Lrig1 is a cell-intrinsic modulator of hippocampal dendrite complexity and BDNF signaling

EMBO Reports

Volumn 17, Issue 4, 2016, Pages 601-616

  Alsina, Fernando Cruz ^a   Hita, Francisco Javier ^a   Fontanet, Paula Aldana ^a   Irala, Dolores ^a   Hedman, Häkan ^b   Ledda, Fernanda ^a   Paratcha, Gustavo ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

dendrite morphogenesis; hippocampal neurons; Lrig1; neurotrophins; TrkB

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; LEUCINE RICH REPEAT IMMUNOGLOBULIN LIKE DOMAIN 1; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; GLYCOPROTEIN; LRG1 PROTEIN, HUMAN; LRIG1 PROTEIN, MOUSE; NERVE PROTEIN; NEUROTROPIN; POLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; GENETIC TRANSFECTION; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VIVO STUDY; MORPHOGENESIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SOCIAL BEHAVIOR; SOCIAL INTERACTION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CHLOROCEBUS AETHIOPS; CV-1 CELL LINE; CYTOLOGY; DEFICIENCY; GENE INACTIVATION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; NERVE CELL; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; DENDRITES; GENE KNOCKOUT TECHNIQUES; GLYCOPROTEINS; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MORPHOGENESIS; NERVE TISSUE PROTEINS; NEURONS; POLYSACCHARIDES; SIGNAL TRANSDUCTION;

EID: 84959298789     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201541218     Document Type: Article

References (65)

1. Parrish JZ, Emoto K, Kim MD, Jan YN, (2007) Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu Rev Neurosci 30: 399-423
2. Wong RO, Ghosh A, (2002) Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 3: 803-812
3. Whitford KL, Dijkhuizen P, Polleux F, Ghosh A, (2002) Molecular control of cortical dendrite development. Annu Rev Neurosci 25: 127-149
4. Reichardt LF, (2006) Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 361: 1545-1564
5. Segal RA, Pomeroy SL, Stiles CD, (1995) Axonal growth and fasciculation linked to differential expression of BDNF and NT3 receptors in developing cerebellar granule cells. J Neurosci 15: 4970-4981
6. McAllister AK, Katz LC, Lo DC, (1996) Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17: 1057-1064
7. Horch HW, Kruttgen A, Portbury SD, Katz LC, (1999) Destabilization of cortical dendrites and spines by BDNF. Neuron 23: 353-364
8. Jin X, Hu H, Mathers PH, Agmon A, (2003) Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures. J Neurosci 23: 5662-5673
9. Ji Y, Lu Y, Yang F, Shen W, Tang TT, Feng L, Duan S, Lu B, (2010) Acute and gradual increases in BDNF concentration elicit distinct signaling and functions in neurons. Nat Neurosci 13: 302-309
10. Greenberg ME, Xu B, Lu B, Hempstead BL, (2009) New insights in the biology of BDNF synthesis and release: implications in CNS function. J Neurosci 29: 12764-12767
11. McAllister AK, Lo DC, Katz LC, (1995) Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15: 791-803
12. Cheung ZH, Chin WH, Chen Y, Ng YP, Ip NY, (2007) Cdk5 is involved in BDNF-stimulated dendritic growth in hippocampal neurons. PLoS Biol 5: e63
13. Kwon M, Fernandez JR, Zegarek GF, Lo SB, Firestein BL, (2011) BDNF-promoted increases in proximal dendrites occur via CREB-dependent transcriptional regulation of cypin. J Neurosci 31: 9735-9745
14. Lazo OM, Gonzalez A, Ascano M, Kuruvilla R, Couve A, Bronfman FC, (2013) BDNF regulates Rab11-mediated recycling endosome dynamics to induce dendritic branching. J Neurosci 33: 6112-6122
15. de Wit J, Hong W, Luo L, Ghosh A, (2011) Role of leucine-rich repeat proteins in the development and function of neural circuits. Annu Rev Cell Dev Biol 27: 697-729
16. Proenca CC, Gao KP, Shmelkov SV, Rafii S, Lee FS, (2011) Slitrks as emerging candidate genes involved in neuropsychiatric disorders. Trends Neurosci 34: 143-153
17. Chen Y, Hor HH, Tang BL, (2012) AMIGO is expressed in multiple brain cell types and may regulate dendritic growth and neuronal survival. J Cell Physiol 227: 2217-2229
18. de Wit J, Ghosh A, (2014) Control of neural circuit formation by leucine-rich repeat proteins. Trends Neurosci 37: 539-550
19. Suzuki Y, Miura H, Tanemura A, Kobayashi K, Kondoh G, Sano S, Ozawa K, Inui S, Nakata A, Takagi T, et al, (2002) Targeted disruption of LIG-1 gene results in psoriasiform epidermal hyperplasia. FEBS Lett 521: 67-71
20. Nilsson J, Vallbo C, Guo D, Golovleva I, Hallberg B, Henriksson R, Hedman H, (2001) Cloning, characterization, and expression of human LIG1. Biochem Biophys Res Commun 284: 1155-1161
21. Gur G, Rubin C, Katz M, Amit I, Citri A, Nilsson J, Amariglio N, Henriksson R, Rechavi G, Hedman H, et al, (2004) LRIG1 restricts growth factor signaling by enhancing receptor ubiquitylation and degradation. EMBO J 23: 3270-3281
22. Laederich MB, Funes-Duran M, Yen L, Ingalla E, Wu X, Carraway KL 3rd, Sweeney C, (2004) The leucine-rich repeat protein LRIG1 is a negative regulator of ErbB family receptor tyrosine kinases. J Biol Chem 279: 47050-47056
23. Shattuck DL, Miller JK, Laederich M, Funes M, Petersen H, Carraway KL 3rd, Sweeney C, (2007) LRIG1 is a novel negative regulator of the Met receptor and opposes Met and Her2 synergy. Mol Cell Biol 27: 1934-1946
24. 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
25. Alsina FC, Ledda F, Paratcha G, (2012) New insights into the control of neurotrophic growth factor receptor signaling: implications for nervous system development and repair. J Neurochem 123: 652-661
26. Kwon CH, Luikart BW, Powell CM, Zhou J, Matheny SA, Zhang W, Li Y, Baker SJ, Parada LF, (2006) Pten regulates neuronal arborization and social interaction in mice. Neuron 50: 377-388
27. Sholl A, Uttley AM, (1953) Pattern discrimination and the visual cortex. Nature 171: 387-388
28. Kaufmann WE, Moser HW, (2000) Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 10: 981-991
29. Penzes P, Woolfrey KM, Srivastava DP, (2011) Epac2-mediated dendritic spine remodeling: implications for disease. Mol Cell Neurosci 46: 368-380
30. Jan YN, Jan LY, (2010) Branching out: mechanisms of dendritic arborization. Nat Rev Neurosci 11: 316-328
31. Felix-Ortiz AC, Tye KM, (2014) Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior. J Neurosci 34: 586-595
32. Phelps SM, Campbell P, Zheng DJ, Ophir AG, (2010) Beating the boojum: comparative approaches to the neurobiology of social behavior. Neuropharmacology 58: 17-28
33. Nibuya M, Morinobu S, Duman RS, (1995) Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 15: 7539-7547
34. Tongiorgi E, Righi M, Cattaneo A, (1997) Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J Neurosci 17: 9492-9505
35. Drake CT, Milner TA, Patterson SL, (1999) Ultrastructural localization of full-length trkB immunoreactivity in rat hippocampus suggests multiple roles in modulating activity-dependent synaptic plasticity. J Neurosci 19: 8009-8026
36. Elmariah SB, Crumling MA, Parsons TD, Balice-Gordon RJ, (2004) Postsynaptic TrkB-mediated signaling modulates excitatory and inhibitory neurotransmitter receptor clustering at hippocampal synapses. J Neurosci 24: 2380-2393
37. Ledda F, Paratcha G, (2007) Negative regulation of receptor tyrosine kinase (RTK) signaling: a developing field. Biomarker Insights 2: 45-58
38. Dikic I, Giordano S, (2003) Negative receptor signalling. Curr Opin Cell Biol 15: 128-135
39. Puram SV, Bonni A, (2013) Cell-intrinsic drivers of dendrite morphogenesis. Development 140: 4657-4671
40. Del Rio T, Nishitani AM, Yu WM, Goodrich LV, (2013) In vivo analysis of Lrig genes reveals redundant and independent functions in the inner ear. PLoS Genet 9: e1003824
41. van Erp S, van den Heuvel DM, Fujita Y, Robinson RA, Hellemons AJ, Adolfs Y, Van Battum EY, Blokhuis AM, Kuijpers M, Demmers JA, et al, (2015) Lrig2 negatively regulates ectodomain shedding of axon guidance receptors by ADAM proteases. Dev Cell 35: 537-552
42. Mandai K, Guo T, St Hillaire C, Meabon JS, Kanning KC, Bothwell M, Ginty DD, (2009) LIG family receptor tyrosine kinase-associated proteins modulate growth factor signals during neural development. Neuron 63: 614-627
43. de Wit J, Sylwestrak E, O'Sullivan ML, Otto S, Tiglio K, Savas JN, Yates JR 3rd, Comoletti D, Taylor P, Ghosh A, (2009) LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron 64: 799-806
44. Takahashi H, Katayama K, Sohya K, Miyamoto H, Prasad T, Matsumoto Y, Ota M, Yasuda H, Tsumoto T, Aruga J, et al, (2012) Selective control of inhibitory synapse development by Slitrk3-PTPdelta trans-synaptic interaction. Nat Neurosci 15 (389-398): S381-S382
45. Linhoff MW, Lauren J, Cassidy RM, Dobie FA, Takahashi H, Nygaard HB, Airaksinen MS, Strittmatter SM, Craig AM, (2009) An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron 61: 734-749
46. Nam J, Mah W, Kim E, (2011) The SALM/Lrfn family of leucine-rich repeat-containing cell adhesion molecules. Semin Cell Dev Biol 22: 492-498
47. Takahashi H, Arstikaitis P, Prasad T, Bartlett TE, Wang YT, Murphy TH, Craig AM, (2011) Postsynaptic TrkC and presynaptic PTPsigma function as a bidirectional excitatory synaptic organizing complex. Neuron 69: 287-303
48. McIlroy G, Foldi I, Aurikko J, Wentzell JS, Lim MA, Fenton JC, Gay NJ, Hidalgo A, (2013) Toll-6 and Toll-7 function as neurotrophin receptors in the Drosophila melanogaster CNS. Nat Neurosci 16: 1248-1256
49. Song M, Giza J, Proenca CC, Jing D, Elliott M, Dincheva I, Shmelkov SV, Kim J, Schreiner R, Huang SH, et al, (2015) Slitrk5 mediates BDNF-dependent TrkB receptor trafficking and signaling. Dev Cell 33: 690-702
50. Kulkarni VA, Firestein BL, (2012) The dendritic tree and brain disorders. Mol Cell Neurosci 50: 10-20
51. Cohen S, Greenberg ME, (2008) Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu Rev Cell Dev Biol 24: 183-209
52. Yang J, Harte-Hargrove LC, Siao CJ, Marinic T, Clarke R, Ma Q, Jing D, Lafrancois JJ, Bath KG, Mark W, et al, (2014) proBDNF negatively regulates neuronal remodeling, synaptic transmission, and synaptic plasticity in hippocampus. Cell Rep 7: 796-806
53. Cosker KE, Segal RA, (2014) Neuronal signaling through endocytosis. Cold Spring Harb Perspect Biol 6: a020669
54. Ouyang Q, Lizarraga SB, Schmidt M, Yang U, Gong J, Ellisor D, Kauer JA, Morrow EM, (2013) Christianson syndrome protein NHE6 modulates TrkB endosomal signaling required for neuronal circuit development. Neuron 80: 97-112
55. Nilsson J, Starefeldt A, Henriksson R, Hedman H, (2003) LRIG1 protein in human cells and tissues. Cell Tissue Res 312: 65-71
56. Abraira VE, Satoh T, Fekete DM, Goodrich LV, (2010) Vertebrate Lrig3-ErbB interactions occur in vitro but are unlikely to play a role in Lrig3-dependent inner ear morphogenesis. PLoS ONE 5: e8981
57. Bibel M, Hoppe E, Barde YA, (1999) Biochemical and functional interactions between the neurotrophin receptors trk and p75NTR. EMBO J 18: 616-622
58. Rondahl V, Holmlund C, Karlsson T, Wang B, Faraz M, Henriksson R, Hedman H, (2013) Lrig2-deficient mice are protected against PDGFB-induced glioma. PLoS ONE 8: e73635
59. Jensen KB, Watt FM, (2006) Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence. Proc Natl Acad Sci USA 103: 11958-11963
60. Nakamura T, Hamuro J, Takaishi M, Simmons S, Maruyama K, Zaffalon A, Bentley AJ, Kawasaki S, Nagata-Takaoka M, Fullwood NJ, et al, (2014) LRIG1 inhibits STAT3-dependent inflammation to maintain corneal homeostasis. J Clin Invest 124: 385-397
61. Berghuis P, Dobszay MB, Wang X, Spano S, Ledda F, Sousa KM, Schulte G, Ernfors P, Mackie K, Paratcha G, et al, (2005) Endocannabinoids regulate interneuron migration and morphogenesis by transactivating the TrkB receptor. Proc Natl Acad Sci USA 102: 19115-19120
62. Paratcha G, Ledda F, Ibanez CF, (2003) The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113: 867-879
63. Otero MG, Alloatti M, Cromberg LE, Almenar-Queralt A, Encalada SE, Pozo Devoto VM, Bruno L, Goldstein LS, Falzone TL, (2014) Fast axonal transport of the proteasome complex depends on membrane interaction and molecular motor function. J Cell Sci 127: 1537-1549
64. Alfieri JA, Pino NS, Igaz LM, (2014) Reversible behavioral phenotypes in a conditional mouse model of TDP-43 proteinopathies. J Neurosci 34: 15244-15259
65. Nadler JJ, Moy SS, Dold G, Trang D, Simmons N, Perez A, Young NB, Barbaro RP, Piven J, Magnuson TR, et al, (2004) Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav 3: 303-314