Low intracellular iron increases the stability of Matriptase-2

Journal of Biological Chemistry

Volumn 290, Issue 7, 2015, Pages 4432-4446

  Zhao, Ningning ^a   Nizzi, Christopher P ^b   Anderson, Sheila A ^b   Wang, Jiaohong ^c   Ueno, Akiko ^c   Tsukamoto, Hidekazu ^c,d   Eisenstein, Richard S ^b   Enns, Caroline A ^a   Zhang, An Sheng ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

CELLULAR IRONS; CYTOPLASMIC DOMAINS; HEPATOCYTES; HEPCIDIN; INTRACELLULAR IRON; IRON DEPLETION; IRON HOMEOSTASIS; MATRIPTASE;

IRON;

BONE MORPHOGENETIC PROTEIN; HEPCIDIN; IRON; MATRIPTASE; MATRIPTASE 2; MESSENGER RNA; UNCLASSIFIED DRUG; HFE2 PROTEIN, MOUSE; MEMBRANE PROTEIN; SERINE PROTEINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BMP6 GENE; CELL LEVEL; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; ENZYME STABILITY; GENE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; ID1 GENE; INTERNALIZATION; IRON DEFICIENCY; IRON DEPLETION; LIVER CELL; MALE; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; RAT; SIGNAL TRANSDUCTION; TMPRSS6 GENE; TRANSLATION REGULATION; ANIMAL; BIOTINYLATION; CELL CULTURE; CHEMISTRY; CYTOLOGY; DEFICIENCY; ENZYME IMMUNOASSAY; GENETICS; HEPG2 CELL LINE; HOMEOSTASIS; HUMAN; IMMUNOPRECIPITATION; KNOCKOUT MOUSE; LIVER; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BIOTINYLATION; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEINS; CELLS, CULTURED; GENE EXPRESSION REGULATION; HEP G2 CELLS; HEPATOCYTES; HOMEOSTASIS; HUMANS; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; IRON; LIVER; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; RATS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 84922789739     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.611913     Document Type: Article

References (53)

1. De Domenico, I., Nemeth, E., Nelson, J. M., Phillips, J. D., Ajioka, R. S., Kay, M. S., Kushner, J. P., Ganz, T., Ward, D. M., and Kaplan, J. (2008) The hepcidin-binding site on ferroportin is evolutionarily conserved. Cell Metab. 8, 146-156
2. Ganz, T., and Nemeth, E. (2012) Hepcidin and iron homeostasis. Biochim. Biophys. Acta 1823, 1434-1443
3. Nemeth, E., Tuttle, M. S., Powelson, J., Vaughn, M. B., Donovan, A., Ward, D. M., Ganz, T., and Kaplan, J. (2004) Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306, 2090-2093
4. Roetto, A., Papanikolaou, G., Politou, M., Alberti, F., Girelli, D., Christakis, J., Loukopoulos, D., and Camaschella, C. (2003) Mutant antimicrobial peptide hepcidin is associated with severe juvenile hemochromatosis. Nat. Genet. 33, 21-22
5. Weinstein, D. A., Roy, C. N., Fleming, M. D., Loda, M. F., Wolfsdorf, J. I., and Andrews, N. C. (2002) Inappropriate expression of hepcidin is associated with iron refractory anemia: implications for the anemia of chronic disease. Blood 100, 3776-3781
6. Huang, F. W., Pinkus, J. L., Pinkus, G. S., Fleming, M. D., and Andrews, N. C. (2005) A mouse model of juvenile hemochromatosis. J. Clin. Invest. 115, 2187-2191
7. Niederkofler, V., Salie, R., and Arber, S. (2005) Hemojuvelin is essential for dietary iron sensing, and its mutation leads to severe iron overload. J. Clin. Invest. 115, 2180-2186
8. Meynard, D., Kautz, L., Darnaud, V., Canonne-Hergaux, F., Coppin, H., and Roth, M. P. (2009) Lack of the bone morphogenetic protein BMP6 induces massive iron overload. Nat. Genet. 41, 478-481
9. Andriopoulos, B., Jr., Corradini, E., Xia, Y., Faasse, S. A., Chen, S., Grgurevic, L., Knutson, M. D., Pietrangelo, A., Vukicevic, S., Lin, H. Y., and Babitt, J. L. (2009) BMP6 is a key endogenous regulator of hepcidin expression and iron metabolism. Nat. Genet. 41, 482-487
10. Steinbicker, A. U., Bartnikas, T. B., Lohmeyer, L. K., Leyton, P., Mayeur, C., Kao, S. M., Pappas, A. E., Peterson, R. T., Bloch, D. B., Yu, P. B., Fleming, M. D., and Bloch, K. D. (2011) Perturbation of hepcidin expression by BMP type I receptor deletion induces iron overload in mice. Blood 118, 4224-4230
11. Lee, D. H., Zhou, L. J., Zhou, Z., Xie, J. X., Jung, J. U., Liu, Y., Xi, C. X., Mei, L., and Xiong, W. C. (2010) Neogenin inhibits HJV secretion and regulates BMP-induced hepcidin expression and iron homeostasis. Blood 115, 3136-3145
12. Babitt, J. L., and Lin, H. Y. (2011) The molecular pathogenesis of hereditary hemochromatosis. Semin. Liver Dis. 31, 280-292
13. Finberg, K. E., Heeney, M. M., Campagna, D. R., Aydinok, Y., Pearson, H. A., Hartman, K. R., Mayo, M. M., Samuel, S. M., Strouse, J. J., Markianos, K., Andrews, N. C., and Fleming, M. D. (2008) Mutations in TMPRSS6 cause iron-refractory iron deficiency anemia (IRIDA). Nat. Genet. 40, 569-571
14. Folgueras, A. R., de Lara, F. M., Pendás, A. M., Garabaya, C., Rodríguez, F., Astudillo, A., Bernal, T., Cabanillas, R., López-Otín, C., and Velasco, G. (2008) The membrane-bound serine protease matriptase-2 (Tmprss6) is an essential regulator of iron homeostasis. Blood 112, 2539-2545
15. Du, X., She, E., Gelbart, T., Truksa, J., Lee, P., Xia, Y., Khovananth, K., Mudd, S., Mann, N., Moresco, E. M., Beutler, E., and Beutler, B. (2008) The serine protease TMPRSS6 is required to sense iron deficiency. Science 320, 1088-1092
16. Velasco, G., Cal, S., Quesada, V., Sánchez, L. M., and López-Otín, C. (2002) Matriptase-2, a membrane-bound mosaic serine proteinase predominantly expressed in human liver and showing degrading activity against extracellular matrix proteins. J. Biol. Chem. 277, 37637-37646
17. Zhang, A. S., Anderson, S. A., Wang, J., Yang, F., DeMaster, K., Ahmed, R., Nizzi, C. P., Eisenstein, R. S., Tsukamoto, H., and Enns, C. A. (2011) Suppression of hepatic hepcidin expression in response to acute iron deprivation is associated with an increase of matripatase-2 protein. Blood 117, 1687-1699
18. Ramsay, A. J., Hooper, J. D., Folgueras, A. R., Velasco, G., and López-Otín, C. (2009) Matriptase-2 (TMPRSS6): a proteolytic regulator of iron homeostasis. Haematologica 94, 840-849
19. Béliveau, F., Brulé, C., Désilets, A., Zimmerman, B., Laporte, S. A., Lavoie, C. L., and Leduc, R. (2011) Essential role of endocytosis of the type II transmembrane serine protease TMPRSS6 in regulating its functionality. J. Biol. Chem. 286, 29035-29043
20. Silvestri, L., Pagani, A., Nai, A., De Domenico, I., Kaplan, J., and Camaschella, C. (2008) The serine protease matriptase-2 (TMPRSS6) inhibits hepcidin activation by cleaving membrane hemojuvelin. Cell Metab. 8, 502-511
21. Zhang, A. S., West, A. P., Jr., Wyman, A. E., Bjorkman, P. J., and Enns, C. A. (2005) Interaction of hemojuvelin with neogenin results in iron accumulation in human embryonic kidney 293 cells. J. Biol. Chem. 280, 33885-33894
22. Papanikolaou, G., Samuels, M. E., Ludwig, E. H., MacDonald, M. L., Franchini, P. L., Dubé, M. P., Andres, L., MacFarlane, J., Sakellaropoulos, N., Politou, M., Nemeth, E., Thompson, J., Risler, J. K., Zaborowska, C., Babakaiff, R., Radomski, C. C., Pape, T. D., Davidas, O., Christakis, J., Brissot, P., Lockitch, G., Ganz, T., Hayden, M. R., and Goldberg, Y. P. (2004) Mutations in HFE2 cause iron overload in chromosome 1q-linked juvenile hemochromatosis. Nat. Genet. 36, 77-82
23. Zhang, A. S., Yang, F., Wang, J., Tsukamoto, H., and Enns, C. A. (2009) Hemojuvelin-neogenin interaction is required for bone morphogenic protein- 4-induced hepcidin expression. J. Biol. Chem. 284, 22580-22589
24. Babitt, J. L., Huang, F. W., Wrighting, D. M., Xia, Y., Sidis, Y., Samad, T. A., Campagna, J. A., Chung, R. T., Schneyer, A. L., Woolf, C. J., Andrews, N. C., and Lin, H. Y. (2006) Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat. Genet. 38, 531-539
25. Chen, W., Huang, F. W., de Renshaw, T. B., and Andrews, N. C. (2011) Skeletal muscle hemojuvelin is dispensable for systemic iron homeostasis. Blood 117, 6319-6325
26. Finberg, K. E., Whittlesey, R. L., Fleming, M. D., and Andrews, N. C. (2010) Downregulation of Bmp/Smad signaling by Tmprss6 is required for maintenance of systemic iron homeostasis. Blood 115, 3817-3826
27. Meynard, D., Vaja, V., Sun, C. C., Corradini, E., Chen, S., López-Otín, C., Grgurevic, L., Hong, C. C., Stirnberg, M., Gütschow, M., Vukicevic, S., Babitt, J. L., and Lin, H. Y. (2011) Regulation of TMPRSS6 by BMP6 and iron in human cells and mice. Blood 118, 747-756
28. Enns, C. A., Ahmed, R., and Zhang, A. S. (2012) Neogenin interacts with matriptase-2 to facilitate hemojuvelin cleavage. J. Biol. Chem. 287, 35104-35117
29. Zhao, N., Gao, J., Enns, C. A., and Knutson, M. D. (2010) ZRT/IRT-like protein 14 (ZIP14) promotes the cellular assimilation of iron from transferrin. J. Biol. Chem. 285, 32141-32150
30. Uhles, S., Moede, T., Leibiger, B., Berggren, P. O., and Leibiger, I. B. (2007) Selective gene activation by spatial segregation of insulin receptor B signaling. FASEB J. 21, 1609-1621
31. Zhang, A. S., Anderson, S. A., Meyers, K. R., Hernandez, C., Eisenstein, R. S., and Enns, C. A. (2007) Evidence that inhibition of hemojuvelin shedding in response to iron is mediated through neogenin. J. Biol. Chem. 282, 12547-12556
32. Anderson, S. A., Nizzi, C. P., Chang, Y. I., Deck, K. M., Schmidt, P. J., Galy, B., Damnernsawad, A., Broman, A. T., Kendziorski, C., Hentze, M. W., Fleming, M. D., Zhang, J., and Eisenstein, R. S. (2013) The IRP1-HIF-2' axis coordinates iron and oxygen sensing with erythropoiesis and iron absorption. Cell Metab. 17, 282-290
33. Anthony, T. G., Anthony, J. C., Yoshizawa, F., Kimball, S. R., and Jefferson, L. S. (2001) Oral administration of leucine stimulates ribosomal protein mRNA translation but not global rates of protein synthesis in the liver of rats. J. Nutr. 131, 1171-1176
34. Zhang, A. S., Gao, J., Koeberl, D. D., and Enns, C. A. (2010) The role of hepatocyte hemojuvelin in the regulation of bone morphogenic protein-6 and hepcidin expression in vivo. J. Biol. Chem. 285, 16416-16423
35. Enns, C. A., Ahmed, R., Wang, J., Ueno, A., Worthen, C., Tsukamoto, H., and Zhang, A. S. (2013) Increased iron loading induces Bmp6 expression in the non-parenchymal cells of the liver independent of the BMP-signaling pathway. PloS one 8, e60534
36. Maxson, J. E., Chen, J., Enns, C. A., and Zhang, A. S. (2010) Matriptase-2- and proprotein convertase-cleaved forms of hemojuvelin have different roles in the down-regulation of hepcidin expression. J. Biol. Chem. 285, 39021-39028
37. Young, S. P., Fahmy, M., and Golding, S. (1997) Ceruloplasmin, transferrin and apotransferrin facilitate iron release from human liver cells. FEBS Lett. 411, 93-96
38. Baker, E., Page, M., and Morgan, E. H. (1985) Transferrin and iron release from rat hepatocytes in culture. Am. J. Physiol. 248, G93-G97
39. Li, H., Rybicki, A. C., Suzuka, S. M., von Bonsdorff, L., Breuer, W., Hall, C. B., Cabantchik, Z. I., Bouhassira, E. E., Fabry, M. E., and Ginzburg, Y. Z. (2010) Transferrin therapy ameliorates disease in β-thalassemic mice. Nat. Med. 16, 177-182
40. Stirnberg, M., Maurer, E., Horstmeyer, A., Kolp, S., Frank, S., Bald, T., Arenz, K., Janzer, A., Prager, K., Wunderlich, P., Walter, J., and Gütschow, M. (2010) The proteolytic processing of the serine protease matriptase-2: identification of the cleavage sites required for its autocatalytic release from the cell surface. Biochem. J. 430, 87-95
41. Zhao, N., Zhang, A. S., Worthen, C., Knutson, M. D., and Enns, C. A. (2014) An iron-regulated and glycosylation-dependent proteasomal degradation pathway for the plasma membrane metal transporter ZIP14. Proc. Natl. Acad. Sci. U.S.A. 111, 9175-9180
42. Hentze, M. W., Muckenthaler, M. U., Galy, B., and Camaschella, C. (2010) Two to tango: regulation of mammalian iron metabolism. Cell 142, 24-38
43. Chen, O. S., Blemings, K. P., Schalinske, K. L., and Eisenstein, R. S. (1998) Dietary iron intake rapidly influences iron regulatory proteins, ferritin subunits and mitochondrial aconitase in rat liver. J. Nutr. 128, 525-535
44. Chen, O. S., Schalinske, K. L., and Eisenstein, R. S. (1997) Dietary iron intake modulates the activity of iron regulatory proteins and the abundance of ferritin and mitochondrial aconitase in rat liver. J. Nutr. 127, 238-248
45. Schalinske, K. L., and Eisenstein, R. S. (1996) Phosphorylation and activation of both iron regulatory proteins 1 and 2 in HL-60 cells. J. Biol. Chem. 271, 7168-7176
46. Zhao, N., Zhang, A. S., and Enns, C. A. (2013) Iron regulation by hepcidin. J. Clin. Invest. 123, 2337-2343
47. Nai, A., Pagani, A., Silvestri, L., and Camaschella, C. (2010) Increased susceptibility to iron deficiency of Tmprss6-haploinsufficient mice. Blood 116, 851-852
48. Maurer, E., Gütschow, M., and Stirnberg, M.(2013) Hepatocyte growth factor activator inhibitor type 2 (HAI-2) modulates hepcidin expression by inhibiting the cell surface protease matriptase-2. Biochem. J. 450, 583-593
49. Zhao, B., Yuan, C., Li, R., Qu, D., Huang, M., and Ngo, J. C. (2013) Crystal structures of matriptase in complex with its inhibitor hepatocyte growth factor activator inhibitor-1. J. Biol. Chem. 288, 11155-11164
50. Szabo, R., Hobson, J. P., Christoph, K., Kosa, P., List, K., and Bugge, T. H. (2009) Regulation of cell surface protease matriptase by HAI2 is essential for placental development, neural tube closure and embryonic survival in mice. Development 136, 2653-2663
51. Larsen, B. R., Steffensen, S. D., Nielsen, N. V., Friis, S., Godiksen, S., Bornholdt, J., Soendergaard, C., Nonboe, A. W., Andersen, M. N., Poulsen, S. S., Szabo, R., Bugge, T. H., Lin, C. Y., Skovbjerg, H., Jensen, J. K., and Vogel, L. K. (2013) Hepatocyte growth factor activator inhibitor-2 prevents shedding of matriptase. Exp. Cell Res. 319, 918-929
52. Parr, C., Sanders, A. J., and Jiang, W. G. (2010) Hepatocyte growth factor activation inhibitors- therapeutic potential in cancer. Anticancer Agents Med. Chem. 10, 47-57
53. Gkouvatsos, K., Wagner, J., Papanikolaou, G., Sebastiani, G., and Pantopoulos, K. (2011) Conditional disruption of mouse HFE2 gene: maintenance of systemic iron homeostasis requires hepatic but not skeletal muscle hemojuvelin. Hepatology 54, 1800-1807