Extensive peptide and natural protein substrate screens reveal that mouse caspase-11 has much narrower substrate specificity than caspase-1

Journal of Biological Chemistry

Volumn 293, Issue 18, 2018, Pages 7058-7067

  Gonzalez Ramirez, Monica L ^a   Poreba, Marcin ^a,b   Snipas, Scott J ^a   Groborz, Katarzyna ^b   Drag, Marcin ^b   Salvesen, Guy S ^a  

^a BURNHAM INSTITUTE   (United States)

^b WROCLAW UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; PROTEINS;

INFLAMMATORY CELLS; INFLAMMATORY MEDIATORS; LIMITED PROTEOLYSIS; NATURAL PROTEINS; NATURAL SUBSTRATES; PATHOGENIC INFECTIONS; PROTEIN SUBSTRATE; SUBSTRATE SPECIFICITY;

SUBSTRATES;

CASPASE 11; GASDERMIN D; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEIN PRECURSOR; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; AUTACOID; CASP1 PROTEIN, MOUSE; CASP11 PROTEIN, MOUSE; CASPASE; CYTOKINE; GSDMD PROTEIN, MOUSE; INTERLEUKIN 10; PEPTIDE; RECOMBINANT PROTEIN;

CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYROPTOSIS; REVIEW; ANIMAL; CELL DEATH; METABOLISM; MOUSE; PROTEIN DEGRADATION;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CASPASE 1; CASPASES; CELL DEATH; CYTOKINES; INFLAMMATION MEDIATORS; INTERLEUKIN-10; INTERLEUKIN-1BETA; MICE; PEPTIDES; PROTEOLYSIS; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 85046620741     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.RA117.001329     Document Type: Review

References (57)

1. Kayagaki, N., Warming, S., Lamkanfi, M., Vande Walle, L., Louie, S., Dong, J., Newton, K., Qu, Y., Liu, J., Heldens, S., Zhang, J., Lee, W. P., Roose-Girma, M., and Dixit, V. M. (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479, 117–121 CrossRef Medline
2. Lamkanfi, M., and Dixit, V. M. (2014) Mechanisms and functions of inflammasomes. Cell 157, 1013–1022 CrossRef Medline
3. Viganò, E., Diamond, C. E., Spreafico, R., Balachander, A., Sobota, R. M., and Mortellaro, A. (2015) Human caspase-4 and caspase-5 regulate the one-step non-canonical inflammasome activation in monocytes. Nat. Commun. 6, 8761 CrossRef Medline
4. Yang, J., Zhao, Y., and Shao, F. (2015) Non-canonical activation of inflammatory caspases by cytosolic LPS in innate immunity. Curr. Opin. Immunol. 32, 78 – 83 CrossRef Medline
5. Martinon, F., and Tschopp, J. (2004) Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 117, 561–574 CrossRef Medline
6. Zamboni, D. S., and Lima-Junior, D. S. (2015) Inflammasomes in host response to protozoan parasites. Immunol. Rev. 265, 156–171 CrossRef Medline
7. Hagar, J. A., Powell, D. A., Aachoui, Y., Ernst, R. K., and Miao, E. A. (2013) Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341, 1250 –1253 CrossRef Medline
8. Shi, J., Zhao, Y., Wang, Y., Gao, W., Ding, J., Li, P., Hu, L., and Shao, F. (2014) Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514, 187–192 CrossRef Medline
9. Renatus, M., Stennicke, H. R., Scott, F. L., Liddington, R. C., and Salvesen, G. S. (2001) Dimer formation drives the activation of the cell death protease caspase 9. Proc. Natl. Acad. Sci. U.S.A. 98, 14250 –14255 CrossRef Medline
10. Boatright, K. M., and Salvesen, G. S. (2003) Mechanisms of caspase activation. Curr. Opin. Cell Biol. 15, 725–731 CrossRef Medline
11. Aglietti, R. A., Estevez, A., Gupta, A., Ramirez, M. G., Liu, P. S., Kayagaki, N., Ciferri, C., Dixit, V. M., and Dueber, E. C. (2016) GsdmD p30 elicited by caspase-11 during pyroptosis forms pores in membranes. Proc. Natl. Acad. Sci. U.S.A. 113, 7858 –7863 CrossRef Medline
12. Ding, J., Wang, K., Liu, W., She, Y., Sun, Q., Shi, J., Sun, H., Wang, D. C., and Shao, F. (2016) Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535, 111–116 CrossRef Medline
13. Liu, X., Zhang, Z., Ruan, J., Pan, Y., Magupalli, V. G., Wu, H., and Lieberman, J. (2016) Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535, 153–158 CrossRef Medline
14. Sborgi, L., Rühl, S., Mulvihill, E., Pipercevic, J., Heilig, R., Stahlberg, H., Farady, C. J., Müller, D. J., Broz, P., and Hiller, S. (2016) GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J. 35, 1766 –1778 CrossRef Medline
15. Salvesen, G. S., Hempel, A., and Coll, N. S. (2016) Protease signaling in animal and plant-regulated cell death. FEBS J. 283, 2577–2598 CrossRef Medline
16. Black, R. A., Kronheim, S. R., Merriam, J. E., March, C. J., and Hopp, T. P. (1989) A pre-aspartate-specific protease from human leukocytes that cleaves pro-interleukin-1b. J. Biol. Chem. 264, 5323–5326 Medline
17. Kostura, M. J., Tocci, M. J., Limjuco, G., Chin, J., Cameron, P., Hillman, A. G., Chartrain, N. A., and Schmidt, J. A. (1989) Identification of a monocyte specific pre-interleukin 1b convertase activity. Proc. Natl. Acad. Sci. U.S.A. 86, 5227–5231 CrossRef Medline
18. Howard, A. D., Kostura, M. J., Thornberry, N., Ding, G. J., Limjuco, G., Weidner, J., Salley, J. P., Hogquist, K. A., Chaplin, D. D., Mumford, R. A., Schmidt, J. A., and Tocci, M. J. (1991) IL-1 converting enzyme requires aspartic acid residues for processing of the IL-1b precursor at two distinct sites and does not cleave 31-kDa IL-1a. J. Immunol. 147, 2964 –2969 Medline
19. Brough, D., and Rothwell, N. J. (2007) Caspase-1-dependent processing of pro-interleukin-1 is cytosolic and precedes cell death. J. Cell Sci. 120, 772–781 CrossRef Medline
20. Ghayur, T., Banerjee, S., Hugunin, M., Butler, D., Herzog, L., Carter, A., Quintal, L., Sekut, L., Talanian, R., Paskind, M., Wong, W., Kamen, R., Tracey, D., and Allen, H. (1997) Caspase-1 processes IFN--inducing factor and regulates LPS-induced IFN- production. Nature 386, 619 – 623 CrossRef Medline
21. Gu, Y., Kuida, K., Tsutsui, H., Ku, G., Hsiao, K., Fleming, M. A., Hayashi, N., Higashino, K., Okamura, H., Nakanishi, K., Kurimoto, M., Tanimoto, T., Flavell, R. A., Sato, V., Harding, M. W., Livingston, D. J., and Su, M. S. (1997) Activation of interferon- inducing factor mediated by interleukin-1 converting enzyme. Science 275, 206 –209 CrossRef Medline
22. Kuida, K., Lippke, J. A., Ku, G., Harding, M. W., Livingston, D. J., Su, M. S., and Flavell, R. A. (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1-beta converting enzyme. Science 267, 2000 –2003 CrossRef Medline
23. Auron, P. E., Warner, S. J., Webb, A. C., Cannon, J. G., Bernheim, H. A., McAdam, K. J., Rosenwasser, L. J., LoPreste, G., Mucci, S. F., and Dinarello, C. A. (1987) Studies on the molecular nature of human interleukin 1. J. Immunol. 138, 1447–1456 Medline
24. Kayagaki, N., Stowe, I. B., Lee, B. L., O’Rourke, K., Anderson, K., Warming, S., Cuellar, T., Haley, B., Roose-Girma, M., Phung, Q. T., Liu, P. S., Lill, J. R., Li, H., Wu, J., Kummerfeld, S., et al. (2015) Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526, 666 – 671 CrossRef Medline
25. Shi, J., Zhao, Y., Wang, K., Shi, X., Wang, Y., Huang, H., Zhuang, Y., Cai, T., Wang, F., and Shao, F. (2015) Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526, 660 – 665 CrossRef Medline
26. Poreba, M., and Drag, M. (2010) Current strategies for probing substrate specificity of proteases. Curr. Med. Chem. 17, 3968 –3995 Medline
27. Rano, T. A., Timkey, T., Peterson, E. P., Rotonda, J., Nicholson, D. W., Becker, J. W., Chapman, K. T., and Thornberry, N. A. (1997) A combinatorial approach for determining protease specificities: application to interleukin-1b converting enzyme (ICE). Chem. Biol. 4, 149 –155 CrossRef Medline
28. Thornberry, N. A., Rano, T. A., Peterson, E. P., Rasper, D. M., Timkey, T., Garcia-Calvo, M., Houtzager, V. M., Nordstrom, P. A., Roy, S., Vaillancourt, J. P., Chapman, K. T., and Nicholson, D. W. (1997) A combinatorial approach defines specificities of members of the caspase family and gran-zyme B. Functional relationships established for key mediators of apoptosis. J. Biol. Chem. 272, 17907–17911 CrossRef Medline
29. Poreba, M., Szalek, A., Kasperkiewicz, P., Rut, W., Salvesen, G. S., and Drag, M. (2015) Small molecule active site directed tools for studying human caspases. Chem. Rev. 115, 12546 –12629 CrossRef Medline
30. Harris, J. L., Backes, B. J., Leonetti, F., Mahrus, S., Ellman, J. A., and Craik, C. S. (2000) Rapid and general profiling of protease specificity by using combinatorial fluorogenic substrate libraries. Proc. Natl. Acad. Sci. U.S.A. 97, 7754 –7759 CrossRef Medline
31. Poreba, M., Salvesen, G. S., and Drag, M. (2017) Synthesis of a HyCoSuL peptide substrate library to dissect protease substrate specificity. Nat. Protoc. 12, 2189 –2214 CrossRef Medline
32. Poreba, M., Kasperkiewicz, P., Snipas, S. J., Fasci, D., Salvesen, G. S., and Drag, M. (2014) Unnatural amino acids increase sensitivity and provide for the design of highly selective caspase substrates. Cell Death Differ. 21, 1482–1492 CrossRef Medline
33. Shen, W., Yun, S., Tam, B., Dalal, K., and Pio, F. F. (2005) Target selection of soluble protein complexes for structural proteomics studies. Proteome Sci. 3, 3 CrossRef Medline
34. Burgess, R. R. (2009) Refolding solubilized inclusion body proteins. Methods Enzymol. 463, 259 –282 CrossRef Medline
35. Garcia-Calvo, M., Peterson, E. P., Rasper, D. M., Vaillancourt, J. P., Zamboni, R., Nicholson, D. W., and Thornberry, N. A. (1999) Purification and catalytic properties of human caspase family members. Cell Death Diff. 6, 362–369 CrossRef
36. Ng, N. M., Pike, R. N., and Boyd, S. E. (2009) Subsite cooperativity in protease specificity. Biol. Chem. 390, 401– 407 Medline
37. Poreba, M., Szalek, A., Rut, W., Kasperkiewicz, P., Rutkowska-Wlodarc-zyk, I., Snipas, S. J., Itoh, Y., Turk, D., Turk, B., Overall, C. M., Kaczmarek, L., Salvesen, G. S., and Drag, M. (2017) Highly sensitive and adaptable fluorescence-quenched pair discloses the substrate specificity profiles in diverse protease families. Sci. Rep. 7, 43135 CrossRef Medline
38. Lechtenberg, B. C., Kasperkiewicz, P., Robinson, H., Drag, M., and Riedl, S. J. (2015) The elastase-PK101 structure: mechanism of an ultrasensitive activity-based probe revealed. ACS Chem. Biol. 10, 945–951 CrossRef Medline
39. He, Y., Hara, H., and Núñez, G. (2016) Mechanism and regulation of NLRP3 inflammasome activation. Trends Biochem. Sci. 41, 1012–1021 CrossRef Medline
40. Sleath, P. R., Hendrickson, R. C., Kronheim, S. R., March, C. J., and Black, R. A. (1990) Substrate specificity of the protease that processes human interleukin-1b. J. Biol. Chem. 265, 14526 –14528 Medline
41. Thornberry, N. A., Bull, H. G., Calaycay, J. R., Chapman, K. T., Howard, A. D., Kostura, M. J., Miller, D. K., Molineaux, S. M., Weidner, J. R., Aunins, J., Elliston, K. O., Ayala, J. M., Casano, F. J., Chin, J., Ding, G. J., et al. (1992) A novel heterodimeric cysteine protease is required for interleukin-1 processing in monocytes. Nature 356, 768 –774 CrossRef Medline
42. Thornberry, N. A., and Molineaux, S. M. (1995) Interleukin-1b converting enzyme: A novel cysteine protease required for IL-1b production and implicated in programmed cell death. Protein Sci. 4, 3–12 Medline
43. Kang, S. J., Wang, S., Hara, H., Peterson, E. P., Namura, S., Amin-Hanjani, S., Huang, Z., Srinivasan, A., Tomaselli, K. J., Thornberry, N. A., Moskow-itz, M. A., and Yuan, J. (2000) Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions. J. Cell Biol. 149, 613– 622 CrossRef Medline
44. Fenton, J. W., 2nd, Olson, T. A., Zabinski, M. P., and Wilner, G. D. (1988) Anion-binding exosite of human -thrombin and fibrin(ogen) recognition. Biochemistry 27, 7106 –7112 CrossRef Medline
45. Overall, C. M. (2002) Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol. Biotechnol. 22, 51– 86 CrossRef Medline
46. Drag, M., and Salvesen, G. S. (2008) DeSUMOylating enzymes–SENPs. IUBMB Life 60, 734 –742 CrossRef Medline
47. Boucher, D., Blais, V., and Denault, J. B. (2012) Caspase-7 uses an exosite to promote poly(ADP ribose) polymerase 1 proteolysis. Proc. Natl. Acad. Sci. U.S.A. 109, 5669 –5674 CrossRef Medline
48. Sharma, V., Panwar, P., O’Donoghue, A. J., Cui, H., Guido, R. V., Craik, C. S., and Brömme, D. (2015) Structural requirements for the collagenase and elastase activity of cathepsin K and its selective inhibition by an exosite inhibitor. Biochem. J. 465, 163–173 CrossRef Medline
49. Schmid-Burgk, J. L., Gaidt, M. M., Schmidt, T., Ebert, T. S., Bartok, E., and Hornung, V. (2015) Caspase-4 mediates non-canonical activation of the NLRP3 inflammasome in human myeloid cells. Eur. J. Immunol. 45, 2911–2917 CrossRef Medline
50. Baker, P. J., Boucher, D., Bierschenk, D., Tebartz, C., Whitney, P. G., D’Silva, D. B., Tanzer, M. C., Monteleone, M., Robertson, A. A., Cooper, M. A., Alvarez-Diaz, S., Herold, M. J., Bedoui, S., Schroder, K., and Masters, S. L. (2015) NLRP3 inflammasome activation downstream of cytoplasmic LPS recognition by both caspase-4 and caspase-5. Eur. J. Immunol. 45, 2918 –2926 CrossRef Medline
51. Rühl, S., and Broz, P. (2015) Caspase-11 activates a canonical NLRP3 inflammasome by promoting K efflux. Eur. J. Immunol. 45, 2927–2936 CrossRef Medline
52. Taabazuing, C. Y., Okondo, M. C., and Bachovchin, D. A. (2017) Pyroptosis and apoptosis pathways engage in bidirectional crosstalk in monocytes and macrophages. Cell Chem. Biol. 24, 507–514 CrossRef Medline
53. Akita, K., Ohtsuki, T., Nukada, Y., Tanimoto, T., Namba, M., Okura, T., Takakura-Yamamoto, R., Torigoe, K., Gu, Y., Su, M. S., Fujii, M., Satoh-Itoh, M., Yamamoto, K., Kohno, K., Ikeda, M., and Kurimoto, M. (1997) Involvement of caspase-1 and caspase-3 in the production and processing of mature human interleukin 18 in monocytic THP.1 cells. J. Biol. Chem. 272, 26595–26603 CrossRef Medline
54. Afonina, I. S., Müller, C., Martin, S. J., and Beyaert, R. (2015) Proteolytic processing of interleukin-1 family cytokines: variations on a common theme. Immunity 42, 991–1004 CrossRef Medline
55. Denault, J. B., and Salvesen, G. S. (2003) Expression, purification, and characterization of caspases. Curr. Protoc. Protein Sci. Chapter 21, Unit 21 13 CrossRef Medline
56. Stennicke, H. R., and Salvesen, G. S. (2000) Caspase assays. Methods Enzymol. 322, 91–100 CrossRef Medline
57. Pop, C., Salvesen, G. S., and Scott, F. L. (2008) Caspase assays: identifying caspase activity and substrates in vitro and in vivo. Methods Enzymol. 446, 351–367 CrossRef Medline