Release of MICAL autoinhibition by semaphorin-plexin signaling promotes interaction with collapsin response mediator protein

Journal of Neuroscience

Volumn 28, Issue 9, 2008, Pages 2287-2297

  Schmidt, Eric F ^a   Shim, Sang Ohk ^a   Strittmatter, Stephen M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Axonal guidance; CRMP; Growth cone collapse; MICAL; Neuropilin; Plexin; Semaphorin

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN; NEUROPILIN; NEUROPILIN 1; PLEXIN; RECOMBINANT PROTEIN; SEMAPHORIN; VIRUS VECTOR;

ARTICLE; CELL STRAIN COS7; CONTROLLED STUDY; GENE; GROWTH CONE; HUMAN; HUMAN CELL; MICAL GENE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION;

ANIMALS; CELL ADHESION MOLECULES; CELL LINE, TRANSFORMED; CHICK EMBRYO; CYTOSKELETAL PROTEINS; FLAVIN-ADENINE DINUCLEOTIDE; GANGLIA, SPINAL; GENETIC VECTORS; HIV; HUMANS; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE GLYCOPROTEINS; MUTATION; NERVE TISSUE PROTEINS; NEURITES; NEURONS; PEPTIDE FRAGMENTS; PROTEIN BINDING; SEMAPHORIN-3A; SEMAPHORINS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 39849089206     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5646-07.2008     Document Type: Article

References (45)

1. Abe I, Kashiwagi K, Noguchi H (2000a) Antioxidative galloyl esters as enzyme inhibitors of p-hydroxybenzoate hydroxylase. FEBS Lett 483:131-134.
2. Abe I, Seki T, Umehara K, Miyase T, Noguchi H, Sakakibara J, Ono T (2000b) Green tea polyphenols: novel and potent inhibitors of squalene epoxidase. Biochem Biophys Res Commun 268:767-771.
3. Aizawa H, Wakatsuki S, Ishii A, Moriyama K, Sasaki Y, Ohashi K, Sekine-Aizawa Y, Sehara-Fujisawa A, Mizuno K, Goshima Y, Yahara I (2001) Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat Neurosci 4:367-373.
4. Castellani V, Falk J, Rougon G (2004) Semaphorin3A-induced receptor endocytosis during axon guidance responses is mediated by L1 CAM. Mol Cell Neurosci 26:89-100.
5. Deo RC, Schmidt EF, Elhabazi A, Togashi H, Burley SK, Strittmatter SM (2004) Structural bases for CRMP function in plexin-dependent semaphorin3A signaling. EMBO J 23:9-22.
6. Eickholt BJ, Walsh FS, Doherty P (2002) An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling. J Cell Biol 157:211-217.
7. Entsch B, van Berkel WJ (1995) Structure and mechanism of parahydroxybenzoate hydroxylase. FASEB J 9:476-483.
8. Finkel T (1998) Oxygen radicals and signaling. Curr Opin Cell Biol 10:248-253.
9. Fischer J, Weide T, Barnekow A (2005) The MICAL proteins and rab1: a possible link to the cytoskeleton? Biochem Biophys Res Commun 328:415-423.
10. Fournier AE, Nakamura F, Kawamoto S, Goshima Y, Kalb RG, Strittmatter SM (2000) Semaphorin3A enhances endocytosis at sites of receptor-F-actin colocalization during growth cone collapse. J Cell Biol 149:411-422.
11. Fraaije MW, Mattevi A (2000) Flavoenzymes: diverse catalysts with recurrent features. Trends Biochem Sci 25:126-132.
12. Gimona M, Djinovic-Carugo K, Kranewitter WJ, Winder SJ (2002) Functional plasticity of CH domains. FEBS Lett 513:98-106.
13. Goshima Y, Nakamura F, Strittmatter P, Strittmatter SM (1995) Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 376:509-514.
14. He Z, Tessier-Lavigne M (1997) Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell 90:739-751.
15. Jin Z, Strittmatter SM (1997) Rac1 mediates collapsin-1-induced growth cone collapse. J Neurosci 17:6256-6263.
16. Jurney WM, Gallo G, Letourneau PC, McLoon SC (2002) Rac1-mediated endocytosis during ephrin-A2- and semaphorin 3A-induced growth cone collapse. J Neurosci 22:6019-6028.
17. Kolodkin AL, Levengood DV, Rowe EG, Tai YT, Giger RJ, Ginty DD (1997) Neuropilin is a semaphorin III receptor. Cell 90:753-762.
18. Lander HM, Hajjar DP, Hempstead BL, Mirza UA, Chait BT, Campbell S, Quilliam LA (1997) A molecular redox switch on p21(ras). Structural basis for the nitric oxide-p21(ras) interaction. J Biol Chem 272:4323-4326.
19. Luo Y, Raible D, Raper JA (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75:217-227.
20. Massey V (1994) Activation of molecular oxygen by flavins and flavoproteins. J Biol Chem 269:22459-22462.
21. Massey V (1995) Introduction: flavoprotein structure and mechanism. FASEB J 9:473-475.
22. Mitsui N, Inatome R, Takahashi S, Goshima Y, Yamamura H, Yanagi S (2002) Involvement of Fes/Fps tyrosine kinase in semaphorin3A signaling. EMBO J 21:3274-3285.
23. Munoz LM, Zayachkivsky A, Kunz RB, Hunt JM, Wang G, Scott SA (2005) Ephrin-A5 inhibits growth of embryonic sensory neurons. Dev Biol 283:397-408.
24. Nadella M, Bianchet MA, Gabelli SB, Barrila J, Amzel LM (2005) Structure and activity of the axon guidance protein MICAL. Proc Natl Acad Sci USA 102:16830-16835.
25. Nakamura F, Tanaka M, Takahashi T, Kalb RG, Strittmatter SM (1998) Neuropilin-1 extracellular domains mediate semaphorin D/III-induced growth cone collapse. Neuron 21:1093-1100.
26. Pasterkamp RJ, Kolodkin AL (2003) Semaphorin junction: making tracks toward neural connectivity. Curr Opin Neurobiol 13:79-89.
27. Pasterkamp RJ, Dai HN, Terman JR, Wahlin KJ, Kim B, Bregman BS, Popovich PG, Kolodkin AL (2005) MICAL flavoprotein monooxygenases: expression during neural development and following spinal cord injuries in the rat. Mol Cell Neurosci 31:52-69.
28. Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453-465.
29. Sasaki Y, Cheng C, Uchida Y, Nakajima O, Ohshima T, Yagi T, Taniguchi M, Nakayama T, Kishida R, Kudo Y, Ohno S, Nakamura F, Goshima Y (2002) Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron 35:907-920.
30. Sattler M, Salgia R, Shrikhande G, Verma S, Uemura N, Law SF, Golemis EA, Griffin JD (1997) Differential signaling after beta1 integrin ligation is mediated through binding of CRKL to p120(CBL) and p110(HEF1). J Biol Chem 272:14320-14326.
31. Siebold C, Berrow N, Walter TS, Harlos K, Owens RJ, Stuart DI, Terman JR, Kolodkin AL, Pasterkamp RJ, Jones EY (2005) High-resolution structure of the catalytic region of MICAL (molecule interacting with CasL), a multidomain flavoenzyme-signaling molecule. Proc Natl Acad Sci USA 102:16836-16841.
32. Suzuki T, Nakamoto T, Ogawa S, Seo S, Matsumura T, Tachibana K, Morimoto C, Hirai H (2002) MICAL, a novel CasL interacting molecule, associates with vimentin. J Biol Chem 277:14933-14941.
33. Takahashi T, Strittmatter SM (2001) Plexina1 autoinhibition by the plexin sema domain. Neuron 29:429-439.
34. Takahashi T, Nakamura F, Jin Z, Kalb RG, Strittmatter SM (1998) Semaphorins A and E act as antagonists of neuropilin-1 and agonists of neuropilin-2 receptors. Nat Neurosci 1:487-493.
35. Takahashi T, Fournier A, Nakamura F, Wang LH, Murakami Y, Kalb RG, Fujisawa H, Strittmatter SM (1999) Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99:59-69.
36. Tamagnone L, Artigiani S, Chen H, He Z, Ming GI, Song H, Chedotal A, Winberg ML, Goodman CS, Poo M, Tessier-Lavigne M, Comoglio PM (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99:71-80.
37. Terman JR, Mao T, Pasterkamp RJ, Yu HH, Kolodkin AL (2002) MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell 109:887-900.
38. Togashi H, Schmidt EF, Strittmatter SM (2006) RanBPM contributes to Semaphorin3A signaling through plexin-A receptors. J Neurosci 26:4961-4969.
39. Toyofuku T, Yoshida J, Sugimoto T, Zhang H, Kumanogoh A, Hori M, Kikutani H (2005) FARP2 triggers signals for Sema3A-mediated axonal repulsion. Nat Neurosci 8:1712-1719.
40. Turner LJ, Hall A (2006) Plexin-induced collapse assay in COS cells. Methods Enzymol 406:665-676.
41. Turner LJ, Nicholls S, Hall A (2004) The activity of the plexin-A1 receptor is regulated by Rac. J Biol Chem 279:33199-33205.
42. Ventura A, Pelicci PG (2002) Semaphorins: green light for redox signaling? Sci STKE 2002:PE44.
43. Wang LH, Strittmatter SM (1997) Brain CRMP forms heterotetramers similar to liver dihydropyrimidinase. J Neurochem 69:2261-2269.
44. Weide T, Teuber J, Bayer M, Barnekow A (2003) MICAL-1 isoforms, novel rab1 interacting proteins. Biochem Biophys Res Commun 306:79-86.
45. Zanata SM, Hovatta I, Rohm B, Puschel AW (2002) Antagonistic effects of Rnd1 and RhoD GTPases regulate receptor activity in Semaphorin 3A-induced cytoskeletal collapse. J Neurosci 22:471-477.