A transcription factor code defines nine sensory interneuron subtypes in the mechanosensory area of the spinal cord

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Del Barrio, Marta Garcia ^a   Bourane, Steeve ^a   Grossmann, Katja ^a   Schüle, Roland ^b   Britsch, Stefan ^c,d   O'Leary, Dennis D M ^a   Goulding, Martyn ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d UNIVERSITY OF ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOID RELATED ORPHAN RECEPTOR ALPHA; RETINOID RELATED ORPHAN RECEPTOR BETA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR C MAF; TRANSCRIPTION FACTOR GBX1; TRANSCRIPTION FACTOR LBX1; TRANSCRIPTION FACTOR LMX1B; TRANSCRIPTION FACTOR MAFA; TRANSCRIPTION FACTOR MAFB; TRANSCRIPTION FACTOR PAX2; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL TYPE; CONTROLLED STUDY; EXCITATORY INTERNEURON; GENETIC MANIPULATION; INHIBITORY INTERNEURON; INTERNEURON; MOUSE; NOCICEPTION; NONHUMAN; PAIN RECEPTOR; RENSHAW CELL; SENSORY SYSTEM; SKIN RECEPTOR; SOMATOSENSORY SYSTEM; SPINAL CORD NERVE CELL; TEMPERATURE SENSE; TOUCH;

ANIMALS; INTERNEURONS; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, TRANSGENIC; POSTERIOR HORN CELLS; SENSORY RECEPTOR CELLS; SPINAL CORD; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84892421746     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077928     Document Type: Article

References (67)

1. Brown AG (1981) Organization in the Spinal Cord. Berlin, Germany: Springer-Verlag.
2. Willis W, Coggeshall R (2004) Sensory Mechanisms of the Spinal Cord. 3 ed. New York: Kluwer Academic/Plenum.
3. Fitzgerald M (2005) The development of nociceptive circuits. Nat Rev Neurosci 6: 507-520.
4. Zylka MJ, Rice FL, Anderson DJ (2005) Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 45: 17-25.
5. Chen C, Broom DC, Liu Y, de Nooij JC, Li Z, et al. (2006) Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron 49: 365-377.
6. Basbaum AI, Bautista DM, Scherrer G, Julius D (2009) Cellular and molecular mechanisms of pain Cell 139, 267-284.
7. Todd AJ (2010) Neuronal circuitry for pain processing in the dorsal horn. Nat Rev Neurosci 11: 823-836.
8. Li L, Rutlin M, Abraira VE, Cassidy C, Kus L, et al. (2011) The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147: 1615-1627.
9. Jankowska E (1992). Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38, 335-378.
10. Arber S, Ladle DR, Lin JH, Frank E, Jessell TM (2000) ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 101: 485-498.
11. Gross MK, Dottori M, Goulding M (2002) Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34: 535-549.
12. Muller T, Brohmann H, Pierani A, Heppenstall PA, Lewin GR, et al. (2002) The homeodomain factor lbx1 distinguishes two major programs of neuronal differentiation in the dorsal spinal cord. Neuron 34: 551-562.
13. Chen ZF, Rebelo S, White F, Malmberg AB, Baba H, et al. (2001) The paired homeodomain protein DRG11 is required for the projection of cutaneous sensory afferent fibers to the dorsal spinal cord. Neuron 31: 59-73.
14. Cheng L, Arata A, Mizuguchi R, Qian Y, Karunaratne A, et al. (2004) Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat Neurosci 7: 510-517.
15. Ding YQ, Yin J, Kania A, Zhao ZQ, Johnson RL, et al. (2004) Lmx1b controls the differentiation and migration of the superficial dorsal horn neurons of the spinal cord. Development 131: 3693-3703.
16. Li MZ, Wang JS, Jiang DJ, Xiang CX, Wang FY, et al. (2006) Molecular mapping of developing dorsal horn-enriched genes by microarray and dorsal/ ventral subtractive screening. Dev Biol 292: 555-564.
17. Goulding M (2009) Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci 10: 507-518.
18. Grillner S, Jessell TM (2009) Measured motion: searching for simplicity in spinal locomotor networks. Curr Opin Neurobiol 19: 572-586.
19. Grossmann KS, Giraudin A, Britz O, Zhang J, Goulding M (2010) Genetic dissection of rhythmic motor networks in mice. Prog Brain Res 187: 19-37.
20. Ohyama T, Groves AK (2004) Generation of Pax2-Cre mice by modification of a Pax2 bacterial artificial chromosome. Genesis 38: 195-199.
21. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133-140.
22. Blanchi B, Kelly LM, Viemari JC, Lafon I, Burnet H, et al. (2003) MafB deficiency causes defective respiratory rhythmogenesis and fatal central apnea at birth. Nat Neurosci 6: 1091-1100.
23. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, et al. (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467: 60-79.
24. Chen H, Lun Y, Ovchinnikov D, Kokubo H, Oberg KC, et al. (1998) Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nat Genet 19: 51-55.
25. Chou SJ, Babot Z, Leingartner A, Studer M, Nakagawa Y, et al. (2013) Geniculocortical input derives genetic distinctions between primary and higherorder visual areas. Science 340: 1239-1242.
26. Cheng L, Arata A, Mizuguchi R, Qian Y, Karunaratne A, et al. (2004) Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat Neurosci 7: 510-517.
27. Cheng L, Samad OA, Xu Y, Mizuguchi R, Luo P, et al. (2005) Lbx1 and Tlx3 are opposing switches in determining GABAergic versus glutamatergic transmitter phenotypes. Nat Neurosci 8: 1510-1515.
28. Pillai A, Mansouri A, Behringer R, Westphal H, Goulding M (2007) Lhx1 and Lhx5 maintain the inhibitory-neurotransmitter status of interneurons in the dorsal spinal cord. Development 134: 357-366.
29. Huang M, Huang T, Xiang Y, Xie Z, Chen Y, et al. (2008) Ptf1a, Lbx1 and Pax2 coordinate glycinergic and peptidergic transmitter phenotypes in dorsal spinal inhibitory neurons. Dev Biol 322: 394-405.
30. John A, Wildner H, Britsch S (2005) The homeodomain transcription factor Gbx1 identifies a subpopulation of late-born GABAergic interneurons in the developing dorsal spinal cord. Dev Dyn 234: 767-771.
31. Sakai M, Imaki J, Yoshida K, Ogata A, Matsushima-Hibaya Y, et al. (1997) Rat maf related genes: specific expression in chondrocytes, lens and spinal cord. Oncogene 14: 745-750.
32. Stam FJ, Hendricks TJ, Zhang J, Geiman EJ, Francius C, et al. (2012) Renshaw cell interneuron specialization is controlled by a temporally restricted transcription factor program. Development 139: 179-190.
33. Varoqui H, Schafer MK, Zhu H, Weihe E, Erickson JD (2002) Identification of the differentiation-associated Na+/PI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 22: 142-155.
34. Todd AJ, Hughes DI, Polgar E, Nagy GG, Mackie M, et al. (2003) The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17: 13-27.
35. Alvarez FJ, Villalba RM, Zerda R, Schneider SP (2004) Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses. J Comp Neurol 472: 257-280.
36. Hang Y, Stein R (2011) MafA and MafB activity in pancreatic beta cells. Trends Endocrinol Metab 22: 364-373.
37. Li Y, Zhao LJ, Xia FZ, Li YX, Lu YL (2012) Transdifferentiation of hepatic oval cells into pancreatic islet beta-cells. Front Biosci 17: 2391-2395.
38. Aziz A, Soucie E, Sarrazin S, Sieweke MH (2009) MafB/c-Maf deficiency enables self-renewal of differentiated functional macrophages. Science 326: 867-871.
39. Han SI, Yasuda K, Kataoka K (2011) ATF2 interacts with beta-cell-enriched transcription factors, MafA, Pdx1, and beta2, and activates insulin gene transcription. J Biol Chem 286: 10449-10456.
40. Yang Y, Cvekl A (2007) Large Maf Transcription Factors: Cousins of AP-1 Proteins and Important Regulators of Cellular Differentiation. Einstein J Biol Med 23: 2-11.
41. Kanai K, Reza HM, Kamitani A, Hamazaki Y, Han SI, et al. (2010) SUMOylation negatively regulates transcriptional and oncogenic activities of MafA. Genes Cells 15: 971-982.
42. Wende H, Lechner SG, Cheret C, Bourane S, Kolanczyk ME, et al. (2012) The transcription factor c-Maf controls touch receptor development and function. Science 335: 1373-1376.
43. Jetten AM (2009) Retinoid-related orphan receptors (RORs): critical roles in development, immunity, circadian rhythm, and cellular metabolism. Nucl Recept Signal 7: e003.
44. Hochman S, Garraway SM, Pockett S (1997) Membrane properties of deep dorsal horn neurons from neonatal rat spinal cord in vitro. Brain Res 767: 214-219.
45. Jiang MC, Cleland CL, Gebhart GF (1995) Intrinsic properties of deep dorsal horn neurons in the L6-S1 spinal cord of the intact rat. J Neurophysiol 74: 1819-1827.
46. Schneider SP (1992) Functional properties and axon terminations of interneurons in laminae III-V of the mammalian spinal dorsal horn in vitro. J Neurophysiol 68: 1746-1759.
47. Schneider SP (2003) Spike frequency adaptation and signaling properties of identified neurons in rodent deep spinal dorsal horn. J Neurophysiol 90: 245-258.
48. Schneider SP (2005) Mechanosensory afferent input and neuronal firing properties in rodent spinal laminae III-V: re-examination of relationships with analysis of responses to static and time-varying stimuli. Brain Res 1034: 71-89.
49. Watson C, Paxinos G, Kayalioglu G, editors (2009) The spinal cord: Academic press.
50. Altman J, Bayer SA (2001) Development of the Human Spinal Cord: An Interpretation Based on Experimental Studies in Animals: Oxford University Press.
51. Ramon y Cajal S, editor (1909) Histology of the Nervous System of Man and Vertebrates New York: Oxford University Press.
52. Yasaka T, Tiong SY, Hughes DI, Riddell JS, Todd AJ (2010) Populations of inhibitory and excitatory interneurons in lamina II of the adult rat spinal dorsal horn revealed by a combined electrophysiological and anatomical approach. Pain 151: 475-488.
53. Brohl D, Strehle M, Wende H, Hori K, Bormuth I, et al. (2008) A transcriptional network coordinately determines transmitter and peptidergic fate in the dorsal spinal cord. Dev Biol 322: 381-393.
54. Xu Y, Lopes C, Qian Y, Liu Y, Cheng L, et al. (2008) Tlx1 and Tlx3 coordinate specification of dorsal horn pain-modulatory peptidergic neurons. J Neurosci 28: 4037-4046.
55. Antal M, Polgar E, Chalmers J, Minson JB, Llewellyn-Smith I, et al. (1991) Different populations of parvalbumin- and calbindin-D28k-immunoreactive neurons contain GABA and accumulate 3H-D-aspartate in the dorsal horn of the rat spinal cord. J Comp Neurol 314: 114-124.
56. Sardella TC, Polgar E, Watanabe M, Todd AJ (2011) A quantitative study of neuronal nitric oxide synthase expression in laminae I-III of the rat spinal dorsal horn. Neuroscience 192: 708-720.
57. Al-Khater KM, Kerr R, Todd AJ (2008) A quantitative study of spinothalamic neurons in laminae I, III, and IV in lumbar and cervical segments of the rat spinal cord. J Comp Neurol 511: 1-18.
58. Hu J, Huang T, Li T, Guo Z, Cheng L (2012) c-Maf is required for the development of dorsal horn laminae III/IV neurons and mechanoreceptive DRG axon projections. J Neurosci 32: 5362-5373.
59. Glasgow SM, Henke RM, Macdonald RJ, Wright CV, Johnson JE (2005) Ptf1a determines GABAergic over glutamatergic neuronal cell fate in the spinal cord dorsal horn. Development 132: 5461-5469.
60. Waters ST, Wilson CP, Lewandoski M (2003) Cloning and embryonic expression analysis of the mouse Gbx1 gene. Gene Expr Patterns 3: 313-317.
61. Rhinn M, Lun K, Werner M, Simeone A, Brand M (2004) Isolation and expression of the homeobox gene Gbx1 during mouse development. Dev Dyn 229: 334-339.
62. Lecoin L, Rocques N, El-Yakoubi W, Ben Achour S, Larcher M, et al. (2010) MafA transcription factor identifies the early ret-expressing sensory neurons. Dev Neurobiol 70: 485-497.
63. Eichmann A, Grapin-Botton A, Kelly L, Graf T, Le Douarin NM, et al. (1997) The expression pattern of the mafB/kr gene in birds and mice reveals that the kreisler phenotype does not represent a null mutant. Mech Dev 65: 111-122.
64. Qian Y, Shirasawa S, Chen CL, Cheng L, Ma Q (2002) Proper development of relay somatic sensory neurons and D2/D4 interneurons requires homeobox genes Rnx/Tlx-3 and Tlx-1. Genes Dev 16: 1220-1233.
65. Schouenborg J (2008) Action-based sensory encoding in spinal sensorimotor circuits. Brain Res Rev 57: 111-117.
66. Kania A, Johnson RL, Jessell TM (2000) Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102: 161-173.
67. Xiang C, Zhang KH, Yin J, Arends JJ, Erzurumlu RS, et al. (2010) The transcription factor, Lmx1b, is necessary for the development of the principal trigeminal nucleus-based lemniscal pathway. Mol Cell Neurosci 44: 394-403.