Differential effects of TGF-β1 and BMP-4 on the hypoxic induction of cyclooxygenase-2 in human pulmonary artery smooth muscle cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 287, Issue 5 31-5, 2004, Pages

  Sheares, Karen K K ^a   Jeffery, Trina K ^a   Long, Lu ^a   Yang, Xudong ^a   Morrell, Nicholas W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Bone morphogenetic protein; Hypoxia; Prostaglandins; Pulmonary hypertension; Transforming growth factor 1

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CYCLOOXYGENASE 2; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN; PROTEIN KINASE B; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; AUTOCRINE EFFECT; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME INHIBITION; HUMAN; HUMAN CELL; HYPOXIA; LUNG BLOOD VESSEL; LUNG CIRCULATION; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERY; PULMONARY HYPERTENSION; SMOOTH MUSCLE FIBER;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANOXIA; ANTIBODIES; BONE MORPHOGENETIC PROTEINS; CELLS, CULTURED; CYCLOOXYGENASE 2; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; HYPERTENSION, PULMONARY; ISOENZYMES; MEMBRANE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUSCLE, SMOOTH, VASCULAR; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; PULMONARY ARTERY; SMAD PROTEINS; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 6344248758     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00012.2004     Document Type: Article

References (49)

1. Alvarez-Tejado M, Naranjo-Suarez S, Jimenez C, Carrera AC, Landazuri MO, and del Peso L. Hypoxia induces the activation of the phosphatidylinositol 3-kinase/Akt cell survival pathway in PC12 cells: protective role in apoptosis. J Biol Chem 276: 22368-22374, 2001.
2. Blancher C, Moore JW, Robertson N, and Harris AL. Effects of ras and von Hippel-Lindau (VHL) gene mutations on hypoxia-inducible factor (HIF)-1α, HIF-2α, and vascular endothelial growth factor expression and their regulation by the phosphatidylinositol 3-kinase/Akt signaling pathway. Cancer Res 61: 7349-7355, 2001.
3. Botney MD, Parks WC, Crouch EC, Stenmark K, and Mecham RP. Transforming growth factor-β1 is decreased in remodeling hypertensive bovine pulmonary arteries. J Clin Invest 89: 1629-1635, 1992.
4. Bradbury DA, Newton R, Zhu YM, Stocks J, Corbett L, Holland ED, Pang LH, and Knox AJ. Effect of bradykinin, TGF-β1, IL-1β, and hypoxia on COX-2 expression in pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 283: L717-L725, 2002.
5. Chen YG, Hata A, Lo RS, Wotton D, Shi Y, Pavletich N, and Massague J. Determinants of specificity in TGF-β signal transduction. Genes Dev 12: 2144-2152, 1998.
6. Cocolakis E, Lemay S, Ali S, and Lebrun JJ. The p38 MAPK pathway is required for cell growth inhibition of human breast cancer cells in response to activin. J Biol Chem 276: 18430-18436, 2001.
7. Das M, Bouchey DM, Moore MJ, Hopkins DC, Nemenoff RA, and Stenmark KR. Hypoxia-induced proliferative response of vascular adventitial fibroblasts is dependent on G protein-mediated activation of mitogen-activated protein kinases. J Biol Chem 276: 15631-15640, 2001.
8. Deng Z, Morse JH, Slager SL, Cuervo N, Moore KJ, Venetos G, Kalachikov S, Cayanis E, Fischer SG, Barst RJ, Hodge SE, and Knowles JA. Familial primary pulmonary hypertension (gene PPH1) is caused by mutations in the bone morphogenetic protein receptor-II gene. Am J Hum Genet 67: 737-744, 2000.
9. 2 release in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 279: L201-L207, 2000.
10. Fruman DA and Cantley LC. Phosphoinositide 3-kinase in immunological systems. Semin Immunol 14: 7-18, 2002.
11. Geraci MW, Gao B, Shepherd DC, Moore MD, Westcott JY, Fagan KA, Alger LA, Tuder RM, and Voelkel NF. Pulmonary prostacyclin synthase overexpression in transgenic mice protects against development of hypoxic pulmonary hypertension. J Clin Invest 103: 1509-1515, 1999.
12. Goldberg PL, MacNaughton DE, Clements RT, Minnear FL, and Vincent PA. p38 MAPK activation by TGF-β1 increases MLC phosphorylation and endothelial monolayer permeability. Am J Physiol Lung Cell Mol Physiol 282: L146-L154, 2002.
13. Goncharova EA, Ammit AJ, Irani C, Carroll RG, Eszterhas AJ, Panettieri RA, and Krymskaya VP. PI3K is required for proliferation and migration of human pulmonary vascular smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 283: L354-L363, 2002.
14. Guan Z, Baier LD, and Morrison AR. p38 Mitogen-activated protein kinase down-regulates nitric oxide and up-regulates prostaglandin E2 biosynthesis stimulated by interleukin-1β. J Biol Chem 272: 8083-8089, 1997.
15. 2-terminal kinase and p38 MAPK signal pathways in rat renal mesangial cells. J Biol Chem 273: 28670-28676, 1998.
16. Guan Z, Buckman SY, Pentland AP, Templeton DJ, and Morrison AR. Induction of cyclooxygenase-2 by the activated MEKK1 -→ SEK1/MKK4 -→ p38 mitogen-activated protein kinase pathway. J Biol Chem 273: 12901-12908, 1998.
17. Hartsough MT and Mulder KM. Transforming growth factor β activation of p44mapk in proliferating cultures of epithelial cells. J Biol Chem 270: 7117-7124, 1995.
18. Herschman HR. Prostaglandin synthase 2. Biochim Biophys Acta 1299: 125-140, 1996.
19. Hislop A and Reid L. New findings in pulmonary arteries of rats with hypoxia-induced pulmonary hypertension. Br J Exp Pathol 57: 542-554, 1976.
20. Hogg N, Browning J, Howard T, Winterford C, Fitzpatrick D, and Gobe G. Apoptosis in vascular endothelial cells caused by serum deprivation, oxidative stress and transforming growth factor-β. Endothelium 7: 35-49, 1999.
21. Hoshikawa Y, Voelkel NF, Gesell TL, Moore MD, Morris KG, Alger LA, Narumiya S, and Geraci MW. Prostacyclin receptor-dependent modulation of pulmonary vascular remodeling. Am J Respir Crit Care Med 164: 314-318, 2001.
22. Jeffery TK and Morrell NW. Molecular and cellular basis of pulmonary vascular remodeling in pulmonary hypertension. Prog Cardiovasc Dis 45: 173-202, 2002.
23. Jin N, Hatton N, Swartz DR, Xia X, Harrington MA, Larsen SH, and Rhoades RA. Hypoxia activates jun-N-terminal kinase, extracellular signal-regulated protein kinase, and p38 kinase in pulmonary arteries. Am J Respir Cell Mol Biol 23: 593-601, 2000.
24. Lane KB, Machado RD, Pauciulo MW, Thomson JR, Phillips JA III, Loyd JE, Nichols WC, and Trembath RC. Heterozygous germline mutations in BMPR2, encoding a TGF-β receptor, cause familial primary pulmonary hypertension. The International PPH Consortium. Nat Genet 26: 81-84, 2000.
25. Machado RD, Pauciulo MW, Thomson JR, Lane KB, Morgan NV, Wheeler L, Phillips JA III, Newman J, Williams D, Galie N, Manes A, McNeil K, Yacoub M, Mikhail G, Rogers P, Corris P, Humbert M, Donnai D, Martensson G, Tranebjaerg L, Loyd JE, Trembath RC, and Nichols WC. BMPR2 haploinsufficiency as the inherited molecular mechanism for primary pulmonary hypertension. Am J Hum Genet 68: 92-102, 2001.
26. Massague J and Chen YG. Controlling TGF-β signaling. Genes Dev 14: 627-644, 2000.
27. Meyrick B and Reid L. The effect of continued hypoxia on rat pulmonary arterial circulation. An ultrastructural study. Lab Invest 38: 188-200, 1978.
28. Monick MM, Robeff PK, Butler NS, Flaherty DM, Carter AB, Peterson MW, and Hunninghake GW. Phosphatidylinositol 3-kinase activity negatively regulates stability of cyclooxygenase 2 mRNA. J Biol Chem 277: 32992-33000, 2002.
29. Morrell NW, Yang X, Upton PD, Jourdan KB, Morgan N, Sheares KK, and Trembath RC. Altered growth responses of pulmonary artery smooth muscle cells from patients with primary pulmonary hypertension to transforming growth factor-β1 and bone morphogenetic proteins. Circulation 104: 790-795, 2001.
30. Mottet D, Dumont V, Deccache Y, Demazy C, Ninane N, Raes M, and Michiels C. Regulation of hypoxia-inducible factor-1α protein level during hypoxic conditions by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3β pathway in HepG2 cells. J Biol Chem 278: 31277-31285, 2003.
31. Moustakas A, Souchelnytskyi S, and Heldin CH. Smad regulation in TGF-β signal transduction. J Cell Sci 114: 4359-4369, 2001.
32. Nohe A, Hassel S, Ehrlich M, Neubauer F, Sebald W, Henis YI, and Knaus P. The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J Biol Chem 277: 5330-5338, 2002.
33. Ohnaka K, Numaguchi K, Yamakawa T, and Inagami T. Induction of cyclooxygenase-2 by angiotensin II in cultured rat vascular smooth muscle cells. Hypertension 35: 68-75, 2000.
34. Ohno R, Yoshinaga K, Fujita T, Hasegawa K, Iseki H, Tsunozaki H, Ichikawa W, Nihei Z, and Sugihara K. Depth of invasion parallels increased cyclooxygenase-2 levels in patients with gastric carcinoma. Cancer 91: 1876-1881, 2001.
35. Orton EC, LaRue SM, Ensley B, and Stenmark K. Bromodeoxyuridine labeling and DNA content of pulmonary arterial medial cells from hypoxia-exposed and nonexposed healthy calves. Am J Vet Res 53: 1925-1930, 1992.
36. Rabinovitch M, Gamble W, Nadas AS, Miettinen OS, and Reid L. Rat pulmonary circulation after chronic hypoxia: hemodynamic and structural features. Am J Physiol Heart Circ Physiol 236: H818-H827, 1979.
37. Reddy ST, Wadleigh DJ, and Herschman HR. Transcriptional regulation of the cyclooxygenase-2 gene in activated mast cells. J Biol Chem 275: 3107-3113, 2000.
38. Sanchez-Elsner T, Botella LM, Velasco B, Langa C, and Bernabeu C. Endoglin expression is regulated by transcriptional cooperation between the hypoxia and transforming growth factor-β pathways. J Biol Chem 277: 43799-43808, 2002.
39. Scott PH, Paul A, Belham CM, Peacock AJ, Wadsworth RM, Gould GW, Welsh D, and Plevin R. Hypoxic stimulation of the stress-activated protein kinases in pulmonary artery fibroblasts. Am J Respir Crit Care Med 158: 958-962, 1998.
40. Seko Y, Takahashi N, Tobe K, Kadowaki T, and Yazaki Y. Hypoxia and hypoxia/reoxygenation activate p65PAK, p38 mitogen-activated protein kinase (MAPK), and stress-activated protein kinase (SAPK) in cultured rat cardiac myocytes. Biochem Biophys Res Commun 239: 840-844, 1997.
41. Semenza GL. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 88: 1474-1480, 2000.
42. Toker A and Cantley LC. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 387: 673-676, 1997.
43. Welsh DJ, Peacock AJ, MacLean M, and Harnett M. Chronic hypoxia induces constitutive p38 mitogen-activated protein kinase activity that correlates with enhanced cellular proliferation in fibroblasts from rat pulmonary but not systemic arteries. Am J Respir Crit Care Med 164: 282-289, 2001.
44. Wharton J, Davie N, Upton PD, Yacoub MH, Polak JM, and Morrell NW. Prostacyclin analogues differentially inhibit growth of distal and proximal human pulmonary artery smooth muscle cells. Circulation 102: 3130-3136, 2000.
45. Wilkinson M, Langhorne CA, Heath D, Barer GR, and Howard P. A pathophysiological study of 10 cases of hypoxic cor pulmonale. QJM 66: 65-85, 1988.
46. Yang X, Hou F, Taylor L, and Polgar P. Characterization of human cyclooxygenase 2 gene promoter localization of a TGF-β response element. Biochim Biophys Acta 1350: 287-292, 1997.
47. Yang X, Sheares KK, Davie N, Upton PD, Taylor GW, Horsley J, Wharton J, and Morrell NW. Hypoxic induction of cox-2 regulates proliferation of human pulmonary artery smooth muscle cells. Am J Respir Cell Mol Biol 27: 688-696, 2002.
48. Yu L, Hebert MC, and Zhang YE. TGF-β receptor-activated p38 MAP kinase mediates Smad-independent TGF-β responses. EMBO J 21: 3749-3759, 2002.
49. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F, and Kalluri R. BMP-7 counteracts TGF-β1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 9: 964-968, 2003.