Home LiteratureArticle Details
PMID: 7791754 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Human type II receptor for bone morphogenic proteins (BMPs): extension of the two-kinase receptor model to the BMPs.

Molecular and cellular biology ·Vol. 15 ·No. 7 ·1995-07-00 ·Pages 3479-86

Liu F, Ventura F, Doody J, Massagué J

Abstract

Bone morphogenic proteins (BMPs) are universal regulators of animal development. We report the identification and cloning of the BMP type II receptor (BMPR-II), a missing component of this receptor system in vertebrates. BMPR-II is a transmembrane serine/threonine kinase that binds BMP-2 and BMP-7 in association with multiple type I receptors, including BMPR-IA/Brk1, BMPR-IB, and ActR-I, which is also an activin type I receptor. Cloning of BMPR-II resulted from a strong interaction of its cytoplasmic domain with diverse transforming growth factor beta family type I receptor cytoplasmic domains in a yeast two-hybrid system. In mammalian cells, however, the interaction of BMPR-II is restricted to BMP type I receptors and is ligand dependent. BMPR-II binds BMP-2 and -7 on its own, but binding is enhanced by coexpression of type I BMP receptors. BMP-2 and BMP-7 can induce a transcriptional response when added to cells coexpressing ActR-I and BMPR-II but not to cells expressing either receptor alone. The kinase activity of both receptors is essential for signaling. Thus, despite their ability to bind to type I and II receptors receptors separately, BMPs appear to require the cooperation of these two receptors for optimal binding and for signal transduction. The combinatorial nature of these receptors and their capacity to crosstalk with the activin receptor system may underlie the multifunctional nature of their ligands.

MeSH Terms
Activin Receptors Activin Receptors, Type I Amino Acid Sequence Bone Morphogenetic Protein Receptors, Type I Bone Morphogenetic Protein Receptors, Type II Bone Morphogenetic Proteins Cloning, Molecular Humans Models, Biological Molecular Sequence Data Protein Binding Protein Serine-Threonine Kinases/genetics,metabolism Proteins/metabolism Receptor, Transforming Growth Factor-beta Type I Receptors, Growth Factor/metabolism Receptors, Transforming Growth Factor beta/metabolism Saccharomyces cerevisiae/genetics Signal Transduction
Chemicals
Bone Morphogenetic Proteins Proteins Receptors, Growth Factor Receptors, Transforming Growth Factor beta Protein Serine-Threonine Kinases Activin Receptors Activin Receptors, Type I BMPR1A protein, human BMPR1B protein, human BMPR2 protein, human Bone Morphogenetic Protein Receptors, Type I Bone Morphogenetic Protein Receptors, Type II Receptor, Transforming Growth Factor-beta Type I
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Liu F
Cell Biology and Genetics Program, Memorial Sloan-Kettering Cancer Center, New York, New York 10021, USA.
Ventura F
Doody J
Massagué J
References (50)
50 references, click to expand
  1. Reconstitution and transphosphorylation of TGF-beta receptor complexes.
    EMBO J. 1994 Dec 1;13(23):5581-9 PMID: 7988555
  2. Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4.
    J Biol Chem. 1994 Jun 24;269(25):16985-8 PMID: 8006002
  3. Mxi1, a protein that specifically interacts with Max to bind Myc-Max recognition sites.
    Cell. 1993 Jan 29;72(2):223-32 PMID: 8425219
  4. GS domain mutations that constitutively activate T beta R-I, the downstream signaling component in the TGF-beta receptor complex.
    EMBO J. 1995 May 15;14(10):2199-208 PMID: 7774578
  5. The alphas, betas, and kinases of cytokine receptor complexes.
    Cell. 1993 Aug 27;74(4):587-90 PMID: 8395346
  6. Signaling activity of transforming growth factor beta type II receptors lacking specific domains in the cytoplasmic region.
    Mol Cell Biol. 1993 Dec;13(12):7239-47 PMID: 8246946
  7. Characterization of type I receptors for transforming growth factor-beta and activin.
    Science. 1994 Apr 1;264(5155):101-4 PMID: 8140412
  8. Specific interaction of type I receptors of the TGF-beta family with the immunophilin FKBP-12.
    Science. 1994 Jul 29;265(5172):674-6 PMID: 7518616
  9. A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-beta family.
    Nature. 1987 Jan 1-7;325(6099):81-4 PMID: 3467201
  10. The DVR gene family in embryonic development.
    Trends Genet. 1991 Nov-Dec;7(11-12):408-12 PMID: 1820688
  11. Identification of human activin and TGF beta type I receptors that form heteromeric kinase complexes with type II receptors.
    Cell. 1993 Nov 19;75(4):671-80 PMID: 8242742
  12. Novel regulators of bone formation: molecular clones and activities.
    Science. 1988 Dec 16;242(4885):1528-34 PMID: 3201241
  13. Growth inhibition by transforming growth factor beta (TGF-beta) type I is restored in TGF-beta-resistant hepatoma cells after expression of TGF-beta receptor type II cDNA.
    Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5359-63 PMID: 8389483
  14. Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells.
    Mol Cell Biol. 1994 Sep;14(9):5961-74 PMID: 8065329
  15. Expression cloning of the TGF-beta type II receptor, a functional transmembrane serine/threonine kinase.
    Cell. 1992 Feb 21;68(4):775-85 PMID: 1310899
  16. Transforming growth factor-beta: latent forms, binding proteins and receptors.
    Growth Factors. 1993;8(1):11-22 PMID: 8383513
  17. A novel member of the transmembrane serine/threonine kinase receptor family is specifically expressed in the gonads and in mesenchymal cells adjacent to the müllerian duct.
    Development. 1994 Jan;120(1):189-97 PMID: 8119126
  18. Characterization and relationship of Dpp receptors encoded by the saxophone and thick veins genes in Drosophila.
    Cell. 1994 Jul 29;78(2):251-61 PMID: 8044839
  19. Identification of receptors for type-beta transforming growth factor.
    Methods Enzymol. 1987;146:174-95 PMID: 2891018
  20. The TGF-beta family and its composite receptors.
    Trends Cell Biol. 1994 May;4(5):172-8 PMID: 14731645
  21. Interleukin-6 and its receptor: a paradigm for cytokines.
    Science. 1992 Oct 23;258(5082):593-7 PMID: 1411569
  22. Cloning, expression, and alternative splicing of the receptor for anti-Müllerian hormone.
    Mol Endocrinol. 1994 Aug;8(8):1006-20 PMID: 7997230
  23. A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo.
    Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10255-9 PMID: 7937936
  24. An absolute requirement for both the type II and type I receptors, punt and thick veins, for dpp signaling in vivo.
    Cell. 1995 Mar 24;80(6):889-97 PMID: 7697719
  25. Drosophila Dpp signaling is mediated by the punt gene product: a dual ligand-binding type II receptor of the TGF beta receptor family.
    Cell. 1995 Mar 24;80(6):899-908 PMID: 7697720
  26. Novel activin receptors: distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors.
    Cell. 1992 Jan 10;68(1):97-108 PMID: 1310075
  27. Distinct transforming growth factor-beta (TGF-beta) receptor subsets as determinants of cellular responsiveness to three TGF-beta isoforms.
    J Biol Chem. 1990 Nov 25;265(33):20533-8 PMID: 1700790
  28. TGF beta signals through a heteromeric protein kinase receptor complex.
    Cell. 1992 Dec 11;71(6):1003-14 PMID: 1333888
  29. Expression cloning of an activin receptor, a predicted transmembrane serine kinase.
    Cell. 1991 Jun 14;65(6):973-82 PMID: 1646080
  30. What do BMPs do in mammals? Clues from the mouse short-ear mutation.
    Trends Genet. 1994 Jan;10(1):16-21 PMID: 8146910
  31. A transforming growth factor beta type I receptor that signals to activate gene expression.
    Science. 1994 Jan 7;263(5143):87-9 PMID: 8272871
  32. Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo.
    Cell. 1992 Oct 30;71(3):451-61 PMID: 1423606
  33. Functional expression and growth factor activation of an epitope-tagged p44 mitogen-activated protein kinase, p44mapk.
    Mol Biol Cell. 1992 Jan;3(1):63-71 PMID: 1372523
  34. Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2.
    Cell. 1993 Nov 19;75(4):791-803 PMID: 8242750
  35. The TGF beta homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina.
    Cell. 1993 Dec 3;75(5):913-26 PMID: 8252627
  36. Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo.
    Cell. 1994 Oct 7;79(1):169-79 PMID: 7522972
  37. Vertebrate embryonic induction: mesodermal and neural patterning.
    Science. 1994 Oct 28;266(5185):596-604 PMID: 7939714
  38. Immunophilin-sensitive protein phosphatase action in cell signaling pathways.
    Cell. 1992 Aug 7;70(3):365-8 PMID: 1379518
  39. Identification of a Drosophila activin receptor.
    Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9475-9 PMID: 8415726
  40. Cloning of a novel type II serine/threonine kinase receptor through interaction with the type I transforming growth factor-beta receptor.
    J Biol Chem. 1995 Mar 10;270(10):5625-30 PMID: 7890683
  41. The daf-4 gene encodes a bone morphogenetic protein receptor controlling C. elegans dauer larva development.
    Nature. 1993 Oct 14;365(6447):644-9 PMID: 8413626
  42. The transforming growth factor beta family and induction of the vertebrate mesoderm: bone morphogenetic proteins are ventral inducers.
    Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10243-6 PMID: 7937933
  43. Cloning of a TGF beta type I receptor that forms a heteromeric complex with the TGF beta type II receptor.
    Cell. 1993 Nov 19;75(4):681-92 PMID: 8242743
  44. OP-1 cDNA encodes an osteogenic protein in the TGF-beta family.
    EMBO J. 1990 Jul;9(7):2085-93 PMID: 2357959
  45. Mechanism of activation of the TGF-beta receptor.
    Nature. 1994 Aug 4;370(6488):341-7 PMID: 8047140
  46. TGF-beta receptors and actions.
    Biochim Biophys Acta. 1994 May 26;1222(1):71-80 PMID: 8186268
  47. Inactivation of the type II receptor reveals two receptor pathways for the diverse TGF-beta activities.
    Science. 1993 May 28;260(5112):1335-8 PMID: 8388126
  48. Type I receptors specify growth-inhibitory and transcriptional responses to transforming growth factor beta and activin.
    Mol Cell Biol. 1994 Jun;14(6):3810-21 PMID: 8196624
  49. Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a decapentaplegic receptor.
    Cell. 1994 Jul 29;78(2):239-50 PMID: 8044838
  50. Disruption of transforming growth factor beta signaling by a mutation that prevents transphosphorylation within the receptor complex.
    Mol Cell Biol. 1995 Mar;15(3):1573-81 PMID: 7862150
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1995-07-00
Pages
3479-86
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC230584
Subset
IM
Grants
NCI NIH HHS · CA34610 · United States
Databases
GENBANK
U25110
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com