Smad-independent pathway involved in transforming growth factor β1-induced Nox4 expression and proliferation of endothelial cells

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 388, Issue 3, 2015, Pages 319-326

  Hakami, Nora Y ^a,b   Wong, Henry ^b   Shah, Manisha H ^c   Dusting, Gregory J ^a,b   Jiang, Fan ^b,d   Peshavariya, Hitesh M ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b O'Brien Institute   (Australia)

^c ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d SHANDONG UNIVERSITY   (China)

Author keywords

Endothelial cells; ERK1 2; Nox4; Proliferation; TGF 1

Indexed keywords

MESSENGER RNA; NOX4 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

CELL CULTURE; CELL PROLIFERATION; DRUG EFFECTS; ENDOTHELIUM CELL; GENETICS; HUMAN; METABOLISM; SIGNAL TRANSDUCTION;

CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; NADPH OXIDASE; RNA, MESSENGER; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84925462840     PISSN: 00281298     EISSN: 14321912     Source Type: Journal    
DOI: 10.1007/s00210-014-1070-5     Document Type: Article

References (40)

1. Bai G, Hock TD, Logsdon N, Zhou Y, Thannickal VJ (2014) A far-upstream AP-1/Smad binding box regulates human NOX4 promoter activation by transforming growth factor-beta. Gene 540:62-67
2. Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245-313
3. Boudreau HE, Casterline BW, Rada B, Korzeniowska A, Leto TL (2012) Nox4 involvement in TGF-beta and SMAD3-driven induction of the epithelial-to-mesenchymal transition and migration of breast epithelial cells. Free Radic Biol Med 53:1489-1499
4. Carnesecchi S, Deffert C, Donati Y, Basset O, Hinz B, Preynat-Seauve O, Guichard C, Arbiser JL, Banfi B, Pache JC, Barazzone-Argiroffo C, Krause KH (2011) A key role for NOX4 in epithelial cell death during development of lung fibrosis. Antioxid Redox Signal 15:607-619
5. Chambard JC, Lefloch R, Pouyssegur J, Lenormand P (2007) ERK implication in cell cycle regulation. Biochim Biophys Acta 1773:1299-1310
6. Chan EC, Jiang F, Peshavariya HM, Dusting GJ (2009) Regulation of cell proliferation by NADPH oxidase-mediated signaling: potential roles in tissue repair, regenerative medicine and tissue engineering. Pharmacol Ther 122:97-108
7. Craige SM, Chen K, Pei Y, Li C, Huang X, Chen C, Shibata R, Sato K, Walsh K, Keaney JF Jr (2011) NADPH oxidase 4 promotes endothelial angiogenesis through endothelial nitric oxide synthase activation. Circulation 124:731-740
8. Datla SR, Peshavariya H, Dusting GJ, Mahadev K, Goldstein BJ, Jiang F (2007) Important role of Nox4 type NADPH oxidase in angiogenic responses in human microvascular endothelial cells in vitro. Arterioscler Thromb Vasc Biol 27:2319-2324
9. Finlay GA, Thannickal VJ, Fanburg BL, Paulson KE (2000) Transforming growth factor-beta 1-induced activation of the ERK pathway/activator protein-1 in human lung fibroblasts requires the autocrine induction of basic fibroblast growth factor. J Biol Chem 275:27650-27656
10. Goumans MJ, Liu Z, ten Dijke P (2009) TGF-beta signaling in vascular biology and dysfunction. Cell Res 19:116-127
11. Hecker L, Vittal R, Jones T, Jagirdar R, Luckhardt TR, Horowitz JC, Pennathur S, Martinez FJ, Thannickal VJ (2009) NADPH oxidase-4 mediates myofibroblast activation and fibrogenic responses to lung injury. Nat Med 15:1077-1081
12. Heldin CH, Moustakas A (2012) Role of Smads in TGFbeta signaling. Cell Tissue Res 347:21-36
13. Hu T, Ramachandrarao SP, Siva S, Valancius C, Zhu Y, Mahadev K, Toh I, Goldstein BJ, Woolkalis M, Sharma K (2005) Reactive oxygen species production via NADPH oxidase mediates TGF-beta-induced cytoskeletal alterations in endothelial cells. Am J Physiol Ren Physiol 289:F816-F825
14. Jakobsson L, van Meeteren LA (2013) Transforming growth factor beta family members in regulation of vascular function: in the light of vascular conditional knockouts. Exp Cell Res 319:1264-1270
15. Joko T, Shiraishi A, Akune Y, Tokumaru S, Kobayashi T, Miyata K, Ohashi Y (2013) Involvement of P38MAPK in human corneal endothelial cell migration induced by TGF-beta(2). Exp Eye Res 108:23-32
16. Kamato D, Burch ML, Piva TJ, Rezaei HB, Rostam MA, Xu S, Zheng W, Little PJ, Osman N (2013) Transforming growth factor-beta signalling: role and consequences of Smad linker region phosphorylation. Cell Signal 25:2017-2024
17. Laping NJ, Grygielko E, Mathur A, Butter S, Bomberger J, Tweed C, Martin W, Fornwald J, Lehr R, Harling J, Gaster L, Callahan JF, Olson BA (2002) Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542. Mol Pharmacol 62:58-64
18. Lee NY, Blobe GC (2007) The interaction of endoglin with beta-arrestin2 regulates transforming growth factor-beta-mediated ERK activation and migration in endothelial cells. J Biol Chem 282:21507-21517
19. Lee YH, Kayyali US, Sousa AM, Rajan T, Lechleider RJ, Day RM (2007) Transforming growth factor-beta1 effects on endothelial monolayer permeability involve focal adhesion kinase/Src. Am J Respir Cell Mol Biol 37:485-493
20. Lee CF, Qiao M, Schroder K, Zhao Q, Asmis R (2010) Nox4 is a novel inducible source of reactive oxygen species in monocytes and macrophages and mediates oxidized low density lipoprotein-induced macrophage death. Circ Res 106:1489-1497
21. Lu Q, Patel B, Harrington EO, Rounds S (2009) Transforming growth factor-beta1 causes pulmonary microvascular endothelial cell apoptosis via ALK5. Am J Physiol Lung Cell Mol Physiol 296:L825-L838
22. Martin-Garrido A, Brown DI, Lyle AN, Dikalova A, Seidel-Rogol B, Lassegue B, San Martin A, Griendling KK (2011) NADPH oxidase 4 mediates TGF-beta-induced smooth muscle alpha-actin via p38MAPK and serum response factor. Free Radic Biol Med 50:354-362
23. Mebratu Y, Tesfaigzi Y (2009) How ERK1/2 activation controls cell proliferation and cell death: is subcellular localization the answer? Cell Cycle 8:1168-1175
24. Myoken Y, Kan M, Sato GH, McKeehan WL, Sato JD (1990) Bifunctional effects of transforming growth factor-beta (TGF-beta) on endothelial cell growth correlate with phenotypes of TGF-beta binding sites. Exp Cell Res 191:299-304
25. Pardali E, Goumans MJ, ten Dijke P (2010) Signaling by members of the TGF-beta family in vascular morphogenesis and disease. Trends Cell Biol 20:556-567
26. Peshavariya H, Dusting GJ, Jiang F, Halmos LR, Sobey CG, Drummond GR, Selemidis S (2009) NADPH oxidase isoform selective regulation of endothelial cell proliferation and survival. Naunyn Schmiedeberg's Arch Pharmacol 380:193-204
27. Peshavariya HM, Chan EC, Liu GS, Jiang F, Dusting GJ (2014) Transforming growth factor-beta1 requires NADPH oxidase 4 for angiogenesis in vitro and in vivo. J Cell Mol Med 18(6):1172-1183
28. Pfeiffer A, Middelberg-Bisping K, Drewes C, Schatz H (1996) Elevated plasma levels of transforming growth factor-beta 1 in NIDDM. Diabetes Care 19:1113-1117
29. Roberts AB, Sporn MB (1989) Regulation of endothelial cell growth, architecture, and matrix synthesis by TGF-beta. Am Rev Respir Dis 140:1126-1128
30. Sampson N, Koziel R, Zenzmaier C, Bubendorf L, Plas E, Jansen-Durr P, Berger P (2011) ROS signaling by NOX4 drives fibroblast-to-myofibroblast differentiation in the diseased prostatic stroma. Mol Endocrinol 25:503-515
31. Scaglione R, Argano C, di Chiara T, Colomba D, Parrinello G, Corrao S, Avellone G, Licata G (2003) Central obesity and hypertensive renal disease: association between higher levels of BMI, circulating transforming growth factor beta1 and urinary albumin excretion. Blood Press 12:269-276
32. Schroder K, Zhang M, Benkhoff S, Mieth A, Pliquett R, Kosowski J, Kruse C, Luedike P, Michaelis UR, Weissmann N, Dimmeler S, Shah AM, Brandes RP (2012) Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circ Res 110:1217-1225
33. Segura I, Serrano A, De Buitrago GG, Gonzalez MA, Abad JL, Claveria C, Gomez L, Bernad A, Martinez AC, Riese HH (2002) Inhibition of programmed cell death impairs in vitro vascular-like structure formation and reduces in vivo angiogenesis. FASEB J Off Publ Fed Am Soc Exp Biol 16:833-841
34. Sturrock A, Cahill B, Norman K, Huecksteadt TP, Hill K, Sanders K, Karwande SV, Stringham JC, Bull DA, Gleich M, Kennedy TP, Hoidal JR (2006) Transforming growth factor-beta1 induces Nox4 NAD(P)H oxidase and reactive oxygen species-dependent proliferation in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 290:L661-L673
35. Takac I, Schroder K, Zhang L, Lardy B, Anilkumar N, Lambeth JD, Shah AM, Morel F, Brandes RP (2011) The E-loop is involved in hydrogen peroxide formation by the NADPH oxidase Nox4. J Biol Chem 286:13304-13313
36. ten Dijke P, Arthur HM (2007) Extracellular control of TGFbeta signalling in vascular development and disease. Nat Rev Mol Cell Biol 8:857-869
37. Vinals F, Pouyssegur J (2001) Transforming growth factor beta1 (TGF-beta1) promotes endothelial cell survival during in vitro angiogenesis via an autocrine mechanism implicating TGF-alpha signaling. Mol Cell Biol 21:7218-7230
38. Yan F, Wang Y, Wu X, Peshavariya HM, Dusting GJ, Zhang M, Jiang F (2014) Nox4 and redox signaling mediate TGF-beta-induced endothelial cell apoptosis and phenotypic switch. Cell Death Dis 5:e1010
39. Zhang YE (2009) Non-Smad pathways in TGF-beta signaling. Cell Res 19:128-139
40. Zhang M, Brewer AC, Schroder K, Santos CX, Grieve DJ, Wang M, Anilkumar N, Yu B, Dong X, Walker SJ, Brandes RP, Shah AM (2010) NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc Natl Acad Sci U S A 107:18121-18126