Compromised mutant EFEMP1 secretion associated with macular dystrophy remedied by proteostasis network alteration

Molecular Biology of the Cell

Volumn 22, Issue 24, 2011, Pages 4765-4775

  Hulleman, John D ^a   Kaushal, Shalesh ^b   Balch, William E ^a   Kelly, Jeffery W ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC AMINO ACID; EPIDERMAL GROWTH FACTOR CONTAINING FIBULIN LIKE EXTRACELLULAR MATRIX PROTEIN 1; FIBULIN; LUCIFERASE; MUTANT PROTEIN; SCLEROPROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CELL CULTURE; CELL GROWTH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; DISULFIDE BOND; FUSION GENE; GENE CONSTRUCT; GENE FUSION; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; LUMINESCENCE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEOSTASIS DEFICIENCY; RETINA MACULA DEGENERATION;

AMINO ACID SUBSTITUTION; DISULFIDES; EXTRACELLULAR MATRIX PROTEINS; HEK293 CELLS; HUMANS; MACULAR DEGENERATION; MUTATION, MISSENSE; PROTEIN FOLDING;

EID: 84055211699     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-08-0695     Document Type: Article

References (55)

1. Attebo K, Mitchell P, Smith W (1996). Visual acuity and the causes of visual loss in Australia. The Blue Mountains Eye Study. Ophthalmology 103, 357-364. (Pubitemid 26085889)
2. Baik JY, Lee MS, An SR, Yoon SK, Joo EJ, Kim YH, Park HW, Lee GM (2006). Initial transcriptome and proteome analyses of low culture temperature-induced expression in CHO cells producing erythropoietin. Biotechnol Bioeng 93, 361-371.
3. Balch WE, Morimoto RI, Dillin A, Kelly JW (2008). Adapting proteostasis for disease intervention. Science 319, 916-919. (Pubitemid 351263754)
4. Bressler NM, Bressler SB, Fine SL (1988). Age-related macular degeneration. Surv Ophthalmol 32, 375-413.
5. Bulaj G, Goldenberg DP (1999). Early events in the disulfide-coupled folding of BPTI. Protein Sci 8, 1825-1842. (Pubitemid 29430483)
6. Chang JY, Li L, Lai PH (2001). A major kinetic trap for the oxidative folding of human epidermal growth factor. J Biol Chem 276, 4845-4852.
7. Chang JY, Schindler P, Ramseier U, Lai PH (1995). The disulfide folding pathway of human epidermal growth factor. J Biol Chem 270, 9207-9216.
8. Cohen E et al. (2009). Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell 139, 1157-1169.
9. Crimmins DL, Mische SM, Denslow ND (2005). Chemical cleavage of proteins in solution. Curr Protoc Protein Sci Chapter 11, Unit 11.14.
10. de Jong PT (2006). Age-related macular degeneration. N Engl J Med 355, 1474-1485.
11. Denning GM, Anderson MP, Amara JF, Marshall J, Smith AE, Welsh MJ (1992). Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358, 761-764.
12. Evans CG, Chang L, Gestwicki JE (2010). Heat shock protein 70 (hsp70) as an emerging drug target. J Med Chem 53, 4585-4602.
13. Ferre F, Clote P (2005). DiANNA: a web server for disulfide connectivity prediction. Nucleic Acids Res 33, W230-W232. (Pubitemid 44529914)
14. Fomenko DE, Gladyshev VN (2002). CxxS: fold-independent redox motif revealed by genome-wide searches for thiol/disulfide oxidoreductase function. Protein Sci 11, 2285-2296.
15. Fomenko DE, Gladyshev VN (2003). Identity and functions of CxxC-derived motifs. Biochemistry 42, 11214-11225. (Pubitemid 37158888)
16. Fu L, Garland D, Yang Z, Shukla D, Rajendran A, Pearson E, Stone EM, Zhang K, Pierce EA (2007). The R345W mutation in EFEMP1 is pathogenic and causes AMD-like deposits in mice. Hum Mol Genet 16, 2411-2422. (Pubitemid 47500628)
17. Fujita J (1999). Cold shock response in mammalian cells. J Mol Microbiol Biotechnol 1, 243-255.
18. Hutt DM et al. (2010). Reduced histone deacetylase 7 activity restores function to misfolded CFTR in cystic fibrosis. Nat Chem Biol 6, 25-33.
19. Jager RD, Mieler WF, Miller JW (2008). Age-related macular degeneration. N Engl J Med 358, 2606-2617.
20. Jessop CE, Chakravarthi S, Garbi N, Hammerling GJ, Lovell S, Bulleid NJ (2007). ERp57 is essential for efficient folding of glycoproteins sharing common structural domains. EMBO J 26, 28-40. (Pubitemid 46094697)
21. Kostka G, Giltay R, Bloch W, Addicks K, Timpl R, Fassler R, Chu ML (2001). Perinatal lethality and endothelial cell abnormalities in several vessel compartments of fibulin-1-deficient mice. Mol Cell Biol 21, 7025-7034. (Pubitemid 32911262)
22. Kulka RG, Raboy B, Schuster R, Parag HA, Diamond G, Ciechanover A, Marcus M (1988). A Chinese hamster cell cycle mutant arrested at G2 phase has a temperature-sensitive ubiquitin-activating enzyme, E1. J Biol Chem 263, 15726-15731.
23. Kundzewicz A, Munier F, Matter JM (2008). Expression and cell compartmentalization of EFEMP1, a protein associated with malattia leventinese. Adv Exp Med Biol 613, 277-281.
24. Marmorstein L (2004). Association of EFEMP1 with malattia leventinese and age-related macular degeneration: a mini-review. Ophthalmic Genet 25, 219-226.
25. Marmorstein LY, McLaughlin PJ, Peachey NS, Sasaki T, Marmorstein AD (2007). Formation and progression of sub-retinal pigment epithelium deposits in Efemp1 mutation knock-in mice: a model for the early pathogenic course of macular degeneration. Hum Mol Genet 16, 2423-2432. (Pubitemid 47500629)
26. Marmorstein LY, Munier FL, Arsenijevic Y, Schorderet DF, McLaughlin PJ, Chung D, Traboulsi E, Marmorstein AD (2002). Aberrant accumulation of EFEMP1 underlies drusen formation in malattia leventinese and age-related macular degeneration. Proc Natl Acad Sci USA 99, 13067-13072.
27. McCracken AA, Werner ED, Brodsky JL (1998). Endoplasmic reticulum-associated protein degradation: an unconventional route to a familiar fate. Adv Mol Cell Biol 27, 165-200.
28. McLaughlin PJ, Bakall B, Choi J, Liu Z, Sasaki T, Davis EC, Marmorstein AD, Marmorstein LY (2007). Lack of fibulin-3 causes early aging and herniation, but not macular degeneration in mice. Hum Mol Genet 16, 3059-3070. (Pubitemid 350131324)
29. McLaughlin PJ et al. (2006). Targeted disruption of fibulin-4 abolishes elastogenesis and causes perinatal lethality in mice. Mol Cell Biol 26, 1700-1709.
30. Michalovitz D, Halevy O, Oren M (1990). Conditional inhibition of transformation and of cell proliferation by a temperature-sensitive mutant of p53. Cell 62, 671-680.
31. Mu TW, Ong DS, Wang YJ, Balch WE, Yates JR 3rd, Segatori L, Kelly JW (2008). Chemical and biological approaches synergize to ameliorate protein-folding diseases. Cell 134, 769-781.
32. Mullins RF, Olvera MA, Clark AF, Stone EM (2007). Fibulin-5 distribution in human eyes: relevance to age-related macular degeneration. Exp Eye Res 84, 378-380. (Pubitemid 44958467)
33. Piguet B, Haimovici R, Bird AC (1995). Dominantly inherited drusen represent more than one disorder: a historical review. Eye 9, 34-41.
34. Ringer AL, Senenko A, Sherrill CD (2007). Models of S/pi interactions in protein structures: comparison of the H2S benzene complex with PDB data. Protein Sci 16, 2216-2223. (Pubitemid 47481656)
35. Ron D, Walter P (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nature Rev 8, 519-529. (Pubitemid 46985379)
36. Roybal CN, Marmorstein LY, Vander Jagt DL, Abcouwer SF (2005). Aberrant accumulation of fibulin-3 in the endoplasmic reticulum leads to activation of the unfolded protein response and VEGF expression. Invest Ophthalmol Vis Sci 46, 3973-3979. (Pubitemid 44264595)
37. Schultz DW et al. (2003). Analysis of the ARMD1 locus: evidence that a mutation in HEMICENTIN-1 is associated with age-related macular degeneration in a large family. Hum Mol Genet 12, 3315-3323. (Pubitemid 37541077)
38. Sevier CS, Kaiser CA (2002). Formation and transfer of disulphide bonds in living cells. Nat Rev Mol Cell Biol 3, 836-847. (Pubitemid 35285274)
39. Sevier CS, Qu H, Heldman N, Gross E, Fass D, Kaiser CA (2007). Modulation of cellular disulfide-bond formation and the ER redox environment by feedback regulation of Ero1. Cell 129, 333-344. (Pubitemid 46574965)
40. Siegel MR, Sisler HD (1963). Inhibition of protein synthesis in vitro by cycloheximide. Nature 200, 675-676.
41. Sifers RN (2010). Manipulating proteostasis. Nat Chem Biol 6, 400-401.
42. Stone EM et al. (1999). A single EFEMP1 mutation associated with both malattia leventinese and Doyne honeycomb retinal dystrophy. Nat Genet 22, 199-202. (Pubitemid 29264819)
43. Stone EM, Sheffield VC, Hageman GS (2001). Molecular genetics of age-related macular degeneration. Hum Mol Genet 10, 2285-2292. (Pubitemid 32998843)
44. Tabas I, Ron D (2011). Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 13, 184-190.
45. Tannous BA, Kim DE, Fernandez JL, Weissleder R, Breakefield XO (2005). Codon-optimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. Mol Ther 11, 435-443. (Pubitemid 40277320)
46. Tielsch JM, Javitt JC, Coleman A, Katz J, Sommer A (1995). The prevalence of blindness and visual impairment among nursing home residents in Baltimore. N Engl J Med 332, 1205-1209.
47. Timpl R, Sasaki T, Kostka G, Chu ML (2003). Fibulins: a versatile family of extracellular matrix proteins. Nature Rev 4, 479-489. (Pubitemid 36648593)
48. Underhill MF, Smales CM (2007). The cold-shock response in mammalian cells: investigating the HeLa cell cold-shock proteome. Cytotechnology 53, 47-53. (Pubitemid 46944868)
49. Usui K, Hulleman JD, Paulsson JF, Siegel SJ, Powers ET, Kelly JW (2009). Site-specific modification of Alzheimer's peptides by cholesterol oxidation products enhances aggregation energetics and neurotoxicity. Proc Natl Acad Sci USA 106, 18563-18568.
50. Waldo GS, Standish BM, Berendzen J, Terwilliger TC (1999). Rapid protein-folding assay using green fluorescent protein. Nat Biotechnol 17, 691-695. (Pubitemid 29316148)
51. Wang X, Koulov AV, Kellner WA, Riordan JR, Balch WE (2008). Chemical and biological folding contribute to temperature-sensitive DeltaF508 CFTR trafficking. Traffic 9, 1878-1893.
52. Werner ED, Brodsky JL, McCracken AA (1996). Proteasome-dependent endoplasmic reticulum-associated protein degradation: an unconventional route to a familiar fate. Proc Natl Acad Sci USA 93, 13797-13801. (Pubitemid 26424200)
53. Williamson MP (1994). The structure and function of proline-rich regions in proteins. Biochem J 297, 249-260.
54. Young RW (1987). Pathophysiology of age-related macular degeneration. Surv Ophthalmol 31, 291-306.
55. Zhang Y, Marmorstein LY (2009). Focus on molecules: fibulin-3 (EFEMP1). Exp Eye Res 90, 374-375.