2a07 Citations

Structure of the forkhead domain of FOXP2 bound to DNA.

Structure 14 159-66 (2006)
Cited: 129 times
EuropePMC logo PMID: 16407075

Abstract

FOXP (FOXP1-4) is a newly defined subfamily of the forkhead box (FOX) transcription factors. A mutation in the FOXP2 forkhead domain cosegregates with a severe speech disorder, whereas several mutations in the FOXP3 forkhead domain are linked to the IPEX syndrome in human and a similar autoimmune phenotype in mice. Here we report a 1.9 A crystal structure of the forkhead domain of human FOXP2 bound to DNA. This structure allows us to revise the previously proposed DNA recognition mechanism and provide a unifying model of DNA binding for the FOX family of proteins. Our studies also reveal that the FOXP2 forkhead domain can form a domain-swapped dimer, made possible by a strategic substitution of a highly conserved proline in conventional FOX proteins with alanine in the P subfamily. Disease-causing mutations in FOXP2 and FOXP3 map either to the DNA binding surface or the domain-swapping dimer interface, functionally corroborating the crystal structure.

Reviews - 2a07 mentioned but not cited (3)

Articles - 2a07 mentioned but not cited (16)

  1. Functional exploration of the adult ovarian granulosa cell tumor-associated somatic FOXL2 mutation p.Cys134Trp (c.402C>G). Benayoun BA, Caburet S, Dipietromaria A, Georges A, D'Haene B, Pandaranayaka PJ, L'Hôte D, Todeschini AL, Krishnaswamy S, Fellous M, De Baere E, Veitia RA. PLoS One 5 e8789 (2010)
  2. Alternative splicing and gene duplication in the evolution of the FoxP gene subfamily. Santos ME, Athanasiadis A, Leitão AB, DuPasquier L, Sucena E. Mol Biol Evol 28 237-247 (2011)
  3. Bispecific Forkhead Transcription Factor FoxN3 Recognizes Two Distinct Motifs with Different DNA Shapes. Rogers JM, Waters CT, Seegar TCM, Jarrett SM, Hallworth AN, Blacklow SC, Bulyk ML. Mol Cell 74 245-253.e6 (2019)
  4. Three-Dimensional Domain Swapping Changes the Folding Mechanism of the Forkhead Domain of FoxP1. Medina E, Córdova C, Villalobos P, Reyes J, Komives EA, Ramírez-Sarmiento CA, Babul J. Biophys J 110 2349-2360 (2016)
  5. FOXP2 variation in great ape populations offers insight into the evolution of communication skills. Staes N, Sherwood CC, Wright K, de Manuel M, Guevara EE, Marques-Bonet T, Krützen M, Massiah M, Hopkins WD, Ely JJ, Bradley BJ. Sci Rep 7 16866 (2017)
  6. Structure-based prediction of transcription factor binding specificity using an integrative energy function. Farrel A, Murphy J, Guo JT. Bioinformatics 32 i306-i313 (2016)
  7. β-catenin regulates FOXP2 transcriptional activity via multiple binding sites. Richter G, Gui T, Bourgeois B, Koyani CN, Ulz P, Heitzer E, von Lewinski D, Burgering BMT, Malle E, Madl T. FEBS J 288 3261-3284 (2021)
  8. Characterization of a recurrent missense mutation in the forkhead DNA-binding domain of FOXP1. Johnson TB, Mechels K, Anderson RH, Cain JT, Sturdevant DA, Braddock S, Pinz H, Wilson MA, Landsverk M, Roux KJ, Weimer JM. Sci Rep 8 16161 (2018)
  9. Crystal and solution structures reveal oligomerization of individual capsid homology domains of Drosophila Arc. Hallin EI, Markússon S, Böttger L, Torda AE, Bramham CR, Kursula P. PLoS One 16 e0251459 (2021)
  10. The influence of various regions of the FOXP2 sequence on its structure and DNA-binding function. Thulo M, Rabie MA, Pahad N, Donald HL, Blane AA, Perumal CM, Penedo JC, Fanucchi S. Biosci Rep 41 BSR20202128 (2021)
  11. Gds1 Interacts with NuA4 To Promote H4 Acetylation at Ribosomal Protein Genes. Joo YJ, Buratowski S. Mol Cell Biol 42 e0037321 (2022)
  12. Rapid diversification of FoxP2 in teleosts through gene duplication in the teleost-specific whole genome duplication event. Song X, Song X, Wang Y, Tang Y. PLoS One 8 e83858 (2013)
  13. Structure-based virtual screening identified novel FOXM1 inhibitors as the lead compounds for ovarian cancer. Zhou ZY, Han XY, Sun LQ, Li SY, Xue ST, Li ZR. Front Chem 10 1058256 (2022)
  14. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)
  15. DNA facilitates heterodimerization between human transcription factors FoxP1 and FoxP2 by increasing their conformational flexibility. Coñuecar R, Asela I, Rivera M, Galaz-Davison P, González-Higueras J, Hamilton GL, Engelberger F, Ramírez-Sarmiento CA, Babul J, Sanabria H, Medina E. iScience 26 107228 (2023)
  16. Single-molecule optical tweezers reveals folding steps of the domain swapping mechanism of a protein. Bustamante A, Rivera R, Floor M, Babul J, Baez M. Biophys J 120 4809-4818 (2021)


Reviews citing this publication (23)

  1. A census of human transcription factors: function, expression and evolution. Vaquerizas JM, Kummerfeld SK, Teichmann SA, Luscombe NM. Nat Rev Genet 10 252-263 (2009)
  2. The emerging roles of forkhead box (Fox) proteins in cancer. Myatt SS, Lam EW. Nat Rev Cancer 7 847-859 (2007)
  3. The evolution of Fox genes and their role in development and disease. Hannenhalli S, Kaestner KH. Nat Rev Genet 10 233-240 (2009)
  4. Fox transcription factors: from development to disease. Golson ML, Kaestner KH. Development 143 4558-4570 (2016)
  5. Forkhead transcription factors: key players in health and disease. Benayoun BA, Caburet S, Veitia RA. Trends Genet 27 224-232 (2011)
  6. Structure/function relationships underlying regulation of FOXO transcription factors. Obsil T, Obsilova V. Oncogene 27 2263-2275 (2008)
  7. Update of human and mouse forkhead box (FOX) gene families. Jackson BC, Carpenter C, Nebert DW, Vasiliou V. Hum Genomics 4 345-352 (2010)
  8. Interaction-site prediction for protein complexes: a critical assessment. Zhou HX, Qin S. Bioinformatics 23 2203-2209 (2007)
  9. In control of biology: of mice, men and Foxes. Wijchers PJ, Burbach JP, Smidt MP. Biochem J 397 233-246 (2006)
  10. Location, location, location: it's all in the timing for replication origins. Aparicio OM. Genes Dev 27 117-128 (2013)
  11. FOXP3 and NFAT: partners in tolerance. Rudensky AY, Gavin M, Zheng Y. Cell 126 253-256 (2006)
  12. Genetic polymorphism in FOXP3 gene: imbalance in regulatory T-cell role and development of human diseases. Oda JM, Hirata BK, Guembarovski RL, Watanabe MA. J Genet 92 163-171 (2013)
  13. Understanding Language from a Genomic Perspective. Graham SA, Fisher SE. Annu Rev Genet 49 131-160 (2015)
  14. Regulatory T Cell and Forkhead Box Protein 3 as Modulators of Immune Homeostasis. Pereira LMS, Gomes STM, Ishak R, Vallinoto ACR. Front Immunol 8 605 (2017)
  15. FOXP transcription factors in vertebrate brain development, function, and disorders. Co M, Anderson AG, Konopka G. Wiley Interdiscip Rev Dev Biol 9 e375 (2020)
  16. FOXP3 and its partners: structural and biochemical insights into the regulation of FOXP3 activity. Zhou Z, Song X, Li B, Greene MI. Immunol Res 42 19-28 (2008)
  17. Hydrogen-deuterium exchange mass spectrometry reveals folding and allostery in protein-protein interactions. Ramirez-Sarmiento CA, Komives EA. Methods 144 43-52 (2018)
  18. The Emerging Roles of Fox Family Transcription Factors in Chromosome Replication, Organization, and Genome Stability. Jin Y, Liang Z, Lou H. Cells 9 E258 (2020)
  19. Molecular windows into speech and language disorders. Fisher SE. Folia Phoniatr Logop 59 130-140 (2007)
  20. Forkhead Box P family members at the crossroad between tolerance and immunity: a balancing act. Fleskens V, van Boxtel R. Int Rev Immunol 33 94-109 (2014)
  21. Therapeutic Potential of Gene-Modified Regulatory T Cells: From Bench to Bedside. Chae WJ, Bothwell ALM. Front Immunol 9 303 (2018)
  22. Decoding the role of coiled-coil motifs in human prion-like proteins. Behbahanipour M, García-Pardo J, Ventura S. Prion 15 143-154 (2021)
  23. Human FoxP Transcription Factors as Tractable Models of the Evolution and Functional Outcomes of Three-Dimensional Domain Swapping. Villalobos P, Ramírez-Sarmiento CA, Babul J, Medina E. Int J Mol Sci 22 10296 (2021)

Articles citing this publication (87)

  1. FOXP3 controls regulatory T cell function through cooperation with NFAT. Wu Y, Borde M, Heissmeyer V, Feuerer M, Lapan AD, Stroud JC, Bates DL, Guo L, Han A, Ziegler SF, Mathis D, Benoist C, Chen L, Rao A. Cell 126 375-387 (2006)
  2. Regulatory T cell development in the absence of functional Foxp3. Lin W, Haribhai D, Relland LM, Truong N, Carlson MR, Williams CB, Chatila TA. Nat Immunol 8 359-368 (2007)
  3. An alternative splicing switch regulates embryonic stem cell pluripotency and reprogramming. Gabut M, Samavarchi-Tehrani P, Wang X, Slobodeniuc V, O'Hanlon D, Sung HK, Alvarez M, Talukder S, Pan Q, Mazzoni EO, Nedelec S, Wichterle H, Woltjen K, Hughes TR, Zandstra PW, Nagy A, Wrana JL, Blencowe BJ. Cell 147 132-146 (2011)
  4. Identification of the transcriptional targets of FOXP2, a gene linked to speech and language, in developing human brain. Spiteri E, Konopka G, Coppola G, Bomar J, Oldham M, Ou J, Vernes SC, Fisher SE, Ren B, Geschwind DH. Am J Hum Genet 81 1144-1157 (2007)
  5. High-throughput analysis of promoter occupancy reveals direct neural targets of FOXP2, a gene mutated in speech and language disorders. Vernes SC, Spiteri E, Nicod J, Groszer M, Taylor JM, Davies KE, Geschwind DH, Fisher SE. Am J Hum Genet 81 1232-1250 (2007)
  6. De novo mutations in FOXP1 in cases with intellectual disability, autism, and language impairment. Hamdan FF, Daoud H, Rochefort D, Piton A, Gauthier J, Langlois M, Foomani G, Dobrzeniecka S, Krebs MO, Joober R, Lafrenière RG, Lacaille JC, Mottron L, Drapeau P, Beauchamp MH, Phillips MS, Fombonne E, Rouleau GA, Michaud JL. Am J Hum Genet 87 671-678 (2010)
  7. Transcriptional control of SLC26A4 is involved in Pendred syndrome and nonsyndromic enlargement of vestibular aqueduct (DFNB4). Yang T, Vidarsson H, Rodrigo-Blomqvist S, Rosengren SS, Enerback S, Smith RJ. Am J Hum Genet 80 1055-1063 (2007)
  8. Sea urchin Forkhead gene family: phylogeny and embryonic expression. Tu Q, Brown CT, Davidson EH, Oliveri P. Dev Biol 300 49-62 (2006)
  9. Crystal structure of the human FOXO3a-DBD/DNA complex suggests the effects of post-translational modification. Tsai KL, Sun YJ, Huang CY, Yang JY, Hung MC, Hsiao CD. Nucleic Acids Res 35 6984-6994 (2007)
  10. Structural basis for DNA recognition by FoxO1 and its regulation by posttranslational modification. Brent MM, Anand R, Marmorstein R. Structure 16 1407-1416 (2008)
  11. DNA-binding specificity changes in the evolution of forkhead transcription factors. Nakagawa S, Gisselbrecht SS, Rogers JM, Hartl DL, Bulyk ML. Proc Natl Acad Sci U S A 110 12349-12354 (2013)
  12. Functional genetic analysis of mutations implicated in a human speech and language disorder. Vernes SC, Nicod J, Elahi FM, Coventry JA, Kenny N, Coupe AM, Bird LE, Davies KE, Fisher SE. Hum Mol Genet 15 3154-3167 (2006)
  13. Structure of a domain-swapped FOXP3 dimer on DNA and its function in regulatory T cells. Bandukwala HS, Wu Y, Feuerer M, Chen Y, Barboza B, Ghosh S, Stroud JC, Benoist C, Mathis D, Rao A, Chen L. Immunity 34 479-491 (2011)
  14. Structure of the FoxM1 DNA-recognition domain bound to a promoter sequence. Littler DR, Alvarez-Fernández M, Stein A, Hibbert RG, Heidebrecht T, Aloy P, Medema RH, Perrakis A. Nucleic Acids Res 38 4527-4538 (2010)
  15. Analyses of a Mutant Foxp3 Allele Reveal BATF as a Critical Transcription Factor in the Differentiation and Accumulation of Tissue Regulatory T Cells. Hayatsu N, Miyao T, Tachibana M, Murakami R, Kimura A, Kato T, Kawakami E, Endo TA, Setoguchi R, Watarai H, Nishikawa T, Yasuda T, Yoshida H, Hori S. Immunity 47 268-283.e9 (2017)
  16. Foxi3 transcription factors and Notch signaling control the formation of skin ionocytes from epidermal precursors of the zebrafish embryo. Jänicke M, Carney TJ, Hammerschmidt M. Dev Biol 307 258-271 (2007)
  17. Structural and biological features of FOXP3 dimerization relevant to regulatory T cell function. Song X, Li B, Xiao Y, Chen C, Wang Q, Liu Y, Berezov A, Xu C, Gao Y, Li Z, Wu SL, Cai Z, Zhang H, Karger BL, Hancock WW, Wells AD, Zhou Z, Greene MI. Cell Rep 1 665-675 (2012)
  18. Crystal structures of multiple GATA zinc fingers bound to DNA reveal new insights into DNA recognition and self-association by GATA. Bates DL, Chen Y, Kim G, Guo L, Chen L. J Mol Biol 381 1292-1306 (2008)
  19. DNA binding by GATA transcription factor suggests mechanisms of DNA looping and long-range gene regulation. Chen Y, Bates DL, Dey R, Chen PH, Machado AC, Laird-Offringa IA, Rohs R, Chen L. Cell Rep 2 1197-1206 (2012)
  20. Pan-Cancer Analysis of Mutation Hotspots in Protein Domains. Miller ML, Reznik E, Gauthier NP, Aksoy BA, Korkut A, Gao J, Ciriello G, Schultz N, Sander C. Cell Syst 1 197-209 (2015)
  21. FoxP1 orchestration of ASD-relevant signaling pathways in the striatum. Araujo DJ, Anderson AG, Berto S, Runnels W, Harper M, Ammanuel S, Rieger MA, Huang HC, Rajkovich K, Loerwald KW, Dekker JD, Tucker HO, Dougherty JD, Gibson JR, Konopka G. Genes Dev 29 2081-2096 (2015)
  22. The mutant leucine-zipper domain impairs both dimerization and suppressive function of Foxp3 in T cells. Chae WJ, Henegariu O, Lee SK, Bothwell AL. Proc Natl Acad Sci U S A 103 9631-9636 (2006)
  23. Adaptive autoimmunity and Foxp3-based immunoregulation in zebrafish. Quintana FJ, Iglesias AH, Farez MF, Caccamo M, Burns EJ, Kassam N, Oukka M, Weiner HL. PLoS One 5 e9478 (2010)
  24. Structure of Smad1 MH1/DNA complex reveals distinctive rearrangements of BMP and TGF-beta effectors. BabuRajendran N, Palasingam P, Narasimhan K, Sun W, Prabhakar S, Jauch R, Kolatkar PR. Nucleic Acids Res 38 3477-3488 (2010)
  25. Prospective investigation of FOXP1 syndrome. Siper PM, De Rubeis S, Trelles MDP, Durkin A, Di Marino D, Muratet F, Frank Y, Lozano R, Eichler EE, Kelly M, Beighley J, Gerdts J, Wallace AS, Mefford HC, Bernier RA, Kolevzon A, Buxbaum JD. Mol Autism 8 57 (2017)
  26. Identification and functional characterization of de novo FOXP1 variants provides novel insights into the etiology of neurodevelopmental disorder. Sollis E, Graham SA, Vino A, Froehlich H, Vreeburg M, Dimitropoulou D, Gilissen C, Pfundt R, Rappold GA, Brunner HG, Deriziotis P, Fisher SE. Hum Mol Genet 25 546-557 (2016)
  27. The identification and characterization of a FOXL2 response element provides insights into the pathogenesis of mutant alleles. Benayoun BA, Caburet S, Dipietromaria A, Bailly-Bechet M, Batista F, Fellous M, Vaiman D, Veitia RA. Hum Mol Genet 17 3118-3127 (2008)
  28. Comparative Genomics Reveals Key Gain-of-Function Events in Foxp3 during Regulatory T Cell Evolution. Andersen KG, Nissen JK, Betz AG. Front Immunol 3 113 (2012)
  29. The Fox/Forkhead transcription factor family of the hemichordate Saccoglossus kowalevskii. Fritzenwanker JH, Gerhart J, Freeman RM, Lowe CJ. Evodevo 5 17 (2014)
  30. A common ancestry for BAP1 and Uch37 regulators. Sanchez-Pulido L, Kong L, Ponting CP. Bioinformatics 28 1953-1956 (2012)
  31. Structural determinants of DNA binding by a P. falciparum ApiAP2 transcriptional regulator. Lindner SE, De Silva EK, Keck JL, Llinás M. J Mol Biol 395 558-567 (2010)
  32. DNA binding by FOXP3 domain-swapped dimer suggests mechanisms of long-range chromosomal interactions. Chen Y, Chen C, Zhang Z, Liu CC, Johnson ME, Espinoza CA, Edsall LE, Ren B, Zhou XJ, Grant SF, Wells AD, Chen L. Nucleic Acids Res 43 1268-1282 (2015)
  33. Foxp2 inhibits Nkx2.1-mediated transcription of SP-C via interactions with the Nkx2.1 homeodomain. Zhou B, Zhong Q, Minoo P, Li C, Ann DK, Frenkel B, Morrisey EE, Crandall ED, Borok Z. Am J Respir Cell Mol Biol 38 750-758 (2008)
  34. Dbf4 recruitment by forkhead transcription factors defines an upstream rate-limiting step in determining origin firing timing. Fang D, Lengronne A, Shi D, Forey R, Skrzypczak M, Ginalski K, Yan C, Wang X, Cao Q, Pasero P, Lou H. Genes Dev 31 2405-2415 (2017)
  35. Conserved forkhead dimerization motif controls DNA replication timing and spatial organization of chromosomes in S. cerevisiae. Ostrow AZ, Kalhor R, Gan Y, Villwock SK, Linke C, Barberis M, Chen L, Aparicio OM. Proc Natl Acad Sci U S A 114 E2411-E2419 (2017)
  36. 2,3,7,8-Tetrachlorodibenzo-p-dioxin upregulates FoxQ1b in zebrafish jaw primordium. Planchart A, Mattingly CJ. Chem Res Toxicol 23 480-487 (2010)
  37. Domain swapping proceeds via complete unfolding: a 19F- and 1H-NMR study of the Cyanovirin-N protein. Liu L, Byeon IJ, Bahar I, Gronenborn AM. J Am Chem Soc 134 4229-4235 (2012)
  38. Solution structure and backbone dynamics of the DNA-binding domain of FOXP1: insight into its domain swapping and DNA binding. Chu YP, Chang CH, Shiu JH, Chang YT, Chen CY, Chuang WJ. Protein Sci 20 908-924 (2011)
  39. Structure of the Forkhead Domain of FOXA2 Bound to a Complete DNA Consensus Site. Li J, Dantas Machado AC, Guo M, Sagendorf JM, Zhou Z, Jiang L, Chen X, Wu D, Qu L, Chen Z, Chen L, Rohs R, Chen Y. Biochemistry 56 3745-3753 (2017)
  40. Binding of transcription factor GabR to DNA requires recognition of DNA shape at a location distinct from its cognate binding site. Al-Zyoud WA, Hynson RM, Ganuelas LA, Coster AC, Duff AP, Baker MA, Stewart AG, Giannoulatou E, Ho JW, Gaus K, Liu D, Lee LK, Böcking T. Nucleic Acids Res 44 1411-1420 (2016)
  41. Intracellular distribution of a speech/language disorder associated FOXP2 mutant. Mizutani A, Matsuzaki A, Momoi MY, Fujita E, Tanabe Y, Momoi T. Biochem Biophys Res Commun 353 869-874 (2007)
  42. The language-related transcription factor FOXP2 is post-translationally modified with small ubiquitin-like modifiers. Estruch SB, Graham SA, Deriziotis P, Fisher SE. Sci Rep 6 20911 (2016)
  43. Mutant Forkhead L2 (FOXL2) proteins associated with premature ovarian failure (POF) dimerize with wild-type FOXL2, leading to altered regulation of genes associated with granulosa cell differentiation. Kuo FT, Bentsi-Barnes IK, Barlow GM, Pisarska MD. Endocrinology 152 3917-3929 (2011)
  44. Opposing roles of FoxP1 and Nfat3 in transcriptional control of cardiomyocyte hypertrophy. Bai S, Kerppola TK. Mol Cell Biol 31 3068-3080 (2011)
  45. Structural basis for DNA recognition by FOXC2. Chen X, Wei H, Li J, Liang X, Dai S, Jiang L, Guo M, Qu L, Chen Z, Chen L, Chen Y. Nucleic Acids Res 47 3752-3764 (2019)
  46. Microfluidic affinity and ChIP-seq analyses converge on a conserved FOXP2-binding motif in chimp and human, which enables the detection of evolutionarily novel targets. Nelson CS, Fuller CK, Fordyce PM, Greninger AL, Li H, DeRisi JL. Nucleic Acids Res 41 5991-6004 (2013)
  47. Molecular shape and prominent role of beta-strand swapping in organization of dUTPase oligomers. Takács E, Barabás O, Petoukhov MV, Svergun DI, Vértessy BG. FEBS Lett 583 865-871 (2009)
  48. Equivalent missense variant in the FOXP2 and FOXP1 transcription factors causes distinct neurodevelopmental disorders. Sollis E, Deriziotis P, Saitsu H, Miyake N, Matsumoto N, Hoffer MJV, Ruivenkamp CAL, Alders M, Okamoto N, Bijlsma EK, Plomp AS, Fisher SE. Hum Mutat 38 1542-1554 (2017)
  49. Mechanism of forkhead transcription factors binding to a novel palindromic DNA site. Li J, Dai S, Chen X, Liang X, Qu L, Jiang L, Guo M, Zhou Z, Wei H, Zhang H, Chen Z, Chen L, Chen Y. Nucleic Acids Res 49 3573-3583 (2021)
  50. The Key Regulator for Language and Speech Development, FOXP2, is a Novel Substrate for SUMOylation. Meredith LJ, Wang CM, Nascimento L, Liu R, Wang L, Yang WH. J Cell Biochem 117 426-438 (2016)
  51. Forkhead Domains of FOXO Transcription Factors Differ in both Overall Conformation and Dynamics. Psenakova K, Kohoutova K, Obsilova V, Ausserlechner MJ, Veverka V, Obsil T. Cells 8 E966 (2019)
  52. Functional characterization of rare FOXP2 variants in neurodevelopmental disorder. Estruch SB, Graham SA, Chinnappa SM, Deriziotis P, Fisher SE. J Neurodev Disord 8 44 (2016)
  53. Solution structure of the N-terminal domain of Bacillus subtilis delta subunit of RNA polymerase and its classification based on structural homologs. Motácková V, Sanderová H, Zídek L, Novácek J, Padrta P, Svenková A, Korelusová J, Jonák J, Krásný L, Sklenár V. Proteins 78 1807-1810 (2010)
  54. Distribution of language-related Cntnap2 protein in neural circuits critical for vocal learning. Condro MC, White SA. J Comp Neurol 522 169-185 (2014)
  55. The FOXP2-Driven Network in Developmental Disorders and Neurodegeneration. Oswald F, Klöble P, Ruland A, Rosenkranz D, Hinz B, Butter F, Ramljak S, Zechner U, Herlyn H. Front Cell Neurosci 11 212 (2017)
  56. Dissecting FOXP2 Oligomerization and DNA Binding. Häußermann K, Young G, Kukura P, Dietz H. Angew Chem Int Ed Engl 58 7662-7667 (2019)
  57. Protein-Protein Interaction Among the FoxP Family Members and their Regulation of Two Target Genes, VLDLR and CNTNAP2 in the Zebra Finch Song System. Mendoza E, Scharff C. Front Mol Neurosci 10 112 (2017)
  58. Multiple transcription start sites for FOXP2 with varying cellular specificities. Schroeder DI, Myers RM. Gene 413 42-48 (2008)
  59. Predicting and understanding transcription factor interactions based on sequence level determinants of combinatorial control. van Dijk AD, ter Braak CJ, Immink RG, Angenent GC, van Ham RC. Bioinformatics 24 26-33 (2008)
  60. The crystal structure of human forkhead box N1 in complex with DNA reveals the structural basis for forkhead box family specificity. Newman JA, Aitkenhead H, Gavard AE, Rota IA, Handel AE, Hollander GA, Gileadi O. J Biol Chem 295 2948-2958 (2020)
  61. Identification and analysis of evolutionary selection pressures acting at the molecular level in five forkhead subfamilies. Fetterman CD, Rannala B, Walter MA. BMC Evol Biol 8 261 (2008)
  62. A Single Amino Acid in the Hinge Loop Region of the FOXP Forkhead Domain is Significant for Dimerisation. Perumal K, Dirr HW, Fanucchi S. Protein J 34 111-121 (2015)
  63. FOXP1 haploinsufficiency: Phenotypes beyond behavior and intellectual disability? Myers A, du Souich C, Yang CL, Borovik L, Mwenifumbo J, Rupps R, Study C, Lehman A, Boerkoel CF. Am J Med Genet A 173 3172-3181 (2017)
  64. Heterozygous variants that disturb the transcriptional repressor activity of FOXP4 cause a developmental disorder with speech/language delays and multiple congenital abnormalities. Snijders Blok L, Vino A, den Hoed J, Underhill HR, Monteil D, Li H, Reynoso Santos FJ, Chung WK, Amaral MD, Schnur RE, Santiago-Sim T, Si Y, Brunner HG, Kleefstra T, Fisher SE. Genet Med 23 534-542 (2021)
  65. Transcription factor FOXP2 is a flow-induced regulator of collecting lymphatic vessels. Hernández Vásquez MN, Ulvmar MH, González-Loyola A, Kritikos I, Sun Y, He L, Halin C, Petrova TV, Mäkinen T. EMBO J 40 e107192 (2021)
  66. Chemokine signaling links cell-cycle progression and cilia formation for left-right symmetry breaking. Liu J, Zhu C, Ning G, Yang L, Cao Y, Huang S, Wang Q. PLoS Biol 17 e3000203 (2019)
  67. The transcription factor FoxP3 can fold into two dimerization states with divergent implications for regulatory T cell function and immune homeostasis. Leng F, Zhang W, Ramirez RN, Leon J, Zhong Y, Hou L, Yuki K, van der Veeken J, Rudensky AY, Benoist C, Hur S. Immunity 55 1354-1369.e8 (2022)
  68. FOXA2-Interacting FOXP2 Prevents Epithelial-Mesenchymal Transition of Breast Cancer Cells by Stimulating E-Cadherin and PHF2 Transcription. Liu Y, Chen T, Guo M, Li Y, Zhang Q, Tan G, Yu L, Tan Y. Front Oncol 11 605025 (2021)
  69. Intrinsically Disordered Regions of the DNA-Binding Domain of Human FoxP1 Facilitate Domain Swapping. Medina E, Villalobos P, Hamilton GL, Komives EA, Sanabria H, Ramírez-Sarmiento CA, Babul J. J Mol Biol 432 5411-5429 (2020)
  70. The protonation state of an evolutionarily conserved histidine modulates domainswapping stability of FoxP1. Medina E, Villalobos P, Coñuecar R, Ramírez-Sarmiento CA, Babul J. Sci Rep 9 5441 (2019)
  71. Crystal Structure of FOXC2 in Complex with DNA Target. Li S, Pradhan L, Ashur S, Joshi A, Nam HJ. ACS Omega 4 10906-10914 (2019)
  72. FOXP3 rs3761548 polymorphism is associated with knee osteoarthritis in a Turkish population. Cekin N, Pinarbasi E, Bildirici AE, Donmez G, Oztemur Z, Bulut O, Arslan S. Int J Rheum Dis 21 1779-1786 (2018)
  73. Pathogenic missense mutation pattern of forkhead box genes in neurodevelopmental disorders. Han L, Chen M, Wang Y, Wu H, Quan Y, Bai T, Li K, Duan G, Gao Y, Hu Z, Xia K, Guo H. Mol Genet Genomic Med 7 e00789 (2019)
  74. The forkhead domain hinge-loop plays a pivotal role in DNA binding and transcriptional activity of FOXP2. Morris G, Stoychev S, Naicker P, Dirr HW, Fanucchi S. Biol Chem 399 881-893 (2018)
  75. Comprehensive phenotypic and functional analysis of dominant and recessive FOXE3 alleles in ocular developmental disorders. Reis LM, Sorokina EA, Dudakova L, Moravikova J, Skalicka P, Malinka F, Seese SE, Thompson S, Bardakjian T, Capasso J, Allen W, Glaser T, Levin AV, Schneider A, Khan A, Liskova P, Semina EV. Hum Mol Genet 30 1591-1606 (2021)
  76. A Phosphomimetic Study Implicates Ser557 in Regulation of FOXP2 DNA Binding. Blane A, Dirr HW, Fanucchi S. Protein J 37 311-323 (2018)
  77. Identification of Fkh1 and Fkh2 binding site variants associated with dynamically bound DNA elements including replication origins. Ostrow AZ, Aparicio OM. Nucleus 8 600-604 (2017)
  78. Structural aspects of the FOXP3 regulatory complex as an immunopharmacological target. Zhou Z, Song X, Berezov A, Li B, Greene MI. Int Immunopharmacol 9 518-520 (2009)
  79. The -3279C>A and -924A>G polymorphisms in the FOXP3 Gene Are Associated With Viral Load and Liver Enzyme Levels in Patients With Chronic Viral Liver Diseases. Pereira LMS, Amoras EDSG, da Silva Conde SRS, Demachki S, Monteiro JC, Martins-Feitosa RN, da Silva ANMR, Ishak R, Vallinoto ACR. Front Immunol 9 2014 (2018)
  80. Transcription factor Foxp1 stimulates angiogenesis in adult rats after myocardial infarction. Wang D, Liu B, Xiong T, Yu W, Yang H, Wang J, Jing X, She Q. Cell Death Discov 8 381 (2022)
  81. Upregulation of FOXP1 is a new independent unfavorable prognosticator and a specific predictor of lymphatic dissemination in cutaneous melanoma patients. Donizy P, Pagacz K, Marczuk J, Fendler W, Maciejczyk A, Halon A, Matkowski R. Onco Targets Ther 11 1413-1422 (2018)
  82. Bombyx mori transcription factors FoxA and SAGE divergently regulate the expression of wing cuticle protein gene 4 during metamorphosis. Hu Q, Zhu Z, Zhao D, Zeng B, Zheng S, Song Q, Deng H, Feng Q. J Biol Chem 294 632-643 (2019)
  83. A comprehensive in silico analysis of the deleterious nonsynonymous SNPs of human FOXP2 protein. Akter M, Khan SF, Sajib AA, Rima FS. PLoS One 17 e0272625 (2022)
  84. Assessing the dynamics and macromolecular interactions of the intrinsically disordered protein YY1. Donald H, Blane A, Buthelezi S, Naicker P, Stoychev S, Majakwara J, Fanucchi S. Biosci Rep 43 BSR20231295 (2023)
  85. Broadly Applicable Control Approaches Improve Accuracy of ChIP-Seq Data. Petrie MV, He Y, Gan Y, Ostrow AZ, Aparicio OM. Int J Mol Sci 24 9271 (2023)
  86. Domain tethering impacts dimerization and DNA-mediated allostery in the human transcription factor FoxP1. Cruz P, Paredes N, Asela I, Kolimi N, Molina JA, Ramírez-Sarmiento CA, Goutam R, Huang G, Medina E, Sanabria H. J Chem Phys 158 195101 (2023)
  87. PolyQ length-based molecular encoding of vocalization frequency in FOXP2. Vaglietti S, Villeri V, Dell'Oca M, Marchetti C, Cesano F, Rizzo F, Miller D, LaPierre L, Pelassa I, Monje FJ, Colnaghi L, Ghirardi M, Fiumara F. iScience 26 108036 (2023)