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Journal of Cell Science, Vol 112, Issue 24 4557-4568, Copyright © 1999 by Company of Biologists

JOURNAL ARTICLES

TGF-(beta) type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells

E Piek, A Moustakas, A Kurisaki, CH Heldin and P ten Dijke
Ludwig Institute for Cancer Research, Box 595, S-75124 Uppsala, Sweden.

The capacities of different transforming growth factor-(beta) (TGF-(beta)) superfamily members to drive epithelial to mesenchymal transdifferentiation of the murine mammary epithelial cell line NMuMG were investigated. TGF-(beta)1, but not activin A or osteogenic protein-1 (OP-1)/bone morphogenetic protein-7 (BMP-7), was able to induce morphological transformation of NMuMG cells as shown by reorganisation of the actin cytoskeleton and relocalisation/downregulation of E-cadherin and (beta)-catenin, an effect that was abrogated by the more general serine/threonine kinase and protein kinase C inhibitor, staurosporine. TGF-(beta)1 bound to TGF-(beta) type I receptor (T(beta)R-I)/ALK-5 and T(beta)R-II, but not to activin type I receptor (ActR-I)/ALK-2. Activin A bound to ActR-IB/ALK-4 and ActR-II, and BMP-7 bound to ActR-I/ALK-2, BMP type I receptor (BMPR-I)/ALK-3, ActR-II and BMPR-II. TGF-(beta)1 and BMP-7 activated the Smad-binding element (SBE)(4) promoter with equal potency, whereas activin A had no effect. Transfection of constitutively active (CA)-ALK-4 activated the 3TP promoter to the same extent as TGF-(beta)1 and CA-ALK-5 indicating that activin signalling downstream of type I receptors was functional in NMuMG cells. In agreement with this, activin A induced low levels of plasminogen activator inhibitor I expression compared to the high induction by TGF-(beta)1. In contrast to activin A and BMP-7, TGF-(beta)1 strongly induced Smad2 phosphorylation. Consistent with these findings, TGF-(beta)1 induced the nuclear accumulation of Smad2 and/or Smad3. In addition, NMuMG cells transiently infected with adenoviral vectors expressing high level CA-ALK-5 exhibited full transdifferentiation. On the other hand, infections with low level CA-ALK-5, which alone did not result in transdifferentiation, together with Smad2 and Smad4, or with Smad3 and Smad4 led to transdifferentiation. In conclusion, TGF-(beta)1 signals potently and passes the activation threshold to evoke NMuMG cell transdifferentiation. The TGF-(beta) type I receptor (ALK-5) and its effector Smad proteins mediate the epithelial to mesenchymal transition. Activin A does not induce mesenchymal transformation, presumably because the number of activin receptors is limited, while BMP-7-initiated signalling cannot mediate transdifferentiation.
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N. Dumont, A. V. Bakin, and C. L. Arteaga
Autocrine Transforming Growth Factor-beta Signaling Mediates Smad-independent Motility in Human Cancer Cells
J. Biol. Chem., January 24, 2003; 278(5): 3275 - 3285.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
M. Grande, A. Franzen, J.-O. Karlsson, L. E. Ericson, N.-E. Heldin, and M. Nilsson
Transforming growth factor-{beta} and epidermal growth factor synergistically stimulate epithelial to mesenchymal transition (EMT) through a MEK-dependent mechanism in primary cultured pig thyrocytes
J. Cell Sci., November 15, 2002; 115(22): 4227 - 4236.
[Abstract] [Full Text] [PDF]

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 Mol Cancer ResHome page
F. Valdes, A. M. Alvarez, A. Locascio, S. Vega, B. Herrera, M. Fernandez, M. Benito, M. A. Nieto, and I. Fabregat
The Epithelial Mesenchymal Transition Confers Resistance to the Apoptotic Effects of Transforming Growth Factor {beta} in Fetal Rat Hepatocytes
Mol. Cancer Res., November 1, 2002; 1(1): 68 - 78.
[Abstract] [Full Text] [PDF]

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 J. Am. Soc. Nephrol.Home page
E. P. Bottinger and M. Bitzer
TGF-{beta} Signaling in Renal Disease
J. Am. Soc. Nephrol., October 1, 2002; 13(10): 2600 - 2610.
[Abstract] [Full Text] [PDF]

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 Hum Mol GenetHome page
N. Rudarakanchana, J. A. Flanagan, H. Chen, P. D. Upton, R. Machado, D. Patel, R. C. Trembath, and N. W. Morrell
Functional analysis of bone morphogenetic protein type II receptor mutations underlying primary pulmonary hypertension
Hum. Mol. Genet., June 15, 2002; 11(13): 1517 - 1525.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
J. Gotzmann, H. Huber, C. Thallinger, M. Wolschek, B. Jansen, R. Schulte-Hermann, H. Beug, and W. Mikulits
Hepatocytes convert to a fibroblastoid phenotype through the cooperation of TGF-{beta}1 and Ha-Ras: steps towards invasiveness
J. Cell Sci., March 15, 2002; 115(6): 1189 - 1202.
[Abstract] [Full Text] [PDF]

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 Mol. Biol. CellHome page
S. Edlund, M. Landstrom, C.-H. Heldin, and P. Aspenstrom
Transforming Growth Factor-beta -induced Mobilization of Actin Cytoskeleton Requires Signaling by Small GTPases Cdc42 and RhoA
Mol. Biol. Cell, March 1, 2002; 13(3): 902 - 914.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
A. V. Bakin, C. Rinehart, A. K. Tomlinson, and C. L. Arteaga
p38 mitogen-activated protein kinase is required for TGF{beta}-mediated fibroblastic transdifferentiation and cell migration
J. Cell Sci., January 8, 2002; 115(15): 3193 - 3206.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
L. You and F. E. Kruse
Differential Effect of Activin A and BMP-7 on Myofibroblast Differentiation and the Role of the Smad Signaling Pathway
Invest. Ophthalmol. Vis. Sci., January 1, 2002; 43(1): 72 - 81.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
N. A. Bhowmick, R. Zent, M. Ghiassi, M. McDonnell, and H. L. Moses
Integrin beta 1 Signaling Is Necessary for Transforming Growth Factor-beta Activation of p38MAPK and Epithelial Plasticity
J. Biol. Chem., December 7, 2001; 276(50): 46707 - 46713.
[Abstract] [Full Text] [PDF]

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 J. Am. Soc. Nephrol.Home page
S.-N. WANG, J. LAPAGE, and R. HIRSCHBERG
Loss of Tubular Bone Morphogenetic Protein--7 in Diabetic Nephropathy
J. Am. Soc. Nephrol., November 1, 2001; 12(11): 2392 - 2399.
[Abstract] [Full Text] [PDF]

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 Mol. Biol. CellHome page
I. Shin, A. V. Bakin, U. Rodeck, A. Brunet, and C. L. Arteaga
Transforming Growth Factor beta Enhances Epithelial Cell Survival via Akt-dependent Regulation of FKHRL1
Mol. Biol. Cell, November 1, 2001; 12(11): 3328 - 3339.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
P. J. Stahl and D. Felsen
Transforming Growth Factor-{beta}, Basement Membrane, and Epithelial-Mesenchymal Transdifferentiation : Implications for Fibrosis in Kidney Disease
Am. J. Pathol., October 1, 2001; 159(4): 1187 - 1192.
[Full Text]

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 Proc. Natl. Acad. Sci. USAHome page
J. Zavadil, M. Bitzer, D. Liang, Y.-C. Yang, A. Massimi, S. Kneitz, E. Piek, and E. P. Bottinger
Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta
PNAS, June 5, 2001; 98(12): 6686 - 6691.
[Abstract] [Full Text] [PDF]

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 Mol. Biol. CellHome page
N. A. Bhowmick, M. Ghiassi, A. Bakin, M. Aakre, C. A. Lundquist, M. E. Engel, C. L. Arteaga, and H. L. Moses
Transforming Growth Factor-{beta}1 Mediates Epithelial to Mesenchymal Transdifferentiation through a RhoA-dependent Mechanism
Mol. Biol. Cell, January 1, 2001; 12(1): 27 - 36.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
A. V. Bakin, A. K. Tomlinson, N. A. Bhowmick, H. L. Moses, and C. L. Arteaga
Phosphatidylinositol 3-Kinase Function Is Required for Transforming Growth Factor beta -mediated Epithelial to Mesenchymal Transition and Cell Migration
J. Biol. Chem., November 17, 2000; 275(47): 36803 - 36810.
[Abstract] [Full Text] [PDF]

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 JCBHome page
E. Janda, K. Lehmann, I. Killisch, M. Jechlinger, M. Herzig, J. Downward, H. Beug, and S. Grunert
Ras and TGF{beta} cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways
J. Cell Biol., January 21, 2002; 156(2): 299 - 314.
[Abstract] [Full Text] [PDF]


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