Metabolic dysfunction in lymphocytes promotes postoperative morbidity

Clinical Science

Volumn 129, Issue 5, 2015, Pages 423-437

  Edwards, Mark R ^a   Sultan, Pervez ^a   del Arroyo, Ana Gutierrez ^a   Whittle, John ^a   Karmali, Shamir N ^a   Ramani Moonesinghe, S ^a   Haddad, Fares S ^a   Mythen, Michael G ^a   Singer, Mervyn ^a   Ackland, Gareth L ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Apoptosis; Inflammasome; Lymphocyte; Metabolism; Mitochondria; Sepsis

Indexed keywords

CRYOPYRIN; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; REACTIVE OXYGEN METABOLITE; APOPTOSIS REGULATORY PROTEIN; GLUCOCORTICOID; INFLAMMASOME;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; FEMALE; GLYCOLYSIS; HUMAN; HUMAN CELL; JOINT PROSTHESIS; LEUKOCYTE COUNT; LYMPHOCYTE; LYMPHOCYTE PROLIFERATION; LYMPHOCYTOPENIA; MALE; MOUSE; NONHUMAN; POSTOPERATIVE INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURGICAL MORTALITY; ADVERSE EFFECTS; ANIMAL; ARTHROPLASTY; C57BL MOUSE; CELL CULTURE; COMPLICATION; DEVICES; DRUG EFFECTS; ENERGY METABOLISM; GENETICS; IMMUNOLOGY; KAPLAN MEIER METHOD; KNOCKOUT MOUSE; LYMPHOCYTE COUNT; LYMPHOPENIA; METABOLISM; MIDDLE AGED; MORTALITY; PATHOLOGY; PHENOTYPE; PROSTHESIS-RELATED INFECTIONS; RISK FACTOR; TIME; TREATMENT OUTCOME; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; ARTHROPLASTY, REPLACEMENT; CELLS, CULTURED; ENERGY METABOLISM; FEMALE; GLUCOCORTICOIDS; HUMANS; INFLAMMASOMES; JOINT PROSTHESIS; KAPLAN-MEIER ESTIMATE; LYMPHOCYTE COUNT; LYMPHOCYTES; LYMPHOPENIA; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; PHENOTYPE; PROSTHESIS-RELATED INFECTIONS; RISK FACTORS; TIME FACTORS; TREATMENT OUTCOME;

EID: 84951994280     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20150024     Document Type: Article

References (61)

1. Hotchkiss, R.S. and Opal, S. (2010) Immunotherapy for sepsis-a new approach against an ancient foe. N. Engl. J. Med. 363, 87-89.
2. Hotchkiss, R.S. and Karl, I.E. (2003) The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348, 138-150.
3. Kim, K.D., Zhao, J., Auh, S., Yang, X., Du, P., Tang, H. and Fu, Y.X. (2007) Adaptive immune cells temper initial innate responses. Nat. Med. 13, 1248-1252.
4. Palm, N.W. and Medzhitov, R. (2007) Not so fast: adaptive suppression of innate immunity. Nat. Med. 13, 1142-1144.
5. Cabrera-Perez, J., Condotta, S.A., Badovinac, V.P. and Griffith, T.S. (2014) Impact of sepsis on CD4 T cell immunity. J. Leukoc. Biol. 96, 767-777.
6. Drewry, A.M., Samra, N., Skrupky, L.P., Fuller, B.M., Compton, S.M. and Hotchkiss, R.S. (2014) Persistent lymphopenia after diagnosis of sepsis predicts mortality. Shock 42, 383-391.
7. Boomer, J., To, K., Chang, K., Takasu, O., Osborne, D., Walton, A., Bricker, T., Jarman, S., Kreisel, D. et al. (2011) Immunosuppression in patients who die of sepsis and multiple organ failure. JAMA 306, 2594-2605.
8. Fox, C.J., Hammerman, P.S. and Thompson, C.B. (2005) Fuel feeds function: energy metabolism and the T-cell response. Nat. Rev. Immunol. 5, 844-852.
9. Ron-Harel, N., Sharpe, A.H. and Haigis, M.C. (2015) Mitochondrial metabolism in T cell activation and senescence: a mini-review. Gerontology. 61, 131-138.
10. Pearce, E.L., Poffenberger, M.C., Chang, C.H. and Jones, R.G. (2013) Fueling immunity: insights into metabolism and lymphocyte function. Science 342, 1242454.
11. Guarda, G., Dostert, C., Staehli, F., Cabalzar, K., Castillo, R., Tardivel, A., Schneider, P. and Tschopp, J. (2009) T cells dampen innate immune responses through inhibition of NLRP1 and NLRP3 inflammasomes. Nature 460, 269-273.
12. McLoughlin, R.M., Solinga, R.M., Rich, J., Zaleski, K.J., Cocchiaro, J.L., Risley, A., Tzianabos, A.O. and Lee, J.C. (2006) CD4+ T cells and CXC chemokines modulate the pathogenesis of Staphylococcus aureus wound infections. Proc. Natl. Acad. Sci. U.S.A. 103, 10408-10413.
13. Ghaferi, A.A., Birkmeyer, J.D. and Dimick, J.B. (2009) Complications, failure to rescue, and mortality with major inpatient surgery in medicare patients. Ann. Surg. 250, 1029-1034.
14. Bennett-Guerrero, E., Welsby, I., Dunn, T.J., Young, L.R., Wahl, T.A., Diers, T.L., Phillips-Bute, B.G., Newman, M.F. and Mythen, M.G. (1999) The use of a postoperative morbidity survey to evaluate patients with prolonged hospitalization after routine, moderate-risk, elective surgery. Anesth. Analg. 89, 514-519.
15. Kirksey, M., Lin Chiu, Y., Ma, Y., Gonzalez Della Valle, A., Poultsides, L., Gerner, P. and Memtsoudis, S.G. (2012) Trends in in-hospital major morbidity and mortality after total joint arthroplasty: United States 1998-2008. Anesth. Analg. 115, 321-327.
16. Ackland, G.L., Moran, N., Cone, S., Grocott, M.P. and Mythen, M.G. (2011) Chronic kidney disease and postoperative morbidity after elective orthopedic surgery. Anesth. Analg. 112, 1375-1381.
17. Ahmed, A.A., Mooar, P.A., Kleiner, M., Torg, J.S. and Miyamoto, C.T. (2011) Hypertensive patients show delayed wound healing following total hip arthroplasty. PLoS One 6, e23224.
18. Saleh, K., Olson, M., Resig, S., Bershadsky, B., Kuskowski, M., Gioe, T., Robinson, H., Schmidt, R. and McElfresh, E. (2002) Predictors of wound infection in hip and knee joint replacement: results from a 20 year surveillance program. J. Orthop. Res. 20, 506-515.
19. Levis, W.R. and Robbins, J.H. (1972) Methods for obtaining purified lymphocytes, glass-adherent mononuclear cells, and a population containing both cell types from human peripheral blood. Blood 40, 77-89.
20. Reynolds, J.M., Martinez, G.J., Chung, Y. and Dong, C. (2012) Toll-like receptor 4 signaling in T cells promotes autoimmune inflammation. Proc. Natl. Acad. Sci. U.S.A. 109, 13064-13069.
21. Dracheva, S., Marras, S.A., Elhakem, S.L., Kramer, F.R., Davis, K.L. and Haroutunian, V. (2001) N-methyl-D-aspartic acid receptor expression in the dorsolateral prefrontal cortex of elderly patients with schizophrenia. Am. J. Psychiatry 158, 1400-1410.
22. Jones, R.G. and Thompson, C.B. (2007) Revving the engine: signal transduction fuels T cell activation. Immunity 27, 173-178.
23. van der Windt, G.J., O'Sullivan, D., Everts, B., Huang, S.C., Buck, M.D., Curtis, J.D., Chang, C.H., Smith, A.M., Ai, T., Faubert, B. et al. (2013) CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability. Proc. Natl. Acad. Sci. U.S.A. 110, 14336-14341.
24. Chang, C.H., Curtis, J.D., Maggi, Jr, L.B., Faubert, B., Villarino, A.V., O'Sullivan, D., Huang, S.C., van der Windt, G.J., Blagih, J., Qiu, J. et al. (2013) Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 153, 1239-1251.
25. Nagata, S. (1997) Apoptosis by death factor. Cell 88, 355-365.
26. Arch, R.H. and Thompson, C.B. (1999) Lymphocyte survival-the struggle against death. Annu. Rev. Cell Dev. Biol. 15, 113-140.
27. Stahn, C. and Buttgereit, F. (2008) Genomic and nongenomic effects of glucocorticoids. Nat. Clin. Pract. Rheumatol. 4, 525-533.
28. Naito, Y., Tamai, S., Shingu, K., Shindo, K., Matsui, T., Segawa, H., Nakai, Y. and Mori, K. (1992) Responses of plasma adrenocorticotropic hormone, cortisol, and cytokines during and after upper abdominal surgery. Anesthesiology 77, 426-431.
29. Shao, W., Yeretssian, G., Doiron, K., Hussain, S.N. and Saleh, M. (2007) The caspase-1 digestome identifies the glycolysis pathway as a target during infection and septic shock. J. Biol. Chem. 282, 36321-36329.
30. Doitsh, G., Galloway, N.L., Geng, X., Yang, Z., Monroe, K.M., Zepeda, O., Hunt, P.W., Hatano, H., Sowinski, S., Munoz-Arias, I. and Greene, W.C. (2014) Cell death by pyroptosis drives CD4 Tcell depletion in HIV-1 infection. Nature. 505, 509-514.
31. Gibbison, B., Angelini, G.D. and Lightman, S.L. (2013) Dynamic output and control of the hypothalamic-pituitary-adrenal axis in critical illness and major surgery. Br. J. Anaesth. 111, 347-360.
32. Kummer, J.A., Broekhuizen, R., Everett, H., Agostini, L., Kuijk, L., Martinon, F., van Bruggen, R. and Tschopp, J. (2007) Inflammasome components NALP 1 and 3 show distinct but separate expression profiles in human tissues suggesting a site-specific role in the inflammatory response. J. Histochem. Cytochem. 55, 443-452.
33. Munoz-Planillo, R., Kuffa, P., Martinez-Colon, G., Smith, B.L., Rajendiran, T.M. and Nunez, G. (2013) K(+) efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity 38, 1142-1153.
34. Tschopp, J. and Schroder, K. (2010) NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat. Rev. Immunol. 10, 210-215.
35. Brealey, D., Brand, M., Hargreaves, I., Heales, S., Land, J., Smolenski, R., Davies, N.A., Cooper, C.E. and Singer, M. (2002) Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 360, 219-223.
36. Chacko, B.K., Kramer, P.A., Ravi, S., Benavides, G.A., Mitchell, T., Dranka, B.P., Ferrick, D., Singal, A.K., Ballinger, S.W., Bailey, S.M. et al. (2014) The Bioenergetic Health Index: a new concept in mitochondrial translational research. Clin. Sci. 127, 367-373.
37. Wherry, E.J. (2011) T cell exhaustion. Nat. Immunol. 12, 492-499.
38. Vaduganathan, M., Ambrosy, A.P., Greene, S.J., Mentz, R.J., Subacius, H.P., Maggioni, A.P., Swedberg, K., Nodari, S., Zannad, F., Konstam, M.A. et al. (2012) Predictive value of low relative lymphocyte count in patients hospitalized for heart failure with reduced ejection fraction: insights from the EVEREST trial. Circ. Heart Fail. 5, 750-758.
39. Hagen, T.P., Vaughan-Sarrazin, M.S. and Cram, P. (2010) Relation between hospital orthopaedic specialisation and outcomes in patients aged 65 and older: retrospective analysis of US Medicare data. BMJ 340, c165.
40. Jencks, S.F., Williams, M.V. and Coleman, E.A. (2009) Rehospitalizations among patients in the Medicare fee-for-service program. N. Engl. J. Med. 360, 1418-1428.
41. Gibson, P.H., Croal, B.L., Cuthbertson, B.H., Small, G.R., Ifezulike, A.I., Gibson, G., Jeffrey, R.R., Buchan, K.G., El-Shafei, H. and Hillis, G.S. (2007) Preoperative neutrophil-lymphocyte ratio and outcome from coronary artery bypass grafting. Am. Heart J. 154, 995-1002.
42. Christou, N.V., Meakins, J.L., Gordon, J., Yee, J., Hassan-Zahraee, M., Nohr, C.W., Shizgal, H.M. and MacLean, L.D. (1995) The delayed hypersensitivity response and host resistance in surgical patients. 20 years later. Ann. Surg. 222, 534-546.
43. Puyana, J.C., Pellegrini, J.D., De, A.K., Kodys, K., Silva, W.E. and Miller, C.L. (1998) Both T-helper-1-and T-helper-2-type lymphokines are depressed in posttrauma anergy. J. Trauma 44, 1037-1045.
44. Bandyopadhyay, G., De, A., Laudanski, K., Li, F., Lentz, C., Bankey, P. and Miller-Graziano, C. (2007) Negative signaling contributes to T-cell anergy in trauma patients. Crit. Care Med. 35, 794-801.
45. Venet, F., Chung, C.S., Kherouf, H., Geeraert, A., Malcus, C., Poitevin, F., Bohe, J., Lepape, A., Ayala, A. and Monneret, G. (2009) Increased circulating regulatory T cells (CD4(+)CD25 (+)CD127 (-)) contribute to lymphocyte anergy in septic shock patients. Intensive Care Med. 35, 678-686.
46. Rem, J., Brandt, M.R. and Kehlet, H. (1980) Prevention of postoperative lymphopenia and granulocytosis by epidural analgesia. Lancet 1, 283-284.
47. Heffernan, D.S., Monaghan, S.F., Thakkar, R.K., Machan, J.T., Cioffi, W.G. and Ayala, A. (2012) Failure to normalize lymphopenia following trauma is associated with increased mortality, independent of the leukocytosis pattern. Crit. Care 16, R12.
48. Hotchkiss, R.S., Tinsley, K.W., Swanson, P.E., Chang, K.C., Cobb, J.P., Buchman, T.G., Korsmeyer, S.J. and Karl, I.E. (1999) Prevention of lymphocyte cell death in sepsis improves survival in mice. Proc. Natl. Acad. Sci. U.S.A. 96, 14541-14546.
49. Hotchkiss, R.S., Tinsley, K.W., Swanson, P.E., Chang, K.C., Cobb, J.P., Buchman, T.G., Korsmeyer, S.J. and Karl, I.E. (1999) Prevention of lymphocyte cell death in sepsis improves survival in mice. Proc. Natl. Acad. Sci. U.S.A. 96, 14541-14546.
50. Mestas, J. and Hughes, C.C. (2004) Of mice and not men: differences between mouse and human immunology. J. Immunol. 172, 2731-2738.
51. Khuri, S.F., Henderson, W.G., DePalma, R.G., Mosca, C., Healey, N.A. and Kumbhani, D.J. (2005) Determinants of long-term survival after major surgery and the adverse effect of postoperative complications. Ann. Surg. 242, 326-341.
52. Gatza, E., Wahl, D.R., Opipari, A.W., Sundberg, T.B., Reddy, P., Liu, C., Glick, G.D. and Ferrara, J.L. (2011) Manipulating the bioenergetics of alloreactive T cells causes their selective apoptosis and arrests graft-versus-host disease. Sci. Transl. Med. 3, 67ra68.
53. Daniele, R.P., Holian, S.K. and Nowell, P.C. (1978) A potassium ionophore (Nigericin) inhibits stimulation of human lymphocytes by mitogens. J. Exp. Med. 147, 571-581.
54. Busillo, J.M., Azzam, K.M. and Cidlowski, J.A. (2011) Glucocorticoids sensitize the innate immune system through regulation of the NLRP3 inflammasome. J. Biol. Chem. 286, 38703-38713.
55. Lannan, E.A., Galliher-Beckley, A.J., Scoltock, A.B. and Cidlowski, J.A. (2012) Proinflammatory actions of glucocorticoids: glucocorticoids and TNFalpha coregulate gene expression in vitro and in vivo. Endocrinology 153, 3701-3712.
56. Tung, S., Shi, Y., Wong, K., Zhu, F., Gorczynski, R., Laister, R.C., Minden, M., Blechert, A.K., Genzel, Y., Reichl, U. and Spaner, D.E. (2013) PPARalpha and fatty acid oxidation mediate glucocorticoid resistance in chronic lymphocytic leukemia. Blood 122, 969-980.
57. De Iudicibus, S., Stocco, G., Martelossi, S., Londero, M., Ebner, E., Pontillo, A., Lionetti, P., Barabino, A., Bartoli, F., Ventura, A. and Decorti, G. (2011) Genetic predictors of glucocorticoid response in pediatric patients with inflammatory bowel diseases. J. Clin. Gastroenterol. 45, e1-e7.
58. Bowers, N.L., Helton, E.S., Huijbregts, R.P., Goepfert, P.A., Heath, S.L. and Hel, Z. (2014) Immune suppression by neutrophils in HIV-1 infection: role of PD-L1/PD-1 pathway. PLoS Pathog. 10, e1003993.
59. Hotchkiss, R.S., Monneret, G. and Payen, D. (2013) Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach. Lancet Infect. Dis. 13, 260-268.
60. Pillay, J., Kamp, V.M., van Hoffen, E., Visser, T., Tak, T., Lammers, J.W., Ulfman, L.H., Leenen, L.P., Pickkers, P. and Koenderman, L. (2012) A subset of neutrophils in human systemic inflammation inhibits T cell responses through Mac-1. J. Clin. Invest. 122, 327-336.
61. Henson, S.M., Lanna, A., Riddell, N.E., Franzese, O., Macaulay, R., Griffiths, S.J., Puleston, D.J., Watson, A.S., Simon, A.K., Tooze, S.A. and Akbar, A.N. (2014) p38 signaling inhibits mTORC1-independent autophagy in senescent human CD8(+) T cells. J. Clin. Invest. 124, 4004-4016.