Change in the balance of excitatory and inhibitory midline fiber crossing as an explanation for the hopping phenotype in EphA4 knockout mice

European Journal of Neuroscience

Volumn 34, Issue 7, 2011, Pages 1102-1112

  Restrepo, Carlos E ^a,b   Margaryan, Gayane ^a   Borgius, Lotta ^a   Lundfald, Line ^a   Sargsyan, Davit ^a   Kiehn, Ole ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b INSTITUT CURIE   (France)

Author keywords

Central pattern generator; Locomotion; Motor neurons; Spinal cord

Indexed keywords

ACTION POTENTIAL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; BRAIN COMMISSURE; CELL FUNCTION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EPHA4 GENE; GENE; GENE FREQUENCY; HETEROZYGOSITY; HOMOZYGOSITY; LOCOMOTION; MOUSE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; SPINAL CORD; TRANSGENE;

ANIMALS; AXONS; CELL COUNT; ELECTROPHYSIOLOGY; GAIT; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GLYCINE; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; NEURONS; PHENOTYPE; RECEPTOR, EPHA4; SPINAL CORD;

EID: 80053576960     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07838.x     Document Type: Article

References (42)

1. Bannatyne, B.A., Edgley, S.A., Hammar, I., Jankowska, E. & Maxwell, D.J. (2003) Networks of inhibitory and excitatory commissural interneurons mediating crossed reticulospinal actions. Eur. J. Neurosci., 18, 2273-2284.
2. Batschelet, E. (1981) Circular Statistics in Biology. In Sibson, R. & Cohen, J.E. (Eds), Mathematics in Biology. Academic, New York, NY, pp. 31-54.
3. Beg, A.A., Sommer, J.E., Martin, J.H. & Scheiffele, P. (2007) alpha2-Chimaerin is an essential EphA4 effector in the assembly of neuronal locomotor circuits. Neuron, 55, 768-778.
4. Borgius, L., Restrepo, C.E., Leao, R.N., Saleh, N. & Kiehn, O. (2010) A transgenic mouse line for molecular genetic analysis of excitatory glutamatergic neurons. Mol. Cell. Neurosci., 45, 245-257.
5. Butt, S.J. & Kiehn, O. (2003) Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals. Neuron, 38, 953-963.
6. Butt, S.J., Lundfald, L. & Kiehn, O. (2005) EphA4 defines a class of excitatory locomotor-related interneurons. Proc. Natl. Acad. Sci. USA, 102, 14098-14103.
7. Chang, C., Yu, T.W., Bargmann, C.I. & Tessier-Lavigne, M. (2004) Inhibition of netrin-mediated axon attraction by a receptor protein tyrosine phosphatase. Science, 305, 103-106.
8. Coonan, J.R., Greferath, U., Messenger, J., Hartley, L., Murphy, M., Boyd, A.W., Dottori, M., Galea, M.P. & Bartlett, P.F. (2001) Development and reorganization of corticospinal projections in EphA4 deficient mice. J. Comp. Neurol., 436, 248-262.
9. Crone, S.A., Quinlan, K.A., Zagoraiou, L., Droho, S., Restrepo, C.E., Lundfald, L., Endo, T., Setlak, J., Jessell, T.M., Kiehn, O. & Sharma, K. (2008) Genetic ablation of V2a ipsilateral interneurons disrupts left-right locomotor coordination in mammalian spinal cord. Neuron, 60, 70-83.
10. Crone, S.A., Zhong, G., Harris-Warrick, R. & Sharma, K. (2009) In mice lacking V2a interneurons, gait depends on speed of locomotion. J. Neurosci., 29, 7098-7109.
11. Demarque, M. & Spitzer, N.C. (2010) Activity-dependent expression of Lmx1b regulates specification of serotonergic neurons modulating swimming behavior. Neuron, 67, 321-334.
12. Dottori, M., Hartley, L., Galea, M., Paxinos, G., Polizzotto, M., Kilpatrick, T., Bartlett, P.F., Murphy, M., Kontgen, F. & Boyd, A.W. (1998) EphA4 (Sek1) receptor tyrosine kinase is required for the development of the corticospinal tract. Proc. Natl. Acad. Sci. USA, 95, 13248-13253.
13. Eide, A.L., Glover, J., Kjaerulff, O. & Kiehn, O. (1999) Characterization of commissural interneurons in the lumbar region of the neonatal rat spinal cord. J. Comp. Neurol., 403, 332-345.
14. Fawcett, J.P., Georgiou, J., Ruston, J., Bladt, F., Sherman, A., Warner, N., Saab, B.J., Scott, R., Roder, J.C. & Pawson, T. (2007) Nck adaptor proteins control the organization of neuronal circuits important for walking. Proc. Natl. Acad. Sci. USA, 104, 20973-20978.
15. Filosa, A., Paixao, S., Honsek, S.D., Carmona, M.A., Becker, L., Feddersen, B., Gaitanos, L., Rudhard, Y., Schoepfer, R., Klopstock, T., Kullander, K., Rose, C.R., Pasquale, E.B. & Klein, R. (2009) Neuron-glia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport. Nat. Neurosci., 12, 1285-1292.
16. Hinckley, C., Seebach, B. & Ziskind-Conhaim, L. (2005) Distinct roles of glycinergic and GABAergic inhibition in coordinating locomotor-like rhythms in the neonatal mouse spinal cord. Neuroscience, 131, 745-758.
17. Iwasato, T., Katoh, H., Nishimaru, H., Ishikawa, Y., Inoue, H., Saito, Y.M., Ando, R., Iwama, M., Takahashi, R., Negishi, M. & Itohara, S. (2007) Rac-GAP alpha-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell, 130, 742-753.
18. Jankowska, E., Bannatyne, B.A., Stecina, K., Hammar, I., Cabaj, A. & Maxwell, D.J. (2009) Commissural interneurons with input from group I and II muscle afferents in feline lumbar segments: neurotransmitters, projections and target cells. J. Physiol., 587, 401-418.
19. Kiehn, O. (2006) Locomotor circuits in the mammalian spinal cord. Annu. Rev. Neurosci., 29, 279-306.
20. Kiehn, O. & Kjaerulff, O. (1996) Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. J. Neurophysiol., 75, 1472-1482.
21. Kjaerulff, O. & Kiehn, O. (1996) Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J. Neurosci., 16, 5777-5794.
22. Kullander, K., Croll, S.D., Zimmer, M., Pan, L., McClain, J., Hughes, V., Zabski, S., DeChiara, T.M., Klein, R., Yancopoulos, G.D. & Gale, N.W. (2001a) Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control. Genes Dev., 15, 877-888.
23. Kullander, K., Mather, N.K., Diella, F., Dottori, M., Boyd, A.W. & Klein, R. (2001b) Kinase-dependent and kinase-independent functions of EphA4 receptors in major axon tract formation in vivo. Neuron, 29, 73-84.
24. Kullander, K., Butt, S.J., Lebret, J.M., Lundfald, L., Restrepo, C.E., Rydstrom, A., Klein, R. & Kiehn, O. (2003) Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science, 299, 1889-1892.
25. Lanuza, G.M., Gosgnach, S., Pierani, A., Jessell, T.M. & Goulding, M. (2004) Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron, 42, 375-386.
26. Leighton, P.A., Mitchell, K.J., Goodrich, L.V., Lu, X., Pinson, K., Scherz, P., Skarnes, W.C. & Tessier-Lavigne, M. (2001) Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature, 410, 174-179.
27. Lundfald, L., Restrepo, C.E., Butt, S.J., Peng, C.Y., Droho, S., Endo, T., Zeilhofer, H.U., Sharma, K. & Kiehn, O. (2007) Phenotype of V2-derived interneurons and their relationship to the axon guidance molecule EphA4 in the developing mouse spinal cord. Eur. J. Neurosci., 26, 2989-3002.
28. Mellitzer, G., Xu, Q. & Wilkinson, D.G. (1999) Eph receptors and ephrins restrict cell intermingling and communication. Nature, 400, 77-81.
29. Nishimaru, H., Restrepo, C.E., Ryge, J., Yanagawa, Y. & Kiehn, O. (2005) Mammalian motor neurons corelease glutamate and acetylcholine at central synapses. Proc. Natl. Acad. Sci. USA, 102, 5245-5249.
30. Nissen, U.V., Mochida, H. & Glover, J.C. (2005) Development of projection-specific interneurons and projection neurons in the embryonic mouse and rat spinal cord. J. Comp. Neurol., 483, 30-47.
31. Quinlan, K.A. & Kiehn, O. (2007) Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. J. Neurosci., 27, 6521-6530.
32. Restrepo, C.E., Lundfald, L., Szabo, G., Erdelyi, F., Zeilhofer, H.U., Glover, J.C. & Kiehn, O. (2009) Transmitter-phenotypes of commissural interneurons in the lumbar spinal cord of newborn mice. J. Comp. Neurol., 517, 177-192.
33. Sabatier, C., Plump, A.S., Le, M., Brose, K., Tamada, A., Murakami, F., Lee, E.Y. & Tessier-Lavigne, M. (2004) The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell, 117, 157-169.
34. Stepien, A.E., Tripodi, M. & Arber, S. (2010) Monosynaptic rabies virus reveals premotor network organization and synaptic specificity of cholinergic partition cells. Neuron, 68, 456-472.
35. Stokke, M.F., Nissen, U.V., Glover, J.C. & Kiehn, O. (2002) Projection patterns of commissural interneurons in the lumbar spinal cord of the neonatal rat. J. Comp. Neurol., 446, 349-359.
36. Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J., Obata, K. & Kaneko, T. (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.
37. Weber, I., Veress, G., Szucs, P., Antal, M. & Birinyi, A. (2007) Neurotransmitter systems of commissural interneurons in the lumbar spinal cord of neonatal rats. Brain Res., 1178, 65-72.
38. Wegmeyer, H., Egea, J., Rabe, N., Gezelius, H., Filosa, A., Enjin, A., Varoqueaux, F., Deininger, K., Schnutgen, F., Brose, N., Klein, R., Kullander, K. & Betz, A. (2007) EphA4-dependent axon guidance is mediated by the RacGAP alpha2-chimaerin. Neuron, 55, 756-767.
39. Wilson, J.M., Hartley, R., Maxwell, D.J., Todd, A.J., Lieberam, I., Kaltschmidt, J.A., Yoshida, Y., Jessell, T.M. & Brownstone, R.M. (2005) Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. J. Neurosci., 25, 5710-5719.
40. Zar, J.H. (1974). Circular distribution. In McElroy, W.D. & Swanson, C.P. (Eds), Biostatistical Analysis. Prentice-Hall, Englewood Cliffs, NJ, pp. 310-327.
41. Zeilhofer, H.U., Studler, B., Arabadzisz, D., Schweizer, C., Ahmadi, S., Layh, B., Bosl, M.R. & Fritschy, J.M. (2005) Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. J. Comp. Neurol., 482, 123-141.
42. Zhang, Y., Narayan, S., Geiman, E., Lanuza, G.M., Velasquez, T., Shanks, B., Akay, T., Dyck, J., Pearson, K., Gosgnach, S., Fan, C.M. & Goulding, M. (2008) V3 spinal neurons establish a robust and balanced locomotor rhythm during walking. Neuron, 60, 84-96.