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10.1371%2Fjournal.pbio.1000441
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introduction
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Drosophila has become a model for studying the role of hematopoietic (blood) cells and the evolution of cellular immunity (reviews by [>>1<<],[2]). Similar to vertebrates, Drosophila hematopoiesis occurs in two waves during development [3]. A first population of hemocytes is specified in the embryo and gives rise to plasmatocytes involved in phagocytosis and crystal cells
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Drosophila has become a model for studying the role of hematopoietic (blood) cells and the evolution of cellular immunity (reviews by [1],[>>2<<]). Similar to vertebrates, Drosophila hematopoiesis occurs in two waves during development [3]. A first population of hemocytes is specified in the embryo and gives rise to plasmatocytes involved in phagocytosis and crystal cells required
n2:mentions
n3:17394559
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Similar to vertebrates, Drosophila hematopoiesis occurs in two waves during development [>>3<<]. A first population of hemocytes is specified in the embryo and gives rise to plasmatocytes involved in phagocytosis and crystal cells required for melanisation [4]. A second wave of plasmatocyte and crystal cell production occurs at the
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A first population of hemocytes is specified in the embryo and gives rise to plasmatocytes involved in phagocytosis and crystal cells required for melanisation [>>4<<]. A second wave of plasmatocyte and crystal cell production occurs at the end of larval development. Larval hematopoiesis can also give rise to a third cell type, the lamellocytes, which are devoted to the encapsulation of foreign bodies
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Lamellocytes only differentiate in response to specific immune challenges such as parasitisation by wasps, a common threat for higher order insects [>>1<<],[2],[5],[6].
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Lamellocytes only differentiate in response to specific immune challenges such as parasitisation by wasps, a common threat for higher order insects [1],[>>2<<],[5],[6]. Larval hematopoiesis takes place in a specialised organ, the lymph gland (LG), which forms during embryogenesis and grows during larval development. In third instar larvae, the LG is composed of several lobes with the
n2:mentions
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Lamellocytes only differentiate in response to specific immune challenges such as parasitisation by wasps, a common threat for higher order insects [1],[2],[>>5<<],[6]. Larval hematopoiesis takes place in a specialised organ, the lymph gland (LG), which forms during embryogenesis and grows during larval development. In third instar larvae, the LG is composed of several lobes with the anterior-most
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Lamellocytes only differentiate in response to specific immune challenges such as parasitisation by wasps, a common threat for higher order insects [1],[2],[5],[>>6<<]. Larval hematopoiesis takes place in a specialised organ, the lymph gland (LG), which forms during embryogenesis and grows during larval development. In third instar larvae, the LG is composed of several lobes with the anterior-most lobes
n2:mentions
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lobes with the anterior-most lobes organised into a medullary zone (MZ) containing the hematopoietic progenitors, a cortical zone (CZ) containing differentiating hemocytes, and a so-called posterior signalling centre (PSC) (Figure 1F) [>>7<<]. These three zones can be identified by the expression of different markers. Differentiating crystal cells and plasmatocytes in the CZ express prophenoloxidase (proPO) and the P1 Nimrod receptor [8], respectively.
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Differentiating crystal cells and plasmatocytes in the CZ express prophenoloxidase (proPO) and the P1 Nimrod receptor [>>8<<], respectively.
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distinguished by their expression of domeless (dome), which encodes the Drosophila receptor of the janus tyrosine kinase/signal transducers and activators of transcription (JAK/STAT) pathway and tep4, which encodes a thioester protein [>>7<<],[9]. PSC cells express the transcription factors Antennapedia (Antp) and Collier/Knot (Col), the Drosophila Early B-cell Factor (EBF) ortholog [10], and the morphogen Hedgehog (Hh) [7],[11]–[13].
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by their expression of domeless (dome), which encodes the Drosophila receptor of the janus tyrosine kinase/signal transducers and activators of transcription (JAK/STAT) pathway and tep4, which encodes a thioester protein [7],[>>9<<]. PSC cells express the transcription factors Antennapedia (Antp) and Collier/Knot (Col), the Drosophila Early B-cell Factor (EBF) ortholog [10], and the morphogen Hedgehog (Hh) [7],[11]–[13].
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PSC cells express the transcription factors Antennapedia (Antp) and Collier/Knot (Col), the Drosophila Early B-cell Factor (EBF) ortholog [>>10<<], and the morphogen Hedgehog (Hh) [7],[11]–[13].
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PSC cells express the transcription factors Antennapedia (Antp) and Collier/Knot (Col), the Drosophila Early B-cell Factor (EBF) ortholog [10], and the morphogen Hedgehog (Hh) [>>7<<],[11]–[13].
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PSC cells express the transcription factors Antennapedia (Antp) and Collier/Knot (Col), the Drosophila Early B-cell Factor (EBF) ortholog [10], and the morphogen Hedgehog (Hh) [7],[>>11<<]–[13]. The PSC controls the balance between multipotent prohemocytes present in the MZ and differentiating hemocytes [9],[12]. It acts in a non–cell-autonomous manner, perhaps via Hh signalling, to maintain JAK/STAT signalling in
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PSC cells express the transcription factors Antennapedia (Antp) and Collier/Knot (Col), the Drosophila Early B-cell Factor (EBF) ortholog [10], and the morphogen Hedgehog (Hh) [7],[11]–[>>13<<]. The PSC controls the balance between multipotent prohemocytes present in the MZ and differentiating hemocytes [9],[12]. It acts in a non–cell-autonomous manner, perhaps via Hh signalling, to maintain JAK/STAT signalling in prohemocytes,
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The PSC controls the balance between multipotent prohemocytes present in the MZ and differentiating hemocytes [>>9<<],[12]. It acts in a non–cell-autonomous manner, perhaps via Hh signalling, to maintain JAK/STAT signalling in prohemocytes, thus preserving the multipotent character necessary for these cells to adopt a lamellocyte fate upon parasitisation.
n2:mentions
n3:17361184
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The PSC controls the balance between multipotent prohemocytes present in the MZ and differentiating hemocytes [9],[>>12<<]. It acts in a non–cell-autonomous manner, perhaps via Hh signalling, to maintain JAK/STAT signalling in prohemocytes, thus preserving the multipotent character necessary for these cells to adopt a lamellocyte fate upon parasitisation.
n2:mentions
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This key role of the PSC revealed that, in Drosophila, larval hemocyte homeostasis is dependent upon interactions between hematopoietic progenitors and their micro-environment, a role reminiscent of the vertebrate hematopoietic niche [>>9<<],[12],[14].
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key role of the PSC revealed that, in Drosophila, larval hemocyte homeostasis is dependent upon interactions between hematopoietic progenitors and their micro-environment, a role reminiscent of the vertebrate hematopoietic niche [9],[>>12<<],[14].
n2:mentions
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role of the PSC revealed that, in Drosophila, larval hemocyte homeostasis is dependent upon interactions between hematopoietic progenitors and their micro-environment, a role reminiscent of the vertebrate hematopoietic niche [9],[12],[>>14<<].
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Positions of the PG125/domeGal4 P-element insertion [>>67<<] and the lat genomic fragment that was deleted to generate a null allele are indicated by an arrowhead and a red bar, respectively.
n2:mentions
n3:11744370
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JAKs and STATs mediate intracellular signalling in response to secreted type I cytokines [>>15<<]. In mammals, large families of cytokines and single-pass transmembrane receptors, named type I cytokine receptors, which signal as either homodimers or heteromers, have been identified (for review [16]–[19]).
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n3:9287210
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In mammals, large families of cytokines and single-pass transmembrane receptors, named type I cytokine receptors, which signal as either homodimers or heteromers, have been identified (for review [>>16<<]–[19]). JAK kinases are anchored to the intracellular part of signalling receptors. Binding of the cytokine induces conformational changes in the latter that bring two JAKs in close proximity. This allows JAK trans-phosphorylation and
n2:mentions
n3:16480448
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In mammals, large families of cytokines and single-pass transmembrane receptors, named type I cytokine receptors, which signal as either homodimers or heteromers, have been identified (for review [16]–[>>19<<]). JAK kinases are anchored to the intracellular part of signalling receptors. Binding of the cytokine induces conformational changes in the latter that bring two JAKs in close proximity. This allows JAK trans-phosphorylation and
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Recent finding in Drosophila also point to a noncanonical mode of JAK/STAT signalling, which could directly control heterochromatin stability (for review [>>20<<]). Altered JAK/STAT activity has been associated with several human diseases including leukaemia, myocardial hypertrophy, and asthma, while knock-out studies in mice point to a central role in hematopoiesis and regulation of immune
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JAK/STAT activity has been associated with several human diseases including leukaemia, myocardial hypertrophy, and asthma, while knock-out studies in mice point to a central role in hematopoiesis and regulation of immune functions [>>21<<],[22]. In contrast to mammals, only one receptor, Domeless (Dome), one JAK (Hopscotch, Hop), one STAT (Stat92E or Marelle) and three cytokines, Unpaired (Upd), Upd2, and Upd3 have been functionally characterised in Drosophila (for review
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n2:Context
rdf:value
activity has been associated with several human diseases including leukaemia, myocardial hypertrophy, and asthma, while knock-out studies in mice point to a central role in hematopoiesis and regulation of immune functions [21],[>>22<<]. In contrast to mammals, only one receptor, Domeless (Dome), one JAK (Hopscotch, Hop), one STAT (Stat92E or Marelle) and three cytokines, Unpaired (Upd), Upd2, and Upd3 have been functionally characterised in Drosophila (for review [23]).
n2:mentions
n3:14668806
Subject Item
_:vb8412182
rdf:type
n2:Context
rdf:value
In contrast to mammals, only one receptor, Domeless (Dome), one JAK (Hopscotch, Hop), one STAT (Stat92E or Marelle) and three cytokines, Unpaired (Upd), Upd2, and Upd3 have been functionally characterised in Drosophila (for review [>>23<<]). Sequencing of the D. melanogaster genome revealed, however, the existence of a dome-cognate gene (CG14225, renamed here latran [lat]) (Figure 1) [24],[25].
n2:mentions
n3:16794031
Subject Item
_:vb8412183
rdf:type
n2:Context
rdf:value
Sequencing of the D. melanogaster genome revealed, however, the existence of a dome-cognate gene (CG14225, renamed here latran [lat]) (Figure 1) [>>24<<],[25].
n2:mentions
n3:12194841
Subject Item
_:vb8412184
rdf:type
n2:Context
rdf:value
Sequencing of the D. melanogaster genome revealed, however, the existence of a dome-cognate gene (CG14225, renamed here latran [lat]) (Figure 1) [24],[>>25<<].
n2:mentions
n3:12479803
Subject Item
_:vb8412185
rdf:type
n2:Context
rdf:value
A negative regulation of JAK/STAT signalling by a nonsignalling receptor chain has, so far, only been reported in primary and cultured mammalian cells, for short versions of class I cytokine receptors [>>26<<],[27]. However, the in vivo function of these short membrane receptors and how their expression is regulated and linked to tissue homeostasis remain to be established. The specific role of Drosophila lat in controlling a dedicated cellular
n2:mentions
n3:15627637
Subject Item
_:vb8412186
rdf:type
n2:Context
rdf:value
A negative regulation of JAK/STAT signalling by a nonsignalling receptor chain has, so far, only been reported in primary and cultured mammalian cells, for short versions of class I cytokine receptors [26],[>>27<<]. However, the in vivo function of these short membrane receptors and how their expression is regulated and linked to tissue homeostasis remain to be established. The specific role of Drosophila lat in controlling a dedicated cellular
n2:mentions
n3:11861389
Subject Item
_:vb8412187
rdf:type
n5:Section
dc:title
materials and methods
n5:contains
_:vb8412188 _:vb8412189 _:vb8412190 _:vb8412191 _:vb8412200 _:vb8412201 _:vb8412202 _:vb8412203 _:vb8412192 _:vb8412193 _:vb8412194 _:vb8412195 _:vb8412196 _:vb8412197 _:vb8412198 _:vb8412199
Subject Item
_:vb8412188
rdf:type
n2:Context
rdf:value
The following strains were used: pcol85-Gal4;UASmcd8GFP (pcol>GFP) [>>9<<]; PG125-dome-Gal4 (dome-Gal4) [67] and srp-Gal4 [11]. ey-Gal4 and da-Gal4 were obtained from the Bloomington Drosophila Stock Center.
n2:mentions
n3:17361184
Subject Item
_:vb8412189
rdf:type
n2:Context
rdf:value
The following strains were used: pcol85-Gal4;UASmcd8GFP (pcol>GFP) [9]; PG125-dome-Gal4 (dome-Gal4) [>>67<<] and srp-Gal4 [11]. ey-Gal4 and da-Gal4 were obtained from the Bloomington Drosophila Stock Center.
n2:mentions
n3:11744370
Subject Item
_:vb8412190
rdf:type
n2:Context
rdf:value
The following strains were used: pcol85-Gal4;UASmcd8GFP (pcol>GFP) [9]; PG125-dome-Gal4 (dome-Gal4) [67] and srp-Gal4 [>>11<<]. ey-Gal4 and da-Gal4 were obtained from the Bloomington Drosophila Stock Center.
n2:mentions
n3:15314643
Subject Item
_:vb8412191
rdf:type
n2:Context
rdf:value
The dome-MESO, UAS-dome, UAS-DomeΔα, and UAS-DomeΔω strains are from [>>42<<]; the UAS-upd3dsRNA from [50]; and the P[70FLP][70I-SceI)/TM3 and P[ry+; FLP)10 (Chromosome II) from F.
n2:mentions
n3:12783781
Subject Item
_:vb8412192
rdf:type
n2:Context
rdf:value
The dome-MESO, UAS-dome, UAS-DomeΔα, and UAS-DomeΔω strains are from [42]; the UAS-upd3dsRNA from [>>50<<]; and the P[70FLP][70I-SceI)/TM3 and P[ry+; FLP)10 (Chromosome II) from F.
n2:mentions
n3:12967563
Subject Item
_:vb8412193
rdf:type
n2:Context
rdf:value
The procedure was adapted from the Ends out Knock Out method [>>33<<]. A lat KO “donor” transgene was constructed in pW25 [68] by inserting 4 kb of 5′ and of 3′ flanking sequences of the lat gene separated by the mini-white gene and used to transform white mutant flies ().
n2:mentions
n3:12589026
Subject Item
_:vb8412194
rdf:type
n2:Context
rdf:value
A lat KO “donor” transgene was constructed in pW25 [>>68<<] by inserting 4 kb of 5′ and of 3′ flanking sequences of the lat gene separated by the mini-white gene and used to transform white mutant flies ().
n2:mentions
n3:15579699
Subject Item
_:vb8412195
rdf:type
n2:Context
rdf:value
UAS-LatΔα and UAS-LatΔω were constructed using the complete lat cDNA fused to the β-galactosidase Δα and Δω fragments from pUAS-Dome-LacZΔα and pUAS-Dome-LacZΔω, respectively [>>42<<]. The fusion constructs were subcloned into pUAS-attB to generate transgenic flies using the ZH49B and ZH86F attP integration platforms [69]. Act-Lat, Act-HALat, and Act-DomeV5 plasmids were constructed and used for cell culture
n2:mentions
n3:12783781
Subject Item
_:vb8412196
rdf:type
n2:Context
rdf:value
The fusion constructs were subcloned into pUAS-attB to generate transgenic flies using the ZH49B and ZH86F attP integration platforms [>>69<<]. Act-Lat, Act-HALat, and Act-DomeV5 plasmids were constructed and used for cell culture experiments.
n2:mentions
n3:17360644
Subject Item
_:vb8412197
rdf:type
n2:Context
rdf:value
Dissections, in situ hybridisation, and immunostaining procedures were as described in [>>9<<],[70]. The following antibodies were used:
n2:mentions
n3:17361184
Subject Item
_:vb8412198
rdf:type
n2:Context
rdf:value
Dissections, in situ hybridisation, and immunostaining procedures were as described in [9],[>>70<<]. The following antibodies were used:
n2:mentions
n3:18003742
Subject Item
_:vb8412199
rdf:type
n2:Context
rdf:value
The following antibodies were used: rabbit anti-GFP (Torrey) 1/500; mouse anti-β-galactosidase (Promega) 1/800; rabbit anti-proPO 1/200; mouse anti-Col 1/50; rabbit anti-αPS4 [>>9<<] 1/200; mouse anti-V5 (Invitrogen) 1/5,000; mouse and rabbit anti-HA (Covance and Santa Cruz, respectively) 1/1,000.
n2:mentions
n3:17361184
Subject Item
_:vb8412200
rdf:type
n2:Context
rdf:value
X-Gal staining was as described in [>>42<<].
n2:mentions
n3:12783781
Subject Item
_:vb8412201
rdf:type
n2:Context
rdf:value
CT values were collected and analysis was performed according to the 2ΔΔCT method [>>71<<] using rp49 and rpL17A to normalize estimates of relative expression.
n2:mentions
n3:11846609
Subject Item
_:vb8412202
rdf:type
n2:Context
rdf:value
Various amounts of Act-Lat, 0.2 ng of Act-Dome, and 1 ng of either Act-Upd, Upd2, or Upd3 were used to transfect S2-NP cells [>>29<<]. Luciferase assays were performed 4 d later, and the reporter activity was normalised as the ratio of firefly luciferase/Renilla.
n2:mentions
n3:16055650
Subject Item
_:vb8412203
rdf:type
n2:Context
rdf:value
Drosophila S2-NP cells [>>29<<] were maintained in Schneider medium +10% FCS + penicillin-streptomycin (Sigma 1/100) at 25°C without supplemental CO2.
n2:mentions
n3:16055650
Subject Item
_:vb8412204
rdf:type
n5:Section
dc:title
results
n5:contains
_:vb8412244 _:vb8412245 _:vb8412246 _:vb8412247 _:vb8412240 _:vb8412241 _:vb8412242 _:vb8412243 _:vb8412248 _:vb8412249 _:vb8412228 _:vb8412229 _:vb8412230 _:vb8412231 _:vb8412224 _:vb8412225 _:vb8412226 _:vb8412227 _:vb8412236 _:vb8412237 _:vb8412238 _:vb8412239 _:vb8412232 _:vb8412233 _:vb8412234 _:vb8412235 _:vb8412212 _:vb8412213 _:vb8412214 _:vb8412215 _:vb8412208 _:vb8412209 _:vb8412210 _:vb8412211 _:vb8412220 _:vb8412221 _:vb8412222 _:vb8412223 _:vb8412216 _:vb8412217 _:vb8412218 _:vb8412219 _:vb8412205 _:vb8412206 _:vb8412207
Subject Item
_:vb8412205
rdf:type
n2:Context
rdf:value
Dome is the only class I cytokine receptor that has, so far, been characterised in Drosophila [>>28<<]–[31]. Existence of a D. melanogaster gene, CG14225/lat, coding for a protein structurally related to Dome was noticed several years ago [24]. dome and lat are adjacent to each other on the X chromosome and transcribed in the same
n2:mentions
n3:11696329
Subject Item
_:vb8412206
rdf:type
n2:Context
rdf:value
Dome is the only class I cytokine receptor that has, so far, been characterised in Drosophila [28]–[>>31<<]. Existence of a D. melanogaster gene, CG14225/lat, coding for a protein structurally related to Dome was noticed several years ago [24]. dome and lat are adjacent to each other on the X chromosome and transcribed in the same orientation,
n2:mentions
n3:11825879
Subject Item
_:vb8412207
rdf:type
n2:Context
rdf:value
Existence of a D. melanogaster gene, CG14225/lat, coding for a protein structurally related to Dome was noticed several years ago [>>24<<]. dome and lat are adjacent to each other on the X chromosome and transcribed in the same orientation, suggesting that they originated from a gene duplication event (Figure 1A). The key role of JAK/STAT signalling in regulating larval
n2:mentions
n3:12194841
Subject Item
_:vb8412208
rdf:type
n2:Context
rdf:value
The key role of JAK/STAT signalling in regulating larval hemocyte homeostasis [>>9<<],[32] led us to ask whether lat was involved in this regulation.
n2:mentions
n3:17361184
Subject Item
_:vb8412209
rdf:type
n2:Context
rdf:value
The key role of JAK/STAT signalling in regulating larval hemocyte homeostasis [9],[>>32<<] led us to ask whether lat was involved in this regulation.
n2:mentions
n3:18603010
Subject Item
_:vb8412210
rdf:type
n2:Context
rdf:value
The intracellular region of Lat is shorter than that of Dome and shows no consensus STAT binding site (motif YXXQ, [>>25<<]) suggesting that lat encodes a nonsignalling form of cytokine receptor.
n2:mentions
n3:12479803
Subject Item
_:vb8412211
rdf:type
n2:Context
rdf:value
Coexpression of dome and lat in MZ cells, where JAK/STAT signalling is critically required to maintain a pool of hematopoietic progenitors [>>9<<], raised the question of the role of lat in controlling the activation of the JAK/STAT pathway in prohemocytes.
n2:mentions
n3:17361184
Subject Item
_:vb8412212
rdf:type
n2:Context
rdf:value
To determine if lat plays a role in larval hematopoiesis, we generated a lat null allele by homologous recombination [>>33<<]. Several independent recombination events were obtained and homozygous mutant lines were established (Figure S1).
n2:mentions
n3:12589026
Subject Item
_:vb8412213
rdf:type
n2:Context
rdf:value
In particular, no phenotypic defect was observed in the eye, where the JAK/SAT pathway plays an important role in growth and patterning [>>34<<],[35]. We then looked at the morphology of the LG in lat mutant larvae, using specific markers for the MZ (tep4), the PSC (col), or for differentiated hemocytes: crystal cells (doxA3) and plasmatocytes (P1). No obvious difference could be
n2:mentions
n3:15170700
Subject Item
_:vb8412214
rdf:type
n2:Context
rdf:value
In particular, no phenotypic defect was observed in the eye, where the JAK/SAT pathway plays an important role in growth and patterning [34],[>>35<<]. We then looked at the morphology of the LG in lat mutant larvae, using specific markers for the MZ (tep4), the PSC (col), or for differentiated hemocytes: crystal cells (doxA3) and plasmatocytes (P1). No obvious difference could be found
n2:mentions
n3:17079268
Subject Item
_:vb8412215
rdf:type
n2:Context
rdf:value
In wt larvae, the number of circulating lamellocytes reaches its maximum 48 h after wasp egg-laying [>>5<<]. In sharp contrast to wt, virtually no circulating lamellocytes are found in the hemolymph of parasitised lat mutant larvae (Figure 2A, 2B), either 48 or 72 h after wasp egg-laying. Several days later, adult wasps hatch from parasitised
n2:mentions
n3:11161576
Subject Item
_:vb8412216
rdf:type
n2:Context
rdf:value
The scattered distribution of GFP-labelled cells is due to nonuniform activation of the srp-Gal4 driver in the LG [>>11<<]. Nuclei (TOPRO-3) are in blue. Scale bars, 50 µm (A); 80 µm (D).
n2:mentions
n3:15314643
Subject Item
_:vb8412217
rdf:type
n2:Context
rdf:value
Lamellocyte production upon parasitisation involves downregulation of JAK/STAT signalling in the MZ, thereby licensing hematopoietic progenitors to differentiate [>>9<<]. JAK/STAT activity in the LG can be monitored by the expression of a reporter transgene, dome-MESO-lacZ (dome-MESO), where LacZ is under the control of an intronic dome regulatory element [9],[36],[37].
n2:mentions
n3:17361184
Subject Item
_:vb8412218
rdf:type
n2:Context
rdf:value
JAK/STAT activity in the LG can be monitored by the expression of a reporter transgene, dome-MESO-lacZ (dome-MESO), where LacZ is under the control of an intronic dome regulatory element [>>9<<],[36],[37].
n2:mentions
n3:17361184
Subject Item
_:vb8412219
rdf:type
n2:Context
rdf:value
JAK/STAT activity in the LG can be monitored by the expression of a reporter transgene, dome-MESO-lacZ (dome-MESO), where LacZ is under the control of an intronic dome regulatory element [9],[>>36<<],[37]. Under normal conditions, LacZ expression is observed in the MZ of lat mutant as in wt larvae, indicating that the JAK/STAT pathway is active and that lat is not required for this activity (Figures 2 and S4). 30 h postinfestation a
n2:mentions
n3:16277982
Subject Item
_:vb8412220
rdf:type
n2:Context
rdf:value
JAK/STAT activity in the LG can be monitored by the expression of a reporter transgene, dome-MESO-lacZ (dome-MESO), where LacZ is under the control of an intronic dome regulatory element [9],[36],[>>37<<]. Under normal conditions, LacZ expression is observed in the MZ of lat mutant as in wt larvae, indicating that the JAK/STAT pathway is active and that lat is not required for this activity (Figures 2 and S4). 30 h postinfestation a strong
n2:mentions
n3:18802449
Subject Item
_:vb8412221
rdf:type
n2:Context
rdf:value
30 h postinfestation a strong reduction of dome-MESO expression is observed in wt LGs (Figure 2D, 2E) correlating with lamellocyte differentiation (Figure 2E, insert) and premature LG dispersal [>>5<<]. In sharp contrast, dome-MESO remains expressed in lat mutant LGs and these, unlike wt LG, do not prematurely disperse (Figure 2F, 2G), correlating with the absence of circulating lamellocytes in the hemolymph. This shows that lat is
n2:mentions
n3:11161576
Subject Item
_:vb8412222
rdf:type
n2:Context
rdf:value
In order to follow the activity of the pathway after parasitism, we analysed the subcellular localisation of a fluorescent Stat protein, Stat-GFP [>>38<<], expressed in the LG (srp-Gal4;STAT92E-GFP).
n2:mentions
n3:16129580
Subject Item
_:vb8412223
rdf:type
n2:Context
rdf:value
The PSC (niche) is critically required to maintain a balance between JAK/STAT-positive progenitors and JAK/STAT-negative differentiating hemocytes in third instar LG [>>9<<]. The function of lat in the MZ raised the question of the relative contribution of positive and negative regulation by the PSC and lat, respectively, in the maintenance of this balance.
n2:mentions
n3:17361184
Subject Item
_:vb8412224
rdf:type
n2:Context
rdf:value
Whereas in col mutant LGs, which lack a PSC, the MZ disappears and all prohemocytes differentiate [>>9<<], we observed a less severe phenotype in lat;col double mutants, namely the loss of an organised MZ with remaining prohemocytes intermingled with differentiated hemocytes (Figure S5A).
n2:mentions
n3:17361184
Subject Item
_:vb8412225
rdf:type
n2:Context
rdf:value
To further investigate the possible mechanism behind this inhibition, we turned to reporter assay developed in cultured Drosophila Schneider (S2-NP) cells [>>29<<]. S2-NP cells display a basal level of endogenous JAK/STAT activity, as shown by transfection of a STAT reporter gene (10XStat92E-Luciferase reporter). A much stronger activity is observed upon coexpression of either of the cytokines Upd,
n2:mentions
n3:16055650
Subject Item
_:vb8412226
rdf:type
n2:Context
rdf:value
A much stronger activity is observed upon coexpression of either of the cytokines Upd, Upd2 [>>29<<],[30],[36], or Upd3 (Figure S6).
n2:mentions
n3:16055650
Subject Item
_:vb8412227
rdf:type
n2:Context
rdf:value
A much stronger activity is observed upon coexpression of either of the cytokines Upd, Upd2 [29],[>>30<<],[36], or Upd3 (Figure S6).
n2:mentions
n3:16094372
Subject Item
_:vb8412228
rdf:type
n2:Context
rdf:value
A much stronger activity is observed upon coexpression of either of the cytokines Upd, Upd2 [29],[30],[>>36<<], or Upd3 (Figure S6).
n2:mentions
n3:16277982
Subject Item
_:vb8412229
rdf:type
n2:Context
rdf:value
Since high level of forced Dome expression could act as a dominant-negative [>>39<<], we transfected low levels of Act-dome, which modestly increased JAK/STAT signalling (Figure 3E).
n2:mentions
n3:14668372
Subject Item
_:vb8412230
rdf:type
n2:Context
rdf:value
Binding of Upd to Dome induces endocytosis of receptor-ligand complexes and their trafficking through the endosomal compartments, a trafficking required to activate JAK/STAT signalling [>>40<<]. We looked at the intracellular localisation of a tagged Dome (Dome-V5) in cells transfected with both Upd and Act-Dome-V5, where the pathway is active.
n2:mentions
n3:17855388
Subject Item
_:vb8412231
rdf:type
n2:Context
rdf:value
Dome(-V5) was localised in cytoplasmic vesicles as previously described (Figure 3F) [>>40<<]. This localisation was unchanged in cells cotransfected with a tagged Lat (Act-HA-Lat), which results in inactivation of the pathway (Figure 3F, 3G). Both Dome-V5 and HA-Lat were localised in mostly overlapping intracytoplasmic vesicles,
n2:mentions
n3:17855388
Subject Item
_:vb8412232
rdf:type
n2:Context
rdf:value
Long and short forms of vertebrate class 1 cytokine receptors can form heterodimers/multimers [>>17<<],[41]. While Dome was previously shown to form homodimers [42], we tested the possibility that Lat could form heteromers with Dome, by using coimmunoprecipitation (co-IP) assays.
n2:mentions
n3:12773095
Subject Item
_:vb8412233
rdf:type
n2:Context
rdf:value
Long and short forms of vertebrate class 1 cytokine receptors can form heterodimers/multimers [17],[>>41<<]. While Dome was previously shown to form homodimers [42], we tested the possibility that Lat could form heteromers with Dome, by using coimmunoprecipitation (co-IP) assays.
n2:mentions
n3:8272873
Subject Item
_:vb8412234
rdf:type
n2:Context
rdf:value
While Dome was previously shown to form homodimers [>>42<<], we tested the possibility that Lat could form heteromers with Dome, by using coimmunoprecipitation (co-IP) assays.
n2:mentions
n3:12783781
Subject Item
_:vb8412235
rdf:type
n2:Context
rdf:value
We then tested whether Lat and Dome form heteromers in vivo, using the βblue-βblau β-galactosidase complementation technique developed to detect protein-protein interactions in vivo [>>43<<]–[45] and already applied to show that Dome forms homodimers [42].
n2:mentions
n3:9237989
Subject Item
_:vb8412236
rdf:type
n2:Context
rdf:value
We then tested whether Lat and Dome form heteromers in vivo, using the βblue-βblau β-galactosidase complementation technique developed to detect protein-protein interactions in vivo [43]–[>>45<<] and already applied to show that Dome forms homodimers [42].
n2:mentions
n3:10657132
Subject Item
_:vb8412237
rdf:type
n2:Context
rdf:value
whether Lat and Dome form heteromers in vivo, using the βblue-βblau β-galactosidase complementation technique developed to detect protein-protein interactions in vivo [43]–[45] and already applied to show that Dome forms homodimers [>>42<<]. Briefly, this technique uses two β-Gal mutant forms (Δα and Δω) that are separately inactive but can complement each other if brought into proximity by fusing them to proteins that physically interact.
n2:mentions
n3:12783781
Subject Item
_:vb8412238
rdf:type
n2:Context
rdf:value
Like for Dome [>>42<<], Δα and Δω β-galactosidases were fused to the Lat C terminus.
n2:mentions
n3:12783781
Subject Item
_:vb8412239
rdf:type
n2:Context
rdf:value
We used the da-Gal4 driver to coexpress different combinations of Lat and Dome fusion proteins in embryos (Figure 4B–4E), because it leads to strong ubiquitous embryonic expression of the proteins (Figure 4C and unpublished data) [>>42<<]. Contrasting with this ubiquitous expression, X-gal staining was only detected in the salivary glands and hindgut when Dome Δα and Dome Δω were coexpressed as previously reported (Figure 4B) [42].
n2:mentions
n3:12783781
Subject Item
_:vb8412240
rdf:type
n2:Context
rdf:value
Contrasting with this ubiquitous expression, X-gal staining was only detected in the salivary glands and hindgut when Dome Δα and Dome Δω were coexpressed as previously reported (Figure 4B) [>>42<<]. A similar staining pattern was observed upon coexpression of LatΔα/LatΔω LatΔα/DomeΔω or DomeΔα/LatΔω (Figure 4D, 4E, and not shown), while no staining could be detected when only one fusion protein was expressed. These results indicate
n2:mentions
n3:12783781
Subject Item
_:vb8412241
rdf:type
n2:Context
rdf:value
expression of one copy of either Lat, LatΔα or LatΔω resulted in an “outstretched wing” phenotype in adult flies, a phenotype previously described for upd mutant flies, hence the name outstretched (os/upd) given to these mutants [46],[>>47<<]. This observation indicates that both the native and Lat fusion proteins are able to downregulate the JAK/STAT pathway.
n2:mentions
n3:9784499
Subject Item
_:vb8412242
rdf:type
n2:Context
rdf:value
eyeless-Gal4 driven expression of lat in eye discs led to smaller eyes, another phenotype reminiscent of upd mutants (Figure S7) [>>39<<], confirming that lat is able to downregulate JAK/STAT signalling in tissues other than the LG when ectopically expressed.
n2:mentions
n3:14668372
Subject Item
_:vb8412243
rdf:type
n2:Context
rdf:value
Quantitative RT-PCR (qRT-PCR) measurements were performed on total LG RNA from control larvae and larvae 4 h after wasp egg-laying in order to mainly detect primary changes that occur in response to parasitism [>>48<<]. We detected an about 2-fold increase in lat transcripts and 2-fold decrease in dome transcripts, which results in a significant drop in the dome/lat ratio (Figure 5A). Since JAK/STAT signalling remains on after infestation in lat mutant
n2:mentions
n3:16277749
Subject Item
_:vb8412244
rdf:type
n2:Context
rdf:value
Three different ligands, Upd, Upd2, and Upd3, are known to activate JAK/STAT signalling in Drosophila [>>47<<],[49]. In order to determine which of them are expressed in the LG, we first performed RT-PCR experiments, starting from LG mRNA.
n2:mentions
n3:9784499
Subject Item
_:vb8412245
rdf:type
n2:Context
rdf:value
Three different ligands, Upd, Upd2, and Upd3, are known to activate JAK/STAT signalling in Drosophila [47],[>>49<<]. In order to determine which of them are expressed in the LG, we first performed RT-PCR experiments, starting from LG mRNA.
n2:mentions
n3:15925495
Subject Item
_:vb8412246
rdf:type
n2:Context
rdf:value
While a upd3 loss of function mutant is not available, studies performed in vivo and in cell culture have established that upd3 dsRNA expression can efficiently suppress upd3 activity [>>50<<]. We looked at the consequence of upd3 dsRNA expression (UAS-upd3 dsRNA/dome-Gal4), which drastically reduces upd3 mRNA level in the LG (Figure 5D), on dome-MESO expression. No dome-MESO expression could be detected, showing that upd3
n2:mentions
n3:12967563
Subject Item
_:vb8412247
rdf:type
n2:Context
rdf:value
While JAK/STAT signalling is dependent upon the binding of Upd to Dome, dome is itself a target of the JAK/STAT pathway in the embryonic mesoderm [>>36<<], a regulatory loop reproduced by the dome-MESO enhancer in the LG [9],[36].
n2:mentions
n3:16277982
Subject Item
_:vb8412248
rdf:type
n2:Context
rdf:value
While JAK/STAT signalling is dependent upon the binding of Upd to Dome, dome is itself a target of the JAK/STAT pathway in the embryonic mesoderm [36], a regulatory loop reproduced by the dome-MESO enhancer in the LG [>>9<<],[36]. To directly test whether the decreased amount of dome transcripts in the LG that follows wasp parasitisation could result from the drop of upd3 activity, we measured the relative amounts of dome and lat transcripts upon upd3 dsRNA
n2:mentions
n3:17361184
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_:vb8412249
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While JAK/STAT signalling is dependent upon the binding of Upd to Dome, dome is itself a target of the JAK/STAT pathway in the embryonic mesoderm [36], a regulatory loop reproduced by the dome-MESO enhancer in the LG [9],[>>36<<]. To directly test whether the decreased amount of dome transcripts in the LG that follows wasp parasitisation could result from the drop of upd3 activity, we measured the relative amounts of dome and lat transcripts upon upd3 dsRNA
n2:mentions
n3:16277982
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_:vb8412250
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n5:Section
dc:title
discussion
n5:contains
_:vb8412252 _:vb8412253 _:vb8412254 _:vb8412255 _:vb8412251 _:vb8412268 _:vb8412269 _:vb8412270 _:vb8412271 _:vb8412264 _:vb8412265 _:vb8412266 _:vb8412267 _:vb8412260 _:vb8412261 _:vb8412262 _:vb8412263 _:vb8412256 _:vb8412257 _:vb8412258 _:vb8412259 _:vb8412276 _:vb8412272 _:vb8412273 _:vb8412274 _:vb8412275
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Upon wasp infestation, however, JAK/STAT signalling is switched off, leading to a concerted differentiation of prohemocytes into lamellocytes [>>9<<]. In col mutant LGs, which are devoid of PSC cells, no lamellocytes differentiate after wasp infestation as a consequence of the premature loss of multipotent prohemocytes; conversely, in lat mutant larvae, prohemocytes are maintained and
n2:mentions
n3:17361184
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_:vb8412252
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RNA interference experiments show that upd3 is expressed and required in the MZ to maintain JAK/STAT activity in prohemocytes, therefore acting in an autocrine and/or paracrine manner, as previously reported for Upd in embryos [>>47<<],[51],[52].
n2:mentions
n3:9784499
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_:vb8412253
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RNA interference experiments show that upd3 is expressed and required in the MZ to maintain JAK/STAT activity in prohemocytes, therefore acting in an autocrine and/or paracrine manner, as previously reported for Upd in embryos [47],[>>51<<],[52]. The drastic decrease of upd3 expression induced by wasp egg-laying is accompanied by a significant decrease in dome transcripts, showing that dome is both a component and a target of JAK/STAT signalling in the MZ (Figure 5), as
n2:mentions
n3:3084105
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_:vb8412254
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interference experiments show that upd3 is expressed and required in the MZ to maintain JAK/STAT activity in prohemocytes, therefore acting in an autocrine and/or paracrine manner, as previously reported for Upd in embryos [47],[51],[>>52<<]. The drastic decrease of upd3 expression induced by wasp egg-laying is accompanied by a significant decrease in dome transcripts, showing that dome is both a component and a target of JAK/STAT signalling in the MZ (Figure 5), as
n2:mentions
n3:10879541
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_:vb8412255
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by wasp egg-laying is accompanied by a significant decrease in dome transcripts, showing that dome is both a component and a target of JAK/STAT signalling in the MZ (Figure 5), as previously documented in the embryonic mesoderm [>>36<<]. lat and dome mRNA levels are not, however, coregulated in response to parasitisation even though the two genes lie very close to each other on the chromosome, a tandem organisation conserved in other Drosophila species.
n2:mentions
n3:16277982
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we do not know yet how upd3 is downregulated, it is tempting to speculate that it could be at a post-transcriptional level, similar to the importance of post-transcriptional regulation for cytokine levels in vertebrates (for review [>>53<<]). In summary, our results show that a primary immune response to wasp egg-laying is a strong decrease in upd3 mRNA levels in the LG, which induces a downregulation of the JAK/STAT pathway, followed by a decrease of dome and increase of
n2:mentions
n3:18349815
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is related to the human GP130 and cognate GP130-like (GPL) signalling receptors, which form heteromeric complexes with short, nonsignalling receptors such as IL-6R or Oncostatin M receptor (OSM-R) to mediate signalling (Figure S9) [>>26<<],[54],[55].
n2:mentions
n3:15627637
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_:vb8412258
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related to the human GP130 and cognate GP130-like (GPL) signalling receptors, which form heteromeric complexes with short, nonsignalling receptors such as IL-6R or Oncostatin M receptor (OSM-R) to mediate signalling (Figure S9) [26],[>>54<<],[55]. lat encodes a short-type receptor that could either act as IL-6R and confer signalling specificity to Dome or as a dominant-negative receptor similar to what has been described ex vivo for short receptors such as GPL and IL13Rα2
n2:mentions
n3:14504285
Subject Item
_:vb8412259
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to the human GP130 and cognate GP130-like (GPL) signalling receptors, which form heteromeric complexes with short, nonsignalling receptors such as IL-6R or Oncostatin M receptor (OSM-R) to mediate signalling (Figure S9) [26],[54],[>>55<<]. lat encodes a short-type receptor that could either act as IL-6R and confer signalling specificity to Dome or as a dominant-negative receptor similar to what has been described ex vivo for short receptors such as GPL and IL13Rα2 [27].
n2:mentions
n3:14698616
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lat encodes a short-type receptor that could either act as IL-6R and confer signalling specificity to Dome or as a dominant-negative receptor similar to what has been described ex vivo for short receptors such as GPL and IL13Rα2 [>>27<<]. Cell-culture and in vivo assays show that Lat antagonises Dome activity in a dose-dependent manner and forms heteromers with Dome thereby acting as a dominant-negative receptor.
n2:mentions
n3:11861389
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Cytokine signalling pathways are subject to extensive positive and negative feedback regulations, which are crucial to generate appropriate physiological responses [>>22<<]. Two genome-wide RNA interference (RNAi) screens for JAK/STAT signalling components were conducted in Drosophila cultured cells.
n2:mentions
n3:14668806
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putative positive and negative regulators, they failed to detect lat, either because its expression level in cell culture is too low to be functional or because the lat dsRNA constructs used in these screens were not efficient enough [>>29<<],[30],[56]. col/kn was identified in one of these RNAi screens, however, as a positive regulator acting downstream of Hop [30], suggesting another possible level of regulation of JAK/STAT signalling in the LG.
n2:mentions
n3:16055650
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_:vb8412263
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positive and negative regulators, they failed to detect lat, either because its expression level in cell culture is too low to be functional or because the lat dsRNA constructs used in these screens were not efficient enough [29],[>>30<<],[56]. col/kn was identified in one of these RNAi screens, however, as a positive regulator acting downstream of Hop [30], suggesting another possible level of regulation of JAK/STAT signalling in the LG.
n2:mentions
n3:16094372
Subject Item
_:vb8412264
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positive and negative regulators, they failed to detect lat, either because its expression level in cell culture is too low to be functional or because the lat dsRNA constructs used in these screens were not efficient enough [29],[30],[>>56<<]. col/kn was identified in one of these RNAi screens, however, as a positive regulator acting downstream of Hop [30], suggesting another possible level of regulation of JAK/STAT signalling in the LG.
n2:mentions
n3:18586112
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_:vb8412265
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col/kn was identified in one of these RNAi screens, however, as a positive regulator acting downstream of Hop [>>30<<], suggesting another possible level of regulation of JAK/STAT signalling in the LG.
n2:mentions
n3:16094372
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This finding led to the conclusion that upregulation of JAK/STAT signalling triggers lamellocyte differentiation, which is in apparent contradiction with our present data [>>32<<]. Whether constitutive JAK/STAT signalling in differentiating hemocytes could instruct them to become lamellocytes remains an interesting possibility. Of note, a STAT target, chimno, was recently shown to be expressed at higher levels in
n2:mentions
n3:18603010
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_:vb8412267
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Recent studies further suggest a dual role of Wg signalling in the maintenance of prohemocytes and PSC cells [>>58<<]. A tight control of ROS levels in the MZ is also required to maintain a pool of prohemocytes [59]. How these different signalling pathways are interconnected with JAK/STAT signalling in order to maintain hemocyte homeostasis in the LG are
n2:mentions
n3:19460351
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A tight control of ROS levels in the MZ is also required to maintain a pool of prohemocytes [>>59<<]. How these different signalling pathways are interconnected with JAK/STAT signalling in order to maintain hemocyte homeostasis in the LG are important questions to be addressed in the future.
n2:mentions
n3:19727075
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The type I cytokine receptor family has considerably expanded in vertebrates [>>60<<]. This expansion results both from an increased number of receptor genes and from the generation of various protein isoforms that can act as either receptors or coreceptors [61].
n2:mentions
n3:12932349
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This expansion results both from an increased number of receptor genes and from the generation of various protein isoforms that can act as either receptors or coreceptors [>>61<<]. Soluble versions of short receptors isolated from diverse body fluids have also been identified, which behave as antagonists by competing with membrane-associated receptors for ligand binding [62],[63]. These soluble receptors are
n2:mentions
n3:15895091
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Soluble versions of short receptors isolated from diverse body fluids have also been identified, which behave as antagonists by competing with membrane-associated receptors for ligand binding [>>62<<],[63]. These soluble receptors are generated by either limited proteolysis or translation from differently spliced mRNAs. Finally, studies on IL13Rα2 [27] or GPL [64] suggested that short receptors anchored to the membrane could also
n2:mentions
n3:17027515
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Soluble versions of short receptors isolated from diverse body fluids have also been identified, which behave as antagonists by competing with membrane-associated receptors for ligand binding [62],[>>63<<]. These soluble receptors are generated by either limited proteolysis or translation from differently spliced mRNAs. Finally, studies on IL13Rα2 [27] or GPL [64] suggested that short receptors anchored to the membrane could also behave as
n2:mentions
n3:17967718
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Finally, studies on IL13Rα2 [>>27<<] or GPL [64] suggested that short receptors anchored to the membrane could also behave as dominant negative receptors.
n2:mentions
n3:11861389
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Finally, studies on IL13Rα2 [27] or GPL [>>64<<] suggested that short receptors anchored to the membrane could also behave as dominant negative receptors.
n2:mentions
n3:17028186
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Our studies in Drosophila indicate that Lat acts as a dominant-negative receptor rather than a coreceptor, extending in vivo the few observations made in mammalian cell cultures [>>65<<],[66]. Tissue-specific regulation of JAK/STAT signalling in response to environmental cues is crucial for the ability of Drosophila to mount a cellular immune defense. Our results bring to light a new mode of fine tuning of the JAK/STAT
n2:mentions
n3:9212050
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Our studies in Drosophila indicate that Lat acts as a dominant-negative receptor rather than a coreceptor, extending in vivo the few observations made in mammalian cell cultures [65],[>>66<<]. Tissue-specific regulation of JAK/STAT signalling in response to environmental cues is crucial for the ability of Drosophila to mount a cellular immune defense. Our results bring to light a new mode of fine tuning of the JAK/STAT
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