Programmed death-1 inhibition of phosphatidylinositol 3-kinase/akt/mechanistic target of rapamycin signaling impairs sarcoidosis cd41 t cell proliferation

American Journal of Respiratory Cell and Molecular Biology

Volumn 56, Issue 1, 2017, Pages 74-82

  Celada, Lindsay J ^a,b   Rotsinger, Joseph E ^a   Young, Anjuli ^a   Shaginurova, Guzel ^b   Shelton, Debresha ^a   Hawkins, Charlene ^a   Drake, Wonder P ^a,b  

^a Division of Infectious Diseases   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AKT; Lymphocyte cell specific protein tyrosine kinase; Phosphatidylinositol 3 kinase; Programmed death 1; Proliferation; Sarcoidosis

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN KINASE B; T LYMPHOCYTE RECEPTOR; PDCD1 PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE;

ADULT; AGED; ARTICLE; CD4+ T LYMPHOCYTE; CELL CYCLE PROGRESSION; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; MALE; PROTEIN EXPRESSION; SARCOIDOSIS; UPREGULATION; CASE CONTROL STUDY; CELL PROLIFERATION; DEMOGRAPHY; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PATHOLOGY; SIGNAL TRANSDUCTION; YOUNG ADULT;

ADULT; AGED; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DEMOGRAPHY; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; MIDDLE AGED; PHOSPHATIDYLINOSITOL 3-KINASE; PROGRAMMED CELL DEATH 1 RECEPTOR; PROTO-ONCOGENE PROTEINS C-AKT; SARCOIDOSIS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; YOUNG ADULT;

EID: 85008485842     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2016-0037OC     Document Type: Article

References (37)

1. Braun NA, Celada LJ, Herazo-Maya JD, Abraham S, Shaginurova G, Sevin CM, Grutters J, Culver DA, Dworski R, Sheller J, et al. Blockade of the programmed death-1 pathway restores sarcoidosis CD41 T-cell proliferative capacity. Am J Respir Crit Care Med 2014;190:560-571.
2. Oswald-Richter KA, Richmond BW, Braun NA, Isom J, Abraham S, Taylor TR, Drake JM, Culver DA, Wilkes DS, Drake WP. Reversal of global CD41 subset dysfunction is associated with spontaneous clinical resolution of pulmonary sarcoidosis. J Immunol 2013;190: 5446-5453.
3. Chen L, Flies DB. Molecular mechanisms of T cell co-stimulation and coinhibition. Nat Rev Immunol 2013;13:227-242.
4. Nurieva RI, Liu X, Dong C. Yin-Yang of costimulation: crucial controls of immune tolerance and function. Immunol Rev 2009; 229:88-100.
5. Appleman LJ, Berezovskaya A, Grass I, Boussiotis VA. CD28 costimulation mediates T cell expansion via IL-2-independent and IL-2-dependent regulation of cell cycle progression. J Immunol 2000; 164:144-151.
6. Appleman LJ, van Puijenbroek AA, Shu KM, Nadler LM, Boussiotis VA. CD28 costimulation mediates down-regulation of p27kip1 and cell cycle progression by activation of the PI3K/PKB signaling pathway in primary human T cells. J Immunol 2002;168: 2729-2736.
7. Pagès F, Ragueneau M, Rottapel R, Truneh A, Nunes J, Imbert J, Olive D. Binding of phosphatidylinositol-3-OH kinase to CD28 is required for T-cell signalling. Nature 1994;369:327-329.
8. Parry RV, Chemnitz JM, Frauwirth KA, Lanfranco AR, Braunstein I, Kobayashi SV, Linsley PS, Thompson CB, Riley JL. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol 2005;25:9543-9553.
9. Patsoukis N, Brown J, Petkova V, Liu F, Li L, Boussiotis VA. Selective effects of PD-1 on Akt and Ras pathways regulate molecular components of the cell cycle and inhibit T cell proliferation. Sci Signal 2012;5:ra46.
10. Chu K, Littman DR. Requirement for kinase activity of CD4-associated p56lck in antibody-triggered T cell signal transduction. J Biol Chem 1994;269:24095-24101.
11. Straus DB, Weiss A. Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 1992;70:585-593.
12. Rossy J, Owen DM, Williamson DJ, Yang Z, Gaus K. Conformational states of the kinase Lck regulate clustering in early T cell signaling. Nat Immunol 2013;14:82-89.
13. Seddon B, Legname G, Tomlinson P, Zamoyska R. Long-term survival but impaired homeostatic proliferation of Nä?ve T cells in the absence of p56lck. Science 2000;290:127-131.
14. Oswald-Richter KA, Culver DA, Hawkins C, Hajizadeh R, Abraham S, Shepherd BE, Jenkins CA, Judson MA, Drake WP. Cellular responses to mycobacterial antigens are present in bronchoalveolar lavage fluid used in the diagnosis of sarcoidosis. Infect Immun 2009;77:3740-3748.
15. Oswald-Richter K, Sato H, Hajizadeh R, Shepherd BE, Sidney J, Sette A, Newman LS, Drake WP. Mycobacterial ESAT-6 and katG are recognized by sarcoidosis CD41 T cells when presented by the American sarcoidosis susceptibility allele, DRB11101. J Clin Immunol 2010;30:157-166.
16. Wei F, Zhong S, Ma Z, Kong H, Medvec A, Ahmed R, Freeman GJ, Krogsgaard M, Riley JL. Strength of PD-1 signaling differentially affects T-cell effector functions. Proc Natl Acad Sci U S A 2013;110:E2480-E2489.
17. Li QJ, Dinner AR, Qi S, Irvine DJ, Huppa JB, Davis MM, Chakraborty AK. CD4 enhances T cell sensitivity to antigen by coordinating Lck accumulation at the immunological synapse. Nat Immunol 2004;5: 791-799.
18. Xue L, Chiang L, Kang C, Winoto A. The role of the PI3K-AKT kinase pathway in T-cell development beyond the b checkpoint. Eur J Immunol 2008;38:3200-3207.
19. Zhou T, Zhang W, Sweiss NJ, Chen ES, Moller DR, Knox KS, Ma SF, Wade MS, Noth I, Machado RF, et al. Peripheral blood gene expression as a novel genomic biomarker in complicated sarcoidosis. PLoS One 2012;7:e44818.
20. Fischer A, Ellinghaus D, Nutsua M, Hofmann S, Montgomery CG, Iannuzzi MC, Rybicki BA, Petrek M, Mrazek F, Pabst S, et al.; GenPhenReSa Consortium. Identification of immune-relevant factors conferring sarcoidosis genetic risk. Am J Respir Crit Care Med 2015; 192:727-736.
21. Su R, Li MM, Bhakta NR, Solberg OD, Darnell EP, Ramstein J, Garudadri S, Ho M, Woodruff PG, Koth LL. Longitudinal analysis of sarcoidosis blood transcriptomic signatures and disease outcomes. Eur Respir J 2014;44:985-993.
22. Saltini C, Spurzem JR, Lee JJ, Pinkston P, Crystal RG. Spontaneous release of interleukin 2 by lung T lymphocytes in active pulmonary sarcoidosis is primarily from the Leu31DR1 T cell subset. J Clin Invest 1986;77:1962-1970.
23. Pinkston P, Bitterman PB, Crystal RG. Spontaneous release of interleukin-2 by lung T lymphocytes in active pulmonary sarcoidosis. N Engl J Med 1983;308:793-800.
24. Song Z, Marzilli L, Greenlee BM, Chen ES, Silver RF, Askin FB, Teirstein AS, Zhang Y, Cotter RJ, Moller DR. Mycobacterial catalase-peroxidase is a tissue antigen and target of the adaptive immune response in systemic sarcoidosis. J Exp Med 2005;201: 755-767.
25. Oswald-Richter KA, Beachboard DC, Seeley EH, Abraham S, Shepherd BE, Jenkins CA, Culver DA, Caprioli RM, Drake WP. Dual analysis for mycobacteria and propionibacteria in sarcoidosis BAL. J Clin Immunol 2012;32:1129-1140.
26. Allen SS, Evans W, Carlisle J, Hajizadeh R, Nadaf M, Shepherd BE, Pride DT, Johnson JE, Drake WP. Superoxide dismutase A antigens derived from molecular analysis of sarcoidosis granulomas elicit systemic Th-1 immune responses. Respir Res 2008;9:36.
27. Drake WP, Pei Z, Pride DT, Collins RD, Cover TL, Blaser MJ. Molecular analysis of sarcoidosis tissues for mycobacterium species DNA. Emerg Infect Dis 2002;8:1334-1341.
28. Rotsinger JE, Celada LJ, Polosukhin VV, Atkinson JB, Drake WP. Molecular analysis of sarcoidosis granulomas reveals antimicrobial targets. Am J Respir Cell Mol Biol 2016;55:128-134.
29. Richmond BW, Ploetze K, Isom J, Chambers-Harris I, Braun NA, Taylor T, Abraham S, Mageto Y, Culver DA, Oswald-Richter KA, et al. Sarcoidosis Th17 cells are ESAT-6 antigen specific but demonstrate reduced IFN-g expression. J Clin Immunol 2013;33: 446-455.
30. Oswald-Richter KA, Beachboard DC, Zhan X, Gaskill CF, Abraham S, Jenkins C, Culver DA, Drake W. Multiple mycobacterial antigens are targets of the adaptive immune response in pulmonary sarcoidosis. Respir Res 2010;11:161.
31. Chen ES, Wahlström J, Song Z, Willett MH, Wikén M, Yung RC, West EE, McDyer JF, Zhang Y, Eklund A, et al. T cell responses to mycobacterial catalase-peroxidase profile a pathogenic antigen in systemic sarcoidosis. J Immunol 2008;181:8784-8796.
32. Liang J, Slingerland JM. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2003;2:339-345.
33. Chang F, Lee JT, Navolanic PM, Steelman LS, Shelton JG, Blalock WL, Franklin RA, McCubrey JA. Involvement of PI3K/Akt pathway in cell cycle progression, apoptosis, and neoplastic transformation: a target for cancer chemotherapy. Leukemia 2003; 17:590-603.
34. Sen P, Mukherjee S, Ray D, Raha S. Involvement of the Akt/PKB signaling pathway with disease processes. Mol Cell Biochem 2003; 253:241-246.
35. Thomson AW, Turnquist HR, Raimondi G. Immunoregulatory functions of mTOR inhibition. Nat Rev Immunol 2009;9:324-337.
36. Gao N, Zhang Z, Jiang BH, Shi X. Role of PI3K/AKT/mTOR signaling in the cell cycle progression of human prostate cancer. Biochem Biophys Res Commun 2003;310:1124-1132.
37. Casagrande F, Bacqueville D, Pillaire MJ, Malecaze F, Manenti S, Breton-Douillon M, Darbon JM. G1 phase arrest by the phosphatidylinositol 3-kinase inhibitor LY 294002 is correlated to upregulation of p27Kip1 and inhibition of G1 CDKs in choroidal melanoma cells. FEBS Lett 1998;422:385-390.