Prion protein promotes kidney iron uptake via its ferrireductase activity

Journal of Biological Chemistry

Volumn 290, Issue 9, 2015, Pages 5512-5522

  Haldar, Swati ^a   Tripathi, Ajai ^a   Qian, Juan ^a   Beserra, Amber ^a   Suda, Srinivas ^a   McElwee, Matthew ^a   Turner, Jerrold ^c   Hopfer, Ulrich ^b   Singh, Neena ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; NEURODEGENERATIVE DISEASES; PROTEINS;

GASTRIC GAVAGE; INTRACELLULAR VESICLES; INTRAPERITONEALLY; IRON HOMEOSTASIS; IRON METABOLISM; NEURODEGENERATIVE; PROXIMAL TUBULES; TRANSEPITHELIAL TRANSPORT;

IRON;

FERRIREDUCTASE; HEMIN; IRON 59; MUTANT PROTEIN; PRION PROTEIN; REGULATOR PROTEIN; TRANSFERRIN; UNCLASSIFIED DRUG; FERRIC CITRATE IRON REDUCTASE; FLAVINE MONONUCLEOTIDE REDUCTASE; IRON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL IMMORTALIZATION; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFICIENCY; EPITHELIUM CELL; GLOMERULUS FILTRATION; IN VITRO STUDY; IN VIVO STUDY; IRON METABOLISM; IRON TRANSPORT; KIDNEY EPITHELIUM; KIDNEY METABOLISM; KIDNEY PROXIMAL TUBULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; ANIMAL; CONFOCAL MICROSCOPY; CYTOLOGY; FEMALE; GENETICS; ION TRANSPORT; KIDNEY; KNOCKOUT MOUSE; MALE; METABOLISM; TRANSFORMED CELL LINE; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TRANSFORMED; CELL MEMBRANE; FEMALE; FMN REDUCTASE; ION TRANSPORT; IRON; IRON RADIOISOTOPES; KIDNEY; KIDNEY TUBULES, PROXIMAL; MALE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; PRPC PROTEINS; TRANSFERRIN;

EID: 84923913689     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.607507     Document Type: Article

References (51)

1. Aguzzi, A., Nuvolone, M., and Zhu, C. (2013) The immunobiology of prion diseases. Nat. Rev. Immunol. 13, 888-902
2. Ashe, K. H., and Aguzzi, A. (2013) Prions, prionoids, and pathogenic proteins in Alzheimer disease. Prion. 7, 55-59
3. Singh, N. (2014) The role of iron in prion disease and other neurodegenerative diseases. PLoS Pathog. 10, e1004335
4. Singh, N., Haldar, S., Tripathi, A. K., Horback, K., Wong, J., Sharma, D., Beserra, A., Suda, S., Anbalagan, C., Dev, S., Mukhopadhyay, C. K., and Singh, A. (2014) Brain iron homeostasis: from molecular mechanisms to clinical significance and therapeutic opportunities. Antioxid. Redox. Signal. 20, 1324-1363
5. Singh, A., Haldar, S., Horback, K., Tom, C., Zhou, L., Meyerson, H., and Singh, N. (2013) Prion protein regulates iron transport by functioning as a ferrireductase. J. Alzheimers Dis. 35, 541-552
6. Smith, C. P., and Thévenod, F. (2009) Iron transport and the kidney. Biochim. Biophys. Acta 1790, 724-730
7. Wareing, M., Ferguson, C. J., Green, R., Riccardi, D., and Smith, C. P. (2000) In vivo characterization of renal iron transport in the anaesthetized rat. J. Physiol. 524, 581-586
8. Martines, A. M., Masereeuw, R., Tjalsma, H., Hoenderop, J. G., Wetzels, J. F., and Swinkels, D. W. (2013) Iron metabolism in the pathogenesis of iron-induced kidney injury. Nat. Rev. Nephrol. 9, 385-398
9. Kozyraki, R., Fyfe, J., Verroust, P. J., Jacobsen, C., Dautry-Varsat, A., Gburek, J., Willnow, T. E., Christensen, E. I., and Moestrup, S. K. (2001) Mega-lin-dependent cubilin-mediated endocytosis is a major pathway for the apical uptake of transferrin in polarized epithelia. Proc. Natl. Acad. Sci. U.S.A. 98, 12491-12496
10. Moulouel, B., Houamel, D., Delaby, C., Tchernitchko, D., Vaulont, S., Letteron, P., Thibaudeau, O., Puy, H., Gouya, L., Beaumont, C., and Karim, Z. (2013) Hepcidin regulates intrarenal iron handling at the distal nephron. Kidney Int. 84, 756-766
11. Zhang, D., Meyron-Holtz, E., and Rouault, T. A. (2007) Renal iron metabolism: transferrin iron delivery and the role of iron regulatory proteins. J. Am. Soc. Nephrol. 18, 401-406
12. McKie, A. T. (2008) The role of Dcytb in iron metabolism: an update. Biochem. Soc. Trans. 36, 1239-1241
13. Ohgami, R. S., Campagna, D. R., McDonald, A., and Fleming, M. D. (2006) The Steap proteins are metalloreductases. Blood 108, 1388-1394
14. Abbaspour, N., Hurrell, R., and Kelishadi, R. (2014) Review on iron and its importance for human health. J. Res. Med. Sci. 19, 164-174
15. Fournier, J. G., Escaig-Haye, F., Billette de Villemeur, T., Robain, O., Lasmézas, C. I., Deslys, J. P., Dormont, D., and Brown, P. (1998) Distribution and submicroscopic immunogold localization of cellular prion protein (PrPc) in extracerebral tissues. Cell Tissue Res. 292, 77-84
16. Peralta, O. A., and Eyestone, W. H. (2009) Quantitative and qualitative analysis of cellular prion protein (PrP(C)) expression in bovine somatic tissues. Prion 3, 161-170
17. Dagdanova, A., Ilchenko, S., Notari, S., Yang, Q., Obrenovich, M. E., Hatcher, K., McAnulty, P., Huang, L., Zou, W., Kong, Q., Gambetti, P., and Chen, S. G. (2010) Characterization of the prion protein in human urine. J. Biol. Chem. 285, 30489-30495
18. Narang, H. K., Dagdanova, A., Xie, Z., Yang, Q., and Chen, S. G. (2005) Sensitive detection of prion protein in human urine. Exp. Biol. Med. (Maywood) 230, 343-349
19. Van Dorsselaer, A., Carapito, C., Delalande, F., Schaeffer-Reiss, C., Thierse, D., Diemer, H., McNair, D. S., Krewski, D., and Cashman, N. R. (2011) Detection of prion protein in urine-derived injectable fertility products by a targeted proteomic approach. PLoS ONE 6, e17815
20. Chen, S. G., Teplow, D. B., Parchi, P., Teller, J. K., Gambetti, P., and Au-tilio-Gambetti, L. (1995) Truncated forms of the human prion protein in normal brain and in prion diseases. J. Biol. Chem. 270, 19173-19180
21. Parkin, E. T., Watt, N. T., Turner, A. J., and Hooper, N. M. (2004) Dual mechanisms for shedding of the cellular prion protein. J. Biol. Chem. 279, 11170-11178
22. Zhao, H., Klingeborn, M., Simonsson, M., and Linné, T. (2006) Proteolytic cleavage and shedding of the bovine prion protein in two cell culture systems. Virus Res. 115, 43-55
23. Büeler, H., Fischer, M., Lang, Y., Bluethmann, H., Lipp, H. P., DeArmond, S. J., Prusiner, S. B., Aguet, M., and Weissmann, C. (1992) Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356, 577-582
24. Woost, P. G., Kolb, R. J., Chang, C. H., Finesilver, M., Inagami, T., and Hopfer, U. (2007) Development of an AT2-deficient proximal tubule cell line for transport studies. In Vitro Cell Dev. Biol. Anim. 43, 352-360
25. Singh, A., Kong, Q., Luo, X., Petersen, R. B., Meyerson, H., and Singh, N. (2009) Prion protein (PrP) knock-out mice show altered iron metabolism: a functional role for PrP in iron uptake and transport. PLoS ONE 4, e6115
26. Craven, C. M., Alexander, J., Eldridge, M., Kushner, J. P., Bernstein, S., and Kaplan, J. (1987) Tissue distribution and clearance kinetics of non-trans-ferrin-bound iron in the hypotransferrinemic mouse: a rodent model for hemochromatosis. Proc. Natl. Acad. Sci. U.S.A. 84, 3457-3461
27. Das, D., Luo, X., Singh, A., Gu, Y., Ghosh, S., Mukhopadhyay, C. K., Chen, S. G., Sy, M. S., Kong, Q., and Singh, N. (2010) Paradoxical role of prion protein aggregates in redox-iron induced toxicity. PLoS ONE 5, e11420
28. Gu, Y., Hinnerwisch, J., Fredricks, R., Kalepu, S., Mishra, R. S., and Singh, N. (2003) Identification of cryptic nuclear localization signals in the prion protein. Neurobiol. Dis. 12, 133-149
29. Singh, A., Mohan, M. L., Isaac, A. O., Luo, X., Petrak, J., Vyoral, D., and Singh, N. (2009) Prion protein modulates cellular iron uptake: a novel function with implications for prion disease pathogenesis. PLoS ONE 4, e4468
30. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A. (2012) Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682
31. Mishra, R. S., Basu, S., Gu, Y., Luo, X., Zou, W. Q., Mishra, R., Li, R., Chen, S. G., Gambetti, P., Fujioka, H., and Singh, N. (2004) Protease-resistant human prion protein and ferritin are cotransported across Caco-2 epithelial cells: implications for species barrier in prion uptake from the intestine. J. Neurosci. 24, 11280-11290
32. Moriya, M., and Linder, M. C. (2006) Vesicular transport and apotransferrin in intestinal iron absorption, as shown in the Caco-2 cell model. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G301-G309
33. Gu, Y., Verghese, S., Mishra, R. S., Xu, X., Shi, Y., and Singh, N. (2003) Mutant prion protein-mediated aggregation of normal prion protein in the endoplasmic reticulum: implications for prion propagation and neurotoxicity. J. Neurochem. 84, 10-22
34. Nestel, F. P., Greene, R. N., Kichian, K., Ponka, P., and Lapp, W. S. (2000) Activation of macrophage cytostatic effector mechanisms during acute graft-versus-host disease: release of intracellular iron and nitric oxidemediated cytostasis. Blood 96, 1836-1843
35. Basu, S., Mohan, M. L., Luo, X., Kundu, B., Kong, Q., and Singh, N. (2007) Modulation of proteinase K-resistant prion protein in cells and infectious brain homogenate by redox iron: implications for prion replication and disease pathogenesis. Mol. Biol. Cell 18, 3302-3312
36. Lee, K. S., Raymond, L. D., Schoen, B., Raymond, G. J., Kett, L., Moore, R. A., Johnson, L. M., Taubner, L., Speare, J. O., Onwubiko, H. A., Baron, G. S., Caughey, W. S., and Caughey, B. (2007) Hemin interactions and alterations of the subcellular localization of prion protein. J. Biol. Chem. 282, 36525-36533
37. Singh, A., Qing, L., Kong, Q., and Singh, N. (2012) Change in the characteristics of ferritin induces iron imbalance in prion disease affected brains. Neurobiol. Dis. 45, 930-938
38. Abouhamed, M., Gburek, J., Liu, W., Torchalski, B., Wilhelm, A., Wolff, N. A., Christensen, E. I., Thévenod, F., and Smith, C. P. (2006) Divalent metal transporter 1 in the kidney proximal tubule is expressed in late endosomes/lysosomal membranes: implications for renal handling of pro-tein-metal complexes. Am. J. Physiol. Renal Physiol. 290, F1525-F1533
39. He, L., Girijashanker, K., Dalton, T. P., Reed, J., Li, H., Soleimani, M., and Nebert, D. W. (2006) ZIP8, member of the solute-carrier-39 (SLC39) met-al-transporter family: characterization of transporter properties. Mol. Pharmacol. 70, 171-180
40. Peters, P. J., Mironov, A., Jr., Peretz, D., van Donselaar, E., Leclerc, E., Erpel, S., DeArmond, S. J., Burton, D. R., Williamson, R. A., Vey, M., and Prusiner, S. B. (2003) Trafficking of prion proteins through a caveolaemediated endosomal pathway. J. Cell Biol. 162, 703-717
41. Caughey, B. (1991) In vitro expression and biosynthesis of prion protein. Curr. Top. Microbiol. Immunol. 172, 93-107
42. Mishra, R. S., Gu, Y., Bose, S., Verghese, S., Kalepu, S., and Singh, N. (2002) Cell surface accumulation of a truncated transmembrane prion protein in Gerstmann-Straussler-Scheinker disease P102L. J. Biol. Chem. 277, 24554-24561
43. Singh, N., Zanusso, G., Chen, S. G., Fujioka, H., Richardson, S., Gambetti, P., and Petersen, R. B. (1997) Prion protein aggregation reverted by low temperature in transfected cells carrying a prion protein gene mutation. J. Biol. Chem. 272, 28461-28470
44. Linder, M. C., Moriya, M., Whon, A., Kassa, A., and Gilley, C. (2006) Vesicular transport of Fe and interaction with other metal ions in polarized Caco2 cell monolayers. Biol. Res. 39, 143-156
45. Odorizzi, G., Pearse, A., Domingo, D., Trowbridge, I. S., and Hopkins, C. R. (1996) Apical and basolateral endosomes of MDCK cells are interconnected and contain a polarized sorting mechanism. J. Cell Biol. 135, 139-152
46. Wang, E., Brown, P. S., Aroeti, B., Chapin, S. J., Mostov, K. E., and Dunn, K. W. (2000) Apical and basolateral endocytic pathways of MDCK cells meet in acidic common endosomes distinct from a nearly-neutral apical recycling endosome. Traffic 1, 480-493
47. Aydinok, Y., Ulger, Z., Nart, D., Terzi, A., Cetiner, N., Ellis, G., Zimmermann, A., and Manz, C. (2007) A randomized controlled 1-year study of daily deferiprone plus twice weekly desferrioxamine compared with daily deferiprone monotherapy in patients with thalassemia major. Haematologica 92, 1599-1606
48. Christoforidis, A., Zevgaridou, E., Tsatra, I., Perifanis, V., Vlachaki, E., Papassotiriou, I., Apostolakou, F., and Athanassiou-Metaxa, M. (2007) Urinary iron excretion in young thalassemic patients receiving combined chelation treatment with deferoxamine and deferiprone. J. Pediatr. Hematol. Oncol. 29, 598-601
49. Sears, D. A., Anderson, P. R., Foy, A. L., Williams, H. L., and Crosby, W. H. (1966) Urinary iron excretion and renal metabolism of hemoglobin in hemolytic diseases. Blood 28, 708-725
50. Singh, A., Isaac, A. O., Luo, X., Mohan, M. L., Cohen, M. L., Chen, F., Kong, Q., Bartz, J., and Singh, N. (2009) Abnormal brain iron homeostasis in human and animal prion disorders. PLoS Pathog 5, e1000336
51. Zhang, X., and Lemasters, J. J. (2013) Translocation of iron from lysosomes to mitochondria during ischemia predisposes to injury after reperfusion in rat hepatocytes. Free Radic. Biol. Med. 63, 243-253