X Chromosome-Inactivation Patterns in 31 Individuals with PHACE Syndrome
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1 Originl Article Invited nd ccepted: August 20, 2012 by M. Vikkul Published online: November 16, Individuls with PHACE Syndrome C.T. Sullivn S.L. Christin J.T.C. Shieh c D. Metry d F. Blei e A. Krol f B.A. Drolet g I.J. Frieden b W.B. Dobyns, b D.H. Siegel f Center for Integrtive Brin Reserch, Settle Children s Reserch Institute, nd b Deprtments of Peditrics nd Neurology, University of Wshington, nd Center for Integrtive Brin Reserch, Settle Children s Reserch Institute, Settle, Wsh., c Division of Medicl Genetics, Deprtment of Peditrics nd Institute for Humn Genetics, University of Cliforni Sn Frncisco, Sn Frncisco, Clif., d Deprtment of Dermtology nd Peditrics, Texs Children s Hospitl, Houston, Tex., e Vsculr Birthmrk Institute of New York, St. Luke s Roosevelt Hospitl, New York, N.Y., f Deprtment of Dermtology, Oregon Helth nd Science University, Portlnd, Oreg., g Deprtment of Dermtology nd Peditrics, Medicl College of Wisconsin, Children s Hospitl of Wisconsin, Milwukee, Wisc., USA Key Words Corcttion of the ort Hemngiom PHACE syndrome Posterior foss nomly X-inctivtion Abstrct Segmentl hemngioms of the hed nd neck cn be ssocited with multiple congenitl nomlies in the disorder known s PHACE syndrome (OMIM ) (posterior foss mlformtions, hemngiom, rteril nomlies, crdic defects, nd eye nomlies). All reported cses of PHACE syndrome to dte hve been spordic, nd the genetic bsis of this disorder hs not yet been estblished. PHACE syndrome hs striking femle predominnce which hs rised the question of X-linked inheritnce. In this study, the X chromosome-inctivtion (XCI) ptterns of 31 femles with PHACE syndrome nd their mothers were nlyzed using blood-derived DNA nd X-chromosome locus methyltion ssy. This study ws performed to test the hypothesis tht some cses of PHACE syndrome re due to X-linked inheritnce nd fvorble skewing in the mothers my protect ginst severe phenotype, but the clinicl phenotype my be unmsked in dughters with rndom pttern of X-inctivtion. XCI nlysis ws informtive in 27/31 mothers. Our results identified skewed XCI in 5 of 27 (19%) informtive mothers, which is not sttisticlly significnt with p vlue of None of the mothers reported significnt medicl problems, lthough full PHACE work-up hs not been performed in these individuls. Skewed XCI in the mothers of children with PHACE ws identified in only minority of cses. Bsed on these results, genetic heterogeneity is likely in PHACE syndrome, lthough it is possible subset of cses re cused by muttion in n X-linked gene. Copyright 2012 S. Krger AG, Bsel Segmentl hemngioms of the hed nd neck cn be ssocited with mlformtions of the hert, cerebrl rteries, brin, nd eyes [Hggstrom et l., 2010]. This ssocition ws first described in prtil form consisting of fcil hemngioms nd crnil rteril nomlies, expnded by dding Dndy-Wlker mlformtion, nd lt- E-Mil krger@krger.com S. Krger AG, Bsel /13/ $38.00/0 Dwn Siegel, MD 8701 Wtertown Plnk Rod TBRC 2nd Floor, C2010 Milwukee, WI (USA) E-Mil mcw.edu
2 er designted s PHACE (posterior foss nomlies, hemngiom, rteril nomlies, crdic nomlies/corcttion of the ort, eye nomlies, nd sternl defects) syndrome [Frieden et l., 1996]. More thn 300 ptients with PHACE syndrome hve been reported in the literture. In 2008, multidisciplinry group of specilists convened to develop consensus sttement on the dignostic criteri for PHACE syndrome [Metry et l., 2009]. A dignosis of definite PHACE syndrome is bsed on fcil hemngiom lrger thn 5 cm plus 1 mjor or 2 minor criteri ( tble 1 ). Severl cse series nd prospective studies hve described skewing of the sex rtio towrd femles [Gorlin et l., 1994; Hemngiom Investigtor Group et l., 2007], with n initil reported 8: 1 femle to mle rtio [Metry et l., 2006]. More recently, lrger studies on individuls with PHACE, s well s dt from the PHACE Syndrome Clinicl Registry nd DNA Repository with 150 subjects enrolled, hve reported slightly lower femle to mle rtio t 5.6: 1 [Hggstrom et l., 2010]. Levin et l. [2007] reported cse of femle infnt with dignosis of PHACE syndrome bsed on periorl hemngioms s well s hemngioms on the chest nd extremities, cerebrovsculr nomlies, sternl scr nd suprumbilicl rphe. X chromosome-inctivtion (XCI) studies showed rndom XCI pttern in the ffected child nd skewed pttern in the mother, suggesting tht the skewed XCI in the mother my hve been protective [Levin nd Kler, 2007]. Given the femle predominnce nd the previous cse report of skewed XCI in PHACE syndrome, the question of whether XCI could hve broder role in the pthogenesis of PHACE hs been rised [Levin nd Kler, 2007]. In generl, XCI is expected to be rndom. It occurs during the blstocyst stge in femle development when one of 2 X chromosomes in ech cell is silenced [Hendrich et l. 1997; Pnning et l., 1997]. However, when muttion is present on one X chromosome, tht cell popultion my hve growth disdvntge, resulting in skewed XCI. Thus, in some cses, nonrndom skewing wy from disese llele my be protective. The X- linked neurodevelopmentl condition, Rett syndrome, hs been used s model to study the influence of XCI [Young nd Zoghbi, 2004]. In some reports, skewed XCI hs been ssocited with milder Rett phenotype, suggesting tht suppression of the mutted llele ws protective [Ishii et l., 2001]. In ddition, in certin clsses of X-linked mentl retrdtion disorders, the crriers hve high rte of skewed ( 1 80: 20) XCI with skewing ginst the cells with the muttion [Plenge et l., 2002]. In this study, we performed XCI studies in 31 motherdughter duos to evlute the ptterns of X-inctivtion in PHACE syndrome. M e t h o d s Subjects This study ws pproved by the Children s Hospitl of Wisconsin Institutionl Review Bord nd IRBs of collborting institutions. Subjects were ll enrolled in the Genetic Anlysis of PHACE Syndrome study s prt of the PHACE Syndrome Interntionl Clinicl Registry nd DNA Repository. Subjects were selected for this X-inctivtion study from the PHACE syndrome Interntionl DNA Repository. All met published dignostic criteri outlined in tble 1. DNA Extrction Peripherl blood ws obtined t the time of enrollment in the Genetic Anlysis of PHACE Syndrome study. The Puregene DNA Purifiction kit ws used to isolte DNA using the mnufcturer s protocol. X-Inctivtion Studies The 2 X chromosomes in humn femles cn be distinguished from ech other by using polymorphic CAG repet on exon 1 of AR (humn ndrogen receptor) in Xq12. The XCI sttus of ech llele is mesured by compring their reltive levels of CpG methyltion, using the methyltion-sensitive restriction enzyme Hp II. Genomic DNA ws digested with either RsI lone or RsI with HpII, nd digests were PCR mplified s previously described [Amos-Lndgrf et l., 2006]. RsI is used s bckground enzyme; it digests genomic DNA, but does not ffect frgment size, s the PCR mplified region does not contin n RsI cutting site. All PCRs were done in duplicte. The forwrd primer ws lbeled with FAM on the 5 end. PCR products were nlyzed on n ABI 3730 XL DNA sequencing nlyzer t Settle BioMed Reserch Institute nd processed using GeneMrker 1.9 softwre (SoftGenetics). The X-inctivtion level of ech llele ws clculted using pek heights with the formuls X 1 = [d1/u1]/[(d1/u1) + (d2/u2)] nd X 2 = [d2/u2]/[(d1/ u1) + (d2/u2)], where d nd u denote HpII-digested nd undigested DNA respectively ( fig. 1 ). The X-inctivtion rtios (X 1 :X 2 ) represent the level of inctivtion of the smller llele compred to tht of the lrger llele. Following stndrd prctice, rndom XCI ws defined s 50: 50 to 79: 31, skewed XCI s 80: 20 or lrger, nd highly skewed s 90: 10 or lrger. Nine individuls hd lleles with only one CAG-repet different in size ( fig. 1 ), which mkes exct rtios difficult to quntify due to overlpping nd lower moleculr weight (MW) stutter-pek rtifcts present in short tndem repet PCRs [Amos-Lndgrf et l., 2006]. The stutter pek heights in our experiments were generlly 33% or less of the pek height of the true llele. To correct for stutter peks in these 4 cses only, 33% of the height of the lrger MW llele ws subtrcted from the smller MW llele before clculting the XI rtio: u1 corrected = u1 0.33! u2, nd d1 corrected = d1 0.33! d2. PHACE Syndrome 115
3 Fig. 1. XI Assy: Microstellite PCR products of AR re shown with (right) nd without (left) Hp II digestion. Arrows indicte peks u1 (red), u2 (blue), d1 (ornge), nd d2 (green) s described in Methods. Individul hd the most skewed XI rtio in this study, t 07: 93. Tble 1. Mjor nd minor dignostic criteri of PHACE syndrome Criteri % Mjor Segmentl hemngiom of the hed 100 Dysplsi of lrge cerebrl rtery 14 Stenosis, occlusion, bsence or hypoplsi of lrge cerebrl rtery 60 Posterior foss nomly 35 Aortic rch nomly 28 Anomlous subclvin rtery 14 Posterior segment nomlies of the eye 8 Sternl defect 22 Umbilicl rphe 9 Minor Persistent embryonic rteries other thn trigeminl 7 Midline nomlies 2 Disorder of migrtion 6 Ventriculr septl defect 13 Anterior segment defect of the eye 8 Sternl ppule 1.5 T he Hemngiom Investigtor Group published consensus sttement on the dignostic criteri of PHACE syndrome [Metry et l., 2009]. Definite PHACE = Segmentl hemngiom of the hed >5 cm plus 1 mjor or 2 minor criteri; possible PHACE = segmentl hemngiom of the hed >5 cm plus 1 minor criteri [modified with permission]. R e s u l t s Demogrphic Informtion Our cohort consisted of 31 femles with PHACE syndrome nd their mothers. The reported ethnicities for the probnds were s follows: Cucsin non-hispnic (25), Cucsin-Hispnic (4), Africn-Americn (1), nd Asin (1). The ge rnge of the mothers t the time of pregnncy ws yers. Phenotypic Chrcteristics of the Cohort Bsed on inclusion criteri, ll subjects hd segmentl hemngiom on the hed nd neck. Structurl brin nomlies were reported in 14/31 (45%). Imging of the cerebrl rteries ws vilble for 29/31 probnds. Cerebrovsculr nomlies were reported in 25/27 (92%). A totl of 11/31 (35%) subjects reported congenitl hert defects nd 4 reported berrnt subclvin rteries. Crdic nd ortic nomlies included: corcttion (5), dilted ort (2), tetrlogy of Fllot (1), VSD (1), nd right ortic rch (2). Eye nomlies were reported in 14/31 (45%). Sternl defects were only reported in 4/31 (13%) subjects. X-Inctivtion Results XCI nlysis ws informtive in 27/31 mothers; 4 mothers were homozygous nd, thus, uninformtive by our ssy. Primry dt re shown in figure 1 nd the results re 116 Sullivn /Christin/Shieh /Metry /Blei / Krol /Drolet /Frieden /Dobyns /Siegel
4 Tble 2. X-chromosome inctivtion results in fmilies of children with PHACE syndrome Probnd Sex XCI rtio Mother XCI rtio F 26: : F 62: : F 62: : F 68: : F 61: : F 70: : F 63: : F 66: : F 83: : F 48: : F 32: : F 51: : F 45: : F 47: : F 07: : F 52: : F 57: : F 70: : F 52: UI F 67: :64 LR F 64:36 LR03-223m 43:57 LR F 61:39 LR03-294m 73:27 LR F 63:37 LR04-119m UI LR F ND LR05-117m 25:75 B061.0 F 84:16 B :29 B084.0 F UI B :49 B138.0 F 62:38 B138.1 UI F 59: : F 50: UI B512.0 F 64:36 B :34 B703.0 F 34:66 B :45 C ses with XCI skewing of 80:20 or lrger re bolded. UI = Uninformtive due to homozygosity t AR locus; ND = testing ws not done. summrized in tble 2. We found skewed XCI in lymphocytes in 5 of the 27 (19%) informtive mothers, which is slightly more thn the expected popultion verge of 15% determined in n nlysis of 415 helthy dult femle controls, lthough not sttisticlly significnt with p vlue of 0.41 (Fisher s exct test) [Amos-Lndgrf et l., 2006]. XCI studies were informtive in 29/31 femle probnds for which we hd DNA. We found skewed XCI in 3 of 29 (10%), which is not sttisticlly significntly different thn the expected popultion verge of 5% determined from nlysis of 590 helthy newborn girls with vlue of 0.23 (Fisher s exct test) [Amos-Lndgrf et l., 2006]. The remining mothers nd probnds hd rndom ptterns of XCI. Discussion PHACE syndrome hs emerged s n importnt neurocutneous nd neurovsculr syndrome, occurring in pproximtely 30% of infnts with segmentl hemngioms of the hed nd neck [Hggstrom et l., 2010]. The incidence of PHACE syndrome hs likely been underestimted. In prospective study performed in peditric dermtology clinics, scertinment of PHACE ws higher thn tht of Sturge-Weber syndrome, suggesting tht PHACE is more common thn ltter [Metry et l., 2006]. The pthogenesis of PHACE syndrome is unknown; however, risk fctors include femle sex (femle:mle rtio = 5.6: 1), white non-hispnic ethnicity (68%) nd premture birth (16%) [Metry et l., 2008]. Although there is femle predominnce, the reported severity of ffected mles seems comprble to ffected femles. One possible exception is the slightly higher occurrence of brin mlformtions in mles with PHACE [Metry et l., 2008]. No specific environmentl influences hve been identified, nd to dte, ll reports of PHACE syndrome hve been spordic. One prior cse report demonstrting skewed X-inctivtion in the mother of femle with PHACE syndrome rised the question of whether skewed XCI my ply protective role in the mothers of children with PHACE [Levin nd Kler, 2007]. In this study, we follow-up on tht report by performing XCI studies on group of 31 femles with PHACE syndrome nd their mothers. Although there ws slight increse in the number of mothers nd dughters with skewed XCI compred with the expected popultion verge, these findings were not sttisticlly significnt. Despite the femle predominnce in PHACE syndrome, we did not find significnt increse in skewed XCI in the probnds or their mothers. In considering the pthogenetic mechnism in PHACE syndrome, severl observtions my provide relevnt clues. The most common nd consistent bnormlities involve rteriopthy of the gret vessels, with the most severely ffected ptients hving extensive bilterl involvement of brin, neck, chest, gstrointestinl trct, nd mesenteric rteries. Less severely ffected ptients my hve unilterl loclized involvement. The regionl locliztion of findings in the mjority of cses hs led some to suggest developmentl field defect or postzygotic mosicism s possible mechnism in PHACE [Metry et l., 2006]. The striking regionl vrition observed in ptients with PHACE, nd relted hemngiom syndromes, lends considerble support to mosic hypothesis. Severl other wellknown developmentl disorders my be cused by either PHACE Syndrome 117
5 germline or mosic muttions of the cusl gene. For exmple, both germline nd mosic muttions hve been observed in focl derml hypoplsi, n X-linked syndrome cused by muttions in the PORCN gene [Grzeschik et l., 2007]. In summry, skewed XCI in the mothers of children with PHACE ws identified in only minority of cses; therefore, we conclude mternl skewed XCI does not highly correlte with most cses of PHACE syndrome. Further studies using next-genertion sequencing my provide further insight into the underlying pthogenetic mechnism in PHACE syndrome. Acknowledgements We would like to thnk the fmilies who prticipted in this study. We re grteful to Gin Im nd Shwn Jochim for their ssistnce with dt mngement. D.H.S. ws supported by the Oregon Clinicl Trnsltionl Reserch Institute (grnt UL1 RR from the Ntionl Center for Reserch Resources (NCRR), component of the Ntionl Institutes of Helth (NIH), nd NIH Rodmp for Medicl Reserch), Dermtology Foundtion Creer Development Awrd nd Ptient Directed Investigtor Awrd nd the Society for Peditric Dermtology Willim L. Weston Reserch Grnt. This study ws supported in prt by grnt from the NIH to Dr. Dobyns (2R01-NS046616). J.T.C.S. is supported by NIH NHLBI. References Amos-Lndgrf JM, Cottle A, Plenge RM, Friez M, Schwrtz CE, et l: X chromosome-inctivtion ptterns of 1,005 phenotypiclly unffected femles. Am J Hum Genet 79: (2006). Frieden IJ, Reese V, Cohen D: PHACE syndrome. The ssocition of posterior foss brin mlformtions, hemngioms, rteril nomlies, corcttion of the ort nd crdic defects, nd eye bnormlities. Arch Dermtol 132: (1996). Gorlin RJ, Kntputr P, Aughton DJ, Mulliken JB: Mrked femle predilection in some syndromes ssocited with fcil hemngioms. Am J Med Genet 52: (1994). Grzeschik KH, Bornholdt D, Oeffner F, König A, del Crmen Boente M, et l: Deficiency of PORCN, regultor of Wnt signling, is ssocited with focl derml hypoplsi. Nt Genet 39: (2007). Hggstrom AN, Grzon MC, Bselg E, Chmlin SL, Frieden IJ, et l: Risk for PHACE syndrome in infnts with lrge fcil hemngioms. Peditrics 126:e (2010). Hemngiom Investigtor Group, Hggstrom AN, Drolet BA, Bselg E, Chmlin SL, et l: Prospective study of infntile hemngioms: demogrphic, prentl, nd perintl chrcteristics. J Peditr 150: (2007). Hendrich BD, Plenge RM, Willrd HF: Identifiction nd chrcteriztion of the humn XIST gene promoter: implictions for models of X chromosome inctivtion. Nucleic Acids Res 25: (1997). Ishii T, Mkit Y, Ogw A, Ammiy S, Ymmoto M, et l: The role of different X-inctivtion pttern on the vrible clinicl phenotype with Rett syndrome. Brin Dev 23 Suppl 1:S (2001). Levin JH, Kler SG: Non-rndom mternl X- chromosome inctivtion ssocited with PHACES. Clin Genet 72: (2007). Metry DW, Hggstrom AN, Drolet BA, Bselg E, Chmlin S, et l: A prospective study of PHACE syndrome in infntile hemngioms: demogrphic fetures, clinicl findings, nd complictions. Am J Med Genet A 140: (2006). Metry DW, Siegel DH, Cordisco MR, Pope E, Prendiville J, et l: A comprison of disese severity mong ffected mle versus femle ptients with PHACE syndrome. J Am Acd Dermtol 58: (2008). Metry DW, Heyer G, Hess C, Grzon M, Hggstrom A, et l: Consensus Sttement on Dignostic Criteri for PHACE Syndrome. Peditrics 124: (2009). Pnning B, Dusmn J, Jenisch R: X chromosome inctivtion is medited by Xist RNA stbiliztion. Cell 90: (1997). Plenge RM, Stevenson RA, Lubs HA, Schwrtz CE, Willrd HF: Skewed X-chromosome inctivtion is common feture of X-linked mentl retrdtion disorders. Am J Hum Genet 71: (2002). Young JI, Zoghbi HY: X-chromosome inctivtion ptterns re unblnced nd ffect the phenotypic outcome in mouse model of Rett syndrome. Am J Hum Genet 74: (2004). 118 Sullivn /Christin/Shieh /Metry /Blei / Krol /Drolet /Frieden /Dobyns /Siegel
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