Selective binding of RGMc/hemojuvelin, a key protein in systemic iron metabolism, to BMP-2 and neogenin

American Journal of Physiology - Cell Physiology

Volumn 294, Issue 4, 2008, Pages

  Kuns Hashimoto, Robin ^a   Kuninger, David ^a   Nili, Mahta ^a   Rotwein, Peter ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Bone morphogenetic protein; Juvenile hemochromatosis; Repulsive guidance molecule

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; HEMOJUVELIN; HEPCIDIN; NEOGENIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING COMPETITION; CELL STRAIN COS7; CELL STRAIN HEK293; CONTROLLED STUDY; HEMOCHROMATOSIS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IRON METABOLISM; IRON OVERLOAD; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN ISOLATION; PROTEIN PURIFICATION; SURFACE PLASMON RESONANCE;

BONE MORPHOGENETIC PROTEINS; CELL LINE; CELL MEMBRANE; GENE EXPRESSION REGULATION; HEMOCHROMATOSIS; HUMANS; IRON; MEMBRANE PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN ISOFORMS; TRANSFORMING GROWTH FACTOR BETA;

EID: 41949115757     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00563.2007     Document Type: Article

References (48)

1. Andrews NC, Schmidt PJ. Iron homeostasis. Annu Rev Physiol 69: 69-85, 2007.
2. Babitt JL, Huang FW, Wrighting DM, Xia Y, Sidis Y, Samad TA, Campagna JA, Chung RT, Schneyer AL, Woolf CJ, Andrews NC, Lin HY. Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat Genet 38: 531-539, 2006.
3. Babitt JL, Huang FW, Xia Y, Sidis Y, Andrews NC, Lin HY. Modulation of bone morphogenetic protein signaling in vivo regulates systemic iron balance. J Clin Invest 117: 1933-1939. 2007.
4. Babitt JL, Zhang Y, Samad TA, Xia Y, Tang J, Campagna JA, Schneyer AL, Woolf CJ, Lin HY. Repulsive guidance molecule (RGMa), a DRAGON homologue, is a bone morphogenetic protein co-receptor. J Biol Chem 280: 29820-29827, 2005.
5. Bernet A, Mehlen P. Dependence receptors: when apoptosis controls tumor progression. Bull Cancer 94: E12-E17, 2007.
6. Beutler E. Hemochromatosis: genetics and pathophysiology. Annu Rev Med 57: 331-347, 2006.
7. Cirulli V, Yebra M. Netrins: beyond the brain. Nat Rev Mol Cell Biol 8: 296-306, 2007.
8. Flanagan JG, Cheng HJ, Feldheim DA, Hattori M, Lu Q, Vanderhaeghen P. Alkaline phosphatase fusions of ligands or receptors as in situ probes for staining of cells, tissues, and embryos. Methods Enzymol 327: 19-35, 2000.
9. Halbrooks PJ, Ding R, Wozney JM, Bain G. Role of RGM coreceptors in bone morphogenetic protein signaling. J Mol Signal 2: 4, 2007.
10. Hata K, Fujitani M, Yasuda Y, Doya H, Saito T, Yamagishi S, Mueller BK, Yamashita T. RGMa inhibition promotes axonal growth and recovery after spinal cord injury. J Cell Biol 173: 47-58, 2006.
11. Hentze MW, Muckenthaler MU, Andrews NC. Balancing acts: molecular control of mammalian iron metabolism. Cell 117: 285-297, 2004.
12. Huang FW, Pinkus JL, Pinkus GS, Fleming MD, Andrews NC. A mouse model of juvenile hemochromatosis. J Clin Invest 115: 2187-2191, 2005.
13. Keino-Masu K, Masu M, Hinck L, Leonardo ED, Chan SS, Culotti JG, Tessier-Lavigne M. Deleted in colorectal cancer (DCC) encodes a netrin receptor. Cell 87: 175-185, 1996.
14. Kruger RP, Lee J, Li W, Guan KL. Mapping netrin receptor binding reveals domains of Unc5 regulating its tyrosine phosphorylation. J Neurosci 24: 10826-10834, 2004.
15. Kuninger D, Kuns-Hashimoto R, Kuzmickas R, Rotwein P. Complex biosynthesis of the muscle-enriched iron regulator RGMc. J Cell Sci 119: 3273-3283, 2006.
16. Kuninger D, Kuzmickas R, Peng B, Pintar JE, Rotwein P. Gene discovery by microarray: identification of novel genes induced during growth factor-mediated muscle cell survival and differentiation. Genomics 84: 876-889, 2004.
17. Lee HH, Norris A, Weiss JB, Frasch M. Jelly belly protein activates the receptor tyrosine kinase Alk to specify visceral muscle pioneers. Nature 425: 507-512, 2003.
18. Leonardo ED, Hinck L, Masu M, Keino-Masu K, Ackerman SL, Tessier-Lavigne M. Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386: 833-838, 1997.
19. Lin L, Goldberg YP, Ganz T. Competitive regulation of hepcidin mRNA by soluble and cell-associated hemojuvelin. Blood 106: 2884-2889, 2005.
20. Lin L, Nemeth E, Goodnough JB, Thapa DR, Gabayan V, Ganz T. Soluble hemojuvelin is released by proprotein convertase-mediated cleavage at a conserved polybasic RNRR site. Blood Cells Mol Dis 40: 122-131, 2008.
21. Lin L, Valore EV, Nemeth E, Goodnough JB, Gabayan V, Ganz T. Iron transferrin regulates hepcidin synthesis in primary hepatocyte culture through hemojuvelin and BMP2/4. Blood 110: 2182-2189, 2007.
22. Luyten FP, Cunningham NS, Ma S, Muthukumaran N, Hammonds RG, Nevins WB, Woods WI, Reddi AH. Purification and partial amino acid sequence of osteogenin, a protein initiating bone differentiation. J Biol Chem 264: 13377-13380, 1989.
23. Matsunaga E, Nakamura H, Chedotal A. Repulsive guidance molecule plays multiple roles in neuronal differentiation and axon guidance. J Neurosci 26: 6082-6088, 2006.
24. Matsunaga E, Tauszig-Delamasure S, Monnier PP, Mueller BK, Strittmatter SM, Mehlen P, Chedotal A. RGM and its receptor neogenin regulate neuronal survival. Nat Cell Biol 6: 749-755, 2004.
25. Mehlen P, Mazelin L. The dependence receptors DCC and UNC5H as a link between neuronal guidance and survival. Biol Cell 95: 425-436, 2003.
26. Monnier PP, Sierra A, Macchi P, Deitinghoff L, Andersen JS, Mann M, Flad M, Hornberger MR, Stahl B, Bonhoeffer F, Mueller BK. RGM is a repulsive guidance molecule for retinal axons. Nature 419: 392-395, 2002.
27. Mukherjee A, Wilson EM, Rotwein P. Insulin-like growth factor (IGF) binding protein-5 blocks skeletal muscle differentiation by inhibiting IGF actions. Mol Endocrinol 22: 206-215, 2008.
28. Niederkofler V, Salie R, Arber S. Hemojuvelin is essential for dietary iron sensing, and its mutation leads to severe iron overload. J Clin Invest 115: 2180-2186, 2005.
29. Niederkofler V, Salie R, Sigrist M, Arber S. Repulsive guidance molecule (RGM) gene function is required for neural tube closure but not retinal topography in the mouse visual system. J Neurosci 24: 808-818, 2004.
30. Papanikolaou G, Samuels ME, Ludwig EH, MacDonald ML, Franchini PL, Dube MP, Andres L, MacFarlane J, Sakellaropoulos N, Politou M, Nemeth E, Thompson J, Risler JK, Zaborowska C, Babakaiff R, Radomski CC, Pape TD, Davidas O, Christakis J, Brissot P, Lockitch G, Ganz T, Hayden MR, Goldberg YP. Mutations in HFE2 cause iron overload in chromosome 1q-linked juvenile hemochromatosis. Nat Genet 36: 77-82, 2004.
31. Pasquale EB. Eph receptor signalling casts a wide net on cell behaviour. Nat Rev Mol Cell Biol 6: 462-475, 2005.
32. Plaza-Menacho I, Burzynski GM, de Groot JW, Eggen BJ, Hofstra RM. Current concepts in RET-related genetics, signaling and therapeutics. Trends Genet 22: 627-636, 2006.
33. Porter AG, Dhakshinamoorthy S. Apoptosis initiated by dependence receptors: a new paradigm for cell death? Bioessays 26: 656-664, 2004.
34. Rajagopalan S, Deitinghoff L, Davis D, Conrad S, Skutella T, Chedotal A, Mueller BK, Strittmatter SM. Neogenin mediates the action of repulsive guidance molecule. Nat Cell Biol 6: 756-762, 2004.
35. Round J, Stein E. Netrin signaling leading to directed growth cone steering. Curr Opin Neurobiol 17: 15-21, 2007.
36. Samad TA, Rebbapragada A, Bell E, Zhang Y, Sidis Y, Jeong SJ, Campagna JA, Perusini S, Fabrizio DA, Schneyer AL, Lin HY, Brivanlou AH, Attisano L, Woolf CJ. DRAGON, a bone morphogenetic protein co-receptor. J Biol Chem 280: 14122-14129, 2005.
37. Samad TA, Srinivasan A, Karchewski LA, Jeong SJ, Campagna JA, Ji RR, Fabrizio DA, Zhang Y, Lin HY, Bell E, Woolf CJ. DRAGON: a member of the repulsive guidance molecule-related family of neuronaland muscle-expressed membrane proteins is regulated by DRG11 and has neuronal adhesive properties. J Neurosci 24: 2027-2036, 2004.
38. Schmidtmer J, Engelkamp D. Isolation and expression pattern of three mouse homologues of chick RGM. Gene Expr Patterns 4: 105-110, 2004.
39. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700, 2003.
40. Silvestri L, Pagani A, Camaschella C. Furin-mediated release of soluble hemojuvelin: a new link between hypoxia and iron homeostasis. Blood 111: 924-931, 2008.
41. Silvestri L, Pagani A, Fazi C, Gerardi G, Levi S, Arosio P, Camaschella C. Defective targeting of hemojuvelin to plasma membrane is a common pathogenetic mechanism in juvenile hemochromatosis. Blood 109: 4503-4510, 2007.
42. Truksa J, Peng H, Lee P, Beutler E. Bone morphogenetic proteins 2, 4, and 9 stimulate murine hepcidin 1 expression independently of Hfe, transferrin receptor 2 (Tfr2), and IL-6. Proc Natl Acad Sci USA 103: 10289-10293, 2006.
43. Waite KA, Eng C. From developmental disorder to heritable cancer: it's all in the BMP/TGF-beta family. Nat Rev Genet 4: 763-773, 2003.
44. Wilson BD, Ii M, Park KW, Suli A, Sorensen LK, Larrieu-Lahargue F, Urness LD, Suh W, Asai J, Kock GA, Thorne T, Silver M, Thomas KR, Chien CB, Losordo DW, Li DY. Netrins promote developmental and therapeutic angiogenesis. Science 313: 640-644, 2006.
45. Wilson EM, Rotwein P. Control of MyoD function during initiation of muscle differentiation by an autocrine signaling pathway activated by insulin-like growth factor-II. J Biol Chem 281: 29962-29971, 2006.
46. Xia Y, Yu PB, Sidis Y, Beppu H, Bloch KD, Schneyer AL, Lin HY. Repulsive guidance molecule RGMa alters utilization of bone morphogenetic protein (BMP) type II receptors by BMP2 and BMP4. J Biol Chem 282: 18129-18140, 2007.
47. Zhang AS, Anderson SA, Meyers KR, Hernandez C, Eisenstein RS, Enns CA. Evidence that inhibition of hemojuvelin shedding in response to iron is mediated through neogenin. J Biol Chem 282: 12547-12556, 2007.
48. Zhang AS, West APJ, Wyman AE, Bjorkman PJ, Enns CA. Interaction of hemojuvelin with neogenin results in iron accumulation in human embryonic kidney 293 cells. J Biol Chem 280: 33885-33894, 2005.