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Functional Diversification of Motor Neuron-specific Enhancers during Evolution


During evolution, motor neurons became specialized to control movements of different body parts including head, trunk and limbs. Here we report that two enhancers of Isl1, E1 and E2, are active together with transcription factors in motor neurons. Surprisingly, E1 and its response to transcription factors has been conserved in evolution from the lamprey to man, whereas E2 is only found in animals with limbs. Our study provides an evolutionary example of how functional diversification of motor neurons is achieved by a dynamic interplay between enhancers and transcription factors.


Vyšlo v časopise: Functional Diversification of Motor Neuron-specific Enhancers during Evolution. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005560
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005560

Souhrn

During evolution, motor neurons became specialized to control movements of different body parts including head, trunk and limbs. Here we report that two enhancers of Isl1, E1 and E2, are active together with transcription factors in motor neurons. Surprisingly, E1 and its response to transcription factors has been conserved in evolution from the lamprey to man, whereas E2 is only found in animals with limbs. Our study provides an evolutionary example of how functional diversification of motor neurons is achieved by a dynamic interplay between enhancers and transcription factors.


Zdroje

1. Jessell TM (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nature Reviews Genetics 1: 20–29. 11262869

2. Dubreuil V, Hirsch M, Pattyn A, Brunet J, Goridis C (2000) The Phox2b transcription factor coordinately regulates neuronal cell cycle exit and identity. Development 127: 5191–5201. 11060244

3. Pattyn A, Hirsch M, Goridis C, Brunet J-F (2000) Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. Development 127: 1349–1358. 10704382

4. Brunet J-F, Pattyn A (2002) Phox2 genes-from patterning to connectivity. Current Opinion in Genetics & Development 12: 435–440.

5. Thaler JP, Lee S-K, Jurata LW, Gill GN, Pfaff SL (2002) LIM factor Lhx3 contributes to the specification of motor neuron and interneuron identity through cell-type-specific protein-protein interactions. Cell 110: 237–249. 12150931

6. Dasen J, Jessell T (2009) Hox networks and the origins of motor neuron diversity. Current topics in developmental biology 88: 169–200. doi: 10.1016/S0070-2153(09)88006-X 19651305

7. Alexander T, Nolte C, Krumlauf R (2009) Hox genes and segmentation of the hindbrain and axial skeleton. Annual Review of Cell and Developmental 25: 431–456.

8. Philippidou P, Dasen J (2013) Hox Genes: Choreographers in Neural Development, Architects of Circuit Organization. Neuron 80: 12–34. doi: 10.1016/j.neuron.2013.09.020 24094100

9. Pfaff SL, Mendelsohn M, Stewart CL, Edlund T, Jessell TM (1996) Requirement for LIM Homeobox Gene Isl1 in Motor Neuron Generation Reveals a Motor Neuron–Dependent Step in Interneuron Differentiation. Cell 84: 309–320. 8565076

10. Rousso D, Gaber Z, Wellik D, Morrisey E, Novitch B (2008) Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons. Neuron 59: 226–240. doi: 10.1016/j.neuron.2008.06.025 18667151

11. Dasen JS, De Camilli A, Wang B, Tucker PW, Jessell TM (2008) Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1. Cell 134: 304–316. doi: 10.1016/j.cell.2008.06.019 18662545

12. Uemura O, Okada Y, Ando H, Guedj M, Higashijima S, et al. (2005) Comparative functional genomics revealed conservation and diversification of three enhancers of the isl1 gene for motor and sensory neuron-specific expression. Developmental biology 278: 587–606. 15680372

13. Kappen C, Salbaum JM (2009) Identification of regulatory elements in the Isl1 gene locus. The International journal of developmental biology 53: 935–946. doi: 10.1387/ijdb.082819ck 19598113

14. Dufour HD, Chettouh Z, Deyts C, de Rosa R, Goridis C, et al. (2006) Precraniate origin of cranial motoneurons. Proceedings of the National Academy of Sciences 103: 8727–8732.

15. Sugahara F, Aota S-i, Kuraku S, Murakami Y, Takio-Ogawa Y, et al. (2011) Involvement of Hedgehog and FGF signalling in the lamprey telencephalon: evolution of regionalization and dorsoventral patterning of the vertebrate forebrain. Development 138: 1217–1226. doi: 10.1242/dev.059360 21343370

16. Fetcho JR (1992) The spinal motor system in early vertebrates and some of its evolutionary changes. Brain, behavior and evolution 40: 82–97. 1422809

17. Kusakabe R, Kuratani S (2005) Evolution and developmental patterning of the vertebrate skeletal muscles: perspectives from the lamprey. Developmental dynamics 234: 824–834. 16252276

18. Freitas R, Zhang G, Cohn MJ (2006) Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442: 1033–1037. 16878142

19. Funakoshi K, Nakano M (2007) The sympathetic nervous system of anamniotes. Brain, behavior and evolution 69: 105–113. 17230018

20. Osumi N, Hirota A, Ohuchi H, Nakafuku M, Iimura T, et al. (1997) Pax-6 is involved in the specification of hindbrain motor neuron subtype. Development 124: 2961–2972. 9247338

21. Li X, Zhao X, Fang Y, Jiang X, Duong T, et al. (1998) Generation of destabilized green fluorescent protein as a transcription reporter. Journal of Biological Chemistry 273: 34970–34975. 9857028

22. Tsuchida T, Ensini M, Morton S, Baldassare M, Edlund T, et al. (1994) Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79: 957–970. 7528105

23. Stein S, Fritsch R, Lemaire L, Kessel M (1996) Checklist: vertebrate homeobox genes. Mechanisms of development 55: 91–108. 8734502

24. Arber S, Han B, Mendelsohn M, Smith M, Jessell T, et al. (1999) Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23: 659–674. 10482234

25. Dasen J, Jessell T (2008) Hox networks and the origins of motor neuron diversity. Current topics in developmental biology 88: 169–200.

26. Hoffmann S, Berger IM, Glaser A, Bacon C, Li L, et al. (2013) Islet1 is a direct transcriptional target of the homeodomain transcription factor Shox2 and rescues the Shox2-mediated bradycardia. Basic research in cardiology 108: 1–11.

27. Francius C, Clotman F (2010) Dynamic expression of the Onecut transcription factors HNF-6, OC-2 and OC-3 during spinal motor neuron development. Neuroscience 165: 116–129. doi: 10.1016/j.neuroscience.2009.09.076 19800948

28. Sander M, Paydar S, Ericson J, Briscoe J, Berber E, et al. (2000) Ventral neural patterning by Nkx homeobox genes: Nkx6. 1 controls somatic motor neuron and ventral interneuron fates. Genes & development 14: 2134–2139.

29. Ericson J, Rashbass P, Schedl A, Brenner-Morton S, Kawakami A, et al. (1997) Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90: 169–180. 9230312

30. Song M-R, Shirasaki R, Cai C-L, Ruiz EC, Evans SM, et al. (2006) T-Box transcription factor Tbx20 regulates a genetic program for cranial motor neuron cell body migration. Development 133: 4945–4955. 17119020

31. Mazzoni EO, Mahony S, Closser M, Morrison CA, Nedelec S, et al. (2013) Synergistic binding of transcription factors to cell-specific enhancers programs motor neuron identity. Nature neuroscience 16: 1219–1227. doi: 10.1038/nn.3467 23872598

32. Lee S, Lee B, Joshi K, Pfaff SL, Lee JW, et al. (2008) A regulatory network to segregate the identity of neuronal subtypes. Developmental cell 14: 877–889. doi: 10.1016/j.devcel.2008.03.021 18539116

33. Shirasaki R, Pfaff SL (2002) Transcriptional codes and the control of neuronal identity. Annual review of neuroscience 25: 251–281. 12052910

34. Hutchinson SA, Eisen JS (2006) Islet1 and Islet2 have equivalent abilities to promote motoneuron formation and to specify motoneuron subtype identity. Development 133: 2137–2147. 16672347

35. Song M-R, Sun Y, Bryson A, Gill GN, Evans SM, et al. (2009) Islet-to-LMO stoichiometries control the function of transcription complexes that specify motor neuron and V2a interneuron identity. Development 136: 2923–2932. doi: 10.1242/dev.037986 19666821

36. Novitch BG, Chen AI, Jessell TM (2001) Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31: 773–789. 11567616

37. Zhou Q, Anderson DJ (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109: 61–73. 11955447

38. Genethliou N, Panayiotou E, Panayi H, Orford M, Mean R, et al. (2009) SOX1 links the function of neural patterning and Notch signalling in the ventral spinal cord during the neuron-glial fate switch. Biochemical and biophysical research communications 390: 1114–1120. doi: 10.1016/j.bbrc.2009.08.154 19723505

39. Karunaratne A, Hargrave M, Poh A, Yamada T (2002) GATA proteins identify a novel ventral interneuron subclass in the developing chick spinal cord. Developmental biology 249: 30–43. 12217316

40. Kan L, Israsena N, Zhang Z, Hu M, Zhao L, et al. (2004) Sox1 acts through multiple independent pathways to promote neurogenesis. Developmental biology 269: 580–594. 15110721

41. Dorval KM, Bobechko BP, Fujieda H, Chen S, Zack DJ, et al. (2006) CHX10 targets a subset of photoreceptor genes. Journal of Biological Chemistry 281: 744–751. 16236706

42. Smith JJ, Kuraku S, Holt C, Sauka-Spengler T, Jiang N, et al. (2013) Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nature genetics 45: 415–421. doi: 10.1038/ng.2568 23435085

43. McEwen GK, Goode DK, Parker HJ, Woolfe A, Callaway H, et al. (2009) Early evolution of conserved regulatory sequences associated with development in vertebrates. PLoS genetics 5: e1000762. doi: 10.1371/journal.pgen.1000762 20011110

44. Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, et al. (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453: 1064–1071. doi: 10.1038/nature06967 18563158

45. Roy A, Francius C, Rousso DL, Seuntjens E, Debruyn J, et al. (2012) Onecut transcription factors act upstream of Isl1 to regulate spinal motoneuron diversification. Development 139: 3109–3119. doi: 10.1242/dev.078501 22833130

46. Jung H, Lacombe J, Mazzoni EO, Liem KF Jr, Grinstein J, et al. (2010) Global Control of Motor Neuron Topography Mediated by the Repressive Actions of a Single Hox Gene. Neuron 67: 781–796. doi: 10.1016/j.neuron.2010.08.008 20826310

47. Vincentz JW, VanDusen NJ, Fleming AB, Rubart M, Firulli BA, et al. (2012) A Phox2-and Hand2-dependent Hand1cis-regulatory element reveals a unique gene dosage requirement for Hand2 during sympathetic neurogenesis. The Journal of Neuroscience 32: 2110–2120. doi: 10.1523/JNEUROSCI.3584-11.2012 22323723

48. Lee S-K, Lee B, Ruiz EC, Pfaff SL (2005) Olig2 and Ngn2 function in opposition to modulate gene expression in motor neuron progenitor cells. Genes & Development 19: 282–294.

49. Gadd MS, Bhati M, Jeffries CM, Langley DB, Trewhella J, et al. (2011) Structural basis for partial redundancy in a class of transcription factors, the LIM homeodomain proteins, in neural cell type specification. Journal of Biological Chemistry 286: 42971–42980. doi: 10.1074/jbc.M111.248559 22025611

50. Gadd MS, Jacques DA, Nisevic I, Craig VJ, Kwan AH, et al. (2013) A structural basis for the regulation of the LIM-homeodomain protein Islet 1 (Isl1) by intra-and intermolecular interactions. Journal of Biological Chemistry 288: 21924–21935. doi: 10.1074/jbc.M113.478586 23750000

51. Sanchez-Garcia I, Osada H, Forster A, Rabbitts T (1993) The cysteine-rich LIM domains inhibit DNA binding by the associated homeodomain in Isl-1. The EMBO journal 12: 4243–4250. 7901000

52. Liu J, Hunter CS, Du A, Ediger B, Walp E, et al. (2011) Islet-1 Regulates Arx Transcription during Pancreatic Islet α-Cell Development. The Journal of Biological Chemistry 286: 15352–15360. doi: 10.1074/jbc.M111.231670 21388963

53. Zhang H, Wang W, Guo T, Yang J, Chen P, et al. (2009) The LIM-homeodomain protein ISL1 activates insulin gene promoter directly through synergy with BETA2. Journal of molecular biology 392: 566–577. doi: 10.1016/j.jmb.2009.07.036 19619559

54. Nasif S, de Souza F, González L, Yamashita M, Orquera D, et al. (2015) Islet 1 specifies the identity of hypothalamic melanocortin neurons and is critical for normal food intake and adiposity in adulthood. Proceedings of the National Academy of Sciences of the United States of America 112: E1861–1870. doi: 10.1073/pnas.1500672112 25825735

55. Giuliano P, Marino R, Pinto MR, De Santis R (1998) Identification and developmental expression of Ci-isl, a homologue of vertebrate islet genes, in the ascidian Ciona intestinalis. Mechanisms of development 78: 199–202. 9858732

56. Fetcho JR (1987) A review of the organization and evolution of motoneurons innervating the axial musculature of vertebrates. Brain Research Reviews 12: 243–280.

57. Fetcho J, Reich N (1992) Axial motor organization in postmetamorphic tiger salamanders (Ambystoma tigrinum): a segregation of epaxial and hypaxial motor pools is not necessarily associated with terrestrial locomotion. Brain, behavior and evolution 39: 219–228. 1633553

58. Jackman W, Langeland J, Kimmel C (2000) islet Reveals Segmentation in the Amphioxus Hindbrain Homolog. Developmental Biology 220: 16–26. 10720427

59. Murakami Y, Pasqualetti M, Takio Y, Hirano S, Rijli FM, et al. (2004) Segmental development of reticulospinal and branchiomotor neurons in lamprey: insights into the evolution of the vertebrate hindbrain. Development 131: 983–995. 14973269

60. Parker HJ, Bronner ME, Krumlauf R (2014) A Hox regulatory network of hindbrain segmentation is conserved to the base of vertebrates. Nature 514: 490–493. doi: 10.1038/nature13723 25219855

61. Holland LZ, Holland ND (1999) Chordate origins of the vertebrate central nervous system. Current opinion in neurobiology 9: 596–602. 10508734

62. Odom DT, Dowell RD, Jacobsen ES, Gordon W, Danford TW, et al. (2007) Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nature genetics 39: 730–732. 17529977

63. Ritter DI, Li Q, Kostka D, Pollard KS, Guo S, et al. (2010) The importance of being cis: evolution of orthologous fish and mammalian enhancer activity. Molecular biology and evolution 27: 2322–2332. doi: 10.1093/molbev/msq128 20494938

64. Jung H, Mazzoni EO, Soshnikova N, Hanley O, Venkatesh B, et al. (2014) Evolving Hox Activity Profiles Govern Diversity in Locomotor Systems. Developmental Cell 29: 171–187. doi: 10.1016/j.devcel.2014.03.008 24746670

65. Murakami Y, Tanaka M (2011) Evolution of motor innervation to vertebrate fins and limbs. Developmental biology 355: 164–172. doi: 10.1016/j.ydbio.2011.04.009 21540022

66. Eberhart J, Swartz M, Koblar SA, Pasquale E, Krull CE (2002) EphA4 constitutes a population-specific guidance cue for motor neurons. Developmental biology 247: 89–101. 12074554

67. Kania A, Jessell TM (2003) Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A: EphA interactions. Neuron 38: 581–596. 12765610

68. Mehta TK, Ravi V, Yamasaki S, Lee AP, Lian MM, et al. (2013) Evidence for at least six Hox clusters in the Japanese lamprey (Lethenteron japonicum). Proceedings of the National Academy of Sciences 110: 16044–16049.

69. Lee S-K, Jurata LW, Funahashi J, Ruiz EC, Pfaff SL (2004) Analysis of embryonic motoneuron gene regulation: derepression of general activators function in concert with enhancer factors. Development 131: 3295–3306. 15201216

70. Yasugi S, Nakamura H (2000) Gene transfer into chicken embryos as an effective system of analysis in developmental biology. Development, growth & differentiation 42: 195–197.

71. Thaler JP, Koo SJ, Kania A, Lettieri K, Andrews S, et al. (2004) A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 41: 337–350. 14766174

72. Shirasaki R, Lewcock JW, Lettieri K, Pfaff SL (2006) FGF as a target-derived chemoattractant for developing motor axons genetically programmed by the LIM code. Neuron 50: 841–853. 16772167

73. Lee B, Rizzoti K, Kwon DS, Kim S-Y, Oh S, et al. (2012) Direct transcriptional regulation of Six6 is controlled by SoxB1 binding to a remote forebrain enhancer. Developmental biology 366: 393–403. doi: 10.1016/j.ydbio.2012.04.023 22561201

74. Brudno M, Do CB, Cooper GM, Kim MF, Davydov E, et al. (2003) LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome research 13: 721–731. 12654723

75. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic acids research 32: W273–W279. 15215394

76. Loots GG, Ovcharenko I (2004) rVISTA 2.0: evolutionary analysis of transcription factor binding sites. Nucleic acids research 32: W217–W221. 15215384

77. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular biology and evolution 30: 2725–2729. doi: 10.1093/molbev/mst197 24132122

78. Pattyn A, Morin X, Cremer H, Goridis C, Brunet J-F (1997) Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124: 4065–4075. 9374403

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