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n4:pmcid: PMC0
bibo:doi: 10.1101%2Fgad.262816.115
n2:contains: _:vb42012392 _:vb42012365 _:vb42012358

Subject Item: _:vb42012358
rdf:type: n2:Section
dc:title: materials and methods
n2:contains: _:vb42012364 _:vb42012360 _:vb42012361 _:vb42012362 _:vb42012363 _:vb42012359

Subject Item: _:vb42012359
rdf:type: n4:Context
rdf:value: LATS1/2-, MST1/2-, or NF2-deficient HEK293A cells were created through the CRISPR/Cas9 system (Ran et al. >>2013<<). HEK293A cells were transfected with a Cas9 expression plasmid together with single-guide RNA (sgRNA) expression plasmids (PX459; Addgene plasmid no.
n4:mentions: n3:24157548

Subject Item: _:vb42012360
rdf:type: n4:Context
rdf:value: org/crispr or were taken from archived guide sequences from the genome-scale CRISPR knockout (GeCKO2) library (Sanjana et al. >>2014<<). The guide sequences used were 5′-CGTGCAGCTCTCCGCTCTAA-3′ for human LATS1, 5′-TACGCTGGCACCGTAGCCCT-3′ for human LATS2, 5′-ATACACCGAGATATCAAGGC-3′ for human MST1, 5′-AGTACTCCATAACAATCCAG-3′ for human MST2, and 5′-GTCCATGGTGACGATCCTCA-3′
n4:mentions: n3:25075903

Subject Item: _:vb42012361
rdf:type: n4:Context
rdf:value: SV40 large T-immortalized Lats1–/–Lats2F/F MEFs were described previously (Murakami et al. >>2011<<). For Lats2 deletion, MEFs were infected with an adenovirus encoding Cre recombinase (no.
n4:mentions: n3:21245096

Subject Item: _:vb42012362
rdf:type: n4:Context
rdf:value: To achieve liver-specific or intestine-specific gene deletion, YapF/F mice were bred to Albumin-Cre (Zhang et al. >>2010<<) or Villin-Cre (Taniguchi et al. 2015) Tg mice, respectively.
n4:mentions: n3:20643348

Subject Item: _:vb42012363
rdf:type: n4:Context
rdf:value: To achieve liver-specific or intestine-specific gene deletion, YapF/F mice were bred to Albumin-Cre (Zhang et al. 2010) or Villin-Cre (Taniguchi et al. >>2015<<) Tg mice, respectively. For liver-specific YAP Tg mice, 2-mo-old YAP Tg and non-Tg littermates were fed 0.2 mg/mL doxycycline (Sigma) in drinking water supplemented with 2.5% sucrose, as described previously (Dong et al. 2007).
n4:mentions: n3:25731159

Subject Item: _:vb42012364
rdf:type: n4:Context
rdf:value: For liver-specific YAP Tg mice, 2-mo-old YAP Tg and non-Tg littermates were fed 0.2 mg/mL doxycycline (Sigma) in drinking water supplemented with 2.5% sucrose, as described previously (Dong et al. >>2007<<). Two-month-old to 3-mo-old sex-matched mice were used for all experimental procedures.
n4:mentions: n3:17889654

Subject Item: _:vb42012365
rdf:type: n2:Section
dc:title: results
n2:contains: _:vb42012368 _:vb42012369 _:vb42012370 _:vb42012371 _:vb42012372 _:vb42012373 _:vb42012374 _:vb42012375 _:vb42012376 _:vb42012377 _:vb42012378 _:vb42012379 _:vb42012380 _:vb42012381 _:vb42012382 _:vb42012383 _:vb42012366 _:vb42012367 _:vb42012384 _:vb42012385 _:vb42012386 _:vb42012387 _:vb42012388 _:vb42012389 _:vb42012390 _:vb42012391

Subject Item: _:vb42012366
rdf:type: n4:Context
rdf:value: TEAD is the major YAP-associated transcription factor, and its binding to YAP requires the Ser94 residue in YAP (Zhao et al. >>2008<<). Mutating Ser94 abolished the ability of YAP(5SA) to suppress TAZ (Fig. 1D). Consistently, shRNA-mediated depletion of endogenous TEAD1/3/4 (Supplemental Fig. S1B) attenuated the effect of YAP(5SA) on TAZ (Fig. 1E), suggesting that the
n4:mentions: n3:18579750

Subject Item: _:vb42012367
rdf:type: n4:Context
rdf:value: a codependent regulatory relationship between Yorkie (the fly homolog of YAP/TAZ) and dMyc (encoded by the diminutive gene) in which Yorkie induces dMyc transcription, which in turn represses Yorkie expression (Neto-Silva et al. >>2010<<). However, the mRNA abundance of MYC was not increased, but rather decreased, in YAP(5SA)- or TAZ(4SA)-overexpressing MCF10A cells (Supplemental Fig.
n4:mentions: n3:20951343

Subject Item: _:vb42012368
rdf:type: n4:Context
rdf:value: As the protein stability of YAP/TAZ is regulated through phosphorylation by LATS1/2 kinases (Zhao et al. >>2010<<), we examined the phosphorylation status of endogenous YAP in TAZ(4SA)-overexpressing MCF10A cells.
n4:mentions: n3:20048001

Subject Item: _:vb42012369
rdf:type: n4:Context
rdf:value: of LATS1/2 individually, we immunoprecipitated endogenous LATS1 or LATS2 from MCF10A cells and examined the phosphorylation levels of their activation loop (AL) and HM, both of which correlate with LATS kinase activity (Hergovich >>2013<<). Immunoblot analysis revealed that activating phosphorylation of both LATS1 and LATS2 were markedly increased in cells overexpressing TAZ(4SA) (Fig.
n4:mentions: n3:23985307

Subject Item: _:vb42012370
rdf:type: n4:Context
rdf:value: Consistent with the observed LATS1 and LATS2 activation, phosphorylation of angiomotin (AMOT) at Ser175, a known direct substrate site for LATS1/2 kinases (Adler et al. >>2013<<; Chan et al. 2013; Dai et al. 2013; Hirate et al. 2013), was increased in TAZ(4SA)-overexpressing MCF10A cells (Fig.
n4:mentions: n3:24101513

Subject Item: _:vb42012371
rdf:type: n4:Context
rdf:value: Consistent with the observed LATS1 and LATS2 activation, phosphorylation of angiomotin (AMOT) at Ser175, a known direct substrate site for LATS1/2 kinases (Adler et al. 2013; Chan et al. >>2013<<; Dai et al. 2013; Hirate et al. 2013), was increased in TAZ(4SA)-overexpressing MCF10A cells (Fig.
n4:mentions: n3:24225952

Subject Item: _:vb42012372
rdf:type: n4:Context
rdf:value: Consistent with the observed LATS1 and LATS2 activation, phosphorylation of angiomotin (AMOT) at Ser175, a known direct substrate site for LATS1/2 kinases (Adler et al. 2013; Chan et al. 2013; Dai et al. >>2013<<; Hirate et al. 2013), was increased in TAZ(4SA)-overexpressing MCF10A cells (Fig.
n4:mentions: n3:24106267

Subject Item: _:vb42012373
rdf:type: n4:Context
rdf:value: Consistent with the observed LATS1 and LATS2 activation, phosphorylation of angiomotin (AMOT) at Ser175, a known direct substrate site for LATS1/2 kinases (Adler et al. 2013; Chan et al. 2013; Dai et al. 2013; Hirate et al. >>2013<<), was increased in TAZ(4SA)-overexpressing MCF10A cells (Fig. 2E). Moreover, the protein abundance of AMOT was also increased without a corresponding effect on the amount of AMOT mRNA (Supplemental Fig.
n4:mentions: n3:23791731

Subject Item: _:vb42012374
rdf:type: n4:Context
rdf:value: These results are consistent with the previous observation that LATS-dependent phosphorylation stabilizes AMOT (Adler et al. >>2013<<). We also determined endogenous YAP localization in TAZ(4SA)-expressing cells. As expected, TAZ(4SA) overexpression caused a dramatic alteration of YAP subcellular distribution in MCF10A cells (Fig. 2F). There was much more cytoplasmic
n4:mentions: n3:24101513

Subject Item: _:vb42012375
rdf:type: n4:Context
rdf:value: Both YAP and TAZ can be potently dephosphorylated and activated by serum (Yu et al. >>2012<<). As expected, serum stimulation induced YAP dephosphorylation as determined by immunoblotting using an antibody specific to YAP phosphorylated at Ser127 (a direct LATS1/2 phosphorylation site responsible for cytoplasmic localization of
n4:mentions: n3:22863277

Subject Item: _:vb42012376
rdf:type: n4:Context
rdf:value: CTGF (connective tissue growth factor), a known direct target gene of the YAP–TEAD complex (Zhao et al. >>2008<<), and GAPDH (glyceraldehyde 3-phosphate dehydrogenase) were used as a positive and negative control, respectively.
n4:mentions: n3:18579750

Subject Item: _:vb42012377
rdf:type: n4:Context
rdf:value: 3F; Barretina et al. >>2012<<). As expected, there is a strong positive correlation between the two YAP/TAZ target genes CYR61 (cysteine-rich angiogenic inducer 61) and CTGF but no correlation between GAPDH (a negative control) and either CYR61 or CTGF.
n4:mentions: n3:22460905

Subject Item: _:vb42012378
rdf:type: n4:Context
rdf:value: As we observed an increased phosphorylation of LATS1/2 at the HM, a site known to be phosphorylated by MST1/2 (Chan et al. >>2005<<), we investigated whether MST1/2 are responsible for this activation.
n4:mentions: n3:15688006

Subject Item: _:vb42012379
rdf:type: n4:Context
rdf:value: To test this possibility, we deleted MST1/2 in HEK293A cells using CRISPR/Cas9 genome-editing technology (Ran et al. >>2013<<). Consistent with a positive role for MST1/2 in YAP phosphorylation, MST1/2 deletion reduced the basal phosphorylation of YAP (Supplemental Fig. S4A). To avoid the influences from off-target effects, we obtained multiple clones and
n4:mentions: n3:24157548

Subject Item: _:vb42012380
rdf:type: n4:Context
rdf:value: Recently, the tumor suppressor NF2 (Merlin in D. melanogaster) was revealed to promote LATS1/2 kinase activation without activating the intrinsic kinase activity of MST1/2 (Yin et al. >>2013<<). Furthermore, Merlin is already an established transcriptional target of Yorkie, the fly homolog of YAP/TAZ (Hamaratoglu et al. 2006).
n4:mentions: n3:24012335

Subject Item: _:vb42012381
rdf:type: n4:Context
rdf:value: Furthermore, Merlin is already an established transcriptional target of Yorkie, the fly homolog of YAP/TAZ (Hamaratoglu et al. >>2006<<). Indeed, we found that mRNA and protein abundance of NF2 both were markedly increased by YAP(5SA) or TAZ(4SA) overexpression in MCF10A cells (Fig. 4C,D; Supplemental Fig. S4D). ChIP assay revealed that both endogenous YAP and TEAD1
n4:mentions: n3:16341207

Subject Item: _:vb42012382
rdf:type: n4:Context
rdf:value: We then investigated whether this feedback mechanism operates in vivo using YAP transgenic (Tg) mice (Dong et al. >>2007<<). Consistent with what we observed with the cell lines in vitro, a significant increase of Lats2 mRNA, but not Lats1 mRNA, was detected in the livers of YAP Tg mice (Fig.
n4:mentions: n3:17889654

Subject Item: _:vb42012383
rdf:type: n4:Context
rdf:value: Notably, the protein abundance of AMOT was also elevated in the YAP Tg liver, consistent with the previous observation that the phosphorylation stabilizes AMOT (Adler et al. >>2013<<). Collectively, these data support a model in which YAP/TAZ induce LATS activation to constitute a feedback mechanism in the Hippo pathway.
n4:mentions: n3:24101513

Subject Item: _:vb42012384
rdf:type: n4:Context
rdf:value: To further confirm the role of LATS1/2 in feedback regulation, we generated LATS1/2-deficient mouse embryonic fibroblasts (MEFs) by infecting Lats1–/–Lats2F/F MEFs (Kim et al. >>2013<<) with adenoviruses encoding Cre recombinase.
n4:mentions: n3:23644383

Subject Item: _:vb42012385
rdf:type: n4:Context
rdf:value: LPA acts through GPCR to induce YAP activation (Yu et al. >>2012<<). In control MCF10A cells, LPA treatment induced an acute YAP dephosphorylation, as determined by immunoblotting using the phospho-YAP antibody (Fig.
n4:mentions: n3:22863277

Subject Item: _:vb42012386
rdf:type: n4:Context
rdf:value: AMOT is a filamentous actin (F-actin)-binding protein. While YAP and TAZ are known to promote cell migration (Chan et al. >>2008<<; Haskins et al. 2014), recent studies revealed that the phosphorylation of AMOT by LATS1/2 inhibits AMOT binding to F-actin (Chan et al. 2013; Dai et al. 2013; Hirate et al. 2013), reduces actin stress fiber formation, and thereby
n4:mentions: n3:18413727

Subject Item: _:vb42012387
rdf:type: n4:Context
rdf:value: While YAP and TAZ are known to promote cell migration (Chan et al. 2008; Haskins et al. >>2014<<), recent studies revealed that the phosphorylation of AMOT by LATS1/2 inhibits AMOT binding to F-actin (Chan et al. 2013; Dai et al. 2013; Hirate et al. 2013), reduces actin stress fiber formation, and thereby inhibits migration (Dai et
n4:mentions: n3:25492965

Subject Item: _:vb42012388
rdf:type: n4:Context
rdf:value: While YAP and TAZ are known to promote cell migration (Chan et al. 2008; Haskins et al. 2014), recent studies revealed that the phosphorylation of AMOT by LATS1/2 inhibits AMOT binding to F-actin (Chan et al. >>2013<<; Dai et al. 2013; Hirate et al. 2013), reduces actin stress fiber formation, and thereby inhibits migration (Dai et al. 2013).
n4:mentions: n3:24225952

Subject Item: _:vb42012389
rdf:type: n4:Context
rdf:value: While YAP and TAZ are known to promote cell migration (Chan et al. 2008; Haskins et al. 2014), recent studies revealed that the phosphorylation of AMOT by LATS1/2 inhibits AMOT binding to F-actin (Chan et al. 2013; Dai et al. >>2013<<; Hirate et al. 2013), reduces actin stress fiber formation, and thereby inhibits migration (Dai et al. 2013).
n4:mentions: n3:24106267

Subject Item: _:vb42012390
rdf:type: n4:Context
rdf:value: TAZ are known to promote cell migration (Chan et al. 2008; Haskins et al. 2014), recent studies revealed that the phosphorylation of AMOT by LATS1/2 inhibits AMOT binding to F-actin (Chan et al. 2013; Dai et al. 2013; Hirate et al. >>2013<<), reduces actin stress fiber formation, and thereby inhibits migration (Dai et al. 2013).
n4:mentions: n3:23791731

Subject Item: _:vb42012391
rdf:type: n4:Context
rdf:value: studies revealed that the phosphorylation of AMOT by LATS1/2 inhibits AMOT binding to F-actin (Chan et al. 2013; Dai et al. 2013; Hirate et al. 2013), reduces actin stress fiber formation, and thereby inhibits migration (Dai et al. >>2013<<). We thus hypothesized that the LATS-mediated feedback mechanism limits cell migration induced by YAP activation.
n4:mentions: n3:24106267

Subject Item: _:vb42012392
rdf:type: n2:Section
dc:title: discussion
n2:contains: _:vb42012407 _:vb42012400 _:vb42012401 _:vb42012402 _:vb42012403 _:vb42012396 _:vb42012397 _:vb42012398 _:vb42012399 _:vb42012393 _:vb42012394 _:vb42012395 _:vb42012404 _:vb42012405 _:vb42012406

Subject Item: _:vb42012393
rdf:type: n4:Context
rdf:value: The negative feedback mechanism employed by the mammalian Hippo pathway appears to differ significantly from that in D. melanogaster, where Yorkie induces expression of expanded, merlin, four-jointed, or kibra (Cho et al. >>2006<<; Hamaratoglu et al. 2006; Genevet et al. 2010), but not warts (the fly homolog of LATS1/2), in dividing epithelial cells of the wing or eye disc (Jukam et al. 2013).
n4:mentions: n3:16980976

Subject Item: _:vb42012394
rdf:type: n4:Context
rdf:value: feedback mechanism employed by the mammalian Hippo pathway appears to differ significantly from that in D. melanogaster, where Yorkie induces expression of expanded, merlin, four-jointed, or kibra (Cho et al. 2006; Hamaratoglu et al. >>2006<<; Genevet et al. 2010), but not warts (the fly homolog of LATS1/2), in dividing epithelial cells of the wing or eye disc (Jukam et al. 2013).
n4:mentions: n3:16341207

Subject Item: _:vb42012395
rdf:type: n4:Context
rdf:value: by the mammalian Hippo pathway appears to differ significantly from that in D. melanogaster, where Yorkie induces expression of expanded, merlin, four-jointed, or kibra (Cho et al. 2006; Hamaratoglu et al. 2006; Genevet et al. >>2010<<), but not warts (the fly homolog of LATS1/2), in dividing epithelial cells of the wing or eye disc (Jukam et al. 2013).
n4:mentions: n3:20159599

Subject Item: _:vb42012396
rdf:type: n4:Context
rdf:value: expression of expanded, merlin, four-jointed, or kibra (Cho et al. 2006; Hamaratoglu et al. 2006; Genevet et al. 2010), but not warts (the fly homolog of LATS1/2), in dividing epithelial cells of the wing or eye disc (Jukam et al. >>2013<<). On the contrary, Yorkie indirectly suppresses Warts transcription to establish positive feedback regulation in combination with tissue-specific transcription factors in the context of Drosophila eye development (Jukam et al. 2013).
n4:mentions: n3:23989952

Subject Item: _:vb42012397
rdf:type: n4:Context
rdf:value: On the contrary, Yorkie indirectly suppresses Warts transcription to establish positive feedback regulation in combination with tissue-specific transcription factors in the context of Drosophila eye development (Jukam et al. >>2013<<). This is in a dramatic contrast to mammalian cells in which YAP/TAZ activate LATS. It is possible that the mechanism observed in D. melanogaster might be employed in some mammalian cell types. Although the evolutionary conservation of
n4:mentions: n3:23989952

Subject Item: _:vb42012398
rdf:type: n4:Context
rdf:value: This evolutionary divergence in pathway components adds an extra layer of complexity and contributes to the dynamic regulation of the mammalian Hippo pathway (Bossuyt et al. >>2014<<).
n4:mentions: n3:23563179

Subject Item: _:vb42012399
rdf:type: n4:Context
rdf:value: than other well-characterized negative feedback loops mediated by protein modifications, such as receptor phosphorylation by GPCR kinases (GRKs) followed by β-arrestin-mediated uncoupling of the GPCR from the G proteins (Pierce et al. >>2002<<) or feedback phosphorylation of upstream components of a signaling cascade (e.g., inhibitory phosphorylation of RAF by ERK in the MAPK signaling) (Dougherty et al. 2005).
n4:mentions: n3:12209124

Subject Item: _:vb42012400
rdf:type: n4:Context
rdf:value: uncoupling of the GPCR from the G proteins (Pierce et al. 2002) or feedback phosphorylation of upstream components of a signaling cascade (e.g., inhibitory phosphorylation of RAF by ERK in the MAPK signaling) (Dougherty et al. >>2005<<). Thus, the LATS-mediated feedback architecture provides enough time for YAP/TAZ to mediate their biological functions as transcriptional coactivators by taking advantage of the time delay of transcription and translation.
n4:mentions: n3:15664191

Subject Item: _:vb42012401
rdf:type: n4:Context
rdf:value: Notably, the increase of AMOT may also contribute to the negative feedback because AMOT can directly bind to and inhibit YAP/TAZ as well as indirectly activate LATS (Zhao et al. >>2011<<; Hirate et al. 2013).
n4:mentions: n3:21205866

Subject Item: _:vb42012402
rdf:type: n4:Context
rdf:value: Notably, the increase of AMOT may also contribute to the negative feedback because AMOT can directly bind to and inhibit YAP/TAZ as well as indirectly activate LATS (Zhao et al. 2011; Hirate et al. >>2013<<). One can predict with certainty that LATS must have many additional physiological substrates. Sequence analyses of the human proteome show that there are >1000 peptides with the LATS phosphorylation consensus motif (HXRXXS). Therefore,
n4:mentions: n3:23791731

Subject Item: _:vb42012403
rdf:type: n4:Context
rdf:value: Given the observed frequent YAP/TAZ activation in human cancers, the general lack of cancer-relevant somatic or germline mutations in core members of the Hippo pathway is a major conundrum to the field (Harvey et al. >>2013<<; Moroishi et al. 2015; Plouffe et al. 2015). One possibility is that negative feedback control of YAP/TAZ activity suppresses tumorigenesis following small perturbation of the pathway.
n4:mentions: n3:23467301

Subject Item: _:vb42012404
rdf:type: n4:Context
rdf:value: the observed frequent YAP/TAZ activation in human cancers, the general lack of cancer-relevant somatic or germline mutations in core members of the Hippo pathway is a major conundrum to the field (Harvey et al. 2013; Moroishi et al. >>2015<<; Plouffe et al. 2015). One possibility is that negative feedback control of YAP/TAZ activity suppresses tumorigenesis following small perturbation of the pathway.
n4:mentions: n3:25592648

Subject Item: _:vb42012405
rdf:type: n4:Context
rdf:value: YAP/TAZ activation in human cancers, the general lack of cancer-relevant somatic or germline mutations in core members of the Hippo pathway is a major conundrum to the field (Harvey et al. 2013; Moroishi et al. 2015; Plouffe et al. >>2015<<). One possibility is that negative feedback control of YAP/TAZ activity suppresses tumorigenesis following small perturbation of the pathway.
n4:mentions: n3:25702974

Subject Item: _:vb42012406
rdf:type: n4:Context
rdf:value: In support of this idea, genetic mutations inhibiting the functions of key negative feedback regulators are found in human cancer: NF2 is mutated with high frequency in neurofibromatosis (Asthagiri et al. >>2009<<), and loss of NF2 as well as LATS2 is also frequently observed in malignant mesothelioma (Murakami et al. 2011), indicative of their functions as bona fide tumor suppressor genes.
n4:mentions: n3:19476995

Subject Item: _:vb42012407
rdf:type: n4:Context
rdf:value: feedback regulators are found in human cancer: NF2 is mutated with high frequency in neurofibromatosis (Asthagiri et al. 2009), and loss of NF2 as well as LATS2 is also frequently observed in malignant mesothelioma (Murakami et al. >>2011<<), indicative of their functions as bona fide tumor suppressor genes.
n4:mentions: n3:21245096

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