Hypoxia enhances platelet-derived growth factor signaling in the pulmonary vasculature by down-regulation of protein tyrosine phosphatases

American Journal of Respiratory and Critical Care Medicine

Volumn 183, Issue 8, 2011, Pages 1092-1102

  Freyhaus, Henrik Ten ^a   Dagnell, Markus ^b   Leuchs, Maike ^a   Vantler, Marius ^a   Berghausen, Eva M ^a   Caglayan, Evren ^a   Weissmann, Norbert ^c   Dahal, Bhola K ^c   Schermuly, Ralph T ^c,d   Östman, Arne ^b   Kappert, Kai ^e   Rosenkranz, Stephan ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b KAROLINSKA INSTITUTE   (Sweden)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Hypoxia; Platelet derived growth factor; Protein tyrosine phosphatases; Pulmonary hypertension; Vascular remodeling

Indexed keywords

2 METHOXYESTRADIOL; DENSITY ENHANCED PHOSPHATASE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PLC GAMMA PROTEIN; PROTEIN; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE 1B; PROTEIN TYROSINE PHOSPHATASE SHP; SMALL INTERFERING RNA; T LYMPHOCYTE PROTEIN TYROSINE PHOSPHATASE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY MUSCLE; ARTICLE; BINDING SITE; CELL PROLIFERATION; CHEMOTAXIS; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE CONTROL; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOXIA; LUNG ARTERY; LUNG BLOOD VESSEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PULMONARY HYPERTENSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

ANIMALS; ANOXIA; CELL PROLIFERATION; CELLS, CULTURED; CHEMOTAXIS; DOWN-REGULATION; HUMANS; HYPERTENSION, PULMONARY; LUNG; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; PLATELET-DERIVED GROWTH FACTOR; PROTEIN TYROSINE PHOSPHATASES; PULMONARY ARTERY; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; SIGNAL TRANSDUCTION;

EID: 79954585192     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200911-1663OC     Document Type: Article

References (48)

1. Perros F, Montani D, Dorfmuller P, Durand-Gasselin I, Tcherakian C, Le Pavec J, Mazmanian M, Fadel E, Mussot S, Mercier O, et al. Plateletderived growth factor expression and function in idiopathic pulmonary arterial hypertension. Am J Respir Crit Care Med 2008;178:81-88. (Pubitemid 351919196)
2. Schermuly RT, Dony E, Ghofrani HA, Pullamsetti S, Savai R, Roth M, Sydykov A, Lai YJ, Weissmann N, Seeger W, et al. Reversal of experimental pulmonary hypertension by PDGF inhibition. J Clin Invest 2005;115:2811-2821. (Pubitemid 41434408)
3. Gerasimovskaya EV, Tucker DA, Stenmark KR. Activation of phosphatidylinositol 3-kinase, Akt, and mammalian target of rapamycin is necessary for hypoxia-induced pulmonary artery adventitial fibroblast proliferation. J Appl Physiol 2005;98:722-731. (Pubitemid 40129988)
4. Das M, Burns N, Wilson SJ, Zawada WM, Stenmark KR. Hypoxia exposure induces the emergence of fibroblasts lacking replication repressor signals of PKCzeta in the pulmonary artery adventitia. Cardiovasc Res 2008;78:440-448. (Pubitemid 351769755)
5. Rosenkranz S, DeMali KA, Gelderloos JA, Bazenet C, Kazlauskas A. Identification of the receptor-associated signaling enzymes that are required for platelet-derived growth factor-AA-dependent chemotaxis and DNA synthesis. J Biol Chem 1999;274:28335-28343.
6. ten Freyhaus H, Huntgeburth M, Wingler K, Schnitker J, Baumer AT, Vantler M, Bekhite MM, Wartenberg M, Sauer H, Rosenkranz S. Novel Nox inhibitor VAS2870 attenuates PDGF-dependent smooth muscle cell chemotaxis, but not proliferation. Cardiovasc Res 2006;71:331-341.
7. Baumer AT, Ten Freyhaus H, Sauer H, Wartenberg M, Kappert K, Schnabel P, Konkol C, Hescheler J, Vantler M, Rosenkranz S. Pi3 kinase-dependent membrane recruitment of rac-1 and p47phox is critical for alpha PDGF receptor-induced production of reactive oxygen species. J Biol Chem 2007;283:7864-7876.
8. Sano H, Sudo T, Yokode M, Murayama T, Kataoka H, Takakura N, Nishikawa S, Nishikawa SI, Kita T. Functional blockade of plateletderived growth factor receptor-beta but not of receptor-alpha prevents vascular smooth muscle cell accumulation in fibrous cap lesions in apolipoprotein E-deficient mice. Circulation 2001;103:2955-2960. (Pubitemid 32578134)
9. Hart CE, Kraiss LW, Vergel S, Gilbertson D, Kenagy R, Kirkman T, Crandall DL, Tickle S, Finney H, Yarranton G, et al. PDGFbeta receptor blockade inhibits intimal hyperplasia in the baboon. Circulation 1999;99:564-569. (Pubitemid 29061874)
10. Heldin CH, Westermark B. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 1999;79:1283-1316. (Pubitemid 29473317)
11. Kerkela R, Grazette L, Yacobi R, Iliescu C, Patten R, Beahm C, Walters B, Shevtsov S, Pesant S, Clubb FJ, et al. Cardiotoxicity of the cancer therapeutic agent imatinib mesylate. Nat Med 2006;12:908-916. (Pubitemid 44175142)
12. Kappert K, Peters KG, Bohmer FD, Ostman A. Tyrosine phosphatases in vessel wall signaling. Cardiovasc Res 2005;65:587-598. (Pubitemid 40138979)
13. Elchebly M, Payette P, Michaliszyn E, Cromlish W, Collins S, Loy AL, Normandin D, Cheng A, Himms-Hagen J, Chan CC, et al. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 1999;283:1544-1548.
14. Persson C, Savenhed C, Bourdeau A, Tremblay ML, Markova B, Bohmer FD, Haj FG, Neel BG, Elson A, Heldin CH, et al. Siteselective regulation of platelet-derived growth factor beta receptor tyrosine phosphorylation by T-cell protein tyrosine phosphatase. Mol Cell Biol 2004;24:2190-2201. (Pubitemid 38248956)
15. Haj FG, Markova B, Klaman LD, Bohmer FD, Neel BG. Regulation of receptor tyrosine kinase signaling by protein tyrosine phosphatase-1B. J Biol Chem 2003;278:739-744. (Pubitemid 36790744)
16. Jandt E, Denner K, Kovalenko M, Ostman A, Bohmer FD. The proteintyrosine phosphatase DEP-1 modulates growth factor-stimulated cell migration and cell-matrix adhesion. Oncogene 2003;22:4175-4185. (Pubitemid 36876238)
17. Nakata S, Fujita N, Kitagawa Y, Okamoto R, Ogita H, Takai Y. Regulation of platelet-derived growth factor receptor activation by afadin through SHP-2: implications for cellular morphology. J Biol Chem 2007;282:37815-37825.
18. Meyrick B, Reid L. Hypoxia and incorporation of 3H-thymidine by cells of the rat pulmonary arteries and alveolar wall. Am J Pathol 1979;96:51-70. (Pubitemid 9215513)
19. Dempsey EC, McMurtry IF, O'Brien RF. Protein kinase C activation allows pulmonary artery smooth muscle cells to proliferate to hypoxia. Am J Physiol 1991;260:L136-L145.
20. Xu Y, Stenmark KR, Das M, Walchak SJ, Ruff LJ, Dempsey EC. Pulmonary artery smooth muscle cells from chronically hypoxic neonatal calves retain fetal-like and acquire new growth properties. Am J Physiol 1997;273:L234-L245.
21. Schultz K, Fanburg BL, Beasley D. Hypoxia and hypoxia-inducible factor-1alpha promote growth factor-induced proliferation of human vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 2006;290:H2528-H2534. (Pubitemid 43846084)
22. Benitz WE, Coulson JD, Lessler DS, Bernfield M. Hypoxia inhibits proliferation of fetal pulmonary arterial smooth muscle cells in vitro. Pediatr Res 1986;20:966-972. (Pubitemid 16021194)
23. ten Freyhaus H, Leuchs M, Dagnell M, Vantler M, Caglayan E, Weissmann N, Schermuly R, Dahal B, Östman A, Kappert K, et al. Hypoxia enhances platelet-derived growth factor signaling in the pulmonary vasculature by HIF-1-dependent downregulation of protein tyrosine phosphatases. Circulation 2009;120:S1146.
24. Dahal BK, Cornitescu T, Tretyn A, Pullamsetti SS, Kosanovic D, Dumitrascu R, Ghofrani HA, Weissmann N, Voswinckel R, Banat GA, et al. Role of epidermal growth factor inhibition in experimental pulmonary hypertension. Am J Respir Crit Care Med 2009;181:158-167.
25. Sorby M, Sandstrom J, Ostman A. An extracellular ligand increases the specific activity of the receptor-like protein tyrosine phosphatase DEP-1. Oncogene 2001;20:5219-5224. (Pubitemid 32844052)
26. Vantler M, Caglayan E, Zimmermann WH, Baumer AT, Rosenkranz S. Systematic evaluation of anti-apoptotic growth factor signaling in vascular smooth muscle cells. Only phosphatidylinositol 39-kinase is important. J Biol Chem 2005;280:14168-14176. (Pubitemid 40517319)
27. Kappert K, Paulsson J, Sparwel J, Leppanen O, Hellberg C, Ostman A, Micke P. Dynamic changes in the expression of DEP-1 and other PDGF receptor-antagonizing PTPs during onset and termination of neointima formation. FASEB J 2007;21:523-534. (Pubitemid 46213499)
28. Mabjeesh NJ, Escuin D, LaVallee TM, Pribluda VS, Swartz GM, Johnson MS, Willard MT, Zhong H, Simons JW, Giannakakou P. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell 2003;3:363-375. (Pubitemid 38340305)
29. Katayose D, Ohe M, Yamauchi K, Ogata M, Shirato K, Fujita H, Shibahara S, Takishima T. Increased expression of PDGF A-and B-chain genes in rat lungs with hypoxic pulmonary hypertension. Am J Physiol 1993;264:L100-L106. (Pubitemid 23079462)
30. Balasubramaniam V, Le Cras TD, Ivy DD, Grover TR, Kinsella JP, Abman SH. Role of platelet-derived growth factor in vascular remodeling during pulmonary hypertension in the ovine fetus. Am J Physiol Lung Cell Mol Physiol 2003;284:L826-L833. (Pubitemid 36459029)
31. Pak O, Aldashev A, Welsh D, Peacock A. The effects of hypoxia on the cells of the pulmonary vasculature. Eur Respir J 2007;30:364-372. (Pubitemid 47201724)
32. Lanner MC, Raper M, Pratt WM, Rhoades RA. Heterotrimeric G proteins and the PDGFR-fbetag contribute to hypoxic proliferation of smooth muscle cells. Am J Respir Cell Mol Biol 2005;283:412-419. (Pubitemid 41416293)
33. Valius M, Kazlauskas A. Phospholipase C-gamma 1 and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptor's mitogenic signal. Cell 1993;73:321-334. (Pubitemid 23123310)
34. Liu Y, Li M, Warburton RR, Hill NS, Fanburg BL. The 5-HT transporter transactivates the PDGFbeta receptor in pulmonary artery smooth muscle cells. FASEB J 2007;21:2725-2734. (Pubitemid 47372740)
35. Frid MG, Aldashev AA, Dempsey EC, Stenmark KR. Smooth muscle cells isolated from discrete compartments of the mature vascular media exhibit unique phenotypes and distinct growth capabilities. Circ Res 1997;81:940-952. (Pubitemid 27514943)
36. Dempsey EC, Das M, Frid MG, Xu Y, Stenmark KR. Hypoxic growth of bovine pulmonary artery smooth muscle cells: dependence on synergy, heterogeneity, and injury-induced phenotypic change. Chest 1998;114:29S-30S. (Pubitemid 28334846)
37. Ostman A, Hellberg C, Bohmer FD. Protein-tyrosine phosphatases and cancer. Nat Rev Cancer 2006;6:307-320.
38. Tonks NK, Muthuswamy SK. A brake becomes an accelerator: PTP1B-a new therapeutic target for breast cancer. Cancer Cell 2007;11:214-216. (Pubitemid 46349848)
39. Kovalenko M, Denner K, Sandstrom J, Persson C, Gross S, Jandt E, Vilella R, Bohmer F, Ostman A. Site-selective dephosphorylation of the platelet-derived growth factor beta-receptor by the receptor-like protein-tyrosine phosphatase DEP-1. J Biol Chem 2000;275:16219-16226. (Pubitemid 30366934)
40. Zakrzewicz A, Kouri FM, Nejman B, Kwapiszewska G, Hecker M, Sandu R, Dony E, Seeger W, Schermuly RT, Eickelberg O, et al. The transforming growth factor-beta/Smad2, 3 signalling axis is impaired in experimental pulmonary hypertension. Eur Respir J 2007;29:1094-1104. (Pubitemid 46895367)
41. Morrell NW, Upton PD, Kotecha S, Huntley A, Yacoub MH, Polak JM, Wharton J. Angiotensin II activates MAPK and stimulates growth of human pulmonary artery smooth muscle via AT1 receptors. Am J Physiol 1999;277:L440-L448. (Pubitemid 29459662)
42. Bonello S, Zahringer C, Bel Aiba RS, Djordjevic T, Hess J, Michiels C, Kietzmann T, Gorlach A. Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol 2007;27:755-761. (Pubitemid 46606703)
43. Ruas JL, Lendahl U, Poellinger L. Modulation of vascular gene expression by hypoxia. Curr Opin Lipidol 2007;18:508-514. (Pubitemid 47462202)
44. Dahut WL, Lakhani NJ, Gulley JL, Arlen PM, Kohn EC, Kotz H, McNally D, Parr A, Nguyen D, Yang SX, et al. Phase I clinical trial of oral 2-methoxyestradiol, an antiangiogenic and apoptotic agent, in patients with solid tumors. Cancer Biol Ther 2006;5:22-27. (Pubitemid 43234973)
45. Sweeney C, Liu G, Yiannoutsos C, Kolesar J, Horvath D, Staab MJ, Fife K, Armstrong V, Treston A, Sidor C, et al. A phase II multicenter, randomized, double-blind, safety trial assessing the pharmacokinetics, pharmacodynamics, and efficacy of oral 2-methoxyestradiol capsules in hormone-refractory prostate cancer. Clin Cancer Res 2005;11:6625-6633. (Pubitemid 41339003)
46. Tofovic SP, Zhang X, Jackson EK, Dacic S, Petrusevska G. 2-Methoxyestradiol mediates the protective effects of estradiol in monocrotalineinduced pulmonary hypertension. Vascul Pharmacol 2006;45:358-367. (Pubitemid 44765298)
47. Ghofrani HA, Seeger W, Grimminger F. Imatinib for the treatment of pulmonary arterial hypertension. N Engl J Med 2005;353:1412-1413. (Pubitemid 41362714)
48. Chang Y, Ceacareanu B, Zhuang D, Zhang C, Pu Q, Ceacareanu AC, Hassid A. Counter-regulatory function of protein tyrosine phosphatase 1B in platelet-derived growth factor-or fibroblast growth factorinduced motility and proliferation of cultured smooth muscle cells and in neointima formation. Arterioscler Thromb Vasc Biol 2006;26:501-507.