Lrig2 Negatively Regulates Ectodomain Shedding of Axon Guidance Receptors by ADAM Proteases

Developmental Cell

Volumn 35, Issue 5, 2015, Pages 537-552

  Van Erp, Susan ^a   Van den Heuvel, Dianne M A ^a   Fujita, Yuki ^b   Robinson, Ross A ^c   Hellemons, Anita J C G M ^a   Adolfs, Youri ^a   Van Battum, Eljo Y ^a   Blokhuis, Anna M ^a   Kuijpers, Marijn ^d   Demmers, Jeroen A A ^e   Hedman, Håkan ^f   Hoogenraad, Casper C ^d   Siebold, Christian ^c   Yamashita, Toshihide ^b   Pasterkamp, R Jeroen ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UTRECHT UNIVERSITY   (Netherlands)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; MEMBRANE PROTEIN; METALLOPROTEINASE; NEOGENIN; PROTEINASE; TRANSMEMBRANE PROTEIN LRIG2; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNCLASSIFIED DRUG; ADAM PROTEIN; LIGAND; LRIG2 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE;

ANIMAL CELL; ARTICLE; BRAIN CELL; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO DEVELOPMENT; IMMUNOCYTOCHEMISTRY; MOUSE; NERVE CELL; NERVE FIBER; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; ANIMAL; AXON; CELL MEMBRANE; CELL MOTION; CHO CELL LINE; CRICETULUS; EMBRYOLOGY; GENE EXPRESSION REGULATION; HEK293 CELL LINE; HUMAN; METABOLISM; NERVOUS SYSTEM; PHENOTYPE; PROTEIN TERTIARY STRUCTURE; RETINA; SIGNAL TRANSDUCTION;

ADAM PROTEINS; ANIMALS; AXONS; CELL MEMBRANE; CELL MOVEMENT; CHO CELLS; CRICETULUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; LIGANDS; MEMBRANE PROTEINS; MICE; NERVOUS SYSTEM; NEURONS; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; RETINA; SIGNAL TRANSDUCTION;

EID: 84961639766     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.11.008     Document Type: Article

References (43)

1. Bai G., Pfaff S.L. Protease regulation: the Yin and Yang of neural development and disease. Neuron 2011, 72:9-21.
2. Bell C.H., Healey E., van Erp S., Bishop B., Tang C., Gilbert R.J.C., Aricescu A.R., Pasterkamp R.J., Siebold C. Structure of the repulsive guidance molecule (RGM)-neogenin signaling hub. Science 2013, 341:77-80.
3. Blobel C.P. ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol. 2005, 6:32-43.
4. Conrad S., Genth H., Hofmann F., Just I., Skutella T. Neogenin-RGMa signaling at the growth cone is bone morphogenetic protein-independent and involves RhoA, ROCK, and PKC. J. Biol. Chem. 2007, 282:16423-16433.
5. Del Rio T., Nishitani A.M., Yu W.-M., Goodrich L.V. In vivo analysis of Lrig genes reveals redundant and independent functions in the inner ear. PLoS Genet. 2013, 9:e1003824.
6. Demicheva E., Cui Y.-F., Bardwell P., Barghorn S., Kron M., Meyer A.H., Schmidt M., Gerlach B., Leddy M., Barlow E., et al. Targeting repulsive guidance molecule A to promote regeneration and neuroprotection in multiple sclerosis. Cell Rep. 2015, 10:1887-1898.
7. Goldschneider D., Rama N., Guix C., Mehlen P. The neogenin intracellular domain regulates gene transcription via nuclear translocation. Mol. Cell. Biol. 2008, 28:4068-4079.
8. Groen E.J.N., Fumoto K., Blokhuis A.M., Engelen-Lee J., Zhou Y., van den Heuvel D.M.A., Koppers M., van Diggelen F., van Heest J., Demmers J.A.A., et al. ALS-associated mutations in FUS disrupt the axonal distribution and function of SMN. Hum. Mol. Genet. 2013, 22:3690-3704.
9. Gumienny T.L., Macneil L., Zimmerman C.M., Wang H., Chin L., Wrana J.L., Padgett R.W. Caenorhabditis elegans SMA-10/LRIG is a conserved transmembrane protein that enhances bone morphogenetic protein signaling. PLoS Genet. 2010, 6:e1000963.
10. Guo D., Holmlund C., Henriksson R., Hedman H. The LRIG gene family has three vertebrate paralogs widely expressed in human and mouse tissues and a homolog in Ascidiacea. Genomics 2004, 84:157-165.
11. Gur G., Rubin C., Katz M., Amit I., Citri A., Nilsson J., Amariglio N., Henriksson R., Rechavi G., Hedman H., et al. LRIG1 restricts growth factor signaling by enhancing receptor ubiquitylation and degradation. EMBO J. 2004, 23:3270-3281.
12. Hata K., Fujitani M., Yasuda Y., Doya H., Saito T., Yamagishi S., Mueller B.K., Yamashita T. RGMa inhibition promotes axonal growth and recovery after spinal cord injury. J. Cell Biol. 2006, 173:47-58.
13. Hata K., Kaibuchi K., Inagaki S., Yamashita T. Unc5B associates with LARG to mediate the action of repulsive guidance molecule. J. Cell Biol. 2009, 184:737-750.
14. Hattori M., Osterfield M., Flanagan J.G. Regulated cleavage of a contact-mediated axon repellent. Science 2000, 289:1360-1365.
15. Janes P.W., Saha N., Barton W.A., Kolev M.V., Wimmer-Kleikamp S.H., Nievergall E., Blobel C.P., Himanen J.-P., Lackmann M., Nikolov D.B. Adam meets Eph: an ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans. Cell 2005, 123:291-304.
16. Kang J.-S., Yi M.-J., Zhang W., Feinleib J.L., Cole F., Krauss R.S. Netrins and neogenin promote myotube formation. J. Cell Biol. 2004, 167:493-504.
17. Kolodkin A.L., Pasterkamp R.J. SnapShot: Axon guidance II. Cell 2013, 153:722.e1.
18. Laederich M.B., Funes-Duran M., Yen L., Ingalla E., Wu X., Carraway K.L., Sweeney C. The leucine-rich repeat protein LRIG1 is a negative regulator of ErbB family receptor tyrosine kinases. J. Biol. Chem. 2004, 279:47050-47056.
19. Ledda F., Bieraugel O., Fard S.S., Vilar M., Paratcha G. Lrig1 is an endogenous inhibitor of Ret receptor tyrosine kinase activation, downstream signaling, and biological responses to GDNF. J. Neurosci. 2008, 28:39-49.
20. Lindquist D., Kvarnbrink S., Henriksson R., Hedman H. LRIG and cancer prognosis. Acta Oncol. 2014, 53:1135-1142.
21. Maness P.F., Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 2007, 10:19-26.
22. Matsunaga E., Tauszig-Delamasure S., Monnier P.P., Mueller B.K., Strittmatter S.M., Mehlen P., Chédotal A. RGM and its receptor neogenin regulate neuronal survival. Nat. Cell Biol. 2004, 6:749-755.
23. Metzger M., Conrad S., Skutella T., Just L. RGMa inhibits neurite outgrowth of neuronal progenitors from murine enteric nervous system via the neogenin receptor in vitro. J. Neurochem. 2007, 103:2665-2678.
24. Monnier P.P., Sierra A., Macchi P., Deitinghoff L., Andersen J.S., Mann M., Flad M., Hornberger M.R., Stahl B., Bonhoeffer F., Mueller B.K. RGM is a repulsive guidance molecule for retinal axons. Nature 2002, 419:392-395.
25. Moreau-Fauvarque C., Kumanogoh A., Camand E., Jaillard C., Barbin G., Boquet I., Love C., Jones E.Y., Kikutani H., Lubetzki C., et al. The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendrocytes and upregulated after CNS lesion. J. Neurosci. 2003, 23:9229-9239.
26. O'Leary C., Cole S.J., Langford M., Hewage J., White A., Cooper H.M. RGMa regulates cortical interneuron migration and differentiation. PLoS ONE 2013, 8:e81711.
27. Okamura Y., Kohmura E., Yamashita T. TACE cleaves neogenin to desensitize cortical neurons to the repulsive guidance molecule. Neurosci. Res. 2011, 71:63-70.
28. Page M.E., Lombard P., Ng F., Göttgens B., Jensen K.B. The epidermis comprises autonomous compartments maintained by distinct stem cell populations. Cell Stem Cell 2013, 13:471-482.
29. Powell A.E., Wang Y., Li Y., Poulin E.J., Means A.L., Washington M.K., Higginbotham J.N., Juchheim A., Prasad N., Levy S.E., et al. The pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor. Cell 2012, 149:146-158.
30. Rajagopalan S., Deitinghoff L., Davis D., Conrad S., Skutella T., Chedotal A., Mueller B.K., Strittmatter S.M. Neogenin mediates the action of repulsive guidance molecule. Nat. Cell Biol. 2004, 6:756-762.
31. Scheller J., Chalaris A., Garbers C., Rose-John S. ADAM17: a molecular switch to control inflammation and tissue regeneration. Trends Immunol. 2011, 32:380-387.
32. Schmidt E.R.E., Brignani S., Adolfs Y., Lemstra S., Demmers J., Vidaki M., Donahoo A.-L.S., Lilleväli K., Vasar E., Richards L.J., et al. Subdomain-mediated axon-axon signaling and chemoattraction cooperate to regulate afferent innervation of the lateral habenula. Neuron 2014, 83:372-387.
33. Severyn C.J., Shinde U., Rotwein P. Molecular biology, genetics and biochemistry of the repulsive guidance molecule family. Biochem. J. 2009, 422:393-403.
34. Stuart H.M., Roberts N.A., Burgu B., Daly S.B., Urquhart J.E., Bhaskar S., Dickerson J.E., Mermerkaya M., Silay M.S., Lewis M.A., et al. LRIG2 mutations cause urofacial syndrome. Am. J. Hum. Genet. 2013, 92:259-264.
35. Suzuki Y., Miura H., Tanemura A., Kobayashi K., Kondoh G., Sano S., Ozawa K., Inui S., Nakata A., Takagi T., et al. Targeted disruption of LIG-1 gene results in psoriasiform epidermal hyperplasia. FEBS Lett. 2002, 521:67-71.
36. Suzuki K., Kumanogoh A., Kikutani H. Semaphorins and their receptors in immune cell interactions. Nat. Immunol. 2008, 9:17-23.
37. Tassew N.G., Mothe A.J., Shabanzadeh A.P., Banerjee P., Koeberle P.D., Bremner R., Tator C.H., Monnier P.P. Modifying lipid rafts promotes regeneration and functional recovery. Cell Rep. 2014, 8:1146-1159.
38. Van Battum E.Y., Gunput R.-A.F., Lemstra S., Groen E.J.N., Yu K.L., Adolfs Y., Zhou Y., Hoogenraad C.C., Yoshida Y., Schachner M., et al. The intracellular redox protein MICAL-1 regulates the development of hippocampal mossy fibre connections. Nat. Commun. 2014, 5:4317.
39. Weber S., Saftig P. Ectodomain shedding and ADAMs in development. Development 2012, 139:3693-3709.
40. Wong V.W.Y., Stange D.E., Page M.E., Buczacki S., Wabik A., Itami S., van de Wetering M., Poulsom R., Wright N.A., Trotter M.W.B., et al. Lrig1 controls intestinal stem-cell homeostasis by negative regulation of ErbB signalling. Nat. Cell Biol. 2012, 14:401-408.
41. Zhao H., Tanegashima K., Ro H., Dawid I.B. Lrig3 regulates neural crest formation in Xenopus by modulating Fgf and Wnt signaling pathways. Development 2008, 135:1283-1293.
42. Zhou Z., Xie J., Lee D., Liu Y., Jung J., Zhou L., Xiong S., Mei L., Xiong W.-C. Neogenin regulation of BMP-induced canonical Smad signaling and endochondral bone formation. Dev. Cell 2010, 19:90-102.
43. Zhu X.-J., Wang C.-Z., Dai P.-G., Xie Y., Song N.-N., Liu Y., Du Q.-S., Mei L., Ding Y.-Q., Xiong W.-C. Myosin X regulates netrin receptors and functions in axonal path-finding. Nat. Cell Biol. 2007, 9:184-192.