A sequence-specific DNA binding small molecule triggers the release of immunogenic signals and phagocytosis in a model of B-cell lymphoma

Quarterly Reviews of Biophysics

Volumn 48, Issue 4, 2015, Pages 453-464

  Kang, Jeenjoo S ^a   Dervan, Peter B ^a  

^a California Institute of Technology   (United States)

Author keywords

damage associated molecular patterns; DNA binding small molecule; immunogenic cell death; necrotic cell death; Py Im Polyamide; telomere sequence

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALRETICULIN; DNA; HIGH MOBILITY GROUP B1 PROTEIN; HMGB1 PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE; NYLON; PYRROLE DERIVATIVE;

ANIMAL; B CELL LYMPHOMA; CHEMISTRY; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; IMMUNOBLOTTING; INFLAMMATION; K-562 CELL LINE; LUMINESCENCE; MACROPHAGE; METABOLISM; NECROSIS; NEOPLASM; PATHOLOGY; PHAGOCYTOSIS; SIGNAL TRANSDUCTION; TELOMERE; UPREGULATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALRETICULIN; DNA; ENZYME-LINKED IMMUNOSORBENT ASSAY; HMGB1 PROTEIN; HUMANS; IMIDAZOLES; IMMUNOBLOTTING; INFLAMMATION; K562 CELLS; LUMINESCENCE; LYMPHOMA, B-CELL; MACROPHAGES; NECROSIS; NEOPLASMS; NYLONS; PHAGOCYTOSIS; PYRROLES; SIGNAL TRANSDUCTION; TELOMERE; UP-REGULATION;

EID: 84949183500     PISSN: 00335835     EISSN: 14698994     Source Type: Journal    
DOI: 10.1017/S0033583515000104     Document Type: Article

References (50)

1. AYMERIC, L., APETOH, L., GHIRINGHELLI, F., TESNIERE, A., MARTINS, I., KROEMER, G., SMYTH, M. J. & ZITVOGEL, L. (2010). Tumor cell death and ATP release prime dendritic cells and efficient antican-cer immunity. Cancer Research 70, 855-858.
2. BAIRD, E. E. & DERVAN, P. B. (1996). Solid phase synthesis of polya-mides containing imidazole and pyrrole amino acids. Journal of the American Chemical Society 118, 6141-6146.
3. CHAO, M. P., JAISWAL, S., WEISSMAN-TSUKAMOTO, R., ALIZADEH, A. A., GENTLES, A.J., VOLKMER, J., WEISKOPF, K., WILLINGHAM, S.B., RAVEH, T., PARK, C.Y., MAJETI, R. & WEISSMAN, I.L. (2010). Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Science Translational Medicine 2, 63ra94.
4. DERVAN, P. B. & EDELSON, B. S. (2003). Recognition of the DNA minor groove by pyrrole-imidazole polyamides. Current Opinion in Structural Biology 13, 284-299.
5. DUNN, G. P., OLD, L. J. & SCHREIBER, R. D. (2004a). The three Es of cancer immunoediting. Annual Review of Immunology 22, 329-360.
6. DUNN, G. P., OLD, L. J. & SCHREIBER, R. D. (2004b). The immunobiol-ogy of cancer immunosurveillance and immunoediting. Immunity 21, 137-148.
7. EGGERMONT, A., ROBERT, C., SORIA, J. C. & ZITVOGEL, L. (2014). Harnessing the immune system to provide long-term survival in patients with melanoma and other solid tumors. Oncoimmunology 3, e27560.
8. GASSER, S., ORSULIC, S., BROWN, E. J. & RAULET, D.H. (2005). The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436, 1186-1190.
9. GUERRIERO, J. L., DITSWORTH, D., CATANZARO, J. M., SABINO, G., FURIE, M. B., KEW, R. R., CRAWFORD, H. C. & ZONG, W-X. (2011). DNA alkylating therapy induces tumor regression through an HMGB1-mediated activation of innate immunity. Journal of Immunology 186, 3517-3526.
10. HANAHAN, D. & WEINBERG, R. A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
11. HSU, C. F., PHILLIPS, J. W., TRAUGER, J. W., FARKAS, M. E., BELITSKY, J. M., HECKEL, A., OLENYUK, B.Z., PUCKETT, J.W., WANG, C.C. & DERVAN, P. B. (2007). Completion of a programmable DNA-binding small molecule library. Tetrahedron 63, 6146-6151.
12. IDZKO, M., DICHMANN, S., FERRARI, D., DI VIRGILIO, F., LA SALA, A., GIAMPIERO, G., PANTHER, E. & NORGAUER, J. (2002). Nucleotides induce chemotaxis and actin polymerization in immature but not mature human dendritic cells via activation of pertussis toxin-sensitive P2y receptors. Blood 100, 925-932.
13. JAISWAL, S., CHAO, M.P., MAJETI, R. & WEISSMAN, I.L. (2010). Macrophages as mediators of tumor immunosurveillance. Trends in Immunology 31, 212-219.
14. KACZMAREK, A., VANDENABEELE, P. & KRYSKO, D.V. (2013). Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity 38, 209-223.
15. KANG, J. S., MEIER, J. L. & DERVAN, P. B. (2014). Design of sequence-specific DNA binding molecules for DNA methyltransferase inhibition. Journal of the American Chemical Society 136, 3687-3694.
16. KAWAMOTO, Y., BANDO, T., KAMADA, F., LI, Y., HASHIYA, K., MAESHIMA, K. & SUGIYAMA, H. (2013). Development of a new method for synthesis of tandem hairpin pyrrole-imidazole polyamide probes targeting human telomeres. Journal of the American Chemical Society 135, 16468-16477.
17. KEPP, O., GALLUZZI, L., MARTINS, I., SCHLEMMER, F., ADJEMIAN, S., MICHAUD, M., SUKKURWALA, A.Q., MENGER, L., ZITVOGEL, L. & KROEMER, G. (2011). Molecular determinants of immunogenic cell death elicited by anticancer chemotherapy. Cancer Metastasis Reviews 30, 61-69.
18. KIELKOPF, C.L., BAIRD, E. E., DERVAN, P. B. & REES, D.C. (1998a). Structural basis for G.C recognition in the DNA minor groove. Nature Structural Biology 5, 104-109.
19. KIELKOPF, C. L., WHITE, S., SZEWCZYK, J. W., TURNER, J. M., BAIRD, E. E., DERVAN, P. B. & REES, D. C. (1998b). A structural basis for recognition of A•T and T•A base pairs in the minor groove of B-DNA. Science 282, 111-115.
20. KOEBEL, C. M., VERMI, W., SWANN, J. B., ZERAFA, N., RODIG, S. J., OLD, L. J., SMYTH, M. J. & SCHREIBER, R. D. (2007). Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450, 903-907.
21. LIPPINCOTT-SCHWARTZ, J., YUAN, L. C., BONIFACINO, J. S. & KLAUSNER, R. D. (1989). Rapid redistribution of Golgi proteins into the ER in cells treated with Brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801-813.
22. MAESHIMA, K., JANSSEN, S. & LAEMMLI, U. K. (2001). Specific targeting of insect and vertebrate telomeres with pyrrole and imidazole polyamides. The EMBO Journal 20, 3218-3228.
23. MARTÍNEZ, T.F., PHILLIPS, J.W., KARANJA, K.K., POLACZEK, P., WANG, C.-M., LI, B.C., CAMPBELL, J.L. & DERVAN, P.B. (2015). Replication stress by Py-Im polyamides induces a non-canonical ATR-dependent checkpoint response. Nucleic Acids Research 42, 11546-11559.
24. MATZINGER, P. (2002). The danger model: a renewed sense of self. Science 296, 301-305.
25. MEIER, J. L., YU, A. S., KORF, I., SEGAL, D. J. & DERVAN, P. B. (2012). Guiding the design of synthetic DNA-binding molecules with massively parallel sequencing. Journal of the American Chemical Society 134, 17814-17822.
26. MICHALAK, M., GROENENDYK, J., SZABO, E., GOLD, L.I. & OPAS, M. (2009). Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. The Biochemical Journal 417, 651-666.
27. MRKSICH, M., PARKS, M. E. & DERVAN, P. B. (1994). Hairpin peptide motif. A new class of oligopeptides for sequence-specific recognition in the minor groove of double-helical DNA. Journal of the American Chemical Society 116, 7983-7988.
28. NICKOLS, N. G. & DERVAN, P. B. (2007). Suppression of androgen receptor-mediated gene expression by a sequence-specific DNA-binding polyamide. Proceedings of the National Academy of Sciences of the United States of America 104, 10418-10423.
29. NICKOLS, N. G., JACOBS, C. S., FARKAS, M. E. & DERVAN, P. B. (2007). Modulating hypoxia-inducible transcription by disrupting the HIF-1-DNA interface. ACS Chemical Biology 2, 561-571.
30. NICKOLS, N.G., SZABLOWSKI, J.O., HARGROVE, A.E., LI, B.C., RASKATOV, J. A. & DERVAN, P. B. (2013). Activity of a Py-Im poly-amide targeted to the estrogen response element. Molecular Cancer Therapeutics 12, 675-684.
31. OBEID, M., TESNIERE, A., GHIRINGHELLI, F., FIMIA, G. M., APETOH, L., PERFETTINI, J.L., CASTEDO, M., MIGNOT, G., PANARETAKIS, T., CASARES, N., MÉTIVIER, D., LAROCHETTE, N., VAN ENDERT, P., CICCOSANTI, F., PIACENTINI, M., ZITVOGEL, L. & KROEMER, G. (2007). Calreticulin exposure dictates the immunogenicity of cancer cell death. Nature Medicine 13, 54-61.
32. O'SULLIVAN, T., SADDAWI-KONEFKA, R., VERMI, W., KOEBEL, C.M., ARTHUR, C., WHITE, J. M., UPPALURI, R., ANDREWS, D. M., NGIOW, S. F., TENG, M.W., SMYTH, M.J., SCHREIBER, R.D. & BUI, J.D. (2012). Cancer immunoediting by the innate immune system in the absence of adaptive immunity. The Journal of Experimental Medicine 209, 1869-1882.
33. PANARETAKIS, T., KEPP, O., BROCKMEIER, U., TESNIERE, A., BJORKLUND, A. C., CHAPMAN, D. C., DURCHSCHLAG, M., JOZA, N., PIERRON, G., VAN ENDERT, P., YUAN, J., ZITVOGEL, L., MADEO, F., WILLIAMS, D. B. & KROEMER, G. (2009). Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. The EMBO Journal 28, 578-590.
34. PETERS, L. R. & RAGHAVAN, M. (2011). Endoplasmic reticulum calcium depletion impacts chaperone secretion, innate immunity, and phagocytic uptake of cells. Journal of Immunology 187, 919-931.
35. PILCH, D. S., POKLAR, N., GELFAND, C. A., LAW, S. M., BRESLAUER, K. J., BAIRD, E. E. & DERVAN, P. B. (1996). Binding of a hairpin polyam-ide in the minor groove of DNA: sequence-specific enthalpic discrimination. Proceedings of the National Academy of Sciences of the United States of America 93, 8306-8311.
36. PUCKETT, J. W., GREEN, J. T. & DERVAN, P. B. (2012). Microwave assisted synthesis of Py-Im polyamides. Organic Letters 14, 2774-2777.
37. RASKATOV, J. A., MEIER, J. L., PUCKETT, J. W., YANG, F., RAMAKRISHNAN, P. & DERVAN, P. B. (2012). Modulation of NF-κB-dependent gene transcription using programmable DNA minor groove binders. Proceedings of the National Academy of Sciences of the United States of America 109, 1023-1028.
38. ROVERE-QUERINI, P., CAPOBIANCO, A., SCAFFIDI, P., VALENTINIS, B., CATALANOTTI, F., GIAZZON, M., DUMITRIU, I.E., MÜLLER, S., IANNACONE, M., TRAVERSARI, C., BIANCHI, M.E. & MANFREDI, A. A. (2004). HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Reports 5, 825-830.
39. RUBARTELLI, A. & LOTZE, M. T. (2007). Inside, outside, upside down: damage-associated molecular-pattern molecules (DAMPs) and redox. Trends in Immunology 28, 429-436.
40. SCHREIBER, R. D., OLD, L. J. & SMYTH, M. J. (2011). Cancer immunoe-diting: integrating immunity's roles in cancer suppression and promotion. Science Signalling 331, 1565.
41. SWALLEY, S. E., BAIRD, E. E. & DERVAN, P. B. (1996). Recognition of a 5'-(A, T)GGG(A, T)2-3' Sequence in the minor groove of DNA by an eight-ring hairpin polyamide. Journal of the American Chemical Society 118, 8198-8206.
42. TRAUGER, J. W., BAIRD, E. E. & DERVAN, P. B. (1996). Recognition of DNA by designed ligands at subnanomolar concentrations. Nature 382, 559-561.
43. TSENG, D., VOLKMER, J. P., WILLINGHAM, S. B., CONTRERAS-TRUJILLO, H., FATHMAN, J. W., FERNHOFF, N. B., SEITA, J., INLAY, M. A., WEISKOPF, K., MIYANISHI, M. & WEISSMAN, I. L. (2013). Anti-CD47 antibody-mediated phagocytosis of cancer by macrophages primes an effective antitumor T-cell response. Proceedings of the National Academy of Sciences of the United States of America 110, 11103-11108.
44. TUFI, R., PANARETAKIS, T., BIANCHI, K., CRIOLLO, A., FAZI, B., DI SANO, F., TESNIERE, A., KEPP, O., PATERLINI-BRECHOT, P., ZITVOGEL, L., PIACENTINI, M., SZABADKAI, G. & KROEMER, G. (2008). Reduction of endoplasmic reticulum Ca2+ levels favors plasma membrane surface exposure of calreticulin. Cell Death and Differentiation 15, 274-282.
45. WADE, W. S., MRKSICH, M. & DERVAN, P. B. (1992). Design of pep-tides that bind in the minor groove of DNA at 5′-(A, T)G(A, T) C(A, T)-3′ sequences by a dimeric side-by-side motif. Journal of the American Chemical Society 114, 8783-8794.
46. WHITE, S., BAIRD, E. E. & DERVAN, P. B. (1997). On the pairing rules for recognition in the minor groove of DNA by pyrrole-imidazole polyamides. Chemistry & Biology 4, 569-578.
47. WHITE, S., SZEWCZYK, J. W., TURNER, J. M., BAIRD, E. E. & DERVAN, P. B. (1998). Recognition of the four Watson-Crick base pairs in the DNA minor groove by synthetic ligands. Nature 391, 468-471.
48. YANG, F., NICKOLS, N.G., LI, B.C., MARINOV, G.K., SAID, J.W. & DERVAN, P. B. (2013). Antitumor activity of a pyrrole-imidazole polyamide. Proceedings of the National Academy of Sciences of the United States of America 110, 1863-1868.
49. ZITVOGEL, L., APETOH, L., GHIRINGHELLI, F. & KROEMER, G. (2008). Immunological aspects of cancer chemotherapy. Nature Reviews. Immunology 8, 59-73.
50. ZITVOGEL, L., KEPP, O. & KROEMER, G. (2010). Decoding cell death signals in inflammation and immunity. Cell 140, 798-804.