Cited by 1,768Cytokine Signaling Pathways and InteractionsImmune Response and InflammationT-cell and B-cell Immunology

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Impaired immune and acute-phase responses in interleukin-6-deficient mice

Kopf, Manfred, Baumann, Heinz, Freer, Giulia, Freudenberg, Marina, Lamers, Marinus, Kishimoto, Tadamitsu, Zinkernagel, Rolf, Bluethmann, Horst, Köhler, Georges·1994·Nature

DOI 10.1038/368339a0

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Abstract

Interleukin-6 (IL-6) is a multifunctional cytokine that regulates various aspects of the immune response, acute-phase reaction and haematopoiesis (for reviews see refs 1, 2). In vitro, leukaemia inhibitory factor, oncostatin M, ciliary neurotrophic factor and interleukin-11 display overlapping activities with IL-6. This functional redundancy may be explained by the interactions of specific binding receptors with a common signal-transducing receptor (gp130) (for reviews see refs 3, 4). To elucidate the unique function of IL-6 in vivo, we have disrupted the IL-6 gene by homologous recombination. IL-6-deficient mice develop normally. They fail to control efficiently vaccinia virus and infection with Listeria monocytogenes, a facultative intracellular bacterium. The T-cell-dependent antibody response against vesicular stomatitis virus is impaired. Further, the inflammatory acute-phase response after tissue damage or infection is severely compromised, whereas it is only moderately affected after challenge with lipopolysaccharide. We conclude that IL-6 production induced by injury or infection is an important in vivo SOS signal which coordinates activities of liver cells, macrophages and lymphocytes.

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Background
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Background
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Background
Tocilizumab for the treatment of adult patients with severe COVID‐19 pneumonia: A single‐center cohort study
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Background
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Background
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Method
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BackgroundInfluential
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Self-citation
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Background
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Background
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Background
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“and acute-phase responses in mice [8].”
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“Tph1 and Il6 double knockout mice (Tph1-Il6DKO) were bred according to see supplementary material, Figure S1 and genotyped as described previously [19,22].”
Method
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“Surprisingly, IL-6 deficiency does not alter mature numbers of macrophages in vivo, but does make IL-6-/- mice succumb to infections by Listeria monocytogenes—a bacterium that survives and proliferates in macrophages (43).”
Background
Cytokines and persistent viral infections
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“Depending on the injury model, IL6 KO animals show a compromised inflammatory response, gliosis, and specific neuronal survival (Kopf et al., 1994; Penkowa et al., 1999; Murphy et al., 2000; Swartz et al., 2001; Poulsen et al., 2005).”
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BackgroundMethod
INVOLVEMENT OF INTERLEUKIN-6 AND TUMOR NECROSIS FACTOR α IN CYP3A11 AND 2C29 DOWN-REGULATION BY BACILLUS CALMETTE-GUÉRIN AND LIPOPOLYSACCHARIDE IN MOUSE LIVER
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“The IL-1 / KO mice were established by Horai et al. (1998), the TNF KO mice were established by Tagawa et al. (1997), and the IL-6 KO mice were established by Kopf et al. (1994).”
Method
Effect of interleukin 1 and leukaemia inhibitory factor on chondrocyte metabolism in articular cartilage from normal and interleukin-6-deficient mice: role of nitric oxide and IL-6 in the suppression of proteoglycan synthesis.
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Interleukin‐10 Directly Inhibits the Interleukin‐6 Production in T‐Cells
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“These IL-6 KO mice also demonstrated increased susceptibility to Listeria monocytogenes infection, possibly due to reduced bactericidal activity of macrophages [11].”
Mitogen-activated protein kinases (MAPKs) regulate IL-6 over-production during concomitant influenza virus and Staphylococcus aureus infection
Klemm, C., Bruchhagen, C., van Krüchten, A., Niemann, S., Löffler, B., Peters, G., Ludwig, S., & Ehrhardt, C. (2017) · Scientific Reports · doi:10.1038/srep42473 · Cited by 46
“In contrast, the serum levels of the APP SAA and mRNA levels of ORM , whose expression is strongly dependent on IL-6 in mice and humans 28,29 , were significantly enhanced after super-infection compared to IV-infected mice (Fig.”
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Saquib, Q., Siddiqui, M., Ahmed, J., Al-Salim, A., Ansari, S. M., Faisal, M., Al-khedhairy, A., Musarrat, J., Alwathnani, H., Alatar, A., et al. (2016) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2016.01.025 · Cited by 42
A Critical Role of the Transcription Factor Fli‐1 in Murine Lupus Development by Regulation of Interleukin‐6 Expression
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Contribution of vascular cell-derived cytokines to innate and inflammatory pathways in atherogenesis
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“Among the secondary cytokines produced in response to IL-1 or TNF- IL-6 is of major interest, because this cytokine is an important activator of the acute phase response [77].”
Background
Expression and self-regulatory function of cardiac interleukin-6 during endotoxemia
Saitō, H., Patterson, C., Hu, Z., Runge, M. S., Tipnis, U. R., Sinha, M., & Papaconstantinou, J. (2000) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2000.279.5.h2241 · Cited by 41
The intestine: A highly dynamic microenvironment for IgA plasma cells
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Phase separation and zinc-induced transition modulate synaptic distribution and association of autism-linked CTTNBP2 and SHANK3
Shih, P.-Y., Fang, Y.-L., Shankar, S., Lee, S., Hu, H., Chen, H., Wang, T., Hsia, K., & Hsueh, Y. (2022) · Nature Communications · doi:10.1038/s41467-022-30353-0 · Cited by 41
The Soluble Interleukin-6 Receptor Is a Mediator of Hematopoietic and Skeletal Actions of Parathyroid Hormone*
Cho, S., Pirih, F. Q., Koh, A., Michalski, M. N., Eber, M. R., Ritchie, K., Sinder, B., Oh, S., Al‐Dujaili, S. A., Lee, J., et al. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.393363 · Cited by 41
“C57B6 IL-6 / mice (25) were kindly provided by Evan Keller (University of Michigan, Ann Arbor, MI), and breeding was established to generate desired genotypes.”
Method
Genetic Variation in Innate Immunity Pathways and Their Potential Contribution to the SIRS/CARS Debate: Evidence from Human Studies and Animal Models
Kumpf, O., & Schumann, R. R. (2010) · Journal of Innate Immunity · doi:10.1159/000314269 · Cited by 40
“In conclusion, according to the animal knockout data, the role of the IL-1 family in sepsis, SIRS and CARS apparently is complex: while IL-1 seems to mediate effects contributing to lethality, other members of this family, as shown by the experiments with the IL-1R knockout mice, seem to also play a protective role du…”
Background
Attenuated fever in rats during late pregnancy is linked to suppressed interleukin‐6 production after localized inflammation with turpentine
Aguilar‐Valles, A., Poole, S., Mistry, Y., Williams, S., & Luheshi, G. N. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.132829 · Cited by 44
“As mentioned earlier, LPS is capable of stimulating several organs to produce fever mediators that act in a highly redundant fashion, as is further evidenced by the lack of effect of targeted mutations (‘knock out’) of cytokines on LPS-febrile response (Kopf et al. 1994; Zheng et al. 1995; Kozak et al. 1997; Leon, 200…”
Background
Interleukin (IL)-6, but not IL-1, induction in the brain downstream of cyclooxygenase-2 is essential for the induction of febrile response against peripheral IL-1alpha.
Kagiwada, K., Dai, C.-D., Sakatani, T., Asano, M., Nambu, A., Kakuta, S., & Iwakura, Y. (2004) · Endocrinology · doi:10.1210/en.2004-0054 · Cited by 41
The therapeutic potential of interleukin-6 in treating obesity
Wallenius, K., Jansson, J., & Wallenius, V. (2003) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.3.7.1061 · Cited by 41
“In one of the first articles describing IL-6 knockout mice, Kopf and co-workers showed that endogenous IL-6 is essential for the immune response to certain intracellular pathogens, such as Listeria monocytogenes, and viruses, for example, vaccinia [22].”
Background
On the site and mechanism of action of the anti-obesity effects of interleukin-6
Jansson, J., Wallenius, K., Asterholm, I. W., Ohlsson, C., Dickson, S. L., & Wallenius, V. (2003) · Growth Hormone & IGF Research · doi:10.1016/s1096-6374(03)00051-0 · Cited by 34
Distinct tumorigenic potential of abl and raf in B cell neoplasia: abl activates the IL-6 signaling pathway
Hilbert, D. M., Migone, T.-S., Kopf, M., Leonard, W. J., & Rudikoff, S. (1996) · Immunity · doi:10.1016/s1074-7613(00)80312-x · Cited by 40
Self-citation
Cancer-Associated Cachexia: A Systemic Consequence of Cancer Progression
Biswas, A., & Acharyya, S. (2019) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-030419-033642 · Cited by 42
“Still, it is important to consider that sustained blockade in IL-6 signaling can increase the risk of infection from neutropenia and result in compensatory increases in the activity of other proinflammatory cytokines (Kopf et al. 1994).”
Background
Anti-IL6 Autoantibodies in an Infant With CRP-Less Septic Shock
Bloomfield, M., Paračková, Z., Cabelova, T., Pospíšilová, I., Kabícek, P., Houšt'ková, H., & Šedivá, A. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02629 · Cited by 50
“Additionally, an IL-6 knockout murine model was shown to develop normally, but the inflammatory acutephase response after tissue damage or infection was severely compromised (14).”
Background
Association between increased serum interleukin-6 levels and sustained attention deficits in patients with major depressive disorder
Ye, G., Yin, G., Tang, Z., Fu, J. L., Chen, J., Chen, S. S., Li, J., Fu, T., Yu, X., Xu, D. W., et al. (2018) · Psychological Medicine · doi:10.1017/s0033291718000090 · Cited by 47
“Interleukin 6 (IL-6) is a multifunctional cytokine that regulates the growth and differentiation of various cells and plays a critical role in immune response and acute phase reactions (Kopf et al. 1994; Kiecolt-Glaser et al. 2003).”
Background
Measles virus nucleocapsid protein increases osteoblast differentiation in Paget’s disease
Teramachi, J., Nagata, Y., Mohammad, K. S., Inagaki, Y., Ohata, Y., Guise, T. A., Michou, L., Brown, J. P., Windle, J. J., Kurihara, N., et al. (2016) · Journal of Clinical Investigation · doi:10.1172/jci82012 · Cited by 46
Cyclooxygenase-1 orchestrates germinal center formation and antibody class-switch via regulation of IL-17
Blaho, V., Buczynski, M. W., Dennis, E., & Brown, C. R. (2009) · Journal of Immunology · doi:10.4049/jimmunol.0901499 · Cited by 40
“IL-6° mice infected with B. burgdorferi, Listeria monocytogenes, or vesicular stomatitis virus, among others, have significantly lowered serum levels of Ag-specific IgG (55, 56).”
Background
Ozone modulates IL-6 secretion in human airway epithelial and smooth muscle cells.
Damera, G., Zhao, H., Wang, M., Smith, M., Kirby, C., Jester, W., Lawson, J., & Panettieri, R. (2009) · American Journal of Physiology - Lung cellular and Molecular Physiology · doi:10.1152/ajplung.90585.2008 · Cited by 40
“suggest a protective role of IL-6 (38).”
IL-6 and Maturation Govern TLR2 and TLR4 Induced TLR Agonist Tolerance and Cross-Tolerance in Dendritic Cells
Geisel, J., Kahl, F., Müller, M., Wagner, H., Kirschning, C. J., Autenrieth, I. B., & Frick, J.-S. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.9.5811 · Cited by 64
“Naive DC were prepared from IL-6 / mice (21) and stimulated as described above.”
BackgroundMethod
Interleukin-6 and CAAT/enhancer binding protein beta-deficient mice act as tools to dissect the IL-6 signalling pathway and IL-6 regulation.
Alonzi, T., Gorgoni, B., Screpanti, I., Gulino, A., & Poli, V. (1997) · Immunobiology · doi:10.1016/s0171-2985(97)80035-6 · Cited by 40
Induction of interleukin-6 (IL-6) autoantibodies through vaccination with an engineered IL-6 receptor antagonist
Ciapponi, L., Maione, D., Scoumanne, A., Costa, P., Hansen, M. B., Svenson, M., Bendtzen, K., Alonzi, T., Paonessa, G., Cortese, R., et al. (1997) · Nature Biotechnology · doi:10.1038/nbt1097-997 · Cited by 39
A new hepatocyte stimulating factor: cardiotrophin‐1 (CT‐1)
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Investigating the epigenetic profile of the inflammatory gene IL-6 in late-life depression
Ryan, J. L., Pilkington, L., Neuhaus, K., Ritchie, K. A., Ancelin, M., & Saffery, R. (2017) · BMC Psychiatry · doi:10.1186/s12888-017-1515-8 · Cited by 41
“It plays a major role during the immune response and acute-phase reaction [11].”
Background
Multiple lipopolysaccharide (LPS) injections alter interleukin 6 (IL-6), IL-7, IL-10 and IL-6 and IL-7 receptor mRNA in CNS and spleen.
Szot, P., Franklin, A., Figlewicz, D., Beuca, T. P., Bullock, K. M., Hansen, K., Banks, W., Raskind, M., & Peskind, E. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.04.028 · Cited by 39
Essential role of neutrophil mobilization in concanavalin A-induced hepatitis is based on classic IL-6 signaling but not on IL-6 trans-signaling
Malchow, S., Thaiss, W. M., Jänner, N., Waetzig, G. H., Gewiese, J., Garbers, C., Yamamoto, K., Rose‐John, S., & Scheller, J. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.11.009 · Cited by 39
Enhanced progenitor cell recruitment and endothelial repair after selective endothelial injury of the mouse kidney.
Hohenstein, B., Kuo, M.-C., Addabbo, F., Yasuda, K., Ratliff, B., Schwarzenberger, C., Eckardt, K., Hugo, C., & Goligorsky, M. (2010) · AJP - Renal Physiology · doi:10.1152/ajprenal.00025.2010 · Cited by 39
“In contrast, IL-6 and -10 as well as MCP-1 are much more prominent mediators of the inflammatory response upon endothelial injury (42, 43) but have also been linked to some extent with the regulation of progenitor cell activity (29) and endothelial repair (11).”
Background
Lack of gp130 expression results in more bacterial infection and higher mortality during chronic cholestasis in mice
Wuestefeld, T., Klein, C., Streetz, K., Beraza, N., Schölmerich, J., Burgart, L., Zender, L., Kubicka, S., Gores, G., Manns, M., et al. (2005) · Hepatology · doi:10.1002/hep.20912 · Cited by 39
Viral IL-6 Blocks Neutrophil Infiltration during Acute Inflammation1
Fielding, C., McLoughlin, R., Colmont, C. S., Kovaleva, M., Harris, D., Rose-John, S., Topley, N., & Jones, S. A. (2005) · Journal of Immunology · doi:10.4049/jimmunol.175.6.4024 · Cited by 39
“0 3,639 1,417 10,847 2,652 50 6,342 1,851 13,686 3,209 (13,550) 100 7,426 1,728 15,664 2,142 (14,634) 250 10,140 1,779* 17,722 2,749 (17,348) 500 10,436 1,144*** 19,869 3,082* (17,644)”
Suppression of host resistance to Listeria monocytogenes by acute cold/restraint stress: lack of direct IL-6 involvement
Cao, L., & Lawrence, D. A. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00371-5 · Cited by 41
“129 background) without stress showed decreased host resistance to LM (Kopf et al., 1994), Chlamydia trachomatis (Williams et al.”
Background
Molecular Pathogenesis of Multiple Myeloma: Chromosomal Aberrations, Changes in Gene Expression, Cytokine Networks, and the Bone Marrow Microenvironment
Klein, B., Seckinger, A., Moehler, T. M., & Hose, D. (2011) · Recent results in cancer research/Recent Results in Cancer Research · doi:10.1007/978-3-540-85772-3_3 · Cited by 38
Targeting progranulin alleviated silica particles-induced pulmonary inflammation and fibrosis via decreasing Il-6 and Tgf-β1/Smad
Zhao, M., Wang, M., Chen, X., Gao, Y., Chen, Q., Wang, L., Bao, Q., Sun, D., Du, W., Xu, Y., et al. (2023) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2023.133199 · Cited by 39
Transcriptome analysis and histopathology of black carp (Mylopharyngodon piceus) spleen infected by Aeromonas hydrophila
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Pretransplant Levels of CRP and Interleukin-6 Family Cytokines; Effects on Outcome after Allogeneic Stem Cell Transplantation
Tvedt, T. H., Lie, S., Reikvam, H., Rye, K. P., Lindås, R., Gedde-Dahl, T., Ahmed, A., & Bruserud, Ø. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17111823 · Cited by 38
“Mice depleted of IL-6 still retain their ability to produce CRP [16].”
Background
IL‐6 regulates exercise and training‐induced adaptations in subcutaneous adipose tissue in mice
Brandt, C., Jakobsen, A. H., Adser, H., Olesen, J., Iversen, N., Kristensen, J. M., Hojman, P., Wojtaszewski, J., Hidalgo, J., & Pilegaard, H. (2012) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02373.x · Cited by 38
“2002), and it has been demonstrated that serum IL-6 is undetectable in IL-6 KO mice even after an LPS injection (Kopf et al. 1994).”
Background
Downregulation of cilia-localized Il-6R alpha by 17beta-estradiol in mouse and human fallopian tubes.
Shao, R., Nutu, M., Karlsson-Lindahl, L., Benrick, A., Weijdegård, B., Lager, S., Egecioglu, E., Fernandez-Rodriguez, J., Gemzell-Danielsson, K., Ohlsson, C., et al. (2009) · American Journal of Physiology - Cell Physiology · doi:10.1152/ajpcell.00047.2009 · Cited by 38
Unresponsiveness of C-reactive protein in the non-infectious inflammation of systemic lupus erythematosus is associated with interleukin 6.
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Acute CD4+ T lymphocyte–dependent interleukin‐1–driven arthritis selectively requires interleukin‐2 and interleukin‐4, joint macrophages, granulocyte–macrophage colony‐stimulating factor, interleukin‐6, and leukemia inhibitory factor
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The crucial role of systemic responses in the innate (non-adaptive) host defense
Munford, R., & Pugin, J. (2001) · Journal of Endotoxin Research · doi:10.1177/09680519010070040501 · Cited by 38
“Emergency” granulopoiesis in G-CSF–deficient mice in response to Candida albicans infection
Basu, S., HODGSON, G. S., Zhang, H., Katz, M., Quilici, C., & Dunn, A. R. (2000) · Blood · doi:10.1182/blood.v95.12.3725 · Cited by 144
Cytokine mediation of ozone-induced pulmonary adaptation.
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Impairment of antigen-specific antibody production in transgenic mice expressing a dominant-negative form of gp130.
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Self-citation
Analysis of Host Immunological Response of Adenovirus-Based COVID-19 Vaccines
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Expression and Differential Responsiveness of Central Nervous System Glial Cell Populations to the Acute Phase Protein Serum Amyloid A
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RNA-Seq revealed the impairment of immune defence of tilapia against the infection of Streptococcus agalactiae with simulated climate warming
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Piperine metabolically regulates peritoneal resident macrophages to potentiate their functions against bacterial infection
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“It has been known that IL-6 and TNF-α secretion by macrophages upon bacterial infection in turn enhances their phagocytic capacity, thus promoting the clearance of pathogens [31, 46, 47].”
Disrupted glucocorticoid—Immune interactions during stress response in schizophrenia
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“IL-6 is a pleiotropic, pro-inflammatory cytokine that is released from several immune and nonimmune cell types, and mediates acute inflammatory responses to immune challenges (Kishimoto et al 1992; Kopf et al 1994).”
Background
Long pentraxin PTX3 attenuates ischemia reperfusion injury in a cardiac transplantation model
Zhu, H., Cui, D., Liu, K., Wang, L., Huang, L., & Li, J. (2013) · Transplant International · doi:10.1111/tri.12197 · Cited by 36
“IL-6 is a proinflammatory cytokine that plays a key role in both innate and adaptive immune response [28], and it is essential in the induction of Th17 cells in both human and mice [29].”
Background
The in vitro and in ovo responses of chickens to TLR9 subfamily ligands.
Jenkins, K., Lowenthal, J., Kimpton, W., & Bean, A. (2009) · Developmental and Comparative Immunology · doi:10.1016/j.dci.2008.11.009 · Cited by 37

Authors: Kopf, M., Baumann, H., Freer, G., Freudenberg, M., Lamers, M., Kishimoto, T., Zinkernagel, R., Bluethmann, H., & Köhler, G.
Affiliations: University of Zurich (CH)
Max Planck Society (DE)
The University of Osaka (JP)
F. Hoffmann-La Roche AG (CH)
Roswell Park Comprehensive Cancer Center (US)
ORCID: Freer, Giulia
Freudenberg, Marina
Kishimoto, Tadamitsu
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 1994-03-24
Volume: 368
Issue: 6469
Pages: 339-342
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/368339a0
OpenAlex: W2067761476
Cited by: 1,768
References: 0
Citations by year: 2026: 20 · 2025: 33 · 2024: 23 · 2023: 36 · 2022: 44 · 2021: 58 · 2020: 43 · 2019: 52 · 2018: 46 · 2017: 60 · 2016: 57 · 2015: 44 · 2014: 48 · 2013: 56 · 2012: 64
FWCI: 28.71
Type: journal article
Language: en
Open access: closed
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Cytokine Signaling Pathways and Interactions
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: interleukin-6, IL-6-deficient mice, gene disruption, acute phase response, immune response, vaccinia virus infection, Listeria monocytogenes, T cell-dependent antibody response, vesicular stomatitis virus, lipopolysaccharide, gp130, cytokine redundancy, inflammation, macrophages, liver
MeSH terms: Acute-Phase Reaction, Animals, B-Lymphocytes, Immunity, Listeriosis, Lymphoid Tissue, Mice, Inbred C57BL, RNA, Messenger, T-Lymphocytes, Vesicular stomatitis Indiana virus, Interleukin-6, Rhabdoviridae Infections, Mice

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Impaired immune and acute-phase responses in interleukin-6-deficient mice

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