Hyperconservation of the N-formyl peptide binding site of M3: Evidence that M3 is an old eutherian molecule with conserved recognition of a pathogen-associated molecular pattern

Journal of Immunology

Volumn 171, Issue 2, 2003, Pages 836-844

  Doyle, C Kuyler ^a   Davis, Beckley K ^a   Cook, Richard G ^a   Rich, Robert R ^a,b   Rodgers, John R ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD1 ANTIGEN; CYTOCHROME B; FORMYLPEPTIDE; GENOMIC DNA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PATTERN RECOGNITION RECEPTOR; PROTEIN M3; RECEPTOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA SEQUENCE; MOLECULAR EVOLUTION; MOUSE; MURIDAE; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE SEQUENCE; PATHOGEN ASSOCIATED MOLECULAR PATTERN RECOGNITION; PATTERN RECOGNITION; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT;

EID: 0038106600     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.2.836     Document Type: Article

References (68)

1. Loveland, B., C.-R. Wang, H. Yonekawa, E. Hermel, and K. Fischer Lindahl. 1990. Maternally transmitted histocompatibility antigen of mice: a hydrophobic peptide of a mitochondrially encoded protein. Cell 60:971.
2. Shawar, S. M., J. M. Vyas, J. R. Rodgers, R. G. Cook, and R. R. Rich. 1991. Specialized functions of MHC class I molecules. II. Hmt binds N-formylated peptides of mitochondrial and prokaryotic origin. J. Exp. Med. 174:941.
3. Medzhitov, R., and C. A. Janeway, Jr. 2002. Decoding the patterns of self and nonself by the innate immune system. Science 296:298.
4. Le, Y., P. M. Murphy, and J. M. Wang. 2002. Formyl-peptide receptors revisited. Trends Immunol. 23:541.
5. Gumperz, J. E., and M. B. Brenner. 2001. CD1-specific T cells in microbial immunity. Curr. Opin. Immunol. 13:471.
6. Shawar, S. M., J. M. Vyas, J. R. Rodgers, and R. R. Rich. 1994. Antigen presentation by major histocompatibility complex class I-b molecules. Annu. Rev. Immunol. 12:839.
7. Kerksiek, K. M., D. H. Busch, I. M. Pilip, S. E. Allen, and E. G. Pamer. 1999. H2-M3-restricted T cells in bacterial infection: rapid primary but diminished memory responses. J. Exp. Med. 190:195.
8. Seaman, M. S., B. Perarnau, K. Fischer Lindahl, F. A. Lemonnier. and J. Forman. 1999. Response to Listeria monocytogenes in mice lacking MHC class Ia molecules. J. Immunol. 162:5429.
9. + T cells. J. Immunol. 165:4575.
10. Wang, C. R., D. Lambracht, K. Wonigeit, J. C. Howard, and K. Fischer Lindahl. 1995. Rat RTI orthologs of mouse H2-M class Ib genes. Immunogenetics 42:63.
11. Fischer Lindahl, K., D. E. Byers, V. M. Dabhi, R. Hovik, E. P. Jones, G. P. Smith, C. R. Wang, H. Xiao, and M. Yoshino. 1997. H2-M3, a full-service class Ib histocompatibility antigen. Annu. Rev. Immunol. 15:851.
12. Wang, C. R., and K. Fischer Lindahl. 1993. HMT, encoded by H-2M3, is a neoclassical major histocompatibility class I antigen. Proc. Natl. Acad. Sci. USA 90:2784.
13. Doherty, P. C., and R. M. Zinkernagel. 1975. Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256:50.
14. Hughes, A. L. 1999. Adaptive Evolution of Genes and Genomes. Oxford University Press. New York.
15. Hughes, A. L., and M. Nei. 1989. Evolution of the major histocompatibility complex: independent origin of nonclassical class I genes in different groups of mammals. Mol. Biol. Evol. 6:559.
16. Lynch, M., M. O'Hely, B. Walsh, and A. Force. 2001. The probability of preservation of a newly arisen gene duplicate, Genetics 159:1789.
17. Kondrashov, F. A., I. B. Rogozin, Y. I. Wolf, and E. V. Koonin. 2002. Selection in the evolution of gene duplications. Genome Biol. 3:1.
18. Obata, Y., Y. Satta, K. Moriwaki, T. Shiroishi, H. Hasegawa, T. Takahashi, and N. Takahata. 1994. Structure, function, and evolution of mouse TL genes, nonclassical class I genes of the major histocompatibility complex. Proc. Natl. Acad. Sci. USA 91:6589.
19. Davis, B. K., R. G. Cook, R. R. Rich. and J. R. Rodgers. 2002. Hyperconservation of the putative antigen recognition site of the MHC class I-b molecule TL in the subfamily Murinae: evidence that Thymus Leukemia antigen is an ancient mammalian gene. J. Immunol. 169:6890.
20. Wang, C. R., K. Fischer Lindahl, and J. Deisenhofer. 1996. Crystal structure of the MHC class Ib molecule H2-M3. Res. Immunol. 147:313.
21. Bonhomme, F. 1986. Evolutionary relationships in the genus Mus. Curr. Top. Microbiol. Immunol. 127:19.
22. Kumar, S., and S. B. Hedges. 1998. A molecular timescale for vertebrate evolution. Nature 392:917.
23. Adkins, R. M., E. L. Gelke, D. Rowe, and R. L. Honeycutt. 2001. Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes. Mol. Biol. Evol. 18:777.
24. Engel, S. R., K. M. Hogan, J. F. Taylor, and S. K. Davis. 1998. Molecular systematics and paleobiogeography of the South American sigmodontine rodents. Mol. Biol. Evol. 15:35.
25. Ferris, S. D., R. D. Sage, E. M. Prager, U. Ritte, and A. C. Wilson. 1983. Mitochondrial DNA evolution in mice. Genetics 105:681.
26. Rodgers, J. R., C. Smith, S. M. Shawar, and R. R. Rich. 1990. Retrovirus-mediated insertional mutagenesis: phagemid rescue of flanking DNA by selecting plasmid ori. DNA Cell Biol. 9:139.
27. Lander, M. R., and S. K. Chattopadhyay. 1984. A Mus dunni cell line that lacks sequences closely related to endogenous murine leukemia viruses and can be infected by ectropic, amphotropic, xenotropic, and mink cell focus-forming viruses. J. Virol. 52:695.
28. Fisher, P. B., L. E. Babiss, I. B. Weinstein, and H. S. Ginsberg. 1982. Analysis of type 5 adenovirus transformation with a cloned rat embryo cell line (CREF). Proc. Natl. Acad. Sci. USA 79:3527.
29. Cole, Y. 1991. Evolutionary relationship within multiple species of African mice. Doctoral dissertation, Department of Anthropology, New York University College of Arts and Sciences, New York, New York.
30. Suzuki, H., K. Tsuchiya, and N. Takezaki. 2000. A molecular phylogenetic framework for the Ryukyu endemic rodents Tokudaia osimensis and Diplothrix legata. Mol. Phylogenet. Evol. 15:15.
31. Kocher, T. D., W. K. Thomas, A. Meyer, S. V. Edwards, S. Paabo, F. X. Villablanca, and A. C. Wilson. 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 86:6196.
32. Wang, C. R., B. E. Loveland, and K. Fischer Lindahl. 1991. H-2M3 encodes the MHC class I molecule presenting the maternally transmitted antigen of the mouse. Cell 66:335.
33. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673.
34. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95.
35. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTALX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876.
36. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244.
37. Zhang, J., and X. Gu. 1998. Correlation between the substitution rate and rate variation among sites in protein evolution. Genetics 149:1615.
38. Tajima, F. 1993. Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135:599.
39. Nei, M., and T. Gojobori. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3:418.
40. Korber, B. 2001. HIV signature and sequence variation analysis: computational analysis of HIV molecular sequences. In Computational Analysis of HIV Molecular Sequences. A. G. Rodrigo and G. H. Learn, eds. Kluwer, Dordrecht, The Netherlands.
41. Hughes, A. L., and M. Nei. 1988. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167.
42. Nembaware, V., K. Crum, J. Kelso, and C. Seoighe. 2002. Impact of the presence of paralogs on sequence divergence in a set of mouse-human orthologs. Genome Res. 12:1370.
43. Bailey, N. T. J. 1981. Statistical Methods in Biology, 2nd Ed. Wiley, New York.
44. Pullen, J. K., H. D. Hunt, R. M. Horton, and L. R. Pease. 1989. The functional significance of two amino acid polymorphisms in the antigen-presenting domain of class I MHC molecules. J. Immunol. 143:1674.
45. bm12β mutation using site-directed mutagenesis and DNA-mediated gene transfer. J. Immunol. 139:629.
46. Levitt, J. M., D. D. Howell, J. R. Rodgers, and R. R. Rich. 2001. Exogenous peptides enter the endoplasmic reticulum of TAP-deficient cells and induce the maturation of nascent MHC class I molecules. Eur. J. Immunol. 31:1181.
47. d major histocompatibility complex class I chimera. J. Exp. Med. 179:155.
48. Byers, D. E., and K. Fischer Lindahl. 1998. H2-M3 presents a nonformylated viral epitope to CTLs generated in vitro. J. Immunol. 161:90.
49. Silver, L. M. 1995. Mouse Genetics: Concepts and Applications. Oxford University Press, New York.
50. Roitsch, T., and L. Lehle. 1989. Structural requirements for protein N-glycosylation: influence of acceptor peptides on cotranslational glycosylation of yeast invertase and site-directed mutagenesis around a sequon sequence. Eur. J. Biochem. 181:525.
51. Harris, M. R., Y. Y. Yu, C. S. Kindle, T. H. Hansen, and J. C. Solheim. 1998. Calreticulin and calnexin interact with different protein and glycan determinants during the assembly of MHC class I. J. Immunol. 160:5404.
52. Lambracht-Washington, D., K. Wonigeit, and K. Fischer Lindahl. 1999. Gene order of the RT1.M region of the rat MHC exemplifies interspecies conservation with the mouse. Transplant. Proc. 31:1515.
53. Wang, C. R., A. R. Castano, P. A. Peterson, C. Slaughter, K. Fischer Lindahl, and J. Deisenhofer. 1995. Nonclassical binding of formylated peptide in crystal structure of the MHC class Ib molecule H2-M3. Cell 82:655.
54. Hughes, A. L., and M. Yeager. 1997. Comparative evolutionary rates of introns and exons in murine rodents. J. Mol. Evol. 45:125.
55. Bromham, L., M. J. Phillips, and D. Penny. 1999. Growing up with dinosaurs: molecular dates and the mammalian radiation. Trends Ecol. Evol. 14:113.
56. Reyes, A., C. Gissi, G. Pesole, F. M. Catzeflis, and C. Saccone. 2000. Where do rodents fit: evidence from the complete mitochondrial genome of Sciurus vulgaris. Mol. Biol. Evol. 17:979.
57. Springer, M. S., W. J. Murphy, E. Eizirik, and S. J. O'Brien. 2003. Placental mammal diversification and the Cretaceous-Tertiary boundary. Proc. Natl. Acad. Sci. USA 100:1056.
58. Adams, E. J., and P. Parham. 2001. Genomic analysis of common chimpanzee major histocompatibility complex class I genes. Immunogenetics 53:200.
59. Blanco-Gelaz, M. A., A. Lopez-Vazquez, S. Garcia-Fernandez, J. Martinez-Borra, S. Gonzalez, and C. Lopez-Larrea. 2001. Genetic variability, molecular evolution, and geographic diversity of HLA-B27. Hum. Immunol. 62:1042.
60. Guethlein, L. A., and J. C. Howard. 2000. Is a mutator analogous to the Ig hypermutator of the sheep ileal Peyer's patch active on MHC class I genes in the germ line? Immunogenetics 51:462.
61. Jaatinen, T., M. Eholuoto, T. Laitinen, and M. L. Lokki. 2002. Characterization of a de novo conversion in human complement C4 gene producing a C4B5-like protein. J. Immunol. 168:5652.
62. Selsing, E., B. Xu, and D. Sigurdardottir. 1996. Gene conversion and homologous recombination in murine B cells. Semin. Immunol. 8:151.
63. Yauk, C. L., P. R. Bois, and A. J. Jeffreys. 2003. High-resolution sperm typing of meiotic recombination in the mouse MHC Eβ gene. EMBO J. 22:1389.
64. Averof, M., A. Rokas, K. H. Wolfe, and P. M. Sharp. 2000. Evidence for a high frequency of simultaneous double-nucleotide substitutions. Science 287:1283.
65. Eyre-Walker, A., and P. D. Keightley. 1999. High genomic deleterious mutation rates in hominids. Nature 397:344.
66. Bumet, F. M. 1973. Multiple polymorphism in relation to histocompatibility antigens. Nature 245:359.
67. Kasahara, M., J. Nakaya, Y. Satta, and N. Takahata. 1997. Chromosomal duplication and the emergence of the adaptive immune system. Trends Genet. 13:90.
68. Flajnik, M. F., and M. Kasahara. 2001. Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system. Immunity 15:351.