Skip to main content
Top
Published in: Rheumatology International 12/2011

01-12-2011 | Original Article

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

Authors: A. F. Christensen, S. V. Hoegh, T. Lottenburger, U. Holmskov, I. Tornoe, K. Hørslev-Petersen, G. L. Sørensen, P. Junker

Published in: Rheumatology International | Issue 12/2011

Login to get access

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.
Literature
1.
go back to reference Holmskov U (2000) Collectins and collectin receptors in innate immunity. APMIS Suppl 100:1–59PubMed Holmskov U (2000) Collectins and collectin receptors in innate immunity. APMIS Suppl 100:1–59PubMed
2.
go back to reference 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 174:1532–1538PubMed 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 174:1532–1538PubMed
3.
go back to reference Hartshorn KL, White MR, Tecle T et al (2007) Reduced influenza viral neutralizing activity of natural human trimers of surfactant protein D. Respir Res 8:9PubMedCrossRef Hartshorn KL, White MR, Tecle T et al (2007) Reduced influenza viral neutralizing activity of natural human trimers of surfactant protein D. Respir Res 8:9PubMedCrossRef
4.
go back to reference 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–L969 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–L969
5.
go back to reference 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 28:249–256PubMedCrossRef 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 28:249–256PubMedCrossRef
6.
go back to reference 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 50:651–660PubMedCrossRef 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 50:651–660PubMedCrossRef
7.
go back to reference Crouch E, Parghi D, Kuan SF et al (1992) Surfactant protein D: subcellular localization in nonciliated bronchiolar epithelial cells. Am J Physiol 263:L60–L66PubMed Crouch E, Parghi D, Kuan SF et al (1992) Surfactant protein D: subcellular localization in nonciliated bronchiolar epithelial cells. Am J Physiol 263:L60–L66PubMed
8.
go back to reference 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 40:1589–1597PubMedCrossRef 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 40:1589–1597PubMedCrossRef
9.
go back to reference 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 108:29–37PubMedCrossRef 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 108:29–37PubMedCrossRef
10.
go back to reference 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 266:157–171PubMedCrossRef 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 266:157–171PubMedCrossRef
11.
go back to reference Sorensen GL, Madsen J, Kejling K et al (2006) Surfactant protein D is proatherogenic in mice. Am J Physiol Heart Circ Physiol 290:H2286–H2294PubMedCrossRef Sorensen GL, Madsen J, Kejling K et al (2006) Surfactant protein D is proatherogenic in mice. Am J Physiol Heart Circ Physiol 290:H2286–H2294PubMedCrossRef
12.
go back to reference Woodsworth BA, Lathers D, Neal JG et al (2006) Immunolocalization of surfactant protein A and D in sinonasal mucosa. Am J Rhinol 20:461–465CrossRef Woodsworth BA, Lathers D, Neal JG et al (2006) Immunolocalization of surfactant protein A and D in sinonasal mucosa. Am J Rhinol 20:461–465CrossRef
13.
go back to reference Oberley RE, Goss KL, Dahmoush L et al (2005) A role for surfactant protein D in innate immunity of the human prostate. Prostate 65:241–251PubMedCrossRef Oberley RE, Goss KL, Dahmoush L et al (2005) A role for surfactant protein D in innate immunity of the human prostate. Prostate 65:241–251PubMedCrossRef
14.
go back to reference 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 73:2147–2156PubMedCrossRef 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 73:2147–2156PubMedCrossRef
15.
go back to reference Leth-Larsen R, Floridon C, Nielsen O et al (2004) Surfactant protein D in the female genital tract. Mol Hum Reprod 10:149–154PubMedCrossRef Leth-Larsen R, Floridon C, Nielsen O et al (2004) Surfactant protein D in the female genital tract. Mol Hum Reprod 10:149–154PubMedCrossRef
16.
go back to reference Madsen J, Kliem A, Tornoe I et al (2000) Localization of lung surfactant protein D on mucosal surfaces in human tissues. J Immunol 164:5866–5870PubMed Madsen J, Kliem A, Tornoe I et al (2000) Localization of lung surfactant protein D on mucosal surfaces in human tissues. J Immunol 164:5866–5870PubMed
17.
go back to reference Hermans CEDR, Bernard ALFR (1999) Lung epithelium-specific proteins. Characteristics and potential applications as markers. Am J Respir Crit Care Med 159:646–678PubMed Hermans CEDR, Bernard ALFR (1999) Lung epithelium-specific proteins. Characteristics and potential applications as markers. Am J Respir Crit Care Med 159:646–678PubMed
18.
go back to reference Christensen AF, Holmskov U, Sorensen GL et al (2008) Surfactant protein D is decreased in rheumatoid arthritis. Arthritis Rheum 58:S708 Christensen AF, Holmskov U, Sorensen GL et al (2008) Surfactant protein D is decreased in rheumatoid arthritis. Arthritis Rheum 58:S708
19.
go back to reference 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 67:71–76PubMedCrossRef 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 67:71–76PubMedCrossRef
20.
go back to reference Arnett FC, Edworthy SM, Bloch DA et al (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–324PubMedCrossRef Arnett FC, Edworthy SM, Bloch DA et al (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–324PubMedCrossRef
21.
go back to reference 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 30:103–109PubMedCrossRef 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 30:103–109PubMedCrossRef
22.
go back to reference 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 Netherlands 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 Netherlands
23.
go back to reference Larsen A, Dale K, Eek M (1977) Radiographic evaluation of rheumatoid arthritis and related conditions by standard reference films. Acta Radiol Diagn Stockh 18:481–491PubMed Larsen A, Dale K, Eek M (1977) Radiographic evaluation of rheumatoid arthritis and related conditions by standard reference films. Acta Radiol Diagn Stockh 18:481–491PubMed
24.
go back to reference Høier-Madsen M, Nielsen LP, Møller S (1986) Determination of IgM rheumatoid factors by enzyme-linked immunosorbent assay (ELISA). Ugeskr Laeger 148:2018–2021PubMed Høier-Madsen M, Nielsen LP, Møller S (1986) Determination of IgM rheumatoid factors by enzyme-linked immunosorbent assay (ELISA). Ugeskr Laeger 148:2018–2021PubMed
25.
go back to reference 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) 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)
26.
go back to reference Sorensen GL, Husby S, Holmskov U (2007) Surfactant protein A and surfactant protein D variation in pulmonary disease. Immunobiology 212:381–416PubMedCrossRef Sorensen GL, Husby S, Holmskov U (2007) Surfactant protein A and surfactant protein D variation in pulmonary disease. Immunobiology 212:381–416PubMedCrossRef
27.
go back to reference 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 176:3557–3565PubMed 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 176:3557–3565PubMed
28.
go back to reference 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–L80PubMed 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–L80PubMed
29.
go back to reference 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 91529 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 91529
30.
go back to reference Dulkerian SJ, Gonzales LW, Ning Y et al (1996) Regulation of surfactant proetin D in human fetal lung. Am J Respir Cell Mol Biol 15:781–786PubMed Dulkerian SJ, Gonzales LW, Ning Y et al (1996) Regulation of surfactant proetin D in human fetal lung. Am J Respir Cell Mol Biol 15:781–786PubMed
31.
go back to reference 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 51:907–913PubMedCrossRef 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 51:907–913PubMedCrossRef
32.
go back to reference 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) 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.
go back to reference Cutolo M, Straub RH (2008) Circadian rhythms in arthritis: hormonal effects on the immune/inflammatory reaction. Autoimmun Rev 7:223–228PubMedCrossRef Cutolo M, Straub RH (2008) Circadian rhythms in arthritis: hormonal effects on the immune/inflammatory reaction. Autoimmun Rev 7:223–228PubMedCrossRef
34.
go back to reference Petrovsky N, McNair P, Harrison LC (1998) Diurnal rhythms of pro-inflammatory cytokines: regulation by plasma cortisol and therapeutic implications. Cytokine 10:307–312PubMedCrossRef Petrovsky N, McNair P, Harrison LC (1998) Diurnal rhythms of pro-inflammatory cytokines: regulation by plasma cortisol and therapeutic implications. Cytokine 10:307–312PubMedCrossRef
35.
go back to reference 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 64:212–216PubMedCrossRef 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 64:212–216PubMedCrossRef
36.
go back to reference Maestroni GJ, Sulli A, Pizzorni C et al (2002) Melatonin in rheumatoid arthritis: synovial macrophages show melatonin receptors. Ann N Y Acad Sci 966:271–275PubMedCrossRef Maestroni GJ, Sulli A, Pizzorni C et al (2002) Melatonin in rheumatoid arthritis: synovial macrophages show melatonin receptors. Ann N Y Acad Sci 966:271–275PubMedCrossRef
37.
go back to reference Zoli A, Lizzio MM, Ferlisi EM et al (2002) ACTH, cortisol and prolactin in active rheumatoid arthritis. Clin Rheumatol 21:289–293PubMedCrossRef Zoli A, Lizzio MM, Ferlisi EM et al (2002) ACTH, cortisol and prolactin in active rheumatoid arthritis. Clin Rheumatol 21:289–293PubMedCrossRef
38.
go back to reference Straub RH, Cutolo M (2007) Circadian rhythms in rheumatoid arthritis. Implications for pathophysiology and therapeutic management. Arthritis Rheum 56:399–408PubMedCrossRef Straub RH, Cutolo M (2007) Circadian rhythms in rheumatoid arthritis. Implications for pathophysiology and therapeutic management. Arthritis Rheum 56:399–408PubMedCrossRef
39.
go back to reference Pedersen BK, Hoffman-Goetz L (2000) Exercise and the immune system: regulation, integration and adaptation. Physiol Rev 80:1055–1081PubMed Pedersen BK, Hoffman-Goetz L (2000) Exercise and the immune system: regulation, integration and adaptation. Physiol Rev 80:1055–1081PubMed
40.
go back to reference Hill EE, Zack E, Battaglini C et al (2008) Exercise and circulating cortisol level: the intensity threshold effect. J Endocrinol Invest 31:587–591PubMed Hill EE, Zack E, Battaglini C et al (2008) Exercise and circulating cortisol level: the intensity threshold effect. J Endocrinol Invest 31:587–591PubMed
41.
go back to reference Chikanza IC, Petrou P, Kingsley G et al (1992) Defective hypothalamic response to immune and inflammatory stimuli in patients with rheumatoid arthritis. Arthritis Rheum 35:1281–1288PubMed Chikanza IC, Petrou P, Kingsley G et al (1992) Defective hypothalamic response to immune and inflammatory stimuli in patients with rheumatoid arthritis. Arthritis Rheum 35:1281–1288PubMed
42.
go back to reference Eijsbouts AM, van den Hoogen FH, Laan RF et al (2005) Hypothalamic-pituitary-adrenal axis activity in patients with rheumatoid arthritis. Clin Exp Rheumatol 23:658–664PubMed Eijsbouts AM, van den Hoogen FH, Laan RF et al (2005) Hypothalamic-pituitary-adrenal axis activity in patients with rheumatoid arthritis. Clin Exp Rheumatol 23:658–664PubMed
43.
go back to reference 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 43:43–48PubMedCrossRef 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 43:43–48PubMedCrossRef
Metadata
Title
Circadian rhythm and the influence of physical activity on circulating surfactant protein D in early and long-standing rheumatoid arthritis
Authors
A. F. Christensen
S. V. Hoegh
T. Lottenburger
U. Holmskov
I. Tornoe
K. Hørslev-Petersen
G. L. Sørensen
P. Junker
Publication date
01-12-2011
Publisher
Springer-Verlag
Published in
Rheumatology International / Issue 12/2011
Print ISSN: 0172-8172
Electronic ISSN: 1437-160X
DOI
https://doi.org/10.1007/s00296-010-1538-7

Other articles of this Issue 12/2011

Rheumatology International 12/2011 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.