A Single Mammalian Mitochondrial Translation Initiation Factor Functionally Replaces Two Bacterial Factors

Molecular Cell

Volumn 29, Issue 2, 2008, Pages 180-190

  Gaur, Rahul ^a   Grasso, Domenick ^b   Datta, Partha P ^c   Krishna, P D V ^a   Das, Gautam ^a   Spencer, Angela ^b   Agrawal, Rajendra K ^c,d   Spremulli, Linda ^b   Varshney, Umesh ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b University of North Carolina at Chapel Hill   (United States)

^c WADSWORTH CENTER   (United States)

^d STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

DNA

Indexed keywords

INITIATION FACTOR 1; INITIATION FACTOR 2;

ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; ESCHERICHIA COLI; GENE DELETION; GENE FUNCTION; GENE INSERTION; NONHUMAN; PROTEIN FUNCTION;

ANIMALS; CATTLE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EUKARYOTIC INITIATION FACTORS; GENE DELETION; GENETIC COMPLEMENTATION TEST; MITOCHONDRIAL PROTEINS; MODELS, MOLECULAR; PROKARYOTIC INITIATION FACTOR-1; PROKARYOTIC INITIATION FACTOR-2; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); BOVINAE; MAMMALIA;

EID: 38649115355     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.11.021     Document Type: Article

References (54)

1. Allen G.S., and Frank J. Structural insights on the translation initiation complex: ghosts of a universal initiation complex. Mol. Microbiol. 63 (2007) 941-950
2. Allen G.S., Zavialov A., Gursky R., Ehrenberg M., and Frank J. The cryo-EM structure of a translation initiation complex from Escherichia coli. Cell 121 (2005) 703-712
3. Antoun A., Pavlov M.Y., Andersson K., Tenson T., and Ehrenberg M. The roles of initiation factor 2 and guanosine triphosphate in initiation of protein synthesis. EMBO J. 22 (2003) 5593-5601
4. Antoun A., Pavlov M.Y., Lovmar M., and Ehrenberg M. How initiation factors tune the rate of initiation of protein synthesis in bacteria. EMBO J. 25 (2006) 2539-2550
5. Antoun A., Pavlov M.Y., Lovmar M., and Ehrenberg M. How initiation factors maximize the accuracy of tRNA selection in initiation of bacterial protein synthesis. Mol. Cell 23 (2006) 183-193
6. Boelens R., and Gualerzi C.O. Structure and function of bacterial initiation factors. Curr. Protein Pept. Sci. 3 (2002) 107-119
7. Boileau G., Butler P., Hershey J.W., and Traut R.R. Direct cross-links between initiation factors 1, 2, and 3 and ribosomal proteins promoted by 2-iminothiolane. Biochemistry 22 (1983) 3162-3170
8. Brock S., Szkaradkiewicz K., and Sprinzl M. Initiation factors of protein biosynthesis in bacteria and their structural relationship to elongation and termination factors. Mol. Microbiol. 29 (1998) 409-417
9. Carter A.P., Clemons Jr. W.M., Brodersen D.E., Morgan-Warren R.J., Hartsch T., Wimberly B.T., and Ramakrishnan V. Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science 291 (2001) 498-501
10. iMet binding to ribosomes by yIF2, a bacterial IF2 homolog in yeast. Science 280 (1998) 1757-1760
11. Choi S.K., Olsen D.S., Roll-Mecak A., Martung A., Remo K.L., Burley S.K., Hinnebusch A.G., and Dever T.E. Physical and functional interaction between the eukaryotic orthologs of prokaryotic translation initiation factors IF1 and IF2. Mol. Cell. Biol. 20 (2000) 7183-7191
12. Croitoru V., Bucheli-Witschel M., Hagg P., Abdulkarim F., and Isaksson L.A. Generation and characterization of functional mutants in the translation initiation factor IF1 of Escherichia coli. Eur. J. Biochem. 271 (2004) 534-544
13. Cummings H.S., and Hershey J.W. Translation initiation factor IF1 is essential for cell viability in Escherichia coli. J. Bacteriol. 176 (1994) 198-205
14. Datsenko K.A., and Wanner B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97 (2000) 6640-6645
15. Dekker P.J., Papadopoulou B., and Grivell L.A. In-vitro translation of mitochondrial mRNAs by yeast mitochondrial ribosomes is hampered by the lack of start-codon recognition. Curr. Genet. 23 (1993) 22-27
16. Garofalo C., Trinko R., Kramer G., Appling D.R., and Hardesty B. Purification and characterization of yeast mitochondrial initiation factor 2. Arch. Biochem. Biophys. 413 (2003) 243-252
17. Giuliodori A.M., Brandi A., Gualerzi C.O., and Pon C.L. Preferential translation of cold-shock mRNAs during cold adaptation. RNA 10 (2004) 265-276
18. Grasso D.G., Christian B.E., Spencer A.C., and Spremulli L.L. Overexpression and purification of mammalian mitochondrial translational initiation factor 2 and initiation factor 3. Methods Enzymol. 430 (2007) 59-78
19. Gray M.W., Burger G., and Lang B.F. Mitochondrial evolution. Science 283 (1999) 1476-1481
20. Gualerzi C.O., and Pon C.L. Initiation of mRNA translation in prokaryotes. Biochemistry 29 (1990) 5881-5889
21. Harris J.K., Kelley S.T., Spiegelman G.B., and Pace N.R. The genetic core of the universal ancestor. Genome Res. 13 (2003) 407-412
22. Hershey J.W. Protein synthesis. In: Neidhart F.C. (Ed). Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology (1987), American Society for Microbiology, Washington, DC 613-647
23. Jacobs H.T. Disorders of mitochondrial protein synthesis. Hum. Mol. Genet. 12 Spec No 2 (2003) R293-R301
24. Jacobs H.T., and Turnbull D.M. Nuclear genes and mitochondrial translation: a new class of genetic disease. Trends Genet. 21 (2005) 312-314
25. Karimi R., Pavlov M.Y., Heurgue-Hamard V., Buckingham R.H., and Ehrenberg M. Initiation factors IF1 and IF2 synergistically remove peptidyl-tRNAs with short polypeptides from the P-site of translating Escherichia coli ribosomes. J. Mol. Biol. 281 (1998) 241-252
26. Koc E.C., and Spremulli L.L. Identification of mammalian mitochondrial translational initiation factor 3 and examination of its role in initiation complex formation with natural mRNAs. J. Biol. Chem. 277 (2002) 35541-35549
27. Kyrpides N.C., and Woese C.R. Universally conserved translation initiation factors. Proc. Natl. Acad. Sci. USA 95 (1998) 224-228
28. Laalami S., Putzer H., Plumbridge J.A., and Grunberg-Manago M. A severely truncated form of translational initiation factor 2 supports growth of Escherichia coli. J. Mol. Biol. 220 (1991) 335-349
29. Laursen B.S., Siwanowicz I., Larigauderie G., Hedegaard J., Ito K., Nakamura Y., Kenney J.M., Mortensen K.K., and Sperling-Petersen H.U. Characterization of mutations in the GTP-binding domain of IF2 resulting in cold-sensitive growth of Escherichia coli. J. Mol. Biol. 326 (2003) 543-551
30. Laursen B.S., Sorensen H.P., Mortensen K.K., and Sperling-Petersen H.U. Initiation of protein synthesis in bacteria. Microbiol. Mol. Biol. Rev. 69 (2005) 101-123
31. Lee J.H., Choi S.K., Roll-Mecak A., Burley S.K., and Dever T.E. Universal conservation in translation initiation revealed by human and archaeal homologs of bacterial translation initiation factor IF2. Proc. Natl. Acad. Sci. USA 96 (1999) 4342-4347
32. Lee E.C., Yu D., Martinez de Velasco J., Tessarollo L., Swing D.A., Court D.L., Jenkins N.A., and Copeland N.G. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73 (2001) 56-65
33. Liao H.X., and Spremulli L.L. Identification and initial characterization of translational initiation factor 2 from bovine mitochondria. J. Biol. Chem. 265 (1990) 13618-13622
34. Londei P. Evolution of translational initiation: new insights from the archaea. FEMS Microbiol. Rev. 29 (2005) 185-200
35. Ma L., and Spremulli L.L. Cloning and sequence analysis of the human mitochondrial translational initiation factor 2 cDNA. J. Biol. Chem. 270 (1995) 1859-1865
36. Ma J., and Spremulli L.L. Expression, purification, and mechanistic studies of bovine mitochondrial translational initiation factor 2. J. Biol. Chem. 271 (1996) 5805-5811
37. Ma J., Farwell M.A., Burkhart W.A., and Spremulli L.L. Cloning and sequence analysis of the cDNA for bovine mitochondrial translational initiation factor 2. Biochim. Biophys. Acta 1261 (1995) 321-324
38. Marintchev A., Kolupaeva V.G., Pestova T.V., and Wagner G. Mapping the binding interface between human eukaryotic initiation factors 1A and 5B: a new interaction between old partners. Proc. Natl. Acad. Sci. USA 100 (2003) 1535-1540
39. Miller J.H. Experiments in Molecular Genetics (1972), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
40. Myasnikov A.G., Marzi S., Simonetti A., Giuliodori A.M., Gualerzi C.O., Yusupova G., Yusupov M., and Klaholz B.P. Conformational transition of initiation factor 2 from the GTP- to GDP-bound state visualized on the ribosome. Nat. Struct. Mol. Biol. 12 (2005) 1145-1149
41. O'Brien T.W. Evolution of a protein-rich mitochondrial ribosome: implications for human genetic disease. Gene 286 (2002) 73-79
42. Olsen D.S., Savner E.M., Mathew A., Zhang F., Krishnamoorthy T., Phan L., and Hinnebusch A.G. Domains of eIF1A that mediate binding to eIF2, eIF3 and eIF5B and promote ternary complex recruitment in vivo. EMBO J. 22 (2003) 193-204
43. Pel H.J., and Grivell L.A. Protein synthesis in mitochondria. Mol. Biol. Rep. 19 (1994) 183-194
44. Pietromonaco S.F., Hessler R.A., and O'Brien T.W. Evolution of proteins in mammalian cytoplasmic and mitochondrial ribosomes. J. Mol. Evol. 24 (1986) 110-117
45. Roll-Mecak A., Cao C., Dever T.E., and Burley S.K. X-ray structures of the universal translation initiation factor IF2/eIF5B: conformational changes on GDP and GTP binding. Cell 103 (2000) 781-792
46. Roll-Mecak A., Shin B.S., Dever T.E., and Burley S.K. Engaging the ribosome: universal IFs of translation. Trends Biochem. Sci. 26 (2001) 705-709
47. Sambrook J.F., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. Second Edition (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
48. Sharma M.R., Koc E.C., Datta P.P., Booth T.M., Spremulli L.L., and Agrawal R.K. Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell 115 (2003) 97-108
49. Spencer A.C., and Spremulli L.L. The interaction of mitochondrial translational initiation factor 2 with the small ribosomal subunit. Biochim. Biophys. Acta 1750 (2005) 69-81
50. Spremulli L.L., Coursey A., Navratil T., and Hunter S.E. Initiation and elongation factors in mammalian mitochondrial protein biosynthesis. Prog. Nucleic Acid Res. Mol. Biol. 77 (2004) 211-261
51. Tibbetts A.S., Oesterlin L., Chan S.Y., Kramer G., Hardesty B., and Appling D.R. Mammalian mitochondrial initiation factor 2 supports yeast mitochondrial translation without formylated initiator tRNA. J. Biol. Chem. 278 (2003) 31774-31780
52. Towpik J. Regulation of mitochondrial translation in yeast. Cell. Mol. Biol. Lett. 10 (2005) 571-594
53. Vambutas A., Ackerman S.H., and Tzagoloff A. Mitochondrial translational-initiation and elongation factors in Saccharomyces cerevisiae. Eur. J. Biochem. 201 (1991) 643-652
54. Varshney U., Hutcheon T., and van de Sande J.H. Sequence analysis, expression, and conservation of Escherichia coli uracil DNA glycosylase and its gene (ung). J. Biol. Chem. 263 (1988) 7776-7784