Characteristics and molecular mechanism of tumor necrosis factor tolerance_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

 LIU Hong ¹ , YANG Lian ² ,  GONG Jianping ²

1. Department of Hepatobiliary Surgery, The People’s Hospital of Chongqing Changshou District, Changshou, Chongqing 401220, P. R. China;
2. Department of Hepatobiliary Surgery, The Second Affiliated Hospital of Chongqing Medical University, Chongqing 400010, P. R. China;

Corresponding author：

GONG Jianping, Email: gongjianping11@126.com

Keywords：

tumor necrosis factor tolerance; inflammation; mechanism; review

DOI：

10.7507/1007-9424.202205003

Video：

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Objective To summarize and evaluate the significance of tumor necrosis factor (TNF) tolerance, and to understand the general characteristics and known molecular mechanisms of different forms of tolerance, including the roles of transcription factors, signaling systems and receptors. Method The relevant literatures at home and abroad in recent years were collected and readed, and the content related to TNF tolerance was summarized. Results TNF tolerance could be produced after TNF pretreatment, and be divided into absolute tolerance and induced tolerance. TNF tolerance was related to a variety of interrelated and interdependent intracellular signal transduction. There was cross tolerance between TNF and lipopolysaccharide. Conclusions TNF tolerance may represent a protective mechanism, participating in the termination of inflammation and preventing excessive or persistent inflammation. TNF tolerance may also trigger immune paralysis, leading to severe inflammatory diseases, such as sepsis. The understanding of TNF tolerance can promote the diagnosis of inflammation related diseases or the implementation of treatment methods, so as to achieve more accurate evaluation and treatment.

Citation： LIU Hong, YANG Lian, GONG Jianping. Characteristics and molecular mechanism of tumor necrosis factor tolerance. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2022, 29(12): 1644-1647. doi: 10.7507/1007-9424.202205003 Copy

1.	McMillan D, Martinez-Fleites C, Porter J, et al. Structural insights into the disruption of TNF-TNFR1 signalling by small molecules stabilising a distorted TNF. Nat Commun, 2021, 12(1): 582. doi:10.1038/s41467-020-20828-3.
2.	Brinkworth JF, Valizadegan N. Sepsis and the evolution of human increased sensitivity to lipopolysaccharide. Evol Anthropol, 2021, 30(2): 141-157.
3.	Günther J, Vogt N, Hampel K, et al. Identification of two forms of TNF tolerance in human monocytes: differential inhibition of NF-κB/AP-1- and PP1-associated signaling. J Immunol, 2014, 192(7): 3143-3155.
4.	Welz B, Bikker R, Junemann J, et al. Proteome and phosphoproteome analysis in TNF long term-exposed primary human monocytes. Int J Mol Sci, 2019, 20(5): 1241. doi: 10.3390/ijms20051241.
5.	Bernard Q, Hu LT. Innate immune memory to repeated exposure Borrelia burgdorferi correlates with murine in vivo inflammatory phenotypes. J Immunol, 2020, 205(12): 3383-3389.
6.	Li LL, Dai B, Sun YH, et al. Monocytes undergo functional reprogramming to generate immunosuppression through HIF-1α signaling pathway in the late phase of sepsis. Mediators Inflamm, 2020, 2020: 4235909. doi:10.1155/2020/4235909.
7.	Piras IS, Gerhard GS, DiStefano JK. Palmitate and fructose interact to induce human hepatocytes to produce pro-fibrotic transcriptional responses in hepatic stellate cells exposed to conditioned media. Cell Physiol Biochem, 2020, 54(5): 1068-1082.
8.	Pietrzak J, Gronkowska K, Robaszkiewicz A. PARP traps rescue the pro-inflammatory response of human macrophages in the in vitro model of LPS-induced tolerance. Pharmaceuticals (Basel), 2021, 14(2): 170. doi:10.3390/ph14020170.
9.	Zhao S, Jiang J, Jing Y, et al. The concentration of tumor necrosis factor-α determines its protective or damaging effect on liver injury by regulating Yap activity. Cell Death Dis, 2020, 11(1): 70. doi:10.1038/s41419-020-2264-z.
10.	Mul Fedele ML, Aiello I, Caldart CS, et al. Differential thermoregulatory and inflammatory patterns in the circadian response to LPS-induced septic shock. Front Cell Infect Microbiol, 2020, 10: 100. doi:10.3389/fcimb.2020.00100.
11.	Huber R, Bikker R, Welz B, et al. TNF tolerance in monocytes and macrophages: characteristics and molecular mechanisms. J Immunol Res, 2017, 2017: 9570129. doi:10.1155/2017/9570129.
12.	VanderVeen BN, Fix DK, Carson JA. Disrupted skeletal muscle mitochondrial dynamics, mitophagy, and biogenesis during cancer cachexia: a role for inflammation. Oxid Med Cell Longev, 2017, 2017: 3292087. doi:10.1155/2017/3292087.
13.	Mo R, Feng XX, Wu YN, et al. Hepatocytes paradoxically affect intrahepatic IFN-γ production in autoimmune hepatitis due to Gal-9 expression and TLR2/4 ligand release. Mol Immunol, 2020, 123: 106-115.
14.	Yue Y, Wang Y, Li D, et al. A central role for the mammalian target of rapamycin in LPS-induced anorexia in mice. J Endocrinol, 2015, 224(1): 37-47.
15.	Ozkaynak MF, Gilman AL, London WB, et al. A Comprehensive safety trial of chimeric antibody 14.18 with GM-CSF, IL-2, and isotretinoin in high-risk neuroblastoma patients following myeloablative therapy: children's oncology group study ANBL0931. Front Immunol, 2018, 9: 1355. doi:10.3389/fimmu.2018.01355.
16.	Tiegs G, Horst AK. TNF in the liver: targeting a central player in inflammation. Semin Immunopathol, 2022, 44(4): 445-459.
17.	Stutte S, Ruf J, Kugler I, et al. Type Ⅰ interferon mediated induction of somatostatin leads to suppression of ghrelin and appetite thereby promoting viral immunity in mice. Brain Behav Immun, 2021, 95: 429-443.
18.	Dhani S, Zhao Y, Zhivotovsky B. A long way to go: caspase inhibitors in clinical use. Cell Death Dis, 2021, 12(10): 949. doi:10.1038/s41419-021-04240-3.
19.	Akashi-Takamura S, Furuta T, Takahashi K, et al. Agonistic antibody to TLR4/MD-2 protects mice from acute lethal hepatitis induced by TNF-alpha. J Immunol, 2006, 176(7): 4244-4251.
20.	Clark IA, Vissel B. Therapeutic implications of how TNF links apolipoprotein E, phosphorylated tau, α-synuclein, amyloid-β and insulin resistance in neurodegenerative diseases. Br J Pharmacol, 2018, 175(20): 3859-3875.
21.	Hoffmeister L, Diekmann M, Brand K, et al. GSK3: a kinase balancing promotion and resolution of inflammation. Cells, 2020, 9(4): 820. doi:10.3390/cells9040820.
22.	Hou XF, Pan H, Xu LH, et al. Piperine suppresses the expression of CXCL8 in lipopolysaccharide-activated SW480 and HT-29 cells via downregulating the mitogen-activated protein kinase pathways. Inflammation, 2015, 38(3): 1093-1102.
23.	Wang Z, Sheng C, Kan G, et al. RNAi screening identifies that TEX10 promotes the proliferation of colorectal cancer cells by increasing NF-κB activation. Adv Sci (Weinh), 2020, 7(17): 2000593. doi: 10.1002/advs.202000593.
24.	Wang P, Wang Y, Peng H, et al. Functional rare variant in a C/EBPbeta binding site in NINJ2 gene increases the risk of coronary artery disease. Aging (Albany NY), 2021, 13(23): 25393-25407.
25.	Yang P, Liu L, Sun L, et al. Immunological feature and transcriptional signaling of Ly6C monocyte subsets from transcriptome analysis in control and hyperhomocysteinemic mice. Front Immunol, 2021, 12: 632333. doi:10.3389/fimmu.2021.632333.
26.	Piazzi M, Bavelloni A, Faenza I, et al. Glycogen synthase kinase (GSK)-3 and the double-strand RNA-dependent kinase, PKR: When two kinases for the common good turn bad. Biochim Biophys Acta Mol Cell Res, 2020, 1867(10): 118769. doi:10.1016/j.bbamcr. 2020. 118769.
27.	Bechara R, Amatya N, Bailey RD, et al. The m6A reader IMP2 directs autoimmune inflammation through an IL-17- and TNFα-dependent C/EBP transcription factor axis. Sci Immunol, 2021, 6(61): eabd1287. doi:10.1126/sciimmunol.abd1287.
28.	Sabio G, Davis RJ. TNF and MAP kinase signalling pathways. Semin Immunol, 2014, 26(3): 237-245.
29.	Sass G, Shembade ND, Tiegs G. Tumour necrosis factor alpha (TNF)-TNF receptor 1-inducible cytoprotective proteins in the mouse liver: relevance of suppressors of cytokine signalling. Biochem J, 2005, 385(Pt 2): 537-544.
30.	Zhao W, Bendickson L, Nilsen-Hamilton M. The Lipocalin2 gene is regulated in mammary epithelial cells by NFκB and C/EBP in response to mycoplasma. Sci Rep, 2020, 10(1): 7641. doi:10.1038/s41598-020-63393-x.
31.	Aksentijevich I, Soriano A, Hernández-Rodríguez J. Editorial: autoinflammatory diseases: from genes to bedside. Front Immunol, 2020, 11: 1177. doi:10.3389/fimmu.2020.01177.
32.	Nawab A, An L, Wu J, et al. Chicken toll-like receptors and their significance in immune response and disease resistance. Int Rev Immunol, 2019, 38(6): 284-306.
33.	Weyand CM, Goronzy JJ. The immunology of rheumatoid arthritis. Nat Immunol, 2021, 22(1): 10-18.
34.	Mendes AFM, Gomes CM, Kurizky PS, et al. Case report: a case series of immunobiological therapy (Anti-TNF-α) for patients with erythema nodosum leprosum. Front Med (Lausanne), 2022, 9: 879527. doi: 10.3389/fmed.2022.879527.

1. McMillan D, Martinez-Fleites C, Porter J, et al. Structural insights into the disruption of TNF-TNFR1 signalling by small molecules stabilising a distorted TNF. Nat Commun, 2021, 12(1): 582. doi:10.1038/s41467-020-20828-3.
2. Brinkworth JF, Valizadegan N. Sepsis and the evolution of human increased sensitivity to lipopolysaccharide. Evol Anthropol, 2021, 30(2): 141-157.
3. Günther J, Vogt N, Hampel K, et al. Identification of two forms of TNF tolerance in human monocytes: differential inhibition of NF-κB/AP-1- and PP1-associated signaling. J Immunol, 2014, 192(7): 3143-3155.
4. Welz B, Bikker R, Junemann J, et al. Proteome and phosphoproteome analysis in TNF long term-exposed primary human monocytes. Int J Mol Sci, 2019, 20(5): 1241. doi: 10.3390/ijms20051241.
5. Bernard Q, Hu LT. Innate immune memory to repeated exposure Borrelia burgdorferi correlates with murine in vivo inflammatory phenotypes. J Immunol, 2020, 205(12): 3383-3389.
6. Li LL, Dai B, Sun YH, et al. Monocytes undergo functional reprogramming to generate immunosuppression through HIF-1α signaling pathway in the late phase of sepsis. Mediators Inflamm, 2020, 2020: 4235909. doi:10.1155/2020/4235909.
7. Piras IS, Gerhard GS, DiStefano JK. Palmitate and fructose interact to induce human hepatocytes to produce pro-fibrotic transcriptional responses in hepatic stellate cells exposed to conditioned media. Cell Physiol Biochem, 2020, 54(5): 1068-1082.
8. Pietrzak J, Gronkowska K, Robaszkiewicz A. PARP traps rescue the pro-inflammatory response of human macrophages in the in vitro model of LPS-induced tolerance. Pharmaceuticals (Basel), 2021, 14(2): 170. doi:10.3390/ph14020170.
9. Zhao S, Jiang J, Jing Y, et al. The concentration of tumor necrosis factor-α determines its protective or damaging effect on liver injury by regulating Yap activity. Cell Death Dis, 2020, 11(1): 70. doi:10.1038/s41419-020-2264-z.
10. Mul Fedele ML, Aiello I, Caldart CS, et al. Differential thermoregulatory and inflammatory patterns in the circadian response to LPS-induced septic shock. Front Cell Infect Microbiol, 2020, 10: 100. doi:10.3389/fcimb.2020.00100.
11. Huber R, Bikker R, Welz B, et al. TNF tolerance in monocytes and macrophages: characteristics and molecular mechanisms. J Immunol Res, 2017, 2017: 9570129. doi:10.1155/2017/9570129.
12. VanderVeen BN, Fix DK, Carson JA. Disrupted skeletal muscle mitochondrial dynamics, mitophagy, and biogenesis during cancer cachexia: a role for inflammation. Oxid Med Cell Longev, 2017, 2017: 3292087. doi:10.1155/2017/3292087.
13. Mo R, Feng XX, Wu YN, et al. Hepatocytes paradoxically affect intrahepatic IFN-γ production in autoimmune hepatitis due to Gal-9 expression and TLR2/4 ligand release. Mol Immunol, 2020, 123: 106-115.
14. Yue Y, Wang Y, Li D, et al. A central role for the mammalian target of rapamycin in LPS-induced anorexia in mice. J Endocrinol, 2015, 224(1): 37-47.
15. Ozkaynak MF, Gilman AL, London WB, et al. A Comprehensive safety trial of chimeric antibody 14.18 with GM-CSF, IL-2, and isotretinoin in high-risk neuroblastoma patients following myeloablative therapy: children's oncology group study ANBL0931. Front Immunol, 2018, 9: 1355. doi:10.3389/fimmu.2018.01355.
16. Tiegs G, Horst AK. TNF in the liver: targeting a central player in inflammation. Semin Immunopathol, 2022, 44(4): 445-459.
17. Stutte S, Ruf J, Kugler I, et al. Type Ⅰ interferon mediated induction of somatostatin leads to suppression of ghrelin and appetite thereby promoting viral immunity in mice. Brain Behav Immun, 2021, 95: 429-443.
18. Dhani S, Zhao Y, Zhivotovsky B. A long way to go: caspase inhibitors in clinical use. Cell Death Dis, 2021, 12(10): 949. doi:10.1038/s41419-021-04240-3.
19. Akashi-Takamura S, Furuta T, Takahashi K, et al. Agonistic antibody to TLR4/MD-2 protects mice from acute lethal hepatitis induced by TNF-alpha. J Immunol, 2006, 176(7): 4244-4251.
20. Clark IA, Vissel B. Therapeutic implications of how TNF links apolipoprotein E, phosphorylated tau, α-synuclein, amyloid-β and insulin resistance in neurodegenerative diseases. Br J Pharmacol, 2018, 175(20): 3859-3875.
21. Hoffmeister L, Diekmann M, Brand K, et al. GSK3: a kinase balancing promotion and resolution of inflammation. Cells, 2020, 9(4): 820. doi:10.3390/cells9040820.
22. Hou XF, Pan H, Xu LH, et al. Piperine suppresses the expression of CXCL8 in lipopolysaccharide-activated SW480 and HT-29 cells via downregulating the mitogen-activated protein kinase pathways. Inflammation, 2015, 38(3): 1093-1102.
23. Wang Z, Sheng C, Kan G, et al. RNAi screening identifies that TEX10 promotes the proliferation of colorectal cancer cells by increasing NF-κB activation. Adv Sci (Weinh), 2020, 7(17): 2000593. doi: 10.1002/advs.202000593.
24. Wang P, Wang Y, Peng H, et al. Functional rare variant in a C/EBPbeta binding site in NINJ2 gene increases the risk of coronary artery disease. Aging (Albany NY), 2021, 13(23): 25393-25407.
25. Yang P, Liu L, Sun L, et al. Immunological feature and transcriptional signaling of Ly6C monocyte subsets from transcriptome analysis in control and hyperhomocysteinemic mice. Front Immunol, 2021, 12: 632333. doi:10.3389/fimmu.2021.632333.
26. Piazzi M, Bavelloni A, Faenza I, et al. Glycogen synthase kinase (GSK)-3 and the double-strand RNA-dependent kinase, PKR: When two kinases for the common good turn bad. Biochim Biophys Acta Mol Cell Res, 2020, 1867(10): 118769. doi:10.1016/j.bbamcr. 2020. 118769.
27. Bechara R, Amatya N, Bailey RD, et al. The m6A reader IMP2 directs autoimmune inflammation through an IL-17- and TNFα-dependent C/EBP transcription factor axis. Sci Immunol, 2021, 6(61): eabd1287. doi:10.1126/sciimmunol.abd1287.
28. Sabio G, Davis RJ. TNF and MAP kinase signalling pathways. Semin Immunol, 2014, 26(3): 237-245.
29. Sass G, Shembade ND, Tiegs G. Tumour necrosis factor alpha (TNF)-TNF receptor 1-inducible cytoprotective proteins in the mouse liver: relevance of suppressors of cytokine signalling. Biochem J, 2005, 385(Pt 2): 537-544.
30. Zhao W, Bendickson L, Nilsen-Hamilton M. The Lipocalin2 gene is regulated in mammary epithelial cells by NFκB and C/EBP in response to mycoplasma. Sci Rep, 2020, 10(1): 7641. doi:10.1038/s41598-020-63393-x.
31. Aksentijevich I, Soriano A, Hernández-Rodríguez J. Editorial: autoinflammatory diseases: from genes to bedside. Front Immunol, 2020, 11: 1177. doi:10.3389/fimmu.2020.01177.
32. Nawab A, An L, Wu J, et al. Chicken toll-like receptors and their significance in immune response and disease resistance. Int Rev Immunol, 2019, 38(6): 284-306.
33. Weyand CM, Goronzy JJ. The immunology of rheumatoid arthritis. Nat Immunol, 2021, 22(1): 10-18.
34. Mendes AFM, Gomes CM, Kurizky PS, et al. Case report: a case series of immunobiological therapy (Anti-TNF-α) for patients with erythema nodosum leprosum. Front Med (Lausanne), 2022, 9: 879527. doi: 10.3389/fmed.2022.879527.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Characteristics and molecular mechanism of tumor necrosis factor tolerance

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