A role for N-myristoylation in protein targeting: NADH-cytochrome b5 reductase requires myristic acid for association with outer mitochondrial but not ER membranes

Journal of Cell Biology

Volumn 135, Issue 6, 1996, Pages 1501-1513

  Borgese, Nica ^a,b,d   Aggujaro, Diego ^a   Carrera, Paola ^c   Pietrini, Grazia ^a   Bassetti, Monique ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY MEDITERRANEA OF REGGIO CALABRIA   (Italy)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME B5 REDUCTASE;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; MITOCHONDRIAL MEMBRANE; MYRISTYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CELL FRACTIONATION; CELL LINE; CYTOCHROME REDUCTASES; CYTOCHROME-B(5) REDUCTASE; CYTOCHROMES B5; ENDOPLASMIC RETICULUM; FLUORESCENT ANTIBODY TECHNIQUE; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MICROSCOPY, IMMUNOELECTRON; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTATION; MYRISTIC ACID; MYRISTIC ACIDS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; TRANSFECTION;

ANIMALIA; MAMMALIA;

EID: 0030469993     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.6.1501     Document Type: Article

References (72)

1. 2-terminal blocking group of calcineurin B as myristic acid. FEBS Lett. 150:314-318.
2. Ames, J.B., T. Porumb, T. Tanaka, M. Ikura, and L. Stryer. 1995. Amino-terminal myristoylation induces cooperative calcium binding to recoverin. J. Biol. Chem. 270:4526-4533.
3. Andrews, D.W., L. Lauffer, P. Walter, and V.R. Lingappa. 1989. Evidence for a two-step mechanism involved in assembly of functional signal recognition particle receptor. J. Cell Biol. 108:797-810.
4. Ausubel, P.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1987. Current Protocols in Molecular Biology. John Wiley and Sons, Inc.
5. Bassetti, M., D. Lodi Pasini, and P. Rosa. 1995. Degradation of gonadotropin β-subunits retained in the endoplasmic reticulum of the gonadotropes of castrated rats. Endocrinology. 136:1168-1176.
6. Bonner, W.M., and R.A. Laskey. 1974. A film detection method for tritiumlabelled proteins and nucleic acids in polyacrylamide gels. Eur. J. Biochem. 46:83-88.
7. Bordier, C. 1981. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256:1604-1607.
8. 5 reductase, an integral membrane protein. FEBS Lett. 112:216-220.
9. 5 reductase contain covalently bound myristic acid. Quantitative analysis on the polyvinylidene difluoride-immobilized proteins. Biochem. J. 266:341-347.
10. 5 reductase in rat liver cells, studied with a quantitative radioimmunoblotting assay. Biochem. J. 239:393-403.
11. 5 reductase, an integral membrane protein, in rat liver cells. III. Evidence for the independent insertion and turnover of the enzyme in various subcellular compartments. J. Cell Biol. 86:38-45.
12. 5: the problem of postranslational targeting to the endoplasmic reticulum. In Subcellular Biochemistry. Vol. 21. N. Borgese and J.R. Harris, editors. Plenum Press, New York. 313-341.
13. Brewer, C.B., and M.G. Roth. 1991. A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J. Cell Biol. 114:413-421.
14. Busconi, L., and T. Michel. 1993. Endothelial nitric oxide synthase. N-terminal myristoylation determines subcellular localization. J. Biol. Chem. 268:8410-8413.
15. Cao, W., and M.G. Douglas. 1995. Biogenesis of ISP6, a small carboxyl-terminal anchored protein of the receptor complex of the mitochondrial outer membrane. J. Biol. Chem. 270:5674-5679.
16. 2-terminal blocking group of the catalytic subunit of cyclic AMP-dependent protein kinase from bovine cardiac muscle. Proc. Natl. Acad. Sci. USA. 79:6128-6131.
17. Casey, P.J. 1995. Protein lipidation in cell signaling. Science (Wash. DC). 268: 221-225.
18. Cham, B.E., and B.R. Knowles. 1976. A solvent system for delipidation of plasma or serum without protein precipitation. J. Lipid Res. 17:176-181.
19. Chow, M., J.F.E. Newman, D. Filman, J.M. Hogle, D.J. Rowlands, and F. Brown. 1987. Myristoylation of picornavirus capsid protein VP4 and its structural significance. Nature (Lond.). 327:482-486.
20. Cross, F.R., E.A. Garber, D. Pellman, and H. Hanafusa. 1984. A short sequence in the p60src N terminus is required for p60src myristoylation and membrane association and for cell transformation. Mol. Cell. Biol. 4:1834-1842.
21. D'Souza-Schorey, C., and P.D. Stahl. 1995. Myristoylation is required for the intracellular localization and endocytic function of ARF6. Exp. Cell Res. 221:153-159.
22. 5 is contained within the carboxyl-terminal region. FEBS Lett. 370:69-74.
23. 2+ levels. J. Biol. Chem. 270:1337-1341.
24. Graff, J.M., J.I. Gordon, and P.J. Blackshear. 1989. Myristoylated and non-myristoylated forms of a protein are phosphorylated by protein kinase C. Science (Wash. DC). 1989:503-506.
25. Graham, F.L., and A.J. Van der Eb. 1973. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 52:456-467.
26. Hachiya, N., R. Alam, Y. Sakasegawa, K. Mihara, and T. Omura. 1993. A mito chondrial import factor purified from rat liver cytosol is an ATP-dependent conformational modulator for precursor proteins. EMBO (Eur. Mol. Biol. Organ.) J. 12:1579-1586.
27. 5 reductase to two different submitochondrial compartments. Cell. 79:829-839.
28. Harris, M.P.G., and J.C. Neil. 1994. Myristoylation-dependent binding of HIV-1 Nef to CD4. J. Mol. Biol. 241:136-142.
29. Haucke, V., T. Lithgow, S. Rospert, K. Hahne, and G. Schatz. 1995. The yeast mitochondrial protein import receptor Mas20p binds precursor proteins through electrostatic interaction with the positively charged presequence. J. Biol. Chem. 270:5565-5570.
30. Hurt, E.C., U. Müller, and G. Schatz. 1985. The first twelve amino acids of a yeast mitochondrial outer membrane protein can direct a nuclear-coded cytochrome oxidase subunit to the mitochondrial inner membrane. EMBO (Eur. Mol. Biol. Organ.) J. 4:3509-3518.
31. Johnson, D.R., R.S. Bhatnager, L.J. Knoll, and J.I. Gordon. 1994. Genetic and biochemical studies of protein N-myristoylation. Annu. Rev. Biochem. 63: 869-914.
32. Jones, T.L.Z., W.F. Simonds, J.J. Merendino, M.R. Brann, and A.M. Spiegel. 1990. Myristoylation of an inhibitory GTP-binding protein a subunit is essential for its membrane attachment. Proc. Nutl. Acad. Sci. USA. 87:568-572.
33. Katsube, T., N. Sakamoto, Y. Kobayashi, R. Seki, M. Hirano, K. Tanishima, A. Tomoda, E. Takazakura, T. Yubisui, M. Takeshita et al. 1991. Am. J. Hum. Genet. 48:799-808.
34. 5 reductase. Determination of the depth of trp-16 in the bilayer. J. Biol. Chem. 261:7316-7321.
35. Kiebler, M., K. Becker, N. Pfanner, and W. Neupert. 1993. Mitochondrial protein import: specific recognition and membrane translocation of preproteins. J. Membr. Biol. 135:191-207.
36. Kutay, U., E. Hartmann, and T.A. Rapoport. 1993. A class of membrane proteins with C-terminal anchor. Trends Cell Biol. 3:72-75.
37. Kutay, U., G. Ahnert-Hilgen, E. Hartmann, B. Wiedenmann, and T.A. Rapoport. 1995. Transport route for synaptobrevin via a novel pathway of insertion into the endoplasmic reticulum membrane. EMBO (Eur. Mol. Biol. Organ.) J. 14:224-231.
38. oα increases its affinity for βγ. J. Biol. Chem. 266:4654-4659.
39. Louvard, D., H. Reggio, and G. Warren. 1982. Antibodies to the Golgi complex and the rough endoplasmic reticulum. J. Cell Biol. 92:92-107.
40. Lowry, O.H., N.J. Rosebrough, A.L. Farr, and R.J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
41. McBride, H.M., D.G. Millar, J.-M. Li, and G.C. Shore. 1992. A signal-anchor sequence selective for the mitochondrial outer membrane. J. Cell Biol. 119: 1451-1456.
42. McLaughlin, S., and A. Aderem. 1995. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20:272-276.
43. 5 reductase, an integral membrane protein, in rat liver cells. II. Evidence that a single enzyme accounts for the activity in its various subcellular locations. J. Cell Biol. 85:516-526.
44. Mitoma, J.-Y., and A. Ito. 1992. Mitochondrial targeting signal of rat liver monoamine oxidase B is located at its carboxy terminus. J. Biochem. 111:20-24.
45. Mumby, S.M., R.O. Heukeroth, J.I. Gordon, and A.G. Gilman 1990. G-protein α-subunit expression, myristoylation, and membrane association in COS cells. Proc. Natl. Acad. Sci. USA. 87:728-732.
46. Murakami, K., S. Tanase, Y. Morino, and M. Mori. 1992. Presequence binding factor-dependent and -independent import of proteins into mitochondria. J. Biol. Chem. 267:13119-13122.
47. Nguyen, M., D.G. Millar, V.W. Yong, S.J. Korsmeyer, and G.C. Shore. 1993. Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence. J. Biol. Chem 268:25265-25268.
48. Nicchitta, C.V., G. Migliaccio, and G. Blobel. 1991. Biochemical fractionation and assembly of the membrane components that mediate nascent chain targeting and translocation. Cell. 65:587-598.
49. Olmsted, J.B. 1981. Affinity purification of antibodies from diazotized paper blots of heterogeneous protein samples. J. Biol. Chem. 256:11955-11957.
50. 5 reductase as myristic acid and the complete amino acid sequence of the membrane-binding domain. J. Biol. Chem. 259:13349-13354.
51. Parker, B.A., and G.R. Stark. 1979. Regulation of simian virus 40 transcription: sensitive analysis of the RNA species present early in infections by virus or viral DNA. J. Virol. 31:360-369.
52. Peitzsch, R.M., and S. McLaughlin. 1993. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins. Biochemistry. 32:10436-10443.
53. 5 reductase. Proc. Natl. Acad. Sci. USA. 85:7246-7250.
54. 5 reductase. J. Cell Biol. 117:975-986.
55. Randazzo, P.A., T. Terui, S. Sturch, H.M. Fales, A.C. Ferrige, and R.A. Kahn. 1995. The myristylated amino terminus of ADP-ribosylation factor 1 is a phospholipid-and GTP-sensitive switch. J. Biol. Chem. 270:14809-14815.
56. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 545 pp.
57. 5 reductase gene results in hereditary methemoglobinemia type II (generalized type). A functional implication for the role of the COOH-terminal region of the enzyme. J. Biol. Chem. 269:5952-5957.
58. 5 gene results in immunologically undetectable enzyme and impaired NADH-dependent ascorbate regeneration in cultured fibroblasts of a patient with type II hereditary methemoglobinemia. Am. J. Hum. Genet. 57:302-310.
59. Shore, G.C., H.M. McBride, D.G. Millar, N.A.E. Steenaart, and M. Nguyen. 1995. Import and insertion of proteins into the mitochondrial outer membrane. Eur. J. Biochem. 227:9-18.
60. Sigal, C.T., W. Zhou, C.A. Buser, S. McLaughlin, and M.D. Resh. 1994. Aminoterminal basic residues of Src mediate membrane binding through electrostatic interaction with acidic phospholipids. Proc. Natl Acad. Sci. USA. 91: 12253-12257.
61. Sottocasa, G.L., B. Kuylenstierna, L. Ernster, and A. Bergstrand. 1967. An electron transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study. J. Cell Biol. 32:415-438.
62. 5-dimyristoylphosphatidylcholine vesicles. J. Biol. Chem. 268:23168-23171.
63. Tanaka, T., J.B. Ames, T.S. Harvey, L. Stryer, and M. Ikura. 1995. Sequestration of the membrane-targeting myristoyl group of recoverin in the calcium-free state. Nature (Lond.). 376:444-447.
64. Taniguchi, H., and S. Manenti. 1993. Interaction of myristoylated alanine-rich protein kinase C substrate (MARCKS) with membrane phospholipids. J. Biol. Chem. 268:9960-9963.
65. Vaitukaitis, J.L. 1981. Production of antisera with small doses of immunogen: multiple intradermal injections. Methods Enzymol. 73:46-52.
66. 5 spans the bilayer of the endoplasmic reticulum. J. Biol. Chem. 270:3414-3422.
67. Walter, P., and A.E. Johnson. 1994. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol. 10: 87-120.
68. Yonemoto, W., M.L. McGlone, and S.S. Taylor. 1993. N-myristoylation of the catalytic subunit of cAMP-dependent protein kinase conveys structural stability. J. Biol. Chem. 268:2348-2352.
69. 1 complex and the reconstitution of succinate-cytochrome c reductase. J. Biol. Chem. 249:4905-4910.
70. Yu, G., and R.L. Felsted. 1992. Effect of myristoylation on p27 nef subcellular distribution and suppression of HIV-LTR transcription. Virology. 187:46-55.
71. Zhu, D., M.E. Cardenas, and J. Heitman. 1995. Myristoylation of calcineurin B is not required for function or interaction with immunophilin-immunosuppressant complexes in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 270:24831-24838.
72. Zozulya, S., and L. Stryer. 1992. Calcium-myristoyl protein switch. Proc. Natl. Acad. Sci. USA. 89:11569-11573.