Crystal structure of cockroach allergen Bla g 2, an unusual zinc binding aspartic protease with a novel mode of self-inhibition

Journal of Molecular Biology

Volumn 348, Issue 2, 2005, Pages 433-444

  Gustchina, Alla ^a   Li, Mi ^a,b   Wünschmann, Sabina ^c   Chapman, Martin D ^c   Pomés, Anna ^c   Wlodawer, Alexander ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c INDOOR Biotechnologies Inc   (United States)

Author keywords

Active site; Allergy; Aspartic proteases; Metal binding; Self inhibition

Indexed keywords

ALLERGEN; AMINO ACID; ASPARTIC ACID; ASPARTIC PROTEINASE; BINDING PROTEIN; COCKROACH ALLERGEN BLA G 2; DISULFIDE; GLYCINE; PHENYLALANINE; UNCLASSIFIED DRUG; ZINC;

ALLERGENICITY; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CATALYSIS; COCKROACH; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME STABILITY; HUMAN VERSUS ANIMAL COMPARISON; INSECT ALLERGY; METAL BINDING; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SENSITIZATION; SPECIES COMPARISON; STRUCTURE ANALYSIS; THEORETICAL MODEL;

EID: 16244384649     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.02.062     Document Type: Article

References (58)

1. L.K. Arruda, L.D. Vailes, B.J. Mann, J. Shannon, J.W. Fox, and T.S. Vedvick Molecular cloning of a major cockroach (Blattella germanica) allergen, Bla g 2. Sequence homology to the aspartic proteases J. Biol. Chem. 270 1995 19563 19568
2. D.L. Rosenstreich, P. Eggleston, M. Kattan, D. Baker, R.G. Slavin, and P. Gergen The role of cockroach allergy and exposure to cockroach allergen in causing morbidity among inner-city children with asthma N. Engl. J. Med. 336 1997 1356 1363
3. S.M. Pollart, M.D. Chapman, G.P. Fiocco, G. Rose, and T.A. Platts-Mills Epidemiology of acute asthma: IgE antibodies to common inhalant allergens as a risk factor for emergency room visits J. Allergy Clin. Immunol. 83 1989 875 882
4. R.S. Call, T.F. Smith, E. Morris, M.D. Chapman, and T.A. Platts-Mills Risk factors for asthma in inner city children J. Pediatr. 121 1992 862 866
5. L.E. Gelber, L.H. Seltzer, J.K. Bouzoukis, S.M. Pollart, M.D. Chapman, and T.A. Platts-Mills Sensitization and exposure to indoor allergens as risk factors for asthma among patients presenting to hospital Am. Rev. Respir. Dis. 147 1993 573 578
6. S.C. Christiansen, S.B. Martin, N.C. Schleicher, J.A. Koziol, R.G. Hamilton, and B.L. Zuraw Exposure and sensitization to environmental allergen of predominantly Hispanic children with asthma in San Diego's inner city J. Allergy Clin. Immunol. 98 1996 288 294
7. P.A. Eggleston, D. Rosenstreich, H. Lynn, P. Gergen, D. Baker, and M. Kattan Relationship of indoor allergen exposure to skin test sensitivity in inner-city children with asthma J. Allergy Clin. Immunol. 102 1998 563 570
8. L.K. Arruda, L.D. Vailes, V.P. Ferriani, A.B. Santos, A. Pomés, and M.D. Chapman Cockroach allergens and asthma J. Allergy Clin. Immunol. 107 2001 419 428
9. R. Sporik, S.P. Squillace, J.M. Ingram, G. Rakes, R.W. Honsinger, and T.A. Platts-Mills Mite, cat, and cockroach exposure, allergen sensitisation, and asthma in children: a case-control study of three schools Thorax 54 1999 675 680
10. G.A. Stewart, and P.J. Thompson The biochemistry of common aeroallergens Clin. Expt. Allergy 26 1996 1020 1044
11. J. Harris, D.E. Mason, J. Li, K.W. Burdick, B.J. Backes, and T. Chen Activity profile of dust mite allergen extract using substrate libraries and functional proteomic microarrays Chem. Biol. 11 2004 1361 1372
12. C.R. Hewitt, A.P. Brown, B.J. Hart, and D.I. Pritchard A major house dust mite allergen disrupts the immunoglobulin E network by selectively cleaving CD23: innate protection by antiproteases J. Expt. Med. 182 1995 1537 1544
13. O. Schulz, P. Laing, H.F. Sewell, and F. Shakib Der p I,a major allergen of the house dust mite, proteolytically cleaves the low-affinity receptor for human IgE (CD23) Eur. J. Immunol. 25 1995 3191 3194
14. C. King, S. Brennan, P.J. Thompson, and G.A. Stewart Dust mite proteolytic allergens induce cytokine release from cultured airway epithelium J. Immunol. 161 1998 3645 3651
15. H. Wan, H.L. Winton, C. Soeller, E.R. Tovey, D.C. Gruenert, and P.J. Thompson Der p 1 facilitates transepithelial allergen delivery by disruption of tight junctions J. Clin. Invest. 104 1999 123 133
16. A. Pomés, M.D. Chapman, L.D. Vailes, T.L. Blundell, and V. Dhanaraj Cockroach allergen Bla g 2: structure, function, and implications for allergic sensitization Am. J. Respir. Crit. Care Med. 165 2002 391 397
17. S. Wünschmann, A. Gustchina, M.D. Chapman, and A. Pomés Cockroach allergen Bla g 2: an unusual aspartic protease J. Allergy Clin. Immunol. 2005 In the press
18. S.C. Xie, B.G. Low, R.J. Nagel, K.K. Kramer, R.V. Anthony, and A.P. Zoli Identification of the major pregnancy-specific antigens of cattle and sheep as inactive members of the aspartic proteinase family Proc. Natl Acad. Sci. USA 88 1991 10247 10251
19. K. Guruprasad, T.L. Blundell, S. Xie, J. Green, B. Szafranska, and R.J. Nagel Comparative modelling and analysis of amino acid substitutions suggests that the family of pregnancy-associated glycoproteins includes both active and inactive aspartic proteinases Protein Eng. 9 1996 849 856
20. A.R. Sielecki, A.A. Fedorov, A. Boodhoo, N.S. Andreeva, and M.N. James Molecular and crystal structures of monoclinic porcine pepsin refined at 1.8 Å resolution J. Mol. Biol. 214 1990 143 170
21. G.L. Gilliland, E.L. Winborne, J. Nachman, and A. Wlodawer The three-dimensional structure of recombinant bovine chymosin at 2.3 Å resolution Proteins: Struct. Funct. Genet. 8 1990 82 101
22. N.S. Andreeva, A.E. Gustchina, A.A. Fedorov, N.E. Shutzkever, and T.V. Volnova X-ray crystallographic studies of pepsin Advan. Expt. Med. Biol. 95 1977 23 31
23. J. Jenkins, I. Tickle, T. Sewell, L. Ungaretti, A. Wollmer, and T. Blundell X-ray analysis and circular dichroism of the acid protease from Endothia parasitica and chymosin Advan. Expt. Med. Biol. 95 1977 43 60
24. I.N. Hsu, L.T. Delbaere, M.N. James, and T. Hofmann Penicillopepsin: 2.8 Å structure, active site conformation and mechanistic implications Advan. Expt. Med. Biol. 95 1977 61 81
25. N.S. Andreeva, and A.E. Gustchina On the supersecondary structure of acid proteases Biochem. Biophys. Res. Commun. 87 1979 32 42
26. N. Andreeva A consensus template of the aspartic proteinase fold B. Dunn Structure and Function of the Aspartic Proteinases 1991 Plenum Press New York, NY 559 572
27. N.S. Andreeva, and L.D. Rumsh Analysis of crystal structures of aspartic proteinases: on the role of amino acid residues adjacent to the catalytic site of pepsin-like enzymes Protein Sci. 10 2001 2439 2450
28. M. Li, L.H. Phylip, W.E. Lees, J.R. Winther, B.M. Dunn, and A. Wlodawer The aspartic proteinase from S. cerevisiae folds its own inhibitor into a helix Nature Struct. Biol. 7 2000 113 117
29. A.R. Sielecki, K. Hayakawa, M. Fujinaga, M.E. Murphy, M. Fraser, and A.K. Muir Structure of recombinant human renin, a target for cardiovascular-active drugs, at 2.5 Å resolution Science 243 1989 1346 1351
30. L. Pearl, and T. Blundell The active site of aspartic proteinases FEBS Letters 174 1984 96 101
31. J. Rahuel, J.P. Priestle, and M.G. Grutter The crystal structures of recombinant glycosylated human renin alone and in complex with a transition state analog inhibitor J. Struct. Biol. 107 1991 227 236
32. N. Andreeva, J. Dill, and G.L. Gilliland Can enzymes adopt a self-inhibited form? Results of X-ray crystallographic studies of chymosin Biochem. Biophys. Res. Commun. 184 1992 1074 1081
33. A. Gustchina, M. Li, L.H. Phylip, W.E. Lees, J. Kay, and A. Wlodawer An unusual orientation for Tyr75 in the active site of the aspartic proteinase from Saccharomyces cerevisiae Biochem. Biophys. Res. Commun. 295 2002 1020 1026
34. J. Trylska, P. Grochowski, and J.A. McCammon The role of hydrogen bonding in the enzymatic reaction catalyzed by HIV-1 protease Protein Sci. 13 2004 513 528
35. T. Kageyama Rabbit procathepsin E and cathepsin E. Nucleotide sequence of cDNA, hydrolytic specificity for biologically active peptides and gene expression during development Eur. J. Biochem. 216 1993 717 728
36. I. Winkler, J. Bodem, L. Haas, M. Zemba, H. Delius, and R. Flower Characterization of the genome of feline foamy virus and its proteins shows distinct features different from those of primate spumaviruses J. Virol. 71 1997 6727 6741
37. J.A. Green, S. Xie, B. Szafranska, X. Gan, A.G. Newman, K. McDowell, and R.M. Roberts Identification of a new aspartic proteinase expressed by the outer chorionic cell layer of the equine placenta Biol. Reprod. 60 1999 1069 1077
38. R. Cornette, J.P. Farine, B. Quennedey, S. Riviere, and R. Brossut Molecular characterization of Lma-p54, a new epicuticular surface protein in the cockroach Leucophaea maderae (Dictyoptera, oxyhaloinae) Insect Biochem. Mol. Biol. 32 2002 1635 1642
39. M. Lombardero, P.W. Heymann, T.A. Platts-Mills, J.W. Fox, and M.D. Chapman Conformational stability of B cell epitopes on group I and group II Dermatophagoides spp. Allergens. Effect of thermal and chemical denaturation on the binding of murine IgG and human IgE antibodies J. Immunol. 144 1990 1353 1360
40. T. Takai, T. Yokota, M. Yasue, C. Nishiyama, T. Yuuki, and A. Mori Engineering of the major house dust mite allergen Der f 2 for allergen-specific immunotherapy Nature Biotechnol. 15 1997 754 758
41. A.M. Smith, M.D. Chapman, E.A. Taketomi, T.A. Platts-Mills, and S.S. Sung Recombinant allergens for immunotherapy: a Der p 2 variant with reduced IgE reactivity retains T-cell epitopes J. Allergy Clin. Immunol. 101 1998 423 425
42. M.D. Chapman, A.M. Smith, L.D. Vailes, L.K. Arruda, V. Dhanaraj, and A. Pomés Recombinant allergens for diagnosis and therapy of allergic disease J. Allergy Clin. Immunol. 106 2000 409 418
43. O. Schulz, H.F. Sewell, and F. Shakib Proteolytic cleavage of CD25, the alpha subunit of the human T cell interleukin 2 receptor, by Der p 1, a major mite allergen with cysteine protease activity J. Expt. Med. 187 1998 271 275
44. F. Shakib, O. Schulz, and H. Sewell A mite subversive: cleavage of CD23 and CD25 by Der p 1 enhances allergenicity Immunol. Today 19 1998 313 316
45. T. Dudler, D.C. Machado, L. Kolbe, R.R. Annand, N. Rhodes, and M.H. Gelb A link between catalytic activity. IgE-independent mast cell activation, and allergenicity of bee venom phospholipase A2 J. Immunol. 155 1995 2605 2613
46. J.F. Tomee, R. van Weissenbruch, J.G. de Monchy, and H.F. Kauffman Interactions between inhalant allergen extracts and airway epithelial cells: effect on cytokine production and cell detachment J. Allergy Clin. Immunol. 102 1998 75 85
47. Z. Bocskei, C.R. Groom, D.R. Flower, C.E. Wright, S.E. Phillips, and A. Cavaggioni Pheromone binding to two rodent urinary proteins revealed by X-ray crystallography Nature 360 1992 186 188
48. U. Derewenda, J. Li, Z. Derewenda, Z. Dauter, G.A. Mueller, G.S. Rule, and D.C. Benjamin The crystal structure of a major dust mite allergen Der p 2, and its biological implications J. Mol. Biol. 318 2002 189 197
49. L. Kaiser, H. Gronlund, T. Sandalova, H.G. Ljunggren, M. Hage-Hamsten, A. Achour, and G. Schneider The crystal structure of the major cat allergen Fel d 1, a member of the secretoglobin family J. Biol. Chem. 278 2003 37730 37735
50. A. Pomés, L.D. Vailes, R.M. Helm, and M.D. Chapman IgE reactivity of tandem repeats derived from cockroach allergen, Bla g 1 Eur. J. Biochem. 269 2002 3086 3092
51. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
52. T.C. Terwilliger, and J. Berendzen Bayesian MAD phasing Acta Crystallog. sect. D 53 1997 571 579
53. E. de la Fortelle, and G. Bricogne Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods Methods Enzymol. 276 1997 472 494
54. CCP4. Collaborative Computational Project Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallog. sect. D 50 1994 760 763
55. T.C. Terwilliger, and J. Berendzen Automated MAD and MIR structure solution Acta Crystallog. sect. D 55 1999 849 861
56. T.A. Jones, and M. Kjeldgaard Electron-density map interpretation Methods Enzymol. 277 1997 173 208
57. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve Crystallography and NMR system: a new software suite for macromolecular structure determination Acta Crystallog. sect. D 54 1998 905 921
58. G.M. Sheldrick, and T.R. Schneider SHELXL: high-resolution refinement Methods Enzymol. 277 1997 319 343