Non-Smad signaling pathways
- Yabing Mu,
- Shyam Kumar Gudey,
- Maréne Landström
- … show all 3 hide
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Abstract
Transforming growth factor-beta (TGFβ) is a key regulator of cell fate during embryogenesis and has also emerged as a potent driver of the epithelial-mesenchymal transition during tumor progression. TGFβ signals are transduced by transmembrane type I and type II serine/threonine kinase receptors (TβRI and TβRII, respectively). The activated TβR complex phosphorylates Smad2 and Smad3, converting them into transcriptional regulators that complex with Smad4. TGFβ also uses non-Smad signaling pathways such as the p38 and Jun N-terminal kinase (JNK) mitogen-activated protein kinase (MAPK) pathways to convey its signals. Ubiquitin ligase tumor necrosis factor (TNF)-receptor-associated factor 6 (TRAF6) and TGFβ-associated kinase 1 (TAK1) have recently been shown to be crucial for the activation of the p38 and JNK MAPK pathways. Other TGFβ-induced non-Smad signaling pathways include the phosphoinositide 3-kinase-Akt-mTOR pathway, the small GTPases Rho, Rac, and Cdc42, and the Ras-Erk-MAPK pathway. Signals induced by TGFβ are tightly regulated and specified by post-translational modifications of the signaling components, since they dictate the subcellular localization, activity, and duration of the signal. In this review, we discuss recent findings in the field of TGFβ-induced responses by non-Smad signaling pathways.
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- Introduction
- Activation of the type I TGFβ receptor
- The receptors as platforms for the initiation of the Erk-MAPK signaling pathways
- TNF-receptor-associated factor 6 and TAK1 associate with the receptors and are important for TGFβ signaling to p38 MAPK and the EMT
- Smad7 acts as an adaptor protein to cause activation of non-Smad signaling pathways
- The phosphoinositide 3-kinase-Akt pathway
- Small GTPases and TGFβ signaling
- TGFβ receptors and the regulation of Par6 are involved in the EMT
- Cross-talk with integrin signaling pathways
- Non-Smad signals in relation to Smads
- Concluding remarks
- References
- References
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References (88)
- Adhikari A, Xu M, Chen ZJ (2007) Ubiquitin-mediated activation of TAK1 and IKK. Oncogene 26:3214–3226 CrossRef
- Adorno M, Cordenonsi M, Montagner M, Dupont S, Wong C, Hann B, Solari A, Bobisse S, Rondina MB, Guzzardo V, Parenti AR, Rosato A, Bicciato S, Balmain A, Piccolo S (2009) A mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis. Cell 137:87–98 CrossRef
- Bakin AV, Tomlinson AK, Bhowmick NA, Moses HL, Arteaga CL (2000) Phosphatidylinositol 3-kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition and cell migration. J Biol Chem 275:36803–36810 CrossRef
- Bandyopadhyay B, Han A, Dai J, Fan J, Li Y, Chen M, Woodley DT, Li W (2011) TbetaRI/Alk5-independent TbetaRII signaling to ERK1/2 in human skin cells according to distinct levels of TbetaRII expression. J Cell Sci 124:19–24 CrossRef
- Bettermann K, Vucur M, Haybaeck J, Koppe C, Janssen J, Heymann F, Weber A, Weiskirchen R, Liedtke C, Gassler N, Muller M, Vos R de, Wolf MJ, Boege Y, Seleznik GM, Zeller N, Erny D, Fuchs T, Zoller S, Cairo S, Buendia MA, Prinz M, Akira S, Tacke F, Heikenwalder M, Trautwein C, Luedde T (2010) TAK1 suppresses a NEMO-dependent but NF-kappaB-independent pathway to liver cancer. Cancer Cell 17:481–496 CrossRef
- Bhowmick NA, Zent R, Ghiassi M, McDonnell M, Moses HL (2001) Integrin beta 1 signaling is necessary for transforming growth factor-beta activation of p38MAPK and epithelial plasticity. J Biol Chem 276:46707–46713 CrossRef
- Brodin G, Ahgren A, Dijke P ten, Heldin CH, Heuchel R (2000) Efficient TGF-beta induction of the Smad7 gene requires cooperation between AP-1, Sp1, and Smad proteins on the mouse Smad7 promoter. J Biol Chem 275:29023–29030 CrossRef
- Cao Z, Xiong J, Takeuchi M, Kurama T, Goeddel DV (1996) TRAF6 is a signal transducer for interleukin-1. Nature 383:443–446 CrossRef
- Cheng H, Liu P, Wang ZC, Zou L, Santiago S, Garbitt V, Gjoerup OV, Iglehart JD, Miron A, Richardson AL, Hahn WC, Zhao JJ (2009) SIK1 couples LKB1 to p53-dependent anoikis and suppresses metastasis. Sci Signal 2:ra35 CrossRef
- Cordenonsi M, Montagner M, Adorno M, Zacchigna L, Martello G, Mamidi A, Soligo S, Dupont S, Piccolo S (2007) Integration of TGF-beta and Ras/MAPK signaling through p53 phosphorylation. Science 315:840–843 CrossRef
- Denissova NG, Pouponnot C, Long J, He D, Liu F (2000) Transforming growth factor beta-inducible independent binding of SMAD to the Smad7 promoter. Proc Natl Acad Sci USA 97:6397–6402 CrossRef
- Dhillon AS, Hagan S, Rath O, Kolch W (2007) MAP kinase signalling pathways in cancer. Oncogene 26:3279–3290 CrossRef
- DiVito KA, Trabosh VA, Chen YS, Chen Y, Albanese C, Javelaud D, Mauviel A, Simbulan-Rosenthal CM, Rosenthal DS (2010) Smad7 restricts melanoma invasion by restoring N-cadherin expression and establishing heterotypic cell-cell interactions in vivo. Pigment Cell Melanoma Res 23:795–808 CrossRef
- Dupont S, Mamidi A, Cordenonsi M, Montagner M, Zacchigna L, Adorno M, Martello G, Stinchfield MJ, Soligo S, Morsut L, Inui M, Moro S, Modena N, Argenton F, Newfeld SJ, Piccolo S (2009) FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell 136:123–135 CrossRef
- Ebisawa T, Fukuchi M, Murakami G, Chiba T, Tanaka K, Imamura T, Miyazono K (2001) Smurf1 interacts with transforming growth factor-beta type I receptor through Smad7 and induces receptor degradation. J Biol Chem 276:12477–12480 CrossRef
- Edlund S, Landstrom M, Heldin CH, Aspenstrom P (2002) Transforming growth factor-beta-induced mobilization of actin cytoskeleton requires signaling by small GTPases Cdc42 and RhoA. Mol Biol Cell 13:902–914 CrossRef
- Edlund S, Bu S, Schuster N, Aspenstrom P, Heuchel R, Heldin NE, Dijke P ten, Heldin CH, Landstrom M (2003) Transforming growth factor-beta1 (TGF-beta)-induced apoptosis of prostate cancer cells involves Smad7-dependent activation of p38 by TGF-beta-activated kinase 1 and mitogen-activated protein kinase kinase 3. Mol Biol Cell 14:529–544 CrossRef
- Edlund S, Landstrom M, Heldin CH, Aspenstrom P (2004) Smad7 is required for TGF-beta-induced activation of the small GTPase Cdc42. J Cell Sci 117:1835–1847 CrossRef
- Edlund S, Lee SY, Grimsby S, Zhang S, Aspenstrom P, Heldin CH, Landstrom M (2005) Interaction between Smad7 and beta-catenin: importance for transforming growth factor beta-induced apoptosis. Mol Cell Biol 25:1475–1488 CrossRef
- Feng XH, Derynck R (2005) Specificity and versatility in TGF-beta signaling through Smads. Annu Rev Cell Dev Biol 21:659–693 CrossRef
- Funaba M, Zimmerman CM, Mathews LS (2002) Modulation of Smad2-mediated signaling by extracellular signal-regulated kinase. J Biol Chem 277:41361–41368 CrossRef
- Galliher AJ, Schiemann WP (2007) Src phosphorylates Tyr284 in TGF-beta type II receptor and regulates TGF-beta stimulation of p38 MAPK during breast cancer cell proliferation and invasion. Cancer Res 67:3752–3758 CrossRef
- Gingery A, Bradley EW, Pederson L, Ruan M, Horwood NJ, Oursler MJ (2008) TGF-beta coordinately activates TAK1/MEK/AKT/NFkB and SMAD pathways to promote osteoclast survival. Exp Cell Res 314:2725–2738 CrossRef
- Greenblatt MB, Shim JH, Zou W, Sitara D, Schweitzer M, Hu D, Lotinun S, Sano Y, Baron R, Park JM, Arthur S, Xie M, Schneider MD, Zhai B, Gygi S, Davis R, Glimcher LH (2010) The p38 MAPK pathway is essential for skeletogenesis and bone homeostasis in mice. J Clin Invest 120:2457–2473 CrossRef
- Grivennikov SI, Greten FR, Karin M (2010) Immunity, inflammation, and cancer. Cell 140:883–899 CrossRef
- Groppe J, Hinck CS, Samavarchi-Tehrani P, Zubieta C, Schuermann JP, Taylor AB, Schwarz PM, Wrana JL, Hinck AP (2008) Cooperative assembly of TGF-beta superfamily signaling complexes is mediated by two disparate mechanisms and distinct modes of receptor binding. Mol Cell 29:157–168 CrossRef
- Guo X, Wang XF (2009) Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res 19:71–88 CrossRef
- Han G, Li AG, Liang YY, Owens P, He W, Lu S, Yoshimatsu Y, Wang D, Dijke P ten, Lin X, Wang XJ (2006) Smad7-induced beta-catenin degradation alters epidermal appendage development. Dev Cell 11:301–312 CrossRef
- Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674 CrossRef
- Hayashida T, Decaestecker M, Schnaper HW (2003) Cross-talk between ERK MAP kinase and Smad signaling pathways enhances TGF-beta-dependent responses in human mesangial cells. FASEB J 17:1576–1578
- He G, Yu GY, Temkin V, Ogata H, Kuntzen C, Sakurai T, Sieghart W, Peck-Radosavljevic M, Leffert HL, Karin M (2010) Hepatocyte IKKbeta/NF-kappaB inhibits tumor promotion and progression by preventing oxidative stress-driven STAT3 activation. Cancer Cell 17:286–297 CrossRef
- He W, Dorn DC, Erdjument-Bromage H, Tempst P, Moore MA, Massagué J (2006) Hematopoiesis controlled by distinct TIF1gamma and Smad4 branches of the TGFbeta pathway. Cell 125:929–941 CrossRef
- Heide LP van der, Dinther M van, Moustakas A, Dijke P ten (2011) TGFbeta activates mitogen- and stress-activated protein kinase-1 (MSK1) to attenuate cell death. J Biol Chem 286:5003–5011 CrossRef
- Heldin CH, Miyazono K, Dijke P ten (1997) TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390:465–471 CrossRef
- Heldin CH, Landstrom M, Moustakas A (2009) Mechanism of TGF-beta signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition. Curr Opin Cell Biol 21:166–176 CrossRef
- Huang T, David L, Mendoza V, Yang Y, Villarreal M, De K, Sun L, Fang X, Lopez-Casillas F, Wrana JL, Hinck AP (2011) TGF-beta signalling is mediated by two autonomously functioning TbetaRI:TbetaRII pairs. EMBO J 30:1263–1276 CrossRef
- Ikushima H, Miyazono K (2010) TGFbeta signalling: a complex web in cancer progression. Nat Rev Cancer 10:415–424 CrossRef
- Ishida T, Mizushima S, Azuma S, Kobayashi N, Tojo T, Suzuki K, Aizawa S, Watanabe T, Mosialos G, Kieff E, Yamamoto T, Inoue J (1996) Identification of TRAF6, a novel tumor necrosis factor receptor-associated factor protein that mediates signaling from an amino-terminal domain of the CD40 cytoplasmic region. J Biol Chem 271:28745–28748 CrossRef
- Janda E, Lehmann K, Killisch I, Jechlinger M, Herzig M, Downward J, Beug H, Grunert S (2002) Ras and TGF[beta] cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 156:299–313 CrossRef
- Kamiya Y, Miyazono K, Miyazawa K (2010) Smad7 inhibits transforming growth factor-beta family type i receptors through two distinct modes of interaction. J Biol Chem 285:30804–30813 CrossRef
- Kang JS, Liu C, Derynck R (2009) New regulatory mechanisms of TGF-beta receptor function. Trends Cell Biol 19:385–394 CrossRef
- Kim SI, Kwak JH, Na HJ, Kim JK, Ding Y, Choi ME (2009) Transforming growth factor-beta (TGF-beta1) activates TAK1 via TAB1-mediated autophosphorylation, independent of TGF-beta receptor kinase activity in mesangial cells. J Biol Chem 284:22285–22296 CrossRef
- Kiyono K, Suzuki HI, Matsuyama H, Morishita Y, Komuro A, Kano MR, Sugimoto K, Miyazono K (2009) Autophagy is activated by TGF-beta and potentiates TGF-beta-mediated growth inhibition in human hepatocellular carcinoma cells. Cancer Res 69:8844–8852 CrossRef
- Kowanetz M, Lonn P, Vanlandewijck M, Kowanetz K, Heldin CH, Moustakas A (2008) TGFbeta induces SIK to negatively regulate type I receptor kinase signaling. J Cell Biol 182:655–662 CrossRef
- Kretzschmar M, Liu F, Hata A, Doody J, Massagué J (1997) The TGF-beta family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev 11:984–995 CrossRef
- Lamar JM, Iyer V, DiPersio CM (2008) Integrin alpha3beta1 potentiates TGFbeta-mediated induction of MMP-9 in immortalized keratinocytes. J Invest Dermatol 128:575–586
- Lamouille S, Derynck R (2007) Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J Cell Biol 178:437–451 CrossRef
- Lamouille S, Derynck R (2011) Emergence of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin axis in transforming growth factor-beta-induced epithelial-mesenchymal transition. Cells Tissues Organs 193:8–22 CrossRef
- Landstrom M (2010) The TAK1-TRAF6 signalling pathway. Int J Biochem Cell Biol 42:585–589 CrossRef
- Lawler S, Feng XH, Chen RH, Maruoka EM, Turck CW, Griswold-Prenner I, Derynck R (1997) The type II transforming growth factor-beta receptor autophosphorylates not only on serine and threonine but also on tyrosine residues. J Biol Chem 272:14850–14859 CrossRef
- Lee MK, Pardoux C, Hall MC, Lee PS, Warburton D, Qing J, Smith SM, Derynck R (2007) TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA. EMBO J 26:3957–3967 CrossRef
- Liu C, Xu P, Lamouille S, Xu J, Derynck R (2009) TACE-mediated ectodomain shedding of the type I TGF-beta receptor downregulates TGF-beta signaling. Mol Cell 35:26–36 CrossRef
- Lo RS, Wotton D, Massagué J (2001) Epidermal growth factor signaling via Ras controls the Smad transcriptional co-repressor TGIF. EMBO J 20:128–136 CrossRef
- Luedde T, Beraza N, Kotsikoris V, Loo G van, Nenci A, De Vos R, Roskams T, Trautwein C, Pasparakis M (2007) Deletion of NEMO/IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 11:119–132 CrossRef
- Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298:1912–1934 CrossRef
- Margadant C, Sonnenberg A (2010) Integrin-TGF-beta crosstalk in fibrosis, cancer and wound healing. EMBO Rep 11:97–105 CrossRef
- Massagué J (2008) TGFbeta in cancer. Cell 134:215–230 CrossRef
- Moren A, Raja E, Heldin CH, Moustakas A (2011) Negative regulation of TGFbeta signaling by the kinase LKB1 and the scaffolding protein LIP1. J Biol Chem 286:341–353 CrossRef
- Moustakas A, Heldin CH (2005) Non-Smad TGF-beta signals. J Cell Sci 118:3573–3584 CrossRef
- Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, Pittet JF, Kaminski N, Garat C, Matthay MA, Rifkin DB, Sheppard D (1999) The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96:319–328 CrossRef
- Nagarajan RP, Zhang J, Li W, Chen Y (1999) Regulation of Smad7 promoter by direct association with Smad3 and Smad4. J Biol Chem 274:33412–33418 CrossRef
- Neil JR, Schiemann WP (2008) Altered TAB1:I kappaB kinase interaction promotes transforming growth factor beta-mediated nuclear factor-kappaB activation during breast cancer progression. Cancer Res 68:1462–1470 CrossRef
- Oft M, Peli J, Rudaz C, Schwarz H, Beug H, Reichmann E (1996) TGF-beta1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev 10:2462–2477 CrossRef
- Ozdamar B, Bose R, Barrios-Rodiles M, Wang HR, Zhang Y, Wrana JL (2005) Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science 307:1603–1609 CrossRef
- Pechkovsky DV, Scaffidi AK, Hackett TL, Ballard J, Shaheen F, Thompson PJ, Thannickal VJ, Knight DA (2008) Transforming growth factor beta1 induces alphavbeta3 integrin expression in human lung fibroblasts via a beta3 integrin-, c-Src-, and p38 MAPK-dependent pathway. J Biol Chem 283:12898–12908 CrossRef
- Pessah M, Marais J, Prunier C, Ferrand N, Lallemand F, Mauviel A, Atfi A (2002) c-Jun associates with the oncoprotein Ski and suppresses Smad2 transcriptional activity. J Biol Chem 277:29094–29100 CrossRef
- Rincon M, Davis RJ (2009) Regulation of the immune response by stress-activated protein kinases. Immunol Rev 228:212–224 CrossRef
- Schlessinger J (2000) Cell signaling by receptor tyrosine kinases. Cell 103:211–225 CrossRef
- Shaw RJ (2009) Tumor suppression by LKB1: SIK-ness prevents metastasis. Sci Signal 2:pe55 CrossRef
- Sorrentino A, Thakur N, Grimsby S, Marcusson A, Bulow V von, Schuster N, Zhang S, Heldin CH, Landstrom M (2008) The type I TGF-beta receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner. Nat Cell Biol 10:1199–1207 CrossRef
- Wagner EF, Nebreda AR (2009) Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 9:537–549 CrossRef
- Wakefield LM, Roberts AB (2002) TGF-beta signaling: positive and negative effects on tumorigenesis. Curr Opin Genet Dev 12:22–29 CrossRef
- Wilkes MC, Murphy SJ, Garamszegi N, Leof EB (2003) Cell-type-specific activation of PAK2 by transforming growth factor beta independent of Smad2 and Smad3. Mol Cell Biol 23:8878–8889 CrossRef
- Wilkes MC, Mitchell H, Penheiter SG, Dore JJ, Suzuki K, Edens M, Sharma DK, Pagano RE, Leof EB (2005) Transforming growth factor-beta activation of phosphatidylinositol 3-kinase is independent of Smad2 and Smad3 and regulates fibroblast responses via p21-activated kinase-2. Cancer Res 65:10431–10440 CrossRef
- Wrana JL, Attisano L, Wieser R, Ventura F, Massagué J (1994) Mechanism of activation of the TGF-beta receptor. Nature 370:341–347 CrossRef
- Xie M, Zhang D, Dyck JR, Li Y, Zhang H, Morishima M, Mann DL, Taffet GE, Baldini A, Khoury DS, Schneider MD (2006) A pivotal role for endogenous TGF-beta-activated kinase-1 in the LKB1/AMP-activated protein kinase energy-sensor pathway. Proc Natl Acad Sci USA 103:17378–17383 CrossRef
- Xu X, Han J, Ito Y, Bringas P Jr, Deng C, Chai Y (2008) Ectodermal Smad4 and p38 MAPK are functionally redundant in mediating TGF-beta/BMP signaling during tooth and palate development. Dev Cell 15:322–329 CrossRef
- Yamaguchi K, Shirakabe K, Shibuya H, Irie K, Oishi I, Ueno N, Taniguchi T, Nishida E, Matsumoto K (1995) Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science 270:2008–2011 CrossRef
- Yamashita H, Dijke P ten, Franzen P, Miyazono K, Heldin CH (1994) Formation of hetero-oligomeric complexes of type I and type II receptors for transforming growth factor-beta. J Biol Chem 269:20172–20178
- Yamashita M, Fatyol K, Jin C, Wang X, Liu Z, Zhang YE (2008) TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta. Mol Cell 31:918–924 CrossRef
- Yan X, Chen YG (2011) Smad7: not only a regulator, but also a cross-talk mediator of TGF-beta signalling. Biochem J 434:1–10 CrossRef
- Yi JY, Shin I, Arteaga CL (2005) Type I transforming growth factor beta receptor binds to and activates phosphatidylinositol 3-kinase. J Biol Chem 280:10870–10876 CrossRef
- Yu N, Kozlowski JM, Park II, Chen L, Zhang Q, Xu D, Doll JA, Crawford SE, Brendler CB, Lee C (2010) Overexpression of transforming growth factor beta1 in malignant prostate cells is partly caused by a runaway of TGF-beta1 auto-induction mediated through a defective recruitment of protein phosphatase 2A by TGF-beta type I receptor. Urology 76:e1518–e1513 CrossRef
- Zhang S, Ekman M, Thakur N, Bu S, Davoodpour P, Grimsby S, Tagami S, Heldin CH, Landstrom M (2006) TGFbeta1-induced activation of ATM and p53 mediates apoptosis in a Smad7-dependent manner. Cell Cycle 5:2787–2795 CrossRef
- Zhang W, Jiang Y, Wang Q, Ma X, Xiao Z, Zuo W, Fang X, Chen YG (2009) Single-molecule imaging reveals transforming growth factor-beta-induced type II receptor dimerization. Proc Natl Acad Sci USA 106:15679–15683 CrossRef
- Zhang W, Yuan J, Yang Y, Xu L, Wang Q, Zuo W, Fang X, Chen YG (2010) Monomeric type I and type III transforming growth factor-beta receptors and their dimerization revealed by single-molecule imaging. Cell Res 20:1216–1223 CrossRef
- Zhang YE (2009) Non-Smad pathways in TGF-beta signaling. Cell Res 19:128–139 CrossRef
- Zhu HJ, Iaria J, Sizeland AM (1999) Smad7 differentially regulates transforming growth factor beta-mediated signaling pathways. J Biol Chem 274:32258–32264 CrossRef
About this Article
- Title
- Non-Smad signaling pathways
- Journal
-
Cell and Tissue Research
Volume 347, Issue 1 , pp 11-20 - Cover Date
- 2012-01-01
- DOI
- 10.1007/s00441-011-1201-y
- Print ISSN
- 0302-766X
- Online ISSN
- 1432-0878
- Publisher
- Springer-Verlag
- Additional Links
- Topics
- Keywords
-
- Non-Smads
- Smads
- TAK1
- TGFβ
- TRAF6
- Industry Sectors
- Authors
-
- Yabing Mu (1) (2)
- Shyam Kumar Gudey (1)
-
Maréne Landström
(1)
(2)
- Author Affiliations
-
- 1. Medical Biosciences, Umeå University, SE-901 85, Umeå, Sweden
- 2. Ludwig Institute for Cancer Research, Uppsala University, SE-751 24, Uppsala, Sweden