Dual proteolytic pathways govern glycolysis and immune competence

Cell

Volumn 159, Issue 7, 2014, Pages 1578-1590

  Lu, Wei ^a   Zhang, Yu ^a   McDonald, David O ^b   Jing, Huie ^a   Carroll, Bernadette ^b   Robertson, Nic ^b,c   Zhang, Qian ^a   Griffin, Helen ^b   Sanderson, Sharon ^d   Lakey, Jeremy H ^b   Morgan, Neil V ^e   Reynard, Louise N ^b   Zheng, Lixin ^a   Murdock, Heardley M ^a   Turvey, Stuart E ^f   Hackett, Scott J ^g   Prestidge, Tim ^h   Hall, Julie M ^c   Cant, Andrew J ^b,c   Matthews, Helen F ^a   Koref, Mauro F Santibanez ^b   Simon, Anna Katharina ^d   Korolchuk, Viktor I ^b   Lenardo, Michael J ^a   Hambleton, Sophie ^b,c   Su, Helen C ^a   more..

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c Infectious Diseases Allergy   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^g BIRMINGHAM HEARTLANDS HOSPITAL   (United Kingdom)

^h STARSHIP CHILDREN S HOSPITAL   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GLYCOLYTIC ENZYME HEXOKINASE 2; HEXOKINASE; INTERLEUKIN 1BETA; PEPTIDE HYDROLASE; TRIPEPTIDYL PEPTIDASE II; UNCLASSIFIED DRUG; AMINOPEPTIDASE; DIPEPTIDYL PEPTIDASE; SERINE PROTEINASE; TRIPEPTIDYL-PEPTIDASE 2;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; CELL METABOLISM; CHAPERONE-MEDIATED AUTOPHAGY; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE MUTATION; GLYCOLYSIS; HUMAN; HUMAN CELL; IMMUNOCOMPETENCE; INNATE IMMUNITY; LYSOSOME; MALE; MAMMAL CELL; MOUSE; NONHUMAN; PRESCHOOL CHILD; PROTEIN DEGRADATION; RECURRENT INFECTION; SCHOOL CHILD; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; IMMUNE DEFICIENCY; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PEDIGREE; SEQUENCE ALIGNMENT;

MAMMALIA;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; AMINOPEPTIDASES; ANIMALS; DIPEPTIDYL-PEPTIDASES AND TRIPEPTIDYL-PEPTIDASES; FEMALE; GLYCOLYSIS; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC DEFICIENCY SYNDROMES; LYSOSOMES; MALE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEDIGREE; PROTEOLYSIS; SEQUENCE ALIGNMENT; SERINE ENDOPEPTIDASES;

EID: 84919918303     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.12.001     Document Type: Article

References (50)

1. R.M. Bålöw, B. Tomkinson, U. Ragnarsson, and O. Zetterqvist Purification, substrate specificity, and classification of tripeptidyl peptidase II J. Biol. Chem. 261 1986 2409 2417
2. L. Bar-Peled, and D.M. Sabatini Regulation of mTORC1 by amino acids Trends Cell Biol. 24 2014 400 406
3. D.M. Barnes, C.C. Calvert, and K.C. Klasing Source of amino acids for tRNA acylation. Implications for measurement of protein synthesis Biochem. J. 283 1992 583 589
4. C.M. Cham, G. Driessens, J.P. O'Keefe, and T.F. Gajewski Glucose deprivation inhibits multiple key gene expression events and effector functions in CD8+ T cells Eur. J. Immunol. 38 2008 2438 2450
5. C.H. Chang, J.D. Curtis, L.B. Maggi Jr., B. Faubert, A.V. Villarino, D. O'Sullivan, S.C. Huang, G.J. van der Windt, J. Blagih, and J. Qiu Posttranscriptional control of T cell effector function by aerobic glycolysis Cell 153 2013 1239 1251
6. A. Ciechanover Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting Cell Death Differ. 12 2005 1178 1190
7. J.F. Dice Peptide sequences that target cytosolic proteins for lysosomal proteolysis Trends Biochem. Sci. 15 1990 305 309
8. B. Everts, E. Amiel, S.C. Huang, A.M. Smith, C.H. Chang, W.Y. Lam, V. Redmann, T.C. Freitas, J. Blagih, and G.J. van der Windt TLR-driven early glycolytic reprogramming via the kinases TBK1-IKKε supports the anabolic demands of dendritic cell activation Nat. Immunol. 15 2014 323 332
9. R. Gavioli, T. Frisan, S. Vertuani, G.W. Bornkamm, and M.G. Masucci c-myc overexpression activates alternative pathways for intracellular proteolysis in lymphoma cells Nat. Cell Biol. 3 2001 283 288
10. T.R. Gershon, A.J. Crowther, A. Tikunov, I. Garcia, R. Annis, H. Yuan, C.R. Miller, J. Macdonald, J. Olson, and M. Deshmukh Hexokinase-2-mediated aerobic glycolysis is integral to cerebellar neurogenesis and pathogenesis of medulloblastoma Cancer Metab. 1 2013 2
11. M.S. Goyal, M. Hawrylycz, J.A. Miller, A.Z. Snyder, and M.E. Raichle Aerobic glycolysis in the human brain is associated with development and neotenous gene expression Cell Metab. 19 2014 49 57
12. E.F. Greiner, M. Guppy, and K. Brand Glucose is essential for proliferation and the glycolytic enzyme induction that provokes a transition to glycolytic energy production J. Biol. Chem. 269 1994 31484 31490
13. J. Huai, E. Firat, A. Nil, D. Million, S. Gaedicke, B. Kanzler, M. Freudenberg, P. van Endert, G. Kohler, and H.L. Pahl Activation of cellular death programs associated with immunosenescence-like phenotype in TPPII knockout mice Proc. Natl. Acad. Sci. USA 105 2008 5177 5182
14. S. Kaushik, U. Bandyopadhyay, S. Sridhar, R. Kiffin, M. Martinez-Vicente, M. Kon, S.J. Orenstein, E. Wong, and A.M. Cuervo Chaperone-mediated autophagy at a glance J. Cell Sci. 124 2011 495 499
15. M. Kawahara, I.A. York, A. Hearn, D. Farfan, and K.L. Rock Analysis of the role of tripeptidyl peptidase II in MHC class I antigen presentation in vivo J. Immunol. 183 2009 6069 6077
16. M. Kon, R. Kiffin, H. Koga, J. Chapochnick, F. Macian, L. Varticovski, and A.M. Cuervo Chaperone-mediated autophagy is required for tumor growth Sci. Transl. Med. 3 2011 109ra117
17. V.I. Korolchuk, F.M. Menzies, and D.C. Rubinsztein Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems FEBS Lett. 584 2010 1393 1398
18. T.J. Lampidis, M. Kurtoglu, J.C. Maher, H.P. Liu, A. Krishan, V. Sheft, S. Szymanski, I. Fokt, W.R. Rudnicki, and K. Ginalski Efficacy of 2-halogen substituted D-glucose analogs in blocking glycolysis and killing "hypoxic tumor cells" Cancer Chemother. Pharmacol. 58 2006 725 734
19. N.J. MacIver, R.D. Michalek, and J.C. Rathmell Metabolic regulation of T lymphocytes Annu. Rev. Immunol. 31 2013 259 283
20. R.M. McKay, J.P. McKay, J.M. Suh, L. Avery, and J.M. Graff Tripeptidyl peptidase II promotes fat formation in a conserved fashion EMBO Rep. 8 2007 1183 1189
21. E.S. Miller, J.C. Klinger, C. Akin, D.A. Koebel, and G. Sonnenfeld Inhibition of murine splenic T lymphocyte proliferation by 2-deoxy-D-glucose-induced metabolic stress J. Neuroimmunol. 52 1994 165 173
22. K.C. Patra, Q. Wang, P.T. Bhaskar, L. Miller, Z. Wang, W. Wheaton, N. Chandel, M. Laakso, W.J. Muller, and E.L. Allen Hexokinase 2 is required for tumor initiation and maintenance and its systemic deletion is therapeutic in mouse models of cancer Cancer Cell 24 2013 213 228
23. E.L. Pearce, and E.J. Pearce Metabolic pathways in immune cell activation and quiescence Immunity 38 2013 633 643
24. E. Reits, J. Neijssen, C. Herberts, W. Benckhuijsen, L. Janssen, J.W. Drijfhout, and J. Neefjes A major role for TPPII in trimming proteasomal degradation products for MHC class I antigen presentation Immunity 20 2004 495 506
25. H.J. Rideout, I. Lang-Rollin, and L. Stefanis Involvement of macroautophagy in the dissolution of neuronal inclusions Int. J. Biochem. Cell Biol. 36 2004 2551 2562
26. R.B. Robey, and N. Hay Mitochondrial hexokinases, novel mediators of the antiapoptotic effects of growth factors and Akt Oncogene 25 2006 4683 4696
27. A. Roczniak-Ferguson, C.S. Petit, F. Froehlich, S. Qian, J. Ky, B. Angarola, T.C. Walther, and S.M. Ferguson The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis Sci. Signal. 5 2012 ra42
28. C. Rose, F. Vargas, P. Facchinetti, P. Bourgeat, R.B. Bambal, P.B. Bishop, S.M. Chan, A.N. Moore, C.R. Ganellin, and J.C. Schwartz Characterization and inhibition of a cholecystokinin-inactivating serine peptidase Nature 380 1996 403 409
29. T. Ryhänen, J.M. Hyttinen, J. Kopitz, K. Rilla, E. Kuusisto, E. Mannermaa, J. Viiri, C.I. Holmberg, I. Immonen, and S. Meri Crosstalk between Hsp70 molecular chaperone, lysosomes and proteasomes in autophagy-mediated proteolysis in human retinal pigment epithelial cells J. Cell. Mol. Med. 13 9B 2009 3616 3631
30. A.M. Schönegge, E. Villa, F. Förster, R. Hegerl, J. Peters, W. Baumeister, and B. Rockel The structure of human tripeptidyl peptidase II as determined by a hybrid approach Structure 20 2012 593 603
31. Y. Schutz Protein turnover, ureagenesis and gluconeogenesis Int. J. Vit. Nutr. Res. 81 2011 101 107
32. C. Settembre, C. Di Malta, V.A. Polito, M. Garcia Arencibia, F. Vetrini, S. Erdin, S.U. Erdin, T. Huynh, D. Medina, and P. Colella TFEB links autophagy to lysosomal biogenesis Science 332 2011 1429 1433
33. L.Z. Shi, R. Wang, G. Huang, P. Vogel, G. Neale, D.R. Green, and H. Chi HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells J. Exp. Med. 208 2011 1367 1376
34. F.B. Stentz, and A.E. Kitabchi Transcriptome and proteome expression in activated human CD4 and CD8 T-lymphocytes Biochem. Biophys. Res. Commun. 324 2004 692 696
35. G.M. Tannahill, A.M. Curtis, J. Adamik, E.M. Palsson-McDermott, A.F. McGettrick, G. Goel, C. Frezza, N.J. Bernard, B. Kelly, and N.H. Foley Succinate is an inflammatory signal that induces IL-1β through HIF-1α Nature 496 2013 238 242
36. P.M. Taylor Role of amino acid transporters in amino acid sensing Am. J. Clin. Nutr. 99 2014 223S 230S
37. B. Tomkinson Tripeptidyl peptidases: enzymes that count Trends Biochem. Sci. 24 1999 355 359
38. R. Valdor, E. Mocholi, Y. Botbol, I. Guerrero-Ros, D. Chandra, H. Koga, C. Gravekamp, A.M. Cuervo, and F. Macian Chaperone-mediated autophagy regulates T cell responses through targeted degradation of negative regulators of T cell activation Nat. Immunol. 15 2014 1046 1054
39. R. Wang, C.P. Dillon, L.Z. Shi, S. Milasta, R. Carter, D. Finkelstein, L.L. McCormick, P. Fitzgerald, H. Chi, J. Munger, and D.R. Green The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation Immunity 35 2011 871 882
40. C. Wilson, A.M. Gibson, and J.R. McDermott Purification and characterization of tripeptidylpeptidase-II from post-mortem human brain Neurochem. Res. 18 1993 743 749
41. A. Wolf, S. Agnihotri, J. Micallef, J. Mukherjee, N. Sabha, R. Cairns, C. Hawkins, and A. Guha Hexokinase 2 is a key mediator of aerobic glycolysis and promotes tumor growth in human glioblastoma multiforme J. Exp. Med. 208 2011 313 326
42. A. Wolf, S. Agnihotri, D. Munoz, and A. Guha Developmental profile and regulation of the glycolytic enzyme hexokinase 2 in normal brain and glioblastoma multiforme Neurobiol. Dis. 44 2011 84 91
43. J.W. Custer, and R.E. Rau The Harriet Lane Handbook 18th Edition 2009 Elsevier Mosby Philadelphia, PA
44. R.E. Dickinson, H. Griffin, V. Bigley, L.N. Reynard, R. Hussain, M. Haniffa, J.H. Lakey, T. Rahman, X.N. Wang, and N. McGovern Exome sequencing identifies GATA-2 mutation as the cause of dendritic cell, monocyte, B and NK lymphoid deficiency Blood 118 2011 2656 2658
45. N. Guex, and M.C. Peitsch SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling Electrophoresis 18 1997 2714 2723
46. J. Hageman, and H.H. Kampinga Computational analysis of the human HSPH/HSPA/DNAJ family and cloning of a human HSPH/HSPA/DNAJ expression library Cell Stress Chaperones 14 2009 1 21
47. G. Lopez-Herrera, G. Tampella, Q. Pan-Hammarström, P. Herholz, C.M. Trujillo-Vargas, K. Phadwal, A.K. Simon, M. Moutschen, A. Etzioni, and A. Mory Deleterious mutations in LRBA are associated with a syndrome of immune deficiency and autoimmunity Am. J. Hum. Genet. 90 2012 986 1001
48. Schrodinger, LLC (2010). The PyMOL Molecular Graphics System, Version 1.3r1.
49. D. Seelow, M. Schuelke, F. Hildebrandt, and P. Nürnberg HomozygosityMapper - an interactive approach to homozygosity mapping Nucleic Acids Res. 37 Web Server issue 2009 W593 W599
50. Q. Zhang, J.C. Davis, I.T. Lamborn, A.F. Freeman, H. Jing, A.J. Favreau, H.F. Matthews, J. Davis, M.L. Turner, and G. Uzel Combined immunodeficiency associated with DOCK8 mutations N. Engl. J. Med. 361 2009 2046 2055