piPSC克隆猪研究
摘要
小鼠胚胎干细胞(embryonic stem, ES)在生产基因修饰小鼠方面发挥着重要作用,这些基因修饰小鼠极大促进了我们对哺乳动物的生理和病理的认识以及新药的开发。但是由于啮齿类在生理性状以及基因表达方面与人类差异较大,许多小鼠模型并不能够真正的模拟人类疾病,因此,需要与人类更为接近的大动物模型。猪在解剖学、生理学、基因表达、特别是神经系统和心血管系统方面与人类更为相似,近年来被广泛用做人类疾病动物模型,并且猪器官大小与人类相似可以作为异种器官移植的供体。但是由于在猪上缺乏真正的ES,制约了对猪基因组的修饰。目前生产基因修饰猪的主流方法是对培养的体细胞进行基因修饰后再进行体细胞核移植,来获得基因修饰克隆猪。通过该方法已经成功获得了多种转基因猪。但是由于体细胞在体外传代次数有限,同源重组效率远远低于ES(小于10-6),很难实现对基因组的定点修饰,目前只有几种基因打靶猪的报道。虽然猪ES的缺乏限制了对猪基因组的定点修饰,近年来发展起来的诱导性多能干细胞(induced pluripotent stem cell, iPSC)技术,有望为没有获得真正ES系的物种提供一种可用于基因修饰的供体细胞。目前iPSCs已经在许多物种诱导成功,小鼠iPSCs的多能性已经通过最严格的生殖系嵌合验证和四倍体嵌合验证。这些都说明小鼠iPSCs即使不能等同于ES,也已经跟ES非常相似,并且小鼠iPSCs可以通过核移植(nuclear transfer, NT)途径得到克隆小鼠。所有这些都表明iPSCs可以代替ES来实现对动物基因组的修饰。目前已有多个实验室报道成功诱导出猪iPSCs(piPSCs),这些piPSCs具有正常的核型,可以在体外和体内条件下分化成三个胚层的细胞。只有一个实验室报道他们获得的piPSCs可以得到生殖系嵌合猪,但是对于piPSCs生殖系嵌合的鉴定仅仅使用了PCR技术进行鉴定,不足以令人信服。虽然这些piPSCs生殖系嵌合能力还需要进一步研究,但他们能够在长时间传代条件下维持其多能性而不衰老,因此我们可以对其在体外进行长时间的基因修饰操作,并且这些piPSCs在很多方面都与ES相似,提示其可能具有与ES相似的同源重组效率。如果piPSCs能够通过核移植技术获得克隆猪,我们就可以通过piPSCs核移植途径获得基因修饰猪,这将极大促进转基因猪的生产,特别是对于猪基因组的定点修饰。本课题对piPSCs核移植后克隆胚胎发育能力进行了研究。
用于piPSC克隆猪研究的6株piPSCs系由不同的实验室采用不同的诱导系统诱导而来。piPSCs系(iPF4-2,iPM6-11)分别由耳朵成纤维细胞(porcine ear fibroblats, PEFs)和骨髓间充质干细胞(porcine bone marrow cells, pBMCs)采用doxycycline (DOX)诱导型慢病毒载体诱导而来,诱导载体带有EGFP,这2株piPSCs均表达绿色荧光蛋白；piPSCs系(hsC-13,JN2,KSR-4,5%02-1)都是采用逆转录病毒载体系统进行诱导,其中hsC-13由猪胎儿成纤维细胞(porcine fetal fibroblasts, PFFs)诱导而来,JN2由pBMCs诱导而来,KSR-4和5%02-1由PFFs诱导而来。
为了验证piPSCs经过核移植后能否获得piPSC克隆猪,首先,我们以未经任何处理的上述六株piPSCs为供体细胞进行核移植,共构建克隆胚胎11923枚,移植代孕受体71头。其中有25头代孕受体检测到早期妊娠,但是均未获得发育到期的piPSC克隆猪。
与小鼠和人iPSCs不同的是,目前获得的这些piPSCs外源基因均未沉默,我们推测外源基因的高表达可能是导致piPSC克隆胚胎发育停滞的原因之一。我们以iPF4-2,iPM6-11,KSR-4和5%02-1作为研究对象,来进行第二轮的核移植实验。piPSCs(iPF4-2,iPM6-11)在加DOX诱导外源基因表达的情况下才能维持其iPSCs状态,撤掉DOX,以分化培养基培养四天后外源基因表达显著降低,piPSCs呈现分化状态。对于piPSCs(KSR-4,5%02-1)也进行同样的分化处理,虽然其形态已经呈分化状态,但检测其外源基因表达发现,KSR-4外源基因表达量下降不明显,5%02-1部分外源基因表达量甚至上升。KSR-4、5%02-1分化细胞中外源基因(除Sox2外)表达量均高于iPF4-2、iPM6-11分化细胞。我们以这种呈分化状态的细胞作为供体细胞进行核移植,其体外发育囊胚率较以未分化piPSCs为供体细胞时有显著提高。
为了进一步验证piPSCs分化细胞克隆胚胎体内发育能力,我们将KSR-4分化细胞克隆胚胎545枚移植于3头代孕受体,其中早期怀孕2头,但均未发育到期。将iPF4-2分化后核移植胚胎1135枚移植代孕受体7头,3头怀孕。对其中一头妊娠受体在36d进行剖腹手术,得到2个形态发育正常的克隆胎儿,这两个胎儿器官和细胞均表达EGFP,说明其为piPSCs,iPF4-2克隆而来。iPF4-2分化细胞克隆胚胎可以正常发育到36d。其余两头怀孕受体,其中一头在妊娠113天自然分娩,产下发育到期克隆猪一头,但是出生后立即死亡。为了防止再度发生自然分娩出生过程死亡现象,我们对另外一头受体,在妊娠114天时进行剖腹产手术,获得了一头健康存活的克隆猪,这头克隆猪存活了32天。我们获得的这两头克隆猪的皮肤均为白色,与piPSCs来源细胞猪(Danish Landrace)肤色相同,不同于受体太湖猪(黑色),并且从这两头克隆猪分离的PEFs都有EGFP表达,初步说明这两头发育到期的克隆猪为piPSCs,iPF4-2克隆而来。为了进一步确定其piPSC克隆猪的身份,我们对36天克隆胎儿和发育到期的两头克隆猪进行了外源基因整合鉴定和微卫星序列分析,结果均表明他们都是由iPF4-2克隆而来。
为了探明piPSC克隆猪死亡原因,我们对第一头piPSC克隆猪主要器官进行病理切片分析,未发现明显病变,各器官结构发育正常,肺泡内发现着色现象,可能是由于分娩过程中羊水呛入肺中,导致死亡。第二头piPSC克隆猪死亡原因病理分析结果为脑脊髓膜炎。这两头piPSC克隆猪器官发育均正常,死亡原因并不是由于piPSC克隆猪本身存在器官发育缺陷,这说明piPSCs是可以通过核移植途径获得发育正常克隆猪的。
我们以DOX诱导型慢病毒载体系统诱导的piPSCs为供体细胞成功获得了首例piPSC克隆猪,该系统通过撤掉DOX可以快速有效的实现外源基因的沉默,这可能是我们能够获得发育到期存活piPSC克隆猪的原因。piPSC克隆猪的成功,为实现以piPSCs为基础的基因修饰猪的生产初步打通了技术路线。由于外源基未沉默可能是piPSC克隆猪失败的原因,所以未来需要研究获得外源基因沉默或者无外源基因整合的piPSCs。
Mouse embryonic stem (ES) cells have proven powerful in the generation of precisely genetically modified animals that can advance our knowledge of mammalian physiology and disease. In recent years, genetically modified pigs have also been produced by means of somatic cell nuclear transfer (NT). Pigs provide outstanding models for modeling human genetic diseases due to the striking similarities with human anatomy, physiology, and genetics. Yet, progress with porcine genetic engineering has been hampered by the lack of germline-competent pig ES cells. Somatic cells exhibit limited proliferation and have an extremely low frequency of homologous recombination (less than10) compared to ES cells. Hence, only a few knockout pig models have been reported thus far.
Remarkably, induced pluripotent stem cells (iPSCs) have been generated by the reprogramming of somatic cells from multiple mammalian species using defined cocktails of transcription factors. Mouse iPSCs have passed the crucial test of germ line contribution and generation of all-iPSCs mice through tetraploid embryo complementation. This indicates that bona fide iPSCs are, if not identical, very similar to ES cells. Likewise, cloned mice have been obtained from mouse iPSCs by the NT method. These studies indicate that iPSCs can substitute ES cells for the purpose of genomic manipulation.
Pig iPSCs (piPSCs) have been reported by several groups. These piPSC lines could be differentiated into the three germ layers in vitro and in vivo. Only one group reported the piPSCs they generated could pass the crucial test of germ line chimera production, but the germ line chimera was detected only by PCR analysis that was not convinced. More research should be done to obtain germline-competence piPSCs. Nevertheless, piPSCs are capable of long-term proliferation, which potentially allows lengthier and therefore potentially more sophisticated in vitro manipulation. More importantly, they are similar to ES cells in many aspects, suggesting that they may have as well high efficiency of homologous recombination. Hence, if iPSCs were suitable for cloning pigs by NT, gene-targeted pigs could potentially be produced much more efficiently than using fibroblasts as nuclear donors. In the present study, we explored the feasibility of generating cloned pigs from piPSCs.
We used piPSC lines generated by different groups using various strategies. The first2piPSC lines, iPF4-2and iPM6-11, were induced from porcine ear fibroblasts (PEFs) and porcine bone marrow cells (pBMCs), respectively, of a10-week-old Danish Landrace pig using lentiviral vector over-expressing human transcription factors induced with doxycycline (DOX). The third piPSC line, hsC13, was induced from porcine fetal fibroblasts (PFFs) by retroviral over-expression of human transcription factors. The last3piPSC lines (JN2, KSR-4, and5%O2-1) were produced by retroviral over-expression of mouse or porcine transcription factors into pBMCs or PFFs.
In the first round of NT experiments, we used undifferentiated piPSCs as donor cells and transferred the nuclei into enucleated metaphase Ⅱ (MⅡ) oocytes by the electrical fusion method. A total of11923cloned embryos reconstructed with the6piPSC lines were introduced into71surrogate mothers. Among these mothers,25were pregnant as detected by ultrasonography on day24-26following embryo transfer, but none of them developed to term. These results were disappointing considering that mouse iPSCs have been successfully used as donor cells for creating living cloned mice. We then hypothesized that inappropriate silencing of the exogenous transcription genes in the piPSCs may underlie the discrepancy. To test this hypothesis, we performed a second round of experiments, this time using piPSCs that were allowed to spontaneously differentiate for4-6days as donor cells. For this we focused on iPF4-2, iPM6-11, KSR-4and5%O2-1. After spontaneous differentiation, piPSCs became enlarged and flattened, and developed an epithelium-like morphology. For iPF4-2and iPM6-11, all the exogenous were reduced significantly after differentiation. On the other hand, the expression level of all4exogenous genes in KSR-4differentiated cells did not decrease significantly as in iPF4-2and iPM6-11. Some of the exogenous genes in5%O2-1differentiated cells even expressed at a higher level compared to the undifferentiated one. Except for Sox2, the expression level of extrogenous genes was higher in KSR-4and5%O2-1differentiated cells than in iPF4-2and iPM6-11differentiated ones.
The differentiated piPSCs were transferred into enucleated MⅡ oocytes, and it was encouraging to observe that the resulting NT embryos had a significantly increased rate of blastocyst development compared to undifferentiated cells. Reconstructed embryos derived from differentiated iPF4-2and KSR-4cells were transferred into surrogate mothers. A total of545cloned embryos from KSR-4differentiated cells were transferred into3surrogates,2of whom became pregnant but lost their pregnancy between days35to50. A total of1135iPF4-2differentiated cell-NT embryos were transferred into7recipient surrogate mothers,3of whom became pregnant. To detect the early development of the cloned fetuses, one pregnant surrogate was sacrificed after36days of gestation, and2fetuses were retrieved by caesarean section. The2cloned fetuses were morphologically normal and the corresponding fetal fibroblasts grew normally and were positive for EGFP, a maker in iPF4-2. After113days of gestation,1of the pregnant surrogates using iPF4-2cells naturally delivered a piglet and a mummy. But the piglet died within the first hour after birth. The other pregnant surrogate using iPF4-2cells gave cesarean birth to a live and healthy cloned pig after114days of gestation. This piglet survived for32days. Both piglets had a white coat resembling the coat color of the pig (Danish Landrace) from which piPSCs, iPF4-2were derived. The fibroblasts isolated from the2piglets were both positive for EGFP. To further confirm that the fetuses and piglets were generated from iPF4-2piPSCs, we analyzed Oct4, Sox2, and EGFP transgene integration, as well as microsatellite DNA. Tissues from the2fetuses and born piglets contained the exogenous transgenes, as demonstrated by PCR. Analysis of microsatellite DNA revealed as well that the genomes of the fetuses and piglets were the same as iPF4-2cells, but different from the surrogate. These findings proved that the piglets were cloned from the piPSCs.
In order to investigate the cause of death and the organ development status, pathological section was performed. All the investigated organs of the piglets died at birth showed normal morphology, and the cause of death was unclear. Some mniotic fluid got into pulmonary alveoli that maybe cause the death. Pathological section analysis indicated the cause of piglets died at32day was Myeloencephalitis. Organs of the two piPSC cloned piglets showed normal morphology. The death was not caused by inherent organ developmental defects of piPSC cloned piglets that meant normal development piglets could be cloned from piPSCs.
In summary, here we have described the generation of live piPSC-NT piglets from a piPSC line established with a DOX-induced system. This system allows controllable silencing of the exogenous genes and may explain why the NT failed using dedifferentiated piPSCs. The generation of live piglets from piPSCs by NT potentially represents an important step toward a more efficient production of genetically engineered pigs using piPSCs. The latter may facilitate the more generalized use of pigs for human disease modeling and potentially also for agriculture.
用于piPSC克隆猪研究的6株piPSCs系由不同的实验室采用不同的诱导系统诱导而来。piPSCs系(iPF4-2,iPM6-11)分别由耳朵成纤维细胞(porcine ear fibroblats, PEFs)和骨髓间充质干细胞(porcine bone marrow cells, pBMCs)采用doxycycline (DOX)诱导型慢病毒载体诱导而来,诱导载体带有EGFP,这2株piPSCs均表达绿色荧光蛋白；piPSCs系(hsC-13,JN2,KSR-4,5%02-1)都是采用逆转录病毒载体系统进行诱导,其中hsC-13由猪胎儿成纤维细胞(porcine fetal fibroblasts, PFFs)诱导而来,JN2由pBMCs诱导而来,KSR-4和5%02-1由PFFs诱导而来。
为了验证piPSCs经过核移植后能否获得piPSC克隆猪,首先,我们以未经任何处理的上述六株piPSCs为供体细胞进行核移植,共构建克隆胚胎11923枚,移植代孕受体71头。其中有25头代孕受体检测到早期妊娠,但是均未获得发育到期的piPSC克隆猪。
与小鼠和人iPSCs不同的是,目前获得的这些piPSCs外源基因均未沉默,我们推测外源基因的高表达可能是导致piPSC克隆胚胎发育停滞的原因之一。我们以iPF4-2,iPM6-11,KSR-4和5%02-1作为研究对象,来进行第二轮的核移植实验。piPSCs(iPF4-2,iPM6-11)在加DOX诱导外源基因表达的情况下才能维持其iPSCs状态,撤掉DOX,以分化培养基培养四天后外源基因表达显著降低,piPSCs呈现分化状态。对于piPSCs(KSR-4,5%02-1)也进行同样的分化处理,虽然其形态已经呈分化状态,但检测其外源基因表达发现,KSR-4外源基因表达量下降不明显,5%02-1部分外源基因表达量甚至上升。KSR-4、5%02-1分化细胞中外源基因(除Sox2外)表达量均高于iPF4-2、iPM6-11分化细胞。我们以这种呈分化状态的细胞作为供体细胞进行核移植,其体外发育囊胚率较以未分化piPSCs为供体细胞时有显著提高。
为了进一步验证piPSCs分化细胞克隆胚胎体内发育能力,我们将KSR-4分化细胞克隆胚胎545枚移植于3头代孕受体,其中早期怀孕2头,但均未发育到期。将iPF4-2分化后核移植胚胎1135枚移植代孕受体7头,3头怀孕。对其中一头妊娠受体在36d进行剖腹手术,得到2个形态发育正常的克隆胎儿,这两个胎儿器官和细胞均表达EGFP,说明其为piPSCs,iPF4-2克隆而来。iPF4-2分化细胞克隆胚胎可以正常发育到36d。其余两头怀孕受体,其中一头在妊娠113天自然分娩,产下发育到期克隆猪一头,但是出生后立即死亡。为了防止再度发生自然分娩出生过程死亡现象,我们对另外一头受体,在妊娠114天时进行剖腹产手术,获得了一头健康存活的克隆猪,这头克隆猪存活了32天。我们获得的这两头克隆猪的皮肤均为白色,与piPSCs来源细胞猪(Danish Landrace)肤色相同,不同于受体太湖猪(黑色),并且从这两头克隆猪分离的PEFs都有EGFP表达,初步说明这两头发育到期的克隆猪为piPSCs,iPF4-2克隆而来。为了进一步确定其piPSC克隆猪的身份,我们对36天克隆胎儿和发育到期的两头克隆猪进行了外源基因整合鉴定和微卫星序列分析,结果均表明他们都是由iPF4-2克隆而来。
为了探明piPSC克隆猪死亡原因,我们对第一头piPSC克隆猪主要器官进行病理切片分析,未发现明显病变,各器官结构发育正常,肺泡内发现着色现象,可能是由于分娩过程中羊水呛入肺中,导致死亡。第二头piPSC克隆猪死亡原因病理分析结果为脑脊髓膜炎。这两头piPSC克隆猪器官发育均正常,死亡原因并不是由于piPSC克隆猪本身存在器官发育缺陷,这说明piPSCs是可以通过核移植途径获得发育正常克隆猪的。
我们以DOX诱导型慢病毒载体系统诱导的piPSCs为供体细胞成功获得了首例piPSC克隆猪,该系统通过撤掉DOX可以快速有效的实现外源基因的沉默,这可能是我们能够获得发育到期存活piPSC克隆猪的原因。piPSC克隆猪的成功,为实现以piPSCs为基础的基因修饰猪的生产初步打通了技术路线。由于外源基未沉默可能是piPSC克隆猪失败的原因,所以未来需要研究获得外源基因沉默或者无外源基因整合的piPSCs。
Mouse embryonic stem (ES) cells have proven powerful in the generation of precisely genetically modified animals that can advance our knowledge of mammalian physiology and disease. In recent years, genetically modified pigs have also been produced by means of somatic cell nuclear transfer (NT). Pigs provide outstanding models for modeling human genetic diseases due to the striking similarities with human anatomy, physiology, and genetics. Yet, progress with porcine genetic engineering has been hampered by the lack of germline-competent pig ES cells. Somatic cells exhibit limited proliferation and have an extremely low frequency of homologous recombination (less than10) compared to ES cells. Hence, only a few knockout pig models have been reported thus far.
Remarkably, induced pluripotent stem cells (iPSCs) have been generated by the reprogramming of somatic cells from multiple mammalian species using defined cocktails of transcription factors. Mouse iPSCs have passed the crucial test of germ line contribution and generation of all-iPSCs mice through tetraploid embryo complementation. This indicates that bona fide iPSCs are, if not identical, very similar to ES cells. Likewise, cloned mice have been obtained from mouse iPSCs by the NT method. These studies indicate that iPSCs can substitute ES cells for the purpose of genomic manipulation.
Pig iPSCs (piPSCs) have been reported by several groups. These piPSC lines could be differentiated into the three germ layers in vitro and in vivo. Only one group reported the piPSCs they generated could pass the crucial test of germ line chimera production, but the germ line chimera was detected only by PCR analysis that was not convinced. More research should be done to obtain germline-competence piPSCs. Nevertheless, piPSCs are capable of long-term proliferation, which potentially allows lengthier and therefore potentially more sophisticated in vitro manipulation. More importantly, they are similar to ES cells in many aspects, suggesting that they may have as well high efficiency of homologous recombination. Hence, if iPSCs were suitable for cloning pigs by NT, gene-targeted pigs could potentially be produced much more efficiently than using fibroblasts as nuclear donors. In the present study, we explored the feasibility of generating cloned pigs from piPSCs.
We used piPSC lines generated by different groups using various strategies. The first2piPSC lines, iPF4-2and iPM6-11, were induced from porcine ear fibroblasts (PEFs) and porcine bone marrow cells (pBMCs), respectively, of a10-week-old Danish Landrace pig using lentiviral vector over-expressing human transcription factors induced with doxycycline (DOX). The third piPSC line, hsC13, was induced from porcine fetal fibroblasts (PFFs) by retroviral over-expression of human transcription factors. The last3piPSC lines (JN2, KSR-4, and5%O2-1) were produced by retroviral over-expression of mouse or porcine transcription factors into pBMCs or PFFs.
In the first round of NT experiments, we used undifferentiated piPSCs as donor cells and transferred the nuclei into enucleated metaphase Ⅱ (MⅡ) oocytes by the electrical fusion method. A total of11923cloned embryos reconstructed with the6piPSC lines were introduced into71surrogate mothers. Among these mothers,25were pregnant as detected by ultrasonography on day24-26following embryo transfer, but none of them developed to term. These results were disappointing considering that mouse iPSCs have been successfully used as donor cells for creating living cloned mice. We then hypothesized that inappropriate silencing of the exogenous transcription genes in the piPSCs may underlie the discrepancy. To test this hypothesis, we performed a second round of experiments, this time using piPSCs that were allowed to spontaneously differentiate for4-6days as donor cells. For this we focused on iPF4-2, iPM6-11, KSR-4and5%O2-1. After spontaneous differentiation, piPSCs became enlarged and flattened, and developed an epithelium-like morphology. For iPF4-2and iPM6-11, all the exogenous were reduced significantly after differentiation. On the other hand, the expression level of all4exogenous genes in KSR-4differentiated cells did not decrease significantly as in iPF4-2and iPM6-11. Some of the exogenous genes in5%O2-1differentiated cells even expressed at a higher level compared to the undifferentiated one. Except for Sox2, the expression level of extrogenous genes was higher in KSR-4and5%O2-1differentiated cells than in iPF4-2and iPM6-11differentiated ones.
The differentiated piPSCs were transferred into enucleated MⅡ oocytes, and it was encouraging to observe that the resulting NT embryos had a significantly increased rate of blastocyst development compared to undifferentiated cells. Reconstructed embryos derived from differentiated iPF4-2and KSR-4cells were transferred into surrogate mothers. A total of545cloned embryos from KSR-4differentiated cells were transferred into3surrogates,2of whom became pregnant but lost their pregnancy between days35to50. A total of1135iPF4-2differentiated cell-NT embryos were transferred into7recipient surrogate mothers,3of whom became pregnant. To detect the early development of the cloned fetuses, one pregnant surrogate was sacrificed after36days of gestation, and2fetuses were retrieved by caesarean section. The2cloned fetuses were morphologically normal and the corresponding fetal fibroblasts grew normally and were positive for EGFP, a maker in iPF4-2. After113days of gestation,1of the pregnant surrogates using iPF4-2cells naturally delivered a piglet and a mummy. But the piglet died within the first hour after birth. The other pregnant surrogate using iPF4-2cells gave cesarean birth to a live and healthy cloned pig after114days of gestation. This piglet survived for32days. Both piglets had a white coat resembling the coat color of the pig (Danish Landrace) from which piPSCs, iPF4-2were derived. The fibroblasts isolated from the2piglets were both positive for EGFP. To further confirm that the fetuses and piglets were generated from iPF4-2piPSCs, we analyzed Oct4, Sox2, and EGFP transgene integration, as well as microsatellite DNA. Tissues from the2fetuses and born piglets contained the exogenous transgenes, as demonstrated by PCR. Analysis of microsatellite DNA revealed as well that the genomes of the fetuses and piglets were the same as iPF4-2cells, but different from the surrogate. These findings proved that the piglets were cloned from the piPSCs.
In order to investigate the cause of death and the organ development status, pathological section was performed. All the investigated organs of the piglets died at birth showed normal morphology, and the cause of death was unclear. Some mniotic fluid got into pulmonary alveoli that maybe cause the death. Pathological section analysis indicated the cause of piglets died at32day was Myeloencephalitis. Organs of the two piPSC cloned piglets showed normal morphology. The death was not caused by inherent organ developmental defects of piPSC cloned piglets that meant normal development piglets could be cloned from piPSCs.
In summary, here we have described the generation of live piPSC-NT piglets from a piPSC line established with a DOX-induced system. This system allows controllable silencing of the exogenous genes and may explain why the NT failed using dedifferentiated piPSCs. The generation of live piglets from piPSCs by NT potentially represents an important step toward a more efficient production of genetically engineered pigs using piPSCs. The latter may facilitate the more generalized use of pigs for human disease modeling and potentially also for agriculture.
引文
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