The TGFbeta superfamily signaling pathway

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 2, Issue 1, 2013, Pages 47-63

  Weiss, Alexander ^a   Attisano, Liliana ^b  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FOLLISTATIN RELATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; MYOSTATIN; NEOGENIN; NOGGIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SERINE THREONINE KINASE; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

DNA BINDING; DROSOPHILA; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; LIGAND BINDING; METASTASIS; NERVE CELL PLASTICITY; NUCLEOTIDE SEQUENCE; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; HUMANS; SIGNAL TRANSDUCTION; TGF-BETA SUPERFAMILY PROTEINS;

EID: 84880048839     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.86     Document Type: Review

References (93)

1. Affolter M, Basler K. The decapentaplegic morphogen gradient: from pattern formation to growth regulation. Nat Rev Genet 2007, 8:663-674. doi:10.1038/ nrg2166.
2. Mizutani CM, Bier E. EvoD/Vo: the origins of BMP signalling in the neuroectoderm. Nat Rev Genet 2008, 9:663-677. doi:10.1038/nrg2417.
3. Zakin L, De Robertis EM. Extracellular regulation of BMP signaling. Curr Biol 2010, 20:R89-R92. doi:10.1016/j.cub.2009.11.021.
4. Arnold SJ, Robertson EJ. Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 2009, 10:91-103. doi:10.1038/nrm2618.
5. Schier AF. Nodal morphogens. Cold Spring Harb Perspect Biol 2009, 1:a003459. doi:10.1101/cshperspect. a003459.
6. Pera MF, Tam PPL. Extrinsic regulation of pluripotent stem cells. Nature 2010, 465:713-720. doi:10. 1038/nature09228.
7. Gordon KJ, Blobe GC. Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim Biophys Acta 2008, 1782:197-228. doi:10.1016/j.bbadis.2008.01.006.
8. Ikushima H, Miyazono K. TGFβ signalling: a complex web in cancer progression. Nat Rev Cancer 2010, 10:415-424. doi:10.1038/nrc2853.
9. Massagué J. TGFβ in cancer. Cell 2008, 134:215-230. doi:10.1016/j.cell.2008.07.001.
10. Harrison CA, Al-Musawi SL, Walton KL. Prodomains regulate the synthesis, extracellular localisation and activity of TGF-β superfamily ligands. Growth Factors 2011, 29:174-186. doi:10.3109/08977194. 2011.608666.
11. Bragdon B, Moseychuk O, Saldanha S, King D, Julian J, Nohe A. Bone morphogenetic proteins: a critical review. Cell Signal 2011, 23:609-620. doi:10.1016/j. cellsig.2010.10.003.
12. Umulis D, O'Connor MB, Blair SS. The extracellular regulation of bone morphogenetic protein signaling. Development 2009, 136:3715-3728. doi:10. 1242/dev.031534.
13. Vuilleumier R, Springhorn A, Patterson L, Koidl S, Hammerschmidt M, Affolter M, Pyrowolakis G. Control of Dpp morphogen signalling by a secreted feedback regulator. Nat Cell Biol 2010, 12:611-617. doi:10.1038/ncb2064.
14. Rainger J, van Beusekom E, Ramsay JK, McKie L, Al-Gazali L, Pallotta R, Saponari A, Branney P, Fisher M, Morrison H, et al. Loss of the BMP antagonist, SMOC-1, causes ophthalmo-acromelic (Waardenburg Anophthalmia) syndrome in humans and mice. PLoS Genet 2011, 7:e1002114. doi:10.1371/ journal.pgen.1002114.
15. Wrana JL, Attisano L, Wieser R, Ventura F, Massagué J. Mechanism of activation of the TGF-β receptor. Nature 1994, 370:341-347. doi:10.1038/370341a0.
16. Feng X-H, Derynck R. Specificity and versatility in TGF-β signaling through Smads. Annu Rev Cell Dev Biol 2005, 21:659-693. doi:10.1146/annurev. cellbio.21.022404.142018.
17. Schmierer B, Hill CS. TGFβ-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 2007, 8:970-982. doi:10.1038/nrm2297.
18. Moustakas A, Heldin C-H. The regulation of TGFβ signal transduction. Development 2009, 136:3699-3714. doi:10.1242/dev.030338.
19. Rebbapragada A, Benchabane H, Wrana JL, Celeste AJ, Attisano L. Myostatin signals through a transforming growth factor-like signaling pathway to block adipogenesis. Mol Cell Biol 2003, 23:7230-7242. doi:10.1128/MCB.23.20.
20. Patterson GI, Padgett RW. TGFβ-related pathways. Trends Genet 2000, 16:27-33. doi:10.1016/S0168-9525(99)01916-2.
21. Groppe J, Hinck CS, Samavarchi-Tehrani P, Zubieta C, Schuermann JP, Taylor AB, Schwarz PM, Wrana JL, Hinck AP. Cooperative assembly of TGF-β superfamily signaling complexes is mediated by two disparate mechanisms and distinct modes of receptor binding. Mol Cell 2008, 29:157-168. doi:10.1016/j.molcel.2007.11.039.
22. Feng XH, Derynck R. A kinase subdomain of transforming growth factor-beta (TGF-β) type I receptor determines the TGF-β intracellular signaling specificity. EMBO J 1997, 16:3912-3923. doi:10.1093/emboj/ 16.13.3912.
23. Bernabeu C, Lopez-Novoa JM, Quintanilla M. The emerging role of TGF-β superfamily coreceptors in cancer. Biochim Biophys Acta 2009, 1792:954-973. doi:10.1016/j.bbadis.2009.07.003.
24. López-Casillas F, Cheifetz S, Doody J, Andres JL, Lane WS, Massagué J. Structure and expression of the membrane proteoglycan betaglycan, a component of the TGF-β receptor system. Cell 1991, 67:785-795. doi:10.1016/0092-8674(91)90073-8.
25. Gritsman K, Zhang J, Cheng S, Heckscher E, Talbot WS, Schier AF. The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell 1999, 97:121-132. doi:10.1016/S0092-8674(00)80720-5.
26. Constam DB. Riding shotgun: a dual role for the epidermal growth factor-Cripto/FRL-1/Cryptic protein Cripto in nodal trafficking. Traffic 2009, 10:783-791. doi:10.1111/j.1600-0854.2009.00874.x.
27. Samad TA, Rebbapragada A, Bell E, Zhang Y, Sidis Y, Jeong SJ, Campagna JA, Perusini S, Fabrizio DA, Schneyer AL, et al. DRAGON, a bone morphogenetic protein co-receptor. J Biol Chem 2005, 280:14122-14129. doi:10.1074/jbc.M410034200.
28. Corradini E, Babitt JL, Lin HY. The RGM/DRAGON family of BMP co-receptors. Cytokine Growth Factor Rev 2009, 20:389-398. doi:10. 1016/j.cytogfr.2009.10.008.
29. Jackson SM, Nakato H, Sugiura M, Jannuzi A, Oakes R, Kaluza V, Golden C, Selleck SB. dally, a Drosophila glypican, controls cellular responses to the TGF-β-related morphogen, Dpp. Development 1997, 124:4113-4120.
30. Belenkaya TY, Han C, Yan D, Opoka RJ, Khodoun M, Liu H, Lin X. Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell 2004, 119:231-244. doi:10. 1016/j.cell.2004.09.031.
31. Gumienny TL, MacNeil LT, Wang H, de Bono M, Wrana JL, Padgett RW. Glypican LON-2 is a conserved negative regulator of BMP-like signaling in Caenorhabditis elegans. Curr Biol 2007, 17:159-164. doi:10.1016/j.cub.2006.11.065.
32. Tian C, Sen D, Shi H, Foehr ML, Plavskin Y, Vatamaniuk OK, Liu J. The RGM protein DRAG-1 positively regulates a BMP-like signaling pathway in Caenorhabditis elegans. Development 2010, 137:2375-2384. doi:10.1242/dev.051615.
33. Zhou Z, Xie J, Lee D, Liu Y, Jung J, Zhou L, Xiong S, Mei L, Xiong WC. Neogenin regulation of BMP-induced canonical Smad signaling and endochondral bone formation. Dev Cell 2010, 19:90-102. doi:10.1016/j.devcel.2010.06.016.
34. Onichtchouk D, Chen YG, Dosch R, Gawantka V, Delius H, Massagué J, Niehrs C. Silencing of TGF-β signalling by the pseudoreceptor BAMBI. Nature 1999, 401:480-485. doi:10.1038/46794.
35. Aramaki T, Sasai N, Yakura R, Sasai Y. Jiraiya attenuates BMP signaling by interfering with type II BMP receptors in neuroectodermal patterning. Dev Cell 2010, 19:547-561. doi:10.1016/j.devcel.2010.09.001.
36. Gumienny TL, Macneil L, Zimmerman CM, Wang H, Chin L, Wrana JL, Padgett RW. Caenorhabditis elegans SMA-10/LRIG is a conserved transmembrane protein that enhances bone morphogenetic protein signaling. PLoS Genet 2010, 6:e1000963. doi:10. 1371/journal.pgen.1000963.
37. Huminiecki L, Goldovsky L, Freilich S, Moustakas A, Ouzounis C, Heldin C-H. Emergence, development and diversification of the TGF-β signalling pathway within the animal kingdom. BMC Evol Biol 2009, 9:28. doi:10.1186/1471-2148-9-28.
38. Mu Y, Gudey SK, Landström M. Non-Smad signaling pathways. Cell Tissue Res 2012, 347:11-20. doi:10.1007/s00441-011-1201-y.
39. Zhang YE. Non-Smad pathways in TGF-β signaling. Cell Res 2009, 19:128-139. doi:10.1038/cr.2008.328.
40. Lamouille S, Derynck R. Emergence of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin axis in transforming growth factor-β-induced epithelial-mesenchymal transition. Cells Tissues Organs 2011, 193:8-22. doi:10.1159/000320172.
41. Bierie B, Moses HL. Tumour microenvironment: TGFβ: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer 2006, 6:506-520. doi:10.1038/nrc1926.
42. Ozdamar B, Bose R, Barrios-Rodiles M, Wang H-R, Zhang Y, Wrana JL. Regulation of the polarity protein Par6 by TGFβ receptors controls epithelial cell plasticity. Science 2005, 307:1603-1609. doi:10.1126/ science.1105718.
43. Viloria-Petit AM, David L, Jia JY, Erdemir T, Bane AL, Pinnaduwage D, Roncari L, Narimatsu M, Bose R, Moffat J, et al. A role for the TGFβ-Par6 polarity pathway in breast cancer progression. Proc Natl Acad Sci USA 2009, 106:14028-14033. doi:10.1073/pnas.0906796106.
44. Yi JJ, Barnes AP, Hand R, Polleux F, Ehlers MD. TGF-β signaling specifies axons during brain development. Cell 2010, 142:144-157. doi:10.1016/j.cell.2010.06.010.
45. Kardassis D, Murphy C, Fotsis T, Moustakas A, Stournaras C. Control of transforming growth factor beta signal transduction by small GTPases. FEBS J 2009, 276:2947-2965. doi:10.1111/j.1742-4658. 2009.07031.x.
46. Lee-Hoeflich ST, Causing CG, Podkowa M, Zhao X, Wrana JL, Attisano L. Activation of LIMK1 by binding to the BMP receptor, BMPRII, regulates BMP-dependent dendritogenesis. EMBO J 2004, 23:4792-4801. doi:10.1038/sj.emboj.7600418.
47. Podkowa M, Zhao X, Chow C-WW, Coffey ET, Davis RJ, Attisano L. Microtubule stabilization by bone morphogenetic protein receptor-mediated scaffolding of c-Jun N-terminal kinase promotes dendrite formation. Mol Cell Biol 2010, 30:2241-2250. doi:10.1128/MCB.01166-09.
48. Foletta VC, Lim MA, Soosairajah J, Kelly AP, Stanley EG, Shannon M, He W, Das S, Massague J, Bernard O, et al. Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1. J Cell Biol 2003, 162:1089-1098. doi:10.1083/jcb.200212060.
49. Eaton BA, Davis GW. LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron 2005, 47:695-708. doi:10.1016/j. neuron.2005.08.010.
50. Wen Z, Han L, Bamburg JR, Shim S, Ming G-Li, Zheng JQ. BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin. J Cell Biol 2007, 178:107-119. doi:10.1083/jcb.200703055.
51. Yamashita M, Fatyol K, Jin C, Wang X, Liu Z, Zhang YE. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-β. Mol Cell 2008, 31:918-924. doi:10.1016/j.molcel.2008.09.002.
52. Sorrentino A, Thakur N, Grimsby S, Marcusson A, von Bulow V, Schuster N, Zhang S, Heldin C-H, Landström M. The type I TGF-β receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner. Nat Cell Biol 2008, 10:1199-1207. doi:10.1038/ncb1780.
53. Wendt MK, Allington TM, Schiemann WP. Mechanisms of the epithelial-mesenchymal transition by TGF-β. Future Oncol 2009, 5:1145-1168. doi:10. 2217/fon.09.90.
54. Itoh S, Itoh F. Inhibitory machinery for the TGF-β family signaling pathway. Growth Factors 2011, 29:163-173. doi:10.3109/08977194.2011.614236.
55. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL. Distinct endocytic pathways regulate TGF-β receptor signalling and turnover. Nat Cell Biol 2003, 5:410-421. doi:10.1038/ncb975.
56. Inoue Y, Imamura T. Regulation of TGF-β family signaling by E3 ubiquitin ligases. Cancer Sci 2008, 99:2107-2112. doi:10.1111/j.1349-7006.2008. 00925.x.
57. Ogunjimi AA, Briant DJ, Pece-Barbara N, Le Roy C, Di Guglielmo GM, Kavsak P, Rasmussen RK, Seet BT, Sicheri F, Wrana JL. Regulation of Smurf2 ubiquitin ligase activity by anchoring the E2 to the HECT domain. Mol Cell 2005, 19:297-308. doi:10.1016/j. molcel.2005.06.028.
58. Xia L, Jia S, Huang S, Wang H, Zhu Y, Mu Y, Kan L, Zheng W, Wu D, Li X, et al. The Fused/Smurf complex controls the fate of Drosophila germline stem cells by generating a gradient BMP response. Cell 2010, 143:978-990. doi:10.1016/j.cell.2010.11.022.
59. Hill CS. Nucleocytoplasmic shuttling of Smad proteins. Cell Res 2009, 19:36-46. doi:10.1038/cr.2008.325.
60. Wrighton KH, Feng X-H. To (TGF)β or not to (TGF)β: fine-tuning of Smad signaling via post-translational modifications. Cell Signal 2008, 20:1579-1591. doi:10.1016/j.cellsig.2008.02.003.
61. Eivers E, Demagny H, De Robertis EM. Integration of BMP and Wnt signaling via vertebrate Smad1/5/8 and Drosophila Mad. Cytokine Growth Factor Rev 2009, 20:357-365. doi:10.1016/j.cytogfr.2009.10.017.
62. Varelas X, Samavarchi-Tehrani P, Narimatsu M, Weiss A, Cockburn K, Larsen BG, Rossant J, Wrana JL. The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-β-SMAD pathway. Dev Cell 2010, 19:831-844. doi:10. 1016/j.devcel.2010.11.012.
63. Shi Y, Wang YF, Jayaraman L, Yang H, Massagué J, Pavletich NP. Crystal structure of a Smad MH1 domain bound to DNA: insights on DNA binding in TGF-β signaling. Cell 1998, 94:585-594. doi:10.1016/S0092-8674(00)81600-1.
64. Labbé E, Silvestri C, Hoodless PA, Wrana JL, Attisano L. Smad2 and Smad3 positively and negatively regulate TGFβ-dependent transcription through the forkhead DNA-binding protein FAST2. Mol Cell 1998, 2:109-120. doi:10.1016/S1097-2765(00)80119-7.
65. Kim J, Johnson K, Chen HJ, Carroll S, Laughon A. Drosophila Mad binds to DNA and directly mediates activation of vestigial by decapentaplegic. Nature 1997, 388:304-308. doi:10.1038/40906.
66. Zawel L, Dai JL, Buckhaults P, Zhou SB, Kinzler KW, Vogelstein B, Kern SE. Human Smad3 and Smad4 are sequence-specific transcription activators. Mol Cell 1998, 1:611-617. doi:10.1016/S1097-2765(00) 80061-1.
67. Chen X, Rubock MJ, Whitman M. A transcriptional partner for MAD proteins in TGF-β signalling. Nature 1996, 383:691-696. doi:10.1038/383691a0.
68. Deheuninck J, Luo K. Ski and SnoN, potent negative regulators of TGF-β signaling. Cell Res 2009, 19:47-57. doi:10.1038/cr.2008.324.
69. Blitz IL, Cho KWY. Finding partners: how BMPs select their targets. Dev Dyn 2009, 238:1321-1331. doi:10.1002/dvdy.21984.
70. Wharton SJ, Basu SP, Ashe HL. Smad affinity can direct distinct readouts of the embryonic extracellular Dpp gradient in Drosophila. Curr Biol 2004, 14:1550-1558. doi:10.1016/j.cub.2004.08.053.
71. Pyrowolakis G, Hartmann B, Müller B, Basler K, Affolter M. A simple molecular complex mediates widespread BMP-induced repression during Drosophila development. Dev Cell 2004, 7:229-240. doi:10.1016/j.devcel.2004.07.008.
72. Morikawa M, Koinuma D, Tsutsumi S, Vasilaki E, Kanki Y, Heldin C-H, Aburatani H, Miyazono K. ChIP-seq reveals cell type-specific binding patterns of BMP-specific Smads and a novel binding motif. Nucleic Acids Res 2011, 39:8712-8727. doi:10.1093/nar/gkr572.
73. Weiss A, Charbonnier E, Ellertsdóttir E, Tsirigos A, Wolf C, Schuh R, Pyrowolakis G, Affolter M. A conserved activation element in BMP signaling during Drosophila development. Nat Struct Mol Biol 2010, 17:69-76. doi:10.1038/nsmb.1715.
74. Mullen AC, Orlando DA, Newman JJ, Lovén J, Kumar RM, Bilodeau S, Reddy J, Guenther MG, Dekoter RP, Young RA. Master transcription factors determine cell-type-specific responses to TGF-β signaling. Cell 2011, 147:565-576. doi:10.1016/j.cell.2011.08.050.
75. Trompouki E, Bowman TV, Lawton LN, Fan ZP, Wu D-C, DiBiase A, Martin CS, Cech JN, Sessa AK, Leblanc JL, et al. Lineage regulators direct BMP and Wnt pathways to cell-specific programs during differentiation and regeneration. Cell 2011, 147:577-589. doi:10.1016/j.cell.2011.09.044.
76. Brown S, Teo A, Pauklin S, Hannan N, Cho CH-H, Lim B, Vardy L, Dunn RN, Trotter MWB, Pedersen R, et al. Activin/nodal signalling controls divergent transcriptional networks in human embryonic stem cells and in endoderm progenitors. Stem Cells 2011, 29:1176-1185. doi:10.1002/stem.666.
77. Kim SW, Yoon S-J, Chuong E, Oyolu C, Wills A, Gupta R, Baker J. Chromatin and transcriptional signatures for nodal signaling during endoderm formation in hESCs. Dev Biol 2011, 357:492-504. doi:10. 1016/j.ydbio.2011.06.009.
78. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008, 133:1106-1117. doi:10.1016/j.cell.2008.04.043.
79. Xi Q, Wang Z, Zaromytidou A-I, Zhang XH-F, Chow-Tsang L-F, Liu JX, Kim H, Barlas A, Manova-Todorova K, Kaartinen V, et al. A poised chromatin platform for TGF-β access to master regulators. Cell 2011, 147:1511-1524. doi:10.1016/j.cell.2011.11.032.
80. Dahle Ø, Kumar A, Kuehn MR. Nodal signaling recruits the histone demethylase Jmjd3 to counteract polycomb-mediated repression at target genes. Sci Signal 2010, 3:ra48. doi:10.1126/scisignal.2000841.
81. Inui M, Manfrin A, Mamidi A, Martello G, Morsut L, Soligo S, Enzo E, Moro S, Polo S, Dupont S, et al. USP15 is a deubiquitylating enzyme for receptor-activated SMADs. Nat Cell Biol 2011, 13:1368-1375. doi:10.1038/ncb2346.
82. Agricola E, Randall RA, Gaarenstroom T, Dupont S, Hill CS. Recruitment of TIF1γ to chromatin via its PHD finger-bromodomain activates its ubiquitin ligase and transcriptional repressor activities. Mol Cell 2011, 43:85-96. doi:10.1016/j.molcel.2011.05.020.
83. Dupont S, Mamidi A, Cordenonsi M, Montagner M, Zacchigna L, Adorno M, Martello G, Stinchfield MJ, Soligo S, Morsut L, et al. FAM/USP9x, a deubiquitinating enzyme essential for TGFβ signaling, controls Smad4 monoubiquitination. Cell 2009, 136:123-135. doi:10.1016/j.cell.2008.10.051.
84. He W, Dorn DC, Erdjument-Bromage H, Tempst P, Moore MAS, Massagué J. Hematopoiesis controlled by distinct TIF1γ and Smad4 branches of the TGFβ pathway. Cell 2006, 125:929-941. doi:10.1016/j.cell. 2006.03.045.
85. Grönroos E, Hellman U, Heldin C-H, Ericsson J. Control of Smad7 stability by competition between acetylation and ubiquitination. Mol Cell 2002, 10:483-493. doi:10.1016/S1097-2765(02)00639-1.
86. Lönn P, van der Heide LP, Dahl M, Hellman U, Heldin C-H, Moustakas A. PARP-1 attenuates Smad-mediated transcription. Mol Cell 2010, 40:521-532. doi:10. 1016/j.molcel.2010.10.029.
87. Alarcón C, Zaromytidou A-I, Xi Q, Gao S, Yu J, Fujisawa S, Barlas A, Miller AN, Manova-Todorova K, Macias MJ, et al. Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-β pathways. Cell 2009, 139:757-769. doi:10.1016/j. cell.2009.09.035.
88. Wang G, Matsuura I, He D, Liu F. Transforming growth factor-β-inducible phosphorylation of Smad3. J Biol Chem 2009, 284:9663-9673. doi:10.1074/ jbc.M809281200.
89. Guo X, Wang X-F. Signaling cross-talk between TGF-β/BMP and other pathways. Cell Res 2009, 19:71-88. doi:10.1038/cr.2008.302.
90. Inui M, Martello G, Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 2010, 11:252-263. doi:10.1038/nrm2868.
91. Davis BN, Hilyard AC, Nguyen PH, Lagna G, Hata A. Smad proteins bind a conserved RNA sequence to promote microRNA maturation by Drosha. Mol Cell 2010, 39:373-384. doi:10.1016/j.molcel.2010.07.011.
92. Derynck R, Miyazono K, eds. The TGF-β Family. New York, USA: Cold Spring Harbor Laboratory Press; 2007, 1114p. ISBN 9780879697525.
93. Ten Dijke P, Heldin C-H, eds. Smad Signal Transduction. Dordrecht: Springer; 2006, 486p. ISBN 9781402045424.