A splice isoform of DNedd4, DNedd4-Long, negatively regulates neuromuscular synaptogenesis and viability in Drosophila

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Zhong, Yunan ^a,b   Shtineman Kotler, Alina ^a,b   Nguyen, Leo ^a,b   Iliadi, Konstantin G ^a,b   Boulianne, Gabrielle L ^a,b   Rotin, Daniela ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; NEDD4 LONG PROTEIN; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; ESCRT PROTEIN; NEDD4 UBIQUITIN PROTEIN LIGASES; PROTEIN KINASE B; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CATALYSIS; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNEDD4LO GENE; DROSOPHILA; EMBRYO DEVELOPMENT; GENE; GENE OVEREXPRESSION; LETHALITY; LOCOMOTION; NEGATIVE FEEDBACK; NEUROMUSCULAR FUNCTION; NONHUMAN; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SYNAPTOGENESIS; WILD TYPE; ANIMAL; BIOCATALYSIS; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; LARVA; METABOLISM; MUSCLE; MUTATION; NEUROMUSCULAR SYNAPSE; PHYSIOLOGY;

ANIMALS; BIOCATALYSIS; DROSOPHILA MELANOGASTER; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GENE EXPRESSION REGULATION; LARVA; LOCOMOTION; MUSCLES; MUTATION; NEUROMUSCULAR JUNCTION; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-AKT; UBIQUITIN-PROTEIN LIGASES;

EID: 81055145718     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027007     Document Type: Article

References (45)

1. Rotin D, Kumar S, (2009) Physiological functions of the HECT family of ubiquitin ligases. Nat Rev Mol Cell Biol 10: 398-409.
2. Plant PJ, Lafont F, Lecat S, Verkade P, Simons K, et al. (2000) Apical membrane targeting of Nedd4 is mediated by an association of its C2 domain with annexin XIIIb. J Cell Biol 149: 1473-1484.
3. Dunn R, Klos DA, Adler AS, Hicke L, (2004) The C2 domain of the Rsp5 ubiquitin ligase binds membrane phosphoinositides and directs ubiquitination of endosomal cargo. J Cell Biol 165: 135-144.
4. Staub O, Dho S, Henry P, Correa J, Ishikawa T, et al. (1996) WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle's syndrome. EMBO J 15: 2371-2380.
5. Kasanov J, Pirozzi G, Uveges AJ, Kay BK, (2001) Characterizing Class I WW domains defines key specificity determinants and generates mutant domains with novel specificities. Chem Biol 8: 231-241.
6. Kanelis V, Rotin D, Forman-Kay JD, (2001) Solution structure of a Nedd4 WW domain-ENaC peptide complex. Nat Struct Biol 8: 407-412.
7. Abriel H, Loffing J, Rebhun JF, Pratt JH, Schild L, et al. (1999) Defective regulation of the epithelial Na+ channel by Nedd4 in Liddle's syndrome. J Clin Invest 103: 667-673.
8. Kamynina E, Debonneville C, Bens M, Vandewalle A, Staub O, (2001) A novel mouse Nedd4 protein suppresses the activity of the epithelial Na+ channel. FASEB J 15: 204-214.
9. Harvey KF, Dinudom A, Cook DI, Kumar S, (2001) The Nedd4-like protein KIAA0439 is a potential regulator of the epithelial sodium channel. J Biol Chem 276: 8597-8601.
10. Lu C, Pribanic S, Debonneville A, Jiang C, Rotin D, (2007) The PY motif of ENaC, mutated in Liddle syndrome, regulates channel internalization, sorting and mobilization from subapical pool. Traffic 8: 1246-1264.
11. Staub O, Gautschi I, Ishikawa T, Breitschopf K, Ciechanover A, et al. (1997) Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination. EMBO J 16: 6325-6336.
12. Lifton RP, Gharavi AG, Geller DS, (2001) Molecular mechanisms of human hypertension. Cell 104: 545-556.
13. Debonneville C, Flores SY, Kamynina E, Plant PJ, Tauxe C, et al. (2001) Phosphorylation of Nedd4-2 by Sgk1 regulates epithelial Na(+) channel cell surface expression. EMBO J 20: 7052-7059.
14. Snyder PM, Olson DR, Thomas BC, (2002) Serum and glucocorticoid-regulated kinase modulates Nedd4-2-mediated inhibition of the epithelial Na+ channel. J Biol Chem 277: 5-8.
15. Cao XR, Lill NL, Boase N, Shi PP, Croucher DR, et al. (2008) Nedd4 controls animal growth by regulating IGF-1 signaling. Sci Signal 1: ra5.
16. Yang B, Gay DL, MacLeod MK, Cao X, Hala T, et al. (2008) Nedd4 augments the adaptive immune response by promoting ubiquitin-mediated degradation of Cbl-b in activated T cells. Nat Immunol 9: 1356-1363.
17. Fouladkou F, Lu C, Jiang C, Zhou L, She Y, et al. (2010) The ubiquitin ligase Nedd4-1 is required for heart development and is a suppressor of thrombospondin-1. J Biol Chem 285: 6770-6780.
18. Kawabe H, Neeb A, Dimova K, Young SM Jr, Takeda M, et al. (2010) Regulation of Rap2A by the ubiquitin ligase Nedd4-1 controls neurite development. Neuron 65: 358-372.
19. Ing B, Shteiman-Kotler A, Castelli M, Henry P, Pak Y, et al. (2007) Regulation of Commissureless by the ubiquitin ligase DNedd4 is required for neuromuscular synaptogenesis in Drosophila melanogaster. Mol Cell Biol 27: 481-496.
20. Liu Y, Oppenheim RW, Sugiura Y, Lin W, (2009) Abnormal development of the neuromuscular junction in Nedd4-deficient mice. Dev Biol 330: 153-166.
21. Myat A, Henry P, McCabe V, Flintoft L, Rotin D, et al. (2002) Drosophila Nedd4, a ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the roundabout receptor. Neuron 35: 447-459.
22. Keshishian H, Chiba A, (1993) Neuromuscular development in Drosophila: insights from single neurons and single genes. Trends Neurosci 16: 278-283.
23. Wolf B, Seeger MA, Chiba A, (1998) Commissureless endocytosis is correlated with initiation of neuromuscular synaptogenesis. Development 125: 3853-3863.
24. Kanelis V, Bruce MC, Skrynnikov NR, Rotin D, Forman-Kay JD, (2006) Structural determinants for high-affinity binding in a Nedd4 WW3* domain-Comm PY motif complex. Structure 14: 543-553.
25. Roseman RR, Pirrotta V, Geyer PK, (1993) The su(Hw) protein insulates expression of the Drosophila melanogaster white gene from chromosomal position-effects. EMBO J 12: 435-442.
26. Guo Y, Zhang SX, Sokol N, Cooley L, Boulianne GL, (2000) Physical and genetic interaction of filamin with presenilin in Drosophila. J Cell Sci 113 Pt 19: 3499-3508.
27. Lee T, Luo L, (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451-461.
28. Sakata T, Sakaguchi H, Tsuda L, Higashitani A, Aigaki T, et al. (2004) Drosophila Nedd4 regulates endocytosis of notch and suppresses its ligand-independent activation. Curr Biol 14: 2228-2236.
29. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
30. Roman G, Davis RL, (2002) Conditional expression of UAS-transgenes in the adult eye with a new gene-switch vector system. Genesis 34: 127-131.
31. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, et al. (2003) A nutrient sensor mechanism controls Drosophila growth. Cell 114: 739-749.
32. Jenkins AB, McCaffery JM, Van Doren M, (2003) Drosophila E-cadherin is essential for proper germ cell-soma interaction during gonad morphogenesis. Development 130: 4417-4426.
33. Schuster CM, Davis GW, Fetter RD, Goodman CS, (1996) Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 17: 655-667.
34. McCabe BD, Marques G, Haghighi AP, Fetter RD, Crotty ML, et al. (2003) The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 39: 241-254.
35. Zaffran S, Astier M, Gratecos D, Semeriva M, (1997) The held out wings (how) Drosophila gene encodes a putative RNA-binding protein involved in the control of muscular and cardiac activity. Development 124: 2087-2098.
36. Beumer K, Matthies HJ, Bradshaw A, Broadie K, (2002) Integrins regulate DLG/FAS2 via a CaM kinase II-dependent pathway to mediate synapse elaboration and stabilization during postembryonic development. Development 129: 3381-3391.
37. Kohsaka H, Takasu E, Nose A, (2007) In vivo induction of postsynaptic molecular assembly by the cell adhesion molecule Fasciclin2. J Cell Biol 179: 1289-1300.
38. Li XM, Dong XP, Luo SW, Zhang B, Lee DH, et al. (2008) Retrograde regulation of motoneuron differentiation by muscle beta-catenin. Nat Neurosci 11: 262-268.
39. Schwander M, Shirasaki R, Pfaff SL, Muller U, (2004) Beta1 integrins in muscle, but not in motor neurons, are required for skeletal muscle innervation. J Neurosci 24: 8181-8191.
40. Bruce MC, Kanelis V, Fouladkou F, Debonneville A, Staub O, et al. (2008) Regulation of Nedd4-2 self-ubiquitination and stability by a PY motif located within its HECT-domain. Biochem J 415: 155-163.
41. Gallagher E, Gao M, Liu YC, Karin M, (2006) Activation of the E3 ubiquitin ligase Itch through a phosphorylation-induced conformational change. Proc Natl Acad Sci U S A 103: 1717-1722.
42. Wiesner S, Ogunjimi AA, Wang HR, Rotin D, Sicheri F, et al. (2007) Autoinhibition of the HECT-type ubiquitin ligase Smurf2 through its C2 domain. Cell 130: 651-662.
43. Wang Y, Chen Z, Bergmann A, (2010) Regulation of EGFR and Notch signaling by distinct isoforms of D-cbl during Drosophila development. Dev Biol 342: 1-10.
44. Brent JR, Werner KM, McCabe BD, (2009) Drosophila larval NMJ dissection. J Vis Exp.
45. Knight D, Iliadi K, Charlton MP, Atwood HL, Boulianne GL, (2007) Presynaptic plasticity and associative learning are impaired in a Drosophila presenilin null mutant. Dev Neurobiol 67: 1598-1613.