Citrullination of proteins: A common post-translational modification pathway induced by different nanoparticles in vitro and in vivo

Nanomedicine

Volumn 7, Issue 8, 2012, Pages 1181-1195

  Mohamed, Bashir M ^a   Verma, Navin K ^a   Davies, Anthony M ^a   McGowan, Aoife ^a   Crosbie Staunton, Kieran ^a   Prina Mello, Adriele ^a   Kelleher, Dermot ^a   Botting, Catherine H ^b   Causey, Corey P ^c   Thompson, Paul R ^c,d   Pruijn, Ger J M ^e   Kisin, Elena R ^f   Tkach, Alexey V ^f   Shvedova, Anna A ^a,f,g   Volkov, Yuri ^a,f  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^f NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

^g WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

autoimmunity; high content analysis; immune system; inflammation; nanomaterial; nanoparticle; peptidylargininedeiminase; post translational modification; protein citrullination; rheumatoid arthritis

Indexed keywords

CALCIUM; CITRULLINE; CYTOKERATIN 18; CYTOKERATIN 7; CYTOKERATIN 8; NANOPARTICLE; PLECTIN; PROTEIN ARGININE DEIMINASE; SILICON DIOXIDE; SINGLE WALLED NANOTUBE; VERAPAMIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNE SYSTEM; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CITRULLINATION; PROTEIN PROCESSING; PROTEIN TARGETING; RHEUMATOID ARTHRITIS;

ANIMALS; CALCIUM; CARBON; CELL LINE; CITRULLINE; FEMALE; HUMANS; HYDROLASES; LUNG; MICE; MICE, INBRED C57BL; NANOSTRUCTURES; NANOTUBES, CARBON; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; SILICON DIOXIDE; SOOT;

EID: 84867874704     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.11.177     Document Type: Article

References (71)

1. André N. Air pollution-related illness: effects of particles. Science. 308, 804-806 (2005).
2. Sun Q, Hong X, Wold LE. Cardiovascular effects of ambient particulate air pollution exposure. Circulation 121, 2755-2765 (2010).
3. Gilmour PS, Ziesenis A, Morrison ER et al. Pulmonary and systemic effects of short-term inhalation exposure to ultrafine carbon black particles. Toxicol. Appl. Pharmacol. 195, 35-44 (2004). (Pubitemid 38177497)
4. Williams PR, Phelka AD, Paustenbach DJ. A review of historical exposures to asbestos among skilled craftsmen (1940-2006). J. Toxicol. Environ. Health B Crit. Rev. 10, 319-377 (2007). (Pubitemid 47237776)
5. El-Ansary A, Al-Daihan S. On the toxicity of therapeutically used nanoparticles: an overview. J. Toxicol. 2009, 754810 (2009).
6. Shvedova AA, Kisin E, Murray AR et al. Inhalation vs aspiration of single-walled carbon nanotubes in C57BL/6 mice: inflammation, fibrosis, oxidative stress, and mutagenesis. Am. J. Physiol. Lung Cell Mol. Physiol. 295, L552-L565 (2008).
7. Ryman-Rasmussen JP, Cesta MF, Brody AR et al. Inhaled carbon nanotubes reach the subpleural tissue in mice. Nat. Nanotechnol. 4, 747-751 (2009).
8. Schwartz J. Harvesting and long term exposure effects in the relation between air pollution and mortality. Am. J. Epidemiol. 151, 440-448, (2000). (Pubitemid 30471017)
9. Farhat SC, Silva CA, Orione MA et al. Air pollution in autoimmune rheumatic diseases: a review. Autoimmun. Rev. 11, 14-21, (2011).
10. Stolt P, Kallberg H, Lundberg I et al. Silica exposure is associated with increased risk of developing rheumatoid arthritis: results from the Swedish EIRA study. Ann. Rheum. Dis. 64, 582-586 (2005). (Pubitemid 40469088)
11. Stolt P, Bengtsson C, Nordmark B et al. Quantification of the influence of cigarette smoking on rheumatoid arthritis: results from a population based case-control study, using incident cases. Ann. Rheum. Dis. 62, 835-841 (2003). (Pubitemid 37026493)
12. Klareskog L, Stolt P, Lundberg K et al. A new model for an etiology of rheumatoid arthritis: smoking may trigger HLA-DR (shared epitope)-restricted immune reactions to autoantigens modified by citrullination. Arthritis Rheum. 54, 38-46 (2006). (Pubitemid 43122184)
13. Lukens JR, Dixit VD, Kanneganti TD. Inflammasome activation in obesity-related inflammatory diseases and autoimmunity. Discov. Med. 12, 65-74 (2011).
14. Hart JE, Laden F, Puett RC, Costenbader KH, Karlson EW. Exposure to traffic pollution and increased risk of rheumatoid arthritis. Environ. Health Perspect. 117, 1065-1069 (2009).
15. Wottrich R, Diabaté S, Krug HF.Biological effects of ultrafine model particles in human macrophages and epithelial cells in mono-and co-culture. Int. J. Hyg. Environ. Health 207, 353-361 (2004). (Pubitemid 39222729)
16. Choi SJ, Oh JM, Choy JH. Toxicological effects of inorganic nanoparticles on human lung cancer A549 cells. J. Inorg.Biochem. 103, 463-471 (2009).
17. Eom HJ, Choi J. Oxidative stress of silica nanoparticles in human bronchial epithelial cell, Beas-2B. Toxicol. In Vitro 23, 1326-1332 (2009).
18. Chen M, von Mikecz A. Formation of nucleoplasmic protein aggregates impairs nuclear function in response to SiO2 nanoparticles. Exp. Cell. Res. 305, 51-62 (2005). (Pubitemid 40380653)
19. Konduru NV, Tyurina YY, Feng W et al. Phosphatidylserine targets single-walled carbon nanotubes to professional phagocytes in vitro and in vivo. PLoS ONE 4, e4398 (2009).
20. Kurien BT, Hensley K, Bachmann M, Scofield RH. Oxidatively modified autoantigens in autoimmune diseases. Free Radic. Biol. Med. 41, 549-556 (2006). (Pubitemid 44080517)
21. Vossenaar ER, Robinson WH. Citrullination and autoimmune disease: 8th Bertine Koperberg meeting. Ann. Rheum. Dis. 64, 1513-1515 (2005). (Pubitemid 41623869)
22. Gyorgy B, Toth E, Tarcsa E, Falus A, Buzas EI. Citrullination: a posttranslational modification in health and disease. Int. J. Biochem. Cell Biol. 38, 1662-1677 (2006). (Pubitemid 43947646)
23. Nishimura K, Sugiyama D, Kogata Y et al. Meta-analysis: diagnostic accuracy of anti-cyclic citrullinated peptide antibody and rheumatoid factor for rheumatoid arthritis. Ann. Intern. Med. 146, 797-808 (2007). (Pubitemid 351650500)
24. Klareskog L, Ronnelid J, Lundberg K, Padyukov L, Alfredsson L. Immunity to citrullinated proteins in rheumatoid arthritis. Annu. Rev. Immunol. 26, 651-675 (2008). (Pubitemid 351600388)
25. Lundberg K, Nijenhuis S, Vossenaar ER et al. Citrullinated proteins have increased immunogenicity and arthritogenicity and their presence in arthritic joints correlates with disease severity. Arthritis Res. Ther. 7, R458-R467 (2005).
26. Vossenaar ER, Radstake TR, van der Heijden A et al. Expression and activity of citrullinating peptidylarginine deiminase enzymes in monocytes and macrophages. Ann. Rheum. Dis. 63, 373-381 (2004). (Pubitemid 38453302)
27. Vossenaar ER, Zendman AJ, Van Venrooij WJ, Pruijn GJ. PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease. Bioessays 25, 1106-1118 (2003). (Pubitemid 37411770)
28. Foulquier C, Sebbag M, Clavel C et al. Peptidyl arginine deiminase type 2 (PAD-2) and PAD-4 but not PAD-1, PAD-3, and PAD-6 are expressed in rheumatoid arthritis synovium in close association with tissue inflammation. Arthritis Rheum. 56, 3541-3553 (2007). (Pubitemid 350100687)
29. Willis VC, Gizinski AM, Banda NK et al. N-a-benzoyl-N5-(2-chloro-1- iminoethyl)-l-ornithine amide, a protein arginine deiminase inhibitor, reduces the severity of murine collagen-induced arthritis. J. Immunol. 186, 4396-4404 (2011).
30. Wang Y, Li M, Stadler Set al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J. Cell Biol. 184, 205-213 (2009).
31. Struyf S, Noppen S, Loos T et al. Citrullination of CXCL12 differentially reduces CXCR4 and CXCR7 binding with loss of inflammatory and anti-HIV-1 activity via CXCR4. J. Immunol. 182, 666-674 (2009).
32. Proost P, Loos T, Mortier A et al. Citrullination of CXCL8 by peptidylargininedeiminase alters receptor usage, prevents proteolysis, and dampens tissue inflammation. J. Exp. Med. 205, 2085-2097 (2008).
33. Loos T, Mortier A, Gouwy M et al. Citrullination of CXCL10 and CXCL11 by peptidylargininedeiminase: a naturally occurring posttranslational modification of chemokines and new dimension of immunoregulation. Blood 112, 2648-2656 (2008).
34. Barnes CA, Elsaesser A, Arkusz J et al. Reproducible comet assay of amorphous silica nanoparticles detects no genotoxicity. Nano Lett. 8, 3069-3074 (2008).
35. Shvedova AA, Fabisiak JP, Kisin ER et al. Sequential exposure to carbon nanotubes and bacteria enhances pulmonary inflammation and infectivity. Am. J. Respir. Cell Mol. Biol. 38, 579-590 (2008). (Pubitemid 351758677)
36. Causey CP, Thompson PR An improved synthesis of haloaceteamidine-based inactivators of protein arginine deiminase 4 (PAD4). Tetrahedron Lett. 49, 4383-4385 (2008).
37. Williams Y, Byrne S, Bashir M et al. Comparison of three cell fixation methods for high content analysis assays utilizing quantum dots. J. Microsc. 232, 91-98 (2008).
38. Mercer RR, Scabilloni J, Wang L et al. Alteration of deposition pattern and pulmonary response as a result of improved dispersion of aspirated single-walled carbon nanotubes in a mouse model. Am. J. Physiol. Lung Cell Mol. Physiol. 294, L87-L97 (2008). (Pubitemid 351380321)
39. Mohamed BM, Feighery C, Kelly J et al. Increased protein expression of matrix metalloproteinases -1, -3, and -9 and TIMP-1 in patients with gluten-sensitive enteropathy. Dig. Dis. Sci. 51, 1862-1868 (2006).
40. Pham NA, Morrison A, Schwock J et al. Quantitative image analysis of immunohistochemical stains using a CMYK color model. Diagn. Pathol. 2, 8 (2007).
41. Verma NK, Dourlat J, Davies AM et al. STAT3-stathmin interactions control microtubule dynamics in migrating T-cells. J. Biol. Chem. 284, 12349-12362 (2009).
42. Verma NK, Dempsey E, Conroy J et al. A new microtubule-targeting compound PBOX-15 inhibits T-cell migration via post-translational modifications of tubulin. J. Mol. Med. 86, 457-469 (2008).
43. Verma NK, Dempsey E, Freeley M et al. Analysis of dynamic tyrosine phosphoproteome in LFA-1 triggered migrating T-cells. J. Cell. Physiol. 226, 1489-1498 (2011).
44. Kozak K, Bakos G, Hoff A et al. Workflow-based software environment for large-scale biological experiments. J. Biomol. Screen. 15, 892-899 (2010).
45. Freeley M, Bakos G, Davies A, Kelleher D, Long A, Dunican D. A high-content analysis toolbox permits dissection of diverse signaling pathways for T lymphocyte polarization. J. Biomol. Screen. 15, 541-555 (2010).
46. Mohamed BM, Verma NK, Prina-Mello A et al. Activation of stress-related signalling pathway in human cells upon SiO2 nanoparticles exposure as an early indicator of cytotoxicity. J. Nanobiotechnology 9, 29(2011).
47. Birmingham A, Selfors LM, Forster T et al. Statistical methods for analysis of high-throughput RNA interference screens. Nat. Methods 6, 569-575 (2009).
48. Knuckley B, Causey CP, Pellechia PJ, Cook PF, Thompson PR. Haloacetamidine-based inactivators of protein arginine deiminase 4 (PAD4): evidence that general acid catalysis promotes efficient inactivation. Chembiochem. 11, 161-165 (2010).
49. Knuckley B, Causey CP, Jones JE et al. Substrate specificity and kinetic studies of PADs 1, 3, and 4 identify potent and selective inhibitors of protein arginine deiminase 3. Biochemistry 49, 4852-4863 (2010).
50. Luo Y, Arita K, Bhatia M et al. Inhibitors and inactivators of protein arginine deiminase 4: functional and structural characterization. Biochemistry 45, 11727-11736 (2006). (Pubitemid 44497800)
51. Li P, Yao H, Zhang Z et al. Regulation of p53 target gene expression by peptidylargininedeiminase 4. Mol. Cell. Biol. 28, 4745-4758 (2008).
52. Kearney PL, Bhatia M, Jones NG et al. Kinetic characterization of protein arginine deiminase 4: a transcriptional corepressor implicated in the onset and progression of rheumatoid arthritis. Biochemistry 44, 10570-10582 (2005). (Pubitemid 41098234)
53. Snir O, Widhe M, Hermansson M et al. Antibodies to several citrullinated antigens are enriched in the joints of rheumatoid arthritis patients. Arthritis Rheum. 62, 44-52 (2010).
54. Hill JA, Southwood S, Sette A et al. The conversion of arginine to citrulline allows for a high-affinity peptide interaction with the rheumatoid arthritis-associated HLA-DRB1.*0401 MHC class II molecule. J. Immunol. 171, 538-541 (2003). (Pubitemid 36871358)
55. Coulombe PA, Omary MB. 'Hard' and 'soft' principles defining the structure, function and regulation of keratin intermediate filaments. Curr. Opin. Cell. Biol. 14, 110-122 (2002). (Pubitemid 34131664)
56. Alix-Panabieres C, Vendrell JP, Slijper M et al. Full-length cytokeratin-19 is released by human tumor cells: a potential role in metastatic progression of breast cancer. Breast Cancer Res. 11, R39 (2009).
57. Wiche G. Role of plectin in cytoskeleton organization and dynamics. J. Cell Sci. 111, 2477-2486 (1998). (Pubitemid 28474951)
58. Asaga H, Yamada M, Senshu T. Selective deimination of vimentin in calcium ionophore-induced apoptosis of mouse peritoneal macrophages. Biochem. Biophys. Res. Commun. 243, 641-646 (1998). (Pubitemid 28414131)
59. Wang Z, Nicholls SJ, Rodriguez ER et al. Protein carbamylation links inflammation, smoking, uremia and atherogenesis. Nat. Med. 13, 1176-1184 (2007). (Pubitemid 47530630)
60. Mydel P, Wang Z, Brisslert Met al. Carbamylation-dependent activation of T cells: a novel mechanism in the pathogenesis of autoimmune arthritis. J. Immunol. 184, 6882-6890 (2010).
61. Schreier SM, Steinkellner H, Jirovetz L et al. S-carbamoylation impairs the oxidant scavenging activity of cysteine: its possible impact on increased LDL modification in uraemia. Biochimie. 93, 772-777 (2011).
62. Shvedova AA, Kisin ER, Mercer R et al. Unusual inflammatory and fibrogenic pulmonary responses to single walled carbon nanotubes in mice. Am. J. Physiol. Lung Cell Mol. Physiol. 289, 698-708 (2005).
63. Tkach AV, Shurin GV, Shurin MR et al. Direct effects of carbon nanotubes on dendritic cells induce immune suppression upon pulmonary exposure. ACS Nano. 26, 5755-5762 (2011).
64. Yoshino S, Sagai M. Enhancement of collagen-induced arthritis in mice by diesel exhaust particles. J. Pharmacol. Exp. Ther. 290, 524-529 (1999). (Pubitemid 29344542)
65. Yoshino S, Hayashi H, Taneda S, Sagai M, Mori Y. Effect of diesel exhaust particle extracts on collagen-induced arthritis in mice. Autoimmunity 35, 57-61 (2002). (Pubitemid 34678722)
66. Makrygiannakis D, Hermansson M, Ulfgren AK et al. Smoking increases peptidylargininedeiminase 2 enzyme expression in human lungs and increases citrullination in BAL cells. Ann. Rheum. Dis. 67, 1488-1492 (2008).
67. Madl AK, Pinkerton KE. Health effects of inhaled engineered and incidental nanoparticles. Crit. Rev. Toxicol. 39, 629-658 (2009).
68. Chen EYT, Garnica M, Wang Y-C, Chen C-S, Chin W-C. Mucin secretion induced by titanium dioxide nanoparticles. PLoS ONE 6, e16198 (2011).
69. Stone V, Tuinman M, Vamvakopoulos JE et al. Increased calcium influx in a monocytic cell line on exposure to ultrafine carbon black. Eur. Respir. J. 15, 297-303 (2000). (Pubitemid 30085956)
70. Chen J, Hessler JA, Putchakayala K et al. Cationic nanoparticles induce nanoscale disruption in living cell plasma membranes. J. Phys. Chem. B. 113, 11179-11185 (2009).
71. Ireland J, Herzog J, Unanue ER. Cutting edge: unique T cells that recognize citrullinated peptides are a feature of protein immunization. J. Immunol. 177, 1421-1425 (2006). (Pubitemid 44092474)