Protein associated with SMAD1 (PAWS1/FAM83G) is a substrate for type I bone morphogenetic protein receptors and modulates bone morphogenetic protein signalling

Open Biology

Volumn 4, Issue FEB, 2014, Pages

  Vogt, Janis ^a   Dingwell, Kevin S ^b   Herhaus, Lina ^a   Gourlay, Robert ^a   Macartney, Thomas ^a   Campbell, David ^a   Smith, James C ^b   Sapkota, Gopal P ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

ALK3; BMPR1; Bone morphogenetic protein; FAM83G; PAWS1; SMAD1

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXY 1 METHYLTETRALIN; BMPR1A PROTEIN, HUMAN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; NEDD9 PROTEIN, HUMAN; PAWS1 PROTEIN, HUMAN; PHOSPHOPROTEIN; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMAD1 PROTEIN; SMAD4 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; BMPR1; CELL LINE; DRUG ANTAGONISM; DRUG EFFECT; ENZYME SPECIFICITY; FAM83G; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HUMAN; METABOLISM; MUTATION; PAWS1; PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMAD1;

ALK3; BMPR1; BONE MORPHOGENETIC PROTEIN; FAM83G; PAWS1; SMAD1;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CELL LINE; HEK293 CELLS; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTATION; PHOSPHOPROTEINS; PHOSPHORYLATION; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; SMAD4 PROTEIN; SUBSTRATE SPECIFICITY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84937413187     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.130210     Document Type: Article

References (46)

1. Chen D, Zhao M, Mundy GR 2004 Bone morphogenetic proteins. Growth Factors 22, 233-241. (doi:10.1080/08977190412331279890) (Pubitemid 40136452)
2. De Robertis EM, Kuroda H. 2004 Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20, 285-308. (doi:10.1146/annurev.cellbio.20.011403.154124) (Pubitemid 39488640)
3. Harland R. 2000 Neural induction. Curr. Opin. Genet. Dev. 10, 357-362. (doi:10.1016/S0959-437X(00)00096-4) (Pubitemid 30450037)
4. Schier AF, Talbot WS 2005 Molecular genetics of axis formation in zebrafish. Annu. Rev. Genet. 39, 561-613. (doi:10.1146/annurev.genet.37.110801. 143752) (Pubitemid 43011127)
5. Varga AC, Wrana JL 2005 The disparate role of BMP in stem cell biology. Oncogene 24, 5713-5721. (doi:10.1038/sj.onc.1208919) (Pubitemid 43086131)
6. Bandyopadhyay A, Yadav PS, Prashar P. 2013 BMP signaling in development and diseases: a pharmacological perspective. Biochem. Pharmacol. 85, 857-864. (doi:10.1016/j.bcp.2013.01.004)
7. Harradine KA, Akhurst RJ 2006 Mutations of TGFbeta signaling molecules in human disease. Ann. Med. 38, 403-414. (doi:10.1080/07853890600919911) (Pubitemid 44484878)
8. Yu PB et al. 2008 BMP type I receptor inhibition reduces heterotopic [corrected] ossification. Nat. Med. 14, 1363-1369. (doi:10.1038/nm.1888)
9. Cai J, Pardali E, Sanchez-Duffhues G, ten Dijke P. 2012 BMP signaling in vascular diseases. FEBS Lett. 586, 1993-2002. (doi:10.1016/j.febslet.2012.04. 030)
10. Massague J, Blain SW, Lo RS 2000 TGFb signaling in growth control, cancer, and heritable disorders. Cell 103, 295-309. (doi:10.1016/S0092-8674(00) 00121-5)
11. Al-Salihi MA, Herhaus L, Sapkota GP 2012 Regulation of the transforming growth factor b pathway by reversible ubiquitylation. Open Biol. 2, 120082. (doi:10.1098/rsob.120082)
12. Bruce DL, Sapkota GP 2012 Phosphatases in SMAD regulation. FEBS Lett. 586, 1897-1905. (doi:10.1016/j.febslet.2012.02.001)
13. Rider CC, Mulloy B. 2010 Bone morphogenetic protein and growth differentiation factor cytokine families and their protein antagonists. Biochem. J. 429, 1-12. (doi:10.1042/BJ20100305)
14. Shi Y, Massague J. 2003 Mechanisms of TGF-b signaling from cell membrane to the nucleus. Cell 113, 685-700. (doi:10.1016/S0092-8674(03)00432-X) (Pubitemid 36724933)
15. Massague J, Gomis RR 2006 The logic of TGFb signaling. FEBS Lett. 580, 2811-2820. (doi:10.1016/j.febslet.2006.04.033)
16. Massague J. 2008 TGFb in cancer. Cell 134, 215-230. (doi:10.1016/j.cell. 2008.07.001)
17. Miyaki M, Kuroki T. 2003 Role of Smad4 (DPC4) inactivation in human cancer. Biochem. Biophys. Res. Commun. 306, 799-804. (doi:10.1016/S0006-291X(03) 01066-0) (Pubitemid 36776201)
18. Beck SE, Carethers JM 2007 BMP suppresses PTEN expression via RAS/ERK signaling. Cancer Biol. Ther. 6, 1313-1317. (doi:10.4161/cbt.6.8.4507) (Pubitemid 351590388)
19. Beck SE et al. 2006 Bone morphogenetic protein signaling and growth suppression in colon cancer. Am. J. Physiol. Gastrointest. Liver Physiol. 291, G135-G145. (doi:10.1152/ajpgi.00482.2005) (Pubitemid 44024671)
20. Morikawa Y, Zehir A, Maska E., Deng C, Schneider MD, Mishina Y, Cserjesi P. 2009 BMP signaling regulates sympathetic nervous system development through Smad4-dependent and -independent pathways. Development 136, 3575-3584. (doi:10.1242/dev.038133)
21. Perron JC, Dodd J. 2009 ActRIIA and BMPRII Type II BMP receptor subunits selectively required for Smad4-independent BMP7-evoked chemotaxis. PLoS ONE 4, e8198. (doi:10.1371/journal.pone.0008198)
22. Xu X, Han J, Ito Y., Bringas Jr P, Deng C, Chai Y. 2008 Ectodermal Smad4 and p38 MAPK are functionally redundant in mediating TGF-b/BMP signaling during tooth and palate development. Dev. Cell 15, 322-329. (doi:10.1016/j.devcel.2008. 06.004)
23. Deng H, Ravikumar TS, Yang WL 2009 Overexpression of bone morphogenetic protein 4 enhances the invasiveness of Smad4-deficient human colorectal cancer cells. Cancer Lett. 281, 220-231. (doi:10.1016/j.canlet.2009.02.046)
24. Gottlin EB, Rudolph AE, Zhao Y, Matthews HR, Dixon JE 1998 Catalytic mechanism of the phospholipase D superfamily proceeds via a covalent phosphohistidine intermediate. Proc. Natl Acad. Sci. USA 95, 9202-9207. (doi:10.1073/pnas.95.16.9202) (Pubitemid 28506209)
25. Boyer AP, Collier TS, Vidavsky I, Bose R. 2013 Quantitative proteomics with siRNA screening identifies novel mechanisms of trastuzumab resistance in HER2 amplified breast cancers. Mol. Cell. Proteomics 12, 180-193. (doi:10.1074/mcp.M112.020115)
26. Lee SY, Meier R, Furuta S., Lenburg ME, Kenny PA, Xu R, Bissell MJ 2012 FAM83A confers EGFR-TKI resistance in breast cancer cells and in mice. J. Clin. Invest. 122, 3211-3220. (doi:10.1172/JCI60498)
27. Kim JW et al. 2008 FAM83H mutations in families with autosomal-dominant hypocalcified amelogenesis imperfecta. Am. J. Hum. Genet. 82, 489-494. (doi:10.1016/j.ajhg.2007.09.020)
28. Zhang Y, Chang C, Gehling DJ, Hemmati-Brivanlou A, Derynck R. 2001 Regulation of Smad degradation and activity by Smurf2, an E3 ubiquitin ligase. Proc. Natl Acad. Sci. USA 98, 974-979. (doi:10.1073/pnas.98.3.974) (Pubitemid 32121172)
29. Lagna G, Hata A, Hemmati-Brivanlou A, Massague J. 1996 Partnership between DPC4 and SMAD proteins in TGF-b signalling pathways. Nature 383, 832-836. (doi:10.1038/383832a0) (Pubitemid 26372668)
30. Raju GP, Dimova N, Klein PS, Huang HC 2003 SANE, a novel LEM domain protein, regulates bone morphogenetic protein signaling through interaction with Smad1.J. Biol. Chem. 278, 428-437. (doi:10.1074/jbc.M210505200) (Pubitemid 36043593)
31. Vogt J, Traynor R, Sapkota GP 2011 The specificities of small molecule inhibitors of the TGFb and BMP pathways. Cell. Signal. 23, 1831-1842. (doi:10.1016/j.cellsig.2011.06.019)
32. Lopez-Rovira T., Chalaux E, Massague J., Rosa JL, Ventura F. 2002 Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J. Biol. Chem. 277, 3176-3185. (doi:10.1074/jbc.M106826200) (Pubitemid 34953179)
33. Alarcon C et al. 2009 Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-b pathways. Cell 139, 757-769. (doi:10.1016/j.cell. 2009.09.035)
34. Sun J, Liu YH, Chen H, Nguyen MP, Mishina Y., Upperman JS, Ford HR, Shi W. 2007 Deficient Alk3-mediated BMP signaling causes prenatal omphalocelelike defect. Biochem. Biophys. Res. Commun. 360, 238-243. (doi:10.1016/j.bbrc.2007. 06.049) (Pubitemid 46990348)
35. Komatsu Y, Scott G, Nagy A., Kaartinen V, Mishina Y 2007 BMP type I receptor ALK2 is essential for proper patterning at late gastrulation during mouse embryogenesis. Dev. Dyn. 236, 512-517. (doi:10.1002/dvdy.21021) (Pubitemid 46233294)
36. Fukuda T, Scott G, Komatsu Y., Araya R, Kawano M, Ray MK, Yamada M., Mishina Y 2006 Generation of a mouse with conditionally activated signaling through the BMP receptor, ALK2. Genesis 44, 159-167. (doi:10.1002/dvg.20201) (Pubitemid 43727738)
37. Clarke TR, Hoshiya Y, Yi SE, Liu X., Lyons KM, Donahoe PK 2001 Mullerian inhibiting substance signaling uses a bone morphogenetic protein (BMP)-like pathway mediated by ALK2 and induces SMAD6 expression. Mol. Endocrinol. 15, 946-959. (Pubitemid 32510641)
38. Goumans MJ, Mummery C. 2000 Functional analysis of the TGFb receptor/Smad pathway through gene ablation in mice. Int. J. Dev. Biol. 44, 253-265. (Pubitemid 30368069)
39. Ahn J, Sanz-Moreno V, Marshall CJ 2012 The metastasis gene NEDD9 product acts through integrin b3 and Src to promote mesenchymal motility and inhibit amoeboid motility. J. Cell Sci. 125, 1814-1826. (doi:10.1242/jcs.101444)
40. Chang JX, Gao F, Zhao GQ, Zhang GJ 2012 Role of NEDD9 in invasion and metastasis of lung adenocarcinoma. Exp. Ther. Med. 4, 795-800. (doi:10.3892/etm.2012.693)
41. Lorenzi PL, Weinstein JN 2009 Asparagine synthetase: a new potential biomarker in ovarian cancer. Drug News Perspect. 22, 61-64. (doi:10.1358/dnp. 2009.22.1.1303820)
42. Herhaus L, Al-Salihi M, Macartney T., Weidlich S, Sapkota GP 2013 OTUB1 enhances TGFb signalling by inhibiting the ubiquitylation and degradation of active SMAD2/3. Nat. Commun. 4, 2519. (doi:10.1038/ncomms3519)
43. Al-Salihi MA, Herhaus L, Macartney T., Sapkota GP 2012 USP11 augments TGFb signalling by deubiquitylating ALK5. Open Biol. 2, 120063. (doi:10.1098/rsob.120063)
44. Bruce DL, Macartney T, Yong W., Shou W, Sapkota GP 2012 Protein phosphatase 5 modulates SMAD3 function in the transforming growth factor-b pathway. Cell. Signal. 24, 1999-2006. (doi:10.1016/j.cellsig.2012.07.003)
45. Pfaffl MW. 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45. (doi:10.1093/nar/29.9.e45)
46. Campbell DG, Morrice NA 2002 Identification of protein phosphorylation sites by a combination of mass spectrometry and solid phase Edman sequencing. J. Biomol. Tech. 13, 119-130.