Roles of interferon-stimulated gene 15 protein in bovine embryo development
Shuan Zhao A B , Yi Wu C , Hui Gao A , Alexander Evans D and Shen-Ming Zeng A E
+ Author Affiliations
- Author Affiliations
A College of Animal Science and Technology, Yangzhou University, 225009, Jiangsu, China.
B Department of Biochemistry, School of Life Sciences, Fudan University, Shanghai, 200438, China.
C Development of Laboratory Animal Science, School of Basic Medical Science, Capital Medical University, 100069, Beijing, China.
D School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland,
E Corresponding author. Email: zengshenming@gmail.com
Reproduction, Fertility and Development 29(6) 1209-1216 https://doi.org/10.1071/RD15209
Submitted: 28 May 2015 Accepted: 25 March 2016 Published: 11 May 2016
Abstract
Interferon (IFN)-stimulated gene 15 (ISG15) is one of several proteins induced by conceptus-derived Type I or II IFNs in the uterus, and is implicated as an important factor in determining uterine receptivity to embryos in ruminants. But little is known about the role the ISG15 gene or gene product plays during embryo development. In the present study, both the expression profile and function of ISG15 were investigated in early bovine embryos in vitro. ISG15 mRNA was detectable in Day 0, 2, 6 and 8 bovine embryos, but IFN-τ (IFNT) mRNA only appeared from Day 6. This means that embryonic expression of ISG15 on Days 0 and 2 was not induced by embryonic IFNT. However, ISG15 mRNA expression paralleled the expression of IFNT mRNA in Day 6 and 8 embryos. ISG15–lentivirus interference plasmid (ISG15i) was injected into 2-cell embryos to knockdown ISG15 expression. This resulted in decreases in the proportion of hatching blastocysts, the diameter of blastocysts and cell number per diameter of blastocysts compared with control embryos. In addition, ISG15i inhibited IFNT, Ets2 (E26 oncogene homolog 2) mRNA and connexion 43 protein expression in Day 8 blastocysts, whereas exogenous IFNT treatment (100 ng mL–1, from Day 4 to Day 8) improved ISG15 mRNA and connexion 43 protein expression. In conclusion, it appears that ISG15 is involved in early bovine embryo development and that it regulates IFNT expression in the blastocyst.
Additional keywords: blastocyst, interferon-stimulated gene 15 (ISG15) knockdown, interferon-τ (IFNT).
References
Ashley, R. L., Henkes, L. E., Bouma, G. J., Pru, J. K., and Hansen, T. R. (2010). Deletion of the Isg15 gene results in up-regulation of decidual cell survival genes and down-regulation of adhesion genes: implication for regulation by IL-1beta. Endocrinology 151, 4527–4536.| Deletion of the Isg15 gene results in up-regulation of decidual cell survival genes and down-regulation of adhesion genes: implication for regulation by IL-1beta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtF2qtrvE&md5=fa91480bd1c651fbd1e8aa231b52c5e8CAS | 20660068PubMed |
Austin, K. J., Ward, S. K., Teixeira, M. G., Dean, V. C., Moore, D. W., and Hansen, T. R. (1996). Ubiquitin cross-reactive protein is released by the bovine uterus in response to interferon during early pregnancy. Biol. Reprod. 54, 600–606.
| Ubiquitin cross-reactive protein is released by the bovine uterus in response to interferon during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtFCjt7Y%3D&md5=997ea5979a1478613c226bd106e500e8CAS | 8835381PubMed |
Austin, K. J., Bany, B. M., Belden, E. L., Rempel, L. A., Cross, J. C., and Hansen, T. R. (2003). Interferon-stimulated gene-15 (Isg15) expression is up-regulated in the mouse uterus in response to the implanting conceptus. Endocrinology 144, 3107–3113.
| Interferon-stimulated gene-15 (Isg15) expression is up-regulated in the mouse uterus in response to the implanting conceptus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvF2ktLo%3D&md5=05000d9470254fcfe7d13e3ad87d7f87CAS | 12810567PubMed |
Austin, K. J., Carr, A. L., Pru, J. K., Hearne, C. E., George, E. L., Belden, E. L., and Hansen, T. R. (2004). Localization of ISG15 and conjugated proteins in bovine endometrium using immunohistochemistry and electron microscopy. Endocrinology 145, 967–975.
| Localization of ISG15 and conjugated proteins in bovine endometrium using immunohistochemistry and electron microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovFSktA%3D%3D&md5=7f23a5996599ce5c1603c4374e724f21CAS | 14563704PubMed |
Bao, Z. J., Zhao, S., Haq, I. U., and Zeng, S. M. (2014). Recombinant bovine interferon-tau enhances in vitro development of bovine embryos by upregulating expression of connexin 43 and E-cadherin. J. Dairy Sci. 97, 6917–6925.
| Recombinant bovine interferon-tau enhances in vitro development of bovine embryos by upregulating expression of connexin 43 and E-cadherin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFylur%2FF&md5=2dc2c7a16fc7f9002a30d7ffc54cbdadCAS | 25242422PubMed |
Bazer, F. W., and Johnson, H. M. (1991). Type I conceptus interferons: maternal recognition of pregnancy signals and potential therapeutic agents. Am. J. Reprod. Immunol. 26, 19–22.
| Type I conceptus interferons: maternal recognition of pregnancy signals and potential therapeutic agents.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2FnsFWgsw%3D%3D&md5=98aa37ec029334e4a0e4b82548f8b234CAS | 1741934PubMed |
Bebington, C., Bell, S. C., Doherty, F. J., Fazleabas, A. T., and Fleming, S. D. (1999a). Localization of ubiquitin and ubiquitin cross-reactive protein in human and baboon endometrium and decidua during the menstrual cycle and early pregnancy. Biol. Reprod. 60, 920–928.
| Localization of ubiquitin and ubiquitin cross-reactive protein in human and baboon endometrium and decidua during the menstrual cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitVGqsbg%3D&md5=b1e7bdc76bad79627aaa192c0bb99b49CAS | 10084967PubMed |
Bebington, C., Doherty, F. J., and Fleming, S. D. (1999b). Ubiquitin cross-reactive protein gene expression is increased in decidualized endometrial stromal cells at the initiation of pregnancy. Mol. Hum. Reprod. 5, 966–972.
| Ubiquitin cross-reactive protein gene expression is increased in decidualized endometrial stromal cells at the initiation of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFaguro%3D&md5=43c0f5e4ba9d00de0d798cf7dc830d20CAS | 10508226PubMed |
Brackett, B. G., and Oliphant, G. (1975). Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12, 260–274.
| Capacitation of rabbit spermatozoa in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28Xnt1WltQ%3D%3D&md5=8bdb4d5b8aa38c3c50168ef421c41016CAS | 1122333PubMed |
Dao, C. T., and Zhang, D. E. (2005). ISG15: a ubiquitin-like enigma. Front. Biosci. 10, 2701–2722.
| ISG15: a ubiquitin-like enigma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntFGisLo%3D&md5=7b69faed654dfe76b614ba1d1bae1660CAS | 15970528PubMed |
Desai, S. D., Haas, A. L., Wood, L. M., Tsai, Y. C., Pestka, S., Rubin, E. H., Saleem, A., Nur, E. K. A., and Liu, L. F. (2006). Elevated expression of ISG15 in tumor cells interferes with the ubiquitin/26S proteasome pathway. Cancer Res. 66, 921–928.
| Elevated expression of ISG15 in tumor cells interferes with the ubiquitin/26S proteasome pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlsFOqtA%3D%3D&md5=d30aed8956b1123bcbe639eac906fdb2CAS | 16424026PubMed |
Ezashi, T., Ealy, A. D., Ostrowski, M. C., and Roberts, R. M. (1998). Control of interferon-tau gene expression by Ets-2. Proc. Natl Acad. Sci. USA 95, 7882–7887.
| Control of interferon-tau gene expression by Ets-2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXks1SnsL0%3D&md5=ba72f96d07f1a1f8aab71a9b1bda6bb7CAS | 9653109PubMed |
Farrell, P. J., Broeze, R. J., and Lengyel, P. (1979). Accumulation of an mRNA and protein in interferon-treated Ehrlich ascites tumour cells. Nature 279, 523–525.
| Accumulation of an mRNA and protein in interferon-treated Ehrlich ascites tumour cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksFCh&md5=872074558e10f43083e7318bbd933dccCAS | 571963PubMed |
Ghosh, D., Ezashi, T., Ostrowski, M. C., and Roberts, R. M. (2003). A central role for Ets-2 in the transcriptional regulation and cyclic adenosine 5′-monophosphate responsiveness of the human chorionic gonadotropin-beta subunit gene. Mol. Endocrinol. 17, 11–26.
| A central role for Ets-2 in the transcriptional regulation and cyclic adenosine 5′-monophosphate responsiveness of the human chorionic gonadotropin-beta subunit gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtFOhsQ%3D%3D&md5=22e570d2a8beff67c2d7e23e514f3c2dCAS | 12511603PubMed |
Haas, A. L., Ahrens, P., Bright, P. M., and Ankel, H. (1987). Interferon induces a 15-kilodalton protein exhibiting marked homology to ubiquitin. J. Biol. Chem. 262, 11 315–11 323.
| 1:CAS:528:DyaL2sXltlagtb8%3D&md5=2ac502fa29615458eddd6d1aaf7994b6CAS |
Han, C. S., Mathialagan, N., Klemann, S. W., and Roberts, R. M. (1997). Molecular cloning of ovine and bovine type I interferon receptor subunits from uteri, and endometrial expression of messenger ribonucleic acid for ovine receptors during the estrous cycle and pregnancy. Endocrinology 138, 4757–4767.
| 1:CAS:528:DyaK2sXmslGrt7o%3D&md5=9ff10ef467adf61683780f293b81b688CAS | 9348203PubMed |
Hsiang, T. Y., Zhao, C., and Krug, R. M. (2009). Interferon-induced ISG15 conjugation inhibits influenza A virus gene expression and replication in human cells. J. Virol. 83, 5971–5977.
| Interferon-induced ISG15 conjugation inhibits influenza A virus gene expression and replication in human cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFWqt7c%3D&md5=2589f4861a2d6a37ac7a790bdfa89df3CAS | 19357168PubMed |
Johnson, W., and Jameson, J. L. (2000). Role of Ets2 in cyclic AMP regulation of the human chorionic gonadotropin beta promoter. Mol. Cell. Endocrinol. 165, 17–24.
| Role of Ets2 in cyclic AMP regulation of the human chorionic gonadotropin beta promoter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFCjs78%3D&md5=e7a7c8381c38cce784769b54a24ca878CAS | 10940479PubMed |
Johnson, G. A., Austin, K. J., Van Kirk, E. A., and Hansen, T. R. (1998). Pregnancy and interferon-tau induce conjugation of bovine ubiquitin cross-reactive protein to cytosolic uterine proteins. Biol. Reprod. 58, 898–904.
| Pregnancy and interferon-tau induce conjugation of bovine ubiquitin cross-reactive protein to cytosolic uterine proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXit1Khsbg%3D&md5=f5bb92d40bee75044ec574b193802a71CAS | 9546718PubMed |
Johnson, G. A., Austin, K. J., Collins, A. M., Murdoch, W. J., and Hansen, T. R. (1999a). Endometrial ISG17 mRNA and a related mRNA are induced by interferon-tau and localized to glandular epithelial and stromal cells from pregnant cows. Endocrine 10, 243–252.
| Endometrial ISG17 mRNA and a related mRNA are induced by interferon-tau and localized to glandular epithelial and stromal cells from pregnant cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlt1Ols78%3D&md5=30bbcb790fe4f3ec88678c179017b48cCAS | 10484288PubMed |
Johnson, G. A., Spencer, T. E., Hansen, T. R., Austin, K. J., Burghardt, R. C., and Bazer, F. W. (1999b). Expression of the interferon tau inducible ubiquitin cross-reactive protein in the ovine uterus. Biol. Reprod. 61, 312–318.
| Expression of the interferon tau inducible ubiquitin cross-reactive protein in the ovine uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktFKnsrg%3D&md5=91c397638191f432eba495d1fc50d632CAS | 10377064PubMed |
Klein, C., Scoggin, K. E., and Troedsson, M. H. (2011). The expression of interferon-stimulated gene 15 in equine endometrium. Reprod. Domest. Anim. 46, 692–698.
| The expression of interferon-stimulated gene 15 in equine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2hsL3N&md5=6ff3cf11fa14373318339dd88066c5c4CAS | 21241378PubMed |
Künzi, M. S., and Pitha, P. M. (1996). Role of interferon-stimulated gene ISG-15 in the interferon-omega-mediated inhibition of human immunodeficiency virus replication. J. Interferon Cytokine Res. 16, 919–927.
| Role of interferon-stimulated gene ISG-15 in the interferon-omega-mediated inhibition of human immunodeficiency virus replication.Crossref | GoogleScholarGoogle Scholar | 8938567PubMed |
Licht, J. D. (2001). AML1 and the AML1-ETO fusion protein in the pathogenesis of t(8;21) AML. Oncogene 20, 5660–5679.
| AML1 and the AML1-ETO fusion protein in the pathogenesis of t(8;21) AML.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt12gtbw%3D&md5=50455986cc3fc76367e25cc06a53f60eCAS | 11607817PubMed |
Liu, L. Q., Ilaria, R., Kingsley, P. D., Iwama, A., van Etten, R. A., Palis, J., and Zhang, D. E. (1999). A novel ubiquitin-specific protease, UBP43, cloned from leukemia fusion protein AML1-ETO-expressing mice, functions in hematopoietic cell differentiation. Mol. Cell. Biol. 19, 3029–3038.
| A novel ubiquitin-specific protease, UBP43, cloned from leukemia fusion protein AML1-ETO-expressing mice, functions in hematopoietic cell differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXit1altLw%3D&md5=82ab6a94389827cea8e4446f53549151CAS | 10082570PubMed |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT Method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT Method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=3d53b7f31b0c4fa91bfc79f22f87effaCAS | 11846609PubMed |
Loeb, K. R., and Haas, A. L. (1992). The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins. J. Biol. Chem. 267, 7806–7813.
| 1:CAS:528:DyaK38XktVGku7g%3D&md5=02da77d4431539d7e85e0c693abd9dffCAS | 1373138PubMed |
Malakhov, M. P., Kim, K. I., Malakhova, O. A., Jacobs, B. S., Borden, E. C., and Zhang, D. E. (2003). High-throughput immunoblotting. Ubiquitiin-like protein ISG15 modifies key regulators of signal transduction. J. Biol. Chem. 278, 16 608–16 613.
| High-throughput immunoblotting. Ubiquitiin-like protein ISG15 modifies key regulators of signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVKnsb4%3D&md5=edf78b539dfe9d9f379a4eb9d24840eaCAS |
Malakhova, O., Malakhov, M., Hetherington, C., and Zhang, D. E. (2002). Lipopolysaccharide activates the expression of ISG15-specific protease UBP43 via interferon regulatory factor 3. J. Biol. Chem. 277, 14 703–14 711.
| Lipopolysaccharide activates the expression of ISG15-specific protease UBP43 via interferon regulatory factor 3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjslSgs7k%3D&md5=e5ea8c94ef19f9285ba84352c9681a25CAS |
Mémet, S., Besançon, F., Bourgeade, M. F., and Thang, M. N. (1991). Direct induction of interferon-gamma- and interferon-alpha/beta-inducible genes by double-stranded RNA. J. Interferon Res. 11, 131–141.
| Direct induction of interferon-gamma- and interferon-alpha/beta-inducible genes by double-stranded RNA.Crossref | GoogleScholarGoogle Scholar | 1919073PubMed |
Paradis, F., Vigneault, C., Robert, C., and Sirard, M.-A. (2005). RNA interference as a tool to study gene function in bovine oocytes. Mol. Reprod. Dev. 70, 111–121.
| RNA interference as a tool to study gene function in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltlSksw%3D%3D&md5=4a4706f1ad61606ec0d2680a107192d2CAS | 15570624PubMed |
Recht, M., Borden, E. C., and Knight, E. (1991). A human 15-kDa IFN-induced protein induces the secretion of IFN-gamma. J. Immunol. 147, 2617–2623.
| 1:CAS:528:DyaK38XkvF2i&md5=d04a7bd60a245ecbe255d5d55d4c8123CAS | 1717569PubMed |
Ritchie, K. J., Hahn, C. S., Kim, K. I., Yan, M., Rosario, D., Li, L., de la Torre, J. C., and Zhang, D. E. (2004). Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat. Med. 10, 1374–1378.
| Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVCisbfI&md5=1932c3c1601ec452250231d3ff0d7f16CAS | 15531891PubMed |
Roberts, R. M., Cross, J. C., Farin, C. E., Hansen, T. R., Klemann, S. W., and Imakawa, K. (1990). Interferons at the placental interface. J. Reprod. Fertil. Suppl. 41, 63–74.
| 1:CAS:528:DyaK3MXmt12lu7g%3D&md5=4aa42783798f5f0d6fff9a25392c4c0dCAS | 2213717PubMed |
Robinson, R. S., Fray, M. D., Wathes, D. C., Lamming, G. E., and Mann, G. E. (2006). In vivo expression of interferon tau mRNA by the embryonic trophoblast and uterine concentrations of interferon tau protein during early pregnancy in the cow. Mol. Reprod. Dev. 73, 470–474.
| In vivo expression of interferon tau mRNA by the embryonic trophoblast and uterine concentrations of interferon tau protein during early pregnancy in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFals74%3D&md5=85878bbb5be35d1599ad4bb04500686cCAS | 16435375PubMed |
Rosenfeld, C. S., Han, C. S., Alexenko, A. P., Spencer, T. E., and Roberts, R. M. (2002). Expression of interferon receptor subunits, IFNAR1 and IFNAR2, in the ovine uterus. Biol. Reprod. 67, 847–853.
| Expression of interferon receptor subunits, IFNAR1 and IFNAR2, in the ovine uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmsV2jsLY%3D&md5=7c2dbdaababa3eadada2cfa4b8685982CAS | 12193393PubMed |
Rosenkrans, C. F., Zeng, G. Q., McNamara, G. T., Schoff, P. K., and First, N. L. (1993). Development of bovine embryos in vitro as affected by energy substrates. Biol. Reprod. 49, 459–462.
| Development of bovine embryos in vitro as affected by energy substrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFWk&md5=d2a13ee59124ad0e172c9bea00ca2fd9CAS | 8399836PubMed |
Rozen, S., and Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365–386.
| 1:CAS:528:DyaK1MXmslKqsbo%3D&md5=1cd753cebad8c22280bc02afb139b0ccCAS | 10547847PubMed |
Sun, Y., and Duckworth, M. L. (1999). Identification of a placental-specific enhancer in the rat placental lactogen II gene that contains binding sites for members of the Ets and AP-1 (activator protein 1) families of transcription factors. Mol. Endocrinol. 13, 385–399.
| Identification of a placental-specific enhancer in the rat placental lactogen II gene that contains binding sites for members of the Ets and AP-1 (activator protein 1) families of transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhslWgsb4%3D&md5=d8882c374a4f257365a15524db6ca067CAS | 10076996PubMed |
Tesfaye, D., Regassa, A., Rings, F., Ghanem, N., Phatsara, C., Tholen, E., Herwig, R., Un, C., Schellander, K., and Hoelker, M. (2010). Suppression of the transcription factor MSX1 gene delays bovine preimplantation embryo development in vitro. Reproduction 139, 857–870.
| Suppression of the transcription factor MSX1 gene delays bovine preimplantation embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVCgsLg%3D&md5=9261defdaa448992c2df5d359ebc08dfCAS | 20176746PubMed |
Thatcher, W. W., Meyer, M. D., and Danet-Desnoyers, G. (1995). Maternal recognition of pregnancy. J. Reprod. Fertil. Suppl. 49, 15–28.
| 1:CAS:528:DyaK2MXmslWit7o%3D&md5=0c84400ef58d01c323af5af417e8d14fCAS | 7623310PubMed |
Wang, X. L., Wang, K., Han, G. C., and Zeng, S. M. (2013). A potential autocrine role for interferon tau in ovine trophectoderm. Reprod. Domest. Anim. 48, 819–825.
| A potential autocrine role for interferon tau in ovine trophectoderm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVOgs7rN&md5=531661c3e2fbd770d8fb292f1401ef47CAS | 23551360PubMed |
Yu, J., Valerius, M. T., Duah, M., Staser, K., Hansard, J. K., Guo, J. J., McMahon, J., Vaughan, J., Faria, D., Georgas, K., Rumballe, B., Ren, Q., Krautzberger, A. M., Junker, J. P., Thiagarajan, R. D., Machanick, P., Gray, P. A., van Oudenaarden, A., Rowitch, D. H., Stiles, C. D., Ma, Q., Grimmond, S. M., Bailey, T. L., Little, M. H., and McMahon, A. P. (2012). Identification of molecular compartments and genetic circuitry in the developing mammalian kidney. Development 139, 1863–1873.
| Identification of molecular compartments and genetic circuitry in the developing mammalian kidney.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsFWgsL4%3D&md5=d61f8247005b67dc67fb4d4f420c5007CAS | 22510988PubMed |
