Formin mDia1 mediates vascular remodeling via integration of oxidative and signal transduction pathways

Circulation Research

Volumn 110, Issue 10, 2012, Pages 1279-1293

  Touré, Fatouma ^a   Fritz, Günter ^b   Li, Qing ^a   Rai, Vivek ^a   Daffu, Gurdip ^a   Zou, Yu Shan ^a   Rosario, Rosa ^a   Ramasamy, Ravichandran ^a   Alberts, Arthur S ^c   Yan, Shi Fang ^a   Schmidt, Ann Marie ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

^c VAN ANDEL RESEARCH INSTITUTE   (United States)

Author keywords

cellular migration; formin; restenosis; signal transduction; vascular smooth muscle cell

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; MAMMALIAN DIAPHANOUS RELATED FORMIN; METHENAMINE; PROTEIN KINASE B; PROTEIN KINASE P60; RAC1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTERY INJURY; ARTICLE; CELL MIGRATION; FEMORAL ARTERY; GLYCATION; IN VIVO STUDY; MALE; MOUSE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UPREGULATION; VASCULAR SMOOTH MUSCLE;

ACTIN CYTOSKELETON; ANIMALS; CARRIER PROTEINS; CELL MOVEMENT; CELLS, CULTURED; FEMORAL ARTERY; GLYCOGEN SYNTHASE KINASE 3; GLYCOSYLATION END PRODUCTS, ADVANCED; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICROTUBULES; MUSCLE, SMOOTH, VASCULAR; NADH, NADPH OXIDOREDUCTASES; NEOINTIMA; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS PP60(C-SRC); RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION;

EID: 84861098989     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.262519     Document Type: Article

References (51)

1. Baarlink C, Brandt D, Grosse R. SnapShot: Formins. Cell. 2010;142: 172,e171.
2. Bartolini F, Gundersen GG. Formins and microtubules. Biochim Biophys Acta. 2010;1803:164-173.
3. Goode BL, Eck MJ. Mechanism and function of formins in the control of actin assembly. Annu Rev Biochem. 2007;76:593-627.
4. Wallar BJ, and Alberts AS. The formins: Active scaffolds that remodel the cytoskeleton. Trends Cell Biol. 2003;13:435-446. (Pubitemid 36897648)
5. Habas, Kato Y, He X. Wnt/frizzled activation of Rho regulates vertebrate gastrulation and requires a novel formin homology protein Daam1. Cell. 2001;107:843-854. (Pubitemid 34084976)
6. Kitzing TM, Sahadevan AS, Brandt DT, Knieling H, Hannemann S, Fackler OT, Grosshans J, Grosse R. Positive feedback between Dia1, LARG and RhoA regulates cell morphology and invastion. Genes Dev. 2007;21:1478-1483. (Pubitemid 46955720)
7. Lynch ED, Lee MK, Morrow JE, Welcsh PL. Leon PE, King MC. Nonsyndromic deafness DFNA1 associated with mutation of a human homolog of the Drosophila gene diaphanous. Science. 1997;278: 1315-1318. (Pubitemid 27495747)
8. DeWard AD, Eisenmann KM, Matheson SF, Alberts AS. The role of formins in human disease. Biochim Biophys Acta. 2010;1803:226-233.
9. Xu Y, Toure F, Qu W, Lin L, Song F, Shen X, Rosario R, Garcia J, Schmidt AM, Yan SF. Advanced glycation end product (AGE)-receptor for AGE (RAGE) signaling and up-regulation of Egr-1 in hypoxic macrophages. J Biol Chem. 2010;285:23233-23240.
10. Hudson BI, Kalea AZ, Del Mar Arriero M, Harja E, Boulanger E, D'Agati V, Schmidt AM. Interaction of the RAGE cytoplasmic domain with diaphanous-1 is required for ligand-stimulated cellular migration through activation of Rac1 and Cdc42. J Biol Chem. 2008;283: 34457-34468.
11. Neeper M, Schmidt AM, Brett J, Yan SD, Wang F, Pan YC, Elliston K, Stern D, Shaw A. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem. 1992;267: 14998-15004.
12. Taguchi A, Blood DC, del Toro G, et al. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature. 2000;405: 354-360. (Pubitemid 30337069)
13. Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A, Slattery T, Zhao L, Nagashima M, Morser J, Migheli A, Nawroth P, Stern D, Schmidt AM. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature. 1996;382:685-691. (Pubitemid 26282167)
14. Deane R, Du Yan S, Submamaryan RK, et al. RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med. 2003;9:907-913. (Pubitemid 36889934)
15. Liliensiek B, Weigand MA, Bierhaus A, et al. Receptor for advanced glycation end products (RAGE) regulates sepsis but not the adaptive immune response. J Clin Invest. 2004;113:1641-1650. (Pubitemid 39071688)
16. Harja E, Bu DX, Hudson BI, et al. Vascular and inflammatory stresses mediate atherosclerosis via RAGE and its ligands in apoE-/- mice. J Clin Invest. 2008;118:183-194.
17. Sakaguchi T, Yan SF, Yan SD, Belov D, Rong LL, Sousa M, Andrassy M, Marso SP, Duda S, Arnold B, Liliensiek B, Nawroth PP, Stern DM, Schmidt AM, Naka Y. 2003. Central role of RAGE-dependent neointimal expansion in arterial restenosis. J Clin Invest. 2003;111:959-972. (Pubitemid 36397472)
18. Schmidt AM, Yan SD, Yan SF, Stern DM. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest. 2001;108:949-955. (Pubitemid 32946067)
19. Peng J, Kitchen SM. West RA. Sigler R. Eisenmann KM. Alberts A.S. Myeloproliferative defects following targeting of the Drf1 gene encoding the mammalian diaphanous related formin mDia1. Cancer Res. 2007;67: 7565-7571. (Pubitemid 47287487)
20. Peng J, Wallar BJ, Flanders A, Swiatek PJ, Alberts AS. Disruption of the Diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42. Curr Biol. 2003;13:534-545. (Pubitemid 36391930)
21. Roque M, Fallon JT, Badimon JJ, Zhang WX, Taubman MB, Reis ED. Mouse model of femoral artery denudation injury associated with the rapid accumulation of adhesion molecules on the luminal surface and recruitment of neutrophils. Arterioscler Thromb Vasc Biol. 2000;20: 335-342.
22. Tarvo P, Barret G. Differences in proliferation of primary cultures of vascular smooth muscle cells taken from male and female rats. Blood Vessels. 1980;17:110-116.
23. Ostendorp T, Leclerc E, Galichet A, Koch M, Demling N, Weigle B, Heizmann CW, Kroneck PM, Fritz G. Structural and functional insights into RAGE activation by multimeric S100B. EMBO J. 2007;26: 3868-3878. (Pubitemid 47295872)
24. Liu S, Tobias R, McClure S, Styba G, Shi Q, Jackowski G. Removal of endotoxin from recombinant protein preparations. Clin Biochem. 1997; 30:455-463. (Pubitemid 27418541)
25. Abid MR, Spokes KC, Shih SC, Aird WC. NADPH oxidase activity selectively modulates vascular endothelial growth factor signaling pathways. J Biol Chem. 2007;282:35373-35385. (Pubitemid 350232487)
26. Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, Neurath MF, Slattery T, Beach D, McClary J, Nagashima M, Morser J, Stern D, Schmidt AM. RAGE mediates a novel proinflammatory axis: A central cell surface receptor for S100/calgranulin polypeptides. Cell. 1999;97:889-901. (Pubitemid 29375048)
27. Kislinger TK, Fu C, Huber B, Qu W, Taguchi A, Du Yan S, Hofmann M, Yan SF, Pischetsrieder M, Stern D, Schmidt AM. N(epsilon)- (carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation endproducts that activate cell signaling pathways and modulate gene expression. J Biol Chem. 1999;274:31740-31749.
28. Sarmiento C, Wang W, Dovas A, Yamaguchi H, Sidani M, El-Sibai M, Desmarais V, Holman HA, Kitchen S, Backer JM, Alberts A, Condeelis J. WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. J Cell Biol. 2008;180: 1245-1260. (Pubitemid 351468478)
29. Eng CH, Huckaba TM, Gundersen GG. The formin mDia regulates GSK3beta through novel PKCs to promote microtubule stabilization but not MTOC reorientation in migrating fibroblasts. Mol Biol Cell. 2006; 17:5004-5016. (Pubitemid 44907346)
30. Park KW, Yang HM, Youn SW, Yang HJ, Chae IH, Oh BH, Lee MM, Park YB, Choi YS, Kim HS, Walsh K. Constitutively active glycogen synthase kinase-3beta gene transfer sustains apoptosis, inhibits proliferation of vascular smooth muscle cells, and reduces neointima formation after balloon injury in rats. Arterioscler Thromb Vasc Biol. 2003;23: 1364-1369. (Pubitemid 36994523)
31. Griendling KK, Sorescu D, Lassègue B, Ushio-Fukai M. Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler Thromb Vasc Biol. 2000;20:2175-2183.
32. Lassegue B, Clempus RE. Vascular NAD(P)H oxidases: specific features, expression and regulation. Am J Physiol Regul, Integr Comp Physiol. 2003;285:R277-R297. (Pubitemid 36898897)
33. Reddy MA, Li SL, Sahar S, Kim YS, Xu ZG, Lanting L, Natarajan R. Key role of Src kinase in S100B-induced activation of the receptor for advanced glycation end products in vascular smooth muscle cells. J Biol Chem. 2006;281:13685-13693. (Pubitemid 43855284)
34. Tominaga T, Sahai E, Chardin P, McCormick F, Courtneidge SA, Alberts AS. Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol Cell. 2000;5:13-25. (Pubitemid 30105432)
35. Gasman S, Kalaidzidis Y, Zerial M. RhoD regulates endosome dynamics through diaphanous-related formin and Src tyrosine kinase. Nat Cell Biol. 2003;5:195-204. (Pubitemid 36322245)
36. Eisenmann KM, West RA, Hildebrand D, Kitchen SM, Peng J, Sigler R, Zhang J, Siminovitch KA, Alberts AS. T cell responses in mammalian diaphanous-related formin mDia1 knock-out mice. J Biol Chem. 2007; 282:25152-25158. (Pubitemid 47347549)
37. Sakata D, Taniguchi H, Yasuda S, Adachi-Morishima A, Hamazaki Y, Nakayama R, Miki T, Minato N, Narumiya S. Impaired T lymphocyte trafficking in mice deficient in an actin-nucleating protein, mDia1. J Exp Med. 2007;204:2031-2038. (Pubitemid 47360865)
38. Zhou Z, Wang K, Penn MS, Marso SP, Lauer MA, Forudi F, Zhou X, Qu W, Lu Y, Stern DM, Schmidt AM, Lincoff AM, Topol EJ. Receptor for AGE (RAGE) mediates neointimal formation in response to injury. Circ. 2003;107:2238-2243. (Pubitemid 36547219)
39. Chang JS, Wendt T, Qu W, Kong L, Zou YS, Schmidt AM, Yan SF. Oxygen deprivation triggers upregulation of early growth response-1 by the receptor for advanced glycation end products. Circ Res. 2008;102: 905-913. (Pubitemid 351591549)
40. Guo J. Ananthakrishnan R, Qu W, Lu Y, Reiniger N, Zeng S, Ma W, Rosario R, Yan SF, Ramasamy R, D'Agati V, Schmidt AM. RAGE mediates podocyte injury in adriamycin-induced glomerulosclerosis. J Am Soc Nephrol. 2008;19:961-972.
41. Wautier JL, Wautier MP, Schmidt AM, Anderson GM, Hori O, Zoukourian C, Capron L, Chappey O, Yan SD, Brett J, Guillausseau PJ, Stern D. Advanced glycation end products (AGEs) on the surface of diabetic erythrocytes bind to the vessel wall via a specific receptor inducing oxidant stress in the vasculature: A link between surface-associated AGEs and diabetic complications. Proc Natl Acad Sci U S A. 1994;91: 7742-7746.
42. El-Benna J, Dang PM, Gougerot-Pocidalo MA, Marie JC, Braut-Boucher F. p47phox, the phagocyte NADPH oxidase/NOX2 organizer: structure, phosphorylation and implication in diseases. Exp Mol Med. 2009;41: 217-225.
43. Narumiya S, Tanji M, Ishizaki T. Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev. 2009; 28:65-76.
44. Young KG, Copeland JW. Formins in cell signaling. Biochim Biophys Acta. 2010;1803:183-190.
45. Tanji M, Ishizaki T, Ebrahimi S, Tsuboguchi Y, Sukezane T, Akagi T, Frame MC, Hashimoto N, Miyamoto S, Narumiya S. mDia1 targets v-Src to the cell periphery and facilitates cell transformation, tumorigenesis, and invasion. Mol Cell Biol. 2010;30:4604-4615.
46. Meng W, Numazaki M, Takeuchi K, Uchibori Y, Ando-Akatsuka Y, Tominaga M, Tominaga T. DIP (mDia interacting protein) is a key molecule regulating Rho and Rac in a Src-dependent manner. Embo J. 2004;23:760-771. (Pubitemid 38418743)
47. Satoh S, Tominaga T. mDia-interacting protein acts downstream of Rho-mDia and modifies Src activation and stress fiber formation. J Biol Chem. 2001;276:39290-39294.
48. Kim L, Kimmel AR. GSK3, a master switch regulating cell-fate specification and tumorigenesis. Curr Opin Genet Dev. 2000;10:508-14.
49. Pertz O, Hodgson L, Klemke RL, and Hahn KM. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature. 2006;440: 1069-1072.
50. Vouret-Craviari V, Bourcier C, Boulter E, and van Obberghen-Schilling E. Distinct signals via Rho GTPases and Src drive shape changes by thrombin and sphingosine-1-phosphate in endothelial cells. J Cell Sci. 2002;115:2475-2484. (Pubitemid 34778065)
51. Rai V, Maldonado AY, Burz DS, Reverdatto S, Yan SF, Schmidt AM, Shekhtman A. Signal transduction in receptor for advanced glycation endproducts (RAGE): solution structure of C terminal RAGE (ct-RAGE) and its binding to mDia1. J Biol Chem. 2012;287:5133-5144.