Retroviral rem protein requires processing by signal peptidase and retrotranslocation for nuclear function

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 27, 2010, Pages 12287-12292

  Byun, Hyewon ^a   Halani, Nimita ^a   Mertz, Jennifer A ^a,b   Ali, Almas F ^a   Lozano, Mary M ^a   Dudley, Jaquelin P ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b Department of Structural Biology   (United States)

Author keywords

ERAD; Mouse mammary tumor virus; Retrotranslocation; Retrovirus; Signal peptide

Indexed keywords

ADENOSINE TRIPHOSPHATASE; COMPLEMENTARY DNA; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; PEPTIDASE; PROTEASOME; PROTEASOME INHIBITOR; PROTEIN REM; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; REPORTER GENE; VIRUS INFECTION; VIRUS MUTATION; WILD TYPE;

ACTIVE TRANSPORT, CELL NUCLEUS; ALTERNATIVE SPLICING; ANIMALS; BINDING SITES; BLOTTING, WESTERN; CELL LINE; CELL NUCLEUS; GLYCOSYLATION; GREEN FLUORESCENT PROTEINS; HUMANS; JURKAT CELLS; MAMMARY TUMOR VIRUS, MOUSE; MEMBRANE PROTEINS; MICE; MICROSCOPY, FLUORESCENCE; MUTATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SORTING SIGNALS; SERINE ENDOPEPTIDASES; VIRAL ENVELOPE PROTEINS;

MOUSE MAMMARY TUMOR VIRUS; MURINAE;

EID: 77955457544     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1004303107     Document Type: Article

References (29)

1. Mertz JA, Simper MS, Lozano MM, Payne SM, Dudley JP (2005) Mouse mammary tumor virus encodes a self-regulatory RNA export protein and is a complex retrovirus. J Virol 79:14737-14747.
2. Indik S, Günzburg WH, Salmons B, Rouault F (2005) A novel, mouse mammary tumor virus encoded protein with Rev-like properties. Virology 337:1-6. (Pubitemid 40725435)
3. Stauber R, Gaitanaris GA, Pavlakis GN (1995) Analysis of trafficking of Rev and transdominant Rev proteins in living cells using green fluorescent protein fusions: Transdominant Rev blocks the export of Rev from the nucleus to the cytoplasm. Virology 213:439-449.
4. Heger P, Rosorius O, Hauber J, Stauber RH (1999) Titration of cellular export factors, but not heteromultimerization, is the molecular mechanism of trans-dominant HTLV-1 rex mutants. Oncogene 18:4080-4090.
5. Mertz JA, Lozano MM, Dudley JP (2009) Rev and Rex proteins of human complex retroviruses function with the MMTV Rem-responsive element. Retrovirology 6:10-22.
6. Mertz JA, Chadee AB, Byun H, Russell R, Dudley JP (2009) Mapping of the functional boundaries and secondary structure of the mouse mammary tumor virus Remresponsive element. J Biol Chem 284:25642-25652.
7. Dultz E, et al. (2008) The signal peptide of the mouse mammary tumor virus Rem protein is released from the endoplasmic reticulum membrane and accumulates in nucleoli. J Biol Chem 283:9966-9976.
8. Johnson AE, Haigh NG (2000) The ER translocon and retrotranslocation: Is the shift into reverse manual or automatic? Cell 102:709-712.
9. Nakatsukasa K, Brodsky JL (2008) The recognition and retrotranslocation of misfolded proteins from the endoplasmic reticulum. Traffic 9:861-870.
10. Wolfe MS (2009) Intramembrane-cleaving proteases. J Biol Chem 284:13969-13973.
11. Hoch-Marchaim H, Hasson T, Rorman E, Cohen S, Hochman J (1998) Nucleolar localization of mouse mammary tumor virus proteins in T-cell lymphomas. Virology 242:246-254.
12. Hoch-Marchaim H, et al. (2003) The leader peptide of MMTV Env precursor localizes to the nucleoli in MMTV-derived T cell lymphomas and interacts with nucleolar protein B23. Virology 313:22-32.
13. Shackleford GM, Varmus HE (1988) Construction of a clonable, infectious, and tumorigenic mouse mammary tumor virus provirus and a derivative genetic vector. Proc Natl Acad Sci USA 85:9655-9659.
14. Caporale M, et al. (2009) The signal peptide of a simple retrovirus envelope functions as a posttranscriptional regulator of viral gene expression. J Virol 83:4591-4604.
15. Hofacre A, Nitta T, Fan H (2009) Jaagsiekte sheep retrovirus encodes a regulatory factor, Rej, required for synthesis of Gag protein. J Virol 83:12483-12498.
16. Hosokawa N, et al. (2008) Human XTP3-B forms an endoplasmic reticulum quality control scaffold with the HRD1-SEL1L ubiquitin ligase complex and BiP. J Biol Chem 283:20914-20924.
17. Halawani D, Latterich M (2006) p97: The cell's molecular purgatory? Mol Cell 22: 713-717.
18. Ye Y, Meyer HH, Rapoport TA (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414:652-656.
19. Paetzel M, Karla A, Strynadka NC, Dalbey RE (2002) Signal peptidases. Chem Rev 102: 4549-4580.
20. Golde TE, Wolfe MS, Greenbaum DC (2009) Signal peptide peptidases: A family of intramembrane-cleaving proteases that cleave type 2 transmembrane proteins. Semin Cell Dev Biol 20:225-230.
21. Hirayama H, Seino J, Kitajima T, Jigami Y, Suzuki T (2010) Free oligosaccharides to monitor glycoprotein endoplasmic reticulum-associated degradation in Saccharomyces cerevisiae. J Biol Chem 285:12390-12404.
22. Carlson EJ, Pitonzo D, Skach WR (2006) p97 functions as an auxiliary factor to facilitate TM domain extraction during CFTR ER-associated degradation. EMBO J 25: 4557-4566.
23. Magin C, Hesse J, Löwer J, Löwer R (2000) Corf, the Rev/Rex homologue of HTDV/ HERV-K, encodes an arginine-rich nuclear localization signal that exerts a transdominant phenotype when mutated. Virology 274:11-16.
24. Cullen BR (2002) Using retroviruses to study the nuclear export of mRNA. Results Probl Cell Differ 35:151-168.
25. Targett-Adams P, Hope G, Boulant S, McLauchlan J (2008) Maturation of hepatitis C virus core protein by signal peptide peptidase is required for virus production. J Biol Chem 283:16850-16859.
26. Vij N (2008) AAA ATPase p97/VCP: Cellular functions, disease and therapeutic potential. J Cell Mol Med 12 (6A):2511-2518.
27. Ringold GM, Yamamoto KR, Tomkins GM, Bishop M, Varmus HE (1975) Dexamethasone-mediated induction of mouse mammary tumor virus RNA: A system for studying glucocorticoid action. Cell 6:299-305.
28. Katz E, et al. (2005) MMTV Env encodes an ITAM responsible for transformation of mammary epithelial cells in three-dimensional culture. J Exp Med 201:431-439.
29. Bramblett D, et al. (1995) A redundant nuclear protein binding site contributes to negative regulation of the mouse mammary tumor virus long terminal repeat. J Virol 69:7868-7876.