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n3:pmcid: PMC0
bibo:doi: 10.1084%2Fjem.20110447
n10:contains: _:vb13364234 _:vb13364241 _:vb13364259

Subject Item: _:vb13364234
rdf:type: n10:Section
dc:title: materials and methods
n10:contains: _:vb13364236 _:vb13364237 _:vb13364238 _:vb13364239 _:vb13364235 _:vb13364240

Subject Item: _:vb13364235
rdf:type: n3:Context
rdf:value: Heterozygous Evi1 KO mice (Evi1+/− mice) were previously described (Goyama et al., >>2008<<). C57BL/6-Ly5.1 mice were crossed with Ly5.2 mice to obtain Ly5.1/Ly5.2 mice. Littermates were used as controls in all experiments. All animal experiments were approved by the University of Tokyo Ethics Committee for Animal Experiments
n3:mentions: n2:18682242

Subject Item: _:vb13364236
rdf:type: n3:Context
rdf:value: Evi1+/− mice were genotyped by PCR as previously described (Goyama et al., >>2008<<). Evi1+/GFP mice were genotyped using a multiplex PCR to detect both WT and Evi1-IRES-GFP alleles.
n3:mentions: n2:18682242

Subject Item: _:vb13364237
rdf:type: n3:Context
rdf:value: When CD48+ CD150− LSK cells were transplanted, nonblocking anti-CD48 antibody (MRC OX78 clone) was used (Grassinger et al., >>2010<<).
n3:mentions: n2:20631378

Subject Item: _:vb13364238
rdf:type: n3:Context
rdf:value: Western blotting was performed as previously described (Goyama et al., >>2008<<). In brief, mouse embryo fibroblast cells were lysed in TNE buffer, subjected to 7% SDS-PAGE, and transferred to a PVDF membrane (Millipore).
n3:mentions: n2:18682242

Subject Item: _:vb13364239
rdf:type: n3:Context
rdf:value: ECs were defined as CD31+ TER-119− CD45−, OBs were defined as CD31− TER-119− CD45− Sca-1− ALCAM+ cells (Nakamura et al., >>2010<<), and MSCs were defined as CD31− TER-119− CD45− Sca-1+ PDGFRα+ cells (Morikawa et al., 2009).
n3:mentions: n2:20472830

Subject Item: _:vb13364240
rdf:type: n3:Context
rdf:value: ECs were defined as CD31+ TER-119− CD45−, OBs were defined as CD31− TER-119− CD45− Sca-1− ALCAM+ cells (Nakamura et al., 2010), and MSCs were defined as CD31− TER-119− CD45− Sca-1+ PDGFRα+ cells (Morikawa et al., >>2009<<).
n3:mentions: n2:19841085

Subject Item: _:vb13364241
rdf:type: n10:Section
dc:title: results
n10:contains: _:vb13364256 _:vb13364257 _:vb13364258 _:vb13364242 _:vb13364243 _:vb13364244 _:vb13364245 _:vb13364246 _:vb13364247 _:vb13364248 _:vb13364249 _:vb13364250 _:vb13364251 _:vb13364252 _:vb13364253 _:vb13364254 _:vb13364255

Subject Item: _:vb13364242
rdf:type: n3:Context
rdf:value: Evi1 mRNA has been shown to be expressed at significantly higher levels in HSPCs (Lin− Sca-1+ c-kit+ [LSK]) and common lymphoid progenitors (CLPs) than in other hematopoietic cells (Yuasa et al., >>2005<<; Chen et al., 2008). To gain insight into the biological function of Evi1 through its cell type–specific expression pattern, the distribution of GFP+ cells was examined in adult BM from Evi1+/GFP mice.
n3:mentions: n2:15889140

Subject Item: _:vb13364243
rdf:type: n3:Context
rdf:value: Evi1 mRNA has been shown to be expressed at significantly higher levels in HSPCs (Lin− Sca-1+ c-kit+ [LSK]) and common lymphoid progenitors (CLPs) than in other hematopoietic cells (Yuasa et al., 2005; Chen et al., >>2008<<). To gain insight into the biological function of Evi1 through its cell type–specific expression pattern, the distribution of GFP+ cells was examined in adult BM from Evi1+/GFP mice.
n3:mentions: n2:18455126

Subject Item: _:vb13364244
rdf:type: n3:Context
rdf:value: In contrast to the previous study (Chen et al., >>2008<<), GFP was not expressed in CLPs (Fig.
n3:mentions: n2:18455126

Subject Item: _:vb13364245
rdf:type: n3:Context
rdf:value: When LSK cells were subdivided according to CD34 and Flk-2 expression (Orford and Scadden, >>2008<<), the Flk-2− CD34− LSK fraction, which is considered to contain most LT-HSC activity, had the highest expression of GFP, and its expression decreased with differentiation to hematopoietic progenitors (Fig.
n3:mentions: n2:18202695

Subject Item: _:vb13364246
rdf:type: n3:Context
rdf:value: In addition, further enrichment for LT-HSCs within the LSK fraction using SLAM family receptors (CD48 and CD150; Kiel et al., >>2005<<) revealed that GFP+ cells were found in greatest abundance within CD48− CD150+ LSK cells, in which LT-HSCs are highly enriched.
n3:mentions: n2:15989959

Subject Item: _:vb13364247
rdf:type: n3:Context
rdf:value: Although it is controversial whether CD48+ CD150− LSK cells are transiently reconstituting MPPs/ST-HSCs or lymphoid-biased LT-HSCs with limited long-term engraftment and strong predominance of lymphoid reconstitution (Kiel et al., >>2005<<; Weksberg et al., 2008; Grassinger et al., 2010), Evi1-expressing cells possess higher repopulating capacity within this fraction.
n3:mentions: n2:15989959

Subject Item: _:vb13364248
rdf:type: n3:Context
rdf:value: whether CD48+ CD150− LSK cells are transiently reconstituting MPPs/ST-HSCs or lymphoid-biased LT-HSCs with limited long-term engraftment and strong predominance of lymphoid reconstitution (Kiel et al., 2005; Weksberg et al., >>2008<<; Grassinger et al., 2010), Evi1-expressing cells possess higher repopulating capacity within this fraction.
n3:mentions: n2:18055867

Subject Item: _:vb13364249
rdf:type: n3:Context
rdf:value: LSK cells are transiently reconstituting MPPs/ST-HSCs or lymphoid-biased LT-HSCs with limited long-term engraftment and strong predominance of lymphoid reconstitution (Kiel et al., 2005; Weksberg et al., 2008; Grassinger et al., >>2010<<), Evi1-expressing cells possess higher repopulating capacity within this fraction.
n3:mentions: n2:20631378

Subject Item: _:vb13364250
rdf:type: n3:Context
rdf:value: There are several major phenotypic and functional differences between fetal and adult HSCs in surface marker profile, cell cycle status, self-renewal potential, gene expression profile, and regulatory mechanism (Mikkola and Orkin, >>2006<<; Orkin and Zon, 2008).
n3:mentions: n2:16968814

Subject Item: _:vb13364251
rdf:type: n3:Context
rdf:value: major phenotypic and functional differences between fetal and adult HSCs in surface marker profile, cell cycle status, self-renewal potential, gene expression profile, and regulatory mechanism (Mikkola and Orkin, 2006; Orkin and Zon, >>2008<<). Fetal HSCs, in particular, divide rapidly and undergo massive expansion, whereas adult HSCs are mostly quiescent (Bowie et al., 2006).
n3:mentions: n2:18295580

Subject Item: _:vb13364252
rdf:type: n3:Context
rdf:value: Fetal HSCs, in particular, divide rapidly and undergo massive expansion, whereas adult HSCs are mostly quiescent (Bowie et al., >>2006<<). It is known that Evi1 is highly expressed in the yolk sac, paraaortic splanchnopleura, and HSPCs (CD45+ CD34+ c-kit+) in early embryo (Yuasa et al., 2005). Therefore, we sought to determine whether Evi1 expression can mark fetal HSCs
n3:mentions: n2:17016561

Subject Item: _:vb13364253
rdf:type: n3:Context
rdf:value: It is known that Evi1 is highly expressed in the yolk sac, paraaortic splanchnopleura, and HSPCs (CD45+ CD34+ c-kit+) in early embryo (Yuasa et al., >>2005<<). Therefore, we sought to determine whether Evi1 expression can mark fetal HSCs despite their distinct features from adult HSCs, and thus analyzed the expression pattern of GFP in Evi1+/GFP embryos. As expected, GFP expression was highly
n3:mentions: n2:15889140

Subject Item: _:vb13364254
rdf:type: n3:Context
rdf:value: 5, A-C; Takakura et al., >>2000<<; Kim et al., 2006; McKinney-Freeman et al., 2009).
n3:mentions: n2:10943840

Subject Item: _:vb13364255
rdf:type: n3:Context
rdf:value: 5, A-C; Takakura et al., 2000; Kim et al., >>2006<<; McKinney-Freeman et al., 2009).
n3:mentions: n2:16569764

Subject Item: _:vb13364256
rdf:type: n3:Context
rdf:value: 5, A-C; Takakura et al., 2000; Kim et al., 2006; McKinney-Freeman et al., >>2009<<). When the distribution of GFP+ cells in the fetal hematopoietic system was analyzed, most GFP+ cells exhibited the HSPC-specific marker profile in all embryonic tissues examined (Fig. 5, D–F), indicating the predominant expression of
n3:mentions: n2:19420357

Subject Item: _:vb13364257
rdf:type: n3:Context
rdf:value: We previously showed that heterozygosity of Evi1 leads to decreased numbers of LSK and CD34− LSK cells, as well as impaired long-term repopulating activity (Goyama et al., >>2008<<). In the current study, although Flk-2+ CD34+ and Flk-2− CD34+ LSK cells were moderately decreased, Flk-2− CD34− LSK cells from Evi1+/− mice exhibited a marked reduction in frequency compared with WT controls (Fig. 6, A and C). Likewise,
n3:mentions: n2:18682242

Subject Item: _:vb13364258
rdf:type: n3:Context
rdf:value: Because both ME and Evi1 are inactivated in our Evi1 KO model (Goyama et al., >>2008<<), we attempted to genetically dissect the relative roles of ME and Evi1 in maintaining LT-HSCs.
n3:mentions: n2:18682242

Subject Item: _:vb13364259
rdf:type: n10:Section
dc:title: discussion
n10:contains: _:vb13364264 _:vb13364265 _:vb13364266 _:vb13364267 _:vb13364268 _:vb13364269 _:vb13364270 _:vb13364271 _:vb13364260 _:vb13364261 _:vb13364262 _:vb13364263 _:vb13364272 _:vb13364273 _:vb13364274 _:vb13364275

Subject Item: _:vb13364260
rdf:type: n3:Context
rdf:value: We show that mesenchymal stem cells (MSCs), one of the few tissue stem cell types that have been established to self-renew in vivo (Morikawa et al., >>2009<<), do not express Evi1.
n3:mentions: n2:19841085

Subject Item: _:vb13364261
rdf:type: n3:Context
rdf:value: atlas and prior studies examining the expression pattern of Evi1 in various tissues have reported Evi1 expression in the kidney, ovary, uterus, intestine, stomach, lung, trachea, and nasal cavity in the adult mouse (Morishita et al., >>1990<<; Perkins et al., 1991; Su et al., 2004). It will be interesting to determine, using Evi1-IRES-GFP knock-in mice, whether Evi1-expressing cells in these organs are enriched with tissue stem cells.
n3:mentions: n2:1699199

Subject Item: _:vb13364262
rdf:type: n3:Context
rdf:value: examining the expression pattern of Evi1 in various tissues have reported Evi1 expression in the kidney, ovary, uterus, intestine, stomach, lung, trachea, and nasal cavity in the adult mouse (Morishita et al., 1990; Perkins et al., >>1991<<; Su et al., 2004). It will be interesting to determine, using Evi1-IRES-GFP knock-in mice, whether Evi1-expressing cells in these organs are enriched with tissue stem cells.
n3:mentions: n2:1893871

Subject Item: _:vb13364263
rdf:type: n3:Context
rdf:value: expression pattern of Evi1 in various tissues have reported Evi1 expression in the kidney, ovary, uterus, intestine, stomach, lung, trachea, and nasal cavity in the adult mouse (Morishita et al., 1990; Perkins et al., 1991; Su et al., >>2004<<). It will be interesting to determine, using Evi1-IRES-GFP knock-in mice, whether Evi1-expressing cells in these organs are enriched with tissue stem cells.
n3:mentions: n2:15075390

Subject Item: _:vb13364264
rdf:type: n3:Context
rdf:value: In addition, a recent gene expression profile analysis showed that Evi1 binding sites are enriched in the upstream region of genes expressed selectively in LT-HSCs (Forsberg et al., >>2010<<). In fact, several molecules involved in the regulation of HSC self-renewal have been identified as downstream targets or interacting proteins of Evi1, including Gata2 (Sato et al., 2008; Yuasa et al., 2005), Pbx1 (Shimabe et al., 2009),
n3:mentions: n2:20098702

Subject Item: _:vb13364265
rdf:type: n3:Context
rdf:value: In fact, several molecules involved in the regulation of HSC self-renewal have been identified as downstream targets or interacting proteins of Evi1, including Gata2 (Sato et al., >>2008<<; Yuasa et al., 2005), Pbx1 (Shimabe et al., 2009), Runx1 (Senyuk et al., 2007), and TGF-β (Kurokawa et al., 1998).
n3:mentions: n2:18452556

Subject Item: _:vb13364266
rdf:type: n3:Context
rdf:value: In fact, several molecules involved in the regulation of HSC self-renewal have been identified as downstream targets or interacting proteins of Evi1, including Gata2 (Sato et al., 2008; Yuasa et al., >>2005<<), Pbx1 (Shimabe et al., 2009), Runx1 (Senyuk et al., 2007), and TGF-β (Kurokawa et al., 1998).
n3:mentions: n2:15889140

Subject Item: _:vb13364267
rdf:type: n3:Context
rdf:value: In fact, several molecules involved in the regulation of HSC self-renewal have been identified as downstream targets or interacting proteins of Evi1, including Gata2 (Sato et al., 2008; Yuasa et al., 2005), Pbx1 (Shimabe et al., >>2009<<), Runx1 (Senyuk et al., 2007), and TGF-β (Kurokawa et al., 1998). Together with these findings, our data strongly support a model in which Evi1 gene dosage is a critical determinant of HSC self-renewal potential.
n3:mentions: n2:19767769

Subject Item: _:vb13364268
rdf:type: n3:Context
rdf:value: involved in the regulation of HSC self-renewal have been identified as downstream targets or interacting proteins of Evi1, including Gata2 (Sato et al., 2008; Yuasa et al., 2005), Pbx1 (Shimabe et al., 2009), Runx1 (Senyuk et al., >>2007<<), and TGF-β (Kurokawa et al., 1998). Together with these findings, our data strongly support a model in which Evi1 gene dosage is a critical determinant of HSC self-renewal potential.
n3:mentions: n2:17575132

Subject Item: _:vb13364269
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rdf:value: self-renewal have been identified as downstream targets or interacting proteins of Evi1, including Gata2 (Sato et al., 2008; Yuasa et al., 2005), Pbx1 (Shimabe et al., 2009), Runx1 (Senyuk et al., 2007), and TGF-β (Kurokawa et al., >>1998<<). Together with these findings, our data strongly support a model in which Evi1 gene dosage is a critical determinant of HSC self-renewal potential.
n3:mentions: n2:9665135

Subject Item: _:vb13364270
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rdf:value: Inappropriate expression of EVI1 confers poor prognosis in patients with AML (Lugthart et al., >>2008<<; Gröschel et al., 2010), and therefore improvement of the therapeutic outcome of leukemia with high EVI1 expression is needed.
n3:mentions: n2:18272813

Subject Item: _:vb13364271
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rdf:value: Inappropriate expression of EVI1 confers poor prognosis in patients with AML (Lugthart et al., 2008; Gröschel et al., >>2010<<), and therefore improvement of the therapeutic outcome of leukemia with high EVI1 expression is needed.
n3:mentions: n2:20308656

Subject Item: _:vb13364272
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rdf:value: Our data fit with other studies showing that retroviral integration at the Evi1 locus can be associated with long-term in vivo clonal dominance, occasionally leading to leukemic transformation (Stein et al., >>2010<<). The genetic events underlying AML pathogenesis fall into two groups: (1) mutations that enhance proliferation and survival of hematopoietic progenitors, or (2) mutations that result in impaired differentiation or aberrant acquisition of
n3:mentions: n2:20098431

Subject Item: _:vb13364273
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rdf:value: two groups: (1) mutations that enhance proliferation and survival of hematopoietic progenitors, or (2) mutations that result in impaired differentiation or aberrant acquisition of self-renewal properties of HSPCs (Fröhling et al., >>2005<<). Our data indicate that Evi1 activation can function as the latter mutation and confer enhanced self-renewal capacity in myeloid neoplasms.
n3:mentions: n2:16155011

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rdf:value: These findings may explain the underlying mechanisms of the clinical observations that, irrespective of ME expression, aberrant EVI1 expression carries an adverse prognostic value in AML (Lugthart et al., >>2008<<, 2010). As it is becoming evident that leukemic stem cells share self-renewal machinery with normal HSCs, the elucidation of how Evi1 controls HSC self-renewal may provide biological insight into the pathogenesis of Evi1-related leukemia.
n3:mentions: n2:18272813

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rdf:value: These findings may explain the underlying mechanisms of the clinical observations that, irrespective of ME expression, aberrant EVI1 expression carries an adverse prognostic value in AML (Lugthart et al., 2008, >>2010<<). As it is becoming evident that leukemic stem cells share self-renewal machinery with normal HSCs, the elucidation of how Evi1 controls HSC self-renewal may provide biological insight into the pathogenesis of Evi1-related leukemia.
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