Chronic inflammation triggered by the NLRP3 inflammasome in myeloid cells promotes growth plate dysplasia by mesenchymal cells

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Wang, Chun ^a   Xu, Can Xin ^a   Alippe, Yael ^a   Qu, Chao ^a   Xiao, Jianqiu ^a   Schipani, Ernestina ^b   Civitelli, Roberto ^a   Abu Amer, Yousef ^a   Mbalaviele, Gabriel ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; HIF1A PROTEIN, MOUSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INFLAMMASOME; INTERLEUKIN 1; NOD-LIKE RECEPTOR PROTEIN 3 INFLAMMASOME, MOUSE;

ANIMAL; BONE MARROW CELL; CHONDROCYTE; CINCA SYNDROME; DISEASE MODEL; DOWN REGULATION; EPIPHYSIS PLATE; INFLAMMATION; METABOLISM; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CHONDROCYTES; CRYOPYRIN-ASSOCIATED PERIODIC SYNDROMES; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GROWTH PLATE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1; MICE; MYELOID CELLS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 85022088701     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-05033-5     Document Type: Article

References (51)

1. Hoffman, H. M. & Broderick, L. The role of the inflammasome in patients with autoinflammatory diseases. J Allergy Clin Immunol 138, 3-14 (2016).
2. de Jesus, A. A., Canna, S. W., Liu, Y. & Goldbach-Mansky, R. Molecular mechanisms in genetically defined autoinflammatory diseases: disorders of amplified danger signaling. Annu Rev Immunol 33, 823-874 (2015).
3. Aksentijevich, I. et al. De novo CIAS1 mutations, cytokine activation, and evidence for genetic heterogeneity in patients with neonatal-onset multisystem inflammatory disease (NOMID): a new member of the expanding family of pyrin-associated autoinflammatory diseases. Arthritis and rheumatism 46, 3340-3348 (2002).
4. Zaki, F. M., Sridharan, R., Pei, T. S., Ibrahim, S. & Ping, T. S. NOMID: the radiographic and MRI features and review of literature. J Radiol Case Rep 6, 1-8 (2012).
5. Hill, S. C. et al. Arthropathy of neonatal onset multisystem inflammatory disease (NOMID/CINCA). Pediatr Radiol 37, 145-152 (2007).
6. Feldmann, J. et al. Chronic infantile neurological cutaneous and articular syndrome is caused by mutations in CIAS1, a gene highly expressed in polymorphonuclear cells and chondrocytes. Am J Hum Genet 71, 198-203 (2002).
7. Guo, H., Callaway, J. B. & Ting, J. P. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nature medicine 21, 677-687 (2015).
8. Broz, P. & Dixit, V. M. Inflammasomes: mechanism of assembly, regulation and signalling. Nat Rev Immunol 16, 407-420 (2016).
9. Segovia, J. et al. TLR2/MyD88/NF-kappaB pathway, reactive oxygen species, potassium efflux activates NLRP3/ASC inflammasome during respiratory syncytial virus infection. PloS one 7, e29695 (2012).
10. Bauernfeind, F. G. et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. Journal of immunology 183, 787-791 (2009).
11. Brydges, S. D. et al. Inflammasome-mediated disease animal models reveal roles for innate but not adaptive immunity. Immunity 30, 875-887 (2009).
12. Meng, G., Zhang, F., Fuss, I., Kitani, A. & Strober, W. A mutation in the Nlrp3 gene causing inflammasome hyperactivation potentiates Th17 cell-dominant immune responses. Immunity 30, 860-874 (2009).
13. McCall, S. H. et al. Osteoblasts express NLRP3, a nucleotide-binding domain and leucine-rich repeat region containing receptor implicated in bacterially induced cell death. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research 23, 30-40 (2008).
14. Bonar, S. L. et al. Constitutively activated NLRP3 inflammasome causes inflammation and abnormal skeletal development in mice. PloS one 7, e35979 (2012).
15. Yokoyama, K. et al. Enhanced chondrogenesis of induced pluripotent stem cells from patients with neonatal-onset multisystem inflammatory disease occurs via the caspase 1-independent cAMP/protein kinase A/CREB pathway. Arthritis & rheumatology 67, 302-314 (2015).
16. Almeida, M. Q. et al. Protein kinase A regulates caspase-1 via Ets-1 in bone stromal cell-derived lesions: a link between cyclic AMP and pro-inflammatory pathways in osteoblast progenitors. Human molecular genetics 20, 165-175 (2011).
17. Hawkins, P. N., Lachmann, H. J., Aganna, E. & McDermott, M. F. Spectrum of clinical features in Muckle-Wells syndrome and response to anakinra. Arthritis and rheumatism 50, 607-612 (2004).
18. Agostini, L. et al. NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity 20, 319-325 (2004).
19. Kone-Paut, I. & Galeotti, C. Current treatment recommendations and considerations for cryopyrin-associated periodic syndrome. Expert review of clinical immunology 11, 1083-1092 (2015).
20. Anton, J. et al. Efficacy and safety of canakinumab in cryopyrin-associated periodic syndromes: results from a Spanish cohort. Clin Exp Rheumatol 33, S67-71 (2015).
21. Sibley, C. H. et al. Sustained response and prevention of damage progression in patients with neonatal-onset multisystem inflammatory disease treated with anakinra: a cohort study to determine three-and five-year outcomes. Arthritis and rheumatism 64, 2375-2386 (2012).
22. Neven, B. et al. Long-term efficacy of the interleukin-1 receptor antagonist anakinra in ten patients with neonatal-onset multisystem inflammatory disease/chronic infantile neurologic, cutaneous, articular syndrome. Arthritis and rheumatism 62, 258-267 (2010).
23. Rigante, D., Leone, A., Marrocco, R., Laino, M. E. & Stabile, A. Long-term response after 6-year treatment with anakinra and onset of focal bone erosion in neonatal-onset multisystem inflammatory disease (NOMID/CINCA). Rheumatol Int 31, 1661-1664 (2011).
24. Wang, C. et al. Poly-ADP-ribosylation-mediated degradation of ARTD1 by the NLRP3 inflammasome is a prerequisite for osteoclast maturation. Cell death & disease 7, e2153 (2016).
25. Qu, C. et al. NLRP3 mediates osteolysis through inflammation-dependent and-independent mechanisms. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 29, 1269-1279 (2015).
26. Malireddi, R. K., Ippagunta, S., Lamkanfi, M. & Kanneganti, T. D. Cutting edge: proteolytic inactivation of poly(ADP-ribose) polymerase 1 by the Nlrp3 and Nlrc4 inflammasomes. Journal of immunology 185, 3127-3130 (2010).
27. Erener, S. et al. Inflammasome-activated caspase 7 cleaves PARP1 to enhance the expression of a subset of NF-kappaB target genes. Molecular cell 46, 200-211 (2012).
28. Snouwaert, J. N. et al. An NLRP3 Mutation Causes Arthropathy and Osteoporosis in Humanized Mice. Cell reports 17, 3077-3088 (2016).
29. Mbalaviele, G. et al. A novel, highly selective, tight binding IkappaB kinase-2 (IKK-2) inhibitor: a tool to correlate IKK-2 activity to the fate and functions of the components of the nuclear factor-kappaB pathway in arthritis-relevant cells and animal models. The Journal of pharmacology and experimental therapeutics 329, 14-25 (2009).
30. Swarnkar, G., Zhang, K., Mbalaviele, G., Long, F. & Abu-Amer, Y. Constitutive activation of IKK2/NF-kappaB impairs osteogenesis and skeletal development. PloS one 9, e91421 (2014).
31. Miyamae, T. et al. Effect of anakinra on arthropathy in CINCA/NOMID syndrome. Pediatric rheumatology online journal 8, 9 (2010).
32. Robaszkiewicz, A. et al. ARTD1 regulates osteoclastogenesis and bone homeostasis by dampening NF-kappaB-dependent transcription of IL-1beta. Scientific reports 6, 21131 (2016).
33. Cramer, T., Schipani, E., Johnson, R. S., Swoboda, B. & Pfander, D. Expression of VEGF isoforms by epiphyseal chondrocytes during low-oxygen tension is HIF-1 alpha dependent. Osteoarthritis and cartilage 12, 433-439 (2004).
34. Maes, C. et al. VEGF-independent cell-autonomous functions of HIF-1alpha regulating oxygen consumption in fetal cartilage are critical for chondrocyte survival. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research 27, 596-609 (2012).
35. Panchanathan, R., Liu, H. & Choubey, D. Hypoxia primes human normal prostate epithelial cells and cancer cell lines for the NLRP3 and AIM2 inflammasome activation. Oncotarget 7, 28183-28194 (2016).
36. Folco, E. J., Sukhova, G. K., Quillard, T. & Libby, P. Moderate hypoxia potentiates interleukin-1beta production in activated human macrophages. Circulation research 115, 875-883 (2014).
37. Brydges, S. D. et al. Divergence of IL-1, IL-18, and cell death in NLRP3 inflammasomopathies. The Journal of clinical investigation 123, 4695-4705 (2013).
38. Weiss, G. & Goodnough, L. T. Anemia of chronic disease. The New England journal of medicine 352, 1011-1023 (2005).
39. Kheansaard, W., Panichob, P., Fucharoen, S. & Tanyong, D. I. Cytokine-induced apoptosis of beta-thalassemia/hemoglobin E erythroid progenitor cells via nitric oxide-mediated process in vitro. Acta haematologica 126, 224-230 (2011).
40. Jelkmann, W. Proinflammatory cytokines lowering erythropoietin production. Journal of interferon & cytokine research: the official journal of the International Society for Interferon and Cytokine Research 18, 555-559 (1998).
41. Pinero, D. J., Hu, J., Cook, B. M., Scaduto, R. C. Jr. & Connor, J. R. Interleukin-1beta increases binding of the iron regulatory protein and the synthesis of ferritin by increasing the labile iron pool. Biochimica et biophysica acta 1497, 279-288 (2000).
42. Rogers, J. T. et al. Translational control during the acute phase response. Ferritin synthesis in response to interleukin-1. The Journal of biological chemistry 265, 14572-14578 (1990).
43. Clausen, B. E., Burkhardt, C., Reith, W., Renkawitz, R. & Forster, I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic research 8, 265-277 (1999).
44. Ovchinnikov, D. A., Deng, J. M., Ogunrinu, G. & Behringer, R. R. Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis 26, 145-146 (2000).
45. Yu, K. et al. Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130, 3063-3074 (2003).
46. Lewis, R. et al. Disruption of the developmentally-regulated Col2a1 pre-mRNA alternative splicing switch in a transgenic knock-in mouse model. Matrix biology: journal of the International Society for Matrix Biology 31, 214-226 (2012).
47. Merceron, C. et al. Loss of HIF-1alpha in the notochord results in cell death and complete disappearance of the nucleus pulposus. PloS one 9, e110768 (2014).
48. Calvi, L. M. et al. Activated parathyroid hormone/parathyroid hormone-related protein receptor in osteoblastic cells differentially affects cortical and trabecular bone. The Journal of clinical investigation 107, 277-286 (2001).
49. Takeshita, S., Kaji, K. & Kudo, A. Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research 15, 1477-1488 (2000).
50. Mirando, A. J., Dong, Y., Kim, J. & Hilton, M. J. Isolation and culture of murine primary chondrocytes. Methods in molecular biology 1130, 267-277 (2014).
51. Koch, M. A. et al. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nature immunology 10, 595-602 (2009).