Skip to main content

Advertisement

SpringerLink
Log in

Adiponectin in Asthma and Obesity: Protective Agent or Risk Factor for More Severe Disease?

  • Published:
Lung Aims and scope Submit manuscript

Abstract

Purpose

The relationship between asthma and obesity is well established, although the pathophysiological mechanisms linking both diseases remain unknown. Adiponectin is a hormone secreted by adipose cells, plays a role in the modulation of inflammation and may be the key linking these two types of inflammation.

Methods

We conducted a cross-sectional study with asthma with different body mass indices (BMI); the patients were classified as eutrophic, overweight, or obese. We assessed disease control using the GINA consensus, and the levels of adiponectin, C-reactive protein (CRP) and interleukin 33 (IL-33) in each of the patients.

Results

We evaluated 75 of the 96 patients eligible for the study, including 25 in each BMI group. The CRP levels were significantly higher in the obese patients compared with both the eutrophic (p = 0.01) and the overweight (p = 0.03) patients. The mean adiponectin level was 21.82 ± 9.93 mg/L for the eutrophic asthmatics, which is a level that was significantly higher than in the overweight (15.31 ± 6.27 mg/L, p = 0.0140) and the obese (16.69 ± 11.45 mg/L, p = 0.0287) patients. The patients with higher adiponectin levels exhibited smaller FEV1 (p = 0.02) and lower FVC (p = 0.003). The IL-33 levels were not different between the groups.

Conclusions

Adiponectin does not protect against the development of inflammation in the setting of asthma and may in fact exacerbate the disease via its anti-TH1 inflammatory effects, allowing for increased TH2 differentiation and a more severe allergic response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Shore SA, Johnston RA (2006) Obesity and asthma. Pharmacol Ther 110:83–203

    Article  CAS  PubMed  Google Scholar 

  2. Ford ES (2005) The epidemiology of obesity and asthma. J Allergy Clin Immunol 115:897–909

    Article  PubMed  Google Scholar 

  3. Delgado J, Barranco P, Quirce S (2008) Obesity and asthma. J Investig Allergol Clin Immunol 18:420–425

    CAS  PubMed  Google Scholar 

  4. Camilo DF, Ribeiro JD, Toro ADCT, Baracat ECE, Barros Filho AA (2010) Obesidade e asma: associação ou coincidência? J Pediatr (Rio J) 86:6–14

    Google Scholar 

  5. Liu MC, Hubbard WC, Proud D, Stealey BA, Galli SJ, Kagey-Sobotka A, Bleecker ER, Lichtenstein LM (1991) Immediate and late inflammatory responses to ragweed antigen challenge of the peripheral airways in allergic asthmatics. Cellular, mediator, and permeability changes. Am Rev Respir Dis 144:51–58

    Article  CAS  PubMed  Google Scholar 

  6. Patel PS, Buras ED, Balasubramanyam A (2013) The role of the immune system in obesity and insulin resistance. J Obes 2013:616193

    PubMed Central  PubMed  Google Scholar 

  7. Hotamisligil GS, Shargill NS, Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259:87–91

    Article  CAS  PubMed  Google Scholar 

  8. Trayhurn P, Wood IS (2005) Signalling role of adipose tissue: adipokines and inflammation in obesity. Biochem Soc Trans 33:1078–1081

    Article  CAS  PubMed  Google Scholar 

  9. Florez H, Castillo-Florez S, Mendez A, Casanova-Romero P, Larreal-Urdaneta C, Lee D, Goldberg R (2006) C-reactive protein is elevated in obese patients with the metabolic syndrome. Diabetes Res Clin Pract 71:92–100

    Article  CAS  PubMed  Google Scholar 

  10. Miller AM (2011) Role of IL-33 in inflammation and disease. J Inflamm (Lond) 8:22

    Article  CAS  Google Scholar 

  11. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X, Gorman DM, Bazan JF, Kastelein RA (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23:479–490

    Article  CAS  PubMed  Google Scholar 

  12. Oboki K, Ohno T, Kajiwara N, Arae K, Morita H, Ishii A, Nambu A, Abe T, Kiyonari H, Matsumoto K, Sudo K, Okumura K, Saito H, Nakae S (2010) IL-33 is a crucial amplifier of innate rather than acquired immunity. Prac Natl Acad Sci USA 107:18581–18586

    Article  CAS  Google Scholar 

  13. Miller AM, Asquith DL, Hueber AJ, Anderson LA, Holmes WM, McKenzie AN, Xu D, Sattar N, McInnes IB, Liew FY (2010) Interleukin-33 induces protective effects in adipose tissue inflammation during obesity in mice. Circ Res 107:650–658

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, Hotta K, Shimomura I, Nakamura T, Miyaoka K, Kuriyama H, Nishida M, Yamashita S, Okubo K, Matsubara K, Muraguchi M, Ohmoto Y, Funahashi T, Matsuzawa Y (1999) Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 257:79–83

    Article  CAS  PubMed  Google Scholar 

  15. Pellegrino R, Viegi G, Brusasco V, Crapo RO, Burgos F, Casaburi R, Coates A, van der Grinten CP, Gustafsson P, Hankinson J, Jensen R, Johnson DC, MacIntyre N, McKay R, Miller MR, Navajas D, Pedersen OF, Wanger J (2005) Interpretative strategies for lung function tests. Eur Respir J 26:948–968

    Article  CAS  PubMed  Google Scholar 

  16. Xu A, Wang Y, Keshaw H, Xu LY, Lam KSL, Cooper GJS (2003) The fat-derived hormone adiponectin alleviates alcoholic and nonalcoholic fatty liver diseases in mice. J Clin Invest. doi:10.1172/JCI200317797

    Google Scholar 

  17. Spanevello A, Confalonieri M, Sulotto F, Romano F, Balzano G, Migliori GB, Bianchi A, Michetti G (2000) Induced sputum cellularity. Reference values and distribution in normal volunteers. Am J Respir Crit Care Med 162:1172–1174

    Article  CAS  PubMed  Google Scholar 

  18. Global initiative for asthma (2014) Global strategy for asthma management and prevention. http://www.ginasthma.org. Accessed 06 June 2015

  19. Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3:23–35

    Article  CAS  PubMed  Google Scholar 

  20. Fain JN, Madan AK, Hiler ML, Cheema P, Bahouth SW (2004) Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 145:2273–2282

    Article  CAS  PubMed  Google Scholar 

  21. Masaki T, Chiba S, Tatsukawa H, Yasuda T, Noguchi H, Seike M, Yoshimatsu H (2004) Adiponectin protects LPS-induced liver injury through modulation of TNF-alpha in KK-Ay obese mice. Hepatology 40:177–184

    Article  CAS  PubMed  Google Scholar 

  22. Kumada M, Kihara S, Ouchi N, Kobayashi H, Okamoto Y, Ohashi K, Maeda K, Nagaretani H, Kishida K, Maeda N, Nagasawa A, Funahashi T, Matsuzawa Y (2004) Adiponectin specifically increased tissue inhibitor of metalloproteinase-1 through interleukin-10 expression in human macrophages. Circulation 109:2046–2049

    Article  CAS  PubMed  Google Scholar 

  23. Wolff B, Cieza A, Parentin A, Rauch A, Sigl T, Brockow T, Stucki A (2004) Identifying the concepts contained in outcome measures of clinical trials on four internal disorders using the International Classification of Functioning, Disability and Health as a reference. J Rehabil Med 44(Suppl):37–42

    Article  PubMed  Google Scholar 

  24. Wulster-Radcliffe MC, Ajuwon KM, Wang J, Christian JA, Spurlock ME (2004) Adiponectin differentially regultes cytocines in porcine macrophages. Biochem Biophys Res Commun 316:37–42

    Article  Google Scholar 

  25. Shore SA, Terry RD, Flynt L, Xu A, Hug C (2006) Adiponectin attenuates allergen-induced airway inflammation and hyperresponsiveness in mice. J Allergy Clin Immunol 118:389–395

    Article  CAS  PubMed  Google Scholar 

  26. Medoff BD, Okamoto Y, Leyton P, Weng M, Sandall BP, Raher MJ, Kihara S, Bloch KD, Libby P, Luster AD (2009) Adiponectin deficiency increases allergic airway inflammation and pulmonary vascular remodeling. Am J Respir Cell Mol Biol 41:397–406

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Lugogo NL, Bappanad D, Kraft M (2011) Obesity, metabolic dysregulation and oxidative stress in asthma. Biochim Biophys Acta 1810:1120–1126

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Sood A, Cui X, Qualls C, Beckett WS, Gross MD, Steffes MW, Smith LJ, Jacobs DR (2008) Association between asthma and serum adiponectin concentration in women. Thorax 63:877–882

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Sood A, Qualls C, Schuyler M, Thyagarajan B, Steffes MW, Smith LJ, Jacobs DR (2012) Low serum Adiponectin predicts future risk for asthma in women. Am J Respir Crit Care Med 186:41–47

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Sood A, Dominic E, Qualls C, Steffes MW, Thyagarajan B, Smith LJ, Lewis CE, Jacobs DR (2011) Serum adiponectin is associated with adverse outcomes of asthma in men but not in women. Front Pharmacol 2:1–11

    Article  Google Scholar 

  31. Salome CM, King GG, Berend N (2010) Physiology of obesity and effects on lung function. J Appl Physiol (1985) 108:206–211

    Article  Google Scholar 

  32. Ghabashi AE, Iqbal M (2006) Obesity and its correlation with spirometric variables in patients with asthma. MedGenMed 8:58

    PubMed Central  PubMed  Google Scholar 

  33. Lécart S, Lecointe N, Subramaniam A, Alkan S, Ni D, Chen R, Boulay V, Pène J, Kuroiwa K, Tominaga S, Yssel H (2002) Activated, but not resting human Th2 cells, in contrast to Th1 and T regulatory cells, produce soluble ST2 and express low levels of ST2L at the cell surface. Eur J Immunol 32:2979–2987

    Article  PubMed  Google Scholar 

  34. Moussion C, Ortega N, Girard JP (2008) The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel “alarmin”? PLoS ONE 3:e3331

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, CEP 20551-030, Brazil

    Renato de Lima Azambuja, Layla Salomao Eulalio da Costa Santos Azambuja, Cláudia Costa & Rogério Rufino

  2. Pulmonology Department, Hospital Universitário Pedro Ernesto, Avenida 28 de Setembro, 77, Rio de Janeiro, RJ, CEP 20551-030, Brazil

    Rogério Rufino

Authors
  1. Renato de Lima Azambuja
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Layla Salomao Eulalio da Costa Santos Azambuja
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cláudia Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rogério Rufino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rogério Rufino.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Lima Azambuja, R., da Costa Santos Azambuja, L.S.E., Costa, C. et al. Adiponectin in Asthma and Obesity: Protective Agent or Risk Factor for More Severe Disease?. Lung 193, 749–755 (2015). https://doi.org/10.1007/s00408-015-9793-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00408-015-9793-8

Keywords

Search

Navigation