Serotonin induces Rho/ROCK-dependent activation of Smads 1/5/8 in pulmonary artery smooth muscle cells

FASEB Journal

Volumn 23, Issue 7, 2009, Pages 2299-2306

  Liu, Yinglin ^a   Ren, Wenying ^a   Warburton, Rod ^a   Toksoz, Deniz ^a   Fanburg, Barry L ^a  

^a TUFTS MEDICAL CENTER   (United States)

Author keywords

5 HT; 5 HT1B receptor; BMP receptor; Pulmonary hypertension; RhoA

Indexed keywords

3 (3 DIMETHYLAMINOPROPYL) 4 HYDROXY N [4 (4 PYRIDINYL)PHENYL]BENZAMIDE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; BONE MORPHOGENETIC PROTEIN RECEPTOR; BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SERINE THREONINE KINASE; RHO FACTOR; RHO KINASE; SEROTONIN; SEROTONIN 1B RECEPTOR; SEROTONIN 1D RECEPTOR; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; RECEPTOR REGULATED SMAD PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTERY LIGATION; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; COW; CYTOPLASM; GENE OVEREXPRESSION; GENE TRANSLOCATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VIVO STUDY; INFUSION; LUNG PARENCHYMA; MOLECULAR INTERACTION; MOUSE; NONHUMAN; OSMOTIC PUMP; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PULMONARY ARTERY; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; ANIMAL; C57BL MOUSE; CATTLE; CYTOLOGY; GENETICS; METABOLISM; TRANSCRIPTION INITIATION; VASCULAR SMOOTH MUSCLE;

BOVINAE; MUS;

ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CATTLE; HUMANS; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PULMONARY ARTERY; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; SEROTONIN; SMAD PROTEINS, RECEPTOR-REGULATED; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTIONAL ACTIVATION;

EID: 68549098152     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-127910     Document Type: Article

References (34)

1. Rosenzweig, B. L., Imamura, T., Okadome, T., Cox, G. N., Yamashita, H., ten Dijke, P., Heldin, C. H., and Miyazono, K. (1995) Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc. Natl. Acad. Sci. U. S. A. 92, 7632-7636
2. Valcourt, U., Kowanetz, M., Niimi, H., Heldin, C. H., and Moustakas, A. (2005) TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Molec. Biol. Cell. 16, 1987-2002 (Pubitemid 40471965)
3. Kintscher, U., Lyon, C., Wakino, S., Bruemmer, D., Feng, X., Goetze, S., Graf, K., Moustakas, A., Staels, B., Fleck, E., Hsueh, W. A., and Law, R. E. (2002) PPARα inhibits TGF-β-induced β5 integrin transcription in vascular smooth muscle cells by interacting with Smad4. Circ. Res. 91, e35-e44
4. Yu, P. B., Beppu, H., Kawai, N., Li, E., and Bloch, K. D. (2005) Bone morphogenetic protein (BMP) type II receptor deletion reveals BMP ligand-specific gain of signaling in pulmonary artery smooth muscle cells. J. Biol. Chem. 280, 24443-24450 (Pubitemid 40934529)
5. Yu, P. B., Deng, D. Y., Beppu, H., Hong, C. C., Lai, C., Hoyng, S. A., Kawai, N., and Bloch, K. D. (2008) Bone morphogenetic protein (BMP) type II receptor is required for BMP-mediated growth arrest and differentiation in pulmonary artery smooth muscle cells. J. Biol. Chem. 283, 3877-3888
6. Morse, J. H., Deng, Z., and Knowles, J. A. (2001) Genetic aspects of pulmonary arterial hypertension. Ann. Med. 33, 596-603 (Pubitemid 34081497)
7. Thomson, J., Machado, R., Pauciulo, M., Morgan, N., Yacoub, M., Corris, P., McNeil, K., Loyd, J., Nichols, W., and Trembath, R. (2001) Familial and sporadic primary pulmonary hypertension is caused by BMPR2 gene mutations resulting in haploinsufficiency of the bone morphogenetic protein tuype II receptor. J. Heart Lung Transplant. 20, 149
8. Thomson, J. R., Machado, R. D., Pauciulo, M. W., Morgan, N. V., Humbert, M., Elliott, G. C., Ward, K., Yacoub, M., Mikhail, G., Rogers, P., Newman, J., Wheeler, L., Higenbottam, T., Gibbs, J. S., Egan, J., Crozier, A., Peacock, A., Allcock, R., Corris, P., Loyd, J. E., Trembath, R. C., and Nichols, W. C. (2000) Sporadic primary pulmonary hypertension is associated with germline mutations of the gene encoding BMPR-II, a receptor member of the TGF-β family. J. Med. Genet. 37, 741-745 (Pubitemid 30793785)
9. Atkinson, C., Stewart, S., Upton, P. D., Machado, R., Thomson, J. R., Trembath, R. C., and Morrell, N. W. (2002) Primary pulmonary hypertension is associated with reduced pulmonary vascular expression of type II bone morphogenetic protein receptor. Circulation 105, 1672-1678 (Pubitemid 34298611)
10. Adnot, S., and Eddahibi, S. (2003) [Genetics and physiopathology of primary or secondary pulmonary artery hypertension]. Bull. Acad. Natl. Med. 187, 1529-1542; discussion 1543-11525
11. Herve, P., Drouet, L., Dosquet, C., Launay, J. M., Rain, B., Simonneau, G., Caen, J., and Duroux, P. (1990) Primary pulmonary hypertension in a patient with a familial platelet storage pool disease: role of serotonin. Am. J. Med. 89, 117-120 (Pubitemid 20196727)
12. Jian, B., Xu, J., Connolly, J., Savani, R. C., Narula, N., Liang, B., and Levy, R. J. (2002) Serotonin mechanisms in heart valve disease I: serotonin-induced up-regulation of transforming growth factor-beta1 via G-protein signal transduction in aortic valve interstitial cells. Am. J. Pathol. 161, 2111-2121 (Pubitemid 35434857)
13. Grewal, J. S., Mukhin, Y. V., Garnovskaya, M. N., Raymond, J. R., and Greene, E. L. (1999) Serotonin 5-HT2A receptor induces TGF-beta1 expression in mesangial cells via ERK: proliferative and fibrotic signals. Am. J. Physiol. 276, F922-F930
14. Long, L., MacLean, M. R., Jeffery, T. K., Morecroft, I., Yang, X., Rudarakanchana, N., Southwood, M., James, V., Trembath, R. C., and Morrell, N. W. (2006) Serotonin increases susceptibility to pulmonary hypertension in BMPR2-deficient mice. Circ. Res. 98, 818-827 (Pubitemid 43755266)
15. Edlund, S., Landstrom, M., Heldin, C. H., and Aspenstrom, P. (2002) Transforming growth factor-beta-induced mobilization of actin cytoskeleton requires signaling by small GTPases Cdc42 and RhoA. Molec. Biol. Cell 13, 902-914 (Pubitemid 34250354)
16. Kamaraju, A. K., and Roberts, A. B. (2005) Role of Rho/ROCK and p38 MAP kinase pathways in transforming growth factor-β-mediated Smad-dependent growth inhibition of human breast carcinoma cells in vivo. J. Biol. Chem. 280, 1024-1036
17. Lee, S. L., Wang, W. W., Moore, B. J., and Fanburg, B. L. (1991) Dual effect of serotonin on growth of bovine pulmonary artery smooth muscle cells in culture. Circ. Res. 68, 1362-1368
18. Lee, S. L., Wang, W. W., Finlay, G. A., and Fanburg, B. L. (1999) Serotonin stimulates mitogen-activated protein kinase activity through the formation of superoxide anion. Am. J. Physiol. Lung Physiol. 277, L282-L291
19. Liu, Y., and Fanburg, B. L. (2006) Serotonin-induced growth of pulmonary artery smooth muscle requires activation of phosphatidylinositol 3-kinase/serine-threonine protein kinase B/mammalian target of rapamycin/p70 ribosomal S6 kinase 1. Am. J. Respir. Cell Mol. Biol. 34, 182-191 (Pubitemid 43202465)
20. Liu, Y., Suzuki, Y. J., Day, R. M., and Fanburg, B. L. (2004) Rho kinase-induced nuclear translocation of ERK1/ERK2 in smooth muscle cell mitogenesis caused by serotonin. Circ. Res. 95, 579-586 (Pubitemid 39274372)
21. Liu, Y., Li, M., Warburton, R. R., Hill, N. S., and Fanburg, B. L. (2007) The 5-HT transporter transactivates the PDGFβ receptor in pulmonary artery smooth muscle cells. FASEB J. 21, 2725-2734 (Pubitemid 47372740)
22. Liu, Y., and Fanburg, B. L. (2008) Phospholipase D signaling in serotonin-induced mitogenesis of pulmonary artery smooth muscle cells. Am. J. Physiol. 295, L471-L478
23. Day, R. M., Agyeman, A. S., Segel, M. J., Chevere, R. D., Angelosanto, J. M., Suzuki, Y. J., and Fanburg, B. L. (2006) Serotonin induces pulmonary artery smooth muscle cell migration. Biochem. Pharmacol. 71, 386-397 (Pubitemid 41817297)
24. Foletta, V. C., Lim, M. A., Soosairajah, J., Kelly, A. P., Stanley, E. G., Shannon, M., He, W., Das, S., Massague, J., and Bernard, O. (2003) Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1. J. Cell Biol. 162, 1089-1098 (Pubitemid 37174191)
25. Wen, Z., Han, L., Bamburg, J. R., Shim, S., Ming, G. L., and Zheng, J. Q. (2007) BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin. J. Cell Biol. 178, 107-119 (Pubitemid 47026406)
26. Theriault, B. L., Shepherd, T. G., Mujoomdar, M. L., and Nachtigal, M. W. (2007) BMP4 induces EMT and Rho GTPase activation in human ovarian cancer cells. Carcinogenesis 28, 1153-1162
27. Eguchi, S., and Inagami, T. (2000) Signal transduction of angiotensin II type 1 receptor through receptor tyrosine kinase. Regul. Pept. 91, 13-20 (Pubitemid 30674465)
28. Heeneman, S., Haendeler, J., Saito, Y., Ishida, M., and Berk, B. C. (2000) Angiotensin II induces transactivation of two different populations of the platelet-derived growth factor beta receptor. Key role for the p66 adaptor protein Shc. J. Biol. Chem. 275, 15926-15932 (Pubitemid 30366895)
29. Nicholl, S. M., Roztocil, E., and Davies, M. G. (2005) Urokinase-induced smooth muscle cell responses require distinct signaling pathways: a role for the epidermal growth factor receptor. J. Vasc. Surg. 41, 672-681 (Pubitemid 40637668)
30. Voisin, L., Foisy, S., Giasson, E., Lambert, C., Moreau, P., and Meloche, S. (2002) EGF receptor transactivation is obligatory for protein synthesis stimulation by G protein-coupled receptors. Am. J. Physiol. Cell. Physiol. 283, C446-C455 (Pubitemid 34787527)
31. Yang, C. M., Lin, M. I., Hsieh, H. L., Sun, C. C., Ma, Y. H., and Hsiao, L. D. (2005) Bradykinin-induced p42/p44 MAPK phosphorylation and cell proliferation via Src, EGF receptors, and PI3-K/Akt in vascular smooth muscle cells. J. Cell. Physiol. 203, 538-546
32. Rudarakanchana, N., Flanagan, J. A., Chen, H., Upton, P. D., Machado, R., Patel, D., Trembath, R. C., and Morrell, N. W. (2002) Functional analysis of bone morphogenetic protein type II receptor mutations underlying primary pulmonary hypertension. Hum. Molec. Genet. 11, 1517-1525 (Pubitemid 34679252)
33. Sztrymf, B., Yaici, A., Jais, X., Sitbon, O., Simonneau, G., and Humbert, M. (2005) Idiopathic pulmonary hypertension: what did we learn from genes? Sarcoidosis Vasc. Diffuse Lung Dis. 22(Suppl. 1), S91-S100 (Pubitemid 43166297)
34. De Caestecker, M., and Meyrick, B. (2001) Bone morphogenetic proteins, genetics and the pathophysiology of primary pulmonary hypertension. Respir. Res. 2, 193-197 (Pubitemid 34187926)