An ER Complex of ODR-4 and ODR-8/Ufm1 Specific Protease 2 Promotes GPCR Maturation by a Ufm1-Independent Mechanism

PLoS Genetics

Volumn 10, Issue 3, 2014, Pages

  Chen, Changchun ^a   Itakura, Eisuke ^a   Weber, Katherine P ^a   Hegde, Ramanujan S ^a   de Bono, Mario ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE PROTEINASE; G PROTEIN COUPLED RECEPTOR; PROTEIN ODR 4; UFM1 SPECIFIC PROTEASE 2; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; ODR-10 PROTEIN, C ELEGANS; ODR-4 PROTEIN, C ELEGANS; OLFACTORY RECEPTOR; PROTEIN; UFM1 PROTEIN, HUMAN; UFSP2 PROTEIN, MOUSE;

ARTICLE; BIOGENESIS; CATALYSIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; FRAMESHIFT MUTATION; GENE FREQUENCY; GENETIC CONSERVATION; HOMOZYGOSITY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MICROSCOPY; MOLECULAR EVOLUTION; OPEN READING FRAME; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTON TRANSPORT; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; CAENORHABDITIS ELEGANS; CHEMORECEPTOR CELL; EUKARYOTIC FLAGELLUM; GENETICS; HELA CELL LINE; METABOLISM; MOUSE; ODOR; OLFACTORY RECEPTOR;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHEMORECEPTOR CELLS; CILIA; CYSTEINE ENDOPEPTIDASES; ENDOPLASMIC RETICULUM; HELA CELLS; HUMANS; MICE; OLFACTORY RECEPTOR NEURONS; PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, ODORANT; SMELL;

EID: 84897472462     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004082     Document Type: Article

References (49)

1. Buchberger A, Bukau B, Sommer T, (2010) Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms. Mol Cell 40: 238-252.
2. Rosenbaum EE, Brehm KS, Vasiljevic E, Liu CH, Hardie RC, et al. (2011) XPORT-dependent transport of TRP and rhodopsin. Neuron 72: 602-615.
3. Halevi S, McKay J, Palfreyman M, Yassin L, Eshel M, et al. (2002) The C. elegans ric-3 gene is required for maturation of nicotinic acetylcholine receptors. EMBO J 21: 1012-1020.
4. Muchowski PJ, Wacker JL, (2005) Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 6: 11-22.
5. Venkatakrishnan AJ, Deupi X, Lebon G, Tate CG, Schertler GF, et al. (2013) Molecular signatures of G-protein-coupled receptors. Nature 494: 185-194.
6. Park E, Rapoport TA, (2012) Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu Rev Biophys 41: 21-40.
7. Mizrachi D, Segaloff DL, (2004) Intracellularly located misfolded glycoprotein hormone receptors associate with different chaperone proteins than their cognate wild-type receptors. Mol Endocrinol 18: 1768-1777.
8. Morello JP, Salahpour A, Petaja-Repo UE, Laperriere A, Lonergan M, et al. (2001) Association of calnexin with wild type and mutant AVPR2 that causes nephrogenic diabetes insipidus. Biochemistry 40: 6766-6775.
9. Lu M, Echeverri F, Moyer BD, (2003) Endoplasmic reticulum retention, degradation, and aggregation of olfactory G-protein coupled receptors. Traffic 4: 416-433.
10. Saito H, Kubota M, Roberts RW, Chi Q, Matsunami H, (2004) RTP family members induce functional expression of mammalian odorant receptors. Cell 119: 679-691.
11. Stamnes MA, Shieh BH, Chuman L, Harris GL, Zuker CS, (1991) The cyclophilin homolog ninaA is a tissue-specific integral membrane protein required for the proper synthesis of a subset of Drosophila rhodopsins. Cell 65: 219-227.
12. Bermak JC, Li M, Bullock C, Zhou QY, (2001) Regulation of transport of the dopamine D1 receptor by a new membrane-associated ER protein. Nat Cell Biol 3: 492-498.
13. Hurt CM, Ho VK, Angelotti T, (2013) Systematic and quantitative analysis of G protein-coupled receptor trafficking motifs. Methods Enzymol 521: 171-187.
14. Mendes HF, Zaccarini R, Cheetham ME, (2010) Pharmacological manipulation of rhodopsin retinitis pigmentosa. Adv Exp Med Biol 664: 317-323.
15. Morello JP, Bichet DG, (2001) Nephrogenic diabetes insipidus. Annu Rev Physiol 63: 607-630.
16. Maya-Nunez G, Janovick JA, Ulloa-Aguirre A, Soderlund D, Conn PM, et al. (2002) Molecular basis of hypogonadotropic hypogonadism: restoration of mutant (E(90)K) GnRH receptor function by a deletion at a distant site. J Clin Endocrinol Metab 87: 2144-2149.
17. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI, (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83: 207-218.
18. Thomas JH, Robertson HM, (2008) The Caenorhabditis chemoreceptor gene families. BMC Biol 6: 42.
19. Sengupta P, Chou JH, Bargmann CI, (1996) odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84: 899-909.
20. Dwyer ND, Troemel ER, Sengupta P, Bargmann CI, (1998) Odorant receptor localization to olfactory cilia is mediated by ODR-4, a novel membrane-associated protein. Cell 93: 455-466.
21. de Bono M, Tobin DM, Davis MW, Avery L, Bargmann CI, (2002) Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli. Nature 419: 899-903.
22. Rogers C, Persson A, Cheung B, de Bono M, (2006) Behavioral motifs and neural pathways coordinating O2 responses and aggregation in C. elegans. Curr Biol 16: 649-659.
23. Komatsu M, Chiba T, Tatsumi K, Iemura S, Tanida I, et al. (2004) A novel protein-conjugating system for Ufm1, a ubiquitin-fold modifier. EMBO J 23: 1977-1986.
24. Sasakawa H, Sakata E, Yamaguchi Y, Komatsu M, Tatsumi K, et al. (2006) Solution structure and dynamics of Ufm1, a ubiquitin-fold modifier 1. Biochem Biophys Res Commun 343: 21-26.
25. Ha BH, Jeon YJ, Shin SC, Tatsumi K, Komatsu M, et al. (2011) Structure of ubiquitin-fold modifier 1-specific protease UfSP2. J Biol Chem 286: 10248-10257.
26. Kang SH, Kim GR, Seong M, Baek SH, Seol JH, et al. (2007) Two novel ubiquitin-fold modifier 1 (Ufm1)-specific proteases, UfSP1 and UfSP2. J Biol Chem 282: 5256-5262.
27. Ha BH, Ahn HC, Kang SH, Tanaka K, Chung CH, et al. (2008) Structural basis for Ufm1 processing by UfSP1. J Biol Chem 283: 14893-14900.
28. Rolls MM, Hall DH, Victor M, Stelzer EH, Rapoport TA, (2002) Targeting of rough endoplasmic reticulum membrane proteins and ribosomes in invertebrate neurons. Mol Biol Cell 13: 1778-1791.
29. Witte K, Schuh AL, Hegermann J, Sarkeshik A, Mayers JR, et al. (2011) TFG-1 function in protein secretion and oncogenesis. Nat Cell Biol 13: 550-558.
30. Grant B, Hirsh D, (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10: 4311-4326.
31. Treusch S, Knuth S, Slaugenhaupt SA, Goldin E, Grant BD, et al. (2004) Caenorhabditis elegans functional orthologue of human protein h-mucolipin-1 is required for lysosome biogenesis. Proc Natl Acad Sci U S A 101: 4483-4488.
32. Hermann GJ, Schroeder LK, Hieb CA, Kershner AM, Rabbitts BM, et al. (2005) Genetic analysis of lysosomal trafficking in Caenorhabditis elegans. Mol Biol Cell 16: 3273-3288.
33. Kaplan OI, Molla-Herman A, Cevik S, Ghossoub R, Kida K, et al. (2010) The AP-1 clathrin adaptor facilitates cilium formation and functions with RAB-8 in C. elegans ciliary membrane transport. J Cell Sci 123: 3966-3977.
34. Dwyer ND, Adler CE, Crump JG, L'Etoile ND, Bargmann CI, (2001) Polarized dendritic transport and the AP-1 mu1 clathrin adaptor UNC-101 localize odorant receptors to olfactory cilia. Neuron 31: 277-287.
35. Mizuno-Yamasaki E, Rivera-Molina F, Novick P, (2012) GTPase networks in membrane traffic. Annu Rev Biochem 81: 637-659.
36. Duvernay MT, Filipeanu CM, Wu G, (2005) The regulatory mechanisms of export trafficking of G protein-coupled receptors. Cell Signal 17: 1457-1465.
37. Sumakovic M, Hegermann J, Luo L, Husson SJ, Schwarze K, et al. (2009) UNC-108/RAB-2 and its effector RIC-19 are involved in dense core vesicle maturation in Caenorhabditis elegans. J Cell Biol 186: 897-914.
38. Edwards SL, Charlie NK, Richmond JE, Hegermann J, Eimer S, et al. (2009) Impaired dense core vesicle maturation in Caenorhabditis elegans mutants lacking Rab2. J Cell Biol 186: 881-895.
39. Chun DK, McEwen JM, Burbea M, Kaplan JM, (2008) UNC-108/Rab2 regulates postendocytic trafficking in Caenorhabditis elegans. Mol Biol Cell 19: 2682-2695.
40. Hertel P, Daniel J, Stegehake D, Vaupel H, Kailayangiri S, et al. (2013) The Ubiquitin-fold Modifier 1 (Ufm1) Cascade of Caenorhabditis elegans. J Biol Chem 288: 10661-10671.
41. Chen C, Fenk LA, de Bono M, (2013) Efficient genome editing in Caenorhabditis elegans by CRISPR-targeted homologous recombination. Nucleic Acids Res 41 (20) (): e193.
42. Brodsky JL, (2012) Cleaning up: ER-associated degradation to the rescue. Cell 151: 1163-1167.
43. Nakatsukasa K, Huyer G, Michaelis S, Brodsky JL, (2008) Dissecting the ER-associated degradation of a misfolded polytopic membrane protein. Cell 132: 101-112.
44. Zhang ZR, Bonifacino JS, Hegde RS, (2013) Deubiquitinases sharpen substrate discrimination during membrane protein degradation from the ER. Cell 154: 609-622.
45. Sulston J, Hodgkin J (1988) Methods. In: Wood WB, editor. The nematode Caenorhabditis elegans. Cold Spring Harbor: CSHL Press. pp. 587-606.
46. de Bono M, Bargmann CI, (1998) Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94: 679-689.
47. Bargmann CI, Hartwieg E, Horvitz HR, (1993) Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74: 515-527.
48. Cheung BH, Cohen M, Rogers C, Albayram O, de Bono M, (2005) Experience-dependent modulation of C. elegans behavior by ambient oxygen. Curr Biol 15: 905-917.
49. Tatsumi K, Sou YS, Tada N, Nakamura E, Iemura S, et al. (2010) A novel type of E3 ligase for the Ufm1 conjugation system. J Biol Chem 285: 5417-5427.