Igs expressed by chronic lymphocytic leukemia B cells show limited binding-site structure variability

Journal of Immunology

Volumn 190, Issue 11, 2013, Pages 5771-5778

  Marcatili, Paolo ^a   Ghiotto, Fabio ^b   Tenca, Claudya ^b   Chailyan, Anna ^a   Mazzarello, Andrea N ^b   Yan, Xiao Jie ^c   Colombo, Monica ^d   Albesiano, Emilia ^c   Bagnara, Davide ^c   Cutrona, Giovanna ^d   Morabito, Fortunato ^e   Bruno, Silvia ^b   Ferrarini, Manlio ^d   Chiorazzi, Nicholas ^c,f,g   Tramontano, Anna ^a,h   Fais, Franco ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^d UNIVERSITY OF GENOA   (Italy)

^e Azienda Ospedaliera di Cosenza   (Italy)

^f Hofstra North Shore Long Island Jewish School of Medicine ^*  (United States)

^g DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

^h Pasteur Institute   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN;

AMINO ACID SEQUENCE; ANTIBODY COMBINING SITE; ARTICLE; B LYMPHOCYTE; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; ELECTROSTIMULATION; GENE CLUSTER; GENE REARRANGEMENT; HUMAN; HUMAN CELL; HYDROPHILICITY; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; VDJ RECOMBINATION;

ANTIGENS; BINDING SITES; CLUSTER ANALYSIS; GENE EXPRESSION; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOGLOBULINS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, ANTIGEN, B-CELL;

EID: 84878082007     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300321     Document Type: Article

References (48)

1. Chiorazzi, N., K. R. Rai, and M. Ferrarini. 2005. Chronic lymphocytic leukemia. N. Engl. J. Med. 352: 804-815.
2. Fais, F., F. Ghiotto, S. Hashimoto, B. Sellars, A. Valetto, S. L. Allen, P. Schulman, V. P. Vinciguerra, K. Rai, L. Z. Rassenti, et al. 1998. Chronic lymphocytic leukemia B cells express restricted sets of mutated and unmutated antigen receptors. J. Clin. Invest. 102: 1515-1525. (Pubitemid 28492218)
3. Ghiotto, F., F. Fais, E. Albesiano, C. Sison, A. Valetto, G. Gaidano, J. Reinhardt, J. E. Kolitz, K. Rai, S. L. Allen, et al. 2006. Similarities and differences between the light and heavy chain Ig variable region gene repertoires in chronic lymphocytic leukemia. Mol. Med. 12: 300-308. (Pubitemid 46489823)
4. Hadzidimitriou, A., N. Darzentas, F. Murray, T. Smilevska, E. Arvaniti, C. Tresoldi, A. Tsaftaris, N. Laoutaris, A. Anagnostopoulos, F. Davi, et al. 2009. Evidence for the significant role of immunoglobulin light chains in antigen recognition and selection in chronic lymphocytic leukemia. Blood 113: 403-411.
5. Damle, R. N., T. Wasil, F. Fais, F. Ghiotto, A. Valetto, S. L. Allen, A. Buchbinder, D. Budman, K. Dittmar, J. Kolitz, et al. 1999. Ig V gene mutation status and CD38 expression as novel prognostic indicators in chronic lymphocytic leukemia. Blood 94: 1840-1847. (Pubitemid 29430399)
6. Hamblin, T. J., Z. Davis, A. Gardiner, D. G. Oscier, and F. K. Stevenson. 1999. Unmutated Ig V(H) genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood 94: 1848-1854. (Pubitemid 29430400)
7. Ghiotto, F., F. Fais, A. Valetto, E. Albesiano, S. Hashimoto, M. Dono, H. Ikematsu, S. L. Allen, J. Kolitz, K. R. Rai, et al. 2004. Remarkably similar antigen receptors among a subset of patients with chronic lymphocytic leukemia. J. Clin. Invest. 113: 1008-1016. (Pubitemid 38544122)
8. Messmer, B. T., E. Albesiano, D. G. Efremov, F. Ghiotto, S. L. Allen, J. Kolitz, R. Foa, R. N. Damle, F. Fais, D. Messmer, et al. 2004. Multiple distinct sets of stereotyped antigen receptors indicate a role for antigen in promoting chronic lymphocytic leukemia. J. Exp. Med. 200: 519-525. (Pubitemid 39121908)
9. Tobin, G., U. Thunberg, A. Johnson, I. Eriksson, O. Söderberg, K. Karlsson, M. Merup, G. Juliusson, J. Vilpo, G. Enblad, et al. 2003. Chronic lymphocytic leukemias utilizing the VH3-21 gene display highly restricted Vlambda2-14 gene use and homologous CDR3s: implicating recognition of a common antigen epitope. Blood 101: 4952-4957. (Pubitemid 36857759)
10. Tobin, G., U. Thunberg, K. Karlsson, F. Murray, A. Laurell, K. Willander, G. Enblad, M. Merup, J. Vilpo, G. Juliusson, et al. 2004. Subsets with restricted immunoglobulin gene rearrangement features indicate a role for antigen selection in the development of chronic lymphocytic leukemia. Blood 104: 2879-2885. (Pubitemid 39434975)
11. Widhopf, G. F., II, L. Z. Rassenti, T. L. Toy, J. G. Gribben, W. G. Wierda, and T. J. Kipps. 2004. Chronic lymphocytic leukemia B cells of more than 1% of patients express virtually identical immunoglobulins. Blood 104: 2499-2504.
12. Agathangelidis, A., N. Darzentas, A. Hadzidimitriou, X. Brochet, F. Murray, X. J. Yan, Z. Davis, E. J. van Gastel-Mol, C. Tresoldi, C. C. Chu, et al. 2012. Stereotyped B-cell receptors in one-third of chronic lymphocytic leukemia: a molecular classification with implications for targeted therapies. Blood 119: 4467-4475.
13. Murray, F., N. Darzentas, A. Hadzidimitriou, G. Tobin, M. Boudjogra, C. Scielzo, N. Laoutaris, K. Karlsson, F. Baran-Marzsak, A. Tsaftaris, et al. 2008. Stereotyped patterns of somatic hypermutation in subsets of patients with chronic lymphocytic leukemia: implications for the role of antigen selection in leukemogenesis. Blood 111: 1524-1533. (Pubitemid 351213442)
14. Stamatopoulos, K., C. Belessi, C. Moreno, M. Boudjograh, G. Guida, T. Smilevska, L. Belhoul, S. Stella, N. Stavroyianni, M. Crespo, et al. 2007. Over 20% of patients with chronic lymphocytic leukemia carry stereotyped receptors: pathogenetic implications and clinical correlations. Blood 109: 259-270. (Pubitemid 46070124)
15. Minden, M. D., R. Ubelhart, D. Schneider, T. Wossning, M. P. Bach, M. Buchner, D. Hofmann, E. Surova, M. Follo, F. Kohler, et al. 2012. Chronic lymphocytic leukaemia is driven by antigen-independent cell-autonomous signalling. Nature. 489: 309-312.
16. Sutton, L. A., E. Kostareli, A. Hadzidimitriou, N. Darzentas, A. Tsaftaris, A. Anagnostopoulos, R. Rosenquist, and K. Stamatopoulos. 2009. Extensive intraclonal diversification in a subgroup of chronic lymphocytic leukemia patients with stereotyped IGHV4-34 receptors: implications for ongoing interactions with antigen. Blood 114: 4460-4468.
17. Thorsélius, M., A. Kröber, F. Murray, U. Thunberg, G. Tobin, A. Bühler, D. Kienle, E. Albesiano, R. Maffei, L. P. Dao-Ung, et al. 2006. Strikingly homologous immunoglobulin gene rearrangements and poor outcome in VH3-21-using chronic lymphocytic leukemia patients independent of geographic origin and mutational status. Blood 107: 2889-2894.
18. Wu, T. T., and E. A. Kabat. 1970. An analysis of the sequences of the variable regions of Bence Jones proteins and myeloma light chains and their implications for antibody complementarity. J. Exp. Med. 132: 211-250.
19. Chothia, C., and A. M. Lesk. 1987. Canonical structures for the hypervariable regions of immunoglobulins. J. Mol. Biol. 196: 901-917. (Pubitemid 17127946)
20. Morea, V., A. Tramontano, M. Rustici, C. Chothia, and A. M. Lesk. 1998. Conformations of the third hypervariable region in the VH domain of immunoglobulins. J. Mol. Biol. 275: 269-294. (Pubitemid 28030004)
21. Tramontano, A., C. Chothia, and A. M. Lesk. 1990. Framework residue 71 is a major determinant of the position and conformation of the second hypervariable region in the VH domains of immunoglobulins. J. Mol. Biol. 215: 175-182. (Pubitemid 20301312)
22. Marcatili, P., A. Rosi, and A. Tramontano. 2008. PIGS: automatic prediction of antibody structures. Bioinformatics 24: 1953-1954.
23. Pedotti, M., L. Simonelli, E. Livoti, and L. Varani. 2011. Computational docking of antibody-antigen complexes, opportunities and pitfalls illustrated by influenza hemagglutinin. Int. J. Mol. Sci. 12: 226-251.
24. Morea, V., A. M. Lesk, and A. Tramontano. 2000. Antibody modeling: implications for engineering and design. Methods 20: 267-279. (Pubitemid 32905162)
25. Almagro, J. C., M. P. Beavers, F. Hernandez-Guzman, J. Maier, J. Shaulsky, K. Butenhof, P. Labute, N. Thorsteinson, K. Kelly, A. Teplyakov, et al. 2011. Antibody modeling assessment. Proteins 79: 3050-3066.
26. Cheson, B. D., J. M. Bennett, M. Grever, N. Kay, M. J. Keating, S. O'Brien, and K. R. Rai. 1996. National Cancer Institute-sponsored Working Group guidelines for chronic lymphocytic leukemia: revised guidelines for diagnosis and treatment. Blood 87: 4990-4997. (Pubitemid 26189840)
27. Pommié, C., S. Levadoux, R. Sabatier, G. Lefranc, and M. P. Lefranc. 2004. IMGT standardized criteria for statistical analysis of immunoglobulin V-REGION amino acid properties. J. Mol. Recognit. 17: 17-32. (Pubitemid 38231461)
28. Bikos, V., N. Darzentas, A. Hadzidimitriou, Z. Davis, S. Hockley, A. Traverse-Glehen, P. Algara, A. Santoro, D. Gonzalez, M. Mollejo, et al. 2012. Over 30% of patients with splenic marginal zone lymphoma express the same immunoglobulin heavy variable gene: ontogenetic implications. Leukemia 26: 1638-1646.
29. Chailyan, A., A. Tramontano, and P. Marcatili. 2012. A database of immunoglobulins with integrated tools: DIGIT. Nucleic Acids Res. 40(Database issue): D1230-D1234.
30. Zemla, A. 2003. LGA: A method for finding 3D similarities in protein structures. Nucleic Acids Res. 31: 3370-3374. (Pubitemid 37442162)
31. Al-Lazikani, B., A. M. Lesk, and C. Chothia. 1997. Standard conformations for the canonical structures of immunoglobulins. J. Mol. Biol. 273: 927-948. (Pubitemid 27493729)
32. Rousseeuw, P. J. 1987. Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. J. Comput. Appl. Math. 20: 53-65.
33. Zhang, Y., and J. Skolnick. 2004. Scoring function for automated assessment of protein structure template quality. Proteins 57: 702-710. (Pubitemid 39626992)
34. Anderberg, M. R. 1973. Cluster Analysis for Applications. Academic Press, New York.
35. Baker, N. A., D. Sept, S. Joseph, M. J. Holst, and J. A. McCammon. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA 98: 10037-10041. (Pubitemid 32802969)
36. Eddy, S. R. 1998. Profile hidden Markov models. Bioinformatics 14: 755-763. (Pubitemid 28552108)
37. Li, W., and A. Godzik. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659. (Pubitemid 43985301)
38. Lee, M., P. Lloyd, X. Zhang, J. M. Schallhorn, K. Sugimoto, A. G. Leach, G. Sapiro, and K. N. Houk. 2006. Shapes of antibody binding sites: qualitative and quantitative analyses based on a geomorphic classification scheme. J. Org. Chem. 71: 5082-5092.
39. MacCallum, R. M., A. C. Martin, and J. M. Thornton. 1996. Antibody-antigen interactions: contact analysis and binding site topography. J. Mol. Biol. 262: 732-745. (Pubitemid 26343518)
40. Sthoeger, Z. M., M. Wakai, D. B. Tse, V. P. Vinciguerra, S. L. Allen, D. R. Budman, S. M. Lichtman, P. Schulman, L. R. Weiselberg, and N. Chiorazzi. 1989. Production of autoantibodies by CD5-expressing B lymphocytes from patients with chronic lymphocytic leukemia. J. Exp. Med. 169: 255-268. (Pubitemid 19035555)
41. Hervé, M., K. Xu, Y. S. Ng, H. Wardemann, E. Albesiano, B. T. Messmer, N. Chiorazzi, and E. Meffre. 2005. Unmutated and mutated chronic lymphocytic leukemias derive from self-reactive B cell precursors despite expressing different antibody reactivity. J. Clin. Invest. 115: 1636-1643. (Pubitemid 40814672)
42. Bomben, R., M. Dal Bo, D. Capello, D. Benedetti, D. Marconi, A. Zucchetto, F. Forconi, R. Maffei, E. M. Ghia, L. Laurenti, et al. 2007. Comprehensive characterization of IGHV3-21-expressing B-cell chronic lymphocytic leukemia: an Italian multicenter study. Blood 109: 2989-2998. (Pubitemid 46482099)
43. Collis, A. V., A. P. Brouwer, and A. C. Martin. 2003. Analysis of the antigen combining site: correlations between length and sequence composition of the hypervariable loops and the nature of the antigen. J. Mol. Biol. 325: 337-354. (Pubitemid 36062692)
44. Catera, R., G. J. Silverman, K. Hatzi, T. Seiler, S. Didier, L. Zhang, M. Hervé, E. Meffre, D. G. Oscier, H. Vlassara, et al. 2008. Chronic lymphocytic leukemia cells recognize conserved epitopes associated with apoptosis and oxidation. Mol. Med. 14: 665-674.
45. Bomben, R., M. Dal Bo, D. Capello, F. Forconi, R. Maffei, L. Laurenti, D. Rossi, M. I. Del Principe, A. Zucchetto, F. Bertoni, et al. 2009. Molecular and clinical features of chronic lymphocytic leukaemia with stereotyped B cell receptors: results from an Italian multicentre study. Br. J. Haematol. 144: 492-506.
46. Chu, C. C., R. Catera, K. Hatzi, X. J. Yan, L. Zhang, X. B. Wang, H. M. Fales, S. L. Allen, J. E. Kolitz, K. R. Rai, and N. Chiorazzi. 2008. Chronic lymphocytic leukemia antibodies with a common stereotypic rearrangement recognize non-muscle myosin heavy chain IIA. Blood 112: 5122-5129.
47. Rossi, D., and G. Gaidano. 2010. Biological and clinical significance of stereotyped B-cell receptors in chronic lymphocytic leukemia. Haematologica 95: 1992-1995.
48. Tobin, G., U. Thunberg, A. Johnson, I. Thörn, O. Söderberg, M. Hultdin, J. Botling, G. Enblad, J. Sällström, C. Sundström, et al. 2002. Somatically mutated Ig V(H)3-21 genes characterize a new subset of chronic lymphocytic leukemia. Blood 99: 2262-2264. (Pubitemid 34525519)