Positional differences of axon growth rates between sensory neurons encoded by runx3

EMBO Journal

Volumn 31, Issue 18, 2012, Pages 3718-3729

  Lallemend, Francois ^a   Sterzenbach, Ulrich ^a   Hadjab Lallemend, Saida ^a   Aquino, Jorge B ^a,d   Castelo Branco, Goncalo ^a   Sinha, Indranil ^a   Villaescusa, J Carlos ^a   Levanon, Ditsa ^b   Wang, Yiqiao ^a   Franck, Marina C M ^a   Kharchenko, Olga ^a   Adameyko, Igor ^a   Linnarsson, Sten ^a   Groner, Yoram ^b   Turner, Eric ^c   Ernfors, Patrik ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^d UNIVERSIDAD AUSTRAL   (Argentina)

Author keywords

axon growth; development; intrinsic; Runx3; sensory neurons

Indexed keywords

TRANSCRIPTION FACTOR RUNX3;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GROWTH RATE; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SPINAL GANGLION;

ANIMALS; AXONS; CELL PROLIFERATION; CHICK EMBRYO; CORE BINDING FACTOR ALPHA 3 SUBUNIT; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; MICE; MICE, TRANSGENIC; MODELS, GENETIC; NERVOUS SYSTEM; NEURONS; RNA; SENSORY RECEPTOR CELLS; TIME FACTORS;

VERTEBRATA;

EID: 84866392794     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.228     Document Type: Article

References (61)

1. 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
2. Bachy I, Franck MC, Li L, Abdo H, Pattyn A, Ernfors P (2011) The transcription factor Cux2 marks development of an A-delta sub-lineage of TrkA sensory neurons. Dev Biol 360: 77-86
3. Bae SC, Ogawa E, Maruyama M, Oka H, Satake M, Shigesada K, Jenkins NA, Gilbert DJ, Copeland NG, Ito Y (1994) PEBP2 alpha B/mouse AML1 consists of multiple isoforms that possess differential transactivation potentials. Mol Cell Biol 14: 3242-3252
4. Bannert N, Vollhardt K, Asomuddinov B, Haag M, Konig H, Norley S, Kurth R (2003) PDZ Domain-mediated interaction of interleukin-16 precursor proteins with myosin phosphatase targeting subunits. J Biol Chem 278: 42190-42199 (Pubitemid 37310485)
5. Caldero J, Prevette D, Mei X, Oakley RA, Li L, Milligan C, Houenou L, Burek M, Oppenheim RW (1998) Peripheral target regulation of the development and survival of spinal sensory and motor neurons in the chick embryo. J Neurosci 18: 356-370 (Pubitemid 28046794)
6. Chen AI, de Nooij JC, Jessell TM (2006) Graded activity of transcription factor Runx3 specifies the laminar termination pattern of sensory axons in the developing spinal cord. Neuron 49: 395-408 (Pubitemid 43152241)
7. Conde C, Caceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10 : 319-332
8. Davies AM (1989) Intrinsic differences in the growth rate of early nerve fibres related to target distance. Nature 337: 553-555 (Pubitemid 19045538)
9. De Marco Garcia NV, Jessell TM (2008) Early motor neuron pool identity and muscle nerve trajectory defined by postmitotic restrictions in Nkx6.1 activity. Neuron 57: 217-231
10. Dickson BJ (2002) Molecular mechanisms of axon guidance. Science 298: 1959-1964 (Pubitemid 35425245)
11. Ernfors P, Lee KF, Kucera J, Jaenisch R (1994) Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 77: 503-512 (Pubitemid 24153991)
12. Even-Ram S, Doyle AD, Conti MA, Matsumoto K, Adelstein RS, Yamada KM (2007) Myosin IIA regulates cell motility and acto-myosin-microtubule crosstalk. Nat Cell Biol 9: 299-309 (Pubitemid 46344609)
13. Genc B, Ozdinler PH, Mendoza AE, Erzurumlu RS (2004) A chemoattractant role for NT-3 in proprioceptive axon guidance. PLoS Biol 2: e403
14. Giannone G, Dubin-Thaler BJ, Rossier O, Cai Y, Chaga O, Jiang G, Beaver W, Dobereiner HG, Freund Y, Borisy G, Sheetz MP (2007) Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128: 561-575 (Pubitemid 46198897)
15. Graef IA, Wang F, Charron F, Chen L, Neilson J, Tessier-Lavigne M, Crabtree GR (2003) Neurotrophins and netrins require calcineur-in/NFAT signaling to stimulate outgrowth of embryonic axons. Cell 113: 657-670 (Pubitemid 36694190)
16. Guan W, Puthenveedu MA, Condic ML (2003) Sensory neuron subtypes have unique substratum preference and receptor expression before target innervation. J Neurosci 23: 1781-1791 (Pubitemid 36314733)
17. Hippenmeyer S, Shneider NA, Birchmeier C, Burden SJ, Jessell TM, Arber S (2002) A role for neuregulin1 signaling in muscle spindle differentiation. Neuron 36: 1035-1049 (Pubitemid 36044506)
18. Hjerling-Leffler J, Marmigere F, Heglind M, Cederberg A, Koltzenburg M, Enerback S, Ernfors P (2005) The boundary cap: a source of neural crest stem cells that generate multiple sensory neuron subtypes. Development 132: 2623-2632 (Pubitemid 40883260)
19. Honig MG, Frase PA, Camilli SJ (1998) The spatial relationships among cutaneous, muscle sensory and motoneuron axons during development of the chick hindlimb. Development 125: 995-1004 (Pubitemid 28171194)
20. Huang da W, Sherman BT, Tan Q, Collins JR, Alvord WG, Roayaei J, Stephens R, Baseler MW, Lane HC, Lempicki RA (2007a) The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol 8: R183
21. Huang da W, Sherman BT, Tan Q, Kir J, Liu D, Bryant D, Guo Y, Stephens R, Baseler MW, Lane HC, Lempicki RA (2007b) DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res 35: W169-W175
22. Huber AB, Kania A, Tran TS, Gu C, De Marco Garcia N, Lieberam I, Johnson D, Jessell TM, Ginty DD, Kolodkin AL (2005) Distinct roles for secreted semaphorin signaling in spinal motor axon guidance. Neuron 48: 949-964 (Pubitemid 41814699)
23. Huber AB, Kolodkin AL, Ginty DD, Cloutier JF (2003) Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 26: 509-563 (Pubitemid 37064943)
24. Inoue K, Ozaki S, Shiga T, Ito K, Masuda T, Okado N, Iseda T, Kawaguchi S, Ogawa M, Bae SC, Yamashita N, Itohara S, Kudo N, Ito Y (2002) Runx3 controls the axonal projection of propriocep-tive dorsal root ganglion neurons. Nat Neurosci 5: 946-954
25. Jacobson M, Huang S (1985) Neurite outgrowth traced by means of horseradish peroxidase inherited from neuronal ancestral cells in frog embryos. Dev Biol 11 0 : 102-113 (Pubitemid 15013814)
26. 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
27. Kovacs M, Toth J, Hetenyi C, Malnasi-Csizmadia A, Sellers JR (2004) Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279: 35557-35563 (Pubitemid 39100557)
28. Kramer ER, Knott L, Su F, Dessaud E, Krull CE, Helmbacher F, Klein R (2006a) Cooperation between GDNF/Ret and ephrinA/EphA4 signals for motor-axon pathway selection in the limb. Neuron 50: 35-47
29. Kramer I, Sigrist M, de Nooij JC, Taniuchi I, Jessell TM, Arber S (2006b) A role for Runx transcription factor signaling in dorsal root ganglion sensory neuron diversification. Neuron 49: 379-393 (Pubitemid 43152240)
30. Kucera J, Fan G, Jaenisch R, Linnarsson S, Ernfors P (1995) Dependence of developing group Ia afferents on neurotrophin-3. J Comp Neurol 363: 307-320
31. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25
32. Lawson SN, Biscoe TJ (1979) Development of mouse dorsal root ganglia: an autoradiographic and quantitative study. J Neurocytol 8: 265-274 (Pubitemid 9198407)
33. Ledda F, Bieraugel O, Fard SS, Vilar M, Paratcha G (2008) Lrig1 is an endogenous inhibitor of Ret receptor tyrosine kinase activation, downstream signaling, and biological responses to GDNF. J Neurosci 28: 39-49
34. Lefcort F, Clary DO, Rusoff AC, Reichardt LF (1996) Inhibition of the NT-3 receptor TrkC, early in chick embryogenesis, results in severe reductions in multiple neuronal subpopulations in the dorsal root ganglia. J Neurosci 16: 3704-3713 (Pubitemid 26149506)
35. Levanon D, Bettoun D, Harris-Cerruti C, Woolf E, Negreanu V, Eilam R, Bernstein Y, Goldenberg D, Xiao C, Fliegauf M, Kremer E, Otto F, Brenner O, Lev-Tov A, Groner Y (2002) The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J 21: 3454-3463 (Pubitemid 34760577)
36. Lin JH, Saito T, Anderson DJ, Lance-Jones C, Jessell TM, Arber S (1998) Functionally related motor neuron pool and muscle sensory afferent subtypes defined by coordinate ETS gene expression. Cell 95: 393-407 (Pubitemid 28507327)
37. Lumsden AG, Davies AM (1983) Earliest sensory nerve fibres are guided to peripheral targets by attractants other than nerve growth factor. Nature 306: 786-788 (Pubitemid 14206043)
38. Luria V, Krawchuk D, Jessell TM, Laufer E, Kania A (2008) Specification of motor axon trajectory by ephrin-B:EphB signaling: symmetrical control of axonal patterning in the developing limb. Neuron 60: 1039-1053
39. Marmigere F, Ernfors P (2007) Specification and connectivity of neuronal subtypes in the sensory lineage. Nat Rev Neurosci 8: 114-127 (Pubitemid 46146950)
40. Marmigere F, Montelius A, Wegner M, Groner Y, Reichardt LF, Ernfors P (2006) The Runx1/AML1 transcription factor selectively regulates development and survival of TrkA nociceptive sensory neurons. Nat Neurosci 9: 180-187 (Pubitemid 43164540)
41. Meyers S, Lenny N, Hiebert SW (1995) The t(8;21) fusion protein interferes with AML-1B-dependent transcriptional activation. Mol Cell Biol 15: 1974-1982
42. Montelius A, Marmigere F, Baudet C, Aquino JB, Enerback S, Ernfors P (2007) Emergence of the sensory nervous system as defined by Foxs1 expression. Differentiation 75: 404-417 (Pubitemid 46802158)
43. Moret F, Renaudot C, Bozon M, Castellani V (2007) Semaphorin and neuropilin co-expression in motoneurons sets axon sensitivity to environmental semaphorin sources during motor axon pathfind-ing. Development 134: 4491-4501
44. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628 (Pubitemid 351911867)
45. O'Donnell M, Chance RK, Bashaw GJ (2009) Axon growth and guidance: receptor regulation and signal transduction. Annu Rev Neurosci 32: 383-412
46. Patel TD, Jackman A, Rice FL, Kucera J, Snider WD (2000) Development of sensory neurons in the absence of NGF/TrkA signaling in vivo. Neuron 25: 345-357
47. Patel TD, Kramer I, Kucera J, Niederkofler V, Jessell TM, Arber S, Snider WD (2003) Peripheral NT3 signaling is required for ETS protein expression and central patterning of proprioceptive sensory afferents. Neuron 38: 403-416 (Pubitemid 36579143)
48. Polleux F, Snider W (2010) Initiating and growing an axon. Cold Spring Harb Perspect Biol 2: a001925
49. Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G (2004) Two distinct actin networks drive the protrusion of migrating cells. Science 305: 1782-1786 (Pubitemid 39249647)
50. Quina LA, Pak W, Lanier J, Banwait P, Gratwick K, Liu Y, Velasquez T, O'Leary DD, Goulding M, Turner EE (2005) Brn3a-expressing retinal ganglion cells project specifically to thalamocortical and collicular visual pathways. J Neurosci 25: 11595-11604 (Pubitemid 43098452)
51. Sharma K, Leonard AE, Lettieri K, Pfaff SL (2000) Genetic and epigenetic mechanisms contribute to motor neuron pathfinding. Nature 406: 515-519 (Pubitemid 30625735)
52. Sherman BT, Huang da W, Tan Q, Guo Y, Bour S, Liu D, Stephens R, Baseler MW, Lane HC, Lempicki RA (2007) DAVID Knowledgebase: a gene-centered database integrating heterogeneous gene annotation resources to facilitate high-throughput gene functional analysis. BMC Bioinformatics 8: 426
53. Stenqvist A, Agerman K, Marmigere F, Minichiello L, Ernfors P (2005) Genetic evidence for selective neurotrophin 3 signalling through TrkC but not TrkB in vivo. EMBO Rep 6: 973-978 (Pubitemid 41521954)
54. Tanaka E, Ho T, Kirschner MW (1995a) The role of microtubule dynamics in growth cone motility and axonal growth. J Cell Biol 128: 139-155
55. Tanaka EM, Kirschner MW (1991) Microtubule behavior in the growth cones of living neurons during axon elongation. J Cell Biol 115: 345-363 (Pubitemid 21926032)
56. Tanaka T, Tanaka K, Ogawa S, Kurokawa M, Mitani K, Nishida J, Shibata Y, Yazaki Y, Hirai H (1995b) An acute myeloid leukemia gene, AML1, regulates hemopoietic myeloid cell differentiation and transcriptional activation antagonistically by two alternative spliced forms. EMBO J 14: 341-350
57. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nature reviews. Mol Cell Biol 10: 778-790
58. Vicente-Manzanares M, Zareno J, Whitmore L, Choi CK, Horwitz AF (2007) Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J Cell Biol 176: 573-580 (Pubitemid 46333973)
59. Wang G, Scott SA (2000) The 'waiting period' of sensory and motor axons in early chick hindlimb: its role in axon pathfinding and neuronal maturation. J Neurosci 20: 5358-5366 (Pubitemid 30457733)
60. White FA, Keller-Peck CR, Knudson CM, Korsmeyer SJ, Snider WD (1998) Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J Neurosci 18: 1428-1439 (Pubitemid 28082428)
61. Wickramasinghe SR, Alvania RS, Ramanan N, Wood JN, Mandai K, Ginty DD (2008) Serum response factor mediates NGF-dependent target innervation by embryonic DRG sensory neurons. Neuron 58: 532-545 (Pubitemid 351672349)