NK cell maturation and cytotoxicity are controlled by the intramembrane aspartyl protease SPPL3

Journal of Immunology

Volumn 196, Issue 6, 2016, Pages 2614-2626

  Hamblet, Corinne E ^a   Makowski, Stefanie L ^a   Tritapoe, Julia M ^a   Pomerantz, Joel L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC PROTEINASE; PROTEIN SPPL3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL COUNT; CELL DIFFERENTIATION; CELL MATURATION; CELL POPULATION; CELL SIZE; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; EXON; IMMUNE RESPONSE; INNATE IMMUNITY; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN TARGETING; SPLEEN CELL; T LYMPHOCYTE; ANIMAL; C57BL MOUSE; CELL MEMBRANE; CYTOLOGY; ENZYMOLOGY; FEMALE; FLOW CYTOMETRY; GENE TARGETING; IMMUNOLOGY; MALE; POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; ASPARTIC ACID PROTEASES; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL MEMBRANE; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; FLOW CYTOMETRY; GENE KNOCK-IN TECHNIQUES; IMMUNITY, INNATE; KILLER CELLS, NATURAL; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; POLYMERASE CHAIN REACTION;

EID: 84962557679     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501970     Document Type: Article

References (32)

1. Vivier, E., E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini. 2008. Functions of natural killer cells. Nat. Immunol. 9:503-510.
2. Lodolce, J. P., D. L. Boone, S. Chai, R. E. Swain, T. Dassopoulos, S. Trettin, and A. Ma. 1998. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9:669-676.
3. Kennedy, M. K., M. Glaccum, S. N. Brown, E. A. Butz, J. L. Viney, M. Embers, N. Matsuki, K. Charrier, L. Sedger, C. R. Willis, et al. 2000. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 191:771-780.
4. Gordon, S. M., J. Chaix, L. J. Rupp, J. Wu, S. Madera, J. C. Sun, T. Lindsten, and S. L. Reiner. 2012. The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 36:55-67.
5. Huntington, N. D., C. A. J. Vosshenrich, and J. P. Di Santo. 2007. Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat. Rev. Immunol. 7:703-714.
6. Chiossone, L., J. Chaix, N. Fuseri, C. Roth, E. Vivier, and T. Walzer. 2009. Maturation of mouse NK cells is a 4-stage developmental program. Blood 113:5488-5496.
7. Hayakawa, Y., and M. J. Smyth. 2006. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 176:1517-1524.
8. Narni-Mancinelli, E., J. Chaix, A. Fenis, Y. M. Kerdiles, N. Yessaad, A. Reynders, C. Gregoire, H. Luche, S. Ugolini, E. Tomasello, et al. 2011. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl. Acad. Sci. USA 108:18324-18329.
9. Kim, S., K. Iizuka, H.-S. P. Kang, A. Dokun, A. R. French, S. Greco, and W. M. Yokoyama. 2002. In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 3:523-528.
10. Friedmann, E., M. K. Lemberg, A. Weihofen, K. K. Dev, U. Dengler, G. Rovelli, and B. Martoglio. 2004. Consensus analysis of signal peptide peptidase and homologous human aspartic proteases reveals opposite topology of catalytic domains compared with presenilins. J. Biol. Chem. 279:50790-50798.
11. Voss, M., B. Schröder, and R. Fluhrer. 2013. Mechanism, specificity, and physiology of signal peptide peptidase (SPP) and SPP-like proteases. Biochim. Biophys. Acta 1828:2828-2839.
12. Lemberg, M. K., F. A. Bland, A. Weihofen, V. M. Braud, and B. Martoglio. 1950-2001. Intramembrane proteolysis of signal peptides: an essential step in the generation of HLA-E epitopes. J. Immunol. Baltim. Md 167:6441-6446.
13. Weihofen, A., K. Binns, M. K. Lemberg, K. Ashman, and B. Martoglio. 2002. Identification of signal peptide peptidase, a presenilin-type aspartic protease. Science 296:2215-2218.
14. El Hage, F., V. Stroobant, I. Vergnon, J.-F. Baurain, H. Echchakir, V. Lazar, S. Chouaib, P. G. Coulie, and F. Mami-Chouaib. 2008. Preprocalcitonin signal peptide generates a cytotoxic T lymphocyte-defined tumor epitope processed by a proteasome-independent pathway. Proc. Natl. Acad. Sci. USA 105:10119-10124.
15. Beisner, D. R., P. Langerak, A. E. Parker, C. Dahlberg, F. J. Otero, S. E. Sutton, L. Poirot, W. Barnes, M. A. Young, S. Niessen, et al. 2013. The intramembrane protease Sppl2a is required for B cell and DC development and survival via cleavage of the invariant chain. J. Exp. Med. 210:23-30.
16. Bergmann, H., M. Yabas, A. Short, L. Miosge, N. Barthel, C. E. Teh, C. M. Roots, K. R. Bull, Y. Jeelall, K. Horikawa, et al. 2013. B cell survival, surface BCR and BAFFR expression, CD74 metabolism, and CD8-dendritic cells require the intramembrane endopeptidase SPPL2A. J. Exp. Med. 210:31-40.
17. Schneppenheim, J., R. Dressel, S. Hüttl, R. Lüllmann-Rauch, M. Engelke, K. Dittmann, J. Wienands, E.-L. Eskelinen, I. Hermans-Borgmeyer, R. Fluhrer, et al. 2013. The intramembrane protease SPPL2a promotes B cell development and controls endosomal traffic by cleavage of the invariant chain. J. Exp. Med. 210:41-58.
18. Lückerath, K., V. Kirkin, I. M. Melzer, F. B. Thalheimer, D. Siele, W. Milani, T. Adler, A. Aguilar-Pimentel, M. Horsch, G. Michel, et al. 2011. Immune modulation by Fas ligand reverse signaling: lymphocyte proliferation is attenuated by the intracellular Fas ligand domain. Blood 117:519-529.
19. Friedmann, E., E. Hauben, K. Maylandt, S. Schleeger, S. Vreugde, S. F. Lichtenthaler, P.-H. Kuhn, D. Stauffer, G. Rovelli, and B. Martoglio. 2006. SPPL2a and SPPL2b promote intramembrane proteolysis of TNFalpha in activated dendritic cells to trigger IL-12 production. Nat. Cell Biol. 8:843-848.
20. Makowski, S. L., Z. Wang, and J. L. Pomerantz. 2015. A protease-independent function for SPPL3 in NFAT activation. Mol. Cell. Biol. 35:451-467.
21. Voss, M., U. Künzel, F. Higel, P.-H. Kuhn, A. Colombo, A. Fukumori, M. Haug-Kröper, B. Klier, G. Grammer, A. Seidl, et al. 2014. Shedding of glycanmodifying enzymes by signal peptide peptidase-like 3 (SPPL3) regulates cellular N-glycosylation. EMBO J. 33:2890-2905.
22. Kuhn, P.-H., M. Voss, M. Haug-Kröper, B. Schröder, U. Schepers, S. Bräse, C. Haass, S. F. Lichtenthaler, and R. Fluhrer. 2015. Secretome analysis identifies novel signal peptide peptidase-like 3 (Sppl3) substrates and reveals a role of Sppl3 in multiple Golgi glycosylation pathways. Mol. Cell. Proteomics 14:1584-1598.
23. Hayashi, S., P. Lewis, L. Pevny, and A. P. McMahon. 2002. Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech. Dev. 119(Suppl 1):S97-S101.
24. De Boer, J., A. Williams, G. Skavdis, N. Harker, M. Coles, M. Tolaini, T. Norton, K. Williams, K. Roderick, A. J. Potocnik, and D. Kioussis. 2003. Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur. J. Immunol. 33:314-325.
25. Wang, H., H. Yang, C. S. Shivalila, M. M. Dawlaty, A. W. Cheng, F. Zhang, and R. Jaenisch. 2013. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910-918.
26. Soderquest, K., N. Powell, C. Luci, N. Van Rooijen, A. Hidalgo, F. Geissmann, T. Walzer, G. M. Lord, and A. Martín-Fontecha. 2011. Monocytes control natural killer cell differentiation to effector phenotypes. Blood 117:4511-4518.
27. Jaeger, B. N., J. Donadieu, C. Cognet, C. Bernat, D. Ordoñez-Rueda, V. Barlogis, N. Mahlaoui, A. Fenis, E. Narni-Mancinelli, B. Beaupain, et al. 2012. Neutrophil depletion impairs natural killer cell maturation, function, and homeostasis. J. Exp. Med. 209:565-580.
28. Laplante, M., and D. M. Sabatini. 2012. mTOR signaling in growth control and disease. Cell 149:274-293.
29. Marçais, A., J. Cherfils-Vicini, C. Viant, S. Degouve, S. Viel, A. Fenis, J. Rabilloud, K. Mayol, A. Tavares, J. Bienvenu, et al. 2014. The metabolic checkpoint kinase mTOR is essential for IL-15 signaling during the development and activation of NK cells. Nat. Immunol. 15:749-757.
30. Voss, M., A. Fukumori, P.-H. Kuhn, U. Künzel, B. Klier, G. Grammer, M. Haug-Kröper, E. Kremmer, S. F. Lichtenthaler, H. Steiner, et al. 2012. Foamy virus envelope protein is a substrate for signal peptide peptidase-like 3 (SPPL3). J. Biol. Chem. 287:43401-43409.
31. Cummings, R. D., and S. Kornfeld. 1982. Characterization of the structural determinants required for the high affinity interaction of asparagine-linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins. J. Biol. Chem. 257:11230-11234.
32. Cummings, R. D., and M. E. Etzler. 2009. Antibodies and lectins in glycan analysis. In Essentials of Glycobiology, 2nd Ed., A. Varki, R. D. Cummings, J. D. Esko, H. H. Freeze, P. Stanley, C. R. Bertozzi, G. W. Hart, and M. E. Etzler, eds. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, p. 633-647.