep ; 11 (9) : 210048. [epub] 20210901

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34465215

Ticks, notorious blood-feeders and disease-vectors, have lost a part of their genetic complement encoding haem biosynthetic enzymes and are, therefore, dependent on the acquisition and distribution of host haem. Solute carrier protein SLC48A1, aka haem-responsive gene 1 protein (HRG1), has been implicated in haem transport, regulating the availability of intracellular haem. HRG1 transporter has been identified in both free-living and parasitic organisms ranging from unicellular kinetoplastids, nematodes, up to vertebrates. However, an HRG1 homologue in the arthropod lineage has not yet been identified. We have identified a single HRG1 homologue in the midgut transcriptome of the tick Ixodes ricinus, denoted as IrHRG, and have elucidated its role as a haem transporter. Data from haem biosynthesis-deficient yeast growth assays, systemic RNA interference and the evaluation of gallium protoporphyrin IX-mediated toxicity through tick membrane feeding clearly show that IrHRG is the bona fide tetrapyrrole transporter. We argue that during evolution, ticks profited from retaining a functional hrg1 gene in the genome because its protein product facilitates host haem escort from intracellularly digested haemoglobin, rendering haem bioavailable for a haem-dependent network of enzymes.

Zobrazit více v PubMed

Perner J, Gasser RB, Oliveira PL, Kopacek P. 2019. Haem biology in metazoan parasites — ‘the bright side of haem’. Trends Parasitol. 35, 213-225. ( 10.1016/j.pt.2019.01.001) PubMed DOI

Gracasouza A, Mayamonteiro C, Paivasilva G, Braz G, Paes M, Sorgine M, Oliveira M, Oliveira P. 2006. Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochem. Mol. Biol. 36, 322-335. ( 10.1016/j.ibmb.2006.01.009) PubMed DOI

Perner J, Sobotka R, Sima R, Konvickova J, Sojka D, Oliveira PL, Hajdusek O, Kopacek P. 2016. Acquisition of exogenous haem is essential for tick reproduction. eLife 5, e12318. ( 10.7554/eLife.12318) PubMed DOI PMC

Sojka D, et al PubMed DOI

Agbede RIS. 1986. Scanning electron microscopy of digest cells in the midgut epithelium of PubMed DOI

Tarnowski BI, Coons LB. 1989. Ultrastructure of the midgut and blood meal digestion in the adult tick PubMed DOI

Lara FA, et al. 2003. A new intracellular pathway of haem detoxification in the midgut of the cattle tick PubMed DOI

Thöny-Meyer L. 2009. Heme transport and incorporation into proteins. In Tetrapyrroles. Molecular biology intelligence unit. New York, NY: Springer.

Chambers IG, Willoughby MM, Hamza I, Reddi AR. 2021. One ring to bring them all and in the darkness bind them: the trafficking of heme without deliverers. Biochim. et Biophys. Acta (BBA) 1868, 118881. ( 10.1016/j.bbamcr.2020.118881) PubMed DOI PMC

Reddi AR, Hamza I. 2016. Heme mobilization in animals: a metallolipid's journey. Accounts Chem. Res. 49, 1104-1110. ( 10.1021/acs.accounts.5b00553) PubMed DOI PMC

Huynh C, Yuan X, Miguel DC, Renberg RL, Protchenko O, Philpott CC, Hamza I, Andrews NW. 2012. Heme uptake by PubMed DOI PMC

Cabello-Donayre M, et al PubMed DOI

Horakova E, et al PubMed DOI PMC

Luck AN, Yuan X, Voronin D, Slatko BE, Hamza I, Foster JM. 2016. Heme acquisition in the parasitic filarial nematode PubMed DOI PMC

Toh SQ, Gobert GN, Malagon Martinez D, Jones MK. 2015. Haem uptake is essential for egg production in the haematophagous blood fluke of humans, PubMed DOI

Rajagopal A, et al PubMed DOI PMC

Pek RH, et al PubMed DOI PMC

White C, et al PubMed DOI PMC

Perner J, et al PubMed DOI PMC

Yuan X, Protchenko O, Philpott CC, Hamza I. 2012. Topologically conserved residues direct heme transport in HRG-1-related proteins. J. Biol. Chem. 287, 4914-4924. ( 10.1074/jbc.M111.326785) PubMed DOI PMC

Misra S, Puertollano R, Kato Y, Bonifacino JS, Hurley JH. 2002. Structural basis for acidic-cluster-dileucine sorting-signal recognition by VHS domains. Nature 415, 933-937. ( 10.1038/415933a) PubMed DOI

Shiba T, et al PubMed DOI

Staudt C, Puissant E, Boonen M. 2016. Subcellular trafficking of mammalian lysosomal proteins: an extended view. Int. J. Mol. Sci. 18, 47. ( 10.3390/ijms18010047) PubMed DOI PMC

Miguel DC, Flannery AR, Mittra B, Andrews NW. 2013. Heme uptake mediated by LHR1 is essential for PubMed DOI PMC

Severance S, Rajagopal A, Rao AU, Cerqueira GC, Mitreva M, El-Sayed NM, Krause M, Hamza I. 2010. Genome-wide analysis reveals novel genes essential for heme homeostasis in PubMed DOI PMC

Protchenko O, Shakoury-Elizeh M, Keane P, Storey J, Androphy R, Philpott CC. 2008. Role of PUG1 in inducible porphyrin and heme transport in PubMed DOI PMC

Zhang J, Chambers I, Yun S, Phillips J, Krause M, Hamza I. 2018. Hrg1 promotes heme-iron recycling during hemolysis in the zebrafish kidney. PLoS Genetics 14, e1007665. ( 10.1371/journal.pgen.1007665) PubMed DOI PMC

Richter K, Van den Driessche F, Coenye T. 2017. Innovative approaches to treat PubMed DOI

Lara FA. 2005. Tracing heme in a living cell: hemoglobin degradation and heme traffic in digest cells of the cattle tick PubMed DOI

Sojka D, et al PubMed DOI

O'Callaghan KM, Ayllon V, O'keeffe J, Wang Y, Cox OT, Loughran G, Forgac M, O'connor R. 2010. Heme-binding protein HRG-1 is induced by insulin-like growth factor I and associates with the vacuolar H PubMed DOI PMC

Franta Z, et al PubMed DOI PMC

Perner J, et al PubMed DOI

Hajdusek O, Sima R, Perner J, Loosova G, Harcubova A, Kopacek P. 2016. Tick iron and heme metabolism — new target for an anti-tick intervention. Ticks Tick-borne Dis. 7, 565-572. ( 10.1016/j.ttbdis.2016.01.006) PubMed DOI

Liao R, et al PubMed DOI PMC

Hajdusek O, Sojka D, Kopacek P, Buresova V, Franta Z, Sauman I, Winzerling J, Grubhoffer L. 2009. Knockdown of proteins involved in iron metabolism limits tick reproduction and development. Proc. Natl Acad. Sci. 106, 1033-1038. ( 10.1073/pnas.0807961106) PubMed DOI PMC

Pagura L, Tevere E, Merli ML, Cricco JA. 2020. A new model for PubMed DOI PMC

Ponka P, Sheftel AD, English AM, Scott Bohle D, Garcia-Santos D. 2017. Do mammalian cells really need to export and import heme? Trends Biochem. Sci. 42, 395-406. ( 10.1016/j.tibs.2017.01.006) PubMed DOI

Lara FA, et al PubMed DOI PMC

Jagt DLV, Hunsaker LA, Campos NM. 1987. Comparison of proteases from chloroquine-sensitive and chloroquine-resistant strains of PubMed DOI

Chugh M, Sundararaman V, Kumar S, Reddy VS, Siddiqui WA, Stuart KD, Malhotra P. 2013. Protein complex directs hemoglobin-to-hemozoin formation in PubMed DOI PMC

Noland GS, Briones N, Sullivan DJ. 2003. The shape and size of hemozoin crystals distinguishes diverse PubMed DOI

Cabello-Donayre M, et al PubMed DOI PMC

Zutz A, Gompf S, Schägger H, Tampé R. 2009. Mitochondrial ABC proteins in health and disease. Biochim. et Biophys. Acta (BBA) 1787, 681-690. ( 10.1016/j.bbabio.2009.02.009) PubMed DOI

Kotsyfakis M, Schwarz A, Erhart J, Ribeiro JM. 2015. Tissue- and time-dependent transcription in PubMed DOI PMC

Laranjeira-Silva MF, Hamza I, Pérez-Victoria JM. 2020. Iron and heme metabolism at the leishmania–host interface. Trends Parasitol. 36, 279-289. ( 10.1016/j.pt.2019.12.010) PubMed DOI PMC

Stojiljkovic I, Kumar V, Srinivasan N. 1999. Non-iron metalloporphyrins: potent antibacterial compounds that exploit haem/Hb uptake systems of pathogenic bacteria. Mol. Microbiol. 31, 429-442. ( 10.1046/j.1365-2958.1999.01175.x) PubMed DOI

Hijazi S, Visca P, Frangipani E. 2017. Gallium-protoporphyrin IX inhibits PubMed DOI PMC

Kröber T, Guerin PM. 2007. PubMed DOI

Ito H, Fukuda Y, Murata K, Kimura A. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168. ( 10.1128/jb.153.1.163-168.1983) PubMed DOI PMC

Iwase T, Tajima A, Sugimoto S, Okuda K, Hironaka I, Kamata Y, Takada K, Mizunoe Y. 2013. A simple assay for measuring catalase activity: a visual approach. Sci. Rep. 3, 03081. ( 10.1038/srep03081) PubMed DOI PMC

Nijhof AM, Balk JA, Postigo M, Jongejan F. 2009. Selection of reference genes for quantitative RT-PCR studies in PubMed DOI PMC

Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. ( 10.1093/molbev/mst010) PubMed DOI PMC

Darriba D, Taboada GL, Doallo R, Posada D. 2011. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164-1165. ( 10.1093/bioinformatics/btr088) PubMed DOI PMC

Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ.. 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 44, W232-W235. ( 10.1093/nar/gkw256) PubMed DOI PMC

Rambaut A. 2019. Figtree v1.4.4. See http://tree.bio.ed.ac.uk/software/figtree/ (accessed 5 Dec 2019).

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Haptoglobin is dispensable for haemoglobin uptake by Trypanosoma brucei

. 2024 ; 15 () : 1441131. [epub] 20240718

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...