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Published in: BMC Immunology 1/2020

Open Access 01-12-2020 | IgA Vasculitis | Research article

Decreased glycolysis induced dysfunction of NK cells in Henoch-Schonlein purpura patients

Authors: Wenjia Chai, Xiaolin Wang, Wei Wang, Hui Wang, Wenjun Mou, Jingang Gui

Published in: BMC Immunology | Issue 1/2020

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Abstract

Background

Henoch-Schonlein purpura (HSP) is the most common systemic vasculitis of the childhood. However, its mechanisms and pathogenesis still need more exploration. Natural killer (NK) cells are innate lymphocytes, and there is a growing appreciation that cellular metabolism is important in determining the immune responsiveness of lymphocytes. Thus, we aimed to analyze the NK cells phenotype and explore the association between glucose metabolism and NK cells function in HSP patients.

Results

A total number of 64 HSP patients and 34 healthy children were included. The HSP patients were divided into two groups according to whether accompanied with nephritis or not. NK cells in HSP patients without nephritis showed a reduced frequency in peripheral blood, a down-regulated expression of activating receptors both NKp30 and NKp46, and an attenuated cytotoxic function against tumor cells. In addition, the function impairment of NK cells was shown to exacerbate in HSPN. Our data further revealed an aberrant metabolic reprogramming of NK cells in HSP patients. Upon stimulation with cytokines (IL-15, IL-12 and IL-2), NK cells from healthy controls switched to an elevated glycolysis rate to support their effector function. By contrast, the glycolysis rate of activated NK cells in HSP group was not significantly up-regulated from the resting level possibly owing to the inhibition of mTORC1.

Conclusions

Our study found that HSP patients were accompanied with dysfunction of NK cells. We concluded that the dysfunction of NK cells in HSP patients was induced with a decreased glycolysis rate and suggested that metabolic reprogramming of NK cells might be a player in the pathogenesis of HSP.
Literature
2.
go back to reference Chen JY, Mao JH. Henoch-Schonlein purpura nephritis in children: incidence, pathogenesis and management. World J Pediatr. 2015;11(1):29–34.PubMedCrossRef Chen JY, Mao JH. Henoch-Schonlein purpura nephritis in children: incidence, pathogenesis and management. World J Pediatr. 2015;11(1):29–34.PubMedCrossRef
3.
go back to reference Rai A, Nast C, Adler S. Henoch-Schonlein purpura nephritis. J Am Soc Nephrol. 1999;10(12):2637–44.PubMed Rai A, Nast C, Adler S. Henoch-Schonlein purpura nephritis. J Am Soc Nephrol. 1999;10(12):2637–44.PubMed
5.
go back to reference Heineke MH, Ballering AV, Jamin A, Ben Mkaddem S, Monteiro RC, Van Egmond M. New insights in the pathogenesis of immunoglobulin a vasculitis (Henoch-Schonlein purpura). Autoimmun Rev. 2017;16(12):1246–53.PubMedCrossRef Heineke MH, Ballering AV, Jamin A, Ben Mkaddem S, Monteiro RC, Van Egmond M. New insights in the pathogenesis of immunoglobulin a vasculitis (Henoch-Schonlein purpura). Autoimmun Rev. 2017;16(12):1246–53.PubMedCrossRef
6.
go back to reference Rigante D, Castellazzi L, Bosco A, Esposito S. Is there a crossroad between infections, genetics, and Henoch-Schonlein purpura? Autoimmun Rev. 2013;12(10):1016–21.PubMedCrossRef Rigante D, Castellazzi L, Bosco A, Esposito S. Is there a crossroad between infections, genetics, and Henoch-Schonlein purpura? Autoimmun Rev. 2013;12(10):1016–21.PubMedCrossRef
7.
go back to reference Tizard EJ, Hamilton-Ayres MJ. Henoch Schonlein purpura. Arch Dis Child Educ Pract Ed. 2008;93(1):1–8.PubMedCrossRef Tizard EJ, Hamilton-Ayres MJ. Henoch Schonlein purpura. Arch Dis Child Educ Pract Ed. 2008;93(1):1–8.PubMedCrossRef
8.
go back to reference Saulsbury FT. Alterations in the O-linked glycosylation of IgA1 in children with Henoch-Schonlein purpura. J Rheumatol. 1997;24(11):2246–9.PubMed Saulsbury FT. Alterations in the O-linked glycosylation of IgA1 in children with Henoch-Schonlein purpura. J Rheumatol. 1997;24(11):2246–9.PubMed
9.
go back to reference Davin JC, Coppo R. Henoch-Schonlein purpura nephritis in children. Nat Rev Nephrol. 2014;10(10):563–73.PubMedCrossRef Davin JC, Coppo R. Henoch-Schonlein purpura nephritis in children. Nat Rev Nephrol. 2014;10(10):563–73.PubMedCrossRef
10.
go back to reference Jen HY, Chuang YH, Lin SC, Chiang BL, Yang YH. Increased serum interleukin-17 and peripheral Th17 cells in children with acute Henoch-Schonlein purpura. Pediatr Allergy Immunol. 2011;22(8):862–8.PubMedCrossRef Jen HY, Chuang YH, Lin SC, Chiang BL, Yang YH. Increased serum interleukin-17 and peripheral Th17 cells in children with acute Henoch-Schonlein purpura. Pediatr Allergy Immunol. 2011;22(8):862–8.PubMedCrossRef
11.
go back to reference Yang YH, Huang YH, Lin YL, Wang LC, Chuang YH, Yu HH, Lin YT, et al. Circulating IgA from acute stage of childhood Henoch-Schonlein purpura can enhance endothelial interleukin (IL)-8 production through MEK/ERK signalling pathway. Clin Exp Immunol. 2006;144(2):247–53.PubMedPubMedCentralCrossRef Yang YH, Huang YH, Lin YL, Wang LC, Chuang YH, Yu HH, Lin YT, et al. Circulating IgA from acute stage of childhood Henoch-Schonlein purpura can enhance endothelial interleukin (IL)-8 production through MEK/ERK signalling pathway. Clin Exp Immunol. 2006;144(2):247–53.PubMedPubMedCentralCrossRef
12.
go back to reference Yang YH, Wang SJ, Chuang YH, Lin YT, Chiang BL. The level of IgA antibodies to human umbilical vein endothelial cells can be enhanced by TNF-alpha treatment in children with Henoch-Schonlein purpura. Clin Exp Immunol. 2002;130(2):352–7.PubMedPubMedCentralCrossRef Yang YH, Wang SJ, Chuang YH, Lin YT, Chiang BL. The level of IgA antibodies to human umbilical vein endothelial cells can be enhanced by TNF-alpha treatment in children with Henoch-Schonlein purpura. Clin Exp Immunol. 2002;130(2):352–7.PubMedPubMedCentralCrossRef
13.
go back to reference Lin CY, Yang YH, Lee CC, Huang CL, Wang LC, Chiang BL. Thrombopoietin and interleukin-6 levels in Henoch-Schonlein purpura. J Microbiol Immunol Infect. 2006;39(6):476–82.PubMed Lin CY, Yang YH, Lee CC, Huang CL, Wang LC, Chiang BL. Thrombopoietin and interleukin-6 levels in Henoch-Schonlein purpura. J Microbiol Immunol Infect. 2006;39(6):476–82.PubMed
14.
go back to reference Li YY, Li CR, Wang GB, Yang J, Zu Y. Investigation of the change in CD4(+) T cell subset in children with Henoch-Schonlein purpura. Rheumatol Int. 2012;32(12):3785–92.PubMedCrossRef Li YY, Li CR, Wang GB, Yang J, Zu Y. Investigation of the change in CD4(+) T cell subset in children with Henoch-Schonlein purpura. Rheumatol Int. 2012;32(12):3785–92.PubMedCrossRef
15.
go back to reference Chen O, Zhu XB, Ren H, Wang YB, Sun R. The imbalance of Th17/Treg in Chinese children with Henoch-Schonlein purpura. Int Immunopharmacol. 2013;16(1):67–71.PubMedCrossRef Chen O, Zhu XB, Ren H, Wang YB, Sun R. The imbalance of Th17/Treg in Chinese children with Henoch-Schonlein purpura. Int Immunopharmacol. 2013;16(1):67–71.PubMedCrossRef
16.
go back to reference Gulhan B, Orhan D, Kale G, Besbas N, Ozen S. Studying cytokines of T helper cells in the kidney disease of IgA vasculitis (Henoch-Schonlein purpura). Pediatr Nephrol. 2015;30(8):1269–77.PubMedCrossRef Gulhan B, Orhan D, Kale G, Besbas N, Ozen S. Studying cytokines of T helper cells in the kidney disease of IgA vasculitis (Henoch-Schonlein purpura). Pediatr Nephrol. 2015;30(8):1269–77.PubMedCrossRef
17.
go back to reference Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9(5):503–10.PubMedCrossRef Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9(5):503–10.PubMedCrossRef
18.
go back to reference Fogler WE, Volker K, McCormick KL, Watanabe M, Ortaldo JR, Wiltrout RH. NK cell infiltration into lung, liver, and subcutaneous B16 melanoma is mediated by VCAM-1/VLA-4 interaction. J Immunol. 1996;156(12):4707–14.PubMed Fogler WE, Volker K, McCormick KL, Watanabe M, Ortaldo JR, Wiltrout RH. NK cell infiltration into lung, liver, and subcutaneous B16 melanoma is mediated by VCAM-1/VLA-4 interaction. J Immunol. 1996;156(12):4707–14.PubMed
19.
go back to reference Coppo R, Amore A. Aberrant glycosylation in IgA nephropathy (IgAN). Kidney Int. 2004;65(5):1544–7.PubMedCrossRef Coppo R, Amore A. Aberrant glycosylation in IgA nephropathy (IgAN). Kidney Int. 2004;65(5):1544–7.PubMedCrossRef
20.
go back to reference Iwatani H, Nagasawa Y, Yamamoto R, Iio K, Mizui M, Horii A, Kitahara T, et al. CD16+CD56+ cells are a potential culprit for hematuria in IgA nephropathy. Clin Exp Nephrol. 2015;19(2):216–24.PubMedCrossRef Iwatani H, Nagasawa Y, Yamamoto R, Iio K, Mizui M, Horii A, Kitahara T, et al. CD16+CD56+ cells are a potential culprit for hematuria in IgA nephropathy. Clin Exp Nephrol. 2015;19(2):216–24.PubMedCrossRef
21.
go back to reference Kimata H, Sherr EH, Saxon A. Human natural killer (NK) cells produce a late-acting B-cell differentiation activity. J Clin Immunol. 1988;8(5):381–9.PubMedCrossRef Kimata H, Sherr EH, Saxon A. Human natural killer (NK) cells produce a late-acting B-cell differentiation activity. J Clin Immunol. 1988;8(5):381–9.PubMedCrossRef
22.
go back to reference Mota G, Manciulea M, Cosma E, Popescu I, Hirt M, Jensen-Jarolim E, Calugaru A, et al. Human NK cells express fc receptors for IgA which mediate signal transduction and target cell killing. Eur J Immunol. 2003;33(8):2197–205.PubMedCrossRef Mota G, Manciulea M, Cosma E, Popescu I, Hirt M, Jensen-Jarolim E, Calugaru A, et al. Human NK cells express fc receptors for IgA which mediate signal transduction and target cell killing. Eur J Immunol. 2003;33(8):2197–205.PubMedCrossRef
23.
go back to reference Komiyama K, Moro I, Crago SS, Mestecky J. Inhibition of natural killer (NK) activity by human colostral and serum IgA. Adv Exp Med Biol. 1987;216A:539–42.PubMedCrossRef Komiyama K, Moro I, Crago SS, Mestecky J. Inhibition of natural killer (NK) activity by human colostral and serum IgA. Adv Exp Med Biol. 1987;216A:539–42.PubMedCrossRef
26.
go back to reference Donnelly RP, Loftus RM, Keating SE, Liou KT, Biron CA, Gardiner CM, Finlay DK. mTORC1-dependent metabolic reprogramming is a prerequisite for NK cell effector function. J Immunol. 2014;193(9):4477–84.PubMedCrossRef Donnelly RP, Loftus RM, Keating SE, Liou KT, Biron CA, Gardiner CM, Finlay DK. mTORC1-dependent metabolic reprogramming is a prerequisite for NK cell effector function. J Immunol. 2014;193(9):4477–84.PubMedCrossRef
27.
go back to reference Keating SE, Zaiatz-Bittencourt V, Loftus RM, Keane C, Brennan K, Finlay DK, Gardiner CM. Metabolic reprogramming supports IFN-gamma production by CD56bright NK cells. J Immunol. 2016;196(6):2552–60.PubMedCrossRef Keating SE, Zaiatz-Bittencourt V, Loftus RM, Keane C, Brennan K, Finlay DK, Gardiner CM. Metabolic reprogramming supports IFN-gamma production by CD56bright NK cells. J Immunol. 2016;196(6):2552–60.PubMedCrossRef
28.
go back to reference Marcais A, Cherfils-Vicini J, Viant C, Degouve S, Viel S, Fenis A, Rabilloud J, et al. The metabolic checkpoint kinase mTOR is essential for IL-15 signaling during the development and activation of NK cells. Nat Immunol. 2014;15(8):749–57.PubMedPubMedCentralCrossRef Marcais A, Cherfils-Vicini J, Viant C, Degouve S, Viel S, Fenis A, Rabilloud J, et al. The metabolic checkpoint kinase mTOR is essential for IL-15 signaling during the development and activation of NK cells. Nat Immunol. 2014;15(8):749–57.PubMedPubMedCentralCrossRef
29.
go back to reference Keppel MP, Saucier N, Mah AY, Vogel TP, Cooper MA. Activation-specific metabolic requirements for NK cell IFN-gamma production. J Immunol. 2015;194(4):1954–62.PubMedCrossRef Keppel MP, Saucier N, Mah AY, Vogel TP, Cooper MA. Activation-specific metabolic requirements for NK cell IFN-gamma production. J Immunol. 2015;194(4):1954–62.PubMedCrossRef
30.
go back to reference Wang Z, Guan D, Wang S, Chai LYA, Xu S, Lam KP. Glycolysis and oxidative phosphorylation play critical roles in natural killer cell receptor-mediated natural killer cell functions. Front Immunol. 2020;11:202.PubMedPubMedCentralCrossRef Wang Z, Guan D, Wang S, Chai LYA, Xu S, Lam KP. Glycolysis and oxidative phosphorylation play critical roles in natural killer cell receptor-mediated natural killer cell functions. Front Immunol. 2020;11:202.PubMedPubMedCentralCrossRef
31.
go back to reference Michelet X, Dyck L, Hogan A, Loftus RM, Duquette D, Wei K, Beyaz S, et al. Metabolic reprogramming of natural killer cells in obesity limits antitumor responses. Nat Immunol. 2018;19(12):1330–40.PubMedCrossRef Michelet X, Dyck L, Hogan A, Loftus RM, Duquette D, Wei K, Beyaz S, et al. Metabolic reprogramming of natural killer cells in obesity limits antitumor responses. Nat Immunol. 2018;19(12):1330–40.PubMedCrossRef
32.
go back to reference Tobin LM, Mavinkurve M, Carolan E, Kinlen D, O'Brien EC, Little MA, Finlay DK, et al. NK cells in childhood obesity are activated, metabolically stressed, and functionally deficient. JCI Insight. 2017;2(24):e94939.PubMedCentralCrossRef Tobin LM, Mavinkurve M, Carolan E, Kinlen D, O'Brien EC, Little MA, Finlay DK, et al. NK cells in childhood obesity are activated, metabolically stressed, and functionally deficient. JCI Insight. 2017;2(24):e94939.PubMedCentralCrossRef
33.
go back to reference Cichocki F, Wu CY, Zhang B, Felices M, Tesi B, Tuininga K, Dougherty P, et al. ARID5B regulates metabolic programming in human adaptive NK cells. J Exp Med. 2018;215(9):2379–95.PubMedPubMedCentralCrossRef Cichocki F, Wu CY, Zhang B, Felices M, Tesi B, Tuininga K, Dougherty P, et al. ARID5B regulates metabolic programming in human adaptive NK cells. J Exp Med. 2018;215(9):2379–95.PubMedPubMedCentralCrossRef
34.
go back to reference Pan YX, Ye Q, Shao WX, Shang SQ, Mao JH, Zhang T, Shen HQ, et al. Relationship between immune parameters and organ involvement in children with Henoch-Schonlein purpura. PLoS One. 2014;9(12):e115261.PubMedPubMedCentralCrossRef Pan YX, Ye Q, Shao WX, Shang SQ, Mao JH, Zhang T, Shen HQ, et al. Relationship between immune parameters and organ involvement in children with Henoch-Schonlein purpura. PLoS One. 2014;9(12):e115261.PubMedPubMedCentralCrossRef
35.
go back to reference Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001;22(11):633–40.PubMedCrossRef Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001;22(11):633–40.PubMedCrossRef
37.
go back to reference Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol. 2011;27:441–64.CrossRefPubMed Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol. 2011;27:441–64.CrossRefPubMed
38.
go back to reference Donnelly RP, Finlay DK. Glucose, glycolysis and lymphocyte responses. Mol Immunol. 2015;68(2 Pt C):513–9.PubMedCrossRef Donnelly RP, Finlay DK. Glucose, glycolysis and lymphocyte responses. Mol Immunol. 2015;68(2 Pt C):513–9.PubMedCrossRef
40.
go back to reference Trapani S, Micheli A, Grisolia F, Resti M, Chiappini E, Falcini F, De Martino M. Henoch Schonlein purpura in childhood: epidemiological and clinical analysis of 150 cases over a 5-year period and review of literature. Semin Arthritis Rheum. 2005;35(3):143–53.PubMedCrossRef Trapani S, Micheli A, Grisolia F, Resti M, Chiappini E, Falcini F, De Martino M. Henoch Schonlein purpura in childhood: epidemiological and clinical analysis of 150 cases over a 5-year period and review of literature. Semin Arthritis Rheum. 2005;35(3):143–53.PubMedCrossRef
42.
go back to reference Xiong LJ, Tong Y, Wang ZL, Mao M. Is helicobacter pylori infection associated with Henoch-Schonlein purpura in Chinese children? A meta-analysis. World J Pediatr. 2012;8(4):301–8.PubMedCrossRef Xiong LJ, Tong Y, Wang ZL, Mao M. Is helicobacter pylori infection associated with Henoch-Schonlein purpura in Chinese children? A meta-analysis. World J Pediatr. 2012;8(4):301–8.PubMedCrossRef
43.
go back to reference Yang M, Li FG, Xie XS, Wang SQ, Fan JM. CagA, a major virulence factor of helicobacter pylori, promotes the production and underglycosylation of IgA1 in DAKIKI cells. Biochem Biophys Res Commun. 2014;444(2):276–81.PubMedCrossRef Yang M, Li FG, Xie XS, Wang SQ, Fan JM. CagA, a major virulence factor of helicobacter pylori, promotes the production and underglycosylation of IgA1 in DAKIKI cells. Biochem Biophys Res Commun. 2014;444(2):276–81.PubMedCrossRef
44.
go back to reference Saulsbury FT. Henoch-Schonlein purpura in children. Report of 100 patients and review of the literature. Medicine (Baltimore). 1999;78(6):395–409.CrossRef Saulsbury FT. Henoch-Schonlein purpura in children. Report of 100 patients and review of the literature. Medicine (Baltimore). 1999;78(6):395–409.CrossRef
45.
go back to reference Blanca IR, Bere EW, Young HA, Ortaldo JR. Human B cell activation by autologous NK cells is regulated by CD40-CD40 ligand interaction: role of memory B cells and CD5+ B cells. J Immunol. 2001;167(11):6132–9.PubMedCrossRef Blanca IR, Bere EW, Young HA, Ortaldo JR. Human B cell activation by autologous NK cells is regulated by CD40-CD40 ligand interaction: role of memory B cells and CD5+ B cells. J Immunol. 2001;167(11):6132–9.PubMedCrossRef
46.
go back to reference Luo S, Liang G, Zhang P, Zhao M, Lu Q. Aberrant histone modifications in peripheral blood mononuclear cells from patients with Henoch-Schonlein purpura. Clin Immunol. 2013;146(3):165–75.PubMedCrossRef Luo S, Liang G, Zhang P, Zhao M, Lu Q. Aberrant histone modifications in peripheral blood mononuclear cells from patients with Henoch-Schonlein purpura. Clin Immunol. 2013;146(3):165–75.PubMedCrossRef
48.
go back to reference Masuda M, Nakanishi K, Yoshizawa N, Iijima K, Yoshikawa N. Group a streptococcal antigen in the glomeruli of children with Henoch-Schonlein nephritis. Am J Kidney Dis. 2003;41(2):366–70.PubMedCrossRef Masuda M, Nakanishi K, Yoshizawa N, Iijima K, Yoshikawa N. Group a streptococcal antigen in the glomeruli of children with Henoch-Schonlein nephritis. Am J Kidney Dis. 2003;41(2):366–70.PubMedCrossRef
49.
go back to reference Carrega P, Bonaccorsi I, Di Carlo E, Morandi B, Paul P, Rizzello V, Cipollone G, et al. CD56(bright) perforin (low) noncytotoxic human NK cells are abundant in both healthy and neoplastic solid tissues and recirculate to secondary lymphoid organs via afferent lymph. J Immunol. 2014;192(8):3805–15.PubMedCrossRef Carrega P, Bonaccorsi I, Di Carlo E, Morandi B, Paul P, Rizzello V, Cipollone G, et al. CD56(bright) perforin (low) noncytotoxic human NK cells are abundant in both healthy and neoplastic solid tissues and recirculate to secondary lymphoid organs via afferent lymph. J Immunol. 2014;192(8):3805–15.PubMedCrossRef
51.
go back to reference Irabu H, Shimizu M, Kaneko S, Inoue N, Mizuta M, Tasaki Y, Ohta K, et al. Apoptosis inhibitor of macrophage as a biomarker for disease activity inJapanese children with IgA nephropathy and Henoch-Schonlein purpura nephritis. Pediatr Research. 2020 May 14. https://doi.org/10.1038/s41390-020-0951-1. Irabu H, Shimizu M, Kaneko S, Inoue N, Mizuta M, Tasaki Y, Ohta K, et al. Apoptosis inhibitor of macrophage as a biomarker for disease activity inJapanese children with IgA nephropathy and Henoch-Schonlein purpura nephritis. Pediatr Research. 2020 May 14. https://​doi.​org/​10.​1038/​s41390-020-0951-1.
52.
go back to reference Yuan L, Wang Q, Zhang S, Zhang L. Correlation between serum inflammatory factors TNF-alpha, IL-8, IL-10 and Henoch-Schonlein purpura with renal function impairment. Exp Ther Med. 2018;15(4):3924–8.PubMedPubMedCentral Yuan L, Wang Q, Zhang S, Zhang L. Correlation between serum inflammatory factors TNF-alpha, IL-8, IL-10 and Henoch-Schonlein purpura with renal function impairment. Exp Ther Med. 2018;15(4):3924–8.PubMedPubMedCentral
53.
go back to reference Wensveen FM, Jelencic V, Valentic S, Sestan M, Wensveen TT, Theurich S, Glasner A, et al. NK cells link obesity-induced adipose stress to inflammation and insulin resistance. Nat Immunol. 2015;16(4):376–85.PubMedCrossRef Wensveen FM, Jelencic V, Valentic S, Sestan M, Wensveen TT, Theurich S, Glasner A, et al. NK cells link obesity-induced adipose stress to inflammation and insulin resistance. Nat Immunol. 2015;16(4):376–85.PubMedCrossRef
54.
go back to reference Lee BC, Kim MS, Pae M, Yamamoto Y, Eberle D, Shimada T, Kamei N, et al. Adipose natural killer cells regulate adipose tissue macrophages to promote insulin resistance in obesity. Cell Metab. 2016;23(4):685–98.PubMedPubMedCentralCrossRef Lee BC, Kim MS, Pae M, Yamamoto Y, Eberle D, Shimada T, Kamei N, et al. Adipose natural killer cells regulate adipose tissue macrophages to promote insulin resistance in obesity. Cell Metab. 2016;23(4):685–98.PubMedPubMedCentralCrossRef
55.
go back to reference Zhou H, Xie X, Jiang B, Ke C. NKp46+ lamina propria natural killer cells undergo metabolic reprogramming in a mouse experimental colitis model. Inflamm Res. 2020;69(4):401–14.PubMedCrossRef Zhou H, Xie X, Jiang B, Ke C. NKp46+ lamina propria natural killer cells undergo metabolic reprogramming in a mouse experimental colitis model. Inflamm Res. 2020;69(4):401–14.PubMedCrossRef
56.
go back to reference Chang CH, Curtis JD, Maggi LB Jr, Faubert B, Villarino AV, O'Sullivan D, Huang SC, et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell. 2013;153(6):1239–51.PubMedPubMedCentralCrossRef Chang CH, Curtis JD, Maggi LB Jr, Faubert B, Villarino AV, O'Sullivan D, Huang SC, et al. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell. 2013;153(6):1239–51.PubMedPubMedCentralCrossRef
57.
go back to reference Schafer JR, Salzillo TC, Chakravarti N, Kararoudi MN, Trikha P, Foltz JA, Wang R, et al. Education-dependent activation of glycolysis promotes the cytolytic potency of licensed human natural killer cells. J Allergy Clin Immunol. 2019;143(1):346–58 e6.PubMedCrossRef Schafer JR, Salzillo TC, Chakravarti N, Kararoudi MN, Trikha P, Foltz JA, Wang R, et al. Education-dependent activation of glycolysis promotes the cytolytic potency of licensed human natural killer cells. J Allergy Clin Immunol. 2019;143(1):346–58 e6.PubMedCrossRef
58.
go back to reference Pfeifer C, Highton AJ, Peine S, Sauter J, Schmidt AH, Bunders MJ, Altfeld M, et al. Natural killer cell education is associated with a distinct glycolytic profile. Front Immunol. 2018;9:3020.PubMedPubMedCentralCrossRef Pfeifer C, Highton AJ, Peine S, Sauter J, Schmidt AH, Bunders MJ, Altfeld M, et al. Natural killer cell education is associated with a distinct glycolytic profile. Front Immunol. 2018;9:3020.PubMedPubMedCentralCrossRef
59.
go back to reference Miranda D, Jara C, Ibanez J, Ahumada V, Acuna-Castillo C, Martin A, Cordova A, et al. PGC-1alpha-dependent mitochondrial adaptation is necessary to sustain IL-2-induced activities in human NK cells. Mediat Inflamm. 2016;2016:9605253.CrossRef Miranda D, Jara C, Ibanez J, Ahumada V, Acuna-Castillo C, Martin A, Cordova A, et al. PGC-1alpha-dependent mitochondrial adaptation is necessary to sustain IL-2-induced activities in human NK cells. Mediat Inflamm. 2016;2016:9605253.CrossRef
60.
go back to reference Assmann N, O'Brien KL, Donnelly RP, Dyck L, Zaiatz-Bittencourt V, Loftus RM, Heinrich P, et al. Srebp-controlled glucose metabolism is essential for NK cell functional responses. Nat Immunol. 2017;18(11):1197–206.PubMedCrossRef Assmann N, O'Brien KL, Donnelly RP, Dyck L, Zaiatz-Bittencourt V, Loftus RM, Heinrich P, et al. Srebp-controlled glucose metabolism is essential for NK cell functional responses. Nat Immunol. 2017;18(11):1197–206.PubMedCrossRef
61.
go back to reference Loftus RM, Assmann N, Kedia-Mehta N, O'Brien KL, Garcia A, Gillespie C, Hukelmann JL, et al. Amino acid-dependent cMyc expression is essential for NK cell metabolic and functional responses in mice. Nat Commun. 2018;9(1):2341.PubMedPubMedCentralCrossRef Loftus RM, Assmann N, Kedia-Mehta N, O'Brien KL, Garcia A, Gillespie C, Hukelmann JL, et al. Amino acid-dependent cMyc expression is essential for NK cell metabolic and functional responses in mice. Nat Commun. 2018;9(1):2341.PubMedPubMedCentralCrossRef
62.
go back to reference Ruperto N, Ozen S, Pistorio A, Dolezalova P, Brogan P, Cabral DA, Cuttica R, et al. EULAR/PRINTO/PRES criteria for Henoch-Schonlein purpura, childhood polyarteritis nodosa, childhood Wegener granulomatosis and childhood Takayasu arteritis: Ankara 2008. Part I: overall methodology and clinical characterisation. Ann Rheum Dis. 2010;69(5):790–7.PubMedCrossRef Ruperto N, Ozen S, Pistorio A, Dolezalova P, Brogan P, Cabral DA, Cuttica R, et al. EULAR/PRINTO/PRES criteria for Henoch-Schonlein purpura, childhood polyarteritis nodosa, childhood Wegener granulomatosis and childhood Takayasu arteritis: Ankara 2008. Part I: overall methodology and clinical characterisation. Ann Rheum Dis. 2010;69(5):790–7.PubMedCrossRef
Metadata
Title
Decreased glycolysis induced dysfunction of NK cells in Henoch-Schonlein purpura patients
Authors
Wenjia Chai
Xiaolin Wang
Wei Wang
Hui Wang
Wenjun Mou
Jingang Gui
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Immunology / Issue 1/2020
Electronic ISSN: 1471-2172
DOI
https://doi.org/10.1186/s12865-020-00382-9

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