HUWE1 Is a molecular link controlling RAF-1 activity supported by the Shoc2 scaffold

Molecular and Cellular Biology

Volumn 34, Issue 19, 2014, Pages 3579-3593

  Jang, Eun Ryoung ^a   Shi, Ping ^a   Bryant, Jamal ^a   Chen, Jing ^a   Dukhande, Vikas ^a   Gentry, Matthew S ^a   Jang, HyeIn ^a   Jeoung, Myoungkun ^a   Galperin, Emilia ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; RAF PROTEIN; SCAFFOLD PROTEIN; SHOC2 SCAFFOLD PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE E3 HUWE1; UNCLASSIFIED DRUG; HUWE1 PROTEIN, HUMAN; SHOC2 PROTEIN, HUMAN; SIGNAL PEPTIDE; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CELL PROLIFERATION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; NEGATIVE FEEDBACK; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; CHEMICAL STRUCTURE; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; GENE EXPRESSION REGULATION; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PROTEIN DOMAIN;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, MOLECULAR; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTO-ONCOGENE PROTEINS C-RAF; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84906954649     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00811-14     Document Type: Article

References (66)

1. Katz M, Amit I, Yarden Y. 2007. Regulation of MAPKs by growth factors and receptor tyrosine kinases. Biochim. Biophys. Acta 1773:1161-1176. http://dx.doi.org/10.1016/j.bbamcr.2007.01.002.
2. Bhattacharyya RP, Remenyi A, Yeh BJ, Lim WA. 2006. Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu. Rev. Biochem. 75:655-680. http://dx.doi.org/10.1146/annurev.biochem.75.103004.142710.
3. Witzel F, Maddison L, Bluthgen N. 2012. How scaffolds shape MAPK signaling: what we know and opportunities for systems approaches. Front. Physiol. 3:475. http://dx.doi.org/10.3389/fphys.2012.00475.
4. Pullikuth AK, Catling AD. 2007. Scaffold mediated regulation of MAPK signaling and cytoskeletal dynamics: a perspective. Cell. Signal. 19:1621- 1632. http://dx.doi.org/10.1016/j.cellsig.2007.04.012.
5. Brown MD, Sacks DB. 2008. Compartmentalised MAPK pathways. Handb. Exp. Pharmacol. 186:205-235. http://dx.doi.org/10.1007/978-3 -540-72843-6_9.
6. Brown MD, Sacks DB. 2009. Protein scaffolds in MAP kinase signalling. Cell. Signal. 21:462-469. http://dx.doi.org/10.1016/j.cellsig.2008.11.013.
7. Good MC, Zalatan JG, Lim WA. 2011. Scaffold proteins: hubs for controlling the flow of cellular information. Science 332:680-686. http://dx.doi.org/10.1126/science.1198701.
8. Sieburth DS, Sun Q, Han M. 1998. SUR-8, a conserved Ras-binding protein with leucine-rich repeats, positively regulates Ras-mediated signaling in C. elegans. Cell 94:119-130. http://dx.doi.org/10.1016/S0092 -8674(00)81227-1.
9. Selfors LM, Schutzman JL, Borland CZ, Stern MJ. 1998. soc-2 encodes a leucine-rich repeat protein implicated in fibroblast growth factor receptor signaling. Proc. Natl. Acad. Sci. U. S. A. 95:6903-6908. http://dx.doi.org/10.1073/pnas.95.12.6903.
10. Cordeddu V, Di Schiavi E, Pennacchio LA, Ma'ayan A, Sarkozy A, Fodale V, Cecchetti S, Cardinale A, Martin J, Schackwitz W, Lipzen A, Zampino G, Mazzanti L, Digilio MC, Martinelli S, Flex E, Lepri F, Bartholdi D, Kutsche K, Ferrero GB, Anichini C, Selicorni A, Rossi C, Tenconi R, Zenker M, Merlo D, Dallapiccola B, Iyengar R, Bazzicalupo P, Gelb BD, Tartaglia M. 2009. Mutation of SHOC2 promotes aberrant protein N-myristoylation and causes Noonan-like syndrome with loose anagen hair. Nat. Genet. 41:1022-1026. http://dx.doi.org/10.1038/ng.425.
11. Yi J, Chen M, Wu X, Yang X, Xu T, Zhuang Y, Han M, Xu R. 2010. Endothelial SUR-8 acts in an ERK-independent pathway during atrioventricular cushion development. Dev. Dyn. 239:2005-2013. http://dx.doi.org/10.1002/dvdy.22343.
12. Li W, Han M, Guan KL. 2000. The leucine-rich repeat protein SUR-8 enhances MAP kinase activation and forms a complex with Ras and Raf. Genes Dev. 14:895-900.
13. Galperin E, Abdelmoti L, Sorkin A. 2012. Shoc2 is targeted to late endosomes and required for Erk1/2 activation in EGF-stimulated cells. PLoS One 7:e36469. http://dx.doi.org/10.1371/journal.pone.0036469.
14. Matsunaga-Udagawa R, Fujita Y, Yoshiki S, Terai K, Kamioka Y, Kiyokawa E, Yugi K, Aoki K, Matsuda M. 2010. The scaffold protein Shoc2/SUR-8 accelerates the interaction of Ras and Raf. J. Biol. Chem. 285:7818-7826. http://dx.doi.org/10.1074/jbc.M109.053975.
15. Yoshiki S, Matsunaga-Udagawa R, Aoki K, Kamioka Y, Kiyokawa E, Matsuda M. 2010. Ras and calcium signaling pathways converge at Raf1 via the Shoc2 scaffold protein. Mol. Biol. Cell 21:1088-1096. http://dx.doi.org/10.1091/mbc.E09-06-0455.
16. de Bie P, Ciechanover A. 2011. Ubiquitination of E3 ligases: selfregulation of the ubiquitin system via proteolytic and non-proteolytic mechanisms. Cell Death Differ. 18:1393-1402. http://dx.doi.org/10.1038/cdd.2011.16.
17. Hoeller D, Hecker CM, Dikic I. 2006. Ubiquitin and ubiquitin-like proteins in cancer pathogenesis. Nat. Rev. Cancer 6:776-788. http://dx.doi.org/10.1038/nrc1994.
18. Kirkin V, Dikic I. 2007. Role of ubiquitin- and Ubl-binding proteins in cell signaling. Curr. Opin. Cell Biol. 19:199-205. http://dx.doi.org/10.1016/j.ceb.2007.02.002.
19. MacGurn JA, Hsu PC, Emr SD. 2012. Ubiquitin and membrane protein turnover: from cradle to grave. Annu. Rev. Biochem. 81:231-259. http://dx.doi.org/10.1146/annurev-biochem-060210-093619.
20. Marchese A, Trejo J. 2013. Ubiquitin-dependent regulation of G proteincoupled receptor trafficking and signaling. Cell. Signal. 25:707-716. http://dx.doi.org/10.1016/j.cellsig.2012.11.024.
21. Grabbe C, Husnjak K, Dikic I. 2011. The spatial and temporal organization of ubiquitin networks. Nat. Rev. Mol. Cell Biol. 12:295-307. http://dx.doi.org/10.1038/nrm3099.
22. Clark K, Nanda S, Cohen P. 2013. Molecular control of the NEMO family of ubiquitin-binding proteins. Nat. Rev. Mol. Cell Biol. 14:673-685. http://dx.doi.org/10.1038/nrm3644.
23. Pervin S, Tran A, Tran L, Urman R, Braga M, Chaudhuri G, Singh R. 2011. Reduced association of anti-apoptotic protein Mcl-1 with E3 ligase Mule increases the stability of Mcl-1 in breast cancer cells. Br. J. Cancer 105:428-437. http://dx.doi.org/10.1038/bjc.2011.242.
24. Shmueli A, Oren M. 2005. Life, death, and ubiquitin: taming the mule. Cell 121:963-965. http://dx.doi.org/10.1016/j.cell.2005.06.018.
25. Zhong Q, Gao W, Du F, Wang X. 2005. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121:1085-1095. http://dx.doi.org/10.1016/j.cell.2005.06.009.
26. Bernassola F, Karin M, Ciechanover A, Melino G. 2008. The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell 14:10-21. http://dx.doi.org/10.1016/j.ccr.2008.06.001.
27. Chen D, Brooks CL, Gu W. 2006. ARF-BP1 as a potential therapeutic target. Br. J. Cancer 94:1555-1558. http://dx.doi.org/10.1038/sj.bjc.6603119.
28. Confalonieri S, Quarto M, Goisis G, Nuciforo P, Donzelli M, Jodice G, Pelosi G, Viale G, Pece S, Di Fiore PP. 2009. Alterations of ubiquitin ligases in human cancer and their association with the natural history of the tumor. Oncogene 28:2959-2968. http://dx.doi.org/10.1038/onc.2009.156.
29. Adhikary S, Marinoni F, Hock A, Hulleman E, Popov N, Beier R, Bernard S, Quarto M, Capra M, Goettig S, Kogel U, Scheffner M, Helin K, Eilers M. 2005. The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell 123: 409-421. http://dx.doi.org/10.1016/j.cell.2005.08.016.
30. Zhang X, Berger FG, Yang J, Lu X. 2011. USP4 inhibits p53 through deubiquitinating and stabilizing ARF-BP1. EMBO J. 30:2177-2189. http://dx.doi.org/10.1038/emboj.2011.125.
31. Zhao X, Heng JI, Guardavaccaro D, Jiang R, Pagano M, Guillemot F, Iavarone A, Lasorella A. 2008. The HECT-domain ubiquitin ligase Huwe1 controls neural differentiation and proliferation by destabilizing the N-Myc oncoprotein. Nat. Cell Biol. 10:643-653. http://dx.doi.org/10.1038/ncb1727.
32. Nava C, Lamari F, Heron D, Mignot C, Rastetter A, Keren B, Cohen D, Faudet A, Bouteiller D, Gilleron M, Jacquette A, Whalen S, Afenjar A, Perisse D, Laurent C, Dupuits C, Gautier C, Gerard M, Huguet G, Caillet S, Leheup B, Leboyer M, Gillberg C, Delorme R, Bourgeron T, Brice A, Depienne C. 2012. Analysis of the chromosome X exome in patients with autism spectrum disorders identified novel candidate genes, including TMLHE. Transl. Psychiatry 2:e179. http://dx.doi.org/10.1038/tp.2012.102.
33. Froyen G, Corbett M, Vandewalle J, Jarvela I, Lawrence O, Meldrum C, Bauters M, Govaerts K, Vandeleur L, Van Esch H, Chelly J, Sanlaville D, van Bokhoven H, Ropers HH, Laumonnier F, Ranieri E, Schwartz CE, Abidi F, Tarpey PS, Futreal PA, Whibley A, Raymond FL, Stratton MR, Fryns JP, Scott R, Peippo M, Sipponen M, Partington M, Mowat D, Field M, Hackett A, Marynen P, Turner G, Gecz J. 2008. Submicroscopic duplications of the hydroxysteroid dehydrogenase HSD17B10 and the E3 ubiquitin ligase HUWE1 are associated with mental retardation. Am. J. Hum. Genet. 82:432-443. http://dx.doi.org/10.1016/j.ajhg.2007.11.002.
34. Galperin E, Sorkin A. 2005. Visualization of Rab5 activity in living cells using FRET microscopy. Methods Enzymol. 403:119-134. http://dx.doi.org/10.1016/S0076-6879(05)03011-9.
35. Galperin E, Sorkin A. 2008. Endosomal targeting of MEK2 requires RAF, MEK kinase activity and clathrin-dependent endocytosis. Traffic 9:1776- 1790. http://dx.doi.org/10.1111/j.1600-0854.2008.00788.x.
36. Hall JR, Kow E, Nevis KR, Lu CK, Luce KS, Zhong Q, Cook JG. 2007. Cdc6 stability is regulated by the Huwe1 ubiquitin ligase after DNA damage. Mol. Biol. Cell 18:3340-3350. http://dx.doi.org/10.1091/mbc.E07-02 -0173.
37. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3:1101-1108. http://dx.doi.org/10.1038/nprot.2008.73.
38. Sorkin A, Duex JE. 2010. Quantitative analysis of endocytosis and turnover of epidermal growth factor (EGF) and EGF receptor. Curr. Protoc. Cell Biol. Chapter 15:Unit 15.14. http://dx.doi.org/10.1002/0471143030.cb1514s46.
39. Jiang X, Sorkin A. 2003. Epidermal growth factor receptor internalization through clathrin-coated pits requires Cbl RING finger and proline-rich domains but not receptor polyubiquitylation. Traffic 4:529-543. http://dx.doi.org/10.1034/j.1600-0854.2003.t01-1-00109.x.
40. Cheng A, Zhang M, Gentry MS, Worby CA, Dixon JE, Saltiel AR. 2007. A role for AGL ubiquitination in the glycogen storage disorders of Lafora and Cori's disease. Genes Dev. 21:2399-2409. http://dx.doi.org/10.1101/gad.1553207.
41. Jeoung M, Abdelmoti L, Jang ER, Vander Kooi CW, Galperin E. 2013. Functional integration of the conserved domains of Shoc2 scaffold. PLoS One 8:e66067. http://dx.doi.org/10.1371/journal.pone.0066067.
42. Rodriguez-Viciana P, Oses-Prieto J, Burlingame A, Fried M, McCormick F. 2006. A phosphatase holoenzyme comprised of Shoc2/ Sur8 and the catalytic subunit of PP1 functions as an M-Ras effector to modulate Raf activity. Mol. Cell 22:217-230. http://dx.doi.org/10.1016/j.molcel.2006.03.027.
43. Jeoung M, Galperin E. 2014. Visualizing of signaling proteins on endosomes utilizing knockdown and reconstitution approach. Methods Enzymol. 534: 47-63. http://dx.doi.org/10.1016/B978-0-12-397926-1.00003-2.
44. Kurokawa M, Kim J, Geradts J, Matsuura K, Liu L, Ran X, Xia W, Ribar TJ, Henao R, Dewhirst MW, Kim WJ, Lucas JE, Wang S, Spector NL, Kornbluth S. 2013. A network of substrates of the E3 ubiquitin ligases MDM2 and HUWE1 control apoptosis independently of p53. Sci. Signal. 6:ra32. http://dx.doi.org/10.1126/scisignal.2003741.
45. Qi CF, Kim YS, Xiang S, Abdullaev Z, Torrey TA, Janz S, Kovalchuk AL, Sun J, Chen D, Cho WC, Gu W, Morse HC, III. 2012. Characterization of ARF-BP1/HUWE1 interactions with CTCF, MYC, ARF and p53 in MYC-driven B cell neoplasms. Int. J. Mol. Sci. 13:6204-6219. http://dx.doi.org/10.3390/ijms13056204.
46. Zhao X, Heng JI, Guardavaccaro D, Jiang R, Pagano M, Guillemot F, Iavarone A, Lasorella A. 2008. The HECT-domain ubiquitin ligase Huwe1 controls neural differentiation and proliferation by destabilizing the N-Myc oncoprotein. Nat. Cell Biol. 10:643-653. http://dx.doi.org/10.1038/ncb1727.
47. Dogan T, Harms GS, Hekman M, Karreman C, Oberoi TK, Alnemri ES, Rapp UR, Rajalingam K. 2008. X-linked and cellular IAPs modulate the stability of C-RAF kinase and cell motility. Nat. Cell Biol. 10:1447-1455. http://dx.doi.org/10.1038/ncb1804
48. Du J, Zeng J, Ou X, Ren X, Cai S. 2006. Methylglyoxal downregulates Raf-1 protein through a ubiquitination-mediated mechanism. Int. J. Biochem. Cell Biol. 38:1084-1091. http://dx.doi.org/10.1016/j.biocel.2005.10.019.
49. Noble C, Mercer K, Hussain J, Carragher L, Giblett S, Hayward R, Patterson C, Marais R, Pritchard CA. 2008. CRAF autophosphorylation of serine 621 is required to prevent its proteasome-mediated degradation. Mol. Cell 31:862-872. http://dx.doi.org/10.1016/j.molcel.2008.08.026.
50. Pandya RK, Partridge JR, Love KR, Schwartz TU, Ploegh HL. 2010. A structural element within the HUWE1 HECT domain modulates selfubiquitination and substrate ubiquitination activities. J. Biol. Chem. 285: 5664-5673. http://dx.doi.org/10.1074/jbc.M109.051805.
51. Hurley JH, Lee S, Prag G. 2006. Ubiquitin-binding domains. Biochem. J. 399:361-372. http://dx.doi.org/10.1042/BJ20061138.
52. Inoue S, Hao Z, Elia AJ, Cescon D, Zhou L, Silvester J, Snow B, Harris IS, Sasaki M, Li WY, Itsumi M, Yamamoto K, Ueda T, Dominguez-Brauer C, Gorrini C, Chio II, Haight J, You-Ten A, McCracken S, Wakeham A, Ghazarian D, Penn LJ, Melino G, Mak TW. 2013. Mule/ Huwe1/Arf-BP1 suppresses Ras-driven tumorigenesis by preventing c-Myc/Miz1-mediated down-regulation of p21 and p15. Genes Dev. 27: 1101-1114. http://dx.doi.org/10.1101/gad.214577.113.
53. Hurley JH, Stenmark H. 2011. Molecular mechanisms of ubiquitindependent membrane traffic. Annu. Rev. Biophys. 40:119-142. http://dx.doi.org/10.1146/annurev-biophys-042910-155404.
54. Nathan JA, Kim HT, Ting L, Gygi SP, Goldberg AL. 2013. Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes? EMBO J. 32:552-565. http://dx.doi.org/10.1038/emboj.2012.354.
55. Kirkpatrick DS, Denison C, Gygi SP. 2005. Weighing in on ubiquitin: the expanding role of mass-spectrometry-based proteomics. Nat. Cell Biol. 7:750-757. http://dx.doi.org/10.1038/ncb0805-750.
56. Denis NJ, Vasilescu J, Lambert JP, Smith JC, Figeys D. 2007. Tryptic digestion of ubiquitin standards reveals an improved strategy for identifying ubiquitinated proteins by mass spectrometry. Proteomics 7:868- 874. http://dx.doi.org/10.1002/pmic.200600410.
57. Papin C, Denouel-Galy A, Laugier D, Calothy G, Eychene A. 1998. Modulation of kinase activity and oncogenic properties by alternative splicing reveals a novel regulatory mechanism for B-Raf. J. Biol. Chem. 273:24939-24947. http://dx.doi.org/10.1074/jbc.273.38.24939.
58. Pumiglia KM, Decker SJ. 1997. Cell cycle arrest mediated by the MEK/ mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. U. S. A. 94:448-452. http://dx.doi.org/10.1073/pnas.94.2.448.
59. Sewing A, Wiseman B, Lloyd AC, Land H. 1997. High-intensity Raf signal causes cell cycle arrest mediated by p21Cip1. Mol. Cell. Biol. 17: 5588-5597.
60. Woods D, Parry D, Cherwinski H, Bosch E, Lees E, McMahon M. 1997. Raf-induced proliferation or cell cycle arrest is determined by the level of Raf activity with arrest mediated by p21Cip1. Mol. Cell. Biol. 17:5598- 5611.
61. Young LC, Hartig N, Munoz-Alegre M, Oses-Prieto JA, Durdu S, Bender S, Vijayakumar V, Vietri Rudan M, Gewinner C, Henderson S, Jathoul AP, Ghatrora R, Lythgoe MF, Burlingame AL, Rodriguez-Viciana P. 2013. An MRAS, SHOC2, and SCRIB complex coordinates ERK pathway activation with polarity and tumorigenic growth. Mol. Cell 52:679-692. http://dx.doi.org/10.1016/j.molcel.2013.10.004.
62. Yoon SY, Lee Y, Kim JH, Chung AS, Joo JH, Kim CN, Kim NS, Choe IS, Kim JW. 2005. Over-expression of human UREB1 in colorectal cancer: HECT domain of human UREB1 inhibits the activity of tumor suppressor p53 protein. Biochem. Biophys. Res. Commun. 326:7-17. http://dx.doi.org/10.1016/j.bbrc.2004.11.004.
63. Zhao X, D'Arca D, Lim WK, Brahmachary M, Carro MS, Ludwig T, Cardo CC, Guillemot F, Aldape K, Califano A, Iavarone A, Lasorella A. 2009. The N-Myc-DLL3 cascade is suppressed by the ubiquitin ligase Huwe1 to inhibit proliferation and promote neurogenesis in the developing brain. Dev. Cell 17:210-221. http://dx.doi.org/10.1016/j.devcel.2009.07.009.
64. de Groot RE, Ganji RS, Bernatik O, Lloyd-Lewis B, Seipel K, Sedova K, Zdrahal Z, Dhople VM, Dale TC, Korswagen HC, Bryja V. 2014. Huwe1-mediated ubiquitylation of dishevelled defines a negative feedback loop in the Wnt signaling pathway. Sci. Signal. 7:ra26. http://dx.doi.org/10.1126/scisignal.2004985.
65. Gripp KW, Zand DJ, Demmer L, Anderson CE, Dobyns WB, Zackai EH, Denenberg E, Jenny K, Stabley DL, Sol-Church K. 2013. Expanding the SHOC2 mutation associated phenotype of Noonan syndrome with loose anagen hair: structural brain anomalies and myelofibrosis. Am. J. Med. Genet. A 161:2420-2430. http://dx.doi.org/10.1002/ajmg.a.36098.
66. Hoban R, Roberts AE, Demmer L, Jethva R, Shephard B. 2012. Noonan syndrome due to a SHOC2 mutation presenting with fetal distress and fatal hypertrophic cardiomyopathy in a premature infant. Am. J. Med. Genet. A 158A:1411-1413. http://dx.doi.org/10.1002/ajmg.a.35318.