Interleukin 10 (IL-10) inhibits the release of proinflammatory cytokines from human polymorphonuclear leukocytes. Evidence for an autocrine role of tumor necrosis factor and IL-1 beta in mediating the production of IL-8 triggered by lipopolysaccharide

doi:10.1084/jem.178.6.2207

This Article

	Full Text (PDF, 586K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JEM
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Cassatella, M. A.
	Articles by Constantin, G.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Cassatella, M. A.
	Articles by Constantin, G.


Social Bookmarking

	What's this?

ARTICLES

Interleukin 10 (IL-10) inhibits the release of proinflammatory cytokines from human polymorphonuclear leukocytes. Evidence for an autocrine role of tumor necrosis factor and IL-1 beta in mediating the production of IL-8 triggered by lipopolysaccharide

MA Cassatella, L Meda, S Bonora, M Ceska and G Constantin
Institute of General Pathology, University of Verona, Italy.

In this study we have examined the effects of interleukin 10 (IL-10) on polymorphonuclear leukocytes (PMN), and found that it is a potent inhibitor of tumor necrosis factor (TNF), IL-1 beta, and IL-8 secretion triggered by lipopolysaccharide (LPS). Cytokine production by phagocytosing PMN was also inhibited by IL-10, but to a lesser extent than the LPS-induced production. As shown by Northern blot analysis, IL- 10 diminished the levels of TNF, IL-1 beta, and IL-8 mRNAs late after the onset of stimulation of PMN with LPS. In addition, we provide evidence that the kinetics of LPS-induced IL-8 production by PMN is composed of two distinct phases. Specifically, our experiments demonstrated that in the first phase, the production of IL-8 is a process directly induced by LPS that lasts for some hours. After this early wave, a second phase begins that is sustained and leads to an elevated production of IL-8 that appears to be due to the endogenous release of TNF and IL-1 beta. This second wave can in fact be blocked by anti-TNF and anti-IL-1 beta neutralizing antibodies, and by IL-10 as the consequence of its downregulatory effects on TNF and IL-1 beta release. Taken together, these findings identify novel biological actions of IL-10 as a suppressor of the inflammatory response.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Fortin, C. F., Ear, T., McDonald, P. P. (2009). Autocrine role of endogenous interleukin-18 on inflammatory cytokine generation by human neutrophils. FASEB J. 23: 194-203 [Abstract] [Full Text]
Brown, C. R., Lai, A. Y.-C., Callen, S. T., Blaho, V. A., Hughes, J. M., Mitchell, W. J. (2008). Adenoviral Delivery of Interleukin-10 Fails To Attenuate Experimental Lyme Disease. Infect. Immun. 76: 5500-5507 [Abstract] [Full Text]
Cunha, T. M., Verri, W. A. Jr., Schivo, I. R., Napimoga, M. H., Parada, C. A., Poole, S., Teixeira, M. M., Ferreira, S. H., Cunha, F. Q. (2008). Crucial role of neutrophils in the development of mechanical inflammatory hypernociception. J. Leukoc. Biol. 83: 824-832 [Abstract] [Full Text]
Tamassia, N., Calzetti, F., Menestrina, N., Rossato, M., Bazzoni, F., Gottin, L., Cassatella, M. A. (2008). Circulating neutrophils of septic patients constitutively express IL-10R1 and are promptly responsive to IL-10. Int Immunol 20: 535-541 [Abstract] [Full Text]
Charmoy, M., Megnekou, R., Allenbach, C., Zweifel, C., Perez, C., Monnat, K., Breton, M., Ronet, C., Launois, P., Tacchini-Cottier, F. (2007). Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection. J. Leukoc. Biol. 82: 288-299 [Abstract] [Full Text]
Cassatella, M. A., da Silva, G. P., Tinazzi, I., Facchetti, F., Scapini, P., Calzetti, F., Tamassia, N., Wei, P., Nardelli, B., Roschke, V., Vecchi, A., Mantovani, A., Bambara, L. M., Edwards, S. W., Carletto, A. (2007). Soluble TNF-Like Cytokine (TL1A) Production by Immune Complexes Stimulated Monocytes in Rheumatoid Arthritis. J. Immunol. 178: 7325-7333 [Abstract] [Full Text]
Nozell, S., Laver, T., Patel, K., Benveniste, E. N. (2006). Mechanism of IFN-beta-Mediated Inhibition of IL-8 Gene Expression in Astroglioma Cells. J. Immunol. 177: 822-830 [Abstract] [Full Text]
Dang, P. M.-C., Elbim, C., Marie, J.-C., Chiandotto, M., Gougerot-Pocidalo, M.-A., El-Benna, J. (2006). Anti-inflammatory effect of interleukin-10 on human neutrophil respiratory burst involves inhibition of GM-CSF-induced p47PHOX phosphorylation through a decrease in ERK1/2 activity. FASEB J. 20: 1504-1506 [Abstract] [Full Text]
Grisaru, D., Pick, M., Perry, C., Sklan, E. H., Almog, R., Goldberg, I., Naparstek, E., Lessing, J. B., Soreq, H., Deutsch, V. (2006). Hydrolytic and Nonenzymatic Functions of Acetylcholinesterase Comodulate Hemopoietic Stress Responses. J. Immunol. 176: 27-35 [Abstract] [Full Text]
Mikamo, H., Johri, A. K., Paoletti, L. C., Madoff, L. C., Onderdonk, A. B. (2004). Adherence to, Invasion by, and Cytokine Production in Response to Serotype VIII Group B Streptococci. Infect. Immun. 72: 4716-4722 [Abstract] [Full Text]
Bannerman, D. D., Paape, M. J., Hare, W. R., Hope, J. C. (2004). Characterization of the Bovine Innate Immune Response to Intramammary Infection with Klebsiella pneumoniae. J DAIRY SCI 87: 2420-2432 [Abstract] [Full Text]
Bannerman, D. D., Paape, M. J., Lee, J.-W., Zhao, X., Hope, J. C., Rainard, P. (2004). Escherichia coli and Staphylococcus aureus Elicit Differential Innate Immune Responses following Intramammary Infection. CVI 11: 463-472 [Abstract] [Full Text]
Deepe, G. S. Jr., Gibbons, R. S. (2003). Protective and Memory Immunity to Histoplasma capsulatum in the Absence of IL-10. J. Immunol. 171: 5353-5362 [Abstract] [Full Text]
Pathmanathan, S, Krishna, M T, Blomberg, A, Helleday, R, Kelly, F J, Sandstrom, T, Holgate, S T, Wilson, S J, Frew, A J (2003). Repeated daily exposure to 2 ppm nitrogen dioxide upregulates the expression of IL-5, IL-10, IL-13, and ICAM-1 in the bronchial epithelium of healthy human airways. Occup. Environ. Med. 60: 892-896 [Abstract] [Full Text]
Asadullah, K., Sterry, W., Volk, H. D. (2003). Interleukin-10 Therapy--Review of a New Approach. Pharmacol. Rev. 55: 241-269 [Abstract] [Full Text]
Ng, P C, Li, K, Wong, R P O, Chui, K, Wong, E, Li, G, Fok, T F (2003). Proinflammatory and anti-inflammatory cytokine responses in preterm infants with systemic infections. Arch. Dis. Child. Fetal Neonatal Ed. 88: F209-F213 [Abstract] [Full Text]
Oei, J, Lui, K, Wang, H, Henry, R (2003). Decreased neutrophil apoptosis in tracheal fluids of preterm infants at risk of chronic lung disease. Arch. Dis. Child. Fetal Neonatal Ed. 88: F245-F249 [Abstract] [Full Text]
Vulcano, M., Struyf, S., Scapini, P., Cassatella, M., Bernasconi, S., Bonecchi, R., Calleri, A., Penna, G., Adorini, L., Luini, W., Mantovani, A., Van Damme, J., Sozzani, S. (2003). Unique Regulation of CCL18 Production by Maturing Dendritic Cells. J. Immunol. 170: 3843-3849 [Abstract] [Full Text]
Von der Thusen, J. H., Kuiper, J., Van Berkel, T. J. C., Biessen, E. A. L. (2003). Interleukins in Atherosclerosis: Molecular Pathways and Therapeutic Potential. Pharmacol. Rev. 55: 133-166 [Abstract] [Full Text]
Vale, M. L., Marques, J. B., Moreira, C. A., Rocha, F. A. C., Ferreira, S. H., Poole, S., Cunha, F. Q., Ribeiro, R. A. (2003). Antinociceptive Effects of Interleukin-4, -10, and -13 on the Writhing Response in Mice and Zymosan-Induced Knee Joint Incapacitation in Rats. J. Pharmacol. Exp. Ther. 304: 102-108 [Abstract] [Full Text]
Sato, T. A., Keelan, J. A., Mitchell, M. D. (2003). Critical Paracrine Interactions Between TNF-{alpha} and IL-10 Regulate Lipopolysaccharide-Stimulated Human Choriodecidual Cytokine and Prostaglandin E2 Production. J. Immunol. 170: 158-166 [Abstract] [Full Text]
Antunes, G., Evans, S.A., Lordan, J.L., Frew, A.J. (2002). Systemic cytokine levels in community-acquired pneumonia and their association with disease severity. Eur Respir J 20: 990-995 [Abstract] [Full Text]
Puliti, M., von Hunolstein, C., Verwaerde, C., Bistoni, F., Orefici, G., Tissi, L. (2002). Regulatory Role of Interleukin-10 in Experimental Group B Streptococcal Arthritis. Infect. Immun. 70: 2862-2868 [Abstract] [Full Text]
Kurosaka, K., Watanabe, N., Kobayashi, Y. (2002). Potentiation by human serum of anti-inflammatory cytokine production by human macrophages in response to apoptotic cells. J. Leukoc. Biol. 71: 950-956 [Abstract] [Full Text]
Chmiel, J. F., Konstan, M. W., Saadane, A., Krenicky, J. E., Lester Kirchner, H., Berger, M. (2002). Prolonged Inflammatory Response to Acute Pseudomonas Challenge in Interleukin-10 Knockout Mice. Am. J. Respir. Crit. Care Med. 165: 1176-1181 [Abstract] [Full Text]
Crepaldi, L., Gasperini, S., Lapinet, J. A., Calzetti, F., Pinardi, C., Liu, Y., Zurawski, S., de Waal Malefyt, R., Moore, K. W., Cassatella, M. A. (2001). Up-Regulation of IL-10R1 Expression Is Required to Render Human Neutrophils Fully Responsive to IL-10. J. Immunol. 167: 2312-2322 [Abstract] [Full Text]
Letterio, J. J., Lehrnbecher, T., Pollack, G., Walsh, T. J., Chanock, S. J. (2001). Invasive Candidiasis Stimulates Hepatocyte and Monocyte Production of Active Transforming Growth Factor {beta}. Infect. Immun. 69: 5115-5120 [Abstract] [Full Text]
Hattar, K., Fink, L., Fietzner, K., Himmel, B., Grimminger, F., Seeger, W., Sibelius, U. (2001). Cell Density Regulates Neutrophil IL-8 Synthesis: Role of IL-1 Receptor Antagonist and Soluble TNF Receptors. J. Immunol. 166: 6287-6293 [Abstract] [Full Text]
YOSHIDA, K., MATSUMOTO, T., TATEDA, K., UCHIDA, K., TSUJIMOTO, S., YAMAGUCHI, K. (2001). Induction of interleukin-10 and down-regulation of cytokine production by Klebsiella pneumoniae capsule in mice with pulmonary infection. J Med Microbiol 50: 456-461 [Abstract] [Full Text]
Elbim, C., Reglier, H., Fay, M., Delarche, C., Andrieu, V., El Benna, J., Gougerot-Pocidalo, M.-A. (2001). Intracellular Pool of IL-10 Receptors in Specific Granules of Human Neutrophils: Differential Mobilization by Proinflammatory Mediators. J. Immunol. 166: 5201-5207 [Abstract] [Full Text]
Bhattacharyya, S., Ghosh, S., Jhonson, P. L., Bhattacharya, S. K., Majumdar, S. (2001). Immunomodulatory Role of Interleukin-10 in Visceral Leishmaniasis: Defective Activation of Protein Kinase C-Mediated Signal Transduction Events. Infect. Immun. 69: 1499-1507 [Abstract] [Full Text]
Murthy, P. K., Dennis, V. A., Lasater, B. L., Philipp, M. T. (2000). Interleukin-10 Modulates Proinflammatory Cytokines in the Human Monocytic Cell Line THP-1 Stimulated with Borrelia burgdorferi Lipoproteins. Infect. Immun. 68: 6663-6669 [Abstract] [Full Text]
Lapinet, J. A., Scapini, P., Calzetti, F., Perez, O., Cassatella, M. A. (2000). Gene Expression and Production of Tumor Necrosis Factor Alpha, Interleukin-1beta (IL-1beta ), IL-8, Macrophage Inflammatory Protein 1alpha (MIP-1alpha ), MIP-1beta , and Gamma Interferon-Inducible Protein 10 by Human Neutrophils Stimulated with Group B Meningococcal Outer Membrane Vesicles. Infect. Immun. 68: 6917-6923 [Abstract] [Full Text]
Hill, A., Gompertz, S., Stockley, R. (2000). Factors influencing airway inflammation in chronic obstructive pulmonary disease. Thorax 55: 970-977 [Full Text]
Bone-Larson, C. L., Hogaboam, C. M., Steinhauser, M. L., Oliveira, S. H. P., Lukacs, N. W., Strieter, R. M., Kunkel, S. L. (2000). Novel Protective Effects of Stem Cell Factor in a Murine Model of Acute Septic Peritonitis : Dependence on MCP-1. Am. J. Pathol. 157: 1177-1186 [Abstract] [Full Text]
Saegusa, K., Ishimaru, N., Yanagi, K., Haneji, N., Nishino, M., Azuma, M., Saito, I., Hayashi, Y. (2000). Autoantigen-Specific CD4+CD28low T Cell Subset Prevents Autoimmune Exocrinopathy in Murine Sjogren's Syndrome. J. Immunol. 165: 2251-2257 [Abstract] [Full Text]
Barbara, G, Xing, Z, Hogaboam, C M, Gauldie, J, Collins, S M (2000). Interleukin 10 gene transfer prevents experimental colitis in rats. Gut 46: 344-349 [Abstract] [Full Text]
McColm, J. R, Stenson, B. J, Biermasz, N., McIntosh, N. (2000). Measurement of interleukin 10 in bronchoalveolar lavage from preterm ventilated infants. Arch. Dis. Child. Fetal Neonatal Ed. 82: 156F-159 [Abstract] [Full Text]
Minter, R. M., Rectenwald, J. E., Fukuzuka, K., Tannahill, C. L., La Face, D., Tsai, V., Ahmed, I., Hutchins, E., Moyer, R., Copeland, E. M. III, Moldawer, L. L. (2000). TNF-{alpha} Receptor Signaling and IL-10 Gene Therapy Regulate the Innate and Humoral Immune Responses to Recombinant Adenovirus in the Lung. J. Immunol. 164: 443-451 [Abstract] [Full Text]
Stämpfli, M. R., Cwiartka, M., Gajewska, B. U., Alvarez, D., Ritz, S. A., Inman, M. D., Xing, Z., Jordana, M. (1999). Interleukin-10 Gene Transfer to the Airway Regulates Allergic Mucosal Sensitization in Mice. Am. J. Respir. Cell Mol. Bio. 21: 586-596 [Abstract] [Full Text]
ZHANG, H., KIM, Y. K., GOVINDARAJAN, A., BABA, A., BINNIE, M., MARCO RANIERI, V., LIU, M., SLUTSKY, A. S. (1999). Effect of Adrenoreceptors on Endotoxin-induced Cytokines and Lipid Peroxidation in Lung Explants. Am. J. Respir. Crit. Care Med. 160: 1703-1710 [Abstract] [Full Text]
Cassatella, M. A., Gasperini, S., Bovolenta, C., Calzetti, F., Vollebregt, M., Scapini, P., Marchi, M., Suzuki, R., Suzuki, A., Yoshimura, A. (1999). Interleukin-10 (IL-10) Selectively Enhances CIS3/SOCS3 mRNA Expression in Human Neutrophils: Evidence for an IL-10-Induced Pathway That Is Independent of STAT Protein Activation. Blood 94: 2880-2889 [Abstract] [Full Text]
Yeh, S.-S., Schuster, M. W (1999). Geriatric cachexia: the role of cytokines. Am. J. Clin. Nutr. 70: 183-197 [Abstract] [Full Text]
Schwartz, D. A., Wohlford-Lenane, C. L., Quinn, T. J., Krieg, A. M. (1999). Bacterial DNA or Oligonucleotides Containing Unmethylated CpG Motifs Can Minimize Lipopolysaccharide-Induced Inflammation in the Lower Respiratory Tract Through an IL-12-Dependent Pathway. J. Immunol. 163: 224-231 [Abstract] [Full Text]
Adib-Conquy, M., Petit, A.-F., Marie, C., Fitting, C., Cavaillon, J.-M. (1999). Paradoxical priming effects of IL-10 on cytokine production. Int Immunol 11: 689-698 [Abstract] [Full Text]
Steinhauser, M. L., Hogaboam, C. M., Lukacs, N. W., Strieter, R. M., Kunkel, S. L. (1999). Multiple Roles for IL-12 in a Model of Acute Septic Peritonitis. J. Immunol. 162: 5437-5443 [Abstract] [Full Text]
Gasperini, S., Marchi, M., Calzetti, F., Laudanna, C., Vicentini, L., Olsen, H., Murphy, M., Liao, F., Farber, J., Cassatella, M. A. (1999). Gene Expression and Production of the Monokine Induced by IFN-{gamma} (MIG), IFN-Inducible T Cell {alpha} Chemoattractant (I-TAC), and IFN-{gamma}-Inducible Protein-10 (IP-10) Chemokines by Human Neutrophils. J. Immunol. 162: 4928-4937 [Abstract] [Full Text]
Warren, G. W., Poloyac, S. M., Gary, D. S., Mattson, M. P., Blouin, R. A. (1999). Hepatic Cytochrome P-450 Expression in Tumor Necrosis Factor-alpha Receptor (p55/p75) Knockout Mice After Endotoxin Administration. J. Pharmacol. Exp. Ther. 288: 945-950 [Abstract] [Full Text]
Ajuebor, M. N., Das, A. M., Virag, L., Flower, R. J., Szabo, C., Perretti, M. (1999). Role of Resident Peritoneal Macrophages and Mast Cells in Chemokine Production and Neutrophil Migration in Acute Inflammation: Evidence for an Inhibitory Loop Involving Endogenous IL-10. J. Immunol. 162: 1685-1691 [Abstract] [Full Text]
Glynn, P, Coakley, R, Kilgallen, I, Murphy, N, O'Neill, S (1999). Circulating interleukin 6�and interleukin 10�in community acquired pneumonia. Thorax 54: 51-55 [Abstract] [Full Text]
Steinhauser, M. L., Hogaboam, C. M., Kunkel, S. L., Lukacs, N. W., Strieter, R. M., Standiford, T. J. (1999). IL-10 Is a Major Mediator of Sepsis-Induced Impairment in Lung Antibacterial Host Defense. J. Immunol. 162: 392-399 [Abstract] [Full Text]
Geissler, K., Ohler, L., Fodinger, M., Kabrna, E., Kollars, M., Skoupy, S., Lechner, K. (1998). Interleukin-10 Inhibits Erythropoietin-Independent Growth of Erythroid Bursts in Patients With Polycythemia Vera. Blood 92: 1967-1972 [Abstract] [Full Text]
Van Laethem, J-L, Eskinazi, R, Louis, H, Rickaert, F, Robberecht, P, Deviere, J (1998). Multisystemic production of interleukin 10�limits the severity of acute pancreatitis in mice. Gut 43: 408-413 [Abstract] [Full Text]
Downing, L. J., Strieter, R. M., Kadell, A. M., Wilke, C. A., Austin, J. C., Hare, B. D., Burdick, M. D., Greenfield, L. J., Wakefield, T. W. (1998). IL-10 Regulates Thrombus-Induced Vein Wall Inflammation and Thrombosis. J. Immunol. 161: 1471-1476 [Abstract] [Full Text]
Marie, C., Muret, J., Fitting, C., Losser, M.-R., Payen, D., Cavaillon, J.-M. (1998). Reduced Ex Vivo Interleukin-8 Production by Neutrophils in Septic and Nonseptic Systemic Inflammatory Response Syndrome. Blood 91: 3439-3446 [Abstract] [Full Text]
Nikolaus, S, Bauditz, J, Gionchetti, P, Witt, C, Lochs, H, Schreiber, S (1998). Increased secretion of pro-inflammatory cytokines by circulating polymorphonuclear neutrophils and regulation by interleukin 10�during intestinal inflammation. Gut 42: 470-476 [Abstract] [Full Text]
Ehrlich, L. C., Hu, S., Sheng, W. S., Sutton, R. L., Rockswold, G. L., Peterson, P. K., Chao, C. C. (1998). Cytokine Regulation of Human Microglial Cell IL-8 Production. J. Immunol. 160: 1944-1948 [Abstract] [Full Text]
Maloney, C. G., Kutchera, W. A., Albertine, K. H., McIntyre, T. M., Prescott, S. M., Zimmerman, G. A. (1998). Inflammatory Agonists Induce Cyclooxygenase Type 2 Expression by Human Neutrophils. J. Immunol. 160: 1402-1410 [Abstract] [Full Text]
Keel, M., Ungethum, U., Steckholzer, U., Niederer, E., Hartung, T., Trentz, O., Ertel, W. (1997). Interleukin-10 Counterregulates Proinflammatory Cytokine-Induced Inhibition of Neutrophil Apoptosis During Severe Sepsis. Blood 90: 3356-3363 [Abstract] [Full Text]
McDonald, P. P., Bald, A., Cassatella, M. A. (1997). Activation of the NF-kappa B Pathway by Inflammatory Stimuli in Human Neutrophils. Blood 89: 3421-3433 [Abstract] [Full Text]
Niiro, H., Otsuka, T., Izuhara, K., Yamaoka, K., Ohshima, K., Tanabe, T., Hara, S., Nemoto, Y., Tanaka, Y., Nakashima, H., Niho, Y. (1997). Regulation by Interleukin-10 and Interleukin-4 of Cyclooxygenase-2 Expression in Human Neutrophils. Blood 89: 1621-1628 [Abstract] [Full Text]
Brown, C. Y., Lagnado, C. A., Vadas, M. A., Goodall, G. J. (1996). Differential Regulation of the Stability of Cytokine mRNAs in Lipopolysaccharide-activated Blood Monocytes in Response to Interleukin-10. J. Biol. Chem. 271: 20108-20112 [Abstract] [Full Text]
Crawley, J. B., Williams, L. M., Mander, T., Brennan, F. M., Foxwell, B. M.J. (1996). Interleukin-10 Stimulation of Phosphatidylinositol 3-Kinase and p70 S6 Kinase Is Required for the Proliferative but Not the Antiinflammatory Effects of the Cytokine. J. Biol. Chem. 271: 16357-16362 [Abstract] [Full Text]
Seghaye, M.-C., Duchateau, J., Bruniaux, J., Demontoux, S., Bosson, C., Serraf, A., Lecronier, G., Mokhfi, E., Planche, C. (1996). INTERLEUKIN-10 RELEASE RELATED TO CARDIOPULMONARY BYPASS IN INFANTS UNDERGOING CARDIAC OPERATIONS. J. Thorac. Cardiovasc. Surg. 111: 545-553 [Abstract] [Full Text]
Rabinovici, R., Neville, L.F., Feuerstein, G. (1995). Current understanding of sepsis: criticism and a proposal. Innate Immunity 2: 163-168 [Abstract]