Bone morphogenetic protein receptor type II C-terminus interacts with c-Src: Implication for a role in pulmonary arterial hypertension

American Journal of Respiratory Cell and Molecular Biology

Volumn 33, Issue 5, 2005, Pages 438-446

  Wong, Wai K P ^a,b   Knowles, James A ^a   Morse, Jane H ^a  

^a New York State Psychiatric Institute ^*  (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

Bone morphogenetic protein receptor type II; c Src tyrosine kinase; Pulmonary arterial hypertension

Indexed keywords

ANGIOTENSIN RECEPTOR; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; COMPLEMENTARY DNA; CYCLIN D; CYCLIN E; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NITRIC OXIDE; OSTEOGENIC PROTEIN 1; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE; RECEPTOR SUBTYPE; SEROTONIN; SEROTONIN 2B RECEPTOR; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN HEK293; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DNA BINDING; EMBRYO; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LUNG ARTERY; LUNG VASOCONSTRICTION; MISSENSE MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE SRC; PATHOGENESIS; PULMONARY HYPERTENSION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TWO HYBRID SYSTEM; YEAST;

BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; BONE MORPHOGENETIC PROTEINS; CELLS, CULTURED; CYTOPLASM; HUMANS; HYPERTENSION, PULMONARY; IMMUNOPRECIPITATION; LUNG; MUTATION; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE KINASES; TWO-HYBRID SYSTEM TECHNIQUES; TYROSINE;

EID: 27644572195     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2005-0103OC     Document Type: Article

References (42)

1. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003;113:685-700.
2. Beppu H, Kawabata M, Hamamoto T, Chytil A, Minowa O, Noda T, Miyazono K. BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev Biol 2000;221:249-258.
3. Delot EC, Bahamonde ME, Zhao M, Lyons KM. BMP signaling is required for septation of the outflow tract of the mammalian heart. Development 2003;130:209-220.
4. Kawabata M, Chytil A, Moses HL. 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;270:5625-5630.
5. Rosenzweig BL, Imamura T, Okadome T, Cox GN, Yamashita H, ten Dijke P, Heldin CH, Miyazono K. Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc Natl Acad Sci USA 1995;92:7632-7636.
6. Liu F, Ventura F, Doody J, Massague J. Human type II receptor for bone morphogenic proteins (BMPs): extension of the two-kinase receptor model to the BMPs. Mol Cell Biol 1995;15:3479-3486.
7. Nohno T, Ishikawa T, Saito T, Hosokawa K, Noji S, Wolsing DH, Rosenbaum JS. Identification of a human type II receptor for bone morphogenetic protein-4 that forms differential heteromeric complexes with bone morphogenetic protein type I receptors. J Biol Chem 1995;270:22522-22526.
8. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhaes TR, Goodman CS. Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 2002;33:545-558.
9. Nishihara A, Watabe T, Imamura T, Miyazono K. Functional heterogeneity of bone morphogenetic protein receptor-II mutants found in patients with primary pulmonary hypertension. Mol Biol Cell 2002;13:3055-3063.
10. Thomson JR, Machado RD, Pauciulo MW, Morgan NV, Humbert M, Elliott GC, Ward K, Yacoub M, Mikhail G, Rogers P, et al. Sporadic primary pulmonary hypertension is associated with germline mutations of the gene encoding BMPR-II, a receptor member of the TGF-beta family. J Med Genet 2000;37:741-745.
11. Lane KB, Machado RD, Pauciulo MW, Thomson JR, Phillips JA 3, Loyd JE, Nichols WC, Trembath RC. Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. The International PPH Consortium. Nat Genet 2000;26:81-84.
12. Deng Z, Morse JH, Slager SL, Cuervo N, Moore KJ, Venetos G, Kalachikov S, Cayanis E, Fischer SG, Barst RJ, et al. Familial primary pulmonary hypertension (gene PPH1) is caused by mutations in the bone morphogenetic protein receptor-II gene. Am J Hum Genet 2000;67:737-744.
13. Yuan JX, Rubin LJ. Pathogenesis of pulmonary arterial hypertension: the need for multiple hits. Circulation 2005;111:534-538.
14. Rubin LJ. Primary pulmonary hypertension. N Engl J Med 1997;336:111-117.
15. Yeatman TJ. A renaissance for SRC. Nat Rev Cancer 2004;4:470-480.
16. Frame MC. Src in cancer: deregulation and consequences for cell behaviour. Biochim Biophys Acta 2002;1602:114-130.
17. Hunter T. A tail of two src's: mutatis mutandis. Cell 1987;49:1-4.
18. Nohe A, Hassel S, Ehrlich M, Neubauer F, Sebald W, Henis YI, Knaus P. The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J Biol Chem 2002;277:5330-5338.
19. Rudarakanchana N, Flanagan JA, Chen H, Upton PD, Machado R, Patel D, Trembath RC, Morrell NW. Functional analysis of bone morphogenetic protein type II receptor mutations underlying primary pulmonary hypertension. Hum Mol Genet 2002;11:1517-1525.
20. Foletta VC, Lim MA, Soosairaiah J, Kelly AP, Stanley EG, Shannon M, He W, Das S, Massague J, Bernard O. Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1. J Cell Biol 2003;162:1089-1098.
21. Machado RD, Rudarakanchana N, Atkinson C, Flanagan JA, Harrison R, Morrell NW, Trembath RC. Functional interaction between BMPR-II and Tctex-1, a light chain of Dynein, is isoform-specific and disrupted by mutations underlying primary pulmonary hypertension. Hum Mol Genet 2003;12:3277-3286.
22. Hassel S, Eichner A, Yakymovych M, Hellman U, Knaus P, Souchelnytskyi S. Proteins associated with type II bone morphogenetic protein receptor (BMPR-II) and identified by two-dimensional gel electrophoresis and mass spectrometry. Proteomics 2004;4:1346-1358.
23. Hubbard SR. Src autoinhibition: let us count the ways. Nat Struct Biol 1999;6:711-714.
24. Williams JC, Weijland A, Gonfloni S, Thompson A, Courtneidge SA, Superti-Furga G, Wierenga RK. The 2.35 A crystal structure of the inactivated form of chicken Src: a dynamic molecule with multiple regulatory interactions. J Mol Biol 1997;274:757-775.
25. Kanner SB, Reynolds AB, Vines RR, Parsons JT. Monoclonal antibodies to individual tyrosine-phosphorylated protein substrates of oncogene-encoded tyrosine kinases. Proc Natl Acad Sci USA 1990;87:3328-3332.
26. Kypta RM, Goldberg Y, Ulug ET, Courtneidge SA. Association between the PDGF receptor and members of the src family of tyrosine kinases. Cell 1990;62:481-492.
27. Oda Y, Renaux B, Bjorge J, Saifeddine M, Fujita DJ, Hollenberg MD. cSrc is a major cytosolic tyrosine kinase in vascular tissue. Can J Physiol Pharmacol 1999;77:606-617.
28. Li X, Lerea KM, Li J, Olson SC. Src kinase mediates angiotensin II-dependent increase in pulmonary endothelial nitric oxide synthase. Am J Respir Cell Mol Biol 2004;31:365-372.
29. Alloua A, Mahajan A, Nishimaru K, Zarei MM, Stefani E, Toro L. Coupling of c-Src to large conductance voltage- and Ca2+-activated K+ channels as a new mechanism of agonist-induced vasoconstriction. Proc Natl Acad Sci USA 2002;99:14560-14565.
30. Nebigil CG, Launay JM, Hickel P, Tournois C, Maroteaux L. 5-hydroxytryptamine 2B receptor regulates cell-cycle progression: cross-talk with tyrosine kinase pathways. Proc Natl Acad Sci USA 2000;97:2591-2596.
31. Abdalla SA, Gallione CJ, Barst RJ, Horn EM, Knowles JA, Marchuk DA, Letarte M, Morse JH. Primary pulmonary hypertension in families with hereditary haemorrhagic telangiectasia. Eur Respir J 2004;23:373-377.
32. Chaouat A, Coulet F, Favre C, Simonneau G, Weitzenblum E, Soubrier F, Humbert M. Endoglin germline mutation in a patient with hereditary haemorrhagic telangiectasia and dexfenfluramine associated pulmonary arterial hypertension. Thorax 2004;59:446-448.
33. Harrison RE, Berger R, Haworth SG, Tulloh R, Mache CJ, Morrell NW, Aldred MA, Trembath RC. Transforming growth factor-beta receptor mutations and pulmonary arterial hypertension in childhood. Circulation 2005;111:435-441.
34. Trembath RC, Thomson JR, Machado RD, Morgan NV, Atkinson C, Winship I, Simonneau G, Galie N, Loyd JE, Humbert M, et al. Clinical and molecular genetic features of pulmonary hypertension in patients with hereditary hemorrhagic telangiectasia. N Engl J Med 2001;345:325-334.
35. Murillo MM, del Castillo G, Sanchez A, Fernandez M, Fabregat I. Involvement of EGF receptor and c-Src in the survival signals induced by TGF-beta1 in hepatocytes. Oncogene 2005;24:4580-4587.
36. Conery AR, Cao Y, Thompson EA, Townsend CM Jr, Ko TC, Luo K. Akt interacts directly with Smad3 to regulate the sensitivity to TGF-beta induced apoptosis. Nat Cell Biol 2004;6:366-372.
37. Remy I, Montmarquette A, Michnick SW. PKB/Akt modulates TGF-beta signalling through a direct interaction with Smad3. Nat Cell Biol 2004;6:358-365.
38. Fitzgerald LW, Burn TC, Brown BS, Patterson JP, Corjay MH, Valentine PA, Sun JH, Link JR, Abbaszade I, Hollis JM, et al. Possible role of valvular serotonin 5-HT(2B) receptors in the cardiopathy associated with fenfluramine. Mol Pharmacol 2000;57:75-81.
39. Humbert M, Deng Z, Simonneau G, Barst RJ, Sitbon O, Wolf M, Cuervo N, Moore KJ, Hodge SE, Knowles JA, et al. BMPR2 germline mutations in pulmonary hypertension associated with fenfluramine derivatives. Eur Respir J 2002;20:518-523.
40. Weir EK, Reeve HL, Huang JM, Michelakis E, Nelson DP, Hampl V, Archer SL. Anorexic agents aminorex, fenfluramine, and dexfenfluramine inhibit potassium current in rat pulmonary vascular smooth muscle and cause pulmonary vasoconstriction. Circulation 1996;94:2216-2220.
41. Holmes TC, Fadool DA, Ren R, Levitan IB. Association of Src tyrosine kinase with a human potassium channel mediated by SH3 domain. Science 1996;274:2089-2091.
42. Yuan XJ, Wang J, Juhaszova M, Gaine SP, Rubin LJ. Attenuated K+ channel gene transcription in primary pulmonary hypertension. Lancet 1998;351:726-727.