The actin-binding protein profilin 2 is a novel regulator of iron homeostasis

Blood

Volumn 130, Issue 17, 2017, Pages 1934-1945

  Luscieti, Sara ^a,b   Galy, Bruno ^c   Gutierrez, Lucia ^d   Reinke, Michael ^e   Couso, Jorge ^a,b   Shvartsman, Maya ^a   Di Pascale, Antonio ^f   Witke, Walter ^e   Hentze, Matthias W ^g   Pilo Boyl, Pietro ^e   Sanchez, Mayka ^a,b  

^a Germans Trias i Pujol Health Research Institute   (Spain)

^b JOSEP CARRERAS LEUKAEMIA RESEARCH INSTITUTE IJC   (Spain)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d INSTITUTO DE CIENCIA DE MATERIALES DE MADRID   (Spain)

^e UNIVERSITY OF BONN   (Germany)

^f UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^g EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; FERRITIN; FERROPORTIN; HEPCIDIN; IRON; MESSENGER RNA; PROFILIN 2; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; IRON REGULATORY FACTOR; PROFILIN; PROTEIN BINDING; REACTIVE OXYGEN METABOLITE;

3' UNTRANSLATED REGION; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BIOINFORMATICS; CONTROLLED STUDY; DUODENUM; ENDOCYTOSIS; GEL MOBILITY SHIFT ASSAY; GENETIC CONSERVATION; HELA CELL LINE; HEMATOPOIESIS; HEPA 1-6 CELL LINE; HIPPOCAMPUS; IN VIVO STUDY; INFLAMMATION; IRON HOMEOSTASIS; IRON METABOLISM; IRON RESPONSIVE ELEMENT; IRON STORAGE; MESENCEPHALON; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; ANIMAL; ANTIBODY SPECIFICITY; BIOLOGICAL MODEL; C57BL MOUSE; CELL LINE; DNA RESPONSIVE ELEMENT; GENETICS; HOMEOSTASIS; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CELL LINE; DUODENUM; HELA CELLS; HOMEOSTASIS; HUMANS; IRON; IRON-REGULATORY PROTEINS; MICE, INBRED C57BL; MODELS, BIOLOGICAL; ORGAN SPECIFICITY; PROFILINS; PROTEIN BINDING; REACTIVE OXYGEN SPECIES; RESPONSE ELEMENTS; RNA, MESSENGER;

EID: 85032500638     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-11-754382     Document Type: Article

References (50)

1. Hentze MW, Muckenthaler MU, Galy B, Camaschella C. Two to tango: Regulation of Mammalian iron metabolism. Cell. 2010;142(1): 24-38.
2. Anderson CP, Shen M, Eisenstein RS, Leibold EA. Mammalian iron metabolism and its control by iron regulatory proteins. Biochim Biophys Acta. 2012;1823(9):1468-1483.
3. Sanchez M, Galy B, Muckenthaler MU, Hentze MW. Iron-regulatory proteins limit hypoxiainducible factor-2alpha expression in iron deficiency. Nat Struct Mol Biol. 2007;14(5): 420-426.
4. Gunshin H, Allerson CR, Polycarpou-Schwarz M, et al. Iron-dependent regulation of the divalent metal ion transporter. FEBS Lett. 2001;509(2): 309-316.
5. McKie AT, Marciani P, Rolfs A, et al. A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol Cell. 2000;5(2):299-309.
6. Walden WE, Selezneva AI, Dupuy J, et al. Structure of dual function iron regulatory protein 1 complexed with ferritin IRE-RNA. Science. 2006; 314(5807):1903-1908.
7. Wilkinson N, Pantopoulos K. The IRP/IRE system in vivo: Insights from mouse models. Front Pharmacol. 2014;5:176.
8. Joshi RS, Moran E, Sanchez M. Cellular iron metabolism-the IRP/IRE regulatory network. In: Sarika Arora, ed. Iron Metabolism. Rijeka, Croatia: InTech; 2012.
9. Yoshinaga M, Nakatsuka Y, Vandenbon A, et al. Regnase-1 maintains iron homeostasis via the degradation of transferrin receptor 1 and prolylhydroxylase-domain-containing protein 3 mRNAs. Cell Reports. 2017;19(8):1614-1630.
10. Galy B, Ferring D, Hentze MW. Generation of conditional alleles of the murine Iron Regulatory Protein (IRP)-1 and -2 genes. Genesis. 2005; 43(4):181-188.
11. Smith SR, Ghosh MC, Ollivierre-Wilson H, Hang Tong W, Rouault TA. Complete loss of iron regulatory proteins 1 and 2 prevents viability of murine zygotes beyond the blastocyst stage of embryonic development. Blood Cells Mol Dis. 2006;36(2):283-287.
12. Galy B, Ferring-Appel D, Becker C, et al. Iron regulatory proteins control a mucosal block to intestinal iron absorption. Cell Reports. 2013;3(3): 844-857.
13. Galy B, Ferring-Appel D, Kaden S, Gröne HJ, Hentze MW. Iron regulatory proteins are essential for intestinal function and control key iron absorption molecules in the duodenum. Cell Metab. 2008;7(1):79-85.
14. Galy B, Ferring-Appel D, Sauer SW, et al. Iron regulatory proteins secure mitochondrial iron sufficiency and function. Cell Metab. 2010;12(2): 194-201.
15. Nairz M, Ferring-Appel D, Casarrubea D, et al. Iron regulatory proteins mediate host resistance to salmonella infection. Cell Host Microbe. 2015; 18(2):254-261.
16. Moroishi T, Nishiyama M, Takeda Y, Iwai K, Nakayama KI. The FBXL5-IRP2 axis is integral to control of iron metabolism in vivo. Cell Metab. 2011;14(3):339-351.
17. Casarrubea D, Viatte L, Hallas T, et al. Abnormal body iron distribution and erythropoiesis in a novel mouse model with inducible gain of iron regulatory protein (IRP)-1 function. J Mol Med (Berl). 2013; 91(7):871-881.
18. Sanchez M, Galy B, Schwanhaeusser B, et al. Iron regulatory protein-1 and -2: Transcriptomewide definition of binding mRNAs and shaping of the cellular proteome by iron regulatory proteins. Blood. 2011;118(22):e168-e179.
19. Witke W. The role of profilin complexes in cell motility and other cellular processes. Trends Cell Biol. 2004;14(8):461-469.
20. Damke H, Binns DD, Ueda H, Schmid SL, Baba T. Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol Biol Cell. 2001;12(9): 2578-2589.
21. Ferguson SM, Brasnjo G, Hayashi M, et al. A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science. 2007;316(5824):570-574.
22. Witke W, Podtelejnikov AV, Di Nardo A, et al. In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly. EMBO J. 1998;17(4):967-976.
23. Gareus R, Di Nardo A, Rybin V, Witke W. Mouse profilin 2 regulates endocytosis and competes with SH3 ligand binding to dynamin 1. J Biol Chem. 2006;281(5):2803-2811.
24. Pilo Boyl P, Di Nardo A, Mulle C, et al. Profilin2 contributes to synaptic vesicle exocytosis, neuronal excitability, and novelty-seeking behavior. EMBO J. 2007;26(12):2991-3002.
25. Gray NK, Quick S, Goossen B, et al. Recombinant iron-regulatory factor functions as an ironresponsive-element-binding protein, a translational repressor and an aconitase. A functional assay for translational repression and direct demonstration of the iron switch. Eur J Biochem. 1993;218(2):657-667.
26. Sanchez M, Galy B, Dandekar T, et al. Iron regulation and the cell cycle: Identification of an iron-responsive element in the 39-untranslated region of human cell division cycle 14A mRNA by a refined microarray-based screening strategy. J Biol Chem. 2006;281(32):22865-22874.
27. Luscieti S, Tolle G, Aranda J, et al. Novel mutations in the ferritin-L iron-responsive element that only mildly impair IRP binding cause hereditary hyperferritinaemia cataract syndrome. Orphanet J Rare Dis. 2013;8:30.
28. Liu Z, Lanford R, Mueller S, et al. Siderophoremediated iron trafficking in humans is regulated by iron. J Mol Med (Berl). 2012;90(10):1209-1221.
29. Epsztejn S, Kakhlon O, Glickstein H, Breuer W, Cabantchik I. Fluorescence analysis of the labile iron pool of mammalian cells. Anal Biochem. 1997;248(1):31-40.
30. Santamaria R, Irace C, Festa M, Maffettone C, Colonna A. Induction of ferritin expression by oxalomalate. Biochim Biophys Acta. 2004; 1691(2-3):151-159.
31. Torrance JD, Bothwell TH. A simple technique for measuring storage iron concentrations in formalinised liver samples. S Afr J Med Sci. 1968; 33(1):9-11.
32. Patel BN, Dunn RJ, Jeong SY, Zhu Q, Julien JP, David S. Ceruloplasmin regulates iron levels in the CNS and prevents free radical injury. J Neurosci. 2002;22(15):6578-6586.
33. Gutiérrez L, Quintana C, Patiño C, et al. Iron speciation study in Hfe knockout mice tissues: Magnetic and ultrastructural characterisation. Biochim Biophys Acta. 2009;1792(6):541-547.
34. Meguro R, Asano Y, Iwatsuki H, Shoumura K. Perfusion-Perls and -Turnbull methods supplemented by DAB intensification for nonheme iron histochemistry: Demonstration of the superior sensitivity of the methods in the liver, spleen, and stomach of the rat. Histochem Cell Biol. 2003; 120(1):73-82.
35. Rodrigues PN, Gomes SS, Neves JV, et al. Mycobacteria-induced anaemia revisited: A molecular approach reveals the involvement of NRAMP1 and lipocalin-2, but not of hepcidin. Immunobiology. 2011;216(10):1127-1134.
36. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:3.
37. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Series B. 1995; 57(1):289-300.
38. Sanchez M, Galy B, Hentze MW, Muckenthaler MU. Identification of target mRNAs of regulatory RNA-binding proteins using mRNP immunopurification and microarrays. Nat Protoc. 2007;2(8):2033-2042.
39. Campillos M, Cases I, Hentze MW, Sanchez M. SIREs: Searching for iron-responsive elements. Nucleic Acids Res. 2010;38(Web Server issue): W360-367.
40. Di Nardo A, Gareus R, Kwiatkowski D, Witke W. Alternative splicing of the mouse profilin II gene generates functionally different profilin isoforms. J Cell Sci. 2000;113(Pt 21):3795-3803.
41. Lambrechts A, Braun A, Jonckheere V, et al. Profilin II is alternatively spliced, resulting in profilin isoforms that are differentially expressed and have distinct biochemical properties. Mol Cell Biol. 2000;20(21):8209-8219.
42. Quintana C, Gutiérrez L. Could a dysfunction of ferritin be a determinant factor in the aetiology of some neurodegenerative diseases?. Biochim Biophys Acta. 2010;1800(8):770-782.
43. Whitnall M, Suryo Rahmanto Y, Huang ML, et al. Identification of nonferritin mitochondrial iron deposits in a mouse model of Friedreich ataxia. Proc Natl Acad Sci USA. 2012;109(50): 20590-20595.
44. Nemeth E, Rivera S, Gabayan V, et al. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest. 2004;113(9): 1271-1276.
45. Devireddy LR, Gazin C, Zhu X, Green MR. A cellsurface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell. 2005; 123(7):1293-1305.
46. Bao G, Clifton M, Hoette TM, et al. Iron traffics in circulation bound to a siderocalin (Ngal)-catechol complex. Nat Chem Biol. 2010;6(8):602-609.
47. Hubert N, Hentze MW. Previously uncharacterized isoforms of divalent metal transporter (DMT)-1: Implications for regulation and cellular function. Proc Natl Acad Sci USA. 2002;99(19):12345-12350.
48. van der Bliek AM, Redelmeier TE, Damke H, Tisdale EJ, Meyerowitz EM, Schmid SL. Mutations in human dynamin block an intermediate stage in coated vesicle formation. J Cell Biol. 1993;122(3):553-563.
49. Chen C, Garcia-Santos D, Ishikawa Y, et al. Snx3 regulates recycling of the transferrin receptor and iron assimilation. Cell Metab. 2013;17(3):343-352.
50. Lim JE, Jin O, Bennett C, et al. A mutation in Sec15l1 causes anemia in hemoglobin deficit (hbd) mice. Nat Genet. 2005;37(11):1270-1273.