Anti-leukemia activity of a bacterial toxin with natural specificity for LFA-1 on white blood cells

Leukemia Research

Volumn 34, Issue 6, 2010, Pages 777-785

  Kachlany, Scott C ^a   Schwartz, Amy B ^a   Balashova, Nataliya V ^a   Hioe, Catarina E ^b   Tuen, Michael ^b   Le, Amy ^a   Kaur, Manpreet ^a   Mei, Yongyi ^a   Rao, Jia ^a  

^a RUTGERS SCHOOL OF DENTAL MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acute myeloid leukemia; Immunotoxin; Lymphoma; Targeted therapy

Indexed keywords

BACTERIAL TOXIN; LEUKOTOXIN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1;

ACUTE GRANULOCYTIC LEUKEMIA; AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER SURVIVAL; CELL INTERACTION; CELL STRAIN; CONTROLLED STUDY; CYTOTOXICITY; DRUG SPECIFICITY; DRUG TARGETING; GENE EXPRESSION; GENE FUNCTION; GENE TARGETING; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; LEUKOCYTE; MACACA; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; SCID MOUSE;

ANIMALS; ANTINEOPLASTIC AGENTS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; HEMOLYSIN PROTEINS; HL-60 CELLS; HUMANS; JURKAT CELLS; LEUKEMIA; LEUKOCYTES; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MACACA MULATTA; MICE; MICE, SCID; MICE, TRANSGENIC; PROTEIN BINDING; SUBSTRATE SPECIFICITY;

EID: 77952098308     PISSN: 01452126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.leukres.2009.08.022     Document Type: Article

References (60)

1. Jain K.K. Use of bacteria as anticancer agents. Expert Opin Biol Ther 2001, 1:291-300.
2. Kreitman R.J. Immunotoxins for targeted cancer therapy. AAPS J 2006, 8:E532-551.
3. Jankovic J. Botulinum toxin in clinical practice. J Neurol Neurosurg Psychiatry 2004, 75:951-957.
4. Duvic M., Kuzel T.M., Olsen E.A., et al. Quality-of-life improvements in cutaneous T-cell lymphoma patients treated with denileukin diftitox (ONTAK). Clin Lymphoma 2002, 2:222-228.
5. Olsen E., Duvic M., Frankel A., et al. Pivotal phase III trial of two dose levels of denileukin diftitox for the treatment of cutaneous T-cell lymphoma. J Clin Oncol 2001, 19:376-388.
6. Kreitman R.J., Pastan I. Immunotoxins in the treatment of hematologic malignancies. Curr Drug Targets 2006, 7:1301-1311.
7. Liu T.F., Urieto J.O., Moore J.E., et al. Diphtheria toxin fused to variant interleukin-3 provides enhanced binding to the interleukin-3 receptor and more potent leukemia cell cytotoxicity. Exp Hematol 2004, 32:277-281.
8. Perentesis J.P., Gunther R., Waurzyniak B., et al. In vivo biotherapy of HL-60 myeloid leukemia with a genetically engineered recombinant fusion toxin directed against the human granulocyte macrophage colony-stimulating factor receptor. Clin Cancer Res 1997, 3:2217-2227.
9. Fine D.H., Kaplan J.B., Kachlany S.C., Schreiner H.C. How we got attached to Actinobacillus actinomycetemcomitans: a model for infectious diseases. Periodontol 2000 2006, 42:114-157.
10. Slots J., Ting M. Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in human periodontal disease: occurrence and treatment. Periodontol 2000 1999, 20:82-121.
11. Taichman N.S., Dean R.T., Sanderson C.J. Biochemical and morphological characterization of the killing of human monocytes by a leukotoxin derived from Actinobacillus actinomycetemcomitans. Infect Immun 1980, 28:258-268.
12. Taichman N.S., Simpson D.L., Sakurada S., Cranfield M., DiRienzo J., Slots J. Comparative studies on the biology of Actinobacillus actinomycetemcomitans leukotoxin in primates. Oral Microbiol Immunol 1987, 2:97-104.
13. Lally E.T., Hill R.B., Kieba I.R., Korostoff J. The interaction between RTX toxins and target cells. Trends Microbiol 1999, 7:356-361.
14. Welch R.A. RTX toxin structure and function: a story of numerous anomalies and few analogies in toxin biology. Curr Top Microbiol Immunol 2001, 257:85-111.
15. Delepelaire P. Type I secretion in Gram-negative bacteria. Biochim Biophys Acta 2004, 1694:149-161.
16. Crosby J.A., Kachlany S.C. TdeA, a TolC-like protein required for toxin and drug export in Aggregatibacter (Actinobacillus) actinomycetemcomitans. Gene 2007, 388:83-92.
17. Isaza M.P., Duncan M.S., Kaplan J.B., Kachlany S.C. Screen for leukotoxin mutants in Aggregatibacter actinomycetemcomitans: genes of the phosphotransferase system are required for leukotoxin biosynthesis. Infect Immun 2008, 76:3561-3568.
18. Stanley P., Koronakis V., Hughes C. Acylation of Escherichia coli hemolysin: a unique protein lipidation mechanism underlying toxin function. Microbiol Mol Biol Rev 1998, 62:309-333.
19. Balashova N.V., Shah C., Patel J.K., Megalla S., Kachlany S.C. Aggregatibacter actinomycetemcomitans LtxC is required for leukotoxin activity and initial interaction between toxin and host cells. Gene 2009, 443:42-47.
20. Lally E.T., Kieba I.R., Sato A., et al. RTX toxins recognize a beta2 integrin on the surface of human target cells. J Biol Chem 1997, 272:30463-30469.
21. Hogg N., Smith A., McDowall A., et al. How T cells use LFA-1 to attach and migrate. Immunol Lett 2004, 92:51-54.
22. Kinashi T. Intracellular signalling controlling integrin activation in lymphocytes. Nat Rev Immunol 2005, 5:546-559.
23. Kachlany S.C., Fine D.H., Figurski D.H. Secretion of RTX leukotoxin by Actinobacillus actinomycetemcomitans. Infect Immun 2000, 68:6094-6100.
24. Kachlany S.C., Fine D.H., Figurski D.H. Purification of secreted leukotoxin (LtxA) from Actinobacillus actinomycetemcomitans. Protein Expr Purif 2002, 25:465-471.
25. Diaz R., Ghofaily L.A., Patel J., et al. Characterization of leukotoxin from a clinical strain of Actinobacillus actinomycetemcomitans. Microb Pathog 2006, 40:48-55.
26. Fong K.P., Pacheco C.M., Otis L.L., et al. Actinobacillus actinomycetemcomitans leukotoxin requires lipid microdomains for target cell cytotoxicity. Cell Microbiol 2006, 8:1753-1767.
27. Yamaguchi N., Kieba I.R., Korostoff J., Howard P.S., Shenker B.J., Lally E.T. Maintenance of oxidative phosphorylation protects cells from Actinobacillus actinomycetemcomitans leukotoxin-induced apoptosis. Cell Microbiol 2001, 3:811-823.
28. Mangan D.F., Taichman N.S., Lally E.T., Wahl S.M. Lethal effects of Actinobacillus actinomycetemcomitans leukotoxin on human T lymphocytes. Infect Immun 1991, 59:3267-3272.
29. Korostoff J., Wang J.F., Kieba I., Miller M., Shenker B.J., Lally E.T. Actinobacillus actinomycetemcomitans leukotoxin induces apoptosis in HL-60 cells. Infect Immun 1998, 66:4474-4483.
30. Bechter O.E., Eisterer W., Dirnhofer S., et al. Expression of LFA-1 identifies different prognostic subgroups in patients with advanced follicle center lymphoma (FCL). Leuk Res 1999, 23:483-488.
31. Horst E., Radaszkiewicz T., Hooftman-den Otter A., et al. Expression of the leucocyte integrin LFA-1 (CD11a/CD18) and its ligand ICAM-1 (CD54) in lymphoid malignancies is related to lineage derivation and stage of differentiation but not to tumor grade. Leukemia 1991, 5:848-853.
32. Inghirami G., Wieczorek R., Zhu B.Y., Silber R., Dalla-Favera R., Knowles D.M. Differential expression of LFA-1 molecules in non-Hodgkin's lymphoma and lymphoid leukemia. Blood 1988, 72:1431-1434.
33. Lu C.F., Springer T.A. The alpha subunit cytoplasmic domain regulates the assembly and adhesiveness of integrin lymphocyte function-associated antigen-1. J Immunol 1997, 159:268-278.
34. Weber K.S., York M.R., Springer T.A., Klickstein L.B. Characterization of lymphocyte function-associated antigen 1 (LFA-1)-deficient T cell lines: the alphaL and beta2 subunits are interdependent for cell surface expression. J Immunol 1997, 158:273-279.
35. Isaza M.P., Chau J.T., Le A., et al. A bioluminescent HL-60 cell line to assay anti-leukaemia therapeutics under physiological conditions. Luminescence 2008, 23:17-21.
36. Simpson D.L., Berthold P., Taichman N.S. Killing of human myelomonocytic leukemia and lymphocytic cell lines by Actinobacillus actinomycetemcomitans leukotoxin. Infect Immun 1988, 56:1162-1166.
37. Taichman N.S., Wilton J.M. Leukotoxicity of an extract from Actinobacillus actinomycetemcomitans for human gingival polymorphonuclear leukocytes. Inflammation 1981, 5:1-12.
38. Tsai C.C., Shenker B.J., DiRienzo J.M., Malamud D., Taichman N.S. Extraction and isolation of a leukotoxin from Actinobacillus actinomycetemcomitans with polymyxin B. Infect Immun 1984, 43:700-705.
39. Dustin M.L., Springer T.A. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 1989, 341:619-624.
40. van Kooyk Y., van de Wiel-van Kemenade P., Weder P., Kuijpers T.W., Figdor C.G. Enhancement of LFA-1-mediated cell adhesion by triggering through CD2 or CD3 on T lymphocytes. Nature 1989, 342:811-813.
41. McCormack E., Bruserud O., Gjertsen B.T. Animal models of acute myelogenous leukaemia-development, application and future perspectives. Leukemia 2005, 19:687-706.
42. Uckun F.M. Severe combined immunodeficient mouse models of human leukemia. Blood 1996, 88:1135-1146.
43. Contag C.H., Bachmann M.H. Advances in in vivo bioluminescence imaging of gene expression. Annu Rev Biomed Eng 2002, 4:235-260.
44. Dalle S., Thieblemont C., Thomas L., Dumontet C. Monoclonal antibodies in clinical oncology. Anti-Cancer Agents Med Chem 2008, 8:523-532.
45. Dileepan T., Kachlany S.C., Balashova N.V., Patel J., Maheswaran S.K. Human CD18 is the functional receptor for Aggregatibacter actinomycetemcomitans leukotoxin. Infect Immun 2007.
46. Angelopoulou M.K., Kontopidou F.N., Pangalis G.A. Adhesion molecules in B-chronic lymphoproliferative disorders. Sem Hematol 1999, 36:178-197.
47. Mengarelli A., Zarcone D., Caruso R., et al. Adhesion molecule expression, clinical features and therapy outcome in childhood acute lymphoblastic leukemia. Leuk Lymphoma 2001, 40:625-630.
48. Pinto A., Carbone A., Gloghini A., Marotta G., Volpe R., Zagonel V. Differential expression of cell adhesion molecules in B-zone small lymphocytic lymphoma and other well-differentiated lymphocytic disorders. Cancer 1993, 72:894-904.
49. Reuss-Borst M.A., Klein G., Waller H.D., Muller C.A. Differential expression of adhesion molecules in acute leukemia. Leukemia 1995, 9:869-874.
50. Taichman N.S., McArthur W.P., Tsai C.C. Leukocidal mechanisms of Actinobacillus actinomycetemcomitans. Host-parasite interactions in periodontal diseases 1982, 261-269. American Society for Microbiology, Washington, DC. R.J. Genco, S.E. Mergenhagen (Eds.).
51. Bousvaros A., Stevens A.C., Strom T.B., Murphy J., Lamont J.T. Interleukin-2 fusion protein (DAB389IL-2) selectively targets activated human peripheral blood and lamina propria lymphocytes. Digest Dis Sci 1997, 42:1542-1548.
52. Bleeker W.K., Munk M.E., Mackus W.J., et al. Estimation of dose requirements for sustained in vivo activity of a therapeutic human anti-CD20 antibody. Br J Haematol 2008, 140:303-312.
53. Drake A.S., Brady M.T., Wang X.H., et al. Targeting 11q23 positive acute leukemia cells with high molecular weight-melanoma associated antigen-specific monoclonal antibodies. Cancer Immunol Immunother 2009, 58(3):415-427.
54. Zhong R.K., Donnenberg A.D., Shultz L.D., et al. Evaluation of monoclonal antibody-mediated anti-acute myeloid leukemia immunotherapy in a SCID/hu model. Leuk Res 1996, 20:581-589.
55. Zhou Y., Du W., Koretsky T., Bagby G.C., Pang Q. TAT-mediated intracellular delivery of NPM-derived peptide induces apoptosis in leukemic cells and suppresses leukemogenesis in mice. Blood 2008, 112:2474-2483.
56. Weldon J.E., Xiang L., Chertov O., et al. A protease-resistant immunotoxin against CD22 with greatly increased activity against CLL and diminished animal toxicity. Blood 2009, 113:3792-3800.
57. Walz G., Zanker B., Brand K., et al. Sequential effects of interleukin 2-diphtheria toxin fusion protein on T-cell activation. Proc Natl Acad Sci USA 1989, 86:9485-9488.
58. Diacovo T.G., deFougerolles A.R., Bainton D.F., Springer T.A. A functional integrin ligand on the surface of platelets: intercellular adhesion molecule-2. J Clin Investig 1994, 94:1243-1251.
59. Soligo D., Cattoretti G., Colombi M., et al. Bone marrow and tissue expression of gpIIb/IIIa, LFA-1, Mac-1 and gp150,95 glycoproteins. Eur J Haematol 1989, 42:173-181.
60. Abrami L., Fivaz M., Decroly E., et al. The pore-forming toxin proaerolysin is activated by furin. J Biol Chem 1998, 273:32656-32661.