Rheumatology International

, Volume 31, Issue 12, pp 1617–1623 | Cite as

Circadian rhythm and the influence of physical activity on circulating surfactant protein D in early and long-standing rheumatoid arthritis

  • A. F. Christensen
  • S. V. Hoegh
  • T. Lottenburger
  • U. Holmskov
  • I. Tornoe
  • K. Hørslev-Petersen
  • G. L. Sørensen
  • P. Junker
Original Article
First Online:
Received:
Accepted:

Abstract

Surfactant protein D (SP-D) belongs to the collectin family and has pro-and anti-inflammatory capacities depending on its oligomerization. Previously, circulating SP-D was shown to be decreased in early rheumatoid arthritis (RA) and negatively correlated to disease activity. This study aimed at assessing the diurnal rhythmicity and the influence of physical activity on circulating SP-D in patients with RA at different stages compared with healthy individuals. Patients with early RA (ERA) with disease duration <6 months and with long-standing RA (LRA) with disease duration 5–15 years were included in two sub-studies. Healthy individuals served as controls. Diurnal variation: blood samples were collected every 3 h from 7 a.m to 10 p.m and the following morning. Physical activity: blood sampling was done before and after standardized physical challenge. SP-D was measured by ELISA. SP-D exhibited diurnal variation in healthy controls (n = 15) and in patients with ERA (n = 9) and LRA (n = 9) with peak values at 10 a.m. and nadir in the evening (controls: P < 0.001, ERA: P = 0.004 and LRA: P = 0.009). Three hours after cessation of physical activity, SP-D decreased below pre-exercise levels in both ERA (n = 10), LRA (n = 10) and controls (n = 13) (ERA: P < 0.001, LRA: P < 0.001 and controls: P = 0.005). In patients with RA, the decline was already observed 1 h post-exercise. Circulating SP-D exhibits diurnal variation both in patients with RA at different stages and in healthy controls. SP-D in serum decreases following physical activity in health and RA disease. This study underscores the need of standardized blood sampling conditions in future studies on SP-D.

Keywords

Rheumatoid arthritis Surfactant Protein D Circadian rhythm Exercise 
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Notes

Acknowledgments

This study was supported by the Danish Rheumatism Association and the A. P Møller Foundation for the Advancement of Medical Science.

References

  1. 1.
    Holmskov U (2000) Collectins and collectin receptors in innate immunity. APMIS Suppl 100:1–59PubMedGoogle Scholar
  2. 2.
    Leth-Larsen R, Garred P, Jensenius H et al (2005) A common polymorphism in the SFTPD gene influences assembly, function, and concentration of surfactant protein D. J Immunol 174:1532–1538PubMedGoogle Scholar
  3. 3.
    Hartshorn KL, White MR, Tecle T et al (2007) Reduced influenza viral neutralizing activity of natural human trimers of surfactant protein D. Respir Res 8:9PubMedCrossRefGoogle Scholar
  4. 4.
    Hartshorn KL, Crouch E, White MR et al (1998) Pulmonary surfactant proteins A and D enhance neutrophil uptake of bacteria. Am J Physiol Lung Cell Mol Physiol 274:L958–L969Google Scholar
  5. 5.
    Bufler P, Schmidt B, Schikor D et al (2003) Surfactant protein A and D differently regulate the immune response to nonmucoid Pseudomonas aeruginosa and its lipopolysaccharide. Am J Respir Cell Mol Biol 28:249–256PubMedCrossRefGoogle Scholar
  6. 6.
    Stahlman MT, Gray ME, Hull WM et al (2002) Immunolocalization of surfactant protein-D (SP-D) in human fetal, newborn, and adult tissues. J Histochem Cytochem 50:651–660PubMedCrossRefGoogle Scholar
  7. 7.
    Crouch E, Parghi D, Kuan SF et al (1992) Surfactant protein D: subcellular localization in nonciliated bronchiolar epithelial cells. Am J Physiol 263:L60–L66PubMedGoogle Scholar
  8. 8.
    Voorhout WF, Veenendaal T, Kuroki Y et al (1992) Immunocytochemical localization of surfactant protein D (SP-D) in type II cells, Clara cells, and alveolar macrophages of rat lung. J Histochem Cytochem 40:1589–1597PubMedCrossRefGoogle Scholar
  9. 9.
    Leth-Larsen R, Nordenbaek C, Tornoe I et al (2003) Surfactant protein D (SP-D) serum levels in patients with community-acquired pneumonia. Clin Immunol 108:29–37PubMedCrossRefGoogle Scholar
  10. 10.
    Nagae H, Takahashi H, Kuroki Y et al (1997) Enzyme-linked immunosorbent assay using F(ab’)2 fragment for the detection of human pulmonary surfactant protein D in sera. Clin Chim Acta 266:157–171PubMedCrossRefGoogle Scholar
  11. 11.
    Sorensen GL, Madsen J, Kejling K et al (2006) Surfactant protein D is proatherogenic in mice. Am J Physiol Heart Circ Physiol 290:H2286–H2294PubMedCrossRefGoogle Scholar
  12. 12.
    Woodsworth BA, Lathers D, Neal JG et al (2006) Immunolocalization of surfactant protein A and D in sinonasal mucosa. Am J Rhinol 20:461–465CrossRefGoogle Scholar
  13. 13.
    Oberley RE, Goss KL, Dahmoush L et al (2005) A role for surfactant protein D in innate immunity of the human prostate. Prostate 65:241–251PubMedCrossRefGoogle Scholar
  14. 14.
    Ni M, Evans DJ, Hawgood S et al (2005) Surfactant protein D is present in human tear fluid and the cornea and inhibits epithelial cell invasion by Pseudomonas aeruginosa. Infect Immun 73:2147–2156PubMedCrossRefGoogle Scholar
  15. 15.
    Leth-Larsen R, Floridon C, Nielsen O et al (2004) Surfactant protein D in the female genital tract. Mol Hum Reprod 10:149–154PubMedCrossRefGoogle Scholar
  16. 16.
    Madsen J, Kliem A, Tornoe I et al (2000) Localization of lung surfactant protein D on mucosal surfaces in human tissues. J Immunol 164:5866–5870PubMedGoogle Scholar
  17. 17.
    Hermans CEDR, Bernard ALFR (1999) Lung epithelium-specific proteins. Characteristics and potential applications as markers. Am J Respir Crit Care Med 159:646–678PubMedGoogle Scholar
  18. 18.
    Christensen AF, Holmskov U, Sorensen GL et al (2008) Surfactant protein D is decreased in rheumatoid arthritis. Arthritis Rheum 58:S708Google Scholar
  19. 19.
    Hoegh SV, Lindegaard HM, Sorensen GL et al (2008) Circulating surfactant protein D is decreased in early rheumatoid arthritis: A 1-year prospective study. Scand J Immunol 67:71–76PubMedCrossRefGoogle Scholar
  20. 20.
    Arnett FC, Edworthy SM, Bloch DA et al (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–324PubMedCrossRefGoogle Scholar
  21. 21.
    Thorsen H, Hansen TM, Mckenna SP et al (2001) Adaption into Danish of the stanford health assessment questionnaire (HAQ) and the rheumatoid arthritis quality of life scale (RaQol). Scand J Rheumatol 30:103–109PubMedCrossRefGoogle Scholar
  22. 22.
    van Riel PL, Scott DL (2004) Eular handbook of clinical assessments in rheumatoid arthritis, 3 edn. Van Zuiden Communications B.V., CC Alphen aan den Rijn, The NetherlandsGoogle Scholar
  23. 23.
    Larsen A, Dale K, Eek M (1977) Radiographic evaluation of rheumatoid arthritis and related conditions by standard reference films. Acta Radiol Diagn Stockh 18:481–491PubMedGoogle Scholar
  24. 24.
    Høier-Madsen M, Nielsen LP, Møller S (1986) Determination of IgM rheumatoid factors by enzyme-linked immunosorbent assay (ELISA). Ugeskr Laeger 148:2018–2021PubMedGoogle Scholar
  25. 25.
    Hoegh SV, Sorensen GL, Tornoe I et al (2009) Long-term stability and circadian variation in circulating levels of surfactant protein D. Immunobiology (Epub ahead of print)Google Scholar
  26. 26.
    Sorensen GL, Husby S, Holmskov U (2007) Surfactant protein A and surfactant protein D variation in pulmonary disease. Immunobiology 212:381–416PubMedCrossRefGoogle Scholar
  27. 27.
    Haczku A, Cao Y, Vass G et al (2006) IL-4 and IL-13 form a negative feedback circuit with surfactant protein-D in the allergic airway response. J Immunol 176:3557–3565PubMedGoogle Scholar
  28. 28.
    Ikegami M, Whitsett JA, Chroneos ZC et al (2000) IL-4 increases surfactant and regulates metabolism in vivo. Am J Physiol Lung Cell Mol Physiol 278:L75–L80PubMedGoogle Scholar
  29. 29.
    Snyder GD, Oberley-Deegan RE, Goss KL et al (2008) Surfactant protein D is expressed and modulates inflammatory responses in human coronary artery smooth muscle cells. Am J Physiol Heart Circ Physiol 91529Google Scholar
  30. 30.
    Dulkerian SJ, Gonzales LW, Ning Y et al (1996) Regulation of surfactant proetin D in human fetal lung. Am J Respir Cell Mol Biol 15:781–786PubMedGoogle Scholar
  31. 31.
    Wang JY, Yeh TF, Lin YC et al (1996) Measurement of pulmonary status and surfactant protein levels during dexamethasone treatment of neonatal respiratory distress syndrome. Thorax 51:907–913PubMedCrossRefGoogle Scholar
  32. 32.
    Fernandez-Real JM, Valdes S, Manco M et al (2010) Surfactant protein D, a marker of lung innate immunity, is positively associated with insulin resistance. Diabetes Care. doi: dc09-0542/DC1 (E-pub ahead of print)
  33. 33.
    Cutolo M, Straub RH (2008) Circadian rhythms in arthritis: hormonal effects on the immune/inflammatory reaction. Autoimmun Rev 7:223–228PubMedCrossRefGoogle Scholar
  34. 34.
    Petrovsky N, McNair P, Harrison LC (1998) Diurnal rhythms of pro-inflammatory cytokines: regulation by plasma cortisol and therapeutic implications. Cytokine 10:307–312PubMedCrossRefGoogle Scholar
  35. 35.
    Cutolo M, Maestroni GJ, Otsa K et al (2005) Circadian melatonin and cortisol levels in rheumatoid arthritis patients in winter time: a north and south Europe comparison. Ann Rheum Dis 64:212–216PubMedCrossRefGoogle Scholar
  36. 36.
    Maestroni GJ, Sulli A, Pizzorni C et al (2002) Melatonin in rheumatoid arthritis: synovial macrophages show melatonin receptors. Ann N Y Acad Sci 966:271–275PubMedCrossRefGoogle Scholar
  37. 37.
    Zoli A, Lizzio MM, Ferlisi EM et al (2002) ACTH, cortisol and prolactin in active rheumatoid arthritis. Clin Rheumatol 21:289–293PubMedCrossRefGoogle Scholar
  38. 38.
    Straub RH, Cutolo M (2007) Circadian rhythms in rheumatoid arthritis. Implications for pathophysiology and therapeutic management. Arthritis Rheum 56:399–408PubMedCrossRefGoogle Scholar
  39. 39.
    Pedersen BK, Hoffman-Goetz L (2000) Exercise and the immune system: regulation, integration and adaptation. Physiol Rev 80:1055–1081PubMedGoogle Scholar
  40. 40.
    Hill EE, Zack E, Battaglini C et al (2008) Exercise and circulating cortisol level: the intensity threshold effect. J Endocrinol Invest 31:587–591PubMedGoogle Scholar
  41. 41.
    Chikanza IC, Petrou P, Kingsley G et al (1992) Defective hypothalamic response to immune and inflammatory stimuli in patients with rheumatoid arthritis. Arthritis Rheum 35:1281–1288PubMedGoogle Scholar
  42. 42.
    Eijsbouts AM, van den Hoogen FH, Laan RF et al (2005) Hypothalamic-pituitary-adrenal axis activity in patients with rheumatoid arthritis. Clin Exp Rheumatol 23:658–664PubMedGoogle Scholar
  43. 43.
    Pool AJ, Whipp BJ, Skasick AJ et al (2004) Serum cortisol reduction and abnormal prolactin and CD4 +/CD8 + T-cell response as a result of controlled exercise in patients with rheumatoid arthritis and systemic lupus erythematosus despite unaltered muscle energetics. Rheumatology 43:43–48PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • A. F. Christensen
    • 1
    • 2
  • S. V. Hoegh
    • 3
  • T. Lottenburger
    • 4
  • U. Holmskov
    • 3
  • I. Tornoe
    • 3
  • K. Hørslev-Petersen
    • 4
  • G. L. Sørensen
    • 3
  • P. Junker
    • 1
    • 2
  1. 1.Department of Rheumatology COdense University HospitalOdenseDenmark
  2. 2.Institute of Clinical ResearchUniversity of Southern DenmarkOdenseDenmark
  3. 3.Institute of Molecular MedicineUniversity of Southern DenmarkOdenseDenmark
  4. 4.Graasten Rheumatism HospitalGraastenDenmark

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