A CULLINary ride across the secretory pathway: More than just secretion

Trends in Cell Biology

Volumn 24, Issue 7, 2014, Pages 389-399

  Lu, Albert ^a   Pfeffer, Suzanne R ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cullin proteins; Cullin RING ligases; Golgi complex; Post translational modification; Ubiquitylation

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CULLINRING UBIQUITIN LIGASE; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; CULLIN;

CELL CYCLE REGULATION; CELL MEMBRANE; DEVELOPMENT; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; GOLGI COMPLEX; HUMAN; INTRACELLULAR SIGNALING; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN QUALITY; PROTEIN SECRETION; QUALITY CONTROL; REGULATORY MECHANISM; REVIEW; SECRETORY PATHWAY; UBIQUITINATION; XENOPUS; ANIMAL; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

EUKARYOTA;

ANIMALS; CULLIN PROTEINS; ENDOSOMES; GOLGI APPARATUS; HUMANS; PROTEIN TRANSPORT; SECRETORY PATHWAY; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84903202076     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2014.02.001     Document Type: Review

References (115)

1. Haglund K., et al. Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem. Sci. 2003, 28:598-603.
2. Iwai K., Tokunaga F. Linear polyubiquitination: a new regulator of NF-kappaB activation. EMBO Rep. 2009, 10:706-713.
3. Metzger M.B., et al. HECT and RING finger families of E3 ubiquitin ligases at a glance. J. Cell Sci. 2012, 125:531-537.
4. Petroski M.D., Deshaies R.J. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2005, 6:9-20.
5. Budnik A., Stephens D.J. ER exit sites - localization and control of COPII vesicle formation. FEBS Lett. 2009, 583:3796-3803.
6. Jin L., et al. Ubiquitin-dependent regulation of COPII coat size and function. Nature 2012, 482:495-500.
7. Ohh M., et al. The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix. Mol. Cell 1998, 1:959-968.
8. Cohen M., et al. Ubp3 requires a cofactor, Bre5, to specifically de-ubiquitinate the COPII protein, Sec23. Nat. Cell Biol. 2003, 5:661-667.
9. Cohen M., et al. Deubiquitination, a new player in Golgi to endoplasmic reticulum retrograde transport. J. Biol. Chem. 2003, 278:51989-51992.
10. Boyadjiev S.A., et al. Cranio-lenticulo-sutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmic-reticulum-to-Golgi trafficking. Nat. Genet. 2006, 38:1192-1197.
11. Fromme J.C., et al. The genetic basis of a craniofacial disease provides insight into COPII coat assembly. Dev. Cell 2007, 13:623-634.
12. Lubensky I.A., et al. Allelic deletions of the VHL gene detected in multiple microscopic clear cell renal lesions in von Hippel-Lindau disease patients. Am. J. Pathol. 1996, 149:2089-2094.
13. Wilson P.D., et al. Abnormal extracellular matrix and excessive growth of human adult polycystic kidney disease epithelia. J. Cell. Physiol. 1992, 150:360-369.
14. Bar-Nun S. The role of p97/Cdc48p in endoplasmic reticulum-associated degradation: from the immune system to yeast. Curr. Top. Microbiol. Immunol. 2005, 300:95-125.
15. Olzmann J.A., et al. The mammalian endoplasmic reticulum-associated degradation system. Cold Spring Harb. Perspect. Biol. 2013, 5:a013185.
16. den Besten W., et al. NEDD8 links cullin-RING ubiquitin ligase function to the p97 pathway. Nat. Struct. Mol. Biol. 2012, 19:511-516. S511.
17. Alexandru G., et al. UBXD7 binds multiple ubiquitin ligases and implicates p97 in HIF1alpha turnover. Cell 2008, 134:804-816.
18. Yoshida Y., et al. E3 ubiquitin ligase that recognizes sugar chains. Nature 2002, 418:438-442.
19. Moremen K.W., et al. Vertebrate protein glycosylation: diversity, synthesis and function. Nat. Rev. Mol. Cell Biol. 2012, 13:448-462.
20. Hirsch C., et al. A role for N-glycanase in the cytosolic turnover of glycoproteins. EMBO J. 2003, 22:1036-1046.
21. Li G., et al. The AAA ATPase p97 links peptide N-glycanase to the endoplasmic reticulum-associated E3 ligase autocrine motility factor receptor. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:8348-8353.
22. Yoshida Y., et al. Fbs2 is a new member of the E3 ubiquitin ligase family that recognizes sugar chains. J. Biol. Chem. 2003, 278:43877-43884.
23. Yoshida Y., et al. Glycoprotein-specific ubiquitin ligases recognize N-glycans in unfolded substrates. EMBO Rep. 2005, 6:239-244.
24. Cai H., et al. BACE1 is the major beta-secretase for generation of Abeta peptides by neurons. Nat. Neurosci. 2001, 4:233-234.
25. Gong B., et al. SCFFbx2-E3-ligase-mediated degradation of BACE1 attenuates Alzheimer's disease amyloidosis and improves synaptic function. Aging Cell 2010, 9:1018-1031.
26. Margottin F., et al. A novel human WD protein, h-beta TrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol. Cell 1998, 1:565-574.
27. Emr S., et al. Journeys through the Golgi - taking stock in a new era. J. Cell Biol. 2009, 187:449-453.
28. Vinke F.P., et al. The multiple facets of the Golgi reassembly stacking proteins. Biochem. J. 2011, 433:423-433.
29. Wagner S.A., et al. Proteomic analyses reveal divergent ubiquitylation site patterns in murine tissues. Mol. Cell. Proteomics 2012, 11:1578-1585.
30. Litterman N., et al. An OBSL1-Cul7Fbxw8 ubiquitin ligase signaling mechanism regulates Golgi morphology and dendrite patterning. PLoS Biol. 2011, 9:5-21.
31. Ye B., et al. Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 2007, 130:717-729.
32. Horton A.C., et al. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 2005, 48:757-771.
33. Lavieu G., et al. Stapled Golgi cisternae remain in place as cargo passes through the stack. Elife 2013, 2:e00558.
34. Feng Y., et al. Structural insight into Golgi membrane stacking by GRASP65 and GRASP55 proteins. J. Biol. Chem. 2013, 288:28418-28427.
35. Thayer D.A., et al. Increased neuronal activity fragments the Golgi complex. Proc. Natl. Acad. Sci. U.S.A. 2012, 110:1482-1487.
36. Kinseth M.A., et al. The Golgi-associated protein GRASP is required for unconventional protein secretion during development. Cell 2007, 130:524-534.
37. Duran J.M., et al. Unconventional secretion of Acb1 is mediated by autophagosomes. J. Cell Biol. 2010, 188:527-536.
38. Manjithaya R., et al. Unconventional secretion of Pichia pastoris Acb1 is dependent on GRASP protein, peroxisomal functions, and autophagosome formation. J. Cell Biol. 2010, 188:537-546.
39. Gee H.Y., et al. Rescue of DeltaF508-CFTR trafficking via a GRASP-dependent unconventional secretion pathway. Cell 2011, 146:746-760.
40. Moreau D., et al. Genome-wide RNAi screens identify genes required for Ricin and PE intoxications. Dev. Cell 2011, 21:231-244.
41. Lu A., Pfeffer S.R. Golgi-associated RhoBTB3 targets Cyclin E for ubiquitylation and promotes cell cycle progression. J. Cell Biol. 2013, 203:233-250.
42. Luhrig S., et al. The novel BTB-kelch protein, KBTBD8, is located in the Golgi apparatus and translocates to the spindle apparatus during mitosis. Cell Div. 2013, 8:3.
43. Uchiyama K., et al. p37 is a p97 adaptor required for Golgi and ER biogenesis in interphase and at the end of mitosis. Dev. Cell 2006, 11:803-816.
44. Tang D., et al. The ubiquitin ligase HACE1 regulates Golgi membrane dynamics during the cell cycle. Nat. Commun. 2011, 2:501.
45. Wilkins A., et al. RhoBTB2 is a substrate of the mammalian Cul3 ubiquitin ligase complex. Genes Dev. 2004, 18:856-861.
46. Berthold J., et al. Characterization of RhoBTB-dependent Cul3 ubiquitin ligase complexes - evidence for an autoregulatory mechanism. Exp. Cell Res. 2008, 314:3453-3465.
47. Chang F.K., et al. DBC2 is essential for transporting vesicular stomatitis virus glycoprotein. J. Mol. Biol. 2006, 364:302-308.
48. Espinosa E.J., et al. RhoBTB3: a Rho GTPase-family ATPase required for endosome to Golgi transport. Cell 2009, 137:938-948.
49. Aspenstrom P., et al. Rho GTPases have diverse effects on the organization of the actin filament system. Biochem. J. 2004, 377:327-337.
50. Siripurapu V., et al. DBC2 significantly influences cell-cycle, apoptosis, cytoskeleton and membrane-trafficking pathways. J. Mol. Biol. 2005, 346:83-89.
51. Anitei M., Hoflack B. Bridging membrane and cytoskeleton dynamics in the secretory and endocytic pathways. Nat. Cell Biol. 2012, 14:11-19.
52. Chen Y., et al. Cullin mediates degradation of RhoA through evolutionarily conserved BTB adaptors to control actin cytoskeleton structure and cell movement. Mol. Cell 2009, 35:841-855.
53. Hudson A.M., Cooley L. Drosophila Kelch functions with Cullin-3 to organize the ring canal actin cytoskeleton. J. Cell Biol. 2010, 188:29-37.
54. Wang W., et al. Gigaxonin interacts with tubulin folding cofactor B and controls its degradation through the ubiquitin-proteasome pathway. Curr. Biol. 2005, 15:2050-2055.
55. Mahammad S., et al. Giant axonal neuropathy-associated gigaxonin mutations impair intermediate filament protein degradation. J. Clin. Invest. 2013, 123:1964-1975.
56. Cullen V.C., et al. Gigaxonin is associated with the Golgi and dimerises via its BTB domain. Neuroreport 2004, 15:873-876.
57. Berthold J., et al. Rho GTPases of the RhoBTB subfamily and tumorigenesis. Acta Pharmacol. Sin. 2008, 29:285-295.
58. Yoshihara T., et al. Cyclin D1 down-regulation is essential for DBC2's tumor suppressor function. Biochem. Biophys. Res. Commun. 2007, 358:1076-1079.
59. Musgrove E.A., et al. Cyclin D as a therapeutic target in cancer. Nat. Rev. Cancer 2011, 11:558-572.
60. Koepp D.M., et al. Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 2001, 294:173-177.
61. Bhaskaran N., et al. Fbw7alpha and Fbw7gamma collaborate to shuttle cyclin E1 into the nucleolus for multiubiquitylation. Mol. Cell. Biol. 2013, 33:85-97.
62. Hwang H.C., Clurman B.E. Cyclin E in normal and neoplastic cell cycles. Oncogene 2005, 24:2776-2786.
63. Matsumoto Y., Maller J.L. A centrosomal localization signal in cyclin E required for Cdk2-independent S phase entry. Science 2004, 306:885-888.
64. Jorgensen P., Tyers M. How cells coordinate growth and division. Curr. Biol. 2004, 14:R1014-R1027.
65. McCusker D., Kellogg D.R. Plasma membrane growth during the cell cycle: unsolved mysteries and recent progress. Curr. Opin. Cell Biol. 2012, 24:845-851.
66. Jackowski S. Cell cycle regulation of membrane phospholipid metabolism. J. Biol. Chem. 1996, 271:20219-20222.
67. Kent C., Carman G.M. Interactions among pathways for phosphatidylcholine metabolism, CTP synthesis and secretion through the Golgi apparatus. Trends Biochem. Sci. 1999, 24:146-150.
68. Chen B.B., et al. Calmodulin antagonizes a calcium-activated SCF ubiquitin E3 ligase subunit, FBXL2, to regulate surfactant homeostasis. Mol. Cell. Biol. 2011, 31:1905-1920.
69. Chen B.B., Mallampalli R.K. Masking of a nuclear signal motif by monoubiquitination leads to mislocalization and degradation of the regulatory enzyme cytidylyltransferase. Mol. Cell. Biol. 2009, 29:3062-3075.
70. Wang C., et al. Identification of FBL2 as a geranylgeranylated cellular protein required for hepatitis C virus RNA replication. Mol. Cell 2005, 18:425-434.
71. Kuchay S., et al. FBXL2- and PTPL1-mediated degradation of p110-free p85beta regulatory subunit controls the PI(3)K signalling cascade. Nat. Cell Biol. 2013, 15:472-480.
72. Chen B.B., et al. FBXL2 is a ubiquitin E3 ligase subunit that triggers mitotic arrest. Cell Cycle 2011, 10:3487-3494.
73. Chen B.B., et al. Skp-cullin-F box E3 ligase component FBXL2 ubiquitinates Aurora B to inhibit tumorigenesis. Cell Death Dis. 2013, 4:e759.
74. Tang D., Wang Y. Cell cycle regulation of Golgi membrane dynamics. Trends Cell Biol. 2013, 23:296-304.
75. Lee R.H., et al. XRab40 and XCullin5 form a ubiquitin ligase complex essential for the noncanonical Wnt pathway. EMBO J. 2007, 26:3592-3606.
76. Choi S.C., Han J.K. Rap2 is required for Wnt/beta-catenin signaling pathway in Xenopus early development. EMBO J. 2005, 24:985-996.
77. Mikryukov A., Moss T. Agonistic and antagonistic roles for TNIK and MINK in non-canonical and canonical Wnt signalling. PLoS ONE 2012, 7:e43330.
78. Gao C., Chen Y.G. Dishevelled: the hub of Wnt signaling. Cell. Signal. 2010, 22:717-727.
79. Pfeffer S.R. Rab GTPases: master regulators of membrane trafficking. Curr. Opin. Cell Biol. 1994, 6:522-526.
80. Rodriguez-Gabin A.G., et al. Vesicle transport in oligodendrocytes: probable role of Rab40c protein. J. Neurosci. Res. 2004, 76:758-770.
81. Tan R., et al. Small GTPase Rab40c associates with lipid droplets and modulates the biogenesis of lipid droplets. PLoS ONE 2013, 8:e63213.
82. Jacob A., et al. Rab40b regulates trafficking of MMP2 and MMP9 during invadopodia formation and invasion of breast cancer cells. J. Cell Sci. 2013, 126:4647-4658.
83. Kumar K.G., et al. SCF(HOS) ubiquitin ligase mediates the ligand-induced down-regulation of the interferon-alpha receptor. EMBO J. 2003, 22:5480-5490.
84. Schaefer H., Rongo C. KEL-8 is a substrate receptor for CUL3-dependent ubiquitin ligase that regulates synaptic glutamate receptor turnover. Mol. Biol. Cell 2006, 17:1250-1260.
85. Meyer-Schaller N., et al. The human Dcn1-like protein DCNL3 promotes Cul3 neddylation at membranes. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:12365-12370.
86. Roberts D., et al. Modulation of phototropic responsiveness in Arabidopsis through ubiquitination of phototropin 1 by the CUL3-Ring E3 ubiquitin ligase CRL3(NPH3). Plant Cell 2011, 23:3627-3640.
87. D'Souza-Schorey C., Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 2006, 7:347-358.
88. Yano H., et al. Fbx8 makes Arf6 refractory to function via ubiquitination. Mol. Biol. Cell 2008, 19:822-832.
89. Cho H.J., et al. c-Myc stimulates cell invasion by inhibiting FBX8 function. Mol. Cells 2010, 30:355-362.
90. Wang F., et al. FBX8 acts as an invasion and metastasis suppressor and correlates with poor survival in hepatocellular carcinoma. PLoS ONE 2013, 8:e65495.
91. Raju T.N. The Nobel chronicles. 1974: Albert Claude (1899-1983), George Emil Palade (b 1912), and Christian Rene de Duve (b 1917). Lancet 1999, 354:1219.
92. Pfeffer S.R. A prize for membrane magic. Cell 2013, 155:1203-1206.
93. Bennett E.J., et al. Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell 2010, 143:951-965.
94. Emanuele M.J., et al. Global identification of modular cullin-RING ligase substrates. Cell 2011, 147:459-474.
95. Chan C.H., et al. Pharmacological inactivation of Skp2 SCF ubiquitin ligase restricts cancer stem cell traits and cancer progression. Cell 2013, 154:556-568.
96. Pei X.H., et al. Cytoplasmic CUL9/PARC ubiquitin ligase is a tumor suppressor and promotes p53-dependent apoptosis. Cancer Res. 2011, 71:2969-2977.
97. Wei D., Sun Y. Small RING finger proteins RBX1 and RBX2 of SCF E3 ubiquitin ligases: the role in cancer and as cancer targets. Genes Cancer 2010, 1:700-707.
98. Zheng N., et al. Structure of the Cul1-Rbx1-Skp1-F box Skp2 SCF ubiquitin ligase complex. Nature 2002, 416:703-709.
99. Duda D.M., et al. Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 2008, 134:995-1006.
100. Saha A., Deshaies R.J. Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation. Mol. Cell 2008, 32:21-31.
101. Xu L., et al. BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 2003, 425:316-321.
102. Pintard L., et al. The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 2003, 425:311-316.
103. Geyer R., et al. BTB/POZ domain proteins are putative substrate adaptors for cullin 3 ubiquitin ligases. Mol. Cell 2003, 12:783-790.
104. Perez-Torrado R., et al. Born to bind: the BTB protein--protein interaction domain. Bioessays 2006, 28:1194-1202.
105. Matsumoto A., et al. Fbxw7beta resides in the endoplasmic reticulum membrane and protects cells from oxidative stress. Cancer Sci. 2011, 102:749-755.
106. Dementieva I.S., et al. Pentameric assembly of potassium channel tetramerization domain-containing protein 5. J. Mol. Biol. 2009, 387:175-191.
107. Bayon Y., et al. KCTD5, a putative substrate adaptor for cullin3 ubiquitin ligases. FEBS J. 2008, 275:3900-3910.
108. Nacak T.G., et al. The BTB-kelch protein LZTR-1 is a novel Golgi protein that is degraded upon induction of apoptosis. J. Biol. Chem. 2006, 281:5065-5071.
109. Wadelin F.R., et al. PRAME is a Golgi-targeted protein that associates with the elongin BC complex and is upregulated by interferon-gamma and bacterial PAMPs. PLoS ONE 2013, 8:e58052.
110. Beranger F., et al. Post-translational processing and subcellular localization of the Ras-related Rap2 protein. Oncogene 1991, 6:1835-1842.
111. Huotari J., et al. Cullin-3 regulates late endosome maturation. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:823-828.
112. Schnatwinkel C., et al. The Rab5 effector Rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLoS Biol. 2004, 2:E261.
113. Henne W.M., et al. The ESCRT pathway. Dev. Cell 2011, 21:77-91.
114. Polo S., et al. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 2002, 416:451-455.
115. Kim B.Y., et al. Spongiform neurodegeneration-associated E3 ligase Mahogunin ubiquitylates TSG101 and regulates endosomal trafficking. Mol. Biol. Cell 2007, 18:1129-1142.