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Endocrine Reviews 23 (6): 787-823
Copyright © 2002 by The Endocrine Society

Genetic Analysis of the Mammalian Transforming Growth Factor-ß Superfamily

Hua Chang, Chester W. Brown and Martin M. Matzuk

Departments of Pathology (H.C., M.M.M.), Molecular and Human Genetics (C.W.B., M.M.M.), Molecular and Cellular Biology (M.M.M.), and Pediatrics (C.W.B.), and Program in Developmental Biology (H.C., M.M.M.), Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030

Correspondence: Address all correspondence and requests for reprints to: Martin M. Matzuk, M.D., Ph.D., The Stuart A. Wallace Chair and Professor, Department of Pathology, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030. E-mail: mmatzuk{at}bcm.tmc.edu

Members of the TGF-ß superfamily, which includes TGF-ßs, growth differentiation factors, bone morphogenetic proteins, activins, inhibins, and glial cell line-derived neurotrophic factor, are synthesized as prepropeptide precursors and then processed and secreted as homodimers or heterodimers. Most ligands of the family signal through transmembrane serine/threonine kinase receptors and SMAD proteins to regulate cellular functions. Many studies have reported the characterization of knockout and knock-in transgenic mice as well as humans or other mammals with naturally occurring genetic mutations in superfamily members or their regulatory proteins. These investigations have revealed that TGF-ß superfamily ligands, receptors, SMADs, and upstream and downstream regulators function in diverse developmental and physiological pathways. This review attempts to collate and integrate the extensive body of in vivo mammalian studies produced over the last decade.




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L McClure, A E O'Connor, S Hayward, G Jenkin, D W Walker, and D J Phillips
Effects of age and pregnancy on the circulatory activin response of sheep to acute inflammatory challenge by lipopolysaccharide
J. Endocrinol., April 1, 2005; 185(1): 139 - 149.
[Abstract] [Full Text] [PDF]

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 ReproductionHome page
K. P McNatty, J. L Juengel, K. L Reader, S. Lun, S. Myllymaa, S. B Lawrence, A. Western, M. F Meerasahib, D. G Mottershead, N. P Groome, et al.
Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function
Reproduction, April 1, 2005; 129(4): 473 - 480.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
B. D. Cherrington, T. A. Farmerie, C. A. Lents, J. D. Cantlon, M. S. Roberson, and C. M. Clay
Activin Responsiveness of the Murine Gonadotropin-Releasing Hormone Receptor Gene Is Mediated by a Composite Enhancer Containing Spatially Distinct Regulatory Elements
Mol. Endocrinol., April 1, 2005; 19(4): 898 - 912.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. P. Sarker, S. M. Wilson, and S. Bonni
SnoN Is a Cell Type-specific Mediator of Transforming Growth Factor-{beta} Responses
J. Biol. Chem., April 1, 2005; 280(13): 13037 - 13046.
[Abstract] [Full Text] [PDF]

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 Mol. Biol. CellHome page
U. Valcourt, M. Kowanetz, H. Niimi, C.-H. Heldin, and A. Moustakas
TGF-{beta} and the Smad Signaling Pathway Support Transcriptomic Reprogramming during Epithelial-Mesenchymal Cell Transition
Mol. Biol. Cell, April 1, 2005; 16(4): 1987 - 2002.
[Abstract] [Full Text] [PDF]

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 Hum Reprod UpdateHome page
J.L. Juengel and K.P. McNatty
The role of proteins of the transforming growth factor-{beta} superfamily in the intraovarian regulation of follicular development
Hum. Reprod. Update, March 1, 2005; 11(2): 144 - 161.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
D. S. Wilkinson, S. K. Ogden, S. A. Stratton, J. L. Piechan, T. T. Nguyen, G. A. Smulian, and M. C. Barton
A Direct Intersection between p53 and Transforming Growth Factor {beta} Pathways Targets Chromatin Modification and Transcription Repression of the {alpha}-Fetoprotein Gene
Mol. Cell. Biol., February 1, 2005; 25(3): 1200 - 1212.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. Bostrom, A. F. Zebboudj, Y. Yao, T. S. Lin, and A. Torres
Matrix GLA Protein Stimulates VEGF Expression through Increased Transforming Growth Factor-{beta}1 Activity in Endothelial Cells
J. Biol. Chem., December 17, 2004; 279(51): 52904 - 52913.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
E. del Re, Y. Sidis, D. A. Fabrizio, H. Y. Lin, and A. Schneyer
Reconstitution and Analysis of Soluble Inhibin and Activin Receptor Complexes in a Cell-free System
J. Biol. Chem., December 17, 2004; 279(51): 53126 - 53135.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
G. Xu, Y. Zhong, S. Munir, B. B. Yang, B. K. Tsang, and C. Peng
Nodal Induces Apoptosis and Inhibits Proliferation in Human Epithelial Ovarian Cancer Cells via Activin Receptor-Like Kinase 7
J. Clin. Endocrinol. Metab., November 1, 2004; 89(11): 5523 - 5534.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
L. Wine-Lee, K. J. Ahn, R. D. Richardson, Y. Mishina, K. M. Lyons, and E. B. Crenshaw III
Signaling through BMP type 1 receptors is required for development of interneuron cell types in the dorsal spinal cord
Development, November 1, 2004; 131(21): 5393 - 5403.
[Abstract] [Full Text] [PDF]

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 ReproductionHome page
K P McNatty, L G Moore, N L Hudson, L D Quirke, S B Lawrence, K Reader, J P Hanrahan, P Smith, N P Groome, M Laitinen, et al.
The oocyte and its role in regulating ovulation rate: a new paradigm in reproductive biology
Reproduction, October 1, 2004; 128(4): 379 - 386.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
K. Bein, E. T. Odell-Fiddler, and M. Drinane
Role of TGF-{beta}1 and JNK signaling in capillary tube patterning
Am J Physiol Cell Physiol, October 1, 2004; 287(4): C1012 - C1022.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
R. M. Monteiro, S. M. C. de Sousa Lopes, O. Korchynskyi, P. t. Dijke, and C. L. Mummery
Spatio-temporal activation of Smad1 and Smad5 in vivo: monitoring transcriptional activity of Smad proteins
J. Cell Sci., September 15, 2004; 117(20): 4653 - 4663.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
D. Tomic, K. P. Miller, H. A. Kenny, T. K. Woodruff, P. Hoyer, and J. A. Flaws
Ovarian Follicle Development Requires Smad3
Mol. Endocrinol., September 1, 2004; 18(9): 2224 - 2240.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
I. Yakymovych, C.-H. Heldin, and S. Souchelnytskyi
Smad2 Phosphorylation by Type I Receptor: CONTRIBUTION OF ARGININE 462 AND CYSTEINE 463 IN THE C TERMINUS OF SMAD2 FOR SPECIFICITY
J. Biol. Chem., August 20, 2004; 279(34): 35781 - 35787.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
T. M. Doherty, L. A. Fitzpatrick, D. Inoue, J.-H. Qiao, M. C. Fishbein, R. C. Detrano, P. K. Shah, and T. B. Rajavashisth
Molecular, Endocrine, and Genetic Mechanisms of Arterial Calcification
Endocr. Rev., August 1, 2004; 25(4): 629 - 672.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. A. Pangas, C. J. Jorgez, and M. M. Matzuk
Growth Differentiation Factor 9 Regulates Expression of the Bone Morphogenetic Protein Antagonist Gremlin
J. Biol. Chem., July 30, 2004; 279(31): 32281 - 32286.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Munir, G. Xu, Y. Wu, B. Yang, P. K. Lala, and C. Peng
Nodal and ALK7 Inhibit Proliferation and Induce Apoptosis in Human Trophoblast Cells
J. Biol. Chem., July 23, 2004; 279(30): 31277 - 31286.
[Abstract] [Full Text] [PDF]

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 Exp. Biol. Med.Home page
M. H. Zile
Vitamin A Requirement for Early Cardiovascular Morphogenesis Specification in the Vertebrate Embryo: Insights from the Avian Embryo
Experimental Biology and Medicine, July 1, 2004; 229(7): 598 - 606.
[Abstract] [Full Text] [PDF]

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 Stem CellsHome page
T. J. Sadlon, I. D. Lewis, and R. J. D'Andrea
BMP4: Its Role in Development of the Hematopoietic System and Potential as a Hematopoietic Growth Factor
Stem Cells, July 1, 2004; 22(4): 457 - 474.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
X. Wu, L. Chen, C. A. Brown, C. Yan, and M. M. Matzuk
Interrelationship of Growth Differentiation Factor 9 and Inhibin in Early Folliculogenesis and Ovarian Tumorigenesis in Mice
Mol. Endocrinol., June 1, 2004; 18(6): 1509 - 1519.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Sudo, O. Avsian-Kretchmer, L. S. Wang, and A. J. W. Hsueh
Protein Related to DAN and Cerberus Is a Bone Morphogenetic Protein Antagonist That Participates in Ovarian Paracrine Regulation
J. Biol. Chem., May 28, 2004; 279(22): 23134 - 23141.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
S. Chen and R. J. Lechleider
Transforming Growth Factor-{beta}-Induced Differentiation of Smooth Muscle From a Neural Crest Stem Cell Line
Circ. Res., May 14, 2004; 94(9): 1195 - 1202.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
W. X. Liao, R. K. Moore, and S. Shimasaki
Functional and Molecular Characterization of Naturally Occurring Mutations in the Oocyte-secreted Factors Bone Morphogenetic Protein-15 and Growth and Differentiation Factor-9
J. Biol. Chem., April 23, 2004; 279(17): 17391 - 17396.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. O. Brown III, X. Chi, E. Garcia-Gras, M. Shirai, X.-H. Feng, and R. J. Schwartz
The Cardiac Determination Factor, Nkx2-5, Is Activated by Mutual Cofactors GATA-4 and Smad1/4 via a Novel Upstream Enhancer
J. Biol. Chem., March 12, 2004; 279(11): 10659 - 10669.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
J. L. Carey, L. M. Sasur, H. Kawakubo, V. Gupta, B. Christian, P. M. Bailey, and S. Maheswaran
Mutually Antagonistic Effects of Androgen and Activin in the Regulation of Prostate Cancer Cell Growth
Mol. Endocrinol., March 1, 2004; 18(3): 696 - 707.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
D. J. Bernard
Both SMAD2 and SMAD3 Mediate Activin-Stimulated Expression of the Follicle-Stimulating Hormone {beta} Subunit in Mouse Gonadotrope Cells
Mol. Endocrinol., March 1, 2004; 18(3): 606 - 623.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
S. Shimasaki, R. K. Moore, F. Otsuka, and G. F. Erickson
The Bone Morphogenetic Protein System In Mammalian Reproduction
Endocr. Rev., February 1, 2004; 25(1): 72 - 101.
[Abstract] [Full Text] [PDF]


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