Subdomain-mediated axon-axon signaling and chemoattraction cooperate to regulate afferent innervation of the lateral habenula

Neuron

Volumn 83, Issue 2, 2014, Pages 372-387

  Schmidt, Ewoud Roberto Eduard ^a,f   Brignani, Sara ^a   Adolfs, Youri ^a   Lemstra, Suzanne ^a   Demmers, Jeroen ^b   Vidaki, Marina ^c   Donahoo, Amber Lee Skye ^d   Lilleväli, Kersti ^e   Vasar, Eero ^e   Richards, Linda Jane ^d   Karagogeos, Domna ^c   Kolk, Sharon Margriet ^a,g   Pasterkamp, Ronald Jeroen ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF TARTU   (Estonia)

^f Department of Neuroscience College of Physicians and Surgeons Columbia University ^*  (United States)

^g RADBOUD UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; NETRIN 1;

AFFERENT INNERVATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AXON AXON SIGNALING; BRAIN NUCLEUS; CELL ADHESION; CHEMOATTRACTION; CHEMOTAXIS; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EFFERENT NERVE; EMBRYO; HABENULA; HABENULOINTERPEDUNCULAR TRACT; INNERVATION; MOLECULAR INTERACTION; MOUSE; NERVE PROJECTION; NERVE TRACT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; CHEMOTACTIC FACTORS; CHEMOTAXIS; DOPAMINERGIC NEURONS; HABENULA; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; NERVE GROWTH FACTORS; NEURAL PATHWAYS; NEURONS, AFFERENT; SYNAPSES; TUMOR SUPPRESSOR PROTEINS;

EID: 84904344844     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.05.036     Document Type: Article

References (68)

1. Aizawa H., Kobayashi M., Tanaka S., Fukai T., Okamoto H. Molecular characterization of the subnuclei in rat habenula. J.Comp. Neurol. 2012, 520:4051-4066.
2. Bagnard D., Lohrum M., Uziel D., Püschel A.W., Bolz J. Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. Development 1998, 125:5043-5053.
3. Baier H. Synaptic laminae in the visual system: molecular mechanisms forming layers of perception. Annu. Rev. Cell Dev. Biol. 2013, 29:385-416.
4. Bianco I.H., Wilson S.W. The habenular nuclei: a conserved asymmetric relay station in the vertebrate brain. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364:1005-1020.
5. Bielle F., Marcos-Mondéjar P., Leyva-Díaz E., Lokmane L., Mire E., Mailhes C., Keita M., García N., Tessier-Lavigne M., Garel S., López-Bendito G. Emergent growth cone responses to combinations of Slit1 and Netrin 1 in thalamocortical axon topography. Curr. Biol. 2011, 21:1748-1755.
6. Chen H., Bagri A., Zupicich J.A., Zou Y., Stoeckli E., Pleasure S.J., Lowenstein D.H., Skarnes W.C., Chédotal A., Tessier-Lavigne M. Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 2000, 25:43-56.
7. Cord B.J., Li J., Works M., McConnell S.K., Palmer T., Hynes M.A. Characterization of axon guidance cue sensitivity of human embryonic stem cell-derived dopaminergic neurons. Mol. Cell. Neurosci. 2010, 45:324-334.
8. Deck M., Lokmane L., Chauvet S., Mailhes C., Keita M., Niquille M., Yoshida M., Yoshida Y., Lebrand C., Mann F., et al. Pathfinding of corticothalamic axons relies on a rendezvous with thalamic projections. Neuron 2013, 77:472-484.
9. Funato H., Saito-Nakazato Y., Takahashi H. Axonal growth from the habenular nucleus along the neuromere boundary region of the diencephalon is regulated by semaphorin 3F and netrin-1. Mol. Cell. Neurosci. 2000, 16:206-220.
10. Gallarda B.W., Bonanomi D., Müller D., Brown A., Alaynick W.A., Andrews S.E., Lemke G., Pfaff S.L., Marquardt T. Segregation of axial motor and sensory pathways via heterotypic trans-axonal signaling. Science 2008, 320:233-236.
11. Giger R.J., Cloutier J.F., Sahay A., Prinjha R.K., Levengood D.V., Moore S.E., Pickering S., Simmons D., Rastan S., Walsh F.S., et al. Neuropilin-2 is required invivo for selective axon guidance responses to secreted semaphorins. Neuron 2000, 25:29-41.
12. Gil O.D., Zhang L., Chen S., Ren Y.Q., Pimenta A., Zanazzi G., Hillman D., Levitt P., Salzer J.L. Complementary expression and heterophilic interactions between IgLON family members neurotrimin and LAMP. J.Neurobiol. 2002, 51:190-204.
13. Goldman J.S., Ashour M.A., Magdesian M.H., Tritsch N.X., Harris S.N., Christofi N., Chemali R., Stern Y.E., Thompson-Steckel G., Gris P., et al. Netrin-1 promotes excitatory synaptogenesis between cortical neurons by initiating synapse assembly. J.Neurosci. 2013, 33:17278-17289.
14. Gruber C., Kahl A., Lebenheim L., Kowski A., Dittgen A., Veh R.W. Dopaminergic projections from the VTA substantially contribute to the mesohabenular pathway in the rat. Neurosci. Lett. 2007, 427:165-170.
15. Grueber W., Sagasti A. Self-avoidance and tiling: mechanisms of dendrite and axon spacing. Cold Spring Harb. Perspect. Biol. 2010, 2:a001750.
16. Hikosaka O. The habenula: from stress evasion to value-based decision-making. Nat. Rev. Neurosci. 2010, 11:503-513.
17. Hikosaka O., Sesack S.R., Lecourtier L., Shepard P.D. Habenula: crossroad between the basal ganglia and the limbic system. J.Neurosci. 2008, 28:11825-11829.
18. Hillenbrand R., Molthagen M., Montag D., Schachner M. The close homologue of the neural adhesion molecule L1 (CHL1): patterns of expression and promotion of neurite outgrowth by heterophilic interactions. Eur. J. Neurosci. 1999, 11:813-826.
19. Huberman A.D., Clandinin T.R., Baier H. Molecular and cellular mechanisms of lamina-specific axon targeting. Cold Spring Harb. Perspect. Biol. 2010, 2:a001743.
20. Imai T., Sakano H. Axon-axon interactions in neuronal circuit assembly: lessons from olfactory map formation. Eur. J. Neurosci. 2011, 34:1647-1654.
21. Imai T., Yamazaki T., Kobayakawa R., Kobayakawa K., Abe T., Suzuki M., Sakano H. Pre-target axon sorting establishes the neural map topography. Science 2009, 325:585-590.
22. Innos J., Philips M.A., Leidmaa E., Heinla I., Raud S., Reemann P., Plaas M., Nurk K., Kurrikoff K., Matto V., et al. Lower anxiety and a decrease in agonistic behaviour in Lsamp-deficient mice. Behav. Brain Res. 2011, 217:21-31.
23. Joo W.J., Sweeney L.B., Liang L., Luo L. Linking cell fate, trajectory choice, and target selection: genetic analysis of Sema-2b in olfactory axon targeting. Neuron 2013, 78:673-686.
24. Kantor D.B., Chivatakarn O., Peer K.L., Oster S.F., Inatani M., Hansen M.J., Flanagan J.G., Yamaguchi Y., Sretavan D.W., Giger R.J., Kolodkin A.L. Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 2004, 44:961-975.
25. Keller F., Rimvall K., Barbe M.F., Levitt P. A membrane glycoprotein associated with the limbic system mediates the formation of the septo-hippocampal pathway invitro. Neuron 1989, 3:551-561.
26. Kimmel R.A., Turnbull D.H., Blanquet V., Wurst W., Loomis C.A., Joyner A.L. Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev. 2000, 14:1377-1389.
27. Kolk S.M., Gunput R.A., Tran T.S., van den Heuvel D.M.A., Prasad A.A., Hellemons A.J., Adolfs Y., Ginty D.D., Kolodkin A.L., Burbach J.P.H., et al. Semaphorin 3F is a bifunctional guidance cue for dopaminergic axons and controls their fasciculation, channeling, rostral growth, and intracortical targeting. J.Neurosci. 2009, 29:12542-12557.
28. Kowski A.B., Veh R.W., Weiss T. Dopaminergic activation excites rat lateral habenular neurons invivo. Neuroscience 2009, 161:1154-1165.
29. Krimpenfort P., Song J.-Y., Proost N., Zevenhoven J., Jonkers J., Berns A. Deleted in colorectal carcinoma suppresses metastasis in p53-deficient mammary tumours. Nature 2012, 482:538-541.
30. Lai Wing Sun K., Correia J.P., Kennedy T.E. Netrins: versatile extracellular cues with diverse functions. Development 2011, 138:2153-2169.
31. Lattemann M., Zierau A., Schulte C., Seidl S., Kuhlmann B., Hummel T. Semaphorin-1a controls receptor neuron-specific axonal convergence in the primary olfactory center of Drosophila. Neuron 2007, 53:169-184.
32. Li B., Piriz J., Mirrione M., Chung C., Proulx C.D., Schulz D., Henn F., Malinow R. Synaptic potentiation onto habenula neurons in the learned helplessness model of depression. Nature 2011, 470:535-539.
33. Li K., Zhou T., Liao L., Yang Z., Wong C., Henn F., Malinow R., Yates J.R., Hu H. βCaMKII in lateral habenula mediates core symptoms of depression. Science 2013, 341:1016-1020.
34. Lin L., Rao Y., Isacson O. Netrin-1 and slit-2 regulate and direct neurite growth of ventral midbrain dopaminergic neurons. Mol. Cell. Neurosci. 2005, 28:547-555.
35. López-Bendito G., Cautinat A., Sánchez J.A., Bielle F., Flames N., Garratt A.N., Talmage D.A., Role L.W., Charnay P., Marín O., Garel S. Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 2006, 125:127-142.
36. Luo L., Flanagan J.G. Development of continuous and discrete neural maps. Neuron 2007, 56:284-300.
37. Manitt C., Mimee A., Eng C., Pokinko M., Stroh T., Cooper H.M., Kolb B., Flores C. The netrin receptor DCC is required in the pubertal organization of mesocortical dopamine circuitry. J.Neurosci. 2011, 31:8381-8394.
38. Manitt C., Eng C., Pokinko M., Ryan R.T., Torres-Berrío A., Lopez J.P., Yogendran S.V., Daubaras M.J., Grant A., Schmidt E.R., et al. dcc orchestrates the development of the prefrontal cortex during adolescence and is altered in psychiatric patients. Transcult. Psychiatry 2013, 3:e338.
39. Mann F., Zhukareva V., Pimenta A., Levitt P., Bolz J. Membrane-associated molecules guide limbic and nonlimbic thalamocortical projections. J.Neurosci. 1998, 18:9409-9419.
40. Matsumoto M., Hikosaka O. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 2007, 447:1111-1115.
41. Matsumoto M., Hikosaka O. Representation of negative motivational value in the primate lateral habenula. Nat. Neurosci. 2009, 12:77-84.
42. Mizumoto K., Shen K. Interaxonal interaction defines tiled presynaptic innervation in C. elegans. Neuron 2013, 77:655-666.
43. Molnár Z., Garel S., López-Bendito G., Maness P., Price D.J. Mechanisms controlling the guidance of thalamocortical axons through the embryonic forebrain. Eur. J. Neurosci. 2012, 35:1573-1585.
44. Osborne P.B., Halliday G.M., Cooper H.M., Keast J.R. Localization of immunoreactivity for deleted in colorectal cancer (DCC), the receptor for the guidance factor netrin-1, in ventral tier dopamine projection pathways in adult rodents. Neuroscience 2005, 131:671-681.
45. Pasterkamp R.J., Kolodkin A.L. SnapShot: axon guidance. Cell 2013, 153:494.
46. Pasterkamp R.J., Peschon J.J., Spriggs M.K., Kolodkin A.L. Semaphorin 7A promotes axon outgrowth through integrins and MAPKs. Nature 2003, 424:398-405.
47. Pasterkamp R.J., Kolk S.M., Hellemons A.J.C.G.M., Kolodkin A.L. Expression patterns of semaphorin7A and plexinC1 during rat neural development suggest roles in axon guidance and neuronal migration. BMC Dev. Biol. 2007, 7:98.
48. Phillipson O.T., Griffith A.C. The neurones of origin for the mesohabenular dopamine pathway. Brain Res. 1980, 197:213-218.
49. Poon V.Y., Klassen M.P., Shen K. UNC-6/netrin and its receptor UNC-5 locally exclude presynaptic components from dendrites. Nature 2008, 455:669-673.
50. Powell A.W., Sassa T., Wu Y., Tessier-Lavigne M., Polleux F. Topography of thalamic projections requires attractive and repulsive functions of Netrin-1 in the ventral telencephalon. PLoS Biol. 2008, 6:e116.
51. Quina L.A., Wang S., Ng L., Turner E.E. Brn3a and Nurr1 mediate a gene regulatory pathway for habenula development. J.Neurosci. 2009, 29:14309-14322.
52. Robles E., Baier H. Assembly of synaptic laminae by axon guidance molecules. Curr. Opin. Neurobiol. 2012, 22:799-804.
53. Sanes J.R., Yamagata M. Many paths to synaptic specificity. Annu. Rev. Cell Dev. Biol. 2009, 25:161-195.
54. Schmidt E.R.E., Morello F., Pasterkamp R.J. Dissection and culture of mouse dopaminergic and striatal explants in three-dimensional collagen matrix assays. J.Vis. Exp. 2012, 10.3791/3691.
55. Schwabe T., Neuert H., Clandinin T.R. A network of cadherin-mediated interactions polarizes growth cones to determine targeting specificity. Cell 2013, 154:351-364.
56. Serafini T., Colamarino S.A., Leonardo E.D., Wang H., Beddington R., Skarnes W.C., Tessier-Lavigne M. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 1996, 87:1001-1014.
57. Shen X., Ruan X., Zhao H. Stimulation of midbrain dopaminergic structures modifies firing rates of rat lateral habenula neurons. PLoS ONE 2012, 7:e34323.
58. Stamatakis A.M., Jennings J.H., Ung R.L., Blair G.A., Weinberg R.J., Neve R.L., Boyce F., Mattis J., Ramakrishnan C., Deisseroth K., Stuber G.D. A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron 2013, 80:1039-1053.
59. Sweeney L.B., Couto A., Chou Y.-H., Berdnik D., Dickson B.J., Luo L., Komiyama T. Temporal target restriction of olfactory receptor neurons by Semaphorin-1a/PlexinA-mediated axon-axon interactions. Neuron 2007, 53:185-200.
60. Takeuchi H., Inokuchi K., Aoki M., Suto F., Tsuboi A., Matsuda I., Suzuki M., Aiba A., Serizawa S., Yoshihara Y., et al. Sequential arrival and graded secretion of Sema3F by olfactory neuron axons specify map topography at the bulb. Cell 2010, 141:1056-1067.
61. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science 1996, 274:1123-1133.
62. Timofeev K., Joly W., Hadjieconomou D., Salecker I. Localized netrins act as positional cues to control layer-specific targeting of photoreceptor axons in Drosophila. Neuron 2012, 75:80-93.
63. Veenvliet J.V., Dos Santos M.T., Kouwenhoven W.M., von Oerthel L., Lim J.L., van der Linden A.J.A., Koerkamp M.J.G., Holstege F.C.P., Smidt M.P. Specification of dopaminergic subsets involves interplay of En1 and Pitx3. Development 2013, 140:3373-3384.
64. Wang L., Marquardt T. What axons tell each other: axon-axon signaling in nerve and circuit assembly. Curr. Opin. Neurobiol. 2013, 23:974-982.
65. Wang L., Klein R., Zheng B., Marquardt T. Anatomical coupling of sensory and motor nerve trajectory via axon tracking. Neuron 2011, 71:263-277.
66. Williams M.E., de Wit J., Ghosh A. Molecular mechanisms of synaptic specificity in developing neural circuits. Neuron 2010, 68:9-18.
67. Xu B., Goldman J.S., Rymar V.V., Forget C., Lo P.S., Bull S.J., Vereker E., Barker P.A., Trudeau L.E., Sadikot A.F., Kennedy T.E. Critical roles for the netrin receptor deleted in colorectal cancer in dopaminergic neuronal precursor migration, axon guidance, and axon arborization. Neuroscience 2010, 169:932-949.
68. Zhukareva V., Levitt P. The limbic system-associated membrane protein (LAMP) selectively mediates interactions with specific central neuron populations. Development 1995, 121:1161-1172.