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Placental Defects and Embryonic Lethality in Mice Lacking Suppressor of Cytokine Signaling 3

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Placental Defects and Embryonic Lethality in Mice Lacking Suppressor of Cytokine Signaling 3 Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3 Andrew W. Roberts*, Lorraine Robb*, Steven Rakar†, Lynne Hartley*, Leonie Cluse*, Nicos A. Nicola*, Donald Metcalf*, Douglas J. Hilton*, and Warren S. Alexander*‡ *The Walter and Eliza Hall Institute of Medical Research and Cooperative Research Centre for Cellular Growth Factors, Post Office, Royal Melbourne Hospital, Victoria 3050, Australia; and †AMRAD Operations Pty. Ltd., Richmond, Victoria 3121, Australia Contributed by Donald Metcalf, May 31, 2001 Mice lacking suppressor of cytokine signaling 3 (SOCS3) exhibited activity of which it ultimately inhibits. SOCS proteins may also embryonic lethality with death occurring between days 11 and 13 target associated signaling molecules for degradation. The SOCS ,of gestation. At this stage, SOCS3؊/؊ embryos were slightly smaller box domain has been shown to interact with elongins B and C than wild type but appeared otherwise normal, and histological proteins involved in the cellular ubiquitination machinery that analysis failed to detect any anatomical abnormalities responsible targets proteins for destruction via the proteasome (9, 10). Thus, for the lethal phenotype. Rather, in all SOCS3؊/؊ embryos exam- SOCS proteins may regulate cytokine responses through control ined, defects were evident in placental development that would of the turnover of signaling proteins as well as directly inhibiting account for their developmental arrest and death. The placental their catalytic activity or recruitment to the signaling complex. spongiotrophoblast layer was significantly reduced and accompa- The physiological significance of SOCS-mediated control of nied by increased numbers of giant trophoblast cells. Delayed cytokine signaling has emerged from studies in which these branching of the chorioallantois was evident, and, although em- regulators have been functionally deleted in mice. SOCS1 is a key bryonic blood vessels were present in the labyrinthine layer of modulator of IFN-␥ signaling. Mice lacking SOCS1 display ؊ ؊ SOCS3 / placentas, the network of embryonic vessels and ma- deregulated responses to IFN-␥ that result in a lethal combina- ternal sinuses was poorly developed. Yolk sac erythropoiesis was tion of fatty degeneration and necrosis of the liver, excessive T ؊ ؊ normal, and, although the SOCS3 / fetal liver was small at day cell activation, lymphopenia, and hematopoietic infiltration of 12.5 of gestation (E12.5), normal frequencies of erythroblasts and multiple organs (11–14). In contrast, mice lacking SOCS2 are hematopoietic progenitor cells, including blast forming unit-eryth- healthy and fertile, but display excessive growth consistent with roid (BFU-E) and, colony forming unit-erythroid (CFU-E) were a negative regulatory role for SOCS2 in GH and͞or insulin-like present at both E11.5 and E12.5. Colony formation for both BFU-E growth factor (IGF)-I signaling (15). SOCS3 has been implicated ؊ ؊ and CFU-E from SOCS3 / mice displayed wild-type quantitative in control of cytokine signaling in several biological systems. For responsiveness to erythropoietin (EPO), in the presence or absence example, in addition to the potential roles for SOCS3 implied by of IL-3 or stem cell factor (SCF). These data suggest that SOCS3 is its capacity to interact with and inhibit signals from the GHR, required for placental development but dispensable for normal IL-2R␤, EPOR, and gp130 receptors (see above), SOCS3 has hematopoiesis in the mouse embryo. also been implicated in processes as disparate as leptin control of energy homeostasis (16) and modulation of intestinal inflam- he eight members of the suppressor of cytokine signaling mation (17). One report on mice lacking SOCS3 described Tfamily of proteins (SOCS1 to -7 and CIS) are characterized embryonic lethality with marked erythrocytosis (18). The au- by the presence of a centrally located Src homology 2 (SH2) thors concluded that SOCS3 is an essential physiological regu- domain, an N-terminal domain of variable length and divergent lator of EPO signaling, a model supported by the occurrence of sequence, and a conserved C-terminal SOCS box domain (1). lethal anemia in transgenic mice constitutively expressing SOCS1 to -3 and CIS have been shown to participate in a SOCS3 (18) and by data showing that SOCS3 binds to and negative feedback loop to regulate cytokine signaling, particu- inhibits signaling from the EPO receptor (6). larly from the hematopoietin class of cytokine receptors (2). In this study, we have independently generated mice lacking Signaling is initiated on cytokine-dependent receptor aggrega- a functional SOCS3 gene. We show that the death of SOCS3Ϫ/Ϫ tion, which activates Janus kinases (JAKs), resulting in tyrosine mice at mid-gestation is not linked to defects in the embryo but phosphorylation of the receptor as well as other signaling is associated with abnormalities in specific regions of the pla- proteins. Additional signaling molecules, such as the signal centa. The nature of these defects and our demonstration that transducers and activators of transcription (STATs) are subse- SOCS3 is expressed at these placental sites suggests that lethality quently activated via recruitment to specific receptor phospho- in SOCS3Ϫ/Ϫ mice results from placental insufficiency. In con- tyrosines (3). trast to the previous study, we found no evidence of defective The SOCS proteins modulate signal transduction by inhibiting erythropoiesis in SOCS3Ϫ/Ϫ mice. components of the JAK͞STAT pathway. Whereas SOCS1 is thought to directly bind the JAK kinases and inhibit their Materials and Methods catalytic activity, CIS appears to act by binding to the receptor, Generation of Targeted Embryonic Stem Cells and Mutant Mice. A preventing recruitment and activation of STATs (reviewed in 3-kb PCR product extending 5Ј from the SOCS3 ATG initiation ref. 2). Recent evidence suggests that SOCS3 action shares codon and a 4.3-kb XbaI-XhoI3Ј SOCS3 fragment (Fig. 1) were aspects of both these mechanisms. Studies of signaling from the GH receptor (GHR; ref. 4), IL-2 receptor beta chain (IL2R␤; ref. 5), erythropoietin receptor (EPOR; ref. 6), and gp130 (7, 8) Abbreviations: SOCS3, suppressor of cytokine signaling 3; BFU-E, blast forming unit- suggest that, whereas SOCS3 expression leads to inhibition of erythroid; CFU-E, colony forming unit-erythroid; STAT, signal transducer and activator of transcription; JAK, Janus kinase; EPO, erythropoietin; SCF, stem cell factor; E, day of JAK kinase activity, SOCS3 does not bind to JAKs with high gestation; CFC, colony-forming units. affinity and depends on the presence of cytokine receptor for ‡To whom reprint requests should be addressed. E-mail: [email protected]. this action. The emerging model suggests that SOCS3 relies on The publication costs of this article were defrayed in part by page charge payment. This interaction with the activated receptor for recruitment to the article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. signaling complex, providing access to the JAK kinases, the §1734 solely to indicate this fact. 9324–9329 ͉ PNAS ͉ July 31, 2001 ͉ vol. 98 ͉ no. 16 www.pnas.org͞cgi͞doi͞10.1073͞pnas.161271798 Downloaded by guest on October 1, 2021 PstI chicken glyceraldehyde-3-phosphate dehydrogenase (GAPDH) fragment. Yolk Sac and Fetal Liver Cultures. We suspended 5 ϫ 103 or 104 yolk sac or fetal liver cells in 1.5% methylcellulose (Fluka) in Iscove’s modified Dulbecco’s medium (IMDM) supplemented with 20% FCS and EPO (2 units͞ml at maximal concentration) with or without IL-3 (10 ng͞ml) and stem cell factor (SCF; 100 ng͞ml). After incubation at 37°C for 7 days [blast forming unit-erythroid (BFU-E) and mixed or myeloid colonies] or 2–3 days [colony forming unit-erythroid (CFU-E)] in a humidified atmosphere of 5% CO2 in air, colonies were scored at 35-fold magnification. Histological Analysis and lacZ Staining. Embryos and placentas from timed matings of SOCS3ϩ/Ϫ mice (day of plug ϭ day 0) were fixed in a solution of 0.2% glutaraldehyde and 1% form- aldehyde, and lacZ activity was detected as described (21). Paraffin-embedded lacZ-stained embryos and placentas were serially sectioned, and alternate sections were stained with nuclear fast red or hematoxylin and eosin. Embryos were genotyped by extraction of yolk sac DNA (22) for PCR with an oligonucleotide set that allowed distinction between wild-type Fig. 1. Disruption of the SOCS3 locus by homologous recombination. (A) The and targeted SOCS3 alleles: 5Ј-CTT CAT GCC ATG ACG TCT structure of the murine SOCS3 locus is illustrated with exons as raised boxes GTG ATG C-3Ј,5Ј-GCC TTC GAG GCT GTC TGA AGA and the coding region shaded (Xb, XbaI; No, NotI; X, XhoI; RV, EcoRV; H3, TGC-3Ј, and 5Ј-GAA GCT GAC TCT AGA CGT TG-3Ј. PCR HindIII). In the targeted allele, the coding region was deleted and a cassette was performed for 30 cycles of 96°C for 30 s, 62°C for 30 s, and fusing the lacZ gene to the SOCS3 ATG and including the selectable PGKneo 72°C for 1 min before visualization of the amplification products gene was included. (B) Southern blot of genomic DNA from E11.5 embryos collected from a cross between SOCS3ϩ/Ϫ mice, including wild-type (ϩ͞ϩ), on 2% agarose gels with ethidium bromide staining. SOCS3ϩ/Ϫ, and SOCS3Ϫ/Ϫ samples. The DNA was digested with HindIII and hybridized with the 3Ј probe, which distinguishes between the targeted (9-kb) Derivation of Primary Embryonic Fibroblasts. Embryos from timed ϩ Ϫ and endogenous (20-kb) SOCS3 loci. (C) Northern blot of RNA extracted from matings of SOCS3 / mice were collected at day 11.5 of gesta- wild-type (ϩ͞ϩ), SOCS3ϩ/Ϫ, and SOCS3Ϫ/Ϫ primary embryo fibroblasts after tion (E11.5) and dissected, and the trunks were individually stimulation with IFN-␥ (ϩ) or saline (Ϫ). The blot was probed with a SOCS3 treated with trypsin before disaggregation by pipetting. The cells coding region probe followed by a GAPDH probe to confirm RNA integrity.
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