Placenta-specific gene manipulation using lentiviral vector and its application

Placenta

Volumn 59, Issue , 2017, Pages S37-S43

  Tobita, Tomohiro ^a,b   Kiyozumi, Daiji ^a   Ikawa, Masahito ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

CRISPR Cas9 system; Gene therapy; Genome editing; Placenta; Preeclampsia; Viral vectors

Indexed keywords

DOUBLE STRANDED DNA; LENTIVIRUS VECTOR; RNA DIRECTED DNA POLYMERASE; SINGLE STRANDED RNA;

ARTICLE; BLASTOCYST; DEVELOPMENTAL STAGE; DNA INTEGRATION; ECTODERM; EMBRYO DEVELOPMENT; GENE EDITING; GENE EXPRESSION; GENETIC MANIPULATION; GENETIC PROCEDURES; GENOME; NONHUMAN; PLACENTA; PRIORITY JOURNAL; TRANSGENE; VIRUS GENOME; ANIMAL; FEMALE; GENE TRANSFER; GENE VECTOR; GENETIC ENGINEERING; HUMAN; LENTIVIRUS; PREGNANCY;

ANIMALS; FEMALE; GENE TRANSFER TECHNIQUES; GENETIC ENGINEERING; GENETIC VECTORS; HUMANS; LENTIVIRUS; PLACENTA; PREGNANCY;

EID: 85030630228     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2017.09.012     Document Type: Article

References (76)

1. Rossant, J., Cross, J.C., Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2 (2001), 538–548.
2. Watson, E., Cross, J., Development of structures and transport functions in the mouse placenta. Physiology 20 (2005), 180–193.
3. Hu, D., Cross, J.C., Development and function of trophoblast giant cells in the rodent placenta. Int. J. Dev. Biol. 54 (2010), 341–354.
4. John, R.M., Epigenetic regulation of placental endocrine lineages and complications of pregnancy. Biochem. Soc. Trans. 41 (2013), 701–709.
5. Beltowski, J., Jamroz, A., Adrenomedullin – what do we know 10 years since its discovery?. Pol. J. Pharmacol. 56 (2004), 5–27.
6. Baeyens, L., Hindi, S., Sorenson, R.L., German, M.S., β-Cell adaptation in pregnancy. Diabetes, Obes. Metab. 18 (2016), 63–70.
7. Soares, M.J., Konno, T., Alam, S.M.K., The prolactin family: effectors of pregnancy-dependent adaptations. Trends Endocrinol. Metab. 18 (2007), 114–121.
8. Cross, J.C., The genetics of pre-eclampsia: a feto-placental or maternal problem?. Clin. Genet. 64 (2003), 96–103.
9. Cross, J.C., Placental function in development and disease. Reprod. Fertil. Dev. 18 (2006), 71–76.
10. Kamat, A., Graves, K.H., Smith, M.E., Richardson, J.A., Mendelson, C.R., A 500-bp region, 40 kb upstream of the human CYP19 (aromatase) gene, mediates placenta-specific expression in transgenic mice. Proc. Natl. Acad. Sci. 96 (1999), 4575–4580.
11. Shida, M.M., Jackson-Grusby, L.L., Ross, S.R., Linzer, D.I., Placental-specific expression from the mouse placental lactogen II gene promoter. Proc. Natl. Acad. Sci. U. S. A. 89 (1992), 3864–3868.
12. Calzonetti, T., Stevenson, L., Rossant, J., A novel regulatory region is required for trophoblast-specific transcription in transgenic mice. Dev. Biol. 171 (1995), 615–626.
13. Su, Y., Liebhaber, S.A., Cooke, N.E., The human growth hormone gene cluster locus control region supports position-independent pituitary- and placenta-specific expression in the transgenic mouse. J. Biol. Chem., 2000, 7902–7909.
14. Senut, M., Suhr, S.T., Gage, F.H., Gene transfer to the rodent placenta in situ a new strategy for delivering gene products to the fetus. J. Clin. Invest., 1998, 1565–1571.
15. Hertzel, a V., Sanders, M. a, Bernlohr, D. a, Adenovirus-mediated gene transfer in primary murine adipocytes. J. Lipid Res. 41 (2000), 1082–1086.
16. Goossens, P.H., Huizinga, T.W.J., Adenoviral-mediated gene transfer to the synovial tissue. Clin. Exp. Rheumatol. 20 (2002), 415–419.
17. Akli, S., Caillaud, C., Vigne, E., Stratford-Perricaudet, L.D., Poenaru, L., Perricaudet, M., Kahn, A., Peschanski, M.R., Transfer of a foreign gene into the brain using adenovirus vectors. Nat. Genet. 3 (1993), 224–228.
18. Gordon, J.W., Adenovirus gene transfer vector toxicity to mouse embryos: implications for human IVF. Hum. Reprod. 17 (2002), 2380–2387.
19. Jähner, D., Haase, K., Mulligan, R., Jaenisch, R., Insertion of the bacterial gpt gene into the germ line of mice by retroviral infection. Proc. Natl. Acad. Sci. U. S. A. 82 (1985), 6927–6931.
20. Cherry, S.R., Biniszkiewicz, D., Van Parijs, L., Baltimore, D., Jaenisch, R., Retroviral expression in embryonic stem cells and hematopoietic stem cells. Mol. Cell. Biol. 20 (2000), 7419–7426.
21. Naldini, L., Blomer, U., Gallay, P., Ory, D., Mulligan, R., Gage, F.H., Verma, I.M., Trono, D., In vivo gene delivery and stable transduction of post mitotic cells by a lentiviral vector. Sci. (80-. ) 272 (1996), 263–267 http://science.sciencemag.org/content/272/5259/263.
22. Pfeifer, A., Ikawa, M., Dayn, Y., Verma, I.M., Transgenesis by lentiviral vectors: lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 2140–2145.
23. Ikawa, M., Tanaka, N., Kao, W.W.-Y., Verma, I.M., Generation of transgenic mice using lentiviral vectors: a novel preclinical assessment of lentiviral vectors for gene therapy. Mol. Ther. 8 (2003), 666–673.
24. Okada, Y., Ueshin, Y., Isotani, A., Saito-Fujita, T., Nakashima, H., Kimura, K., Mizoguchi, A., Oh-Hora, M., Mori, Y., Ogata, M., Oshima, R.G., Okabe, M., Ikawa, M., Complementation of placental defects and embryonic lethality by trophoblast-specific lentiviral gene transfer. Nat. Biotechnol. 25 (2007), 233–237.
25. Georgiades, P., Cox, B., Gertsenstein, M., Chawengsaksophak, K., Rossant, J., Trophoblast-specific gene manipulation using lentivirus-based vectors. Biotechniques 42 (2007), 317–325.
26. Malashicheva, A., Kanzler, B., Tolkunova, E., Trono, D., Tomilin, A., Lentivirus as a tool for lineage-specific gene manipulations. Genesis 45 (2007), 456–459.
27. Dull, T., Zufferey, R., Kelly, M., Mandel, R.J., Nguyen, M., Trono, D., Naldini, L., A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72 (1998), 8463–8471.
28. Miyoshi, H., Blömer, U., Takahashi, M., Gage, F.H., Verma, I.M., Development of a self-inactivating lentivirus vector. J. Virol. 72 (1998), 8150–8157.
29. Zufferey, R., Dull, T., Mandel, R.J., Bukovsky, A., Quiroz, D., Naldini, L., Trono, D., Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J. Virol. 72 (1998), 9873–9880.
30. Finkelshtein, D., Werman, A., Novick, D., Barak, S., Rubinstein, M., LDL receptor and its family members serve as the cellular receptors for vesicular stomatitis virus. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 7306–7311.
31. Purcell, S.H., Cantlon, J.D., Wright, C.D., Henkes, L.E., Seidel, G.E., Anthony, R.V., The involvement of proline-rich 15 in early conceptus development in sheep. Biol. Reprod. 81 (2009), 1112–1121.
32. Lee, D.S., Rumi, M.A.K., Konno, T., Soares, M.J., In vivo genetic manipulation of the rat trophoblast cell lineage using lentiviral vector delivery. Genesis 47 (2009), 433–439.
33. Kent, L.N., Rumi, M. a. K., Kubota, K., Lee, D.-S., Soares, M.J., FOSL1 is integral to establishing the maternal-fetal interface. Mol. Cell. Biol. 31 (2011), 4801–4813.
34. Chakraborty, D., Cui, W., Rosario, G.X., Scott, R.L., Dhakal, P., Renaud, S.J., Tachibana, M., Rumi, M.A.K., Mason, C.W., Krieg, A.J., Soares, M.J., HIF-KDM3A-MMP12 regulatory circuit ensures trophoblast plasticity and placental adaptations to hypoxia. Proc. Natl. Acad. Sci. 113 (2016), E7212–E7221.
35. Kashif, M., Hellwig, A., Hashemolhosseini, S., Kumar, V., Bock, F., Wang, H., Shahzad, K., Ranjan, S., Wolter, J., Madhusudhan, T., Bierhaus, A., Nawroth, P., Isermann, B., Nuclear factor erythroid-derived 2 (Nfe2) regulates junD DNA-binding activity via acetylation: a novel mechanism regulating trophoblast differentiation. J. Biol. Chem. 287 (2012), 5400–5411.
36. Kumasawa, K., Ikawa, M., Kidoya, H., Hasuwa, H., Saito-Fujita, T., Morioka, Y., Takakura, N., Kimura, T., Okabe, M., Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 1451–1455.
37. Chhabra, A., Lechner, A.J., Ueno, M., Acharya, A., Van Handel, B., Wang, Y., Iruela-Arispe, M.L., Tallquist, M.D., Mikkola, H.K.A., Trophoblasts regulate the placental hematopoietic niche through PDGF-B signaling. Dev. Cell. 22 (2012), 651–659.
38. Latos, P.A., Sienerth, A.R., Murray, A., Senner, C.E., Muto, M., Ikawa, M., Oxley, D., Burge, S., Cox, B.J., Hemberger, M., Elf5-centered transcription factor hub controls trophoblast stem cell self-renewal and differentiation through stoichiometry-sensitive shifts in target gene networks. Genes Dev. 29 (2015), 2435–2448.
39. Mishima, T., Sadovsky, E., Gegick, M.E., Sadovsky, Y., Determinants of effective lentivirus-driven microRNA expression in vivo. Sci. Rep., 6, 2016, 33345.
40. Muto, M., Fujihara, Y., Tobita, T., Kiyozumi, D., Ikawa, M., Lentiviral vector-mediated complementation restored fetal viability but not placental hyperplasia in plac1-deficient mice. Biol. Reprod., 94, 2016, 6.
41. Kühnel, E., Kleff, V., Stojanovska, V., Kaiser, S., Waldschütz, R., Herse, F., Plösch, T., Winterhager, E., Gellhaus, A., Placental-specific overexpression of sFlt-1 alters trophoblast differentiation and nutrient transporter expression in an IUGR mouse model. J. Cell. Biochem., 2016, 1–40.
42. Zhou, Z., Zhang, Q., Lu, X., Wang, R., Wang, H., Wang, Y.-L., Zhu, C., Lin, H.-Y., The proprotein convertase furin is required for trophoblast syncytialization. Cell Death Dis., 4, 2013, e593.
43. Pan, Y.B., Gong, Y., Ruan, H.F., Pan, L.Y., Wu, X.K.M., Tang, C., Wang, C.J., Zhu, H.B., Zhang, Z.M., Tang, L.F., Zou, C.C., Wang, H.B., Wu, X.K.M., Sonic hedgehog through Gli2 and Gli3 is required for the proper development of placental labyrinth. Cell Death Dis., 6, 2015, e1653.
44. Zhang, Q., Yu, S., Huang, X., Tan, Y., Zhu, C., Wang, Y.L., Wang, H., Lin, H.Y., Fu, J., Wang, H., New insights into the function of Cullin 3 in trophoblast invasion and migration. Reproduction 150 (2015), 139–149.
45. Morioka, Y., Isotani, A., Oshima, R.G., Okabe, M., Ikawa, M., Placenta-specific gene activation and inactivation using integrase-defective lentiviral vectors with the Cre/LoxP system. Genesis 47 (2009), 793–798.
46. Ueno, M., Lee, L.K., Chhabra, A., Kim, Y., Sasidharan, R., VanHandel, B., Wang, Y., Kamata, M., Kamran, P., Sereti, K.I., Ardehali, R., Jiang, M., Mikkola, H.K.A., C-Met-Dependent multipotent labyrinth trophoblast progenitors establish placental exchange interface. Dev. Cell. 27 (2013), 373–386.
47. Fan, X., Ren, P., Dhal, S., Bejerano, G., Goodman, S.B., Druzin, M.L., Gambhir, S.S., Nayak, N.R., Noninvasive monitoring of placenta-specific transgene expression by bioluminescence imaging. PLoS One, 6, 2011, e16348.
48. Fan, X., Petitt, M., Gamboa, M., Huang, M., Dhal, S., Druzin, M.L., Wu, J.C., Chen-tsai, Y., Nayak, N.R., Transient, inducible, placenta-specific gene expression in mice. Endocrinology, 2012, 5637–5644.
49. Yamamoto, H., Flannery, M.L., Kupriyanov, S., Pearce, J., McKercher, S.R., Henkel, G.W., Maki, R.A., Werb, Z., Oshima, R.G., Defective trophoblast function in mice with a targeted mutation of Ets2. Genes Dev. 12 (1998), 1315–1326.
50. Adams, R.H., Porras, a, Alonso, G., Jones, M., Vintersten, K., Panelli, S., Valladares, a, Perez, L., Klein, R., Nebreda, a R., Essential role of p38alpha MAP kinase in placental but not embryonic cardiovascular development. Mol. Cell. 6 (2000), 109–116.
51. Zarubin, T., Han, J., Activation and signaling of the p38 MAP kinase pathway. Cell Res. 15 (2005), 11–18.
52. Aouadi, M., Binetruy, B., Caron, L., Le Marchand-Brustel, Y., Bost, F., Role of MAPKs in development and differentiation: lessons from knockout mice. Biochimie 88 (2006), 1091–1098.
53. Allen, M., Svensson, L., Roach, M., Hambor, J., McNeish, J., Gabel, C.A., Deficiency of the stress kinase p38α results in embryonic lethality: characterization of the kinase dependence of stress responses of enzyme-deficient embryonic stem cells. J. Exp. Med. 191 (2000), 859–869.
54. Hatano, N., Mori, Y., Oh-hora, M., Kosugi, A., Fujikawa, T., Nakai, N., Niwa, H., Miyazaki, J.I., Hamaoka, T., Ogata, M., Essential role for ERK2 mitogen-activated protein kinase in placental development. Genes Cells 8 (2003), 847–856.
55. Mudgett, J.S., Ding, J., Guh-Siesel, L., Chartrain, N. a, Yang, L., Gopal, S., Shen, M.M., Essential role for p38alpha mitogen-activated protein kinase in placental angiogenesis. Proc. Natl. Acad. Sci. 97 (2000), 10454–10459.
56. Schmidt-Supprian, M., Rajewsky, K., Vagaries of conditional gene targeting. Nat. Immunol. 8 (2007), 665–668.
57. Naiche, L.A., Papaioannou, V.E., Cre activity causes widespread apoptosis and lethal anemia during embryonic development. Genesis 45 (2007), 768–775.
58. Forni, P.E., Scuoppo, C., Imayoshi, I., Taulli, R., Dastrù, W., Sala, V., Betz, U.A.K., Muzzi, P., Martinuzzi, D., Vercelli, A.E., Kageyama, R., Ponzetto, C., High levels of cre expression in neuronal progenitors cause defects in brain development leading to microencephaly and hydrocephaly. J. Neurosci. 26 (2006), 9593–9602.
59. Thomas, G., Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol. 3 (2002), 753–766.
60. Chen, C.-P., Chen, L.-F., Yang, S.-R., Chen, C.-Y., Ko, C.-C., Chang, G.-D., Chen, H., Functional characterization of the human placental fusogenic membrane protein syncytin 2. Biol. Reprod. 79 (2008), 815–823.
61. Dupressoir, A., Vernochet, C., Bawa, O., Harper, F., Pierron, G., Opolon, P., Heidmann, T., Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 12127–12132.
62. Dupressoir, A., Vernochet, C., Harper, F., Guegan, J., Dessen, P., Pierron, G., Heidmann, T., A pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), E1164–E1173.
63. Roebroek, A.J., Umans, L., Pauli, I.G., Robertson, E.J., van Leuven, F., Van de Ven, W.J., Constam, D.B., Failure of ventral closure and axial rotation in embryos lacking the proprotein convertase Furin. Development 125 (1998), 4863–4876.
64. Backes, C.H., Markham, K., Moorehead, P., Cordero, L., Nankervis, C. a, Giannone, P.J., Maternal preeclampsia and neonatal outcomes. J. Pregnancy, 2011, 2011, 214365.
65. Sibai, B., Dekker, G., Kupferminc, M., Way, A.S., Pre-eclampsia. 2005, 785–799.
66. Maynard, S.E., Min, J., Merchan, J., Lim, K.-H., Li, J., Mondal, S., Libermann, T.A., Morgon, J.P., Sellke, F.W., Stillman, I.E., Epstein, F.H., Sukhatme, V.P., Karumanchi, S.A., Excess placental soluble fms-like hypertension, and proteinuria in. J. Clin. Invest. 58 (2003), 564–581.
67. Kureishi, Y., Luo, Z., Shiojima, I., Bialik, a, Fulton, D., Lefer, D.J., Sessa, W.C., Walsh, K., The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat. Med. 6 (2000), 1004–1010.
68. Verlohren, S., Herraiz, I., Lapaire, O., Schlembach, D., Moertl, M., Zeisler, H., Calda, P., Holzgreve, W., Galindo, A., Engels, T., Denk, B., Stepan, H., The sFlt-1/PlGF ratio in different types of hypertensive pregnancy disorders and its prognostic potential in preeclamptic patients. Am. J. Obstet. Gynecol., 206, 2012 58.e1-58.e8.
69. Gaj, T., Gersbach, C.A., Barbas, C.F., ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 31 (2013), 397–405.
70. Mashiko, D., Young, S.A.M., Muto, M., Kato, H., Nozawa, K., Ogawa, M., Noda, T., Kim, Y.J., Satouh, Y., Fujihara, Y., Ikawa, M., Feasibility for a large scale mouse mutagenesis by injecting CRISPR/Cas plasmid into zygotes. Dev. Growth Differ. 56 (2014), 122–129.
71. Perez-Pinera, P., Kocak, D.D., Vockley, C.M., Adler, A.F., Kabadi, A.M., Polstein, L.R., Thakore, P.I., Glass, K.A., Ousterout, D.G., Leong, K.W., Guilak, F., Crawford, G.E., Reddy, T.E., Gersbach, C.A., RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat. Methods 10 (2013), 973–976.
72. Chen, B., Gilbert, L.A., Cimini, B.A., Schnitzbauer, J., Zhang, W., Li, G.W., Park, J., Blackburn, E.H., Weissman, J.S., Qi, L.S., Huang, B., Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155 (2013), 1479–1491.
73. González, F., Zhu, Z., Shi, Z.D., Lelli, K., Verma, N., Li, Q.V., Huangfu, D., An iCRISPR platform for rapid, multiplexable, and inducible genome editing in human pluripotent stem cells. Cell Stem Cell. 15 (2014), 215–226.
74. Morita, S., Noguchi, H., Horii, T., Nakabayashi, K., Kimura, M., Okamura, K., Sakai, A., Nakashima, H., Hata, K., Nakashima, K., Hatada, I., Targeted DNA demethylation in vivo using dCas9–peptide repeat and scFv–TET1 catalytic domain fusions. Nat. Biotechnol. 34 (2016), 1–9.
75. Lombardo, A., Genovese, P., Beausejour, C.M., Colleoni, S., Lee, Y.L., Kim, K.A., Ando, D., Urnov, F.D., Galli, C., Gregory, P.D., Holmes, M.C., Naldini, L., Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat. Biotechnol. 25 (2007), 1298–1306.
76. Gilbert, L.A., Larson, M.H., Morsut, L., Liu, Z., Brar, G.A., Torres, S.E., Stern-Ginossar, N., Brandman, O., Whitehead, E.H., Doudna, J.A., Lim, W.A., Weissman, J.S., Qi, L.S., XCRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154 (2013), 442–451.