Defective Wnt-dependent cerebellar midline fusion in a mouse model of Joubert syndrome
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1 correction notice Nt. Med. 17, (2011) Defective Wnt-dependent cereellr midline fusion in mouse model of Jouert syndrome Mdeline A Lncster, Dipik J Gopl, Joon Kim, Shr N Sleem, Jennifer L Silhvy, Crrie M Louie, Bryn E Thcker, Yuko Willims, Mh S Zki & Joseph G Gleeson In the version of this supplementry file originlly posted online, the Supplementry Discussion ws missing. The Supplementry Discussion is now provided s of 8 July 2011.
2 Supplementry Informtion Defective Wnt-dependent cereellr midline fusion in mouse model of Jouert syndrome Mdeline A. Lncster, Dipik J. Gopl, Joon Kim, Shr N. Sleem, Jennifer L. Silhvy, Crrie M. Louie, Bryn E. Thcker, Yuko Willims, Mh S. Zki, Joseph G. Gleeson
3 15 months Supplementl Figure 1 Are (mm 2 ) Control / Ahi1 Control Ahi1 / * Reltive re (.u.) ** Totl rin size Reltive cereellum size Ahi1 +/+ Ahi1 / c Control Ahi1 / d Control Ahi1 / e Rostrl Ahi1 +/+ Ahi1 / Ahi1 / Cudl Supplementl Figure 1. Lter phenotype ut intct rinstem structures.. Averge totl rin re size mesurements for Ahi1 mutnts compred with littermte controls (left). Averge cereellum re size reltive to totl rin re (.u.=ritrry units) from Ahi1 mutnts compred with littermte controls (right). *P<0.05, **P< Student s t-test, n=3 for ech genotype.. Representtive 15 month old littermte sgittl C-V stined sections reveling persistent size nd folition defects (rrows). c. Top, C-V stined coronl sections reveling intct superior cereellr peduncles (rrow) in Ahi1 / compred with littermte control. Bottom, C-V stined mediolterl sgittl sections reveling intct rinstem structures in Ahi1 mutnts. Arrowheds=deep cereellr nuclei, rrow=superior cereellr peduncle, open rrows=descending trigeminl trct, open rrowheds=dorsl column nuclei. d. C-V stined sgittl prmedicl sections of cereell from Ahi1 mutnt nd control littermte t higher mgnifiction reveling deep cereellr nuclei (rrowheds). e. Biotinylted dextrn mine (BDA) trcing ssy in two Ahi1 mutnts nd littermte control. Coronl sections through rinstem nd spinl cord revel crossing of pyrmidl xons from rostrl to cudl sections. Boxes outline DAB positive xons nd lines revel crossing of xons.
4 3 weeks Supplementl Figure 2 Ahi1 +/ Ahi1 / IGL PC ML IGL PC ML Ahi1 +/ Ahi1 / GABA-ARα6 Cl Hoechst c Ahi1 +/ Ahi1 / Supplementl Figure 2. Norml lyering in Ahi1 mutnt cereell.. High mgnifiction imge of lyering within the cereellr vermis of Ahi1 mutnt nd littermte control s visulized y C-V stining of sgittl sections. Lyers re shown: inner grnule lyer (IGL), Purkinje cell lyer (PC), moleculr lyer (ML).. Stining for cereellr lyers ppers intct in Ahi1 mutnts. Clindin (green) lels Purkinje neurons, GABA-A receptor α6 (GABA-ARα6, red) lels inner grnule lyer. Hoechst (lue) lels nuclei. c. Golgi-Cox stining reveling dendritic tree rchitecture of Purkinje neurons in Ahi1 / nd Ahi1 +/ cereell.
5 Supplementl Figure 3 Reltive PH3 + cells * 0 Con KO Ahi1: N-Myc Tuulin E16.5 +/ / c Ahi1 +/ Ahi1 / Ptc1 Hoechst Ptc1 Supplementl Figure 3. Erly prolifertion defects ut intct Shh signling in Ahi1 mutnts.. Averge numer of phospho-histone H3 (PH3) stined externl grnule lyer neurons (EGL) t E16.5 reltive to totl cells in EGL. *P<0.05, Student s t-test, n=3.. Western lot on whole cereellum lystes from P5 littermtes. N-myc ntiody recognizes primry nd t pproximtely 70kD. Tuulin is the loding control. c. Ptc1 (green) stining in P5 midline sgittl sections from Ahi1 / nd Ahi1 +/ littermtes. Hoechst (lue) lels nuclei.
6 Supplementl Figure 4 Ahi1 +/ Ahi1 / Anterior V D A P Posterior E13.5 Supplementl Figure 4. Roof plte widening in Ahi1 mutnts. Mtched trnsverse C-V stined sections from littermtes rrnged in series from nterior to posterior reveling the progressive posterior widening of the roof plte in Ahi1 mutnt (rs). Digrm inset depicts pproximte loctions of nterior nd posterior sections.
7 cahi1+/ Supplementl Figure 5 Chr /SvJ k wildtype llele trgeting vector HSV-TK PGK-neo 3839 homologous recomintion in ES cells trgeted llele PGK-neo Cre recomintion knockout llele Control Cep290 / NS 10 Are (mm 2 ) Averge loule numer * Control Cep290 / Superior Inferior Control Cep290 / Mouse E16.5 Ahi1 / Inferior Superior Supplementl Figure 5. Cep290 trgeting nd dult phenotype.. Schemtic of trgeting pproch used to generte Cep290 null mice descried in methods. Homologous recomintion is represented y dshed crossing lines, nd resulting lleles re shown. Positions for genotyping primers re shown: Closed rrows re wild-type primers, open rrows re knock-out primers.. Left, representtive midline sgittl C-V stined sections from dult Cep290 / nd littermte control. Arrow points to mild folition defect in Cep290 mutnts. Right, quntifiction of verge vermis re in Cep290 / nd littermte controls. NS=not significnt, Student s t-test, n=3 for ech genotype. Bottom, quntifiction of verge numer of loules in Cep290 / littermte controls. *P<0.05, Student s t-test, n=3 for ech genotype. Error rs re S.E.M. c. Trnsverse C-V stined sections from Ahi1 mutnt nd littermte control shown in series from superior to inferior. Arrow points to fusion defect.
8 Percentge of Cells (%) Supplementl Figure 6 25 kd Vector WT R723Q H896R V443D 150 GFP 50 α-tuulin WT R723Q H896R V443D Jn α-tuulin c WT R723Q H896R V443D Vector WT R723Q H896R V443D Ciliry locliztion Nonciliry (diffuse) locliztion Supplementl Figure 6. Expression nlysis nd locliztion of disese muttions.. Western lot from 293T cells trnsfected with mutnt constructs nd ssyed for GFP levels. Tuulin represents the loding control.. Western lot from IMCD cells trnsfected with mutnt constructs nd ssyed for Jn levels. Tuulin represents the loding control. c. Locliztion of Jn disese muttion constructs (green) in IMCD cells stined for cili (cetylted tuulin, red). Hoechst lels nuclei. Below, quntifiction of cili locliztion in 100 cells for ech construct.
9 Supplementl Figure 7 NS NS c Ac-Tuulin Jn-GFP Tuulin Jn Hoechst Reltive luciferse 100 kd W3A: GFP EV Vector WT R723Q H896R V443D IP: nti-gfp GFP-JnWT * NS GFP-R723Q GFP-H896R GFP-V443D 100 kd GFP EV Lystes GFP-JnWT GFP-R723Q GFP-H896R GFP-V443D WB: β-ctenin 5μm Ac-Tuulin α-jn Tuulin Jn Hoechst 5μm Ac-Tuulin α-β-ctenin Tu β-ct Hoechst 5μm α-jn β-ctenin-gfp Jn β-ct Tuulin GFP GAPDH 5μm Supplementl Figure 7. Disese muttions fil to potentite Wnt signling.. Luciferse ctivity in firolsts trnsfected with wild-type Jn or mutnt constructs nd treted with Wnt3A (W3A) conditioned medi. NS=not significnt, *P<0.05, Student s t-test, n=3. Error rs re S.E.M.. Co-immunoprecipittion in 293T cells of Jn GFP constructs pulled down with GFP ntiody nd western lot for endogenous β-ctenin which revels interction etween β-ctenin nd wild-type Jn s well R723Q nd H896R ut not with V443D. GFP western lot revels efficiency of immunoprecipittion, while GAPDH is negtive control. c. Locliztion of Jn-GFP construct (green, first row) or endogenous Jn (green, second row) to cili (rrows) stined for cetylted tuulin (red) in CGNs isolted from wild-type P5 cereell. Ciliry locliztion of endogenous β-ctenin (green, third row) nd colocliztion of β-ctenin-gfp construct (green, fourth row) with endogenous Jn (lue) t the cilium (cetylted tuulin, red). Hoechst (lue) lels nuclei in the first three rows.
10 Supplementl Figure 8 Ahi1 +/+ Ahi1 / Ac-Tuulin Hoechst Gli1 Ptc1 Merged Ahi1 +/ 100μm Ahi1 / 100μm c Ahi1 +/ Ahi1 / Arl13 Hoechst 20μm 20μm Supplementl Figure 8. Cili stining in Ahi1 mutnt cereellr neurons.. Cili stining (rrows, cetylted tuulin, red) in isolted CGNs from P5 littermtes. Hoechst lels nuclei (lue).. Shh trget gene stining in E14.5 trnsverse sections from Ahi1 / nd Ahi1 +/ littermtes. Gli1 (red) is not expressed t this stge. Ptc1 (green) is lso wekly expressed primrily in the future EGL s well s t the site of fusion. This expression ppers eqully low in the Ahi1 mutnt. Hoechst (lue) lels nuclei. c. Arl13 stining (red) to visulize cili (rrows) on trnsverse sections of Ahi1 / nd littermte control cereell t E13.5. Hoechst (lue) lels nuclei.
11 Supplementl Figure 9 Control Ahi1 / β-glctosidse Hoechst NCl LiCl c Control Ahi1-/- Untreted LiCl Untreted Lithium Control Ahi1 / Control Ahi1 / Ki67 Hoechst Supplementl Figure 9. Wnt ctivity stining in LiCl treted emryos.. β-glctosidse (green) stining of trnsverse sections from E14.5 BATgl+ emryos treted with NCl or LiCl revels incresed Wnt ctivity (rrows) with LiCl tretment in oth control nd Ahi1 / emryos compred with NCl treted emryos. Hoechst (lue) lels nuclei.. Ki67 stining (red, rrows) in Ahi1 / nd Ahi1 +/ littermte controls treted with LiCl compred with untreted controls which ws quntified in Figure 4f. Hoechst lels nuclei. c. Cresyl-violet sgittl sections from P11 littermtes treted with LiCl t E12.5 nd E13.5 or untreted.
12 Supplementl Figure 10 Lterl view of emryo: Dorsl view of MHB: m c lrl IV c lrl V L A P Dorsl view: R D V D R A P Ventrl view: L V E13.5 Control Ahi1-/- D V D 1.E+11 E E+10 1.E+09 1.E+08 1.E+07 1.E+06 1.E+05 1.E+04 1.E+03 WT Ahi1 KO Shh mutnt E11.5 E12.5 E13.5 E14.5 E15.5 E16.5 E17.5 E18.5 E19.5 E20.5 P0 P1 P2 P3 P4 P5 Numer of cells (log scle) x(t) = 2 t/1 x(t) = 2 t/2 x(t) = 2 t/0.5 Stge 1: Wnt Stge 2: Shh Supplementl Figure 10. Fusion model nd mthemticl modeling of two stge prolifertion model.. Model of midline cereellr fusion nd its disruption in Ahi1 mutnt mice. The emryonic hed is shown from the side nd close up view of the mid-hindrin junction (MHB) is shown from the dorsl surfce reveling the midrin (m), cereellr hemispheres (c), lower rhomic lip (lrl) nd fourth ventricle (IV). A dorsl view of the isolted cereellum is shown with depiction of the plne of sectioning for trnsverse sections (shown in schemtic t the right) nd xes t the left: nterior (A), posterior (P), left (L), right (R), ventrl (V), dorsl (D). The ventrl view of the fusing cereellum revels the fusion events tht occur nd re visile on trnsverse sections. A progression from E13.5 to E14.5 is depicted to provide sense of the closure tht occurs.. Mthemticl modeling of the prolifertion defect in Ahi1 knock-out (KO) mice compred with wild-type nd hypotheticl Shh mutnt. Equtions re shown for ech segment. See supplementl text.
13 Supplementry Discussion Mthemticl modeling of the prolifertion defect Our findings suggest tht JS gene muttion leds to erly prolifertion defects in Wntdependent mnner while postntl prolifertion nd Shh signling is reltively preserved. Using the dt we hve otined from BrdU leling t vrious time points, we ttempted to mthemticlly model the prolifertion which occurs erly nd lte in cereellr development. The rte of prolifertion t the midline t E13.5 is quite similr to tht we oserved t E16.5 in control mice, nd this rte increses to pproximtely 2-fold higher y P5. We therefore propose mthemticl model of this prolifertion, which occurs in two stges, n erly Wntdependent stge nd lter Shh-dependent stge. For this model, the sic eqution for exponentil growth cn e written x(t) = t/τ where the quntity x depends upon time t, the constnt is the strting quntity nd the constnt is the growth fctor. τ is the time required for x to increse y fctor of. In our model of cereellr growth, x refers to the numer of cereellr cells t given time t in dys from E11.5 to P5. The constnt is 2 since cereellr prolifertion is process of douling, nd we cn set with n ritrry numer of 1000 t E11.5, since we re interested in reltive growth rther thn solute numer of cells. In the model for 2-stge growth, the second stge exhiits prolifertion rte tht is 2-fold higher thn the initil stge sed upon our BrdU mesurements. Therefore, we ssign τ the vlue of 1 for the initil stge from E12.5 to E16.5 wheres this vlue chnges to 0.5 during the second stge from E17.5 to P5. When plotted on logrithmic scle, cell growth during the initil stge exhiits smller slope compred with the second stge (Supplementl Fig. 10). Next we cn model the effect of reducing the prolifertion rte of only one stge s in the Ahi1 mutnt mice. Since we hve determined tht Ahi1 mutnts exhiit reduction in prolifertion of pproximtely one hlf during erly development, we ssign τ the vlue of 2 during the first stge while τ remins 0.5 during the second stge. This results in decresed
14 slope during stge 1 compred with wild-type wheres during stge 2 the slopes re equl. When compred to mutnt which would ffect stge 2 prolifertion, such s Shh mutnt, if we ssign the sme 2-fold reduction in prolifertion rte, reduction which hs een previously reported with Shh inhiition 1, ut insted for stge 2, then τ is 1 during the first stge nd remins 1 for the second stge s well. This results in reduction in slope only during the second stge wheres the slope is equl to wild-type during stge 1. The finl outcome of this model revels reltively mild effect of disruption of stge 1 compred with stge 2. This supports our findings which revel tht the phenotypic result of loss of Ahi1 is reltively mild compred with mutnts which ffect Shh-dependent lter prolifertion, such s Smo or cili mutnts 2. This mthemticl model cptures the effect seen in Ahi1 mutnts in which vermis growth ppers delyed ut never fully recovers. References 1. Wllce, V.A. Purkinje-cell-derived Sonic hedgehog regultes grnule neuron precursor cell prolifertion in the developing mouse cereellum. Curr Biol 9, (1999). 2. Spssky, N., et l. Primry cili re required for cereellr development nd Shhdependent expnsion of progenitor pool. Dev Biol 317, (2008).
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