Juvenile idiopathic arthritis and physical activity: Possible inflammatory and immune modulation and tracks for interventions in young populations

Autoimmunity Reviews

Volumn 14, Issue 8, 2015, Pages 726-734

  Rochette, Emmanuelle ^a,b,c   Duché, Pascale ^c   Merlin, Etienne ^a,b  

^a UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

^b INSERM   (France)

^c CLERMONT AUVERGNE UNIVERSITY   (France)

Author keywords

Calprotectin; Interleukin; Juvenile idiopathic arthritis; miRNA; Physical exercise; Pro anti inflammatory balance

Indexed keywords

CALGRANULIN; HYDROCORTISONE; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 6; MELATONIN; MICRORNA; CYTOKINES; MICRORNAS;

APOPTOSIS; CELL MIGRATION; CYTOKINE RESPONSE; EXERCISE; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; JUVENILE RHEUMATOID ARTHRITIS; NONHUMAN; PHYSICAL ACTIVITY; PILOT STUDY; QUALITY OF LIFE; RANGE OF MOTION; REVIEW; TH17 CELL; ADOLESCENT; ANIMALS; ARTHRITIS, JUVENILE; CELL MOVEMENT; GENETICS; HUMANS; IMMUNOLOGY;

ADOLESCENT; ANIMALS; ARTHRITIS, JUVENILE; CELL MOVEMENT; CYTOKINES; EXERCISE; HUMANS; MICRORNAS; QUALITY OF LIFE;

EID: 84930937148     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2015.04.007     Document Type: Review

References (122)

1. Long A.R., Rouster-Stevens K.A. The role of exercise therapy in the management of juvenile idiopathic arthritis. Curr Opin Rheumatol 2010, 22:213-217. 10.1097/BOR.0b013e328335d1a2.
2. Macaubas C., Nguyen K., Milojevic D., Park J.L., Mellins E.D. Oligoarticular and polyarticular JIA: epidemiology and pathogenesis. Nat Rev Rheumatol 2009, 5:616-626. 10.1038/nrrheum.2009.209.
3. Lotito A.P.N., Campa A., Silva C.A.A., Kiss M.H.B., Mello S.B.V. Interleukin 18 as a marker of disease activity and severity in patients with juvenile idiopathic arthritis. J Rheumatol 2007, 34:823-830.
4. Lin Y.-T., Wang C.-T., Gershwin M.E., Chiang B.-L. The pathogenesis of oligoarticular/polyarticular vs systemic juvenile idiopathic arthritis. Autoimmun Rev 2011, 10:482-489. 10.1016/j.autrev.2011.02.001.
5. Sandstedt E., Fasth A., Eek M.N., Beckung E. Muscle strength, physical fitness and well-being in children and adolescents with juvenile idiopathic arthritis and the effect of an exercise programme: a randomized controlled trial. Pediatr Rheumatol Online J 2013, 11:7. 10.1186/1546-0096-11-7.
6. Bilginer Y., Topaloglu R., Alikasifoglu A., Kara N., Besbas N., Ozen S., et al. Low cortisol levels in active juvenile idiopathic arthritis. Clin Rheumatol 2010, 29:309-314. 10.1007/s10067-009-1326-5.
7. Straub R.H., Cutolo M., Buttgereit F., Pongratz G. Energy regulation and neuroendocrine-immune control in chronic inflammatory diseases. J Intern Med 2010, 267:543-560. 10.1111/j.1365-2796.2010.02218.x.
8. Gualano B., Sá Pinto A.L., Perondi B., Leite Prado D.M., Omori C., Almeida R.T., et al. Evidence for prescribing exercise as treatment in pediatric rheumatic diseases. Autoimmun Rev 2010, 9:569-573. 10.1016/j.autrev.2010.04.001.
9. Gueddari S., Amine B., Rostom S., Badri D., Mawani N., Ezzahri M., et al. Physical activity, functional ability, and disease activity in children and adolescents with juvenile idiopathic arthritis. Clin Rheumatol 2014, 10.1007/s10067-014-2576-4.
10. Hills A.P., King N.A., Armstrong T.P. The contribution of physical activity and sedentary behaviours to the growth and development of children and adolescents: implications for overweight and obesity. Sports Med 2007, 37:533-545.
11. Hallal P.C., Victora C.G., Azevedo M.R., Wells J.C.K. Adolescent physical activity and health: a systematic review. Sports Med 2006, 36:1019-1030.
12. Mathur N., Pedersen B.K. Exercise as a mean to control low-grade systemic inflammation. Mediators Inflamm 2008, 2008:109502. 10.1155/2008/109502.
13. De Salles Painelli V., Gualano B., Artioli G.G., de Sá Pinto A.L., Bonfá E., Lancha Junior A.H., et al. The possible role of physical exercise on the treatment of idiopathic inflammatory myopathies. Autoimmun Rev 2009, 8:355-359. 10.1016/j.autrev.2008.11.008.
14. Ploeger H.E., Takken T., de Greef M.H.G., Timmons B.W. The effects of acute and chronic exercise on inflammatory markers in children and adults with a chronic inflammatory disease: a systematic review. Exerc Immunol Rev 2009, 15:6-41.
15. Takken T., van der Net J., Helders P.J. Do juvenile idiopathic arthritis patients benefit from an exercise program? A pilot study. Arthritis Rheum 2001, 45:81-85. 10.1002/1529-0131(200102)45:1<81::AID-ANR88>3.0.CO;2-I.
16. Lelieveld O.T.H.M., van Brussel M., Takken T., van Weert E., van Leeuwen M.A., Armbrust W. Aerobic and anaerobic exercise capacity in adolescents with juvenile idiopathic arthritis. Arthritis Rheum 2007, 57:898-904. 10.1002/art.22897.
17. Van Brussel M., Lelieveld O.T.H.M., van der Net J., Engelbert R.H.H., Helders P.J.M., Takken T. Aerobic and anaerobic exercise capacity in children with juvenile idiopathic arthritis. Arthritis Rheum 2007, 57:891-897. 10.1002/art.22893.
18. Van Pelt P.A., Takken T., van Brussel M., de Witte I., Kruize A.A., Wulffraat N.M. Aerobic capacity and disease activity in children, adolescents and young adults with juvenile idiopathic arthritis (JIA). Pediatr Rheumatol Online J 2012, 10:27. 10.1186/1546-0096-10-27.
19. Hulsegge G., Henschke N., McKay D., Chaitow J., West K., Broderick C., et al. Fundamental movement skills, physical fitness and physical activity among Australian children with juvenile idiopathic arthritis. J Paediatr Child Health 2014, 10.1111/jpc.12733.
20. Gualano B., Pinto AL de S., Perondi M.B., Roschel H., Sallum A.M.E., Hayashi A.P.T., et al. Therapeutic effects of exercise training in patients with pediatric rheumatic diseases. Rev Bras Reumatol 2011, 51:490-496.
21. Doğru Apti Mine, Kasap opur Özgür, Mengi Murat, Özturk Gülnur, Metin G khan, et al. Regular aerobic training combined with range of motion exercises in juvenile idiopathic arthritis. BioMed Res Int 2014, 10.1155/2014/748972.
22. Perandini L.A., de Sá-Pinto A.L., Roschel H., Benatti F.B., Lima F.R., Bonfá E., et al. Exercise as a therapeutic tool to counteract inflammation and clinical symptoms in autoimmune rheumatic diseases. Autoimmun Rev 2012, 12:218-224. 10.1016/j.autrev.2012.06.007.
23. Cavallo S., April K.T., Grandpierre V., Majnemer A., Feldman D.E. Leisure in children and adolescents with juvenile idiopathic arthritis: a systematic review. PLoS One 2014, 9:e104642. 10.1371/journal.pone.0104642.
24. Limenis E., Grosbein H.A., Feldman B.M. The relationship between physical activity levels and pain in children with juvenile idiopathic arthritis. J Rheumatol 2014, 41:345-351. 10.3899/jrheum.130734.
25. Brabnikova Maresova K., Jarosova K., Pavelka K., Stepan J.J. The association between lean mass and bone mineral content in the high disease activity group of adult patients with juvenile idiopathic arthritis. BMC Musculoskelet Disord 2014, 15:51. 10.1186/1471-2474-15-51.
26. Bechtold S., Roth J. Natural history of growth and body composition in juvenile idiopathic arthritis. Horm Res 2009, 72(Suppl. 1):13-19. 10.1159/000229758.
27. Van Oort C., Tupper S.M., Rosenberg A.M., Farthing J.P., Baxter-Jones A.D. Safety and feasibility of a home-based six week resistance training program in juvenile idiopathic arthritis. Pediatr Rheumatol Online J 2013, 11:46. 10.1186/1546-0096-11-46.
28. Mendonça T.M., Terreri M.T., Silva C.H., Neto M.B., Pinto R.M., Natour J., et al. Effects of Pilates exercises on health-related quality of life in individuals with juvenile idiopathic arthritis. Arch Phys Med Rehabil 2013, 94:2093-2102. 10.1016/j.apmr.2013.05.026.
29. Tarakci E., Yeldan I., Baydogan S.N., Olgar S., Kasapcopur O. Efficacy of a land-based home exercise programme for patients with juvenile idiopathic arthritis: a randomized, controlled, single-blind study. J Rehabil Med 2012, 44:962-967. 10.2340/16501977-1051.
30. Sandstedt E., Fasth A., Fors H., Beckung E. Bone health in children and adolescents with juvenile idiopathic arthritis and the influence of short-term physical exercise. Pediatr Phys Ther 2012, 24:155-161. [discussion 162]. 10.1097/PEP.0b013e31824cce6e.
31. Singh-Grewal D., Schneiderman-Walker J., Wright V., Bar-Or O., Beyene J., Selvadurai H., et al. The effects of vigorous exercise training on physical function in children with arthritis: a randomized, controlled, single-blinded trial. Arthritis Rheum 2007, 57:1202-1210. 10.1002/art.23008.
32. Singh-Grewal D., Wright V., Bar-Or O., Feldman B.M. Pilot study of fitness training and exercise testing in polyarticular childhood arthritis. Arthritis Rheum 2006, 55:364-372. 10.1002/art.21996.
33. Epps H., Ginnelly L., Utley M., Southwood T., Gallivan S., Sculpher M., et al. Is hydrotherapy cost-effective? A randomised controlled trial of combined hydrotherapy programmes compared with physiotherapy land techniques in children with juvenile idiopathic arthritis. Health Technol Assess 2005, 1-59. [iii - iv, ix - x].
34. Takken T., Van Der Net J., Kuis W., Helders P.J.M. Aquatic fitness training for children with juvenile idiopathic arthritis. Rheumatology (Oxford) 2003, 42:1408-1414. 10.1093/rheumatology/keg386.
35. Klepper S.E. Effects of an eight-week physical conditioning program on disease signs and symptoms in children with chronic arthritis. Arthritis Care Res 1999, 12:52-60.
36. Bacon M.C., Nicholson C., Binder H., White P.H. Juvenile rheumatoid arthritis. Aquatic exercise and lower-extremity function. Arthritis Care Res 1991, 4:102-105.
37. Klepper S.E. Exercise in pediatric rheumatic diseases. Curr Opin Rheumatol 2008, 20:619-624. 10.1097/BOR.0b013e32830634ee.
38. Gibbs J.E., Ray D.W. The role of the circadian clock in rheumatoid arthritis. Arthritis Res Ther 2013, 15:205. 10.1186/ar4146.
39. Cutolo M., Villaggio B., Otsa K., Aakre O., Sulli A., Seriolo B. Altered circadian rhythms in rheumatoid arthritis patients play a role in the disease's symptoms. Autoimmun Rev 2005, 4:497-502. 10.1016/j.autrev.2005.04.019.
40. Petrovsky N., Harrison L.C. The chronobiology of human cytokine production. Int Rev Immunol 1998, 16:635-649.
41. Cutolo M., Straub R.H., Buttgereit F. Circadian rhythms of nocturnal hormones in rheumatoid arthritis: translation from bench to bedside. Ann Rheum Dis 2008, 67:905-908. 10.1136/ard.2008.088955.
42. El-Awady H.M., El-Wakkad A.S.E.-D., Saleh M.T., Muhammad S.I., Ghaniema E.M. Serum melatonin in juvenile rheumatoid arthritis: correlation with disease activity. Pak J Biol Sci 2007, 10:1471-1476.
43. Escames G., Ozturk G., Baño-Otálora B., Pozo M.J., Madrid J.A., Reiter R.J., et al. Exercise and melatonin in humans: reciprocal benefits. J Pineal Res 2012, 52:1-11. 10.1111/j.1600-079X.2011.00924.x.
44. Theron J.J., Oosthuizen J.M., Rautenbach M.M. Effect of physical exercise on plasma melatonin levels in normal volunteers. S Afr Med J 1984, 66:838-841.
45. Carr D.B., Reppert S.M., Bullen B., Skrinar G., Beitins I., Arnold M., et al. Plasma melatonin increases during exercise in women. J Clin Endocrinol Metab 1981, 53:224-225. 10.1210/jcem-53-1-223.
46. Skrinar G.S., Bullen B.A., Reppert S.M., Peachey S.E., Turnbull B.A., McArthur J.W. Melatonin response to exercise training in women. J Pineal Res 1989, 7:185-194.
47. Monteleone P., Maj M., Fuschino A., Kemali D. Physical stress in the middle of the dark phase does not affect light-depressed plasma melatonin levels in humans. Neuroendocrinology 1992, 55:367-371.
48. Monteleone P., Maj M., Fusco M., Orazzo C., Kemali D. Physical exercise at night blunts the nocturnal increase of plasma melatonin levels in healthy humans. Life Sci 1990, 47:1989-1995.
49. Elias A.N., Wilson A.F., Pandian M.R., Rojas F.J., Kayaleh R., Stone S.C., et al. Melatonin and gonadotropin secretion after acute exercise in physically active males. Eur J Appl Physiol Occup Physiol 1993, 66:357-361.
50. Miyazaki T., Hashimoto S., Masubuchi S., Honma S., Honma K.I. Phase-advance shifts of human circadian pacemaker are accelerated by daytime physical exercise. Am J Physiol Regul Integr Comp Physiol 2001, 281:R197-R205.
51. Straub R.H., Cutolo M. Involvement of the hypothalamic-pituitary-adrenal/gonadal axis and the peripheral nervous system in rheumatoid arthritis: viewpoint based on a systemic pathogenetic role. Arthritis Rheum 2001, 44:493-507. 10.1002/1529-0131(200103)44:3<493::AID-ANR95>3.0.CO;2-U.
52. Cutolo M., Sulli A., Pizzorni C., Secchi M.E., Soldano S., Seriolo B., et al. Circadian rhythms. Ann N Y Acad Sci 2006, 1069:289-299. 10.1196/annals.1351.027.
53. Cutolo M., Masi A.T. Circadian rhythms and arthritis. Rheum Dis Clin North Am 2005, 31:115-129. [ix - x]. 10.1016/j.rdc.2004.09.005.
54. Picco P., Gattorno M., Sormani M.P., Vignola S., Buoncompagni A., Battilana N., et al. Involvement of the hypothalamic-pituitary-adrenal axis in children with oligoarticular-onset idiopathic arthritis. Ann N Y Acad Sci 2002, 966:369-372.
55. Benitez-Sillero J.de D., Perez-Navero J.L., Tasset I., Guillen-Del Castillo M., Gil-Campos M., Tunez I. Influence of intense exercise on saliva glutathione in prepubescent and pubescent boys. Eur J Appl Physiol 2009, 106:181-186. 10.1007/s00421-009-1004-y.
56. Budde H., Windisch C., Kudielka B.M., Voelcker-Rehage C. Saliva cortisol in school children after acute physical exercise. Neurosci Lett 2010, 483:16-19. 10.1016/j.neulet.2010.07.036.
57. Thomas N.E., Leyshon A., Hughes M.G., Jasper M.A., Davies B., Graham M.R., et al. Concentrations of salivary testosterone, cortisol, and immunoglobulin A after supra-maximal exercise in female adolescents. J Sports Sci 2010, 28:1361-1368. 10.1080/02640414.2010.510144.
58. Thomas N.E., Leyshon A., Hughes M.G., Davies B., Graham M., Baker J.S. The effect of anaerobic exercise on salivary cortisol, testosterone and immunoglobulin (A) in boys aged 15-16years. Eur J Appl Physiol 2009, 107:455-461. 10.1007/s00421-009-1146-y.
59. Budde H., Voelcker-Rehage C., Pietrassyk-Kendziorra S., Machado S., Ribeiro P., Arafat A.M. Steroid hormones in the saliva of adolescents after different exercise intensities and their influence on working memory in a school setting. Psychoneuroendocrinology 2010, 35:382-391. 10.1016/j.psyneuen.2009.07.015.
60. Antonelli A., Ferrari S.M., Giuggioli D., Ferrannini E., Ferri C., Fallahi P. Chemokine (C-X-C motif) ligand (CXCL)10 in autoimmune diseases. Autoimmun Rev 2014, 13:272-280. 10.1016/j.autrev.2013.10.010.
61. De Jager W., Hoppenreijs E.P.A.H., Wulffraat N.M., Wedderburn L.R., Kuis W., Prakken B.J. Blood and synovial fluid cytokine signatures in patients with juvenile idiopathic arthritis: a cross-sectional study. Ann Rheum Dis 2007, 66:589-598. 10.1136/ard.2006.061853.
62. Perry M.G., Richards L., Harbuz M.S., Jessop D.S., Kirwan J.R. Sequential synovial fluid sampling suggests plasma and synovial fluid IL-6 vary independently in rheumatoid arthritis. Rheumatology (Oxford) 2006, 45:229-230. 10.1093/rheumatology/kei196.
63. Flachenecker P. Autoimmune diseases and rehabilitation. Autoimmun Rev 2012, 11:219-225. 10.1016/j.autrev.2011.05.016.
64. Pedersen B.K., Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 2000, 80:1055-1081.
65. Peake J.M., Della Gatta P., Suzuki K., Nieman D.C. Cytokine expression and secretion by skeletal muscle cells: regulatory mechanisms and exercise effects. Exerc Immunol Rev 2015, 21:8-25.
66. Pedersen B.K., Steensberg A., Keller P., Keller C., Fischer C., Hiscock N., et al. Muscle-derived interleukin-6: lipolytic, anti-inflammatory and immune regulatory effects. Pflugers Arch 2003, 446:9-16. 10.1007/s00424-002-0981-z.
67. Petersen A.M.W., Pedersen B.K. The anti-inflammatory effect of exercise. J Appl Physiol 2005, 98:1154-1162. 10.1152/japplphysiol.00164.2004.
68. Suzuki K., Nakaji S., Kurakake S., Totsuka M., Sato K., Kuriyama T., et al. Exhaustive exercise and type-1/type-2 cytokine balance with special focus on interleukin-12 p40/p70. Exerc Immunol Rev 2003, 9:48-57.
69. Suzuki K., Nakaji S., Yamada M., Totsuka M., Sato K., Sugawara K. Systemic inflammatory response to exhaustive exercise. Cytokine kinetics. Exerc Immunol Rev 2002, 8:6-48.
70. Calle M.C., Fernandez M.L. Effects of resistance training on the inflammatory response. Nutr Res Pract 2010, 4:259-269. 10.4162/nrp.2010.4.4.259.
71. Benatti F.B., Pedersen B.K. Exercise as an anti-inflammatory therapy for rheumatic diseases-myokine regulation. Nat Rev Rheumatol 2015, 11:86-97. 10.1038/nrrheum.2014.193.
72. Brandt C., Pedersen B.K. The role of exercise-induced myokines in muscle homeostasis and the defense against chronic diseases. J Biomed Biotechnol 2010, 2010:520258. 10.1155/2010/520258.
73. Scheller J., Chalaris A., Schmidt-Arras D., Rose-John S. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta 1813, 2011:878-888. 10.1016/j.bbamcr.2011.01.034.
74. Saini A., Faulkner S.H., Moir H., Warwick P., King J.A., Nimmo M.A. Interleukin-6 in combination with the interleukin-6 receptor stimulates glucose uptake in resting human skeletal muscle independently of insulin action. Diabetes Obes Metab 2014, [n/a - n/a]. 10.1111/dom.12299.
75. Keller P., Penkowa M., Keller C., Steensberg A., Fischer C.P., Giralt M., et al. Interleukin-6 receptor expression in contracting human skeletal muscle: regulating role of IL-6. FASEB J 2005, 19:1181-1183. 10.1096/fj.04-3278fje.
76. Nimmo M.A., Leggate M., Viana J.L., King J.A. The effect of physical activity on mediators of inflammation. Diabetes Obes Metab 2013, 15(Suppl. 3):51-60. 10.1111/dom.12156.
77. Peake N.J., Khawaja K., Myers A., Nowell M.A., Jones S.A., Rowan A.D., et al. Interleukin-6 signalling in juvenile idiopathic arthritis is limited by proteolytically cleaved soluble interleukin-6 receptor. Rheumatology (Oxford) 2006, 45:1485-1489. 10.1093/rheumatology/kel154.
78. Leggate M., Carter W.G., Evans M.J.C., Vennard R.A., Sribala-Sundaram S., Nimmo M.A. Determination of inflammatory and prominent proteomic changes in plasma and adipose tissue after high-intensity intermittent training in overweight and obese males. J Appl Physiol 2012, 112:1353-1360. 10.1152/japplphysiol.01080.2011.
79. Robson-Ansley P., Cockburn E., Walshe I., Stevenson E., Nimmo M. The effect of exercise on plasma soluble IL-6 receptor concentration: a dichotomous response. Exerc Immunol Rev 2010, 16:56-76.
80. Fischer C.P. Interleukin-6 in acute exercise and training: what is the biological relevance?. Exerc Immunol Rev 2006, 12:6-33.
81. Pedersen B.K., Fischer C.P. Physiological roles of muscle-derived interleukin-6 in response to exercise. Curr Opin Clin Nutr Metab Care 2007, 10:265-271. 10.1097/MCO.0b013e3280ebb5b3.
82. Febbraio M.A., Pedersen B.K. Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J 2002, 16:1335-1347. 10.1096/fj.01-0876rev.
83. Keller C., Steensberg A., Hansen A.K., Fischer C.P., Plomgaard P., Pedersen B.K. Effect of exercise, training, and glycogen availability on IL-6 receptor expression in human skeletal muscle. J Appl Physiol 2005, 99:2075-2079. 10.1152/japplphysiol.00590.2005.
84. Pedersen B.K., Febbraio M.A. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 2008, 88:1379-1406. 10.1152/physrev.90100.2007.
85. Buford T.W., Cooke M.B., Willoughby D.S. Resistance exercise-induced changes of inflammatory gene expression within human skeletal muscle. Eur J Appl Physiol 2009, 107:463-471. 10.1007/s00421-009-1145-z.
86. Uchida M.C., Nosaka K., Ugrinowitsch C., Yamashita A., Martins E., Moriscot A.S., et al. Effect of bench press exercise intensity on muscle soreness and inflammatory mediators. J Sports Sci 2009, 27:499-507. 10.1080/02640410802632144.
87. Phillips M.D., Mitchell J.B., Currie-Elolf L.M., Yellott R.C., Hubing K.A. Influence of commonly employed resistance exercise protocols on circulating IL-6 and indices of insulin sensitivity. J Strength Cond Res 2010, 24:1091-1101. 10.1519/JSC.0b013e3181cc2212.
88. Peake J.M., Nosaka K., Muthalib M., Suzuki K. Systemic inflammatory responses to maximal versus submaximal lengthening contractions of the elbow flexors. Exerc Immunol Rev 2006, 12:72-85.
89. Hirose L., Nosaka K., Newton M., Laveder A., Kano M., Peake J., et al. Changes in inflammatory mediators following eccentric exercise of the elbow flexors. Exerc Immunol Rev 2004, 10:75-90.
90. MacIntyre D.L., Sorichter S., Mair J., Berg A., McKenzie D.C. Markers of inflammation and myofibrillar proteins following eccentric exercise in humans. Eur J Appl Physiol 2001, 84:180-186. 10.1007/s004210170002.
91. Smith L.L., Anwar A., Fragen M., Rananto C., Johnson R., Holbert D. Cytokines and cell adhesion molecules associated with high-intensity eccentric exercise. Eur J Appl Physiol 2000, 82:61-67. 10.1007/s004210050652.
92. Chalaris A., Rabe B., Paliga K., Lange H., Laskay T., Fielding C.A., et al. Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils. Blood 2007, 110:1748-1755. 10.1182/blood-2007-01-067918.
93. Filardy A.A., Pires D.R., Nunes M.P., Takiya C.M., Freire-de-Lima C.G., Ribeiro-Gomes F.L., et al. Proinflammatory clearance of apoptotic neutrophils induces an IL-12(low)IL-10(high) regulatory phenotype in macrophages. J Immunol 2010, 185:2044-2050. 10.4049/jimmunol.1000017.
94. Smolewska E., Brozik H., Smolewski P., Biernacka-Zielinska M., Darzynkiewicz Z., Stanczyk J. Apoptosis of peripheral blood lymphocytes in patients with juvenile idiopathic arthritis. Ann Rheum Dis 2003, 62:761-763.
95. Smolewska E., Stanczyk J., Robak T., Smolewski P. Inhibited apoptosis of synovial fluid lymphocytes in children with juvenile idiopathic arthritis is associated with increased expression of myeloid cell leukemia 1 and XIAP proteins. J Rheumatol 2006, 33:1684-1690.
96. Smolewska E., Brózik H., Smolewski P., Darzynkiewicz Z., Stańczyk J. Regulation of peripheral blood and synovial fluid lymphocyte apoptosis in juvenile idiopathic arthritis. Scand J Rheumatol 2004, 33:7-12.
97. Smolewska E., Cebula B., Brózik H., Stańczyk J. Relationship between impaired apoptosis of lymphocytes and distribution of dendritic cells in peripheral blood and synovial fluid of children with juvenile idiopathic arthritis. Arch Immunol Ther Exp (Warsz) 2008, 56:283-289. 10.1007/s00005-008-0030-5.
98. Zaldivar F., Wang-Rodriguez J., Nemet D., Schwindt C., Galassetti P., Mills P.J., et al. Constitutive pro- and anti-inflammatory cytokine and growth factor response to exercise in leukocytes. J Appl Physiol 2006, 100:1124-1133. 10.1152/japplphysiol.00562.2005.
99. Steensberg A., Fischer C.P., Keller C., Møller K., Pedersen B.K. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab 2003, 285:E433-E437. 10.1152/ajpendo.00074.2003.
100. Krüger K., Mooren F.C. Exercise-induced leukocyte apoptosis. Exerc Immunol Rev 2014, 20:117-134.
101. Duroux-Richard I., Jorgensen C., Apparailly F. miRNAs and rheumatoid arthritis - promising novel biomarkers. Swiss Med Wkly 2011, 141:w13175. 10.4414/smw.2011.13175.
102. Murata K., Yoshitomi H., Tanida S., Ishikawa M., Nishitani K., Ito H., et al. Plasma and synovial fluid microRNAs as potential biomarkers of rheumatoid arthritis and osteoarthritis. Arthritis Res Ther 2010, 12:R86. 10.1186/ar3013.
103. Xu T., Liu Q., Yao J., Dai Y., Wang H., Xiao J. Circulating microRNAs in response to exercise. Scand J Med Sci Sports 2015, 10.1111/sms.12421.
104. Nielsen S., Åkerström T., Rinnov A., Yfanti C., Scheele C., Pedersen B.K., et al. The miRNA plasma signature in response to acute aerobic exercise and endurance training. PLoS One 2014, e87308. 10.1371/journal.pone.0087308.
105. Aoi W., Sakuma K. Does regulation of skeletal muscle function involve circulating microRNAs?. Front Physiol 2014, 5:39. 10.3389/fphys.2014.00039.
106. Baltimore D., Boldin M.P., O'Connell R.M., Rao D.S., Taganov K.D. MicroRNAs: new regulators of immune cell development and function. Nat Immunol 2008, 9:839-845. 10.1038/ni.f.209.
107. Saba R., Sorensen D.L., Booth S.A. MicroRNA-146a: a dominant, negative regulator of the innate immune response. Front Immunol 2014, 5:578. 10.3389/fimmu.2014.00578.
108. Song G.G., Bae S.-C., Seo Y.H., Kim J.-H., Choi S.J., Ji J.D., et al. The association between susceptibility to inflammatory arthritis and miR-146a, miR-499 and IRAK1 polymorphisms : a meta-analysis. Z Rheumatol 2014, 10.1007/s00393-014-1493-x.
109. Singh S., Rai G., Aggarwal A. Association of microRNA-146a and its target gene IRAK1 polymorphism with enthesitis related arthritis category of juvenile idiopathic arthritis. Rheumatol Int 2014, 34:1395-1400. 10.1007/s00296-014-3001-7.
110. Jiménez-Morales S., Gamboa-Becerra R., Baca V., Del Río-Navarro B.E., López-Ley D.Y., Velázquez-Cruz R., et al. MiR-146a polymorphism is associated with asthma but not with systemic lupus erythematosus and juvenile rheumatoid arthritis in Mexican patients. Tissue Antigens 2012, 80:317-321. 10.1111/j.1399-0039.2012.01929.x.
111. Myles A., Rahman M.T., Aggarwal A. Membrane-bound toll-like receptors are overexpressed in peripheral blood and synovial fluid mononuclear cells of enthesitis-related arthritis category of juvenile idiopathic arthritis (JIA-ERA) patients and lead to secretion of inflammatory mediators. J Clin Immunol 2012, 32:488-496. 10.1007/s10875-011-9640-5.
112. Sjakste T., Paramonova N., Rumba-Rozenfelde I., Trapina I., Sugoka O., Sjakste N. Juvenile idiopathic arthritis subtype- and sex-specific associations with genetic variants in the PSMA6/PSMC6/PSMA3 gene cluster. Pediatr Neonatol 2014, 55:393-403. 10.1016/j.pedneo.2014.01.007.
113. Makarova J.A., Maltseva D.V., Galatenko V.V., Abbasi A., Maximenko D.G., Grigoriev A.I., et al. Exercise immunology meets MiRNAs. Exerc Immunol Rev 2014, 20:135-164.
114. Martini A. Systemic juvenile idiopathic arthritis. Autoimmun Rev 2012, 12:56-59. 10.1016/j.autrev.2012.07.022.
115. Kessel C., Holzinger D., Foell D. Phagocyte-derived S100 proteins in autoinflammation: putative role in pathogenesis and usefulness as biomarkers. Clin Immunol 2013, 147:229-241. 10.1016/j.clim.2012.11.008.
116. Gerss J., Roth J., Holzinger D., Ruperto N., Wittkowski H., Frosch M., et al. Phagocyte-specific S100 proteins and high-sensitivity C reactive protein as biomarkers for a risk-adapted treatment to maintain remission in juvenile idiopathic arthritis: a comparative study. Ann Rheum Dis 2012, 71:1991-1997. 10.1136/annrheumdis-2012-201329.
117. Lee D.-G., Woo J.-W., Kwok S.-K., Cho M.-L., Park S.-H. MRP8 promotes Th17 differentiation via upregulation of IL-6 production by fibroblast-like synoviocytes in rheumatoid arthritis. Exp Mol Med 2013, 45:e20. 10.1038/emm.2013.39.
118. Rahman M.T., Myles A., Gaur P., Misra R., Aggarwal A. TLR4 endogenous ligand MRP8/14 level in enthesitis-related arthritis and its association with disease activity and TLR4 expression. Rheumatology (Oxford) 2014, 53:270-274. 10.1093/rheumatology/ket375.
119. Rothmund F., Gerss J., Ruperto N., Däbritz J., Wittkowski H., Frosch M., et al. Validation of relapse risk biomarkers for routine use in patients with juvenile idiopathic arthritis. Arthritis Care Res (Hoboken) 2014, 66:949-955. 10.1002/acr.22248.
120. Fagerhol M.K., Nielsen H.G., Vetlesen A., Sandvik K., Lyberg T. Increase in plasma calprotectin during long-distance running. Scand J Clin Lab Invest 2005, 65:211-220.
121. Mooren F.C., Lechtermann A., Fobker M., Brandt B., Sorg C., Völker K., et al. The response of the novel pro-inflammatory molecules S100A8/A9 to exercise. Int J Sports Med 2006, 27:751-758. 10.1055/s-2005-872909.
122. Mortensen O.H., Andersen K., Fischer C., Nielsen A.R., Nielsen S., Akerström T., et al. Calprotectin is released from human skeletal muscle tissue during exercise. J Physiol (Lond) 2008, 586:3551-3562. 10.1113/jphysiol.2008.153551.