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n3:pmcid: PMC0
bibo:doi: 10.1371%2Fjournal.pbio.1001083
n5:contains: _:vb11523060 _:vb11523142 _:vb11523107 _:vb11523095

Subject Item: _:vb11523060
rdf:type: n5:Section
dc:title: introduction
n5:contains: _:vb11523092 _:vb11523093 _:vb11523094 _:vb11523088 _:vb11523089 _:vb11523090 _:vb11523091 _:vb11523076 _:vb11523077 _:vb11523078 _:vb11523079 _:vb11523072 _:vb11523073 _:vb11523074 _:vb11523075 _:vb11523084 _:vb11523085 _:vb11523086 _:vb11523087 _:vb11523080 _:vb11523081 _:vb11523082 _:vb11523083 _:vb11523061 _:vb11523062 _:vb11523063 _:vb11523068 _:vb11523069 _:vb11523070 _:vb11523071 _:vb11523064 _:vb11523065 _:vb11523066 _:vb11523067

Subject Item: _:vb11523061
rdf:type: n3:Context
rdf:value: The Hh family of secreted proteins plays pivotal roles during embryonic development and adult tissue homeostasis [>>1<<]–[3]. Aberrant Hh signaling contributes to numerous human disorders including congenital diseases and cancers [4],[5].
n3:mentions: n2:11731473

Subject Item: _:vb11523062
rdf:type: n3:Context
rdf:value: The Hh family of secreted proteins plays pivotal roles during embryonic development and adult tissue homeostasis [1]–[>>3<<]. Aberrant Hh signaling contributes to numerous human disorders including congenital diseases and cancers [4],[5].
n3:mentions: n2:18794343

Subject Item: _:vb11523063
rdf:type: n3:Context
rdf:value: Aberrant Hh signaling contributes to numerous human disorders including congenital diseases and cancers [>>4<<],[5]. In a number of developmental contexts, Hh functions as a morphogen that specifies distinct cell fates in a concentration-dependent manner [1],[2]. For example, in vertebrate neural tube patterning, Shh secreted by the notochord and
n3:mentions: n2:11001584

Subject Item: _:vb11523064
rdf:type: n3:Context
rdf:value: Aberrant Hh signaling contributes to numerous human disorders including congenital diseases and cancers [4],[>>5<<]. In a number of developmental contexts, Hh functions as a morphogen that specifies distinct cell fates in a concentration-dependent manner [1],[2]. For example, in vertebrate neural tube patterning, Shh secreted by the notochord and floor
n3:mentions: n2:11357142

Subject Item: _:vb11523065
rdf:type: n3:Context
rdf:value: In a number of developmental contexts, Hh functions as a morphogen that specifies distinct cell fates in a concentration-dependent manner [>>1<<],[2]. For example, in vertebrate neural tube patterning, Shh secreted by the notochord and floor pate forms a ventral to dorsal concentration gradient that specifies distinct pools of neural progenitor cells [6].
n3:mentions: n2:11731473

Subject Item: _:vb11523066
rdf:type: n3:Context
rdf:value: In a number of developmental contexts, Hh functions as a morphogen that specifies distinct cell fates in a concentration-dependent manner [1],[>>2<<]. For example, in vertebrate neural tube patterning, Shh secreted by the notochord and floor pate forms a ventral to dorsal concentration gradient that specifies distinct pools of neural progenitor cells [6].
n3:mentions: n2:19081070

Subject Item: _:vb11523067
rdf:type: n3:Context
rdf:value: For example, in vertebrate neural tube patterning, Shh secreted by the notochord and floor pate forms a ventral to dorsal concentration gradient that specifies distinct pools of neural progenitor cells [>>6<<].
n3:mentions: n2:18621990

Subject Item: _:vb11523068
rdf:type: n3:Context
rdf:value: Hh exerts its biological function through a signaling cascade that ultimately controls a balance between activator and repressor forms of the Gli family of transcription factors [>>2<<]. In the absence of Hh, Gli2 and Gli3 are processed into truncated repressor forms (GliR).
n3:mentions: n2:19081070

Subject Item: _:vb11523069
rdf:type: n3:Context
rdf:value: The reception system for the Hh signal consists of a twelve-transmembrane protein Patched (Ptc) as the Hh receptor and a seven-transmembrane protein Smoothened (Smo) as the obligatory Hh signal transducer [>>2<<],[3]. Ptc inhibits Smo substoichiometrically through a poorly defined mechanism in the absence of Hh [7]. Binding of Hh to Ptc and the Ihog/Cdo family of proteins alleviates Ptc inhibition of Smo [8]–[14], leading to Smo activation and
n3:mentions: n2:19081070

Subject Item: _:vb11523070
rdf:type: n3:Context
rdf:value: The reception system for the Hh signal consists of a twelve-transmembrane protein Patched (Ptc) as the Hh receptor and a seven-transmembrane protein Smoothened (Smo) as the obligatory Hh signal transducer [2],[>>3<<]. Ptc inhibits Smo substoichiometrically through a poorly defined mechanism in the absence of Hh [7]. Binding of Hh to Ptc and the Ihog/Cdo family of proteins alleviates Ptc inhibition of Smo [8]–[14], leading to Smo activation and signal
n3:mentions: n2:18794343

Subject Item: _:vb11523071
rdf:type: n3:Context
rdf:value: Ptc inhibits Smo substoichiometrically through a poorly defined mechanism in the absence of Hh [>>7<<]. Binding of Hh to Ptc and the Ihog/Cdo family of proteins alleviates Ptc inhibition of Smo [8]–[14], leading to Smo activation and signal transduction. How Smo is activated and how it transduces the Hh signal to regulate GliR and GliA are
n3:mentions: n2:12192414

Subject Item: _:vb11523072
rdf:type: n3:Context
rdf:value: Binding of Hh to Ptc and the Ihog/Cdo family of proteins alleviates Ptc inhibition of Smo [>>8<<]–[14], leading to Smo activation and signal transduction.
n3:mentions: n2:8906787

Subject Item: _:vb11523073
rdf:type: n3:Context
rdf:value: Binding of Hh to Ptc and the Ihog/Cdo family of proteins alleviates Ptc inhibition of Smo [8]–[>>14<<], leading to Smo activation and signal transduction.
n3:mentions: n2:16647303

Subject Item: _:vb11523074
rdf:type: n3:Context
rdf:value: In mammals, Hh signaling depends on the primary cilium, a microtubule-based membrane protrusion found in almost all mammalian cells [>>15<<]. Key components in the Hh pathway are found in cilia and exhibit dynamic patterns depending on the Hh signaling state.
n3:mentions: n2:20395968

Subject Item: _:vb11523075
rdf:type: n3:Context
rdf:value: For example, in the absence of Hh, Ptc localizes to cilia and prevents Smo from accumulating in the cilia; binding of Hh to Ptc triggers reciprocal trafficking of Ptc and Smo, with Ptc moving out of and Smo accumulating in the cilia [>>16<<],[17]. Ciliary accumulation of Smo correlates but is not sufficient for Hh pathway activation [16]–[19].
n3:mentions: n2:16136078

Subject Item: _:vb11523076
rdf:type: n3:Context
rdf:value: example, in the absence of Hh, Ptc localizes to cilia and prevents Smo from accumulating in the cilia; binding of Hh to Ptc triggers reciprocal trafficking of Ptc and Smo, with Ptc moving out of and Smo accumulating in the cilia [16],[>>17<<]. Ciliary accumulation of Smo correlates but is not sufficient for Hh pathway activation [16]–[19].
n3:mentions: n2:17641202

Subject Item: _:vb11523077
rdf:type: n3:Context
rdf:value: Ciliary accumulation of Smo correlates but is not sufficient for Hh pathway activation [>>16<<]–[19]. Additional mechanisms, including conformational change in Smo, are likely to be responsible for Smo activation [20]–[22]. Indeed, fluorescence resonance energy transfer (FRET) analysis indicates that both Drosophila and mammalian
n3:mentions: n2:16136078

Subject Item: _:vb11523078
rdf:type: n3:Context
rdf:value: Ciliary accumulation of Smo correlates but is not sufficient for Hh pathway activation [16]–[>>19<<]. Additional mechanisms, including conformational change in Smo, are likely to be responsible for Smo activation [20]–[22]. Indeed, fluorescence resonance energy transfer (FRET) analysis indicates that both Drosophila and mammalian Smo
n3:mentions: n2:19196978

Subject Item: _:vb11523079
rdf:type: n3:Context
rdf:value: Additional mechanisms, including conformational change in Smo, are likely to be responsible for Smo activation [>>20<<]–[22]. Indeed, fluorescence resonance energy transfer (FRET) analysis indicates that both Drosophila and mammalian Smo proteins exist as constitutive dimers/oligomers, but in the absence of Hh, Smo C-tails adopt a closed conformation that
n3:mentions: n2:10984056

Subject Item: _:vb11523080
rdf:type: n3:Context
rdf:value: Additional mechanisms, including conformational change in Smo, are likely to be responsible for Smo activation [20]–[>>22<<]. Indeed, fluorescence resonance energy transfer (FRET) analysis indicates that both Drosophila and mammalian Smo proteins exist as constitutive dimers/oligomers, but in the absence of Hh, Smo C-tails adopt a closed conformation that
n3:mentions: n2:17960137

Subject Item: _:vb11523081
rdf:type: n3:Context
rdf:value: Hh induces a conformational switch in Smo, leading to dimerization/oligomerization of the C-tails [>>22<<]. The mechanisms underlying mammalian Smo ciliary accumulation, conformational change, and activation are largely unknown.
n3:mentions: n2:17960137

Subject Item: _:vb11523082
rdf:type: n3:Context
rdf:value: In Drosophila, Hh and Ptc reciprocally control Smo cell surface accumulation and conformation through regulating Smo phosphorylation [>>22<<]–[25]. In response to Hh, Smo is phosphorylated by protein kinase A (PKA) and casein kinase 1 (CK1) at multiple sites in its C-tail, and these phosphorylation events activate Smo by promoting its cell surface accumulation and active
n3:mentions: n2:17960137

Subject Item: _:vb11523083
rdf:type: n3:Context
rdf:value: In Drosophila, Hh and Ptc reciprocally control Smo cell surface accumulation and conformation through regulating Smo phosphorylation [22]–[>>25<<]. In response to Hh, Smo is phosphorylated by protein kinase A (PKA) and casein kinase 1 (CK1) at multiple sites in its C-tail, and these phosphorylation events activate Smo by promoting its cell surface accumulation and active
n3:mentions: n2:15616566

Subject Item: _:vb11523084
rdf:type: n3:Context
rdf:value: to Hh, Smo is phosphorylated by protein kinase A (PKA) and casein kinase 1 (CK1) at multiple sites in its C-tail, and these phosphorylation events activate Smo by promoting its cell surface accumulation and active conformation [>>22<<],[25]–[27]. However, vertebrate Smo C-tails diverge significantly from that of Drosophila Smo and do not contain the PKA/CK1 phosphorylation clusters found in Drosophila Smo C-tail [22].
n3:mentions: n2:17960137

Subject Item: _:vb11523085
rdf:type: n3:Context
rdf:value: to Hh, Smo is phosphorylated by protein kinase A (PKA) and casein kinase 1 (CK1) at multiple sites in its C-tail, and these phosphorylation events activate Smo by promoting its cell surface accumulation and active conformation [22],[>>25<<]–[27]. However, vertebrate Smo C-tails diverge significantly from that of Drosophila Smo and do not contain the PKA/CK1 phosphorylation clusters found in Drosophila Smo C-tail [22].
n3:mentions: n2:15616566

Subject Item: _:vb11523086
rdf:type: n3:Context
rdf:value: Hh, Smo is phosphorylated by protein kinase A (PKA) and casein kinase 1 (CK1) at multiple sites in its C-tail, and these phosphorylation events activate Smo by promoting its cell surface accumulation and active conformation [22],[25]–[>>27<<]. However, vertebrate Smo C-tails diverge significantly from that of Drosophila Smo and do not contain the PKA/CK1 phosphorylation clusters found in Drosophila Smo C-tail [22].
n3:mentions: n2:15592457

Subject Item: _:vb11523087
rdf:type: n3:Context
rdf:value: However, vertebrate Smo C-tails diverge significantly from that of Drosophila Smo and do not contain the PKA/CK1 phosphorylation clusters found in Drosophila Smo C-tail [>>22<<]. In addition, a systematic mutagenesis study did not reveal any Ser/Thr residues as essential for mammalian Smo activation [28]. These and other observations led to a proposal that mammalian Smo and Drosophila Smo are regulated by
n3:mentions: n2:17960137

Subject Item: _:vb11523088
rdf:type: n3:Context
rdf:value: In addition, a systematic mutagenesis study did not reveal any Ser/Thr residues as essential for mammalian Smo activation [>>28<<]. These and other observations led to a proposal that mammalian Smo and Drosophila Smo are regulated by fundamentally distinct mechanisms [28],[29].
n3:mentions: n2:16459297

Subject Item: _:vb11523089
rdf:type: n3:Context
rdf:value: These and other observations led to a proposal that mammalian Smo and Drosophila Smo are regulated by fundamentally distinct mechanisms [>>28<<],[29].
n3:mentions: n2:16459297

Subject Item: _:vb11523090
rdf:type: n3:Context
rdf:value: These and other observations led to a proposal that mammalian Smo and Drosophila Smo are regulated by fundamentally distinct mechanisms [28],[>>29<<].
n3:mentions: n2:16339192

Subject Item: _:vb11523091
rdf:type: n3:Context
rdf:value: Several studies suggested that G protein coupled receptor kinase 2 (GRK2) positively regulates Shh signaling [>>30<<]–[32]. Metabolic labeling experiments revealed that GRK2 is required for the basal phosphorylation of an exogenously expressed Smo [30].
n3:mentions: n2:15618519

Subject Item: _:vb11523092
rdf:type: n3:Context
rdf:value: Several studies suggested that G protein coupled receptor kinase 2 (GRK2) positively regulates Shh signaling [30]–[>>32<<]. Metabolic labeling experiments revealed that GRK2 is required for the basal phosphorylation of an exogenously expressed Smo [30].
n3:mentions: n2:18815277

Subject Item: _:vb11523093
rdf:type: n3:Context
rdf:value: Metabolic labeling experiments revealed that GRK2 is required for the basal phosphorylation of an exogenously expressed Smo [>>30<<]. However, it is not clear whether GRK2 directly phosphorylates Smo and how GRK2 activates Shh signaling. In addition, direct evidence for Hh-induced mammalian Smo phosphorylation is lacking. A recent kinome siRNA screen identified CK1α as
n3:mentions: n2:15618519

Subject Item: _:vb11523094
rdf:type: n3:Context
rdf:value: A recent kinome siRNA screen identified CK1α as a positive regulator for Shh signaling, but its mechanism of action remains unknown [>>33<<].
n3:mentions: n2:18827223

Subject Item: _:vb11523095
rdf:type: n5:Section
dc:title: materials and methods
n5:contains: _:vb11523104 _:vb11523105 _:vb11523106 _:vb11523096 _:vb11523097 _:vb11523098 _:vb11523099 _:vb11523100 _:vb11523101 _:vb11523102 _:vb11523103

Subject Item: _:vb11523096
rdf:type: n3:Context
rdf:value: pGE-Smo-CFPC, pGE-Smo-YFPC, and pGE-Smo-CFPL2YFPC have been described previously [>>22<<]. SmoSA and SmoSD substitutions were generated by site-directed PCR mutagenesis.
n3:mentions: n2:17960137

Subject Item: _:vb11523097
rdf:type: n3:Context
rdf:value: and cloned into pCDNA3.1(+) vector, the dominant negative form of bovine GRK2 (bGRK2-K220R) was generated by site-directed PCR mutagenesis strategy, and the pCS2(+)-CK1α and pCS2(+)-DN-CK1α are gifts from John Graff's Lab [>>49<<]. LMP/shRNA against kinase: CK1α, GRK2, or GRK5 were constructed by inserting indicated shRNA fragments into LMP vector (Open Biosystems) containing a PGK-puromycin resistance-IRES-GFP cassette.
n3:mentions: n2:11437445

Subject Item: _:vb11523098
rdf:type: n3:Context
rdf:value: To generate HA-tagged wild type, SA0–5 or SD0–5 versions of Smo C-tail, wild type, or mutant DNA fragments were amplified by PCR and inserted between NotI and XbaI sites in the HA-pUAST vectors [>>50<<], and the HA-tagged constructs were subcloned into pCDNA3.1(+) vector with EcoRI and XbaI sites.
n3:mentions: n2:18025723

Subject Item: _:vb11523099
rdf:type: n3:Context
rdf:value: All the constructs were sequence verified. DN-Kif3b constructs were kindly provided by Dr. Pao-Tien Chuang [>>44<<].
n3:mentions: n2:19684112

Subject Item: _:vb11523100
rdf:type: n3:Context
rdf:value: smo −/− and Kif3a −/− mouse embryonic fibroblasts were kindly provided by Dr. Pao-Tien Chuang [>>44<<]. Wild type MEFs were derived from wild type mice embryos at 9.5 dpc, embryos were dissected to pieces and transferred to 10 cm dishes for adherence, regular DMEM medium were slowly added, fibroblasts cells that migrated from the embryos
n3:mentions: n2:19684112

Subject Item: _:vb11523101
rdf:type: n3:Context
rdf:value: Reagents were used in the following concentrations unless otherwise noted: Recombinant Mouse Sonic Hedgehog N-terminus (ShhNp, R&D systems, Cat #464-SH), 293-Shh-conditioned medium (1∶6 v/v; [>>40<<]), SAG (200 nM), cyclopamine (1 µM), CKI-7 (10 µM; Sigma), and Heparin (1 µM; Sigma).
n3:mentions: n2:12414725

Subject Item: _:vb11523102
rdf:type: n3:Context
rdf:value: Immunoprecipitation experiments were performed as previously described [>>51<<]. The Phos tag-conjugated SDS-PAGE analysis was performed according to the standard protocols [34].
n3:mentions: n2:15691767

Subject Item: _:vb11523103
rdf:type: n3:Context
rdf:value: The Phos tag-conjugated SDS-PAGE analysis was performed according to the standard protocols [>>34<<]. Phos tag-conjugated acrylamide was purchased from the NARD Institute in Japan. First and secondary antibodies used in this study: mouse anti-Myc (1∶5,000; Sigma), rabbit anti-Myc (A-14; Santa Cruz Biotechnologies), mouse anti-HA
n3:mentions: n2:16340016

Subject Item: _:vb11523104
rdf:type: n3:Context
rdf:value: FRET assays were performed essentially as previously described [>>22<<]. Briefly, CFP was exited at 458 nM wavelength and YFP at 514 nM wavelength.
n3:mentions: n2:17960137

Subject Item: _:vb11523105
rdf:type: n3:Context
rdf:value: All constructs were electroporated into the neural tube of HH st11–12 chick embryos [>>52<<]. Embryos were harvested 48 h after electroporation, fixed, and processed for immunohistochemistry as previously described [53].
n3:mentions: n2:1304821

Subject Item: _:vb11523106
rdf:type: n3:Context
rdf:value: Embryos were harvested 48 h after electroporation, fixed, and processed for immunohistochemistry as previously described [>>53<<]. The following antibodies were used: mouse Pax7, Nkx6.1, Nkx2.2 (from DSHB), rabbit Olig2 (Chemicon), rabbit Islet1/2 (a gift from Dr. T. Jessell), and GFP (Biogenesis). Anterior thoracic levels were analyzed in all cases.
n3:mentions: n2:11044400

Subject Item: _:vb11523107
rdf:type: n5:Section
dc:title: results
n5:contains: _:vb11523136 _:vb11523137 _:vb11523138 _:vb11523139 _:vb11523140 _:vb11523141 _:vb11523112 _:vb11523113 _:vb11523114 _:vb11523115 _:vb11523116 _:vb11523117 _:vb11523118 _:vb11523119 _:vb11523108 _:vb11523109 _:vb11523110 _:vb11523111 _:vb11523128 _:vb11523129 _:vb11523130 _:vb11523131 _:vb11523132 _:vb11523133 _:vb11523134 _:vb11523135 _:vb11523120 _:vb11523121 _:vb11523122 _:vb11523123 _:vb11523124 _:vb11523125 _:vb11523126 _:vb11523127

Subject Item: _:vb11523108
rdf:type: n3:Context
rdf:value: A previous study revealed that CK1α siRNA blocked Shh pathway activation in C3H10T1/2 cells [>>33<<]. To determine how CK1α positively regulates Shh signaling, we tested whether CK1α activates Smo.
n3:mentions: n2:18827223

Subject Item: _:vb11523109
rdf:type: n3:Context
rdf:value: In line with a previous finding [>>31<<], coexpression of GRK2 with Smo also activated Gli-luc in NIH3T3 cells (Figure 1A).
n3:mentions: n2:16908539

Subject Item: _:vb11523110
rdf:type: n3:Context
rdf:value: Consistent with previous findings [>>31<<],[33], overexpression of CK1α, GRK2, or both only slightly increased the expression of Gli-luc reporter gene (Figure S1G).
n3:mentions: n2:16908539

Subject Item: _:vb11523111
rdf:type: n3:Context
rdf:value: Consistent with previous findings [31],[>>33<<], overexpression of CK1α, GRK2, or both only slightly increased the expression of Gli-luc reporter gene (Figure S1G).
n3:mentions: n2:18827223

Subject Item: _:vb11523112
rdf:type: n3:Context
rdf:value: Our previous FRET analysis indicated that Shh induces a conformational change in Smo from a closed to an open conformation [>>22<<]. In the closed conformation, Smo exists as a dimer/oligomer through an N-terminal interaction(s), which results in high basal FRET between CFP and YFP fused to the N-termini of two Smo molecules (FRETN); however, Smo C-tail folds back and
n3:mentions: n2:17960137

Subject Item: _:vb11523113
rdf:type: n3:Context
rdf:value: intramolecular FRET between CFP inserted in the second intracellular loop (L2) and YFP fused to the C-terminus (FRETL2C) and low intermolecular FRET between CFP and YFP fused to the C-termini of two Smo molecules (FRETC) (Figure 1B–D) [>>22<<]. Shh induced a marked decrease in FRETL2C and a concomitant increase in FRETC without affecting FRETN (Figure 1B–D) [22], suggesting that Smo C-tails move away from the intracellular loops and form dimers/oligomers.
n3:mentions: n2:17960137

Subject Item: _:vb11523114
rdf:type: n3:Context
rdf:value: Shh induced a marked decrease in FRETL2C and a concomitant increase in FRETC without affecting FRETN (Figure 1B–D) [>>22<<], suggesting that Smo C-tails move away from the intracellular loops and form dimers/oligomers.
n3:mentions: n2:17960137

Subject Item: _:vb11523115
rdf:type: n3:Context
rdf:value: Having established that CK1α and GRK2 act upstream of Smo, we then determined whether CK1α and GRK2 could promote Smo phosphorylation using a Phos-tag gel that specifically retards phosphorylated proteins [>>34<<]. We found that coexpression of CK1α, GRK2, or both with a Myc-tagged Smo (Smo-Myc) resulted in a clear mobility shift of Smo-Myc on Phos-tag PAGE that was abolished by phosphatase treatment (Figure 1E, lanes 5–10), suggesting that CK1α
n3:mentions: n2:16340016

Subject Item: _:vb11523116
rdf:type: n3:Context
rdf:value: Importantly, Shh-induced Smo-Myc mobility shift was greatly reduced by treating cells with a CK1 inhibitor CKI-7 [>>35<<] and/or a GRK inhibitor heparin [36] (Figure 1F), suggesting that Shh induces Smo phosphorylation through CK1 and GRK kinase activities.
n3:mentions: n2:2925675

Subject Item: _:vb11523117
rdf:type: n3:Context
rdf:value: Importantly, Shh-induced Smo-Myc mobility shift was greatly reduced by treating cells with a CK1 inhibitor CKI-7 [35] and/or a GRK inhibitor heparin [>>36<<] (Figure 1F), suggesting that Shh induces Smo phosphorylation through CK1 and GRK kinase activities.
n3:mentions: n2:2541428

Subject Item: _:vb11523118
rdf:type: n3:Context
rdf:value: In line with previous findings [>>31<<]–[33], CK1α or GRK2 shRNA inhibited Shh pathway activity in the Gli-luc reporter assay (Figure 1G, Figure S1C–D, H).
n3:mentions: n2:16908539

Subject Item: _:vb11523119
rdf:type: n3:Context
rdf:value: In line with previous findings [31]–[>>33<<], CK1α or GRK2 shRNA inhibited Shh pathway activity in the Gli-luc reporter assay (Figure 1G, Figure S1C–D, H).
n3:mentions: n2:18827223

Subject Item: _:vb11523120
rdf:type: n3:Context
rdf:value: GRK family kinases tend to phosphorylate S/T in an acidic environment [>>37<<]. aa 608–670 contains three sequences (EPS615ADVS619S620A, QDVS642VT, and EIS666PELE) and aa 770–793 contains one sequence (DADS791DF) that match GRK consensus sites (Figure 2C).
n3:mentions: n2:7781920

Subject Item: _:vb11523121
rdf:type: n3:Context
rdf:value: CK1 phosphorylation sites conform to the consensus: D/E/S/T(P)X1–3S/T [>>38<<]. Site-directed mutagenesis revealed that S615, S619, and S620 mediated CK1 phosphorylation of aa 608–670 (Figure 2A, lanes 8–12; Figure S2A and Figure S2B, lanes 3–9), whereas S774, S777, and S791 mediated CK1 phosphorylation of aa
n3:mentions: n2:15722192

Subject Item: _:vb11523122
rdf:type: n3:Context
rdf:value: Hh signaling strength depends on the level of Hh ligand [>>2<<]. To determine if the level of Shh pathway activity correlates with the level of Smo phosphorylation, NIH3T3 cells transfected with Smo-Myc were treated with different levels of Shh, followed by mobility shift assay on the phospho-tag gel
n3:mentions: n2:19081070

Subject Item: _:vb11523123
rdf:type: n3:Context
rdf:value: Several oncogenic mutations in human Smo have been identified, including M1 and M2 [>>39<<]. The M2 mutation occurs in the seventh transmembrane domain whose murine counterpart is the A1 mutation [20],[39].
n3:mentions: n2:9422511

Subject Item: _:vb11523124
rdf:type: n3:Context
rdf:value: The M2 mutation occurs in the seventh transmembrane domain whose murine counterpart is the A1 mutation [>>20<<],[39]. Previous studies suggest that SmoA1 exhibits constitutive activity, accumulates at primary cilia, and adopts an open conformation [16],[20],[22]. We found that SmoA1 exhibited slower mobility and elevated PS1 signal intensity
n3:mentions: n2:10984056

Subject Item: _:vb11523125
rdf:type: n3:Context
rdf:value: The M2 mutation occurs in the seventh transmembrane domain whose murine counterpart is the A1 mutation [20],[>>39<<]. Previous studies suggest that SmoA1 exhibits constitutive activity, accumulates at primary cilia, and adopts an open conformation [16],[20],[22]. We found that SmoA1 exhibited slower mobility and elevated PS1 signal intensity regardless
n3:mentions: n2:9422511

Subject Item: _:vb11523126
rdf:type: n3:Context
rdf:value: Previous studies suggest that SmoA1 exhibits constitutive activity, accumulates at primary cilia, and adopts an open conformation [>>16<<],[20],[22].
n3:mentions: n2:16136078

Subject Item: _:vb11523127
rdf:type: n3:Context
rdf:value: Previous studies suggest that SmoA1 exhibits constitutive activity, accumulates at primary cilia, and adopts an open conformation [16],[>>20<<],[22]. We found that SmoA1 exhibited slower mobility and elevated PS1 signal intensity regardless of Shh treatment (Figure 2H, lanes 4–5; Figure S2H) and that A1-induced PS1 signal and mobility shift were abolished by the S1–5 mutation
n3:mentions: n2:10984056

Subject Item: _:vb11523128
rdf:type: n3:Context
rdf:value: Previous studies suggest that SmoA1 exhibits constitutive activity, accumulates at primary cilia, and adopts an open conformation [16],[20],[>>22<<]. We found that SmoA1 exhibited slower mobility and elevated PS1 signal intensity regardless of Shh treatment (Figure 2H, lanes 4–5; Figure S2H) and that A1-induced PS1 signal and mobility shift were abolished by the S1–5 mutation
n3:mentions: n2:17960137

Subject Item: _:vb11523129
rdf:type: n3:Context
rdf:value: Previous studies demonstrated that small molecules including SAG and 20α-hydroxycholesterol (20-OHC) promote whereas cyclopamine blocks Smo activation [>>20<<],[21],[40],[41]. We found that SAG and 20-OHC induced whereas cyclopamine blocked Smo phosphorylation at CK1/GRK sites (Figure 2I), suggesting that these small molecules regulate Shh signaling at the level of Smo phosphorylation.
n3:mentions: n2:10984056

Subject Item: _:vb11523130
rdf:type: n3:Context
rdf:value: Previous studies demonstrated that small molecules including SAG and 20α-hydroxycholesterol (20-OHC) promote whereas cyclopamine blocks Smo activation [20],[>>21<<],[40],[41]. We found that SAG and 20-OHC induced whereas cyclopamine blocked Smo phosphorylation at CK1/GRK sites (Figure 2I), suggesting that these small molecules regulate Shh signaling at the level of Smo phosphorylation.
n3:mentions: n2:12391318

Subject Item: _:vb11523131
rdf:type: n3:Context
rdf:value: Previous studies demonstrated that small molecules including SAG and 20α-hydroxycholesterol (20-OHC) promote whereas cyclopamine blocks Smo activation [20],[21],[>>40<<],[41]. We found that SAG and 20-OHC induced whereas cyclopamine blocked Smo phosphorylation at CK1/GRK sites (Figure 2I), suggesting that these small molecules regulate Shh signaling at the level of Smo phosphorylation.
n3:mentions: n2:12414725

Subject Item: _:vb11523132
rdf:type: n3:Context
rdf:value: Previous studies demonstrated that small molecules including SAG and 20α-hydroxycholesterol (20-OHC) promote whereas cyclopamine blocks Smo activation [20],[21],[40],[>>41<<]. We found that SAG and 20-OHC induced whereas cyclopamine blocked Smo phosphorylation at CK1/GRK sites (Figure 2I), suggesting that these small molecules regulate Shh signaling at the level of Smo phosphorylation.
n3:mentions: n2:16707575

Subject Item: _:vb11523133
rdf:type: n3:Context
rdf:value: Furthermore, SD123 and SD0–5 but not SmoWT restored the expression of ventral markers suppressed by a dominant form of Ptc, Ptc1Δloop2 (PtcΔ2), as well as prevented the derepression of the dorsal marker Pax7 (Figure 3E) [>>42<<]. These results suggest that phosphorylation at CK1/GRK sites increased the basal activity of Smo in the chick neural tubes.
n3:mentions: n2:11430830

Subject Item: _:vb11523134
rdf:type: n3:Context
rdf:value: Shh induces ciliary accumulation of Smo that correlates with pathway activation, but the underlying mechanism is poorly understood [>>16<<],[17]. We determined whether Shh promotes Smo ciliary localization by inducing its phosphorylation at CK1/GRK sites by examining ciliary localization of CFP-tagged wild type or phosphorylation site mutant forms of Smo in MEF cells treated
n3:mentions: n2:16136078

Subject Item: _:vb11523135
rdf:type: n3:Context
rdf:value: Shh induces ciliary accumulation of Smo that correlates with pathway activation, but the underlying mechanism is poorly understood [16],[>>17<<]. We determined whether Shh promotes Smo ciliary localization by inducing its phosphorylation at CK1/GRK sites by examining ciliary localization of CFP-tagged wild type or phosphorylation site mutant forms of Smo in MEF cells treated with
n3:mentions: n2:17641202

Subject Item: _:vb11523136
rdf:type: n3:Context
rdf:value: A recent study suggested that β-arrestins mediate Smo ciliary localization by binding to Smo and facilitating its interaction with the kinesin-II motor [>>43<<]. We hypothesized that Shh-induced Smo phosphorylation promotes its ciliary localization by recruiting β-arrestins.
n3:mentions: n2:18497258

Subject Item: _:vb11523137
rdf:type: n3:Context
rdf:value: In line with a previous report [>>17<<], both Shh and SAG induced a rapid ciliary accumulation of Smo-CFP, and the percentage of Smo-CFP positive cilia as well as the mean intensity of SmoCFP signal increased over time (Figure 6B–D).
n3:mentions: n2:17641202

Subject Item: _:vb11523138
rdf:type: n3:Context
rdf:value: To investigate whether primary cilia regulate Smo phosphorylation, we disrupted the cilia using a dominant negative form of Kif3b (DN-Kif3b), a subunit of the kinesin-II motor required for cilia formation [>>44<<]. We found that DN-Kif3b diminished but did not completely block Shh-induced PS1 signal associated with either Smo-Myc or SmoA1-Myc (Figure 6F, lanes 3, 6), suggesting that efficient phosphorylation at S1 depends on the kinesin-II ciliary
n3:mentions: n2:19684112

Subject Item: _:vb11523139
rdf:type: n3:Context
rdf:value: examined how gain- or loss-of-function Smo mutations affect CK1α binding, including two oncogenic mutations (A1 and M1) and three loss-of-function mutations in or near the CK1α binding pocket identified by previous studies (Figure 7A) [>>28<<],[39]. We found that both A1 and M1 resulted in a constitutive CK1α/GRK2 binding and Smo phosphorylation with A1 being more potent than M1 (Figure 7H, lanes 3 and 5; Figure S5).
n3:mentions: n2:16459297

Subject Item: _:vb11523140
rdf:type: n3:Context
rdf:value: how gain- or loss-of-function Smo mutations affect CK1α binding, including two oncogenic mutations (A1 and M1) and three loss-of-function mutations in or near the CK1α binding pocket identified by previous studies (Figure 7A) [28],[>>39<<]. We found that both A1 and M1 resulted in a constitutive CK1α/GRK2 binding and Smo phosphorylation with A1 being more potent than M1 (Figure 7H, lanes 3 and 5; Figure S5).
n3:mentions: n2:9422511

Subject Item: _:vb11523141
rdf:type: n3:Context
rdf:value: Another loss-of-function mutation, I573A, which mainly affected Smo stability [>>28<<], slightly reduced Shh-stimulated CK1α binding and Smo phosphorylation (Figure 7H, lanes 11–12; Figure S5).
n3:mentions: n2:16459297

Subject Item: _:vb11523142
rdf:type: n5:Section
dc:title: discussion
n5:contains: _:vb11523156 _:vb11523157 _:vb11523158 _:vb11523152 _:vb11523153 _:vb11523154 _:vb11523155 _:vb11523148 _:vb11523149 _:vb11523150 _:vb11523151 _:vb11523144 _:vb11523145 _:vb11523146 _:vb11523147 _:vb11523143

Subject Item: _:vb11523143
rdf:type: n3:Context
rdf:value: It has been well established that Drosophila Smo is hyperphosphorylated by multiple kinases in response to Hh stimulation [>>22<<],[23],[25]–[27]; however, sequence divergence between Drosophila and vertebrate Smo proteins makes it unclear whether vertebrate Smo proteins are similarly phosphorylated in response to Hh.
n3:mentions: n2:17960137

Subject Item: _:vb11523144
rdf:type: n3:Context
rdf:value: It has been well established that Drosophila Smo is hyperphosphorylated by multiple kinases in response to Hh stimulation [22],[>>23<<],[25]–[27]; however, sequence divergence between Drosophila and vertebrate Smo proteins makes it unclear whether vertebrate Smo proteins are similarly phosphorylated in response to Hh.
n3:mentions: n2:10966113

Subject Item: _:vb11523145
rdf:type: n3:Context
rdf:value: It has been well established that Drosophila Smo is hyperphosphorylated by multiple kinases in response to Hh stimulation [22],[23],[>>25<<]–[27]; however, sequence divergence between Drosophila and vertebrate Smo proteins makes it unclear whether vertebrate Smo proteins are similarly phosphorylated in response to Hh.
n3:mentions: n2:15616566

Subject Item: _:vb11523146
rdf:type: n3:Context
rdf:value: It has been well established that Drosophila Smo is hyperphosphorylated by multiple kinases in response to Hh stimulation [22],[23],[25]–[>>27<<]; however, sequence divergence between Drosophila and vertebrate Smo proteins makes it unclear whether vertebrate Smo proteins are similarly phosphorylated in response to Hh.
n3:mentions: n2:15592457

Subject Item: _:vb11523147
rdf:type: n3:Context
rdf:value: A prevalent view regarding Smo activation is that Hh activates Smo by inducing its ciliary localization [>>16<<],[17]. However, this view has been challenged by more recent studies showing that the Smo inhibitor cyclopamine promotes instead of blocks ciliary localization of Smo [18],[19],[45], suggesting that ciliary localization of Smo is
n3:mentions: n2:16136078

Subject Item: _:vb11523148
rdf:type: n3:Context
rdf:value: A prevalent view regarding Smo activation is that Hh activates Smo by inducing its ciliary localization [16],[>>17<<]. However, this view has been challenged by more recent studies showing that the Smo inhibitor cyclopamine promotes instead of blocks ciliary localization of Smo [18],[19],[45], suggesting that ciliary localization of Smo is insufficient
n3:mentions: n2:17641202

Subject Item: _:vb11523149
rdf:type: n3:Context
rdf:value: However, this view has been challenged by more recent studies showing that the Smo inhibitor cyclopamine promotes instead of blocks ciliary localization of Smo [>>18<<],[19],[45], suggesting that ciliary localization of Smo is insufficient for its activation.
n3:mentions: n2:19218434

Subject Item: _:vb11523150
rdf:type: n3:Context
rdf:value: However, this view has been challenged by more recent studies showing that the Smo inhibitor cyclopamine promotes instead of blocks ciliary localization of Smo [18],[>>19<<],[45], suggesting that ciliary localization of Smo is insufficient for its activation.
n3:mentions: n2:19196978

Subject Item: _:vb11523151
rdf:type: n3:Context
rdf:value: However, this view has been challenged by more recent studies showing that the Smo inhibitor cyclopamine promotes instead of blocks ciliary localization of Smo [18],[19],[>>45<<], suggesting that ciliary localization of Smo is insufficient for its activation.
n3:mentions: n2:19365551

Subject Item: _:vb11523152
rdf:type: n3:Context
rdf:value: Our previous and current studies demonstrate that Shh induces a conformational switch in Smo that is also induced by the A1 mutation and SAG but is blocked by Smo inhibitors including cyclopamine [>>22<<],[46],[47], suggesting that Hh-induced Smo conformational switch may represent an additional step for Smo activation.
n3:mentions: n2:17960137

Subject Item: _:vb11523153
rdf:type: n3:Context
rdf:value: Our previous and current studies demonstrate that Shh induces a conformational switch in Smo that is also induced by the A1 mutation and SAG but is blocked by Smo inhibitors including cyclopamine [22],[>>46<<],[47], suggesting that Hh-induced Smo conformational switch may represent an additional step for Smo activation.
n3:mentions: n2:19366682

Subject Item: _:vb11523154
rdf:type: n3:Context
rdf:value: Our previous and current studies demonstrate that Shh induces a conformational switch in Smo that is also induced by the A1 mutation and SAG but is blocked by Smo inhibitors including cyclopamine [22],[46],[>>47<<], suggesting that Hh-induced Smo conformational switch may represent an additional step for Smo activation.
n3:mentions: n2:19666565

Subject Item: _:vb11523155
rdf:type: n3:Context
rdf:value: A recent study demonstrated that β-arrestins mediate the interaction between Smo and the anterior-grade trafficking motor kinesin-II [>>43<<]. Thus, Hh-induced phosphorylation may promote Smo ciliary accumulation by facilitating its anterior grade trafficking through recruiting β-arr2. It is also possible that phosphorylation may impede the retrograde trafficking of Smo or may
n3:mentions: n2:18497258

Subject Item: _:vb11523156
rdf:type: n3:Context
rdf:value: Hh-stimulated phosphorylation induces dSmo conformation change by antagonizing multiple Arg clusters in its C-tail [>>22<<]. As the inactive conformation of mSmo is also maintained by a long stretch of basic cluster in its C-tail [22], multisite phosphorylation may promote mSmo conformational change through a similar mechanism. A recent study has demonstrated
n3:mentions: n2:17960137

Subject Item: _:vb11523157
rdf:type: n3:Context
rdf:value: As the inactive conformation of mSmo is also maintained by a long stretch of basic cluster in its C-tail [>>22<<], multisite phosphorylation may promote mSmo conformational change through a similar mechanism.
n3:mentions: n2:17960137

Subject Item: _:vb11523158
rdf:type: n3:Context
rdf:value: A recent study has demonstrated that GRK2 regulates dSmo by both kinase-dependent and kinase-independent mechanisms [>>48<<]. The observation that Shh induces mSmo/GRK2 complex formation raises an interesting possibility that GRK2 may also function as a molecular scaffold to promote mSmo activation.
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