Differential coexpression of FoxP1, FoxP2, and FoxP4 in the Zebra Finch (Taeniopygia guttata) song system

Journal of Comparative Neurology

Volumn 523, Issue 9, 2015, Pages 1318-1340

  Mendoza, Ezequiel ^a   Tokarev, Kirill ^b   Düring, Daniel N ^c   Retamosa, Eva Camarillo ^d   Weiss, Michael ^a   Arpenik, Nshdejan ^a   Scharff, Constance ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^d NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Basal ganglia; Developmental verbal dyspraxia (DVD); FoxP human mutations; FoxP proteins

Indexed keywords

DOPAMINE 1 RECEPTOR; DOPAMINE 1A RECEPTOR; DOPAMINE 1B RECEPTOR; DOPAMINE 2 RECEPTOR; FORKHEAD TRANSCRIPTION FACTOR; MESSENGER RNA; TRANSCRIPTION FACTOR FOXP1; TRANSCRIPTION FACTOR FOXP2; TRANSCRIPTION FACTOR FOXP4; UNCLASSIFIED DRUG; DOPAMINE RECEPTOR;

ANIMAL BEHAVIOR; ARTICLE; BRAIN REGION; CELL DENSITY; CORPUS STRIATUM; DIMERIZATION; HIGH VOCAL CENTER; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MOLECULAR CLONING; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; SINGING; TAENIOPYGIA GUTTATA; TELENCEPHALON; ANIMAL; BRAIN; FINCH; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROPHOTOGRAPHY; NERVE CELL; NEUROANATOMICAL TRACT TRACING;

ANIMALS; BRAIN; FINCHES; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEURONS; PHOTOMICROGRAPHY; RECEPTORS, DOPAMINE; RNA, MESSENGER;

EID: 84928288385     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23731     Document Type: Article

References (72)

1. Banham AH, Beasley N, Campo E, Fernandez PL, Fidler C, Gatter K, Jones M, Mason DY, Prime JE, Trougouboff P, Wood K, Cordell JL. 2001. The FOXP1 winged helix transcription factor is a novel candidate tumor suppressor gene on chromosome 3p. Cancer Res 61:8820-8829.
2. Bolhuis JJ, Okanoya K, Scharff C. 2010. Twitter evolution: converging mechanisms in birdsong and human speech. Nat Rev Neurosci 11:747-759.
3. Bowers JM, Konopka G. 2012. The role of the FOXP family of transcription factors in ASD. Dis Markers 33:251-260.
4. Brown P, Marafioti T, Kusec R, Banham AH. 2005. The FOXP1 transcription factor is expressed in the majority of follicular lymphomas but is rarely expressed in classical and lymphocyte predominant Hodgkin's lymphoma. J Mol Histol 36:249-256.
5. Campbell P, Reep RL, Stoll ML, Ophir AG, Phelps SM. 2009. Conservation and diversity of Foxp2 expression in muroid rodents: functional implications. J Comp Neurol 512:84-100.
6. Carr CW, Moreno-De-Luca D, Parker C, Zimmerman HH, Ledbetter N, Martin CL, Dobyns WB, Abdul-Rahman OA. 2010. Chiari I malformation, delayed gross motor skills, severe speech delay, and epileptiform discharges in a child with FOXP1 haploinsufficiency. Eur J Hum Genet 18:1216-1220.
7. Chatila TA, Blaeser F, Ho N, Lederman HM, Voulgaropoulos C, Helms C, Bowcock AM. 2000. JM2, encoding a fork head-related protein, is mutated in X-linked autoimmunity-allergic disregulation syndrome. J Clin Invest 106:R75-81.
8. Chen CC, Winkler CM, Pfenning AR, Jarvis ED. 2013a. Molecular profiling of the developing avian telencephalon: regional timing and brain subdivision continuities. J Comp Neurol 521:3666-3701.
9. Chen Q, Heston JB, Burkett ZD, White SA. 2013b. Expression analysis of the speech-related genes FoxP1 and FoxP2 and their relation to singing behavior in two songbird species. J Exp Biol 216(Pt 19):3682-3692.
10. de Zoeten EF, Lee I, Wang L, Chen C, Ge G, Wells AD, Hancock WW, Ozkaynak E. 2009. Foxp3 processing by proprotein convertases and control of regulatory T cell function. J Biol Chem 284:5709-5716.
11. Doupe AJ, Kuhl PK. 1999. Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci 22:567-631.
12. Durand SE, Tepper JM, Cheng MF. 1992. The shell region of the nucleus ovoidalis: a subdivision of the avian auditory thalamus. J Comp Neurol 323:495-518.
13. Enard W, Gehre S, Hammerschmidt K, Holter SM, Blass T, Somel M, Bruckner MK, Schreiweis C, Winter C, Sohr R, Becker L, Wiebe V, Nickel B, Giger T, Muller U, Groszer M, Adler T, Aguilar A, Bolle I, Calzada-Wack J, Dalke C, Ehrhardt N, Favor J, Fuchs H, Gailus-Durner V, Hans W, Holzlwimmer G, Javaheri A, Kalaydjiev S, Kallnik M, Kling E, Kunder S, Mossbrugger I, Naton B, Racz I, Rathkolb B, Rozman J, Schrewe A, Busch DH, Graw J, Ivandic B, Klingenspor M, Klopstock T, Ollert M, Quintanilla-Martinez L, Schulz H, Wolf E, Wurst W, Zimmer A, Fisher SE, Morgenstern R, Arendt T, de Angelis MH, Fischer J, Schwarz J, Paabo S. 2009. A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell 137:961-971.
14. Feenders G, Liedvogel M, Rivas M, Zapka M, Horita H, Hara E, Wada K, Mouritsen H, Jarvis ED. 2008. Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin. PLoS One 3:e1768.
15. Ferland RJ, Cherry TJ, Preware PO, Morrisey EE, Walsh CA. 2003. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J Comp Neurol 460:266-279.
16. Fisher SE, Scharff C. 2009. FOXP2 as a molecular window into speech and language. Trends Genet 25:166-177.
17. Gao Y, Lin F, Su J, Gao Z, Li Y, Yang J, Deng Z, Liu B, Tsun A, Li B. 2012. Molecular mechanisms underlying the regulation and functional plasticity of FOXP3(+) regulatory T cells. Genes Immun 13:1-13.
18. Haesler S, Wada K, Nshdejan A, Morrisey EE, Lints T, Jarvis ED, Scharff C. 2004. FoxP2 expression in avian vocal learners and non-learners. J Neurosci 24:3164-3175.
19. Haesler S, Rochefort C, Georgi B, Licznerski P, Osten P, Scharff C. 2007. Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X. PLoS Biol 5:e321.
20. Hamdan FF, Daoud H, Rochefort D, Piton A, Gauthier J, Langlois M, Foomani G, Dobrzeniecka S, Krebs MO, Joober R, Lafreniere RG, Lacaille JC, Mottron L, Drapeau P, Beauchamp MH, Phillips MS, Fombonne E, Rouleau GA, Michaud JL. 2010. De novo mutations in FOXP1 in cases with intellectual disability, autism, and language impairment. Am J Hum Genet 87:671-678.
21. Hannenhalli S, Kaestner KH. 2009. The evolution of Fox genes and their role in development and disease. Nat Rev Genet 10:233-240.
22. Haque R, Lei F, Xiong X, Song J. 2011. The regulation of FoxP3-expressing regulatory T cells. Endocr Metab Immune Disord Drug Targets 11:334-346.
23. Hemmings H, Nairn A, Bibb J, Greengard P. 1995. Signal transduction in the striatum: DARP32, a molecular integrator of multiple signaling pathways. Heidelberg, Germany: Springer. p 283-297.
24. Hisaoka T, Nakamura Y, Senba E, Morikawa Y. 2010. The forkhead transcription factors, Foxp1 and Foxp2, identify different subpopulations of projection neurons in the mouse cerebral cortex. Neuroscience 166:551-563.
25. Horn D, Kapeller J, Rivera-Brugues N, Moog U, Lorenz-Depiereux B, Eck S, Hempel M, Wagenstaller J, Gawthrope A, Monaco AP, Bonin M, Riess O, Wohlleber E, Illig T, Bezzina CR, Franke A, Spranger S, Villavicencio-Lorini P, Seifert W, Rosenfeld J, Klopocki E, Rappold GA, Strom TM. 2010. Identification of FOXP1 deletions in three unrelated patients with mental retardation and significant speech and language deficits. Hum Mutat 31:E1851-1860.
26. Hultsch H, Todt D. 1982. Temporal performance roles during vocal interactions in nightingales (Luscinia-Megarhynchos B). Behav Ecol Sociobiol 11:253-260.
27. Jarvis ED, Yu J, Rivas MV, Horita H, Feenders G, Whitney O, Jarvis SC, Jarvis ER, Kubikova L, Puck AE, Siang-Bakshi C, Martin S, McElroy M, Hara E, Howard J, Pfenning A, Mouritsen H, Chen CC, Wada K. 2013. Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns. J Comp Neurol 521:3614-3665.
28. Kaestner KH, Knochel W, Martinez DE. 2000. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev 14:142-146.
29. Konopka G, Bomar JM, Winden K, Coppola G, Jonsson ZO, Gao F, Peng S, Preuss TM, Wohlschlegel JA, Geschwind DH. 2009. Human-specific transcriptional regulation of CNS development genes by FOXP2. Nature 462:213-217.
30. Kubikova L, Wada K, Jarvis ED. 2009. Dopamine receptors in a songbird brain. J Comp Neurol 518:741-769.
31. Kurt S, Groszer M, Fisher SE, Ehret G. 2009. Modified sound-evoked brainstem potentials in Foxp2 mutant mice. Brain Res 1289:30-36.
32. Lai CS, Fisher SE, Hurst JA, Vargha-Khadem F, Monaco AP. 2001. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413:519-523.
33. Le Fevre AK, Taylor S, Malek NH, Horn D, Carr CW, Abdul-Rahman OA, O'Donnell S, Burgess T, Shaw M, Gecz J, Bain N, Fagan K, Hunter MF. 2013. FOXP1 mutations cause intellectual disability and a recognizable phenotype. Am J Med Genet A 161:3166-3175.
34. Li S, Joel Weidenfeld, Morrisey EE. 2004a. Transcriptional and DNA binding activity of the Foxp1/2/4 family is modulated by heterotypic and homotypic protein interactions. Mol Cell Biol 24:809-822.
35. Li S, Zhou D, Lu MM, Morrisey EE. 2004b. Advanced cardiac morphogenesis does not require heart tube fusion. Science 305:1619-1622.
36. Li S, Wang Y, Zhang Y, Lu MM, Demayo FJ, Dekker JD, Tucker PW, Morrisey EE. 2012. Foxp1/4 control epithelial cell fate during lung development and regeneration through regulation of anterior gradient 2. Development 139:2500-2509.
37. Liegeois F, Baldeweg T, Connelly A, Gadian DG, Mishkin M, Vargha-Khadem F. 2003. Language fMRI abnormalities associated with FOXP2 gene mutation. Nat Neurosci 6:1230-1237.
38. Lu MM, Li S, Yang H, Morrisey EE. 2002. Foxp4: a novel member of the Foxp subfamily of winged-helix genes co-expressed with Foxp1 and Foxp2 in pulmonary and gut tissues. Mech Dev 119(Suppl 1):S197-202.
39. Mann NI, Dingess KA, Slater PJ. 2006. Antiphonal four-part synchronized chorusing in a neotropical wren. Biol Lett 2:1-4.
40. Mashiko H, Yoshida AC, Kikuchi SS, Niimi K, Takahashi E, Aruga J, Okano H, Shimogori T. 2012. Comparative anatomy of marmoset and mouse cortex from genomic expression. J Neurosci 32:5039-5053.
41. Murugan M, Harward S, Scharff C, Mooney R. 2013. Diminished FoxP2 levels affect dopaminergic modulation of corticostriatal signaling important to song variability. Neuron 80:1464-1476.
42. Nieto-Bona MP, Garcia-Segura LM, Torres-Aleman I. 1993. Orthograde transport and release of insulin-like growth factor I from the inferior olive to the cerebellum. J Neurosci Res 36:520-527.
43. Nixdorf-Bergweiler BE, Bischof H-J. 2007. A stereotaxic atlas of the brain of the zebra finch, Taeniopygia guttata. Bielefeld, Germany.
44. Ohkura N, Kitagawa Y, Sakaguchi S. 2013. Development and maintenance of regulatory T cells. Immunity 38:414-423.
45. Palumbo O, D'Agruma L, Minenna AF, Palumbo P, Stallone R, Palladino T, Zelante L, Carella M. 2013. 3p14.1 de novo microdeletion involving the FOXP1 gene in an adult patient with autism, severe speech delay and deficit of motor coordination. Gene 516:107-113.
46. Pariani MJ, Spencer A, Graham JM, Jr., Rimoin DL. 2009. A 785kb deletion of 3p14.1p13, including the FOXP1 gene, associated with speech delay, contractures, hypertonia and blepharophimosis. Eur J Med Genet 52:123-127.
47. Peake TM, Matessi G, McGregor PK, Dabelsteen T. 2005. Song type matching, song type switching and eavesdropping in male great tits. Anim Behav 69:1063-1068.
48. Petkov CI, Jarvis ED. 2012. Birds, primates, and spoken language origins: behavioral phenotypes and neurobiological substrates. Front Evol Neurosci 4:12.
49. Reimers-Kipping S, Hevers W, Paabo S, Enard W. 2010. Humanized Foxp2 specifically affects cortico-basal ganglia circuits. Neuroscience 175:75-84.
50. Reiner A, Brecha NC, Karten HJ. 1982. Basal ganglia pathways to the tectum: the afferent and efferent connections of the lateral spiriform nucleus of pigeon. J Comp Neurol 208:16-36.
51. Reiner A, Perkel DJ, Mello CV, Jarvis ED. 2004. Songbirds and the revised avian brain nomenclature. Ann N Y Acad Sci 1016:77-108.
52. Rousso DL, Pearson CA, Gaber ZB, Miquelajauregui A, Li S, Portera-Cailliau C, Morrisey EE, Novitch BG. 2012. Foxp-mediated suppression of N-cadherin regulates neuroepithelial character and progenitor maintenance in the CNS. Neuron 74:314-330.
53. Scharff C, Petri J. 2011. Evo-devo, deep homology and FoxP2: implications for the evolution of speech and language. Philos Trans R Soc Lond B Biol Sci 366:2124-2140.
54. Searcy WA, Beecher MD. 2009. Song as an aggressive signal in songbirds. Anim Behav 78:1281-1292.
55. Shah R, Medina-Martinez O, Chu LF, Samaco RC, Jamrich M. 2006. Expression of FoxP2 during zebrafish development and in the adult brain. Int J Dev Biol 50:435-438.
56. Shanmugasundaram R, Selvaraj RK. 2011. Regulatory T cell properties of chicken CD4+CD25+ cells. J Immunol 186:1997-2002.
57. Shanmugasundaram R, Selvaraj RK. 2012. Regulatory T cell properties of thymic CD4+CD25+ cells in ducks. Vet Immunol Immunopathol 149:20-27.
58. Shu W, Lu MM, Zhang Y, Tucker PW, Zhou D, Morrisey EE. 2007. Foxp2 and Foxp1 cooperatively regulate lung and esophagus development. Development 134:1991-2000.
59. Takahashi K, Liu FC, Hirokawa K, Takahashi H. 2003. Expression of Foxp2, a gene involved in speech and language, in the developing and adult striatum. J Neurosci Res 73:61-72.
60. Takahashi K, Liu FC, Hirokawa K, Takahashi H. 2008a. Expression of Foxp4 in the developing and adult rat forebrain. J Neurosci Res 86:3106-3116.
61. Takahashi K, Liu FC, Oishi T, Mori T, Higo N, Hayashi M, Hirokawa K, Takahashi H. 2008b. Expression of FOXP2 in the developing monkey forebrain: comparison with the expression of the genes FOXP1, PBX3, and MEIS2. J Comp Neurol 509:180-189.
62. Tam WY, Leung CK, Tong KK, Kwan KM. 2010. Foxp4 is essential in maintenance of purkinje cell dendritic arborization in the mouse cerebellum. Neuroscience 172:562-571.
63. Tamura S, Morikawa Y, Iwanishi H, Hisaoka T, Senba E. 2003. Expression pattern of the winged-helix/forkhead transcription factor Foxp1 in the developing central nervous system. Gene Expr Patterns 3:193-197.
64. Teramitsu I, Kudo LC, London SE, Geschwind DH, White SA. 2004. Parallel FoxP1 and FoxP2 expression in songbird and human brain predicts functional interaction. J Neurosci 24:3152-3163.
65. Teramitsu I, Poopatanapong A, Torrisi S, White SA. 2010. Striatal FoxP2 is actively regulated during songbird sensorimotor learning. PLoS One 5:e8548.
66. Teufel A, Wong EA, Mukhopadhyay M, Malik N, Westphal H. 2003. FoxP4, a novel forkhead transcription factor. Biochim Biophys Acta 1627:147-152.
67. Thompson CK, Schwabe F, Schoof A, Mendoza E, Gampe J, Rochefort C, Scharff C. 2013. Young and intense: FoxP2 immunoreactivity in Area X varies with age, song stereotypy, and singing in male zebra finches. Front Neural Circuits 7:24.
68. Vargha-Khadem F, Watkins KE, Price CJ, Ashburner J, Alcock KJ, Connelly A, Frackowiak RS, Friston KJ, Pembrey ME, Mishkin M, Gadian DG, Passingham RE. 1998. Neural basis of an inherited speech and language disorder. Proc Natl Acad Sci U S A 95:12695-12700.
69. Vernes SC, Oliver PL, Spiteri E, Lockstone HE, Puliyadi R, Taylor JM, Ho J, Mombereau C, Brewer A, Lowy E, Nicod J, Groszer M, Baban D, Sahgal N, Cazier JB, Ragoussis J, Davies KE, Geschwind DH, Fisher SE. 2011. Foxp2 regulates gene networks implicated in neurite outgrowth in the developing brain. PLoS Genet 7:e1002145.
70. Wang B, Lin D, Li C, Tucker P. 2003. Multiple domains define the expression and regulatory properties of Foxp1 forkhead transcriptional repressors. J Biol Chem 278:24259-24268.
71. Wang B, Weidenfeld J, Lu MM, Maika S, Kuziel WA, Morrisey EE, Tucker PW. 2004. Foxp1 regulates cardiac outflow tract, endocardial cushion morphogenesis and myocyte proliferation and maturation. Development 131:4477-4487.
72. Watkins KE, Dronkers NF, Vargha-Khadem F. 2002. Behavioural analysis of an inherited speech and language disorder: comparison with acquired aphasia. Brain 125(Pt 3):452-464.