Joseph Miano
| Title | Associate Professor |
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| Institution | School of Medicine and Dentistry |
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| Department | Medicine in the Aab Cardiovascular Research Institute |
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| Address | Aab Cardiovascular Research Institute
211 Bailey Road
West Henrietta NY 14586
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| Title | Associate Director |
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| Institution | University of Rochester Medical Center |
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| Department | Aab Cardiovascular Research Institute |
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| 1992 |
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| Helen S. Page Memorial Ph.D. | | 1993 |
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| Post-Doctoral National Research Service, Smooth Muscle Cell Differentiation | National Institutes of Health | | 1997 |
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| Manitowoc Heart-A-Rama Research for Life | American Heart Association (AHA) | | 2003 |
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| 2007 | Established Investigator Award
American Heart Association | | 2003 |
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| Who's Who in Medicine and Healthcare |
Research in the Miano Lab is focused on the expression regulation and biology of several genes cloned from vascular smooth muscle cells (SMC).
The genes include serum response factor (SRF) and its coactivator, myocardin (MYOCD), which together represent a powerful transcriptional master-switch for the SMC contractile phenotype; a direct target of this transcriptional switch called SMC calponin (CNN1); a tumor suppressor gene, AKAP12, comprising three independent transcription units including one, AKAP12(alpha), that is a direct target of SRF and another, AKAP12(beta), that is massively induced by anti-cancer drugs called retinoids; and a newly defined SMC-restricted gene called leiomodin 1 (LMOD1). The lab is also studying the role of microRNAs in the regulation of SMC differentiation. Our ideas and efforts span the spectrum from computer to DNA to cells to whole animals. We intend to elucidate the transcriptional and post-transcriptional regulation of these genes and/or their functions during normal or pathological processes involving, but not limited to, the cardiovascular system. For example, the transcriptional program of SMC differentiation is under study to gain insight into basic processes underlying vascular development as well as cancer, Alzheimer's disease, and vascular occlusive disease. Tools in genetics, genomics, bioinformatics, and molecular biology are utilized to characterize regulatory elements called CArG boxes that bind the SRF-Myocardin master switch. Recent efforts are underway to fully elucidate the Human CArGome (all functional CArG boxes in the genome) and functionally variants (SNPs) in and around CArG boxes (CArG-SNPs) that may alter programs of gene expression associated with disease.
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Long X, Cowan SL, Miano JM. Mitogen-activated protein kinase 14 is a novel negative regulatory switch for the vascular smooth muscle cell contractile gene program. Arterioscler Thromb Vasc Biol. 2013 Feb; 33(2):378-86.
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Kitchen CM, Cowan SL, Long X, Miano JM. Expression and promoter analysis of a highly restricted integrin alpha gene in vascular smooth muscle. Gene. 2013 Jan 15; 513(1):82-9.
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Nguyen AT, Gomez D, Bell RD, Campbell JH, Clowes AW, Gabbiani G, Giachelli CM, Parmacek MS, Raines EW, Rusch NJ, Speer MY, Sturek M, Thyberg J, Towler DA, Weiser-Evans MC, Yan C, Miano JM, Owens GK. Smooth muscle cell plasticity: fact or fiction? Circ Res. 2013 Jan 4; 112(1):17-22.
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Nicholson TM, Ricke EA, Marker PC, Miano JM, Mayer RD, Timms BG, Vom Saal FS, Wood RW, Ricke WA. Testosterone and 17ß-estradiol induce glandular prostatic growth, bladder outlet obstruction, and voiding dysfunction in male mice. Endocrinology. 2012 Nov; 153(11):5556-65.
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Davis J, Maillet M, Miano JM, Molkentin JD. Lost in Transgenesis: A User's Guide for Genetically Manipulating the Mouse in Cardiac Research. Circ Res. 2012 Aug 31; 111(6):761-77.
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Chen J, Yuan K, Mao X, Miano JM, Wu H, Chen Y. Serum response factor regulates bone formation via IGF-1 and Runx2 signals. J Bone Miner Res. 2012 Aug; 27(8):1659-68.
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Nanda V, Miano JM. Leiomodin 1, a New Serum Response Factor-dependent Target Gene Expressed Preferentially in Differentiated Smooth Muscle Cells. J Biol Chem. 2012 Jan 20; 287(4):2459-67.
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Miano JM, Small EM. MicroRNA133a: a new variable in vascular smooth muscle cell phenotypic switching. Circ Res. 2011 Sep 30; 109(8):825-7.
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Long X, Slivano OJ, Cowan SL, Georger MA, Lee TH, Miano JM. Smooth muscle calponin: an unconventional CArG-dependent gene that antagonizes neointimal formation. Arterioscler Thromb Vasc Biol. 2011 Oct; 31(10):2172-80.
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Benson CC, Zhou Q, Long X, Miano JM. Identifying functional single nucleotide polymorphisms in the human CArGome. Physiol Genomics. 2011 Sep 22; 43(18):1038-48.
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Long X, Miano JM. Transforming growth factor-beta1 (TGF-beta1) utilizes distinct pathways for the transcriptional activation of microRNA 143/145 in human coronary artery smooth muscle cells. J Biol Chem. 2011 Aug 26; 286(34):30119-29.
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Albinsson S, Skoura A, Yu J, DiLorenzo A, Fernández-Hernando C, Offermanns S, Miano JM, Sessa WC. Smooth muscle miRNAs are critical for post-natal regulation of blood pressure and vascular function. PLoS One. 2011; 6(4):e18869.
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Streb JW, Long X, Lee TH, Sun Q, Kitchen CM, Georger MA, Slivano OJ, Blaner WS, Carr DW, Gelman IH, Miano JM. Retinoid-induced expression and activity of an immediate early tumor suppressor gene in vascular smooth muscle cells. PLoS One. 2011; 6(4):e18538.
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Park C, Hennig GW, Sanders KM, Cho JH, Hatton WJ, Redelman D, Park JK, Ward SM, Miano JM, Yan W, Ro S. Serum response factor-dependent MicroRNAs regulate gastrointestinal smooth muscle cell phenotypes. Gastroenterology. 2011 Jul; 141(1):164-75.
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Xie WB, Li Z, Miano JM, Long X, Chen SY. Smad3-mediated myocardin silencing: a novel mechanism governing the initiation of smooth muscle differentiation. J Biol Chem. 2011 Apr 29; 286(17):15050-7.
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Sullivan AL, Benner C, Heinz S, Huang W, Xie L, Miano JM, Glass CK. Serum response factor utilizes distinct promoter- and enhancer-based mechanisms to regulate cytoskeletal gene expression in macrophages. Mol Cell Biol. 2011 Feb; 31(4):861-75.
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Miano JM. Dicing up microRNA gene expression profiles in normal and neoplastic smooth muscle cells. Am J Pathol. 2010 Aug; 177(2):541-3.
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Miano JM. Role of serum response factor in the pathogenesis of disease. Lab Invest. 2010 Sep; 90(9):1274-84.
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Imamura M, Long X, Nanda V, Miano JM. Expression and functional activity of four myocardin isoforms. Gene. 2010 Sep 15; 464(1-2):1-10.
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Albinsson S, Suarez Y, Skoura A, Offermanns S, Miano JM, Sessa WC. MicroRNAs are necessary for vascular smooth muscle growth, differentiation, and function. Arterioscler Thromb Vasc Biol. 2010 Jun; 30(6):1118-26.
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Miano JM. What is truth? Standards of scientific integrity in American Heart Association journals. Arterioscler Thromb Vasc Biol. 2010 Jan; 30(1):1-4.
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Long X, Tharp DL, Georger MA, Slivano OJ, Lee MY, Wamhoff BR, Bowles DK, Miano JM. The smooth muscle cell-restricted KCNMB1 ion channel subunit is a direct transcriptional target of serum response factor and myocardin. J Biol Chem. 2009 Nov 27; 284(48):33671-82.
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Sun Q, Taurin S, Sethakorn N, Long X, Imamura M, Wang DZ, Zimmer WE, Dulin NO, Miano JM. Myocardin-dependent activation of the CArG box-rich smooth muscle gamma-actin gene: preferential utilization of a single CArG element through functional association with the NKX3.1 homeodomain protein. J Biol Chem. 2009 Nov 20; 284(47):32582-90.
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Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee TH, Miano JM, Ivey KN, Srivastava D. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature. 2009 Aug 6; 460(7256):705-10.
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Lee TH, Chen J, Miano JM. Functional characterization of a putative serine carboxypeptidase in vascular smooth muscle cells. Circ Res. 2009 Jul 31; 105(3):271-8.
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Bell RD, Deane R, Chow N, Long X, Sagare A, Singh I, Streb JW, Guo H, Rubio A, Van Nostrand W, Miano JM, Zlokovic BV. SRF and myocardin regulate LRP-mediated amyloid-beta clearance in brain vascular cells. Nat Cell Biol. 2009 Feb; 11(2):143-53.
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Miano JM. Deck of CArGs. Circ Res. 2008 Jul 3; 103(1):13-5.
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Miano JM. SRF'ing the actin cytoskeleton with no destrin. Physiol Genomics. 2008 Jun 12; 34(1):6-8.
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Long X, Bell RD, Gerthoffer WT, Zlokovic BV, Miano JM. Myocardin is sufficient for a smooth muscle-like contractile phenotype. Arterioscler Thromb Vasc Biol. 2008 Aug; 28(8):1505-10.
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Davis JL, Long X, Georger MA, Scott IC, Rich A, Miano JM. Expression and comparative genomics of two serum response factor genes in zebrafish. Int J Dev Biol. 2008; 52(4):389-96.
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Long X, Creemers EE, Wang DZ, Olson EN, Miano JM. Myocardin is a bifunctional switch for smooth versus skeletal muscle differentiation. Proc Natl Acad Sci U S A. 2007 Oct 16; 104(42):16570-5.
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Long X, Miano JM. Remote control of gene expression. J Biol Chem. 2007 Jun 1; 282(22):15941-5.
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Chow N, Bell RD, Deane R, Streb JW, Chen J, Brooks A, Van Nostrand W, Miano JM, Zlokovic BV. Serum response factor and myocardin mediate arterial hypercontractility and cerebral blood flow dysregulation in Alzheimer's phenotype. Proc Natl Acad Sci U S A. 2007 Jan 16; 104(3):823-8.
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Miano JM, Berk BC. HDAC7 supports vascular integrity. Nat Med. 2006 Sep; 12(9):997-8.
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Miano JM, Long X, Fujiwara K. Serum response factor: master regulator of the actin cytoskeleton and contractile apparatus. Am J Physiol Cell Physiol. 2007 Jan; 292(1):C70-81.
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Miano JM. Fishing for function in zebrafish. Circ Res. 2006 Mar 31; 98(6):723-6.
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Nagel DJ, Aizawa T, Jeon KI, Liu W, Mohan A, Wei H, Miano JM, Florio VA, Gao P, Korshunov VA, Berk BC, Yan C. Role of nuclear Ca2+/calmodulin-stimulated phosphodiesterase 1A in vascular smooth muscle cell growth and survival. Circ Res. 2006 Mar 31; 98(6):777-84.
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Lee TH, Streb JW, Georger MA, Miano JM. Tissue expression of the novel serine carboxypeptidase Scpep1. J Histochem Cytochem. 2006 Jun; 54(6):701-11.
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Rensen SS, Niessen PM, Long X, Doevendans PA, Miano JM, van Eys GJ. Contribution of serum response factor and myocardin to transcriptional regulation of smoothelins. Cardiovasc Res. 2006 Apr 1; 70(1):136-45.
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Miano JM, Georger MA, Rich A, De Mesy Bentley KL. Ultrastructure of zebrafish dorsal aortic cells. Zebrafish. 2006; 3(4):455-63.
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Sun Q, Chen G, Streb JW, Long X, Yang Y, Stoeckert CJ, Miano JM. Defining the mammalian CArGome. Genome Res. 2006 Feb; 16(2):197-207.
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Qiu P, Ritchie RP, Fu Z, Cao D, Cumming J, Miano JM, Wang DZ, Li HJ, Li L. Myocardin enhances Smad3-mediated transforming growth factor-beta1 signaling in a CArG box-independent manner: Smad-binding element is an important cis element for SM22alpha transcription in vivo. Circ Res. 2005 Nov 11; 97(10):983-91.
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Streb JW, Miano JM. Cross-species sequence analysis reveals multiple charged residue-rich domains that regulate nuclear/cytoplasmic partitioning and membrane localization of a kinase anchoring protein 12 (SSeCKS/Gravin). J Biol Chem. 2005 Jul 29; 280(30):28007-14.
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Blaxall BC, Miano JM, Berk BC. Angiotensin II: a devious activator of mineralocorticoid receptor-dependent gene expression. Circ Res. 2005 Apr 1; 96(6):610-1.
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Zlokovic BV, Deane R, Sallstrom J, Chow N, Miano JM. Neurovascular pathways and Alzheimer amyloid beta-peptide. Brain Pathol. 2005 Jan; 15(1):78-83.
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Streb JW, Miano JM. AKAP12alpha, an atypical serum response factor-dependent target gene. J Biol Chem. 2005 Feb 11; 280(6):4125-34.
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Miano JM, Ramanan N, Georger MA, de Mesy Bentley KL, Emerson RL, Balza RO, Xiao Q, Weiler H, Ginty DD, Misra RP. Restricted inactivation of serum response factor to the cardiovascular system. Proc Natl Acad Sci U S A. 2004 Dec 7; 101(49):17132-7.
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Streb JW, Kitchen CM, Gelman IH, Miano JM. Multiple promoters direct expression of three AKAP12 isoforms with distinct subcellular and tissue distribution profiles. J Biol Chem. 2004 Dec 31; 279(53):56014-23.
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Miano JM. Channeling to myocardin. Circ Res. 2004 Aug 20; 95(4):340-2.
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Zhang R, Al-Lamki R, Bai L, Streb JW, Miano JM, Bradley J, Min W. Thioredoxin-2 inhibits mitochondria-located ASK1-mediated apoptosis in a JNK-independent manner. Circ Res. 2004 Jun 11; 94(11):1483-91.
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Hogarth DK, Sandbo N, Taurin S, Kolenko V, Miano JM, Dulin NO. Dual role of PKA in phenotypic modulation of vascular smooth muscle cells by extracellular ATP. Am J Physiol Cell Physiol. 2004 Aug; 287(2):C449-56.
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Jiang M, Mezentsev A, Kemp R, Byun K, Falck JR, Miano JM, Nasjletti A, Abraham NG, Laniado-Schwartzman M. Smooth muscle--specific expression of CYP4A1 induces endothelial sprouting in renal arterial microvessels. Circ Res. 2004 Feb 6; 94(2):167-74.
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Aizawa T, Wei H, Miano JM, Abe J, Berk BC, Yan C. Role of phosphodiesterase 3 in NO/cGMP-mediated antiinflammatory effects in vascular smooth muscle cells. Circ Res. 2003 Sep 5; 93(5):406-13.
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Chen J, Chada S, Mhashilkar A, Miano JM. Tumor suppressor MDA-7/IL-24 selectively inhibits vascular smooth muscle cell growth and migration. Mol Ther. 2003 Aug; 8(2):220-9.
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Miano JM. Serum response factor: toggling between disparate programs of gene expression. J Mol Cell Cardiol. 2003 Jun; 35(6):577-93.
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Davis A, Hogarth K, Fernandes D, Solway J, Niu J, Kolenko V, Browning D, Miano JM, Orlov SN, Dulin NO. Functional significance of protein kinase A activation by endothelin-1 and ATP: negative regulation of SRF-dependent gene expression by PKA. Cell Signal. 2003 Jun; 15(6):597-604.
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Streb JW, Miano JM. Retinoids: pleiotropic agents of therapy for vascular diseases? Curr Drug Targets Cardiovasc Haematol Disord. 2003 Mar; 3(1):31-57.
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Chen J, Kitchen CM, Streb JW, Miano JM. Myocardin: a component of a molecular switch for smooth muscle differentiation. J Mol Cell Cardiol. 2002 Oct; 34(10):1345-56.
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Miano JM. Cardiac-specific gene expression: a HANDful of factors. J Mol Cell Cardiol. 2002 Oct; 34(10):1287-91.
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Miano JM, Kitchen CM, Chen J, Maltby KM, Kelly LA, Weiler H, Krahe R, Ashworth LK, Garcia E. Expression of human smooth muscle calponin in transgenic mice revealed with a bacterial artificial chromosome. Am J Physiol Heart Circ Physiol. 2002 May; 282(5):H1793-803.
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Miano JM. Mammalian smooth muscle differentiation: origins, markers and transcriptional control. Results Probl Cell Differ. 2002; 38:39-59.
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Frame MD, Miano JM, Yang J, Rivers RJ. Localized adenovirus-mediated gene transfer into vascular smooth muscle in the hamster cheek pouch. Microcirculation. 2001 Dec; 8(6):403-13.
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Dulin NO, Orlov SN, Kitchen CM, Voyno-Yasenetskaya TA, Miano JM. G-protein-coupled-receptor activation of the smooth muscle calponin gene. Biochem J. 2001 Jul 15; 357(Pt 2):587-92.
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Chen J, Streb JW, Maltby KM, Kitchen CM, Miano JM. Cloning of a novel retinoid-inducible serine carboxypeptidase from vascular smooth muscle cells. J Biol Chem. 2001 Sep 7; 276(36):34175-81.
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Miano JM, Berk BC. Retinoids: new insight into smooth muscle cell growth inhibition. Arterioscler Thromb Vasc Biol. 2001 May; 21(5):724-6.
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Miano JM, Thomas S, Disteche CM. Expression and chromosomal mapping of the mouse smooth muscle calponin gene. Mamm Genome. 2001 Mar; 12(3):187-91.
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Chen J, Maltby KM, Miano JM. A novel retinoid-response gene set in vascular smooth muscle cells. Biochem Biophys Res Commun. 2001 Feb 23; 281(2):475-82.
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Ou H, Haendeler J, Aebly MR, Kelly LA, Cholewa BC, Koike G, Kwitek-Black A, Jacob HJ, Berk BC, Miano JM. Retinoic acid-induced tissue transglutaminase and apoptosis in vascular smooth muscle cells. Circ Res. 2000 Nov 10; 87(10):881-7.
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Camoretti-Mercado B, Liu HW, Halayko AJ, Forsythe SM, Kyle JW, Li B, Fu Y, McConville J, Kogut P, Vieira JE, Patel NM, Hershenson MB, Fuchs E, Sinha S, Miano JM, Parmacek MS, Burkhardt JK, Solway J. Physiological control of smooth muscle-specific gene expression through regulated nuclear translocation of serum response factor. J Biol Chem. 2000 Sep 29; 275(39):30387-93.
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Miano JM, Berk BC. Retinoids: versatile biological response modifiers of vascular smooth muscle phenotype. Circ Res. 2000 Sep 1; 87(5):355-62.
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Miano JM, Carlson MJ, Spencer JA, Misra RP. Serum response factor-dependent regulation of the smooth muscle calponin gene. J Biol Chem. 2000 Mar 31; 275(13):9814-22.
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Nobrega MA, Shiozawa M, Koike G, Jacob HJ, Miano JM. Gene structure and chromosomal mapping of the rat smooth muscle calponin gene. Mamm Genome. 2000 Feb; 11(2):115-9.
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Molkentin JD, Antos C, Mercer B, Taigen T, Miano JM, Olson EN. Direct activation of a GATA6 cardiac enhancer by Nkx2.5: evidence for a reinforcing regulatory network of Nkx2.5 and GATA transcription factors in the developing heart. Dev Biol. 2000 Jan 15; 217(2):301-9.
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Miano JM, Berk BC. NAB2: a transcriptional brake for activated gene expression in the vessel wall? Am J Pathol. 1999 Oct; 155(4):1009-12.
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Kowal RC, Richardson JA, Miano JM, Olson EN. EVEC, a novel epidermal growth factor-like repeat-containing protein upregulated in embryonic and diseased adult vasculature. Circ Res. 1999 May 28; 84(10):1166-76.
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Miano JM, Garcia E, Krahe R. Radiation Hybrid (RH) Mapping of Human Smooth Muscle-Restricted Genes. Methods Mol Med. 1999; 30:25-35.
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Miano JM, Kelly LA, Artacho CA, Nuckolls TA, Piantedosi R, Blaner WS. all-Trans-retinoic acid reduces neointimal formation and promotes favorable geometric remodeling of the rat carotid artery after balloon withdrawal injury. Circulation. 1998 Sep 22; 98(12):1219-27.
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Zilberman A, Dave V, Miano J, Olson EN, Periasamy M. Evolutionarily conserved promoter region containing CArG*-like elements is crucial for smooth muscle myosin heavy chain gene expression. Circ Res. 1998 Mar 23; 82(5):566-75.
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Firulli AB, Han D, Kelly-Roloff L, Koteliansky VE, Schwartz SM, Olson EN, Miano JM. A comparative molecular analysis of four rat smooth muscle cell lines. In Vitro Cell Dev Biol Anim. 1998 Mar; 34(3):217-26.
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Koike G, Miano JM, Vanvooren P, Shiozawa M, Szpirer C, Jacob HJ. Mapping of the rat SM22 gene to chromosome 8q24: a candidate for high blood pressure and cardiac hypertrophy. Mamm Genome. 1998 Jan; 9(1):76-7.
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Rao RS, Miano JM, Olson EN, Seidel CL. The A10 cell line: a model for neonatal, neointimal, or differentiated vascular smooth muscle cells? Cardiovasc Res. 1997 Oct; 36(1):118-26.
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Miano JM, Krahe R, Garcia E, Elliott JM, Olson EN. Expression, genomic structure and high resolution mapping to 19p13.2 of the human smooth muscle cell calponin gene. Gene. 1997 Sep 15; 197(1-2):215-24.
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Miano JM, Topouzis S, Majesky MW, Olson EN. Retinoid receptor expression and all-trans retinoic acid-mediated growth inhibition in vascular smooth muscle cells. Circulation. 1996 May 15; 93(10):1886-95.
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Miano JM, Olson EN. Expression of the smooth muscle cell calponin gene marks the early cardiac and smooth muscle cell lineages during mouse embryogenesis. J Biol Chem. 1996 Mar 22; 271(12):7095-103.
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Li L, Miano JM, Mercer B, Olson EN. Expression of the SM22alpha promoter in transgenic mice provides evidence for distinct transcriptional regulatory programs in vascular and visceral smooth muscle cells. J Cell Biol. 1996 Mar; 132(5):849-59.
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Li L, Miano JM, Cserjesi P, Olson EN. SM22 alpha, a marker of adult smooth muscle, is expressed in multiple myogenic lineages during embryogenesis. Circ Res. 1996 Feb; 78(2):188-95.
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Firulli AB, Miano JM, Bi W, Johnson AD, Casscells W, Olson EN, Schwarz JJ. Myocyte enhancer binding factor-2 expression and activity in vascular smooth muscle cells. Association with the activated phenotype. Circ Res. 1996 Feb; 78(2):196-204.
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Miano JM, Firulli AB, Olson EN, Hara P, Giachelli CM, Schwartz SM. Restricted expression of homeobox genes distinguishes fetal from adult human smooth muscle cells. Proc Natl Acad Sci U S A. 1996 Jan 23; 93(2):900-5.
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Miano JM, Cserjesi P, Ligon KL, Periasamy M, Olson EN. Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis. Circ Res. 1994 Nov; 75(5):803-12.
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Pritchard KA, O'Banion MK, Miano JM, Vlasic N, Bhatia UG, Young DA, Stemerman MB. Induction of cyclooxygenase-2 in rat vascular smooth muscle cells in vitro and in vivo. J Biol Chem. 1994 Mar 18; 269(11):8504-9.
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Martin JF, Miano JM, Hustad CM, Copeland NG, Jenkins NA, Olson EN. A Mef2 gene that generates a muscle-specific isoform via alternative mRNA splicing. Mol Cell Biol. 1994 Mar; 14(3):1647-56.
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Miano JM, Vlasic N, Tota RR, Stemerman MB. Localization of Fos and Jun proteins in rat aortic smooth muscle cells after vascular injury. Am J Pathol. 1993 Mar; 142(3):715-24.
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Miano JM, Vlasic N, Tota RR, Stemerman MB. Smooth muscle cell immediate-early gene and growth factor activation follows vascular injury. A putative in vivo mechanism for autocrine growth. Arterioscler Thromb. 1993 Feb; 13(2):211-9.
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Miano JM, Tota RR, Vlasic N, Danishefsky KJ, Stemerman MB. Early proto-oncogene expression in rat aortic smooth muscle cells following endothelial removal. Am J Pathol. 1990 Oct; 137(4):761-5.
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Miano JM, Holland JA, Pritchard KA, Rogers NJ, Stemerman MB. Low density lipoprotein-mediated endothelial cell perturbation: effects on endothelial cell eicosanoid metabolism. Adv Prostaglandin Thromboxane Leukot Res. 1989; 19:248-54.
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