NLRP3 inflammasome activation is associated with proliferative diabetic retinopathy

Acta Ophthalmologica

Volumn 95, Issue 8, 2017, Pages 803-808

  Loukovaara, Sirpa ^a   Piippo, Niina ^b   Kinnunen, Kati ^c   Hytti, Maria ^b   Kaarniranta, Kai ^b,c   Kauppinen, Anu ^b  

^a HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

diabetic retinopathy; IL 18; inflammasome; inflammation; NLRP3; vitrectomy

Indexed keywords

CRYOPYRIN; FREE RADICAL; GAMMA INTERFERON; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; OXIDIZED LOW DENSITY LIPOPROTEIN; TUMOR NECROSIS FACTOR; VASCULOTROPIN; NLRP3 PROTEIN, HUMAN;

ACUTE PHASE RESPONSE; ADAPTIVE IMMUNITY; ADULT; APOPTOSIS ASSAY; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC PATIENT; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN TISSUE; MALE; MIDDLE AGED; PATHOGENESIS; PRIORITY JOURNAL; PROLIFERATIVE DIABETIC RETINOPATHY; RETINA DETACHMENT; VITREOUS BODY; WESTERN BLOTTING; APOPTOSIS; DIABETIC RETINOPATHY; FOLLOW UP; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; OPTICAL COHERENCE TOMOGRAPHY; PATHOLOGY; PROCEDURES; PROSPECTIVE STUDY; SIGNAL TRANSDUCTION;

APOPTOSIS; BLOTTING, WESTERN; DIABETIC RETINOPATHY; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FOLLOW-UP STUDIES; HUMANS; IMMUNITY, INNATE; INFLAMMASOMES; MALE; MIDDLE AGED; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; PROSPECTIVE STUDIES; SIGNAL TRANSDUCTION; TOMOGRAPHY, OPTICAL COHERENCE; VITREOUS BODY;

EID: 85014619076     PISSN: 1755375X     EISSN: 17553768     Source Type: Journal    
DOI: 10.1111/aos.13427     Document Type: Article

References (44)

1. Brownlee M, Cerami A & Vlassara H (1988): Advanced glycosylation end products in tissue and the bio-chemical basis of diabetic complications. N Engl J Med 318: 1315–1321.
2. Codolo G, Plotegher N, Pozzobon T, Brucale M, Tessari I, Bubacco L & de Bernard M (2013): Triggering of inflammasome by aggregated alpha-synuclein, an inflammatory response in synucleinopathies. PLoS One 8: e55375.
3. Devi TS, Lee I, Hutteman M, Kumar A, Nantwi KD & Singh LP (2012): TXNIP links innate host defense mechanisms to oxidative stress and inflammation in retinal Müller glia under chronic hyperglycemia: implications for diabetic retinopathy. Exp Diabetes Res 2012: 438238.
4. Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT & Tschopp J (2008): Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Scienc 320: 674–677.
5. Doyle SL, Campbell M, Ozaki E et al. (2012): NLRP3 has a protective role in age-related macular degeneration through the induction of IL-18 by drusen components. Nat Med 18: 791–798.
6. Feldmeyer L, Keller M, Niklaus G, Hohl D, Werner S & Beer HD (2007): The inflammasome mediates UVB-induced activation and secretion of interleukin-1beta by keratinocytes. Curr Biol 17: 1140–1145.
7. Friedlander M (2007): Fibrosis and diseases of the eye. J Clin Invest 117: 576–586.
8. Gombault A, Baron L & Couillin I (2013): ATP release and purinergic signaling in NLRP3 inflammasome activation. Front Immunol 3: 414.
9. Heneka MT, Kummer MP, Stutz A et al. (2013): NLRP3 is activated in Alzheimer's disease and contributes to pathology in APP/PS1 mice. Nature 493: 674–678.
10. Hiramoto K, Kobayashi H, Yamate Y, Ishii M & Sato EF (2012): Intercellular pathway through hyaluronic acid in UVB-induced inflammation. Exp Dermatol 21: 911–914.
11. Kauppinen A, Niskanen H, Suuronen T, Kinnunen K, Salminen A & Kaarniranta K (2012): Oxidative stress activates NLRP3 inflammasomes in ARPE-19 cells-Implications for age-related macular degeneration (AMD). Immunol Lett 147: 29–33.
12. Kowluru RA & Chan PS (2007): Oxidative stress and diabetic retinopathy. Exp Diabetes Res 88: 43603.
13. Loukovaara S, Lehti K, Robciuc A et al. (2013): Ang-2 upregulation correlates with increased levels of MMP-9, VEGF, EPO and TGF β1 in vitrectomized diabetic eyes. Acta Ophthalmol Scand 91: 531–539.
14. Loukovaara S, Koivunen P, Inglés M, Escobar J, Vento M & Andersson S (2014): Elevated protein carbonyl and HIF-1α levels in eyes with proliferative diabetic retinopathy. Acta Ophthalmol 92: 323–327.
15. Loukovaara S, Sahanne S, Jalkanen S & Yegutkin GG (2015a): Increased intravitreal adenosine 5′-triphosphate, adenosine 5′-diphosphate and adenosine 5′-monophosphate levels in patients with proliferative diabetic retinopathy. Acta Ophthalmol 93: 67–73.
16. Loukovaara S, Gucciardo E, Repo P, Vihinen H, Lohi J, Jokitalo E, Salven P & Lehti K (2015b): Indications of lymphatic endothelial differentiation and endothelial progenitor cell activation in the pathology of proliferative diabetic retinopathy. Acta Ophthalmol 93: 512–523.
17. Loukovaara S, Nurkkala H, Tamene F, Gucciardo E, Liu X, Repo P, Lehti K & Varjosalo M (2015c): Quantitative proteomics analysis of vitreous humor from diabetic retinopathy patients. J Proteome Res 14: 5131–5143.
18. Loukovaara S, Sandholm J, Aalto K, Liukkonen J, Jalkanen S & Yegutkin G (2016): Deregulation of ocular nucleotide homeostasis in patients with diabetic retinopathy. J Mol Med (Berl) 95: 193–204.
19. Mariathasan S, Newton K, Monack DM et al. (2004): Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430: 213–218.
20. Martinon F & Tschopp J (2004): Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 117: 561–574.
21. Martinon F, Burns K & Tschopp J (2002): The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10: 417–426.
22. Martinon F, Petrilli V, Mayor A, Tardivel A & Tschopp J (2006): Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440: 237–241.
23. Martinon F, Mayor A & Tchopp J (2009): The inflammasomes: guardians of the body. Annu Rev Immunol 27: 229–265.
24. Medzhitov R (2008): Origin and physiological roles of inflammation. Natur 454: 428–435.
25. Menu P & Vince JE (2011): The NLPR3 inflammasome in health and disease: the good, the bad and the ugly. Clinic Exp Immunol 166: 1–15.
26. O'Connor W Jr, Harton JA, Zhu X, Linhoff MW & Ting JPY (2003): Cutting edge: CIAS1/Cryopyrin/PYPAF1/NALP3/CATERPILLER 1.1 is an inducible inflammatory mediator with nf-kappab suppressive properties. J Immunol 171: 6329–6333.
27. Piippo N, Korkmaz A, Hytti M, Kinnunen K, Salminen A, Atalay M, Kaarniranta K & Kauppinen A (2014): Decline in cellular clearance systems induces inflammasome signaling in human ARPE-19 cells. Biochim Biophys Acta 1843: 3038–3046.
28. Qi Y, Zhao M, Bai Y, Huang L, Yu W, Bian Z, Zhao M & Li X (2014): Retinal ischemia/reperfusion injury is mediated by Toll-like receptor 4 activation of NLRP3 inflammasomes. Invest Ophthalmol Vis Sci 55: 5466–5475.
29. Robert S, Gicquel T, Victoni T, Valença S, Barreto E, Bailly-Maître B, Boichot E & Lagente V (2016): Involvement of matrix metalloproteinases (MMPs) and inflammasome pathway in molecular mechanisms of fibrosis. Biosci Rep 36: pii: e00360.
30. Schroder K & Tschopp J (2010): The inflammasomes. Cell 140: 821–832.
31. Schroder K, Zhou R & Tschopp J (2010): The NLRP3 inflammasome: a sensor for metabolic danger? Science 327: 296–300.
32. Schröder S, Palinski W & Schmid-Schönbein GW (1991): Activated monocytes and granulocytes, capillary non-perfusion, and neovascularization in diabetic retinopathy. Am J Pathol 139: 81–100.
33. Song Z, Sun M, Zhou F, Huang F, Qu J & Chen D (2014): Increased intravitreous interleukin-18 correlated to vascular endothelial growth factor in patients with active proliferative diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 252: 1229–1234.
34. Stienstra R, Joosten LA, Koenen T et al. (2010): The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metab 12: 593–605.
35. Stitt AW, Curtis TM, Chen M et al. (2016): The progress in understanding and treatment of diabetic retinopathy. Prog Retin Eye Res 51: 156–186.
36. Tarallo V, Hirano Y, Gelfand BD et al. (2012): DICER1 loss and Alu RNA induce age-related macular degeneration via the NLRP3 inflammasome and MyD88. Cell 149: 847–859.
37. Watanabe H, Gaide O, Petrilli V et al. (2007): Activation of the IL-1beta-processing inflammasome is involved in contact hypersensitivity. J Invest Dermatol 127: 1956–1963.
38. Wolff SP & Dean RT (1987): Glucose autoxidation and protein modification. The potential role of “autoxidative glycosylation” in diabetes. Biochem J 245: 243–250.
39. Xu H, Chen M & Forrester JV (2009): Para-inflammation in the aging retina. Prog Retin Eye Res 28: 348–368.
40. Xu Y, Cheng Q, Yang B, Yu S, Xu F, Lu L & Liang X (2015): Increased sCD200 levels in vitreous of patients with proliferative diabetic retinopathy and its correlation with VEGF and proinflammatory cytokines. Invest Ophthalmol Vis Sci 56: 6565–6572.
41. Yazdi AS, Guarda G, Riteau N, Drexler SK, Tardivel A, Couillin I & Tschopp J (2010): Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1alpha and IL-1beta. Proc Natl Acad Sci USA 107: 19449–19454.
42. Yoshimura T, Sonoda KH, Sugahara M et al. (2009): Comprehensive analysis of inflammatory immune mediators in vitreoretinal diseases. PLoS One 4: e8158.
43. Zhou J, Wang S & Xia X (2012): Role of intravitreal inflammatory cytokines and angiogenic factors in proliferative diabetic retinopathy. Curr Eye Res 37: 416–420.
44. Zhou R, Yazdi AS, Menu P & Tschopp J (2011): A role for mitochondria in NLPR3 inflammasome activation. Nature 469: 221–226.