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Cited by 40Metabolism, Diabetes, and CancerCaveolin-1 and cellular processesGenomics and Chromatin Dynamics

Emerging roles of the myocardin family of proteins in lipid and glucose metabolism

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Swärd, Karl, Stenkula, Karin G, Rippe, Catarina, Alajbegovic, Azra, Gomez, Maria F., Albinsson, Sebastian·2016·The Journal of Physiology
DOI 10.1113/jp271913PMC PMC5009794
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Abstract

Members of the myocardin family bind to the transcription factor serum response factor (SRF) and act as coactivators controlling genes of relevance for myogenic differentiation and motile function. Binding of SRF to DNA is mediated by genetic elements called CArG boxes, found often but not exclusively in muscle and growth controlling genes. Studies aimed at defining the full spectrum of these CArG elements in the genome (i.e. the CArGome) have in recent years, unveiled unexpected roles of the myocardin family proteins in lipid and glucose homeostasis. This coactivator family includes the protein myocardin (MYOCD), the myocardin‐related transcription factors A and B (MRTF‐A/MKL1 and MRTF‐B/MKL2) and MASTR (MAMSTR). Here we discuss growing evidence that SRF‐driven transcription is controlled by extracellular glucose through activation of the Rho‐kinase pathway and actin polymerization. We also describe data showing that adipogenesis is influenced by MLK activity through actions upstream of peroxisome proliferator‐activated receptor γ with consequences for whole body fat mass and insulin sensitivity. The recently demonstrated involvement of myocardin coactivators in the biogenesis of caveolae, Ω‐shaped membrane invaginations of importance for lipid and glucose metabolism, is finally discussed. These novel roles of myocardin proteins may open the way for new unexplored strategies to combat metabolic diseases such as diabetes, which, at the current incidence, is expected to reach 333 million people worldwide by 2025. This review highlights newly discovered roles of myocardin‐related transcription factors in lipid and glucose metabolism as well as novel insights into their well‐established role as mediators of stretch‐dependent effects in smooth muscle. As co‐factors for serum response factor (SRF), MKLs regulates transcription of genes involved in the contractile function of smooth muscle cells. In addition to mechanical stimuli, this regulation has now been found to be promoted by extracellular glucose levels in smooth muscle. Recent reports also suggest that MKLs can regulate a subset of genes involved in the formation of lipid‐rich invaginations in the cell membrane called caveolae. Finally, a potential role of MKLs in non‐muscle cells has been discovered as they negatively influence adipocyte differentiation. image

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  1. Abebe W, Harris KH & MacLeod KM (1990). Enhanced contractile responses of arteries from diabetic rats to α1‐adrenoceptor stimulation in the absence and presence of extracellular calcium. J Cardiovasc Pharmacol 16, 239–248. [DOI] [PubMed] [Google Scholar]
  2. Albinsson S & Hellstrand P (2007). Integration of signal pathways for stretch‐dependent growth and differentiation in vascular smooth muscle. Am J Physiol Cell Physiol 293, C772–C782. [DOI] [PubMed] [Google Scholar]
  3. Albinsson S, Nordstrom I & Hellstrand P (2004). Stretch of the vascular wall induces smooth muscle differentiation by promoting actin polymerization. J Biol Chem 279, 34849–34855. [DOI] [PubMed] [Google Scholar]
  4. Aravind L & Koonin EV (2000). SAP – a putative DNA‐binding motif involved in chromosomal organization. Trends Biochem Sci 25, 112–114. [DOI] [PubMed] [Google Scholar]
  5. Asparuhova MB, Ferralli J, Chiquet M & Chiquet‐Ehrismann R (2011). The transcriptional regulator megakaryoblastic leukemia‐1 mediates serum response factor‐independent activation of tenascin‐C transcription by mechanical stress. FASEB J 25, 3477–3488. [DOI] [PubMed] [Google Scholar]
  6. Bastiani M, Liu L, Hill MM, Jedrychowski MP, Nixon SJ, Lo HP, Abankwa D, Luetterforst R, Fernandez‐Rojo M, Breen MR, Gygi SP, Vinten J, Walser PJ, North KN, Hancock JF, Pilch PF & Parton RG (2009). MURC/Cavin‐4 and cavin family members form tissue‐specific caveolar complexes. J Cell Biol 185, 1259–1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ben‐Zvi A, Lacoste B, Kur E, Andreone BJ, Mayshar Y, Yan H & Gu C (2014). Mfsd2a is critical for the formation and function of the blood‐brain barrier. Nature 509, 507–511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Black BL & Olson EN (1998). Transcriptional control of muscle development by myocyte enhancer factor‐2 (MEF2) proteins. Annu Rev Cell Dev Biol 14, 167–196. [DOI] [PubMed] [Google Scholar]
  9. Blank RS, McQuinn TC, Yin KC, Thompson MM, Takeyasu K, Schwartz RJ & Owens GK (1992). Elements of the smooth muscle α‐actin promoter required in cis for transcriptional activation in smooth muscle. Evidence for cell type‐specific regulation. J Biol Chem 267, 984–989. [PubMed] [Google Scholar]
  10. Brandt DT, Baarlink C, Kitzing TM, Kremmer E, Ivaska J, Nollau P & Grosse R (2009). SCAI acts as a suppressor of cancer cell invasion through the transcriptional control of β1‐integrin. Nat Cell Biol 11, 557–568. [DOI] [PubMed] [Google Scholar]
  11. Brasacchio D, Okabe J, Tikellis C, Balcerczyk A, George P, Baker EK, Calkin AC, Brownlee M, Cooper ME & El‐Osta A (2009). Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene‐activating epigenetic marks that coexist on the lysine tail. Diabetes 58, 1229–1236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cheng JP, Mendoza‐Topaz C, Howard G, Chadwick J, Shvets E, Cowburn AS, Dunmore BJ, Crosby A, Morrell NW & Nichols BJ (2015). Caveolae protect endothelial cells from membrane rupture during increased cardiac output. J Cell Biol 211, 53–61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL Jr, Jones DW, Materson BJ, Oparil S, Wright JT Jr & Roccella EJ (2003). The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA 289, 2560–2572. [DOI] [PubMed] [Google Scholar]
  14. Cohen AW, Razani B, Wang XB, Combs TP, Williams TM, Scherer PE & Lisanti MP (2003). Caveolin‐1‐deficient mice show insulin resistance and defective insulin receptor protein expression in adipose tissue. Am J Physiol Cell Physiol 285, C222–C235. [DOI] [PubMed] [Google Scholar]
  15. Collard L, Herledan G, Pincini A, Guerci A, Randrianarison‐Huetz V & Sotiropoulos A (2014). Nuclear actin and myocardin‐related transcription factors control disuse muscle atrophy through regulation of Srf activity. J Cell Sci 127, 5157–5163. [DOI] [PubMed] [Google Scholar]
  16. Creemers EE, Sutherland LB, Oh J, Barbosa AC & Olson EN (2006). Coactivation of MEF2 by the SAP domain proteins myocardin and MASTR. Mol Cell 23, 83–96. [DOI] [PubMed] [Google Scholar]
  17. De Marinis Y, Cai M, Bompada P, Atac D, Kotova O, Johansson ME, Garcia‐Vaz E, Gomez MF, Laakso M & Groop L (2016). Epigenetic regulation of the thioredoxin‐interacting protein (TXNIP) gene by hyperglycemia in kidney. Kidney Int 89, 342–353. [DOI] [PubMed] [Google Scholar]
  18. Echarri A & Del Pozo MA (2015). Caveolae – mechanosensitive membrane invaginations linked to actin filaments. J Cell Sci 128, 2747–2758. [DOI] [PubMed] [Google Scholar]
  19. Esnault C, Stewart A, Gualdrini F, East P, Horswell S, Matthews N & Treisman R (2014). Rho‐actin signaling to the MRTF coactivators dominates the immediate transcriptional response to serum in fibroblasts. Genes Dev 28, 943–958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fintha A, Gasparics A, Fang L, Erdei Z, Hamar P, Mozes MM, Kokeny G, Rosivall L & Sebe A (2013). Characterization and role of SCAI during renal fibrosis and epithelial‐to‐mesenchymal transition. Am J Pathol 182, 388–400. [DOI] [PubMed] [Google Scholar]
  21. Fleischhacker E, Esenabhalu VE, Spitaler M, Holzmann S, Skrabal F, Koidl B, Kostner GM & Graier WF (1999). Human diabetes is associated with hyperreactivity of vascular smooth muscle cells due to altered subcellular Ca2+ distribution. Diabetes 48, 1323–1330. [DOI] [PubMed] [Google Scholar]
  22. Gomez‐Ruiz A, Milagro FI, Campion J, Martinez JA & de Miguel C (2010). Caveolin expression and activation in retroperitoneal and subcutaneous adipocytes: influence of a high‐fat diet. J Cell Physiol 225, 206–213. [DOI] [PubMed] [Google Scholar]
  23. Grunstein M (1997). Histone acetylation in chromatin structure and transcription. Nature 389, 349–352. [DOI] [PubMed] [Google Scholar]
  24. Guo Z, Su W, Allen S, Pang H, Daugherty A, Smart E & Gong MC (2005). COX‐2 up‐regulation and vascular smooth muscle contractile hyperreactivity in spontaneous diabetic db/db mice. Cardiovasc Res 67, 723–735. [DOI] [PubMed] [Google Scholar]
  25. Gurbuz I, Ferralli J, Roloff T, Chiquet‐Ehrismann R & Asparuhova MB (2014). SAP domain‐dependent Mkl1 signaling stimulates proliferation and cell migration by induction of a distinct gene set indicative of poor prognosis in breast cancer patients. Mol Cancer 13, 22. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gustavsson J, Parpal S, Karlsson M, Ramsing C, Thorn H, Borg M, Lindroth M, Peterson KH, Magnusson KE & Stralfors P (1999). Localization of the insulin receptor in caveolae of adipocyte plasma membrane. FASEB J 13, 1961–1971. [PubMed] [Google Scholar]
  27. Hayashi K, Watanabe B, Nakagawa Y, Minami S & Morita T (2014). RPEL proteins are the molecular targets for CCG‐1423, an inhibitor of Rho signaling. PLoS One 9, e89016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hayashi YK, Matsuda C, Ogawa M, Goto K, Tominaga K, Mitsuhashi S, Park YE, Nonaka I, Hino‐Fukuyo N, Haginoya K, Sugano H & Nishino I (2009). Human PTRF mutations cause secondary deficiency of caveolins resulting in muscular dystrophy with generalized lipodystrophy. J Clin Invest 119, 2623–2633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Jin W, Goldfine AB, Boes T, Henry RR, Ciaraldi TP, Kim EY, Emecan M, Fitzpatrick C, Sen A, Shah A, Mun E, Vokes V, Schroeder J, Tatro E, Jimenez‐Chillaron J & Patti ME (2011). Increased SRF transcriptional activity in human and mouse skeletal muscle is a signature of insulin resistance. J Clin Invest 121, 918–929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kawamura H, Yokote K, Asaumi S, Kobayashi K, Fujimoto M, Maezawa Y, Saito Y & Mori S (2004). High glucose‐induced upregulation of osteopontin is mediated via Rho/Rho kinase pathway in cultured rat aortic smooth muscle cells. Arterioscler Thromb Vasc Biol 24, 276–281. [DOI] [PubMed] [Google Scholar]
  31. Kim CA, Delepine M, Boutet E, El Mourabit H, Le Lay S, Meier M, Nemani M, Bridel E, Leite CC, Bertola DR, Semple RK, O'Rahilly S, Dugail I, Capeau J, Lathrop M & Magre J (2008). Association of a homozygous nonsense caveolin‐1 mutation with Berardinelli‐Seip congenital lipodystrophy. J Clin Endocrinol Metab 93, 1129–1134. [DOI] [PubMed] [Google Scholar]
  32. Kovtun O, Tillu VA, Ariotti N, Parton RG & Collins BM (2015). Cavin family proteins and the assembly of caveolae. J Cell Sci 128, 1269–1278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Krawczyk KK, Yao Mattisson I, Ekman M, Oskolkov N, Grantinge R, Kotowska D, Olde B, Hansson O, Albinsson S, Miano JM, Rippe C & Sward K (2015). Myocardin family members drive formation of caveolae. PLoS One 10, e0133931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Li L, Liu Z, Mercer B, Overbeek P & Olson EN (1997). Evidence for serum response factor‐mediated regulatory networks governing SM22α transcription in smooth, skeletal, and cardiac muscle cells. Dev Biol 187, 311–321. [DOI] [PubMed] [Google Scholar]
  35. Liu Y, Sinha S, McDonald OG, Shang Y, Hoofnagle MH & Owens GK (2005). Kruppel‐like factor 4 abrogates myocardin‐induced activation of smooth muscle gene expression. J Biol Chem 280, 9719–9727. [DOI] [PubMed] [Google Scholar]
  36. Lo HP, Nixon SJ, Hall TE, Cowling BS, Ferguson C, Morgan GP, Schieber NL, Fernandez‐Rojo MA, Bastiani M, Floetenmeyer M, Martel N, Laporte J, Pilch PF & Parton RG (2015). The caveolin‐cavin system plays a conserved and critical role in mechanoprotection of skeletal muscle. J Cell Biol 210, 833–849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Masson O, Chavey C, Dray C, Meulle A, Daviaud D, Quilliot D, Muller C, Valet P & Liaudet‐Coopman E (2009). LRP1 receptor controls adipogenesis and is up‐regulated in human and mouse obese adipose tissue. PLoS One 4, e7422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Matsusue K, Haluzik M, Lambert G, Yim SH, Gavrilova O, Ward JM, Brewer B Jr, Reitman ML & Gonzalez FJ (2003). Liver‐specific disruption of PPARγ in leptin‐deficient mice improves fatty liver but aggravates diabetic phenotypes. J Clin Invest 111, 737–747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. McDonald ME, Li C, Bian H, Smith BD, Layne MD & Farmer SR (2015). Myocardin‐related transcription factor A regulates conversion of progenitors to beige adipocytes. Cell 160, 105–118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Mendez MG & Janmey PA (2012). Transcription factor regulation by mechanical stress. Int J Biochem Cell Biol 44, 728–732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Miano JM (2003). Serum response factor: toggling between disparate programs of gene expression. J Mol Cell Cardiol 35, 577–593. [DOI] [PubMed] [Google Scholar]
  42. Mikkelsen TS, Xu Z, Zhang X, Wang L, Gimble JM, Lander ES & Rosen ED (2010). Comparative epigenomic analysis of murine and human adipogenesis. Cell 143, 156–169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Miralles F, Posern G, Zaromytidou AI & Treisman R (2003). Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113, 329–342. [DOI] [PubMed] [Google Scholar]
  44. Nguyen LN, Ma D, Shui G, Wong P, Cazenave‐Gassiot A, Zhang X, Wenk MR, Goh EL & Silver DL (2014). Mfsd2a is a transporter for the essential omega‐3 fatty acid docosahexaenoic acid. Nature 509, 503–506. [DOI] [PubMed] [Google Scholar]
  45. Nilsson‐Berglund LM, Zetterqvist AV, Nilsson‐Ohman J, Sigvardsson M, Gonzalez Bosc LV, Smith ML, Salehi A, Agardh E, Fredrikson GN, Agardh CD, Nilsson J, Wamhoff BR, Hultgardh‐Nilsson A & Gomez MF (2010). Nuclear factor of activated T cells regulates osteopontin expression in arterial smooth muscle in response to diabetes‐induced hyperglycemia. Arterioscler Thromb Vasc Biol 30, 218–224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Nobusue H, Onishi N, Shimizu T, Sugihara E, Oki Y, Sumikawa Y, Chiyoda T, Akashi K, Saya H & Kano K (2014). Regulation of MKL1 via actin cytoskeleton dynamics drives adipocyte differentiation. Nat Commun 5, 3368. [DOI] [PubMed] [Google Scholar]
  47. Olson EN & Nordheim A (2010). Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol 11, 353–365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Oshikawa J, Otsu K, Toya Y, Tsunematsu T, Hankins R, Kawabe J, Minamisawa S, Umemura S, Hagiwara Y & Ishikawa Y (2004). Insulin resistance in skeletal muscles of caveolin‐3‐null mice. Proc Natl Acad Sci USA 101, 12670–12675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Posern G & Treisman R (2006). Actin’ together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol 16, 588–596. [DOI] [PubMed] [Google Scholar]
  50. Qiu P, Ritchie RP, Fu Z, Cao D, Cumming J, Miano JM, Wang DZ, Li HJ & Li L (2005). Myocardin enhances Smad3‐mediated transforming growth factor‐β1 signaling in a CArG box‐independent manner: Smad‐binding element is an important cis element for SM22α transcription in vivo. Circ Res 97, 983–991. [DOI] [PubMed] [Google Scholar]
  51. Rajab A, Straub V, McCann LJ, Seelow D, Varon R, Barresi R, Schulze A, Lucke B, Lutzkendorf S, Karbasiyan M, Bachmann S, Spuler S & Schuelke M (2010). Fatal cardiac arrhythmia and long‐QT syndrome in a new form of congenital generalized lipodystrophy with muscle rippling (CGL4) due to PTRF‐CAVIN mutations. PLoS Genet 6, e1000874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Riches K, Alshanwani AR, Warburton P, O'Regan DJ, Ball SG, Wood IC, Turner NA & Porter KE (2014). Elevated expression levels of miR‐143/5 in saphenous vein smooth muscle cells from patients with Type 2 diabetes drive persistent changes in phenotype and function. J Mol Cell Cardiol 74, 240–250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Rikitake Y & Liao JK (2005). Rho‐kinase mediates hyperglycemia‐induced plasminogen activator inhibitor‐1 expression in vascular endothelial cells. Circulation 111, 3261–3268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Rosen ED, Walkey CJ, Puigserver P & Spiegelman BM (2000). Transcriptional regulation of adipogenesis. Genes Dev 14, 1293–1307. [PubMed] [Google Scholar]
  55. Sawant A, Chanda D, Isayeva T, Tsuladze G, Garvey WT & Ponnazhagan S (2012). Noggin is novel inducer of mesenchymal stem cell adipogenesis: implications for bone health and obesity. J Biol Chem 287, 12241–12249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Schleicher ED & Weigert C (2000). Role of the hexosamine biosynthetic pathway in diabetic nephropathy. Kidney Int Suppl 77, S13–18. [DOI] [PubMed] [Google Scholar]
  57. Solway J, Seltzer J, Samaha FF, Kim S, Alger LE, Niu Q, Morrisey EE, Ip HS & Parmacek MS (1995). Structure and expression of a smooth muscle cell‐specific gene, SM22 alpha. J Biol Chem 270, 13460–13469. [DOI] [PubMed] [Google Scholar]
  58. Somogyi K & Rorth P (2004). Cortactin modulates cell migration and ring canal morphogenesis during Drosophila oogenesis. Mech Dev 121, 57–64. [DOI] [PubMed] [Google Scholar]
  59. Sotiropoulos A, Gineitis D, Copeland J & Treisman R (1999). Signal‐regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98, 159–169. [DOI] [PubMed] [Google Scholar]
  60. Spiegelman BM & Heinrich R (2004). Biological control through regulated transcriptional coactivators. Cell 119, 157–167. [DOI] [PubMed] [Google Scholar]
  61. Stone SJ, Myers HM, Watkins SM, Brown BE, Feingold KR, Elias PM & Farese RV Jr (2004). Lipopenia and skin barrier abnormalities in DGAT2‐deficient mice. J Biol Chem 279, 11767–11776. [DOI] [PubMed] [Google Scholar]
  62. Stralfors P (2012). Caveolins and caveolae, roles in insulin signalling and diabetes. Adv Exp Med Biol 729, 111–126. [DOI] [PubMed] [Google Scholar]
  63. Sun Q, Chen G, Streb JW, Long X, Yang Y, Stoeckert CJ Jr & Miano JM (2006). Defining the mammalian CArGome. Genome Res 16, 197–207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Thi Hien T, Turczynska KM, Dahan D, Ekman M, Grossi M, Sjogren J, Nilsson J, Braun T, Boettger T, Garcia Vaz E, Stenkula K, Sward K, Gomez MF & Albinsson S (2016). Elevated glucose levels promote contractile and cytoskeletal gene expression in vascular smooth muscle via Rho/protein kinase C and actin polymerization. J Biol Chem 291, 3552–3568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Towler DA, Bidder M, Latifi T, Coleman T & Semenkovich CF (1998). Diet‐induced diabetes activates an osteogenic gene regulatory program in the aortas of low density lipoprotein receptor‐deficient mice. J Biol Chem 273, 30427–30434. [DOI] [PubMed] [Google Scholar]
  66. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M & Narumiya S (1997). Calcium sensitization of smooth muscle mediated by a Rho‐associated protein kinase in hypertension. Nature 389, 990–994. [DOI] [PubMed] [Google Scholar]
  67. Ungvari Z, Pacher P, Kecskemeti V, Papp G, Szollar L & Koller A (1999). Increased myogenic tone in skeletal muscle arterioles of diabetic rats. Possible role of increased activity of smooth muscle Ca2+ channels and protein kinase C. Cardiovasc Res 43, 1018–1028. [DOI] [PubMed] [Google Scholar]
  68. Wang D, Chang PS, Wang Z, Sutherland L, Richardson JA, Small E, Krieg PA & Olson EN (2001). Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 105, 851–862. [DOI] [PubMed] [Google Scholar]
  69. Wang DZ, Li S, Hockemeyer D, Sutherland L, Wang Z, Schratt G, Richardson JA, Nordheim A & Olson EN (2002). Potentiation of serum response factor activity by a family of myocardin‐related transcription factors. Proc Natl Acad Sci USA 99, 14855–14860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Vartiainen MK, Guettler S, Larijani B & Treisman R (2007). Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316, 1749–1752. [DOI] [PubMed] [Google Scholar]
  71. Weinl C, Castaneda Vega S, Riehle H, Stritt C, Calaminus C, Wolburg H, Mauel S, Breithaupt A, Gruber AD, Wasylyk B, Olson EN, Adams RH, Pichler BJ & Nordheim A (2015). Endothelial depletion of murine SRF/MRTF provokes intracerebral hemorrhagic stroke. Proc Natl Acad Sci USA 112, 9914–9919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. White RE & Carrier GO (1988). Enhanced vascular alpha‐adrenergic neuroeffector system in diabetes: importance of calcium. Am J Physiol Heart Circ Physiol 255, H1036–H1042. [DOI] [PubMed] [Google Scholar]
  73. Villeneuve LM & Natarajan R (2010). The role of epigenetics in the pathology of diabetic complications. Am J Physiol Renal Physiol 299, F14–F25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Xie Z, Gong MC, Su W, Xie D, Turk J & Guo Z (2010). Role of calcium‐independent phospholipase A2β in high glucose‐induced activation of RhoA, Rho kinase, and CPI‐17 in cultured vascular smooth muscle cells and vascular smooth muscle hypercontractility in diabetic animals. J Biol Chem 285, 8628–8638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Xie Z, Su W, Guo Z, Pang H, Post SR & Gong MC (2006). Up‐regulation of CPI‐17 phosphorylation in diabetic vasculature and high glucose cultured vascular smooth muscle cells. Cardiovasc Res 69, 491–501. [DOI] [PubMed] [Google Scholar]
  76. Xu H, Wu X, Qin H, Tian W, Chen J, Sun L, Fang M & Xu Y (2015). Myocardin‐related transcription factor A epigenetically regulates renal fibrosis in diabetic nephropathy. J Am Soc Nephrol 26, 1648–1660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Yin JW, Liang Y, Park JY, Chen D, Yao X, Xiao Q, Liu Z, Jiang B, Fu Y, Bao M, Huang Y, Liu Y, Yan J, Zhu MS, Yang Z, Gao P, Tian B, Li D & Wang G (2012). Mediator MED23 plays opposing roles in directing smooth muscle cell and adipocyte differentiation. Genes Dev 26, 2192–2205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Yin Y, Yuan H, Wang C, Pattabiraman N, Rao M, Pestell RG & Glazer RI (2006). 3‐Phosphoinositide‐dependent protein kinase‐1 activates the peroxisome proliferator‐activated receptor‐γ and promotes adipocyte differentiation. Mol Endocrinol 20, 268–278. [DOI] [PubMed] [Google Scholar]
  79. Zeidan A, Nordstrom I, Albinsson S, Malmqvist U, Sward K & Hellstrand P (2003). Stretch‐induced contractile differentiation of vascular smooth muscle: sensitivity to actin polymerization inhibitors. Am J Physiol Cell Physiol 284, C1387–C1396. [DOI] [PubMed] [Google Scholar]
  80. Zeidan A, Sward K, Nordstrom I, Ekblad E, Zhang JC, Parmacek MS & Hellstrand P (2004). Ablation of SM22α decreases contractility and actin contents of mouse vascular smooth muscle. FEBS Lett 562, 141–146. [DOI] [PubMed] [Google Scholar]
  81. Zeisberg M & Neilson EG (2010). Mechanisms of tubulointerstitial fibrosis. J Am Soc Nephrol 21, 1819–1834. [DOI] [PubMed] [Google Scholar]
  82. Zhong Q & Kowluru RA (2013). Regulation of matrix metalloproteinase‐9 by epigenetic modifications and the development of diabetic retinopathy. Diabetes 62, 2559–2568. [DOI] [PMC free article] [PubMed] [Google Scholar]

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Authors
Swärd, K., Stenkula, K. G., Rippe, C., Alajbegovic, A., Gomez, M. F., & Albinsson, S.
Affiliations
Lund University (SE)
Corresponding author
Albinsson, Sebastian
ORCID
Venue
The Journal of Physiology
Publisher
Wiley
Published
2016-05-10
Volume
594
Issue
17
Pages
4741-4752
ISSN
  • 0022-3751 (ISSN-L)
  • 1469-7793
DOI
10.1113/jp271913
PMC
PMC5009794
OpenAlex
W2323572690
Cited by
40
References
3
Citations by year
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FWCI
0.39
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • The Journal of Physiology (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Lund University Publications (Lund University) (submittedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords
serum response factor, CArG box, MRTF, MKL1, Rho kinase, actin polymerization, glucose detection, adipogenesis, PPARγ, insulin sensitivity, caveolae, lipid metabolism, glucose metabolism, smooth muscle contractility, diabetes mellitus
MeSH terms
Protein Domains, Myocardin, Animals, Glucose, Humans, Nuclear Proteins, Trans-Activators, Caveolae, Adipogenesis, Lipid Metabolism

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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