Prdm12 specifies V1 interneurons through cross-repressive interactions with Dbx1 and Nkx6 genes in Xenopus

Development (Cambridge)

Volumn 142, Issue 19, 2015, Pages 3416-3428

  Thélie, Aurore ^a   Desiderio, Simon ^a   Hanotel, Julie ^a   Quigley, Ian ^b   Van Driessche, Benoit ^a   Rodari, Anthony ^a   Borromeo, Mark D ^c   Kricha, Sadia ^a   Lahaye, François ^d   Croce, Jenifer ^d   Cerda Moya, Gustavo ^e   Fernandez, Jesús Ordoño ^a   Bolle, Barbara ^a   Lewis, Katharine E ^f   Sander, Maike ^g   Pierani, Alessandra ^h   Schubert, Michael ^d   Johnson, Jane E ^c   Kintner, Christopher R ^b   Pieler, Tomas ⁱ   Van Lint, Carine ^a   Henningfeld, Kristine A ⁱ   Bellefroid, Eric J ^a   Van Campenhout, Claude ^a   more..

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d SORBONNE UNIVERSITÉ   (France)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f SYRACUSE UNIVERSITY   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h INSTITUT JACQUES MONOD   (France)

ⁱ UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Interneuron; Neurogenesis; Prdm; Spinal cord; Transcription factor

Indexed keywords

BETA TUBULIN; DBX1 PROTEIN; EARLY GROWTH RESPONSE FACTOR 2; GASTRIN RELEASING PEPTIDE RECEPTOR; GLYCINE TRANSPORTER 2; NOGGIN; RETINOIC ACID; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX6.1; TRANSCRIPTION FACTOR OTX2; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PRDM12; UNCLASSIFIED DRUG; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; CARRIER PROTEIN; COMPLEMENTARY DNA; HOMEODOMAIN PROTEIN; NERVE PROTEIN; PRDM12 PROTEIN, XENOPUS LAEVIS; PRIMER DNA;

ADULT; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BRANCHIOSTOMA; CELL FATE; EMBRYO; GENE EXPRESSION PROFILING; GENE INTERACTION; GENE OVEREXPRESSION; GENE REPRESSION; INTERNEURON; MOLECULAR CLONING; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; RHOMBENCEPHALON; RNA SEQUENCE; SPINAL CORD; UPREGULATION; XENOPUS LAEVIS; ZINC FINGER MOTIF; ANIMAL; BIOLOGY; CHICK EMBRYO; CHROMATIN IMMUNOPRECIPITATION; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; MOLECULAR GENETICS; MORPHOGENESIS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RENSHAW CELL; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; XENOPUS;

ANIMALS; BASE SEQUENCE; CARRIER PROTEINS; CHICK EMBRYO; CHROMATIN IMMUNOPRECIPITATION; COMPUTATIONAL BIOLOGY; DNA PRIMERS; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; NERVE TISSUE PROTEINS; RENSHAW CELLS; RHOMBENCEPHALON; SEQUENCE ANALYSIS, RNA; SPECIES SPECIFICITY; SPINAL CORD; XENOPUS;

EID: 84943520196     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.121871     Document Type: Article

References (51)

1. Alvarez, F. J., Jonas, P. C., Sapir, T., Hartley, R., Berrocal, M. C., Geiman, E. J., Todd, A. J. and Goulding, M. (2005). Postnatal phenotype and localization of spinal cord V1 derived interneurons. J. Comp. Neurol. 493, 177-192.
2. Baudet, C., Pozas, E., Adameyko, I., Andersson, E., Ericson, J. and Ernfors, P. (2008). Retrograde signaling onto Ret during motor nerve terminal maturation. J. Neurosci. 28, 963-975.
3. Benito-Gonzalez, A. and Alvarez, F. J. (2012). Renshaw cells and Ia inhibitory interneurons are generated at different times from p1 progenitors and differentiate shortly after exiting the cell cycle. J. Neurosci. 32, 1156-1170.
4. Borromeo, M. D., Meredith, D. M., Castro, D. S., Chang, J. C., Tung, K.-C., Guillemot, F. and Johnson, J. E. (2014). A transcription factor network specifying inhibitory versus excitatory neurons in the dorsal spinal cord. Development 141, 2803-2812.
5. Briscoe, J. and Novitch, B. G. (2008). Regulatory pathways linking progenitor patterning, cell fates and neurogenesis in the ventral neural tube. Philos. Trans. R. Soc. B Biol. Sci. 363, 57-70.
6. Burrill, J. D., Moran, L., Goulding, M. D. and Saueressig, H. (1997). PAX2 is expressed in multiple spinal cord interneurons, including a population of EN1+ interneurons that require PAX6 for their development. Development 124, 4493-4503.
7. Chang, J. C., Meredith, D. M., Mayer, P. R., Borromeo, M. D., Lai, H. C., Ou, Y.-H. and Johnson, J. E. (2013). Prdm13 mediates the balance of inhibitory and excitatory neurons in somatosensory circuits. Dev. Cell 25, 182-195.
8. Chen, Y.-C., Auer-Grumbach, M., Matsukawa, S., Zitzelsberger, M., Themistocleous, A. C., Strom, T. M., Samara, C., Moore, A. W., Cho, L. T.-Y., Young, G. T. et al. (2015). Transcriptional regulator PRDM12 is essential for human pain perception. Nat. Genet. 47, 803-808.
9. Colin, L., Dekoninck, A., Reichert, M., Calao, M., Merimi, M., Van den Broeke, A., Vierendeel, V., Cleuter, Y., Burny, A., Rohr, O. et al. (2011). Chromatin disruption in the promoter of Bovine Leukemia Virus during transcriptional activation. Nucleic Acids Res. 39, 9559-9573.
10. Coutinho, P., Pavlou, S., Bhatia, S., Chalmers, K. J., Kleinjan, D. A. and van Heyningen, V. (2011). Discovery and assessment of conserved Pax6 target genes and enhancers. Genome Res. 21, 1349-1359.
11. Davis, C. A., Haberland, M., Arnold, M. A., Sutherland, L. B., McDonald, O. G., Richardson, J. A., Childs, G., Harris, S., Owens, G. K. and Olson, E. N. (2006). PRISM/PRDM6, a transcriptional repressor that promotes the proliferative gene program in smooth muscle cells. Mol. Cell. Biol. 26, 2626-2636.
12. Dessaud, E., McMahon, A. P. and Briscoe, J. (2008). Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135, 2489-2503.
13. Dichmann, D. S. and Harland, R. M. (2011). Nkx6 genes pattern the frog neural plate and Nkx6.1 is necessary for motoneuron axon projection. Dev. Biol. 349, 378-386.
14. Durston, A. J., Timmermans, J. P. M., Hage, W. J., Hendriks, H. F. J., de Vries, N. J., Heideveld, M. and Nieuwkoop, P. D. (1989). Retinoic acid causes an anteroposterior transformation in the developing central nervous system. Nature 340, 140-144.
15. Ericson, J., Rashbass, P., Schedl, A., Brenner-Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M. and Briscoe, J. (1997). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169-180.
16. Fog, C. K., Galli, G. G. and Lund, A. H. (2012). PRDMproteins: important players in differentiation and disease. Bioessays 34, 50-60.
17. Francius, C., Harris, A., Rucchin, V., Hendricks, T. J., Stam, F. J., Barber, M., Kurek, D., Grosveld, F. G., Pierani, A., Goulding, M. et al. (2013). Identification of multiple subsets of ventral interneurons and differential distribution along the rostrocaudal axis of the developing spinal cord. PLoS ONE 8, e70325.
18. Gosgnach, S., Lanuza, G. M., Butt, S. J. B., Saueressig, H., Zhang, Y., Velasquez, T., Riethmacher, D., Callaway, E. M., Kiehn, O. and Goulding, M. (2006). V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440, 215-219.
19. Goulding, M. (2009). Circuits controlling vertebrate locomotion: moving in a new direction. Nat. Rev. Neurosci. 10, 507-518.
20. Grillner, S. and Jessell, T. M. (2009). Measured motion: searching for simplicity in spinal locomotor networks. Curr. Opin. Neurobiol. 19, 572-586.
21. Győry, I., Wu, J., Fejér, G., Seto, E. and Wright, K. L. (2004). PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat. Immunol. 5, 299-308.
22. Hanotel, J., Bessodes, N., Thélie, A., Hedderich, M., Parain, K., Driessche, B. V., Brandão, K. D. O., Kricha, S., Jorgensen, M. C., Grapin-Botton, A. et al. (2014). The Prdm13 histone methyltransferase encoding gene is a Ptf1a-Rbpj downstream target that suppresses glutamatergic and promotes GABAergic neuronal fate in the dorsal neural tube. Dev. Biol. 386, 340-357.
23. Higashijima, S.-i., Masino, M. A., Mandel, G. and Fetcho, J. R. (2004). Engrailed-1 expression marks a primitive class of inhibitory spinal interneuron. J. Neurosci. 24, 5827-5839.
24. Hohenauer, T. and Moore, A.W. (2012). The Prdm family: expanding roles in stem cells and development. Development 139, 2267-2282.
25. Kinameri, E., Inoue, T., Aruga, J., Imayoshi, I., Kageyama, R., Shimogori, T. and Moore, A.W. (2008). Prdm proto-oncogene transcription factor family expression and interaction with the Notch-Hes pathway in mouse neurogenesis. PLoS ONE 3, e3859.
26. Li, W.-C., Higashijima, S.-i., Parry, D. M., Roberts, A. and Soffe, S. R. (2004). Primitive roles for inhibitory interneurons in developing frog spinal cord. J. Neurosci. 24, 5840-5848.
27. Lu, S., Shashikant, C. S. and Ruddle, F. H. (1996). Separate cis-acting elements determine the expression of mouse DBX gene in multiple spatial domains of the central nervous system. Mech. Dev. 58, 193-202.
28. Ma, P., Zhao, S., Zeng, W., Yang, Q., Li, C., Lv, X., Zhou, Q. and Mao, B. (2011). Xenopus Dbx2 is involved in primary neurogenesis and early neural plate patterning. Biochem. Biophys. Res. Commun. 412, 170-174.
29. Ma, P., Xia, Y., Ma, L., Zhao, S. and Mao, B. (2013). Xenopus Nkx6.1 and Nkx6.2 are required for mid-hindbrain boundary development. Dev. Genes Evol. 223, 253-259.
30. Ma, L., Quigley, I., Omran, H. and Kintner, C. (2014). Multicilin drives centriole biogenesis via E2f proteins. Genes Dev. 28, 1461-1471.
31. Matise, M. P. and Joyner, A. L. (1997). Expression patterns of developmental control genes in normal and Engrailed-1 mutant mouse spinal cord reveal early diversity in developing interneurons. J. Neurosci. 17, 7805-7816.
32. Matsukawa, S., Miwata, K., Asashima, M. and Michiue, T. (2015). The requirement of histone modification by PRDM12 and Kdm4a for the development of pre-placodal ectoderm and neural crest in Xenopus. Dev. Biol. 399, 164-176.
33. Missler, M. and Südhof, T. C. (1998). Neurexophilins form a conserved family of neuropeptide-like glycoproteins. J. Neurosci. 18, 3630-3638.
34. Nagy, V., Cole, T., Van Campenhout, C., Khoung, T. M., Leung, C., Vermeiren, S., Novatchkova, M., Wenzel, D., Cikes, D., Polyansky, A. A. et al. (2015). The evolutionarily conserved transcription factor PRDM12 controls sensory neuron development and pain perception. Cell Cycle 14, 1799-1808.
35. Oulion, S., Bertrand, S., Belgacem, M. R., Le Petillon, Y. and Escriva, H. (2012). Sequencing and analysis of the Mediterranean amphioxus (Branchiostoma lanceolatum) transcriptome. PLoS ONE 7, e36554.
36. Pierani, A., Brenner-Morton, S., Chiang, C. and Jessell, T. M. (1999). A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97, 903-915.
37. Pierani, A., Moran-Rivard, L., Sunshine, M. J., Littman, D. R., Goulding, M. and Jessell, T. M. (2001). Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29, 367-384.
38. Rungger-Brändle, E., Ripperger, J. A., Steiner, K., Conti, A., Stieger, A., Soltanieh, S. and Rungger, D. (2010). Retinal patterning by Pax6-dependent cell adhesion molecules. Dev. Neurobiol. 70, 764-780.
39. Sander, M., Paydar, S., Ericson, J., Briscoe, J., Berber, E., German, M., Jessell, T. M. and Rubenstein, J. L. (2000). Ventral neural patterning by Nkx homeobox genes: Nkx6.1 controls somatic motor neuron and ventral interneuron fates. Genes Dev. 14, 2134-2139.
40. Saueressig, H., Burrill, J. and Goulding, M. (1999). Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 126, 4201-4212.
41. Siembab, V. C., Smith, C. A., Zagoraiou, L., Berrocal, M. C., Mentis, G. Z. and Alvarez, F. J. (2010). Target selection of proprioceptive and motor axon synapses on neonatal V1-derived Ia inhibitory interneurons and Renshaw cells. J. Comp. Neurol. 518, 4675-4701.
42. Smith, S. T. and Jaynes, J. B. (1996). A conserved region of engrailed, shared among all en-, gsc-, Nk1-, Nk2-and msh-class homeoproteins, mediates active transcriptional repression in vivo. Development 122, 3141-3150.
43. Triezenberg, S. J., Kingsbury, R. C. and McKnight, S. L. (1988). Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression. Genes Dev. 2, 718-729.
44. Vallstedt, A., Muhr, J., Pattyn, A., Pierani, A., Mendelsohn, M., Sander, M., Jessell, T. M. and Ericson, J. (2001). Different levels of repressor activity assign redundant and specific roles to Nkx6 genes in motor neuron and interneuron specification. Neuron 31, 743-755.
45. Vincent, S. D., Mayeuf, A., Niro, C., Saitou, M. and Buckingham, M. (2012). Non conservation of function for the evolutionarily conserved prdm1 protein in the control of the slow twitch myogenic program in the mouse embryo. Mol. Biol. Evol. 29, 3181-3191.
46. Visel, A., Minovitsky, S., Dubchak, I. and Pennacchio, L. A. (2007). VISTA Enhancer Browser-a database of tissue-specific human enhancers. Nucleic Acids Res. 35, D88-D92.
47. Walton, N. M., de Koning, A., Xie, X., Shin, R., Chen, Q., Miyake, S., Tajinda, K., Gross, A. K., Kogan, J. H., Heusner, C. L. et al. (2014). Gastrin-releasing peptide contributes to the regulation of adult hippocampal neurogenesis and neuronal development. Stem Cells 32, 2454-2466.
48. Wenner, P., O'Donovan, M. J. and Matise, M. P. (2000). Topographical and physiological characterization of interneurons that express engrailed-1 in the embryonic chick spinal cord. J. Neurophysiol. 84, 2651-2657.
49. Yang, C. M. and Shinkai, Y. (2013). Prdm12 is induced by retinoic acid and exhibits anti-proliferative properties through the cell cycle modulation of P19 embryonic carcinoma cells. Cell Struct. Funct. 38, 195-204.
50. Zannino, D. A., Downes, G. B. and Sagerström, C. G. (2014). prdm12b specifies the p1 progenitor domain and reveals a role for V1 interneurons in swim movements. Dev. Biol. 390, 247-260.
51. Zhang, J., Lanuza, G. M., Britz, O., Wang, Z., Siembab, V. C., Zhang, Y., Velasquez, T., Alvarez, F. J., Frank, E. and Goulding, M. (2014). V1 and v2b interneurons secure the alternating flexor-extensor motor activity mice require for limbed locomotion. Neuron 82, 138-150.