Nfix Regulates Fetal-Specific Transcription in Developing Skeletal Muscle
Open accessAbstract
Skeletal myogenesis, like hematopoiesis, occurs in successive developmental stages that involve different cell populations and expression of different genes. We show here that the transcription factor nuclear factor one X (Nfix), whose expression is activated by Pax7 in fetal muscle, in turn activates the transcription of fetal specific genes such as MCK and beta-enolase while repressing embryonic genes such as slow myosin. In the case of the MCK promoter, Nfix forms a complex with PKC theta that binds, phosphorylates, and activates MEF2A. Premature expression of Nfix activates fetal and suppresses embryonic genes in embryonic muscle, whereas muscle-specific ablation of Nfix prevents fetal and maintains embryonic gene expression in the fetus. Therefore, Nfix acts as a transcriptional switch from embryonic to fetal myogenesis.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Although their loci are not very near to each other, Nfia, Nfib and Nfix regulate cell-type differentiation in many tissues, function as homo- or heterodimers, and bind to largely common targets.
“Although their loci are not very near to each other, Nfia, Nfib and Nfix regulate cell-type differentiation in many tissues94–96, function as homo- or heterodimers, and bind to largely common targets97.”
From A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain (2023) · cites this paper as [96]
Cites
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Liu, J.-P., Baker, J. C., Perkins, A. S., Robertson, E. J., & Efstratiadis, A. (1993) · Cell · doi:10.1016/s0092-8674(05)80084-4 · Cited by 2,854 · see citing works
Pax7 Is Required for the Specification of Myogenic Satellite Cells
Seale, P., Sabourin, L. A., Girgis-Gabardo, A., Mansouri, A., Gruß, P., & Rudnicki, M. A. (2000) · Cell · doi:10.1016/s0092-8674(00)00066-0 · Cited by 2,345 · see citing works
MatInspector and beyond: promoter analysis based on transcription factor binding sites
Cartharius, K., Frech, K., Grote, K., Klocke, B., Haltmeier, M., Klingenhoff, A., Frisch, M., Bayerlein, M., & Werner, T. (2005) · Computer applications in the biosciences · doi:10.1093/bioinformatics/bti473 · Cited by 1,962 · see citing works
Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice
Kassar-Duchossoy, L., Gayraud-Morel, B., Gomès, D., Rocancourt, D., BUCKINGHAM, M. E., Shinin, V., & Tajbakhsh, S. (2004) · Nature · doi:10.1038/nature02876 · Cited by 677 · see citing works
Roles of the NFI/CTF gene family in transcription and development
Gronostajski, R. M. (2000) · Gene · doi:10.1016/s0378-1119(00)00140-2 · Cited by 545 · see citing works
Self-citationJostes, B., Walther, C., & Gruß, P. (1990) · Mechanisms of Development · doi:10.1016/0925-4773(90)90132-6 · Cited by 400 · see citing works
Stockdale, F. E. (1992) · Developmental Biology · doi:10.1016/0012-1606(92)90068-r · Cited by 388 · see citing works
Kitzmann, M., Carnac, G., Vandromme, M., Primig, M., Lamb, N. J. C., & Fernandez, A. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.6.1447 · Cited by 323 · see citing works
The Transcription Factor Gene Nfib Is Essential for both Lung Maturation and Brain Development
Steele-Perkins, G., Plachez, C., Butz, K. G., Yang, G., Bachurski, C. J., Kinsman, S. L., Litwack, E. D., Richards, L. J., & Gronostajski, R. M. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.2.685-698.2005 · Cited by 310 · see citing works
Self-citationHutcheson, D. A., Zhao, J., Merrell, A. J., Haldar, M., & Kardon, G. (2009) · Genes & Development · doi:10.1101/gad.1769009 · Cited by 301 · see citing works
Cellular heterogeneity during vertebrate skeletal muscle development
Biressi, S., Molinaro, M., & Cossu, G. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.06.006 · Cited by 294 · see citing works
Self-citationdas 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) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.21.11946 · Cited by 236 · see citing works
Self-citationEssential Role for NFI-C/CTF Transcription-Replication Factor in Tooth Root Development
Steele-Perkins, G., Butz, K. G., Lyons, G. E., Zeichner‐David, M., Kim, H., Cho, M., & Gronostajski, R. M. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.3.1075-1084.2003 · Cited by 210 · see citing works
Self-citationThe transcription factor Nfixis essential for normal brain development
Campbell, C. E., Piper, M., Plachez, C., Yeh, Y.-T., Baizer, J. S., Osinski, J. M., Litwack, E. D., Richards, L. J., & Gronostajski, R. M. (2008) · BMC Developmental Biology · doi:10.1186/1471-213x-8-52 · Cited by 179 · see citing works
Self-citationBirk, D. E., Zycband, E., Woodruff, S., Winkelmann, D. A., & Trelstad, R. L. (1997) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(199703)208:3 · Cited by 172 · see citing works
Siedner, S., Krüger, M., Schroeter, M. M., Metzler, D., Roell, W., Fleischmann, B. K., Hescheler, J., Pfitzer, G., & Stehle, R. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.036509 · Cited by 169 · see citing works
NFAT isoforms control activity-dependent muscle fiber type specification
Calabria, E., Ciciliot, S., Moretti, I., Garcia, M., Picard, A., Dyar, K. A., Pallafacchina, G., Tothova, J., Schiaffino, S., & Murgia, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812911106 · Cited by 166 · see citing works
[45] Production of transgenic mice
Gordon, J. W. (1993) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(93)25048-7 · Cited by 158 · see citing works
Biressi, S., Tagliafico, E., Lamorte, G., et al. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.01.016 · Cited by 141 · see citing works
Self-citationNuclear Factor I X Deficiency Causes Brain Malformation and Severe Skeletal Defects
Driller, K., Pagenstecher, A., Uhl, M., Omran, H., Berlis, A., Gründer, A., & Sippel, A. E. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02293-06 · Cited by 139 · see citing works
Chapter 4 β‐Globin Regulation and Long‐Range Interactions
Palstra, R., de Laat, W., & Grosveld, F. (2008) · Advances in genetics · doi:10.1016/s0065-2660(07)00004-1 · Cited by 131 · see citing works
Multiple mechanisms regulate muscle fiber diversity
Gunning, P. W., & Hardeman, E. C. (1991) · The FASEB Journal · doi:10.1096/fasebj.5.15.1835946 · Cited by 127 · see citing works
Funk, W. D., & Wright, W. E. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.20.9484 · Cited by 104 · see citing works
George‐Weinstein, M., Foster, R. F., Gerhart, J. V., & Kaufman, S. J. (1993) · Developmental Biology · doi:10.1006/dbio.1993.1071 · Cited by 104 · see citing works
Kaufmann, U., Kirsch, J., Irintchev, A., et al. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.1.55 · Cited by 77 · see citing works
Identification of a fourth Nuclear Factor I gene in chicken by cDNA cloning: NFI-X
Kruse, U., Feng, Q., & Sippel, A. E. (1991) · Nucleic Acids Research · doi:10.1093/nar/19.23.6641 · Cited by 73 · see citing works
Bachurski, C. J., Yang, G. H., Currier, T. A., et al. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.24.9014-9024.2003 · Cited by 68 · see citing works
MyoD-cre transgenic mice: A model for conditional mutagenesis and lineage tracing of skeletal muscle
Chen, J. C. J., Mortimer, J., Marley, J., et al. (2005) · genesis · doi:10.1002/gene.20104 · Cited by 67 · see citing works
Chaudhry, A. Z., Vitullo, A. D., & Gronostajski, R. M. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.29.18538 · Cited by 66 · see citing works
Self-citationStarnes, L. M., Sorrentino, A., Pelosi, E., Ballarino, M., Morsilli, O., Biffoni, M., Santoro, S., Felli, N., Castelli, G., Marchis, M. L. D., et al. (2009) · Blood · doi:10.1182/blood-2008-12-196196 · Cited by 64 · see citing works
Self-citationMessina, G., Blasi, C., Rocca, S. A. L., Pompili, M., Calconi, A., & Grossi, M. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-07-0612 · Cited by 62 · see citing works
Self-citationFunctional and evolutionary relationships of troponin C
Gillis, T. E., Marshall, C. R., & Tibbits, G. F. (2007) · Physiological Genomics · doi:10.1152/physiolgenomics.00197.2007 · Cited by 59 · see citing works
Feo, S., Antona, V., Barbieri, G., et al. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.11.5991 · Cited by 51 · see citing works
Zappelli, F., Willems, D., Osada, S., et al. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0292 · Cited by 50 · see citing works
Hemoglobin switching: new insights
Peterson, K. R. (2003) · Current Opinion in Hematology · doi:10.1097/00062752-200303000-00004 · Cited by 29 · see citing works
Ferrari, S., Molinari, S., Melchionna, R., Angelis, M. G. C. D., Battini, R., Angelis, L. D., Kelly, R. G., & Cossu, G. (1997) · PubMed · Cited by 28 · see citing works
Self-citationJohanson, M., Meents, H., Ragge, K., et al. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.1390 · Cited by 21 · see citing works
Molinari, S., Relaix, F., Lemonnier, M., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.7.2944-2957.2004 · Cited by 21 · see citing works
Visualizing protein interactions by bimolecular fluorescence complementation in Xenopus
Saka, Y., Hagemann, A. I. H., & Smith, J. C. (2008) · Methods · doi:10.1016/j.ymeth.2008.06.005 · Cited by 16 · see citing works
Jiang, P., Song, J., Gu, G., Slonimsky, E., Li, E., & Rosenthal, N. A. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0574 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Fiber Types in Mammalian Skeletal Muscles
Schiaffino, S., & Reggiani, C. (2011) · Physiological Reviews · doi:10.1152/physrev.00031.2010 · Cited by 3,022 · see citing works
A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain
Yao, Z., van Velthoven, C. T. J., Kunst, M., Zhang, M., McMillen, D., Lee, C., Jung, W., Goldy, J., Abdelhak, A., Aitken, M., et al. (2023) · Nature · doi:10.1038/s41586-023-06812-z · Cited by 1,194 · see citing works
Schiebinger, G., Shu, J., Tabaka, M., Cleary, B., Subramanian, V., Solomon, A., Gould, J., Liu, S., Lin, S., Berube, P., et al. (2019) · Cell · doi:10.1016/j.cell.2019.01.006 · Cited by 829 · see citing works
Zammit, P. S. (2017) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2017.11.011 · Cited by 887 · see citing works
Nfix is a novel regulator of murine hematopoietic stem and progenitor cell survival
Holmfeldt, P., Pardieck, J., Saulsberry, A. C., Nandakumar, S. K., Finkelstein, D., Gray, J. T., Persons, D. A., & McKinney-Freeman, S. (2013) · Blood · doi:10.1182/blood-2013-04-493973 · Cited by 55 · see citing works
Common Regulatory Targets of NFIA, NFIX and NFIB during Postnatal Cerebellar Development
Fraser, J., Essebier, A., Brown, A. S., Davila, R. A., Harkins, D., Zalucki, O., Shapiro, L. P., Penzes, P., Wainwright, B. J., Scott, M. P., et al. (2020) · The Cerebellum · doi:10.1007/s12311-019-01089-3 · Cited by 46 · see citing works
Self-citation
- Authors
- Messina, G., Biressi, S., Monteverde, S., Magli, A., Cassano, M., Perani, L., Roncaglia, E., Tagliafico, E., Starnes, L., Campbell, C. E., Grossi, M., Goldhamer, D. J., Gronostajski, R. M., & Cossu, G.
- Affiliations
- University of Milan (IT)
- Stanford Medicine (US)
- IRCCS Ospedale San Raffaele (IT)
- University of Modena and Reggio Emilia (IT)
- Leuven Stem Cell Institute (BE)
- Sapienza University of Rome (IT)
- University at Buffalo, State University of New York (US)
- University of Connecticut (US)
- Corresponding author
- Cossu, Giulio
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2010-02
- Volume
- 140
- Issue
- 4
- Pages
- 554-566
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2163361011
- Cited by
- 210
- References
- 41
- Citations by year
- 2026: 5 · 2025: 11 · 2024: 9 · 2023: 21 · 2022: 16 · 2021: 12 · 2020: 20 · 2019: 11 · 2018: 18 · 2017: 13 · 2016: 8 · 2015: 16 · 2014: 15 · 2013: 14 · 2012: 11
- FWCI
- 4.56
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1298 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion)
- IRIS UNIMORE (University of Modena and Reggio Emilia) (submittedVersion, cc-by)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Iris (University of Trento) (submittedVersion)
- Institutional Research Information System (Università degli Studi di Trento) (submittedVersion)
- INFM-OAR (INFN Catania) (submittedVersion, other-oa)
- Funders
- U.S. Public Health Service (H080624)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR052777, R01AR052777)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- NFIX, skeletal myogenesis, fetal muscle, embryonic muscle, Pax7, beta-enolase, slow myosin, MEF2A, PKC theta, transcriptional switch, gene expression regulation, skeletal muscle development
- MeSH terms
- Protein Kinase C-theta, Animals, Fetus, Humans, Isoenzymes, Phosphopyruvate Hydratase, Protein Kinase C, Transcription, Genetic, Myogenic Regulatory Factors, Muscle, Skeletal, Gene Expression Regulation, Developmental, Muscle Development, NFATC Transcription Factors, Mice, PAX7 Transcription Factor, NFI Transcription Factors, MEF2 Transcription Factors
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review