The RGM protein DRAG-1 positively regulates a BMP-like signaling pathway in Caenorhabditis elegans

Development

Volumn 137, Issue 14, 2010, Pages 2375-2384

  Tian, Chenxi ^a   Sen, Debjeet ^a   Shi, Herong ^a   Foehr, Marisa L ^a   Plavskin, Yevgeniy ^a   Vatamaniuk, Olena K ^a   Liu, Jun ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

BMP; Body size; C. elegans; Co receptor; DRAG 1; DRAGON; M lineage; Mesoderm; RGM; RGMb; Sma Mab signaling; TGF

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; PROTEIN DRAG 1; RECEPTOR REGULATED SMAD PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BODY SIZE; CAENORHABDITIS ELEGANS; CELL MEMBRANE; CELL TYPE; GENE MUTATION; MESODERM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CAENORHABDITIS ELEGANS; HUMANS; MEMBRANE PROTEINS; MUTATION; NEURONS; PROTEIN BINDING; PROTEINS; SIGNAL TRANSDUCTION;

CAENORHABDITIS ELEGANS;

EID: 77954631778     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.051615     Document Type: Article

References (60)

1. Amin, N. M., Hu, K., Pruyne, D., Terzic, D., Bretscher, A. and Liu, J. (2007). A Zn-finger/FH2-domain containing protein, FOZI-1, acts redundantly with CeMyoD to specify striated body wall muscle fates in the Caenorhabditis elegans postembryonic mesoderm. Development 1, 19-29.
2. Amin, N. M., Lim, S. E., Shi, H., Chan, T. L. and Liu, J. (2009). A conserved Six-Eya cassette acts downstream of Wnt signaling to direct non-myogenic versus myogenic fates in the C. elegans postembryonic mesoderm. Dev. Biol. 331, 350-360.
3. Andriopoulos, B., Jr, Corradini, E., Xia, Y., Faasse, S. A., Chen, S., Grgurevic, L., Knutson, M. D., Pietrangelo, A., Vukicevic, S., Lin, H. Y. et al. (2009). BMP6 is a key endogenous regulator of hepcidin expression and iron metabolism. Nat. Genet. 41, 482-487.
4. Babitt, J. L., Zhang, Y., Samad, T. A., Xia, Y., Tang, J., Campagna, J. A., Schneyer, A. L., Woolf, C. J. and Lin, H. Y. (2005). Repulsive guidance molecule (RGMa), a DRAGON homologue, is a bone morphogenetic protein coreceptor. J. Biol. Chem. 280, 29820-29827. (Pubitemid 41177060)
5. 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. et al. (2006). Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat. Genet. 38, 531-539.
6. Babitt, J. L., Huang, F. W., Xia, Y., Sidis, Y., Andrews, N. C. and Lin, H. Y. (2007). Modulation of bone morphogenetic protein signaling in vivo regulates systemic iron balance. J. Clin. Invest. 117, 1933-1939. (Pubitemid 47036327)
7. Balemans, W. and Van Hul, W. (2002). Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 250, 231-250. (Pubitemid 35216412)
8. Bohme, U. and Cross, G. A. (2002). Mutational analysis of the variant surface glycoprotein GPI-Anchor signal sequence in Trypanosoma brucei. J. Cell Sci. 115, 805-816. (Pubitemid 34196340)
9. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
10. Camus, L. M. and Lambert, L. A. (2007). Molecular evolution of hemojuvelin and the repulsive guidance molecule family. J. Mol. Evol. 65, 68-81.
11. Chatterjee, S. and Mayor, S. (2001). The GPI-anchor and protein sorting. Cell Mol. Life Sci. 58, 1969-1987.
12. Corradini, E., Babitt, J. L. and Lin, H. Y. (2009). The RGM/DRAGON family of BMP co-receptors. Cytokine Growth Factor Rev. 20, 389-398.
13. Estevez, M., Attisano, L., Wrana, J. L., Albert, P. S., Massague, J. and Riddle, D. L. (1993). The Daf-4 gene encodes a bone morphogenetic protein receptor controlling C. elegans dauer larva development. Nature 365, 644-649. (Pubitemid 23350534)
14. Foehr, M. L. and Liu, J. (2008). Dorsoventral patterning of the C. elegans postembryonic mesoderm requires both LIN-12/Notch and TGFbeta signaling. Dev. Biol. 313, 256-266.
15. Foehr, M. L., Lindy, A. S., Fairbank, R. C., Amin, N. M., Xu, M., Yanowitz, J., Fire, A. Z. and Liu, J. (2006). An antagonistic role for the C. elegans schnurri homolog SMA-9 in modulating TGFbeta signaling during mesodermal patterning. Development 133, 2887-2896. (Pubitemid 44314266)
16. Fukushige, T., Hawkins, M. G. and McGhee, J. D. (1998). The GATA-Factor Elt-2 is essential for formation of the Caenorhabditis elegans intestine. Dev. Biol. 198, 286-302. (Pubitemid 28304445)
17. Gao, S., Steffen, J. and Laughon, A. (2005). Dpp-responsive silencers are bound by a trimeric Mad-Medea complex. J. Biol. Chem. 280, 36158-36164. (Pubitemid 41633888)
18. Georgi, L. L., Albert, P. S. and Riddle, D. L. (1990). Daf-1, a C. elegans gene controlling dauer larva development, encodes a novel receptor protein kinase. Cell 61, 635-645. (Pubitemid 120035010)
19. Gilleard, J. S., Shafi, Y., Barry, J. D. and McGhee, J. D. (1999). ELT-3: a caenorhabditis elegans GATA factor expressed in the embryonic epidermis during morphogenesis. Dev. Biol. 208, 265-280. (Pubitemid 29183989)
20. Gordon, K. J. and Blobe, G. C. (2008). Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim. Biophys. Acta 1782, 197-228.
21. Granato, M., Schnabel, H. and Schnabel, R. (1994). Pha-1, a selectable marker for gene transfer in C. elegans. Nucleic Acids Res. 22, 1762-1763. (Pubitemid 24155838)
22. Gumienny, T. L., MacNeil, L. T., Wang, H., de Bono, M., Wrana, J. L. and Padgett, R. W. (2007). Glypican LON-2 is a conserved negative regulator of BMP-like signaling in Caenorhabditis elegans. Curr. Biol. 17, 159-164. (Pubitemid 46107828)
23. Harfe, B. D., Vaz Gomes, A., Kenyon, C., Liu, J., Krause, M. and Fire, A. (1998). Analysis of a Caenorhabditis elegans Twist homolog identifies conserved and divergent aspects of mesodermal patterning. Genes Dev. 12, 2623-2635. (Pubitemid 28406963)
24. Jiang, Y., Shi, H. and Liu, J. (2009). Two hox cofactors, the Meis/Hth homolog UNC-62 and the Pbx/Exd homolog CEH-20, function together during C. elegans postembryonic mesodermal development. Dev. Biol. 334, 535-546.
25. Johnson, K., Kirkpatrick, H., Comer, A., Hoffmann, F. M. and Laughon, A. (1999). Interaction of SMAD complexes with tripartite DNA-binding sites. J. Biol. Chem. 274, 20709-20716.
26. Kramer, J. M. and Johnson, J. J. (1993). Analysis of mutations in the Sqt-1 and Rol-6 collagen genes of Caenorhabditis elegans. Genetics 135, 1035-1045.
27. Krishna, S., Maduzia, L. L. and Padgett, R. W. (1999). Specificity of TGFbeta signaling is conferred by distinct type i receptors and their associated SMAD proteins in Caenorhabditis elegans. Development 126, 251-260.
28. Liang, J., Lints, R., Foehr, M. L., Tokarz, R., Yu, L., Emmons, S. W., Liu, J. and Savage-Dunn, C. (2003). The Caenorhabditis elegans schnurri homolog Sma-9 mediates stage- and cell type-specific responses to DBL-1 BMP-related signaling. Development 130, 6453-6464.
29. Maduzia, L. L., Gumienny, T. L., Zimmerman, C. M., Wang, H., Shetgiri, P., Krishna, S., Roberts, A. F. and Padgett, R. W. (2002). Lon-1 regulates Caenorhabditis elegans body size downstream of the Dbl-1 TGF beta signaling pathway. Dev. Biol. 246, 418-428.
30. Massagué, J. (2008). TGFβ in cancer. Cell 134, 215-230.
31. Massagué, J. and Chen, Y. G. (2000). Controlling TGF-β signaling. Genes Dev. 14, 627-644.
32. Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V. (1991). Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
33. Morita, K., Chow, K. L. and Ueno, N. (1999). Regulation of body length and male tail ray pattern formation of Caenorhabditis elegans by a member of TGF-beta family. Development 126, 1337-1347.
34. Morita, K., Flemming, A. J., Sugihara, Y., Mochii, M., Suzuki, Y., Yoshida, S., Wood, W. B., Kohara, Y., Leroi, A. M. and Ueno, N. (2002). A Caenorhabditis elegans TGF-beta, DBL-1, controls the expression of LON-1, a PR-related protein, that regulates polyploidization and body length. EMBO J. 21, 1063-1073.
35. Moustakas, A. and Heldin, C. H. (2009). The regulation of TGFβ signal transduction. Development 136, 3699-3714.
36. Okkema, P. G., Harrison, S. W., Plunger, V., Aryana, A. and Fire, A. (1993). Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics 135, 385-404. (Pubitemid 23307595)
37. Partridge, F. A., Gravato-Nobre, M. J. and Hodgkin, J. (2010). Signal transduction pathways that function in both development and innate immunity. Dev. Dyn. 239, 1330-1336.
38. Pyrowolakis, G., Hartmann, B., Müller, B., Basler, K. and Affolter, M. (2004). A simple molecular complex mediates widespread BMP-induced repression during Drosophila development. Dev. Cell 7, 229-240. (Pubitemid 39145027)
39. Ren, P., Lim, C. S., Johnsen, R., Albert, P. S., Pilgrim, D. and Riddle, D. L. (1996). Control of C. elegans larval development by neuronal expression of a TGF-Beta homolog. Science 274, 1389-1391. (Pubitemid 26391466)
40. Samad, T. A., Srinivasan, A., Karchewski, L. A., Jeong, S. J., Campagna, J. A., Ji, R. R., Fabrizio, D. A., Zhang, Y., Lin, H. Y., Bell, E. et al. (2004). DRAGON: A member of the repulsive guidance molecule-related family of neuronal- and muscle-expressed membrane proteins is regulated by DRG11 and has neuronal adhesive properties. J. Neurosci. 24, 2027-2036.
41. Samad, T. A., Rebbapragada, A., Bell, E., Zhang, Y., Sidis, Y., Jeong, S. J., Campagna, J. A., Perusini, S., Fabrizio, D. A., Schneyer, A. L. et al. (2005). DRAGON, a bone morphogenetic protein Co-receptor. J. Biol. Chem. 280, 14122-14129.
42. Savage, C., Das, P., Finelli, A. L., Townsend, S. R., Sun, C. Y., Baird, S. E. and Padgett, R. W. (1996). Caenorhabditis elegans genes Sma-2, Sma-3, and Sma-4 define a conserved family of transforming growth factor beta pathway components. Proc. Natl. Acad. Sci. USA 93, 790-794. (Pubitemid 26041170)
43. Savage-Dunn, C. (2005). TGF-β signaling. WormBook (ed. The C. elegans Research Community). doi/10.1895/wormbook.1.22.1, http://www.wormbook. org.
44. Schmierer, B. and Hill, C. S. (2007). TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat. Rev. Mol. Cell Biol. 8, 970-982. (Pubitemid 350174642)
45. Schwartz, M. S., Benci, J. L., Selote, D. S., Sharma, A. K., Chen, A. G. Y., Dang, H., Fares, H. and Vatamaniuk, O. K. (2010). Detoxification of multiple heavy metals by a half-molecule ABC transporter, HMT-1, and coelomocytes of Caenorhabditis elegans. PLoS ONE 5, e9564.
46. Severyn, C. J., Shinde, U. and Rotwein, P. (2009). Molecular biology, genetics and biochemistry of the repulsive guidance molecule family. Biochem. J. 422, 393-403.
47. Shi, Y. and Massagué, J. (2003). Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113, 685-700. (Pubitemid 36724933)
48. Sulston, J. E. and Horvitz, H. R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156. (Pubitemid 8049332)
49. Suzuki, Y., Yandell, M. D., Roy, P. J., Krishna, S., Savage-Dunn, C., Ross, R. M., Padgett, R. W. and Wood, W. B. (1999). A BMP homolog acts as a dose-dependent regulator of body size and male tail patterning in Caenorhabditis elegans. Development 126, 241-250. (Pubitemid 29083962)
50. Umulis, D., O'Connor, M. B. and Blair, S. S. (2009). The extracellular regulation of bone morphogenetic protein signaling. Development 136, 3715-3728.
51. Vatamaniuk, O. K., Bucher, E. A., Sundaram, M. V. and Rea, P. A. (2005). CeHMT-1, a putative phytochelatin transporter, is required for cadmium tolerance in Caenorhabditis elegans. J. Biol. Chem. 280, 23684-23690.
52. Vowels, J. J. and Thomas, J. H. (1992). Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130, 105-123.
53. Wang, J., Tokarz, R. and Savage-Dunn, C. (2002). The expression of TGFbeta signal transducers in the hypodermis regulates body size in C. elegans. Development 129, 4989-4998. (Pubitemid 35355916)
54. Wicks, S. R., Yeh, R. T., Gish, W. R., Waterston, R. H. and Plasterk, R. H. (2001). Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28, 160-164.
55. Wrighton, K. H., Lin, X. and Feng, X. H. (2009). Phospho-control of TGF-beta superfamily signaling. Cell Res. 19, 8-20.
56. Wu, M. Y. and Hill, C. S. (2009). Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev. Cell 16, 329-343.
57. Xia, Y., Babitt, J. L., Sidis, Y., Chung, R. T. and Lin, H. Y. (2008). Hemojuvelin regulates hepcidin expression via a selective subset of BMP ligands and receptors independently of neogenin. Blood 111, 5195-5204.
58. Xia, Y., Babitt, J. L., Bouley, R., Zhang, Y., Da Silva, N., Chen, S., Zhuang, Z., Samad, T. A., Brenner, G. J., Anderson, J. L. et al. (2010). Dragon enhances BMP signaling and increases transepithelial resistance in kidney epithelial cells. J. Am. Soc. Nephrol. 21, 666-677.
59. Yochem, J., Weston, K. and Greenwald, I. (1988). The Caenorhabditis elegans lin-12 gene encodes a transmembrane protein with overall similarity to Drosophila Notch. Nature 335, 547-550.
60. Yoshida, S., Morita, K., Mochii, M. and Ueno, N. (2001). Hypodermal expression of Caenorhabditis elegans TGF-Beta Type I receptor SMA-6 is essential for the growth and maintenance of body length. Dev. Biol. 240, 32-45. (Pubitemid 33141107)