In Vivo Interleukin-6 Protects Neutrophils from Apoptosis in Osteomyelitis
Open accessAbstract
Polymorphonuclear neutrophils are critical for resolution of bacterial infections. In tissues, most of the neutrophils quickly die through apoptosis. Using propidium iodide DNA staining and DNA gel electrophoresis, we found that spontaneous apoptosis of neutrophils from patients suffering osteomyelitis (n= 52) was significantly decreased in relation to control neutrophils (n= 20) (40.2% ± 25.2% versus 54.5% ± 23.5%;P< 0.03). Incubation of neutrophils from normal volunteers with sera from patients with osteomyelitis reduced apoptosis from 79.1% ± 14.8% in control sera to 62.2% ± 18.7% in osteomyelitis sera. A significant increase of serum interleukin-6 (IL-6) and IL-1α was found in osteomyelitis (IL-6, 8.8 ± 11.9 pg/ml versus 1.8 ± 1.2 pg/ml in controls [P< 0.004]; IL-1α, 3.8 ± 6.4 pg/ml versus 1.0 ± 2.2 pg/ml in controls [P< 0.02]). No differences in the levels of other cytokines, such as tumor necrosis factor alpha, were found. There was an inverse correlation between IL-6 levels and neutrophil apoptosis (r= −0.855;P< 0.007), but this was not the case for other cytokines. The antiapoptotic effect of the osteomyelitis sera was reversed with anti-IL-6 antibodies (P< 0.03) and was reproduced with recombinant human IL-6 (P< 0.001). The longer life span of neutrophils in osteomyelitis induced by IL-6 could contribute to the tissue damage that occurs in these chronic bone infections.
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Elevated IL-6 prolongs neutrophil survival by reducing apoptosis.
“elevated levels of IL-6, as either part of the host pathogen response or due to inflammageing, engenders prolonged neutrophil survival through reducing apoptosis87”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [87]
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Nicoletti, I., Migliorati, G., Pagliacci, M. C., Grignani, F., & Riccardi, C. (1991) · Journal of Immunological Methods · doi:10.1016/0022-1759(91)90198-o · Cited by 4,580 · see citing works
Baumann, H., & Gauldie, J. (1994) · Immunology Today · doi:10.1016/0167-5699(94)90137-6 · Cited by 2,907 · see citing works
Impaired immune and acute-phase responses in interleukin-6-deficient mice
Kopf, M., Baumann, H., Freer, G., Freudenberg, M., Lamers, M., Kishimoto, T., Zinkernagel, R., Bluethmann, H., & Köhler, G. (1994) · Nature · doi:10.1038/368339a0 · Cited by 1,768 · cited 1× · see citing works
“This cytokine is released during the acutephase response and in chronic intracellular infections (5), where it plays a critical biologic function in the inflammation, decreasing TNF- , GM-CSF, and IFN- levels and increasing the B-cell differentiation, T-cell proliferation and activation, and antibody secretion (5, 24,…”
BackgroundXing, Z., Gauldie, J., Cox, G., Baumann, H., Jordana, M., Lei, X.-F., & Achong, M. K. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1368 · Cited by 1,578 · see citing works
Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products
Colotta, F., Re, F., Polentarutti, N., Sozzani, S., & Mantovani, A. (1992) · Blood · doi:10.1182/blood.v80.8.2012.2012 · Cited by 1,158 · see citing works
IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation
Kaplanski, G. (2003) · Trends in Immunology · doi:10.1016/s1471-4906(02)00013-3 · Cited by 811 · see citing works
Lee, A., Whyte, M. K. B., & Haslett, C. (1993) · Journal of Leukocyte Biology · doi:10.1002/jlb.54.4.283 · Cited by 714 · see citing works
Role of neutrophils in ischemia-reperfusion-induced microvascular injury
Hernandez, L. A., Grisham, M. B., Twohig, B., Arfors, K. ‐., Harlan, J. M., & Granger, D. N. (1987) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1987.253.3.h699 · Cited by 699 · see citing works
Tissue injury in inflammation. Oxidants, proteinases, and cationic proteins.
Henson, P. M., & Johnston, R. B. (1987) · Journal of Clinical Investigation · doi:10.1172/jci112869 · Cited by 693 · see citing works
Apoptosis in resolution of inflammation
Savill, J. (1997) · Journal of Leukocyte Biology · doi:10.1002/jlb.61.4.375 · Cited by 652 · see citing works
Lew, D. P., & Waldvogel, F. A. (1997) · New England Journal of Medicine · doi:10.1056/nejm199704033361406 · Cited by 618 · see citing works
Molecular control of neutrophil apoptosis
Akgul, C., MOULDING, D. A., & Edwards, S. W. (2001) · FEBS Letters · doi:10.1016/s0014-5793(00)02324-3 · Cited by 488 · see citing works
Neutrophil Apoptosis in the Acute Respiratory Distress Syndrome
Matute‐Bello, G., Liles, W. C., Radella, F., Steinberg, K. P., RUZINSKI, J. T., Jonas, M., CHI, E. Y., Hudson, L. D., & MARTIN, T. R. (1997) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.156.6.96-12081 · Cited by 394 · see citing works
Dysregulated Expression of Neutrophil Apoptosis in the Systemic Inflammatory Response Syndrome
Jimenez, M. F. (1997) · Archives of Surgery · doi:10.1001/archsurg.1997.01430360009002 · Cited by 336 · see citing works
Iwaï, K., Miyawaki, T., Takizawa, T., Konno, A., Ohta, K., Yachie, A., Seki, H., & Taniguchi, N. (1994) · Blood · doi:10.1182/blood.v84.4.1201.1201 · Cited by 314 · see citing works
Murray, J., Barbara, J. A. J., Dunkley, S. A., Lopez, A. F., Ostade, X. V., Condliffe, A. M., Dransfield, I., Haslett, C., & Chilvers, E. R. (1997) · Blood · doi:10.1182/blood.v90.7.2772 · Cited by 294 · see citing works
Dibbert, B., Weber, M., Nikolaizik, W. H., Vogt, P., Schöni, M. H., Blaser, K., & Simon, H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13330 · Cited by 278 · see citing works
Granulocyte clearance by apoptosis in the resolution ofinflammation
Savill, J., & Haslett, C. (1995) · Seminars in Cell Biology · doi:10.1016/s1043-4682(05)80009-1 · Cited by 178 · see citing works
Bcl-Xl– and Bax-–Mediated Regulation of Apoptosis of Human Neutrophils Via Caspase-3
Weinmann, P., Gaehtgens, P. A. L., & Walzog, B. (1999) · Blood · doi:10.1182/blood.v93.9.3106.409k36_3106_3115 · Cited by 174 · see citing works
Ohta, H., Yatomi, Y., Sweeney, E. A., Hakomori, S., & Igarashi, Y. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)01218-0 · Cited by 167 · see citing works
Cierný, G., & Mader, J. T. (1984) · Orthopedics · doi:10.3928/0147-7447-19841001-07 · Cited by 167 · see citing works
Interleukin-6 Delays Neutrophil Apoptosis
Biffl, W. L. (1996) · Archives of Surgery · doi:10.1001/archsurg.1996.01430130026005 · Cited by 152 · see citing works
Rapid acceleration of neutrophil apoptosis by tumor necrosis factor-α
Takeda, Y., Watanabe, H. K., Yonehara, S., Yamashita, T., Salto, S., & Sendo, F. (1993) · International Immunology · doi:10.1093/intimm/5.6.691 · Cited by 151 · see citing works
Bost, K. L., Ramp, W. K., Nicholson, N. C., Bento, J. L., Marriott, I., & Hudson, M. C. (1999) · The Journal of Infectious Diseases · doi:10.1086/315138 · Cited by 132 · see citing works
Afford, S. C., Pongracz, J. E., STOCKLEY, R. A., Crocker, J., & Burnett, D. A. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)36655-4 · Cited by 128 · see citing works
Regulation of apoptosis in neutrophils--Fas track to death?
Liles, W. C., & Klebanoff, S. J. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.155.7.3289 · Cited by 123 · see citing works
Interleukin-6 Delays Neutrophil Apoptosis via a Mechanism Involving Platelet-Activating Factor
Biffl, W. L., Moore, E. E., Moore, F. A., & Barnett, C. C. (1996) · doi:10.1097/00005373-199604000-00009 · Cited by 120 · see citing works
Baran, J., Guzik, K., Hryniewicz, W., Ernst, M., Flad, H. ‐., & Pryjma, J. R. (1996) · Infection and Immunity · doi:10.1128/iai.64.10.4242-4248.1996 · Cited by 111 · see citing works
Interleukin-6 suppression of neutrophil apoptosis is neutrophil concentration dependent
Biffl, W. L., Moore, E. E., Moore, F. A., & Barnett, C. C. (1995) · Journal of Leukocyte Biology · doi:10.1002/jlb.58.5.582 · Cited by 109 · see citing works
Tissue Injury in Inflammation. Oxidants, Proteinases, and Cationic Proteins
Henson, P. M., & Johnston, R. B. (1987) · The Journal of Urology · doi:10.1016/s0022-5347(17)43303-9 · Cited by 102 · see citing works
Ottonello, L. C., Frumento, G., Arduino, N., Bertolotto, M. B., Dapino, P., Mancini, M., & Dallegri, F. (2002) · Journal of Leukocyte Biology · doi:10.1189/jlb.72.1.125 · Cited by 70 · see citing works
Fanning, N. F., Kell, M., Shorten, G., Kirwan, W. O., Bouchier‐Hayes, D. M., Cotter, T. G., & Redmond, H. P. (1999) · Shock · doi:10.1097/00024382-199903000-00003 · Cited by 69 · see citing works
Klosterhalfen, B., Peters, K. M., Töns, C., Hauptmann, S., Klein, C., & Kirkpatrick, C. J. (1996) · doi:10.1097/00005373-199603000-00008 · Cited by 67 · see citing works
Weinmann, P., Scharffetter‐Kochanek, K., Forlow, S. B., Peters, T., & Walzog, B. (2002) · Blood · doi:10.1182/blood-2002-01-0239 · Cited by 67 · see citing works
Evans, C. A., Jellis, J. E., Hughes, S. P. F., Remick, D. G., & Friedland, J. S. (1998) · The Journal of Infectious Diseases · doi:10.1086/515313 · Cited by 60 · see citing works
Inhibition of neutrophil apoptosis after elective surgery
Fanning, N. F., Porter, J., Shorten, G., Kirwan, W. O., Bouchier‐Hayes, D. M., Cotter, T. G., & Redmond, H. P. (1999) · Surgery · doi:10.1016/s0039-6060(99)70094-2 · Cited by 58 · see citing works
Roesgen, M., Hierholzer, G., & Hax, P.-M. (1989) · Archives of Orthopaedic and Trauma Surgery · doi:10.1007/bf00934149 · Cited by 53 · see citing works
Daffern, P. J., Jagels, M. A., & Hugli, T. E. (1999) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.21.2.3605 · Cited by 41 · see citing works
IL‐1α (− 889) promoter polymorphism is a risk factor for osteomyelitis
Asensi, V., Álvarez, V., Valle-Garay, E., Meana, Á., Fierer, J., Coto, E., Carton, J. A., Maradona, J. A., Paz, J., Diéguez, M. Á., et al. (2003) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.20137 · Cited by 40 · see citing works
Self-citationYoon, K.-J., Fitzgerald, R. H., Sud, S., Song, Z.-C., & Wooley, P. H. (1999) · Journal of Orthopaedic Research® · doi:10.1002/jor.1100170313 · Cited by 37 · see citing works
Interleukin-6 and a Delay of Neutrophil Apoptosis After Major Surgery
Kobayashi, E. (1997) · Archives of Surgery · doi:10.1001/archsurg.1997.01430260107023 · Cited by 33 · see citing works
Matsuda, T., Saito, H., Fukatsu, K., Han, I., Inoue, T., Furukawa, S., Ikeda, S., & Hidemura, A. (2001) · Surgery · doi:10.1067/msy.2001.109060 · Cited by 30 · see citing works
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- [8]Biffl, W. L., E. Moore, F. A. Moore, C. C. Barnett, V. S. Carl, and V. M. Peterson. 1996. Interleukin-6 delays neutrophil apoptosis. Arch. Surg. 131:24-30. [DOI] [PubMed] [Google Scholar]
Cited by
Sorted by citations
Emery, P., Keystone, E., Tony, H. P., Cantagrel, A., van Vollenhoven, R., Sanchez, A., Alecock, E., Lee, J., & Kremer, J. (2008) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2008.092932 · Cited by 1,104 · see citing works
Jabłońska, J., Leschner, S., Westphal, K., Lienenklaus, S., & Weiß, S. (2010) · Journal of Clinical Investigation · doi:10.1172/jci37223 · Cited by 563 · see citing works
Raffaghello, L., Bianchi, G., Bertolotto, M. B., Montecucco, F., Busca, A., Dallegri, F., Ottonello, L. C., & Pistoia, V. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0416 · Cited by 518 · see citing works
SARS-CoV-2, COVID-19 and the aging immune system
Bartleson, J. M., Radenkovic, D., Covarrubias, A. J., Furman, D., Winer, D. A., & Verdin, E. (2021) · Nature Aging · doi:10.1038/s43587-021-00114-7 · Cited by 359 · see citing works
Interleukin-6: from an inflammatory marker to a target for inflammatory diseases
Rincón, M. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.07.003 · Cited by 328 · see citing works
Therapeutic targets in rheumatoid arthritis: the interleukin-6 receptor
Dayer, J., & Choy, E. (2009) · Rheumatology · doi:10.1093/rheumatology/kep329 · Cited by 270 · see citing works
Interleukin-6 as a Multifunctional Regulator: Inflammation, Immune Response, and Fibrosis
Choy, E., & Rose-John, S. (2017) · Journal of Scleroderma and Related Disorders · doi:10.5301/jsrd.5000265 · Cited by 174 · see citing works
Shahini, A., & Shahini, A. (2022) · Journal of Cell Communication and Signaling · doi:10.1007/s12079-022-00695-x · Cited by 167 · see citing works
Dumitru, C. A., Gholaman, H., Trellakis, S., Bruderek, K., Dominas, N., Gu, X., Bánkfalvi, Á., Whiteside, T. L., Lang, S., & Brandau, S. (2011) · International Journal of Cancer · doi:10.1002/ijc.25991 · Cited by 142 · see citing works
Kim, M. H., Gorouhi, F., Ramirez, S., Granick, J. L., Byrne, B. A., Soulika, A. M., Simon, S. I., & Isseroff, R. R. (2013) · Journal of Investigative Dermatology · doi:10.1038/jid.2013.415 · Cited by 116 · see citing works
Cianci, E., Recchiuti, A., Trubiani, O., Diomede, F., Marchisio, M., Miscia, S., Colas, R. A., Dalli, J., Serhan, C. N., & Romano, M. (2015) · Stem Cells Translational Medicine · doi:10.5966/sctm.2015-0163 · Cited by 102 · see citing works
Montes, A. H., Asensi, V., Álvarez, V., Valle-Garay, E., Ocaña, M. G., Meana, Á., Carton, J. A., Paz, J., Fierer, J., & Celada, A. (2006) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2005.03002.x · Cited by 95 · see citing works
Self-citationApoptosis-associated uncoupling of bone formation and resorption in osteomyelitis
Marriott, I. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00101 · Cited by 89 · see citing works
Gao, H., Ying, S., & Dai, Y. (2017) · Journal of Immunology Research · doi:10.1155/2017/3743048 · Cited by 86 · see citing works
Russo, T. A., Davidson, B. A., Genagon, S. A., Warholic, N. M., MacDonald, U., Pawlicki, P. D., Beanan, J. M., Olson, R., Holm, B. A., & Knight, P. R. (2005) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00482.2004 · Cited by 81 · see citing works
Caiello, I., Minnone, G., Holzinger, D., Vogl, T., Prencipe, G., Manzo, A., Benedetti, F. D., & Strippoli, R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0107886 · Cited by 75 · see citing works
Wang, S.-X., Abramson, S., Attur, M., Karsdal, M., Preston, R. A., Lozada, C., Kosloski, M., Hong, F., Jiang, P., Saltarelli, M., et al. (2017) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2017.09.007 · Cited by 72 · see citing works
Influence of Neutropenia on the Course of Serotype 8 Pneumococcal Pneumonia in Mice
Marks, M. S., Burns, T., Abadi, M. A., Seyoum, B., Thornton, J. A., TUOMANEN, E. I., & Pirofski, L. (2007) · Infection and Immunity · doi:10.1128/iai.01579-06 · Cited by 69 · see citing works
Mustard gas exposure and carcinogenesis of lung
Hosseini-khalili, A., Haines, D. D., Modirian, E., Soroush, M., Khateri, S., Joshi, R. A., Zendehdel, K., Ghanei, M., & Giardina, C. A. (2009) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2009.05.022 · Cited by 66 · see citing works
Immunosenescence and inflamm-ageing in COVID-19
Zinatizadeh, M. R., Zarandi, P. K., Ghiasi, M., Kooshki, H., Mohammadi, M., Amani, J., & Rezaei, N. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101818 · Cited by 62 · see citing works
Hollenhorst, M. I., Nandigama, R., Evers, S. B., Gamayun, I., Wadood, N. A., Salah, A., Pieper, M., Wyatt, A. K., Stukalov, A., Gebhardt, A., et al. (2022) · Journal of Clinical Investigation · doi:10.1172/jci150951 · Cited by 61 · see citing works
Wu, Y., Lai, A. C., Chi, P., Thio, C. L., Chen, W., Tsai, C., Lee, Y. L., Lukacs, N. W., & Chang, Y. (2019) · Allergy · doi:10.1111/all.14091 · Cited by 60 · see citing works
Contemporary Concepts in the Treatment of Chronic Osteomyelitis
Coviello, V. F., & Stevens, M. R. (2007) · Oral and Maxillofacial Surgery Clinics of North America · doi:10.1016/j.coms.2007.07.001 · Cited by 56 · see citing works
Smoking, an additional risk factor in elder women with primary open-angle glaucoma.
Zanón‐Moreno, V., García‐Medina, J. J., Viguer, V. Z., Moreno-Nadal, M. A., & Pinazo-Duran, M. D. (2009) · PubMed Central · Cited by 52 · see citing works
Asthma Phenotypes as a Guide for Current and Future Biologic Therapies
Hamilton, D., & Lehman, H. K. (2019) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-019-08760-x · Cited by 51 · see citing works
Lin, L., Wang, L., Wang, W.-T., Jin, L.-L., Zhao, X., Zheng, L.-P., Jin, L., Jiang, L., & Xiong, X. (2010) · Anesthesia & Analgesia · doi:10.1213/ane.0b013e3181e368d2 · Cited by 51 · see citing works
Pro-inflammatory and immunomodulatory functions of airway smooth muscle: Emerging concepts
Xia, Y., Redhu, N. S., Moir, L. M., Koziol‐White, C. J., Ammit, A. J., Al-Alwan, L. A., Camoretti-Mercado, B., & Clifford, R. L. (2012) · Pulmonary Pharmacology & Therapeutics · doi:10.1016/j.pupt.2012.05.006 · Cited by 50 · see citing works
Xie, X., Law, H., Wang, L., Li, X., Yang, X., & Liu, E. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e318191f5c6 · Cited by 44 · see citing works
Paul, A. M., Cheng-Campbell, M., Blaber, E. A., Anand, S., Bhattacharya, S., Zwart, S. R., Crucian, B. E., Smith, S. M., Meller, R., Grabham, P. W., et al. (2020) · iScience · doi:10.1016/j.isci.2020.101747 · Cited by 38 · see citing works
The inflammatory response to bone infection – a review based on animal models and human patients
Lüthje, F. L., Jensen, L. K., Jensen, H. E., & Skovgaard, K. (2020) · Apmis · doi:10.1111/apm.13027 · Cited by 37 · see citing works
Chauhan, P., Wagner, J. G., Benninghoff, A. D., Lewandowski, R. P., Favor, O. K., Wierenga, K. A., Gilley, K. N., Ross, E. A., Harkema, J. R., & Pestka, J. J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.635138 · Cited by 36 · see citing works
Martin, W. J., Grainger, R., Harrison, A. A., & Harper, J. L. (2010) · The Journal of Rheumatology · doi:10.3899/jrheum.091080 · Cited by 36 · see citing works
Chen, C., Chen, Y., Huang, J., & Wu, Y. (2014) · Molecular Human Reproduction · doi:10.1093/molehr/gau062 · Cited by 36 · see citing works
Tsezou, A., Poultsides, L. A., Kostopoulou, F., Zintzaras, E., Σάτρα, Μ., Kitsiou‐Tzeli, S., & Malizos, Κ. Ν. (2008) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00209-08 · Cited by 36 · see citing works
The NOS3 (27-bp repeat, intron 4) polymorphism is associated with susceptibility to osteomyelitis
Asensi, V., Montes, A. H., Valle-Garay, E., Ocaña, M. G., Astudillo, A., Álvarez, V., López‐Anglada, E., Solís, A., Coto, E., Meana, Á., et al. (2006) · Nitric Oxide · doi:10.1016/j.niox.2006.06.005 · Cited by 35 · see citing works
Self-citationA functional polymorphism in MMP1 could influence osteomyelitis development
Montes, A. H., Valle-Garay, E., Álvarez, V., Pevida, M., Pérez, E. G., Paz, J., Meana, Á., & Asensi, V. (2009) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.091013 · Cited by 33 · see citing works
Self-citationAutoregulation mechanism of human neutrophil apoptosis during bacterial infection☆
Ocaña, M. G., Asensi, V., Montes, A. H., Meana, Á., Celada, A., & Valle-Garay, E. (2007) · Molecular Immunology · doi:10.1016/j.molimm.2007.10.013 · Cited by 30 · see citing works
Self-citationMcNamee, J. P., Bellier, P. V., Kutzner, B. C., & Wilkins, R. C. (2005) · Cytokine · doi:10.1016/j.cyto.2005.05.001 · Cited by 30 · see citing works
Endotracheal intubation results in acute tracheal damage induced by mtDNA/TLR9/NF-κB activity
Puyo, C. A., Earhart, A., Staten, N. R., Prince, O. A., Haug, C., Kollef, M. H., & Awad, M. M. (2018) · Journal of Leukocyte Biology · doi:10.1002/jlb.5a0718-254rr · Cited by 29 · see citing works
Ocaña, M. G., Valle-Garay, E., Montes, A. H., Meana, Á., Carton, J. A., Fierer, J., Celada, A., & Asensi, V. (2007) · Genetics in Medicine · doi:10.1097/gim.0b013e318039b23d · Cited by 29 · see citing works
Self-citationCOPD monocytes demonstrate impaired migratory ability
Ravi, A., Plumb, J., Gaskell, R., Mason, S., Broome, C. S., Booth, G. C., Catley, M. C., Vestbo, J., & Singh, D. (2017) · Respiratory Research · doi:10.1186/s12931-017-0569-y · Cited by 27 · see citing works
Efficacy and safety of tocilizumab in Korean patients with active rheumatoid arthritis
Baek, H., Lim, M., Park, W., Park, S. H., Shim, S., Yoo, D., Kim, H., Lee, S., Lee, Y.-J., Park, Y., et al. (2018) · The Korean Journal of Internal Medicine · doi:10.3904/kjim.2017.159 · Cited by 26 · see citing works
Rosero, E. P., Heron, S., Jovel, J., O’Neil, C. R., Turvey, S. L., Parashar, P., & Elahi, S. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.780910 · Cited by 27 · see citing works
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Manetsch, M., Seidel, P., Heintz, U., Che, W., Hughes, J. M., Ge, Q., Sukkar, M. B., & Ammit, A. J. (2012) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00317.2011 · Cited by 25 · see citing works
Kim, D., & Haynes, C. L. (2013) · Analytical Chemistry · doi:10.1021/ac4020098 · Cited by 25 · see citing works
Mo, Y., Chen, S., Yang, L., Huang, L., Jin, D., Yu, Z., Wang, L., Wang, L., Luo, S., & Wang, J. (2017) · Mediators of Inflammation · doi:10.1155/2017/8369737 · Cited by 25 · see citing works
Neutrophils rescue gingival epithelial cells from bacterial-induced apoptosis
Galicia, J. C., Benakanakere, M. R., Stathopoulou, P. G., & Kinane, D. F. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.0109003 · Cited by 23 · see citing works
Periodontal ligament stem cells regulate apoptosis of neutrophils
Wang, Q., Ding, G., & Xu, X. (2017) · Open Medicine · doi:10.1515/med-2017-0004 · Cited by 22 · see citing works
Nieto, J. C., Sánchez, E., Romero, C., Román, E., Poca, M., Guarner, C., Juárez, C., Soriano, G., & Vidal, S. (2015) · Journal of Leukocyte Biology · doi:10.1189/jlb.3ab0315-106r · Cited by 21 · see citing works
Guan, R., Wang, D., Wang, B., Jiang, L., & Liu, J. (2020) · BMC Veterinary Research · doi:10.1186/s12917-020-02314-6 · Cited by 20 · see citing works
Neutrophils in cancer: At the crucial crossroads of anti‐tumor and pro‐tumor
Cai, W., Fan, T. T., Xiao, C., Deng, Z., Liu, Y., Li, C., & He, J. (2025) · 癌症:英文版 · doi:10.1002/cac2.70027 · Cited by 16 · see citing works
Gehrke, A.-K. E., Mendoza-Bertelli, A., Ledo, C., Gonzalez, C., Llana, M. N., Blanco, C., Sordelli, D., Putman, N., Cassat, J., Delpino, M., et al. (2022) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01140-22 · Cited by 20 · see citing works
Immunosenescence and Inflammaging in COVID-19
Asghari, F., Asghary, A., Zolbanin, N. M., Faraji, F., & Jafari, R. (2023) · Viral Immunology · doi:10.1089/vim.2023.0045 · Cited by 16 · see citing works
Disentangling the effects of tocilizumab on neutrophil survival and function
Gaber, T., Hahne, M., Strehl, C., Hoff, P., Dörffel, Y., Feist, E., Burmester, G., & Buttgereit, F. (2015) · Immunologic research · doi:10.1007/s12026-015-8770-x
Pérez‐Is, L., Ocaña, M. G., Montes, A. H., Carton, J. A., Álvarez, V., Meana, Á., Fierer, J., Valle-Garay, E., & Asensi, V. (2019) · PLoS ONE · doi:10.1371/journal.pone.0220022 · Cited by 13 · see citing works
Self-citationMurine osteoblasts respond to LPS and IFN-γ similarly to macrophages
Maruyama, K., Sano, G., & Matsuo, K. (2006) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-006-0708-x · Cited by 13 · see citing works
The Cell-Specific Effects of JAK1 Inhibitors in Ulcerative Colitis
Veltkamp, S. H. C., & Voorneveld, P. W. (2025) · Journal of Clinical Medicine · doi:10.3390/jcm14020608 · Cited by 12 · see citing works
Wang, L., Wang, W.-T., Zhao, X., Jin, L., Bai, Y., Yao, H., Zhuo, Q., & Lin, L. (2011) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/ta.0b013e318205e279 · Cited by 12 · see citing works
Chen, C., Zhang, Z., Tan, F., Meng, F., Lai, L., Chi, X., & Zhu, Q. (2020) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00046.2020 · Cited by 12 · see citing works
Tamai, R., Sugiyama, A., & Kiyoura, Y. (2010) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2010.01302.x · Cited by 12 · see citing works
Sarray, S., & Almawi, W. Y. (2015) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00286-15 · Cited by 10 · see citing works
Protective Effects of Dexmedetomidine and Oxycodone in Patients Undergoing Limb Ischemia-Reperfusion
Cheng, W., Wang, M., Liu, P., Zhao, S., Liu, X., & Wang, X. (2019) · Medical Science Monitor · doi:10.12659/msm.918261 · Cited by 9 · see citing works
Hodgkin's lymphoma masquerading as vertebral osteomyelitis in a man with diabetes: a case report
Ignacio, R. B., Liu, A. Y., Sohani, A. R., & Vyas, J. M. (2010) · Journal of Medical Case Reports · doi:10.1186/1752-1947-4-102 · Cited by 7 · see citing works
López‐Anglada, E., Collazos, J., Montes, A. H., Pérez‐Is, L., Pérez-Hevia, I., Jiménez‐Tostado, S., Suárez‐Zarracina, T., Álvarez, V., Valle-Garay, E., & Asensi, V. (2022) · Scientific Reports · doi:10.1038/s41598-022-22693-0 · Cited by 7 · see citing works
Self-citationTuberculosis and COVID-19 in the elderly: factors driving a higher burden of disease
Allué‐Guardia, A., Torrelles, J. B., & Sigal, A. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1250198 · Cited by 8 · see citing works
The effect of IL-6 on the trophoblast cell line HTR-8/SVneo
Krivokuća, M. J., Kovačević, T., Stefanoska, I., & Vićovac, L. (2010) · Archives of Biological Sciences · doi:10.2298/abs1003531j · Cited by 7 · see citing works
The role of cytokines in diabetic foot osteomyelitis
Aragón‐Sánchez, J., & Cabrera, J. J. (2013) · Diabetic Medicine · doi:10.1111/dme.12114 · Cited by 6 · see citing works
Mohamed, M. H., & Hamawy, T. Y. E. (2015) · Egyptian Journal of Anaesthesia · doi:10.1016/j.egja.2015.07.003 · Cited by 6 · see citing works
Ferreira, G. F., Moraes, C. A. D. C., Silveira, A. M. S., Corrêa‐Oliveira, R., Teixeira‐Carvalho, A., Martins‐Filho, O. A., Moreno, E. C., do Carmo, L. S., Fraga, L. A. D. O., & Malaquias, L. C. C. (2012) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02762012000300009 · Cited by 6 · see citing works
Hepatic Inflammation Confers Protective Immunity Against Liver Stages of Malaria Parasite
Grand, M., Waqasi, M., Demarta‐Gatsi, C., Yu, W., Péronet, R., Commère, P., Puig, A., Axelrod, J. H., Caldelari, R., Heussler, V. T., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.585502 · Cited by 6 · see citing works
Mathews, I. T., Saminathan, P., Henglin, M., Liu, M., Nadig, N., Fang, C., Mercader, K., Chee, S., Campbell, A. M., Patel, A. A., et al. (2024) · medRxiv · doi:10.1101/2024.08.07.24310974 · Cited by 5 · see citing works
Yun, J. H., Hong, Y., Hong, M. H., Kim, G., Lee, J.-S., Lee, J.-S., Lee, J., Yang, E. J., & Kim, I. S. (2023) · Cytokine · doi:10.1016/j.cyto.2023.156439 · Cited by 4 · see citing works
Pattern recognition receptors and the innate immune network
van Hensbergen, V. P., & Hu, X. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-818619-0.00131-3 · Cited by 4 · see citing works
Kim, H., You, S., Park, Y., Choi, J. Y., Ma, Y., Hong, K. T., Koh, K., Yun, S., Lee, K. H., Shin, H. Y., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-88963-5 · Cited by 4 · see citing works
Insights into Innate Immune Response Against SARS-CoV-2 Infection
Huţanu, A., Georgescu, A. M., Andrejkovits, Á. V., Au, W. W., & Dobreanu, M. (2021) · Revista română de medicină de laborator · doi:10.2478/rrlm-2021-0022 · Cited by 3 · see citing works
Lu, D.-E., Ou, T.-Y., Kang, J., Ong, J. Y., Chen, I.-J., Lee, C., & Lee, M. (2023) · Journal of Microbiology Immunology and Infection · doi:10.1016/j.jmii.2023.10.011 · Cited by 2 · see citing works
Pattern Recognition Receptors and the Innate Immune Network
Wade, W. F. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397169-2.00026-3 · Cited by 2 · see citing works
A Myeloid Lineage Signifying Anti-tumor Necrosis Factor Resistance in Crohn’s Disease
Munasinghe, S., Geem, D., Duraiarasan, K., Maddipatla, S. C., Murthy, S., Hwang, Y. C., Pelia, R. S., Anbazhagan, M., Sharma, G., Koti, V., et al. (2025) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2025.101636 · Cited by 1 · see citing works
Role of Neutrophils Apoptosis in Osteomyelitis Pathogenesis
Asensi, V., Collazos, J., Celada, A., & Valle-Garay, E. (2017) · Clinical Microbiology Open Access · doi:10.4172/2327-5073.1000e139 · Cited by 1 · see citing works
Self-citationInterplay between Pathogenic and Immune Regulatory Mechanisms in G-alpha-i2 deficient colitis
Götlind, Y.-Y. C. (2011) · Gothenburg University Publications Electronic Archive (Gothenburg University)
Mekata, Y., Kashimura, O., & Kawano, Y. (2008) · 体力科學 · doi:10.7600/jspfsm.57.249
Neutrophil responses to infection with leishmania parasites
Davis, R. E., Wilson, M. E., Varga, S. M., Nauseef, W. M., Allen, L. H., & Sutterwala, F. S. (2016) · doi:10.17077/etd.d088xm24
Exodus Concerto for Guitar and Chamber Orchestra
Kappelman, S. J. (2013)
Sapey, E. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.732544720.793558959
The Covid-19 and TB Syndemic: Differences and Similarities
Kaufmann, S. H. E., Sher, A., Sigal, A., & Sawitzki, B. (2023) · Frontiers research topics · doi:10.3389/978-2-8325-4116-6
Guan, R.-W., Wang, D., Wang, B.-B., Jiang, L.-Y., & Liu, J. (2020) · Figshare · doi:10.6084/m9.figshare.12308186
Macrophage Phenotype Alterations in Treated Periodontitis Patients Suggest a Pro‐Inflammatory Bias
Sloniak, M. C., de Assis, J. B., Saraiva, L. M., Pannuti, C. M., Lepique, A. P., & Villar, C. C. (2026) · Journal of Periodontal Research · doi:10.1111/jre.70098
Neutrophils and tuberculosis - insights into immunobiology and pathogenesis
Raza, M., Kak, G., & Alla, M. R. (2026) · Molecular Biology Reports · doi:10.1007/s11033-026-12453-y
Neutrophil fate in bone infection: Mechanisms, microenvironment, and therapeutic opportunities
Cai, C., Ji, Y., Mei, J., Wang, Z., Liu, Q., Fan, W., Zhao, Y., Chen, X., Zhu, C., 朱万波, et al. (2026) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2026.101232
- Authors
- Asensi, V., Valle, E., Meana, A., Fierer, J., Celada, A., Alvarez, V., Paz, J., Coto, E., Carton, J. A., Maradona, J. A., Dieguez, A., Sarasúa, J., Ocaña, M. G., & Arribas, J. M.
- Affiliations
- Infectious Diseases and Molecular Genetics UnitsDepartments of
- University of California San Diego (US)
- Institut d'Investigacions Biomèdiques de Barcelona (ES)
- Traumatology
- Plastic Surgery, Hospital Central de Asturias, Oviedo University Medical School, Oviedo
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 2004-07
- Volume
- 72
- Issue
- 7
- Pages
- 3823-3828
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- PMC
- PMC427428
- OpenAlex
- W2120399781
- Cited by
- 93
- References
- 42
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 2 · 2023: 5 · 2022: 5 · 2021: 5 · 2020: 6 · 2019: 6 · 2018: 2 · 2017: 8 · 2016: 1 · 2015: 5 · 2014: 4 · 2013: 5 · 2012: 4
- FWCI
- 1.18
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Infection and Immunity (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Immunology and Microbiology › Immunology › Inflammation biomarkers and pathways
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Keywords
- interleukin-6, neutrophil apoptosis, osteomyelitis, IL-1α, anti-apoptotic effects, serum cytokines, anti-IL-6 antibody, neutrophil lifespan, chronic bone infection, tissue damage
- MeSH terms
- Female, Humans, Inflammation, Male, Middle Aged, Neutrophils, Osteomyelitis, Interleukin-6, Cytokines, Apoptosis, Serum
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