User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Monocytes from patients with Primary Ciliary Dyskinesia show enhanced inflammatory properties and produce higher levels of pro-inflammatory cytokines

Primary tabs

download
  • Open access
  • PDF
  • 2.01 M
Cockx, Maaike Gouwy, Mieke Ruytinx, Pieter Lodewijckx, Inge Van Hout, Anneleen Godding, Véronique [UCL] Struyf, Sofie

Patients with Primary Ciliary Dyskinesia (PCD) suffer from recurrent upper and lower airway infections due to defects in the cilia present on the respiratory epithelium. Since chronic inflammatory conditions can cause changes in innate immune responses, we investigated whether monocytes isolated from the peripheral blood of pediatric PCD patients respond differently to inflammatory stimuli, compared to monocytes from healthy children and adults. The receptor for C5a (C5aR) was upregulated in PCD, whereas expression levels of the leukocyte chemoattractant receptors CCR1, CCR2, CCR5, BLT1 and FPR1 on PCD monocytes were similar to those on monocytes from healthy individuals. Also in vitro migration of PCD monocytes towards the ligands of those receptors (CCL2, fMLP, C5a and LTB4) was normal. Compared to healthy children, PCD patients had a higher percentage of the non-classic monocyte subset (CD14+CD16++) in circulation. Finally, PCD monocytes produced higher levels of pro-inflammatory cytokines (IL-1β and TNF-α) and chemokines (CCL3, CCL5, CCL18 and CCL22) in response to LPS, peptidoglycan and/or dsRNA stimulation. These data suggest that monocytes might exacerbate inflammatory reactions in PCD patients and might maintain a positive feedback-loop feeding the inflammatory process.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2017
Language Anglais
Journal information "Scientific Reports" - Vol. 7, no. 1, p. 14657 [1-12] (2017)
Peer reviewed yes
Publisher Nature Publishing Group ((United Kingdom) London)
e-issn 2045-2322
Publication status Publié
Affiliations UCL - SSS/IREC/SLUC - Pôle St.-Luc
UCL - (SLuc) Service de pédiatrie spécialisée
Keywords Multidisciplinary
Links
  1. Boon Mieke, Jorissen Mark, Proesmans Marijke, De Boeck Kris, Primary ciliary dyskinesia, an orphan disease, 10.1007/s00431-012-1785-6
  2. Knowles Michael R., Zariwala Maimoona, Leigh Margaret, Primary Ciliary Dyskinesia, 10.1016/j.ccm.2016.04.008
  3. Werner Claudius, Onnebrink Jörg, Omran Heymut, Diagnosis and management of primary ciliary dyskinesia, 10.1186/s13630-014-0011-8
  4. Munkholm Mathias, Mortensen Jann, Mucociliary clearance: pathophysiological aspects, 10.1111/cpf.12085
  5. Horani Amjad, Brody Steven L., Ferkol Thomas W., Picking up speed: advances in the genetics of primary ciliary dyskinesia, 10.1038/pr.2013.200
  6. Kurkowiak Małgorzata, Ziętkiewicz Ewa, Witt Michał, Recent advances in primary ciliary dyskinesia genetics, 10.1136/jmedgenet-2014-102755
  7. Shapiro Adam J., Zariwala Maimoona A., Ferkol Thomas, Davis Stephanie D., Sagel Scott D., Dell Sharon D., Rosenfeld Margaret, Olivier Kenneth N., Milla Carlos, Daniel Sam J., Kimple Adam J., Manion Michele, Knowles Michael R., Leigh Margaret W., , Diagnosis, monitoring, and treatment of primary ciliary dyskinesia: PCD foundation consensus recommendations based on state of the art review : Diagnosis and Management of PCD, 10.1002/ppul.23304
  8. Satir Peter, Christensen Søren Tvorup, Overview of Structure and Function of Mammalian Cilia, 10.1146/annurev.physiol.69.040705.141236
  9. Kobbernagel Helene E., Buchvald Frederik F., Haarman Eric G., Casaulta Carmen, Collins Samuel A., Hogg Claire, Kuehni Claudia E., Lucas Jane S., Omran Heymut, Quittner Alexandra L., Werner Claudius, Nielsen Kim G., Study protocol, rationale and recruitment in a European multi-centre randomized controlled trial to determine the efficacy and safety of azithromycin maintenance therapy for 6 months in primary ciliary dyskinesia, 10.1186/s12890-016-0261-x
  10. Sagel S. D., Chmiel J. F., Konstan M. W., Sputum Biomarkers of Inflammation in Cystic Fibrosis Lung Disease, 10.1513/pats.200703-044br
  11. Bush Andrew, Payne Donald, Pike Sarah, Jenkins Gavin, Henke Markus O., Rubin Bruce K., Mucus Properties In Children With Primary Ciliary Dyskinesia, 10.1378/chest.129.1.118
  12. Ratjen Felix, Waters Valerie, Klingel Michelle, McDonald Nancy, Dell Sharon, Leahy Timothy Ronan, Yau Yvonne, Grasemann Hartmut, Changes in airway inflammation during pulmonary exacerbations in patients with cystic fibrosis and primary ciliary dyskinesia, 10.1183/13993003.01390-2015
  13. Dale D. C., Boxer L., Liles W. C., The phagocytes: neutrophils and monocytes, 10.1182/blood-2007-12-077917
  14. Headland Sarah E., Norling Lucy V., The resolution of inflammation: Principles and challenges, 10.1016/j.smim.2015.03.014
  15. Yona Simon, Jung Steffen, Monocytes: subsets, origins, fates and functions : , 10.1097/moh.0b013e3283324f80
  16. Murdoch, C. & Finn, A. Chemokine receptors and their role in inflammation and infectious diseases. Blood 95, 3032–3043 (2000).
  17. Luster Andrew D., Chemokines — Chemotactic Cytokines That Mediate Inflammation, 10.1056/nejm199802123380706
  18. Zlotnik Albert, Yoshie Osamu, Chemokines, 10.1016/s1074-7613(00)80165-x
  19. Ziegler-Heitbrock Loems, The CD14+ CD16+ blood monocytes: their role in infection and inflammation, 10.1189/jlb.0806510
  20. Stansfield Brian K, Ingram David A, Clinical significance of monocyte heterogeneity, 10.1186/s40169-014-0040-3
  21. Yegin Olcay, Chemotaxis in Childhood, 10.1203/00006450-198303000-00002
  22. Gerszten Robert E., Garcia-Zepeda Eduardo A., Lim Yaw-Chyn, Yoshida Masayuki, Ding Han A., Gimbrone Michael A., Luster Andrew D., Luscinskas Francis W., Rosenzweig Anthony, MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions, 10.1038/19546
  23. Griffin, J. D. et al. Granulocyte-macrophage colony-stimulating factor and other cytokines regulate surface expression of the leukocyte adhesion molecule-1 on human neutrophils, monocytes, and their precursors. J Immunol 145, 576–584 (1990).
  24. Middleton J., Leukocyte extravasation: chemokine transport and presentation by the endothelium, 10.1182/blood.v100.12.3853
  25. Mortier Anneleen, Loos Tamara, Gouwy Mieke, Ronsse Isabelle, Van Damme Jo, Proost Paul, Posttranslational Modification of the NH2-terminal Region of CXCL5 by Proteases or Peptidylarginine Deiminases (PAD) Differently Affects Its Biological Activity, 10.1074/jbc.m110.119388
  26. Nourshargh Sussan, Alon Ronen, Leukocyte Migration into Inflamed Tissues, 10.1016/j.immuni.2014.10.008
  27. Kzhyshkowska Julia, Gudima Alexandru, Moganti Kondaiah, Gratchev Alexei, Orekhov Alexander, Perspectives for Monocyte/Macrophage-Based Diagnostics of Chronic Inflammation, 10.1159/000444943
  28. Boon Mieke, De Boeck Kris, Jorissen Mark, Meyts Isabelle, Primary ciliary dyskinesia and humoral immunodeficiency – Is there a missing link?, 10.1016/j.rmed.2014.03.009
  29. Mukaida N, Interleukin-8 (IL-8) and monocyte chemotactic and activating factor (MCAF/MCP-1), chemokines essentially involved in inflammatory and immune reactions, 10.1016/s1359-6101(97)00022-1
  30. Zabel Brian A., Rott Alena, Butcher Eugene C., Leukocyte Chemoattractant Receptors in Human Disease Pathogenesis, 10.1146/annurev-pathol-012513-104640
  31. Lee Hyun, Whitfeld Peter L, Mackay Charles R, Receptors for complement C5a. The importance of C5aR and the enigmatic role of C5L2, 10.1038/sj.icb.7100166
  32. Dadfar E., Lundahl J., Jacobson S. H., Monocyte adhesion molecule expression in interstitial inflammation in patients with renal failure, 10.1093/ndt/gfg585
  33. Muniz-Junqueira, M. I. et al. Novel microtechnique for assessment of postnatal maturation of the phagocytic function of neutrophils and monocytes. Clin Diagn Lab Immunol 10, 1096–1102 (2003).
  34. Ziegler-Heitbrock L., Ancuta P., Crowe S., Dalod M., Grau V., Hart D. N., Leenen P. J. M., Liu Y.-J., MacPherson G., Randolph G. J., Scherberich J., Schmitz J., Shortman K., Sozzani S., Strobl H., Zembala M., Austyn J. M., Lutz M. B., Nomenclature of monocytes and dendritic cells in blood, 10.1182/blood-2010-02-258558
  35. Mukherjee Ratnadeep, Kanti Barman Pijus, Kumar Thatoi Pravat, Tripathy Rina, Kumar Das Bidyut, Ravindran Balachandran, Non-Classical monocytes display inflammatory features: Validation in Sepsis and Systemic Lupus Erythematous, 10.1038/srep13886
  36. Old Elizabeth A., Nadkarni Suchita, Grist John, Gentry Clive, Bevan Stuart, Kim Ki-Wook, Mogg Adrian J., Perretti Mauro, Malcangio Marzia, Monocytes expressing CX3CR1 orchestrate the development of vincristine-induced pain, 10.1172/jci71389
  37. Thomas G., Tacke R., Hedrick C. C., Hanna R. N., Nonclassical Patrolling Monocyte Function in the Vasculature, 10.1161/atvbaha.114.304650
  38. Skrzeczynska J., Kobylarz K., Hartwich Z., Zembala M., Pryjma J., CD14+CD16+ Monocytes in the Course of Sepsis in Neonates and Small Children: Monitoring and Functional Studies, 10.1046/j.1365-3083.2002.01092.x
  39. Sorio Claudio, Montresor Alessio, Bolomini-Vittori Matteo, Caldrer Sara, Rossi Barbara, Dusi Silvia, Angiari Stefano, Johansson Jan E., Vezzalini Marzia, Leal Teresinha, Calcaterra Elisa, Assael Baroukh M., Melotti Paola, Laudanna Carlo, Mutations of Cystic Fibrosis Transmembrane Conductance Regulator Gene Cause a Monocyte-Selective Adhesion Deficiency, 10.1164/rccm.201510-1922oc
  40. Van de Weert–van Leeuwen Pauline B., Van Meegen Marit A., Speirs Jennifer J., Pals D. J., Rooijakkers Suzan H. M., Van der Ent Cornelis K., Terheggen-Lagro Suzanne W. J., Arets Hubertus G. M., Beekman Jeffrey M., Optimal Complement-Mediated Phagocytosis ofPseudomonas aeruginosaby Monocytes Is Cystic Fibrosis Transmembrane Conductance Regulator–Dependent, 10.1165/rcmb.2012-0502oc
  41. Bush A., Chodhari R., Collins N., Copeland F., Hall P., Harcourt J., Hariri M., Hogg C., Lucas J., Mitchison H. M, O'Callaghan C., Phillips G., Primary ciliary dyskinesia: current state of the art, 10.1136/adc.2006.096958
  42. Gouwy Mieke, De Buck Mieke, Pörtner Noëmie, Opdenakker Ghislain, Proost Paul, Struyf Sofie, Van Damme Jo, Serum amyloid A chemoattracts immature dendritic cells and indirectly provokes monocyte chemotaxis by induction of cooperating CC and CXC chemokines : Cellular immune response, 10.1002/eji.201444818
Bibliographic reference Cockx, Maaike ; Gouwy, Mieke ; Ruytinx, Pieter ; Lodewijckx, Inge ; Van Hout, Anneleen ; et. al. Monocytes from patients with Primary Ciliary Dyskinesia show enhanced inflammatory properties and produce higher levels of pro-inflammatory cytokines. In: Scientific Reports, Vol. 7, no. 1, p. 14657 [1-12] (2017)
Permanent URL http://hdl.handle.net/2078.1/195894