DOI: 10.1073/pnas.96.21.11946. Disruption of the murine nuclear factor I-A gene ( <i>Nfia</i> ) results in perinatal lethality, hydrocephalus, and agenesis of the corpus callosum

Disruption of the murine nuclear factor I-A gene ( Nfia ) results in perinatal lethality, hydrocephalus, and agenesis of the corpus callosum

10.1073/pnas.96.21.11946

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

The phylogenetically conserved nuclear factor I (NFI) family of transcription/replication proteins is essential both for adenoviral DNA replication and for the transcription of many cellular genes. We showed previously that the four murine NFI genes ( Nfia , Nfib , Nfic, and Nfix ) are expressed in unique but overlapping patterns during mouse development and in adult tissues. Here we show that disruption of the Nfia gene causes perinatal lethality, with >95% of homozygous Nfia −/− animals dying within 2 weeks after birth. Newborn Nfia −/− animals lack a corpus callosum and show ventricular dilation indicating early hydrocephalus. Rare surviving homozygous Nfia −/− mice lack a corpus callosum, show severe communicating hydrocephalus, a full-axial tremor indicative of neurological defects, male-sterility, low female fertility, but near normal life spans. These findings indicate that while the Nfia gene appears nonessential for cell viability and DNA replication in embryonic stem cells and fibroblasts, loss of Nfia function causes severe developmental defects. This finding of an NFI gene required for a developmental process suggests that the four NFI genes may have distinct roles in vertebrate development.

Bibliography

das Neves, L., Duchala, C. S., Godinho, F., Haxhiu, M. A., Colmenares, C., Macklin, W. B., Campbell, C. E., Butz, K. G., & Gronostajski, R. M. (1999). Disruption of the murine nuclear factor I-A gene ( Nfia ) results in perinatal lethality, hydrocephalus, and agenesis of the corpus callosum. Proceedings of the National Academy of Sciences, 96(21), 11946â11951.

Authors 9

Liomar das Neves (first)
Cynthia S. Duchala (additional)
Fatima Godinho (additional)
Musa A. Haxhiu (additional)
Clemencia Colmenares (additional)
Wendy B. Macklin (additional)
Christine E. Campbell (additional)
Kenneth G. Butz (additional)
Richard M. Gronostajski (additional)

References 64 Referenced 196

10.1073/pnas.79.21.6438
10.1002/j.1460-2075.1985.tb03811.x
10.1128/mcb.7.2.875-886.1987
J Hurwitz, S Adhya, J Field, R Gronostajski, R A Guggenheimer, M Kenny, J Lindenbaum, K Nagata Synthesis of Adenoviral DNA with Purified Proteins, ed P A Marks (Academic, New York), pp. 15–24 (1985). / Synthesis of Adenoviral DNA with Purified Proteins by Hurwitz J (1985)
10.1016/0022-2836(85)90263-3
10.1093/nar/13.14.5173
10.1002/(SICI)1097-0177(199703)208:3<313::AID-AJA3>3.0.CO;2-L
10.1074/jbc.271.11.6273
S Kulkarni, R M Gronostajski Cell Growth Differ 7, 501–510 (1996). / Cell Growth Differ by Kulkarni S (1996)
10.1073/pnas.85.23.8963
10.1074/jbc.274.13.8813
10.1128/MCB.15.4.2063
10.1074/jbc.271.47.29688
10.1016/S0021-9258(17)30625-7
10.1523/JNEUROSCI.18-16-06186.1998
10.1074/jbc.273.42.27741
10.1093/nar/18.9.2607
10.1093/nar/19.23.6641
10.1007/s003359901008
10.1016/0092-8674(89)90108-6
10.1021/bi00446a034
10.1002/j.1460-2075.1990.tb08143.x
10.1093/nar/14.22.9117
10.1093/nar/16.10.4419
10.1128/mcb.10.3.1041-1048.1990
10.1006/jmbi.1994.1343
10.1073/pnas.91.9.3901
10.1128/MCB.15.10.5552
10.1093/nar/22.19.3825
10.1074/jbc.273.29.18538
10.1074/jbc.274.11.7072
10.1016/0092-8674(91)90011-M
10.1038/326292a0
10.1038/336348a0
10.1002/jnr.490340509
10.1128/mcb.12.5.2391-2395.1992
10.1002/(SICI)1096-9861(19981019)400:2<197::AID-CNE3>3.0.CO;2-4
10.1523/JNEUROSCI.14-11-06608.1994
10.1111/j.1471-4159.1990.tb03123.x
10.1016/S0021-9258(19)49698-1
10.1016/0014-5793(94)00585-0
10.1093/oxfordjournals.jhered.a111128
10.1016/S0896-6273(00)81092-2
10.1073/pnas.96.8.4656
10.1159/000472311
10.1055/s-2007-973696
10.1136/jmg.35.5.399
10.1038/ng1197-346
10.1093/hmg/7.6.999
10.1101/gad.12.8.1092
10.1006/exnr.1997.6638
10.1002/j.1460-2075.1996.tb00992.x
10.1073/pnas.95.8.4481
W Dobyns Am J Hum Genet 58, 7–16 (1996). / Am J Hum Genet by Dobyns W (1996)
10.1523/JNEUROSCI.17-07-02445.1997
10.1002/cne.903360411
10.1016/0169-328X(92)90156-6
10.1073/pnas.92.4.944
10.1016/0387-7604(95)00103-4
10.1212/WNL.50.4.1122
10.1016/0022-510X(85)90168-6
10.2176/nmc.30.445
10.1046/j.1471-4159.1999.721353.x
10.1016/S0076-6879(97)88015-9

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 10:35 a.m.)
Deposited	3 years, 4 months ago (April 13, 2022, 3:31 p.m.)
Indexed	1 month, 1 week ago (July 25, 2025, 6:34 a.m.)
Issued	25 years, 10 months ago (Oct. 12, 1999)
Published	25 years, 10 months ago (Oct. 12, 1999)
Published Online	25 years, 10 months ago (Oct. 12, 1999)
Published Print	25 years, 10 months ago (Oct. 12, 1999)

Funders 0

None

BibTeX

@article{das_Neves_1999, title={Disruption of the murine nuclear factor I-A gene ( Nfia ) results in perinatal lethality, hydrocephalus, and agenesis of the corpus callosum}, volume={96}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.96.21.11946}, DOI={10.1073/pnas.96.21.11946}, number={21}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={das Neves, Liomar and Duchala, Cynthia S. and Godinho, Fatima and Haxhiu, Musa A. and Colmenares, Clemencia and Macklin, Wendy B. and Campbell, Christine E. and Butz, Kenneth G. and Gronostajski, Richard M.}, year={1999}, month=oct, pages={11946–11951} }

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