1932

Abstract

Iron is an essential micronutrient for all types of organisms; however, iron has chemical properties that can be harmful to cells. Because iron is both necessary and potentially damaging, insects have homeostatic processes that control the redox state, quantity, and location of iron in the body. These processes include uptake of iron from the diet, intracellular and extracellular iron transport, and iron storage. Early studies of iron-binding proteins in insects suggested that insects and mammals have surprisingly different mechanisms of iron homeostasis, including different primary mechanisms for exporting iron from cells and for transporting iron from one cell to another, and subsequent studies have continued to support this view. This review summarizes current knowledge about iron homeostasis in insects, compares insect and mammalian iron homeostasis mechanisms, and calls attention to key remaining knowledge gaps.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-040622-092836
2023-01-23
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/ento/68/1/annurev-ento-040622-092836.html?itemId=/content/journals/10.1146/annurev-ento-040622-092836&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Adamo SA, Fidler TL, Forestell CA. 2007. Illness-induced anorexia and its possible function in the caterpillar, Manduca sexta. Brain Behav. Immun. 21:3292–300
    [Google Scholar]
  2. 2.
    Anderson GJ, Vulpe CD. 2009. Mammalian iron transport. Cell. Mol. Life Sci. 66:203241–61
    [Google Scholar]
  3. 3.
    Arosio P, Ingrassia R, Cavadini P. 2009. Ferritins: a family of molecules for iron storage, antioxidation and more. Biochim. Biophys. Acta 1790:7589–99
    [Google Scholar]
  4. 4.
    Bai L, Qiao M, Zheng R, Deng C, Mei S, Chen W 2016. Phylogenomic analysis of transferrin family from animals and plants. Comp. Biochem. Physiol. D 17:1–8
    [Google Scholar]
  5. 5.
    Baker EN, Baker HM, Kidd RD. 2002. Lactoferrin and transferrin: functional variations on a common structural framework. Biochem. Cell Biol. 80:127–34
    [Google Scholar]
  6. 6.
    Barbehenn R, Dodick T, Poopat U, Spencer B. 2005. Fenton-type reactions and iron concentrations in the midgut fluids of tree-feeding caterpillars. Arch. Insect Biochem. Physiol. 60:132–43
    [Google Scholar]
  7. 7.
    Bernstein SE. 1987. Hereditary hypotransferrinemia with hemosiderosis, a murine disorder resembling human atransferrinemia. J. Lab. Clin. Med. 110:6690–705
    [Google Scholar]
  8. 8.
    Bettedi L, Aslam MF, Szular J, Mandilaras K, Missirlis F. 2011. Iron depletion in the intestines of Malvolio mutant flies does not occur in the absence of a multicopper oxidase. J. Exp. Biol. 214:6971–78
    [Google Scholar]
  9. 9.
    Bou-Abdallah F. 2010. The iron redox and hydrolysis chemistry of the ferritins. Biochim. Biophys. Acta 1800:8719–31
    [Google Scholar]
  10. 10.
    Braz GRC, Moreira MF, Masuda H, Oliveira PL. 2002. Rhodnius heme-binding protein (RHBP) is a heme source for embryonic development in the blood-sucking bug Rhodnius prolixus (Hemiptera, Reduviidae). Insect Biochem. Mol. Biol. 32:4361–67
    [Google Scholar]
  11. 11.
    Brummett LM, Kanost MR, Gorman MJ. 2017. The immune properties of Manduca sexta transferrin. Insect Biochem. Mol. Biol. 81:1–9
    [Google Scholar]
  12. 12.
    Buchon N, Osman D, David FPA, Fang HY, Boquete J-P et al. 2013. Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep 3:51725–38
    [Google Scholar]
  13. 13.
    Budnik V, White K. 1987. Genetic dissection of dopamine and serotonin synthesis in the nervous system of Drosophila melanogaster. J. Neurogenet. 4:6309–14
    [Google Scholar]
  14. 14.
    Burmester T, Hankeln T. 2007. The respiratory proteins of insects. J. Insect Physiol. 53:4285–94
    [Google Scholar]
  15. 15.
    Capurro M de L, Iughetti P, Ribolla PE, de Bianchi AG. 1996. Musca domestica hemolymph ferritin. Arch. Insect Biochem. Physiol. 32:2197–207
    [Google Scholar]
  16. 16.
    Chiabrando D, Vinchi F, Fiorito V, Mercurio S, Tolosano E. 2014. Heme in pathophysiology: a matter of scavenging, metabolism and trafficking across cell membranes. Front. Pharmacol. 5:61
    [Google Scholar]
  17. 17.
    Chintapalli VR, Wang J, Dow JAT. 2007. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 39:6715–20
    [Google Scholar]
  18. 18.
    Coffey R, Ganz T. 2017. Iron homeostasis: an anthropocentric perspective. J. Biol. Chem. 292:3112727–34
    [Google Scholar]
  19. 19.
    Cui L, Yoshioka Y, Suyari O, Kohno Y, Zhang X et al. 2008. Relevant expression of Drosophila heme oxygenase is necessary for the normal development of insect tissues. Biochem. Biophys. Res. Commun. 377:41156–61
    [Google Scholar]
  20. 20.
    Dechen K, Richards CD, Lye JC, Hwang JEC, Burke R. 2015. Compartmentalized zinc deficiency and toxicities caused by ZnT and Zip gene over expression result in specific phenotypes in Drosophila. Int. J. Biochem. Cell Biol. 60:23–33
    [Google Scholar]
  21. 21.
    Dietz JV, Fox JL, Khalimonchuk O. 2021. Down the iron path: mitochondrial iron homeostasis and beyond. Cells 10:92198
    [Google Scholar]
  22. 22.
    Dittmer NT, Kanost MR. 2010. Insect multicopper oxidases: diversity, properties, and physiological roles. Insect Biochem. Mol. Biol. 40:3179–88
    [Google Scholar]
  23. 23.
    Donegan RK, Moore CM, Hanna DA, Reddi AR. 2019. Handling heme: the mechanisms underlying the movement of heme within and between cells. Free Radic. . Biol. Med. 133:88–100
    [Google Scholar]
  24. 24.
    Donovan A, Lima CA, Pinkus JL, Pinkus GS, Zon LI et al. 2005. The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metab. 1:3191–200
    [Google Scholar]
  25. 25.
    Drysdale J, Arosio P, Invernizzi R, Cazzola M, Volz A et al. 2002. Mitochondrial ferritin: a new player in iron metabolism. Blood Cells Mol. Dis. 29:3376–83
    [Google Scholar]
  26. 26.
    Dunkov B, Georgieva T. 2006. Insect iron binding proteins: insights from the genomes. Insect Biochem. Mol. Biol. 36:4300–9
    [Google Scholar]
  27. 27.
    Eggleston H, Adelman ZN. 2020. Transcriptomic analyses of Aedes aegypti cultured cells and ex vivo midguts in response to an excess or deficiency of heme: a quest for transcriptionally-regulated heme transporters. BMC Genom. 21:1604
    [Google Scholar]
  28. 28.
    Farnaud S, Evans RW. 2003. Lactoferrin—a multifunctional protein with antimicrobial properties. Mol. Immunol. 40:7395–405
    [Google Scholar]
  29. 29.
    Folwell JL, Barton CH, Shepherd D. 2006. Immunolocalisation of the D. melanogaster Nramp homologue Malvolio to gut and Malpighian tubules provides evidence that Malvolio and Nramp2 are orthologous. J. Exp. Biol. 209:101988–95
    [Google Scholar]
  30. 30.
    Frazer DM, Anderson GJ. 2014. The regulation of iron transport. Biofactors 40:2206–14
    [Google Scholar]
  31. 31.
    Geiser DL, Conley ZR, Elliott JL, Mayo JJ, Winzerling JJ. 2015. Characterization of Anopheles gambiae (African malaria mosquito) ferritin and the effect of iron on intracellular localization in mosquito cells. J. Insect Sci. 15:68
    [Google Scholar]
  32. 32.
    Geiser DL, Mayo JJ, Winzerling JJ. 2007. The unique regulation of Aedes aegypti larval cell ferritin by iron. Insect Biochem. Mol. Biol. 37:5418–29
    [Google Scholar]
  33. 33.
    Geiser DL, Patel N, Patel P, Bhakta J, Velasquez LS, Winzerling JJ. 2017. Description of a second ferritin light chain homologue from the yellow fever mosquito (Diptera: Culicidae). J. Insect Sci. 17:6123
    [Google Scholar]
  34. 34.
    Geiser DL, Thai TN, Love MB, Winzerling JJ. 2019. Iron and ferritin deposition in the ovarian tissues of the yellow fever mosquito (Diptera: Culicidae). J. Insect Sci. 19:511
    [Google Scholar]
  35. 35.
    Geiser DL, Winzerling JJ. 2012. Insect transferrins: multifunctional proteins. Biochim. Biophys. Acta Gen. Subj. 1820:3437–51
    [Google Scholar]
  36. 36.
    Geiser DL, Zhang DZ, Winzerling JJ. 2006. Secreted ferritin: mosquito defense against iron overload?. Insect Biochem. Mol. Biol. 36:3177–87
    [Google Scholar]
  37. 37.
    Gkouvatsos K, Papanikolaou G, Pantopoulos K. 2012. Regulation of iron transport and the role of transferrin. Biochim. Biophys. Acta Gen. Subj. 1820:3188–202
    [Google Scholar]
  38. 38.
    Gonzalez-Morales N, Mendoza-Ortiz , Blowes LM, Missirlis F, Riesgo-Escovar JR. 2015. Ferritin is required in multiple tissues during Drosophila melanogaster development. PLOS ONE 10:7e0133499
    [Google Scholar]
  39. 39.
    Graça-Souza AV, Maya-Monteiro C, Paiva-Silva GO, Braz GRC, Paes MC et al. 2006. Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochem. Mol. Biol. 36:4322–35
    [Google Scholar]
  40. 40.
    Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM et al. 2011. The developmental transcriptome of Drosophila melanogaster. Nature 471:7339473–79
    [Google Scholar]
  41. 41.
    Gulec S, Anderson GJ, Collins JF. 2014. Mechanistic and regulatory aspects of intestinal iron absorption. Am. J. Physiol. Gastrointest. Liver Physiol. 307:4G397–409
    [Google Scholar]
  42. 42.
    Gutierrez L, Zubow K, Nield J, Gambis A, Mollereau B et al. 2013. Biophysical and genetic analysis of iron partitioning and ferritin function in Drosophila melanogaster. Metallomics 5:8997–1005
    [Google Scholar]
  43. 43.
    Halestrap AP. 2013. The SLC16 gene family—structure, role and regulation in health and disease. Mol. Aspects Med. 34:2–3337–49
    [Google Scholar]
  44. 44.
    Hamburger AE, West AP, Hamburger ZA, Hamburger P, Bjorkman PJ. 2005. Crystal structure of a secreted insect ferritin reveals a symmetrical arrangement of heavy and light chains. J. Mol. Biol. 349:3558–69
    [Google Scholar]
  45. 45.
    Hamill RL, Woods JC, Cook BA. 1991. Congenital atransferrinemia: a case report and review of the literature. Am. J. Clin. Pathol. 96:2215–18
    [Google Scholar]
  46. 46.
    Hara T, Takeda T, Takagishi T, Fukue K, Kambe T, Fukada T. 2017. Physiological roles of zinc transporters: molecular and genetic importance in zinc homeostasis. J. Physiol. Sci. 67:2283–301
    [Google Scholar]
  47. 47.
    Hayashi A, Wada Y, Suzuki T, Shimizu A. 1993. Studies on familial hypotransferrinemia: unique clinical course and molecular pathology. Am. J. Hum. Genet. 53:1201–13
    [Google Scholar]
  48. 48.
    Hehlert P, Hofferek V, Heier C, Eichmann TO, Riedel D et al. 2019. The α/β-hydrolase domain-containing 4- and 5-related phospholipase Pummelig controls energy storage in Drosophila. J. Lipid Res. 60:81365–78
    [Google Scholar]
  49. 49.
    Hellman NE, Gitlin JD. 2002. Ceruloplasmin metabolism and function. Annu. Rev. Nutr. 22:439–58
    [Google Scholar]
  50. 50.
    Helmer OM, Emerson CP. 1934. The iron content of the whole blood of normal individuals. J. Biol. Chem. 104:1157–61
    [Google Scholar]
  51. 51.
    Hrdina A, Iatsenko I. 2021. The roles of metals in insect-microbe interactions and immunity. Curr. Opin. Insect Sci. 49:71–77
    [Google Scholar]
  52. 52.
    Hsu C-Y, Li C-W. 1994. Magnetoreception in honeybees. Science 265:516895–97
    [Google Scholar]
  53. 53.
    Huebers HA, Huebers E, Finch CA, Webb BA, Truman JW et al. 1988. Iron binding proteins and their roles in the tobacco hornworm, Manduca sexta (L.). J. Comp. Physiol. B 158:3291–300
    [Google Scholar]
  54. 54.
    Hughes AL, Friedman R. 2014. Evolutionary diversification of the vertebrate transferrin multi-gene family. Immunogenetics 66:11651–61
    [Google Scholar]
  55. 55.
    Iatsenko I, Marra A, Boquete J-P, Peña J, Lemaitre B. 2020. Iron sequestration by transferrin 1 mediates nutritional immunity in Drosophila melanogaster. PNAS 117:137317–25
    [Google Scholar]
  56. 56.
    Ida H, Suyari O, Shimamura M, Tien Tai T, Yamaguchi M, Taketani S 2013. Genetic link between heme oxygenase and the signaling pathway of DNA damage in Drosophila melanogaster. Tohoku J. Exp. Med. 231:2117–25
    [Google Scholar]
  57. 57.
    Iliadi KG, Avivi A, Iliadi NN, Knight D, Korol AB et al. 2008. Nemy encodes a cytochrome b561 that is required for Drosophila learning and memory. PNAS 105:5019986–91
    [Google Scholar]
  58. 58.
    Khanna MR, Stanley BA, Thomas GH 2010. Towards a membrane proteome in Drosophila: a method for the isolation of plasma membrane. BMC Genom. 11:302
    [Google Scholar]
  59. 59.
    Knight D, Iliadi KG, Iliadi N, Wilk R, Hu J et al. 2015. Distinct regulation of transmitter release at the Drosophila NMJ by different isoforms of nemy. PLOS ONE 10:8e0132548
    [Google Scholar]
  60. 60.
    Knutson MD. 2017. Iron transport proteins: gateways of cellular and systemic iron homeostasis. J. Biol. Chem. 292:3112735–43
    [Google Scholar]
  61. 61.
    Knutson MD. 2019. Non-transferrin-bound iron transporters. Free Radic. . Biol. Med. 133:101–11
    [Google Scholar]
  62. 62.
    Kosman DJ. 2010. Redox cycling in iron uptake, efflux, and trafficking. J. Biol. Chem. 285:3526729–35
    [Google Scholar]
  63. 63.
    Kosman DJ. 2013. Iron metabolism in aerobes: managing ferric iron hydrolysis and ferrous iron autoxidation. Coord. Chem. Rev. 257:1210–17
    [Google Scholar]
  64. 64.
    Kosman DJ. 2018. The teleos of metallo-reduction and metallo-oxidation in eukaryotic iron and copper trafficking. Metallomics 10:3370–77
    [Google Scholar]
  65. 65.
    Kosman DJ. 2020. A holistic view of mammalian (vertebrate) cellular iron uptake. Metallomics 12:91323–34
    [Google Scholar]
  66. 66.
    Kramer KJ, Seib PA. 1982. Ascorbic acid and the growth and development of insects. Adv. Chem. Ser. 200:275–91
    [Google Scholar]
  67. 67.
    Krieg L, Milstein O, Krebs P, Xia Y, Beutler B, Du X. 2011. Mutation of the gastric hydrogen-potassium ATPase alpha subunit causes iron-deficiency anemia in mic. Blood 118:246418–25
    [Google Scholar]
  68. 68.
    Kurama T, Kurata S, Natori S. 1995. Molecular characterization of an insect transferrin and its selective incorporation into eggs during oogenesis. Eur. J. Biochem. 228:2229–35
    [Google Scholar]
  69. 69.
    Lambert LA. 2012. Molecular evolution of the transferrin family and associated receptors. Biochim. Biophys. Acta Gen. Subj. 1820:3244–55
    [Google Scholar]
  70. 70.
    Lane DJR, Bae D-H, Merlot AM, Sahni S, Richardson DR. 2015. Duodenal cytochrome b (DCYTB) in iron metabolism: an update on function and regulation. Nutrients 7:42274–96
    [Google Scholar]
  71. 71.
    Lang M, Braun CL, Kanost MR, Gorman MJ. 2012. Multicopper oxidase-1 is a ferroxidase essential for iron homeostasis in Drosophila melanogaster. PNAS 109:3313337–42
    [Google Scholar]
  72. 72.
    Lara FA, Pohl PC, Gandara AC, da Silva Ferreira J, Nascimento-Silva MC et al. 2015. ATP binding cassette transporter mediates both heme and pesticide detoxification in tick midgut cells. PLOS ONE 10:8e0134779
    [Google Scholar]
  73. 73.
    Larkin A, Marygold SJ, Antonazzo G, Attrill H, dos Santos G et al. 2021. FlyBase: updates to the Drosophila melanogaster knowledge base. Nucleic Acids Res 49:D1D899–907
    [Google Scholar]
  74. 74.
    Le Blanc S, Garrick MD, Arredondo M 2012. Heme carrier protein 1 transports heme and is involved in heme-Fe metabolism. Am. J. Physiol. Cell Physiol. 302:12C1780–85
    [Google Scholar]
  75. 75.
    Li S. 2010. Identification of iron-loaded ferritin as an essential mitogen for cell proliferation and postembryonic development in Drosophila. Cell Res. 20:101148–57
    [Google Scholar]
  76. 76.
    Linder MC. 2013. Mobilization of stored iron in mammals: a review. Nutrients 5:104022–50
    [Google Scholar]
  77. 77.
    Liu X, Sun C, Liu X, Yin X, Wang B et al. 2015. Multicopper oxidase-1 is required for iron homeostasis in Malpighian tubules of Helicoverpa armigera. Sci. Rep. 5:14784
    [Google Scholar]
  78. 78.
    Liuzzi JP, Cousins RJ. 2004. Mammalian zinc transporters. Annu. Rev. Nutr. 24:151–72
    [Google Scholar]
  79. 79.
    Locke M, Nichol H 1992. Iron economy in insects: transport, metabolism, and storage. Annu. Rev. Entomol. 37:195–215
    [Google Scholar]
  80. 80.
    Mandilaras K, Missirlis F. 2012. Genes for iron metabolism influence circadian rhythms in Drosophila melanogaster. Metallomics 4:9928–36
    [Google Scholar]
  81. 81.
    Mandilaras K, Pathmanathan T, Missirlis F. 2013. Iron absorption in Drosophila melanogaster. Nutrients 5:51622–47
    [Google Scholar]
  82. 82.
    Marelja Z, Leimkühler S, Missirlis F. 2018. Iron sulfur and molybdenum cofactor enzymes regulate the Drosophila life cycle by controlling cell metabolism. Front. Physiol. 9:50
    [Google Scholar]
  83. 83.
    Martinez-Barnetche J, Garcia Solache M, Lecona AN, Tello Lopez AT, del Carmen Rodriguez M et al. 2007. Cloning and functional characterization of the Anopheles albimanus DMT1/NRAMP homolog: implications in iron metabolism in mosquitoes. Insect Biochem. Mol. Biol. 37:6532–39
    [Google Scholar]
  84. 84.
    Mehlferber EC, Benowitz KM, Roy-Zokan EM, McKinney EC, Cunningham CB, Moore AJ. 2017. Duplication and sub/neofunctionalization of Malvolio, an insect homolog of Nramp, in the subsocial beetle Nicrophorus vespilloides. G3 7:103393–403
    [Google Scholar]
  85. 85.
    Metzendorf C, Wu W, Lind MI. 2009. Overexpression of Drosophila mitoferrin in l(2)mbn cells results in dysregulation of Fer1HCH expression. Biochem. J. 421:3463–71
    [Google Scholar]
  86. 86.
    Miguel-Aliaga I, Jasper H, Lemaitre B 2018. Anatomy and physiology of the digestive tract of Drosophila melanogaster. Genetics 210:2357–96
    [Google Scholar]
  87. 87.
    Missirlis F, Holmberg S, Georgieva T, Dunkov BC, Rouault TA, Law JH. 2006. Characterization of mitochondrial ferritin in Drosophila. PNAS 103:155893–98
    [Google Scholar]
  88. 88.
    Missirlis F, Kosmidis S, Brody T, Mavrakis M, Holmberg S et al. 2007. Homeostatic mechanisms for iron storage revealed by genetic manipulations and live imaging of Drosophila ferritin. Genetics 177:189–100
    [Google Scholar]
  89. 89.
    Mumbauer S, Pascual J, Kolotuev I, Hamaratoglu F. 2019. Ferritin heavy chain protects the developing wing from reactive oxygen species and ferroptosis. PLOS Genet. 15:9e1008396
    [Google Scholar]
  90. 90.
    Najera DG, Dittmer NT, Weber JJ, Kanost MR, Gorman MJ. 2020. Phylogenetic and sequence analyses of insect transferrins suggest that only transferrin 1 has a role in iron homeostasis. Insect Sci. 28:2495–508
    [Google Scholar]
  91. 91.
    Neckameyer WS, White K. 1993. Drosophila tyrosine hydroxylase is encoded by the pale locus. J. Neurogenet. 8:4189–99
    [Google Scholar]
  92. 92.
    Nichol H, Law JH, Winzerling JJ. 2002. Iron metabolism in insects. Annu. Rev. Entomol. 47:535–59
    [Google Scholar]
  93. 93.
    Nichol H, Locke M. 1990. The localization of ferritin in insects. Tissue Cell 22:6767–77
    [Google Scholar]
  94. 94.
    Nichol H, Locke M. 1999. Secreted ferritin subunits are of two kinds in insects—molecular cloning of cDNAs encoding two major subunits of secreted ferritin from Calpodes ethlius. Insect Biochem. Mol. Biol. 29:11999–1013
    [Google Scholar]
  95. 95.
    Oliveira P, Kawooya J, Ribeiro J, Meyer T, Poorman R et al. 1995. A heme-binding protein from hemolymph and oocytes of the bloodsucking insect, Rhodnius prolixus—isolation and characterization. J. Biol. Chem. 270:1810897–901
    [Google Scholar]
  96. 96.
    Orgad S, Nelson H, Segal D, Nelson N 1998. Metal ions suppress the abnormal taste behavior of the Drosophila mutant Malvolio. J. Exp. Biol. 201:1115–20
    [Google Scholar]
  97. 97.
    Peng Z, Dittmer NT, Lang M, Brummett LM, Braun CL et al. 2015. Multicopper oxidase-1 orthologs from diverse insect species have ascorbate oxidase activity. Insect Biochem. Mol. Biol. 59:58–71
    [Google Scholar]
  98. 98.
    Petrak J, Vyoral D. 2005. Hephaestin—a ferroxidase of cellular iron export. Int. J. Biochem. Cell Biol. 37:61173–78
    [Google Scholar]
  99. 99.
    Pham DQD, Winzerling JJ. 2010. Insect ferritins: typical or atypical?. Biochim. Biophys. Acta 1800:8824–33
    [Google Scholar]
  100. 100.
    Philpott CC, Ryu M-S, Frey A, Patel S. 2017. Cytosolic iron chaperones: proteins delivering iron cofactors in the cytosol of mammalian cells. J. Biol. Chem. 292:3112764–71
    [Google Scholar]
  101. 101.
    Picco C, Scholz-Starke J, Naso A, Preger V, Sparla F et al. 2014. How are cytochrome b561 electron currents controlled by membrane voltage and substrate availability?. Antioxid. Redox Signal. 21:3384–91
    [Google Scholar]
  102. 102.
    Puig S, Ramos-Alonso L, Romero AM, Martínez-Pastor MT. 2017. The elemental role of iron in DNA synthesis and repair. Metallomics 9:111483–500
    [Google Scholar]
  103. 103.
    Qin Q, Wang X, Zhou B. 2013. Functional studies of Drosophila zinc transporters reveal the mechanism for dietary zinc absorption and regulation. BMC Biol. 11:101
    [Google Scholar]
  104. 104.
    Qin S, Yin H, Yang C, Dou Y, Liu Z et al. 2016. A magnetic protein biocompass. Nat. Mater. 15:2217–26
    [Google Scholar]
  105. 105.
    Rosas-Arellano A, Vasquez-Procopio J, Gambis A, Blowes LM, Steller H et al. 2016. Ferritin assembly in enterocytes of Drosophila melanogaster. Int. J. Mol. Sci. 17:227
    [Google Scholar]
  106. 106.
    Scott JG, Wen Z. 2001. Cytochromes P450 of insects: the tip of the iceberg. Pest Manag. Sci. 57:10958–67
    [Google Scholar]
  107. 107.
    Segond D, Khalil EA, Buisson C, Daou N, Kallassy M et al. 2014. Iron acquisition in Bacillus cereus: the roles of IlsA and bacillibactin in exogenous ferritin iron mobilization. PLOS Pathog. 10:2e1003935
    [Google Scholar]
  108. 108.
    Shanbhag S, Tripathi S. 2005. Electrogenic H+ transport and pH gradients generated by a V-H+-ATPase in the isolated perfused larval Drosophila midgut. J. Membr. Biol. 206:161–72
    [Google Scholar]
  109. 109.
    Shawki A, Engevik MA, Kim RS, Knight PB, Baik RA et al. 2016. Intestinal brush-border Na+/H+ exchanger-3 drives H+-coupled iron absorption in the mouse. Am. J. Physiol. Gastrointest. Liver Physiol. 311:3G423–30
    [Google Scholar]
  110. 110.
    Shen Y, Chen Y-Z, Zhang C-X. 2021. RNAi-mediated silencing of ferritin genes in the brown plant-hopper Nilaparvata lugens affects survival, growth and female fecundity. Pest Manag. Sci. 77:1365–77
    [Google Scholar]
  111. 111.
    Southon A, Farlow A, Norgate M, Burke R, Camakaris J. 2008. Malvolio is a copper transporter in Drosophila melanogaster. J. Exp. Biol. 211:Pt. 5709–16
    [Google Scholar]
  112. 112.
    Spencer CS, Yunta C, de Lima GPG, Hemmings K, Lian L-Y et al. 2018. Characterisation of Anopheles gambiae heme oxygenase and metalloporphyrin feeding suggests a potential role in reproduction. Insect Biochem. Mol. Biol. 98:25–33
    [Google Scholar]
  113. 113.
    Sterkel M, Oliveira JHM, Bottino-Rojas V, Paiva-Silva GO, Oliveira PL. 2017. The dose makes the poison: Nutritional overload determines the life traits of blood-feeding arthropods. Trends Parasitol. 33:8633–44
    [Google Scholar]
  114. 114.
    Tang X, Zhou B. 2013. Ferritin is the key to dietary iron absorption and tissue iron detoxification in Drosophila melanogaster. FASEB J. 27:1288–98
    [Google Scholar]
  115. 115.
    Tang X, Zhou B. 2013. Iron homeostasis in insects: insights from Drosophila studies. IUBMB Life 65:10863–72
    [Google Scholar]
  116. 116.
    Terra WR, Barroso IG, Dias RO, Ferreira C. 2019. Molecular physiology of insect midgut. Adv. Insect Physiol. 56:117–63
    [Google Scholar]
  117. 117.
    Tiklová K, Senti K-A, Wang S, Gräslund A, Samakovlis C. 2010. Epithelial septate junction assembly relies on melanotransferrin iron binding and endocytosis in Drosophila. Nat. Cell Biol. 12:111071–77
    [Google Scholar]
  118. 118.
    Tsaousis AD. 2019. On the origin of iron/sulfur cluster biosynthesis in eukaryotes. Front. Microbiol. 10:2478
    [Google Scholar]
  119. 119.
    Tsujimoto H, Anderson MAE, Eggleston H, Myles KM, Adelman ZN. 2021. Aedes aegypti dyspepsia encodes a novel member of the SLC16 family of transporters and is critical for reproductive fitness. PLOS Negl. Trop. Dis. 15:4e0009334
    [Google Scholar]
  120. 120.
    Tsujimoto H, Anderson MAE, Myles KM, Adelman ZN. 2018. Identification of candidate iron transporters from the ZIP/ZnT gene families in the mosquito Aedes aegypti. Front. Physiol. 9:380
    [Google Scholar]
  121. 121.
    Vargas JD, Herpers B, McKie AT, Gledhill S, McDonnell J et al. 2003. Stromal cell-derived receptor 2 and cytochrome b561 are functional ferric reductases. Biochim. Biophys. Acta Proteins Proteom. 1651:1–2116–23
    [Google Scholar]
  122. 122.
    Verelst W, Asard H. 2003. A phylogenetic study of cytochrome b561 proteins. Genome Biol. 4:6R38
    [Google Scholar]
  123. 123.
    Wajnberg E, Alves OC, Perales J, da Rocha SLG, Ferreira AT et al. 2018. Ferritin from the haemolymph of adult ants: an extraction method for characterization and a ferromagnetic study. Eur. Biophys. J. 47:6641–53
    [Google Scholar]
  124. 124.
    Walter-Nuno AB, Oliveira MP, Oliveira MF, Gonçalves RL, Ramos IB et al. 2013. Silencing of maternal heme-binding protein causes embryonic mitochondrial dysfunction and impairs embryogenesis in the blood sucking insect Rhodnius prolixus. J. Biol. Chem. 288:4129323–32
    [Google Scholar]
  125. 125.
    Walter-Nuno AB, Taracena ML, Mesquita RD, Oliveira PL, Paiva-Silva GO. 2018. Silencing of iron and heme-related genes revealed a paramount role of iron in the physiology of the hematophagous vector Rhodnius prolixus. Front. Genet. 9:19
    [Google Scholar]
  126. 126.
    Wan Z, Xu J, Huang Y, Zhai Y, Ma Z et al. 2020. Elevating bioavailable iron levels in mitochondria suppresses the defective phenotypes caused by PINK1 loss-of-function in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 532:2285–91
    [Google Scholar]
  127. 127.
    Wang W, Knovich MA, Coffman LG, Torti FM, Torti SV. 2010. Serum ferritin: past, present and future. Biochim. Biophys. Acta 1800:8760–69
    [Google Scholar]
  128. 128.
    Wang X, Yin S, Yang Z, Zhou B 2018. Drosophila multicopper oxidase 3 is a potential ferroxidase involved in iron homeostasis. Biochim. Biophys. Acta Gen. Subj. 1862:81826–34
    [Google Scholar]
  129. 129.
    Ward PP, Mendoza-Meneses M, Cunningham GA, Conneely OM. 2003. Iron status in mice carrying a targeted disruption of lactoferrin. Mol. Cell. Biol. 23:1178–85
    [Google Scholar]
  130. 130.
    Waterhouse D, Stay B. 1955. Functional differentiation in the midgut epithelium of blowfly larvae as revealed by histochemical tests. Aust. J. Biol. Sci. 8:2253
    [Google Scholar]
  131. 131.
    Waterhouse DF, Day MF 1953. Function of the gut in absorption, excretion, and intermediary metabolism. Insect Physiology KD Roeder 331–49 New York: John Wiley & Sons
    [Google Scholar]
  132. 132.
    Weber JJ, Kanost MR, Gorman MJ. 2020. Iron binding and release properties of transferrin-1 from Drosophila melanogaster and Manduca sexta: implications for insect iron homeostasis. Insect Biochem. Mol. Biol. 125:103438
    [Google Scholar]
  133. 133.
    Weber JJ, Kashipathy MM, Battaile KP, Go E, Desaire H et al. 2020. Structural insight into the novel iron-coordination and domain interactions of transferrin-1 from a model insect, Manduca sexta. Protein Sci. 30:2408–22
    [Google Scholar]
  134. 134.
    Whiten SR, Eggleston H, Adelman ZN. 2018. Ironing out the details: exploring the role of iron and heme in blood-sucking arthropods. Front. Physiol. 8:1134
    [Google Scholar]
  135. 135.
    Winzerling JJ, Pham DQ-D. 2006. Iron metabolism in insect disease vectors: mining the Anopheles gambiae translated protein database. Insect Biochem. Mol. Biol. 36:4310–21
    [Google Scholar]
  136. 136.
    Wu Y, Zhao H, Zhang EE, Liu N. 2021. Identification of PCBP1 as a novel modulator of mammalian circadian clock. Front. Genet. 12:656571
    [Google Scholar]
  137. 137.
    Xiao G, Liu Z-H, Zhao M, Wang H-L, Zhou B. 2019. Transferrin 1 functions in iron trafficking and genetically interacts with ferritin in Drosophila melanogaster. Cell Rep. 26:3748–58
    [Google Scholar]
  138. 138.
    Xiao G, Wan Z, Fan Q, Tang X, Zhou B. 2014. The metal transporter ZIP13 supplies iron into the secretory pathway in Drosophila melanogaster. eLife 3:e03191
    [Google Scholar]
  139. 139.
    Xiao G, Zhou B. 2018. ZIP13: A study of Drosophila offers an alternative explanation for the corresponding human disease. Front. Genet. 8:234
    [Google Scholar]
  140. 140.
    Xu J, Wan Z, Zhou B 2019. Drosophila ZIP13 is posttranslationally regulated by iron-mediated stabilization. Biochim. Biophys. Acta Mol. Cell Res. 1866:91487–97
    [Google Scholar]
  141. 141.
    Xue J, Li G, Ji X, Liu Z-H, Wang H-L, Xiao G. 2022. Drosophila ZIP13 overexpression or transferrin1 RNAi influences the muscle degeneration of Pink1 RNAi by elevating iron levels in mitochondria. J. Neurochem. 160:5540–55
    [Google Scholar]
  142. 142.
    Yanatori I, Kishi F. 2019. DMT1 and iron transport. Free Radic. . Biol. Med. 133:55–63
    [Google Scholar]
  143. 143.
    Yanatori I, Richardson DR, Toyokuni S, Kishi F. 2020. The new role of poly (rC)-binding proteins as iron transport chaperones: proteins that could couple with inter-organelle interactions to safely traffic iron. Biochim. Biophys. Acta Gen. Subj. 1864:11129685
    [Google Scholar]
  144. 144.
    Yoshiga T, Hernandez VP, Fallon AM, Law JH. 1997. Mosquito transferrin, an acute-phase protein that is up-regulated upon infection. PNAS 94:2312337–42
    [Google Scholar]
  145. 145.
    Yu Y, Wu A, Zhang Z, Yan G, Zhang F et al. 2013. Characterization of the GufA subfamily member SLC39A11/Zip11 as a zinc transporter. J. Nutr. Biochem. 24:101697–708
    [Google Scholar]
  146. 146.
    Zhang X, Sato M, Sasahara M, Migita CT, Yoshida T. 2004. Unique features of recombinant heme oxygenase of Drosophila melanogaster compared with those of other heme oxygenases studied. Eur. J. Biochem. 271:91713–24
    [Google Scholar]
  147. 147.
    Zhao M, Zhou B. 2020. A distinctive sequence motif in the fourth transmembrane domain confers ZIP13 iron function in Drosophila melanogaster. Biochim. Biophys. Acta Mol. Cell Res. 1867:2118607
    [Google Scholar]
  148. 148.
    Zhou G, Kohlhepp P, Geiser D, Frasquillo MDC, Vazquez-Moreno L, Winzerling JJ. 2007. Fate of blood meal iron in mosquitoes. J. Insect Physiol. 53:111169–78
    [Google Scholar]
/content/journals/10.1146/annurev-ento-040622-092836
Loading
/content/journals/10.1146/annurev-ento-040622-092836
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error