Skip to main content

Advertisement

SpringerLink
Log in

Serum salusin-β levels in patients with systemic lupus erythematosus

  • ORIGINAL ARTICLE
  • Published:
Clinical Rheumatology Aims and scope Submit manuscript

Abstract

Objective

Endothelial dysfunction (ED) has an important role in the pathogenesis of systemic lupus erythematosus (SLE). Studies on other inflammatory diseases show that salusin-β with various mechanisms may play a role in the promotion of ED and inflammation. The aim of this study was to measure serum salusin-β levels in SLE patients and evaluate it as a potential biomarker in assessing SLE activity and predicting organ involvement.

Methods

In a cross-sectional study, 60 patients diagnosed with SLE and 30 age- and sex-matched healthy controls were enrolled. Disease activity of SLE patients was assessed by the systemic lupus erythematosus disease activity index 2000 (SLEDAI-2 K). Serum levels of salusin-ß were measured using a human salusin-ß enzyme-linked immunosorbent assay kit.

Results

Serum salusin-β levels in SLE and control groups were 474.2 ± 117.1 pg/ml and 157.7 ± 88.7 pg/ml, respectively. The difference was significant (P = 0.001). There was no significant correlation between serum salusin-β levels with age (r =  − 0.06, P = 0.632) and SLEDAI (r =  − 0.185, P = 0.158). In patients with nephritis and thrombosis, serum salusin-β was significantly higher. In addition, in patients with serositis, serum salusin-β was significantly lower. Multiple linear regression analysis showed that serum salusin-β levels retained a significant association with nephritis and thrombosis after model adjustment for serositis, nephritis, and thrombosis.

Conclusions

Our findings showed that salusin-β might have a possible role in the pathogenesis of SLE. Salusin-β may be a potential biomarker for nephritis and thrombosis in SLE.

Key Points

• Serum salusin-β levels were significantly higher in SLE patients than the control group.

• There was no significant correlation between serum salusin-β levels with age and SLEDAI.

• Serum salusin-β levels retained a significant association with nephritis and thrombosis.

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

Similar content being viewed by others

Data availability

The datasets used during the current study are available from the corresponding author on reasonable request.

References

  1. Pisetsky DS (2020) Evolving story of autoantibodies in systemic lupus erythematosus. J Autoimmun 110:102356

    Article  CAS  PubMed  Google Scholar 

  2. Arnaud L, Tektonidou MG (2020) Long-term outcomes in systemic lupus erythematosus: trends over time and major contributors. Rheumatology (Oxford) 59(Suppl5):v29–v38

    Article  CAS  PubMed  Google Scholar 

  3. Shen Y, Qu B, Shen N (2022) Expanding roles of noncoding RNAs in the pathogenesis of systemic lupus erythematosus. Curr Rheumatol Rep 24(3):64–75

    Article  CAS  PubMed  Google Scholar 

  4. Yu H, Nagafuchi Y, Fujio K (2021) Clinical and immunological biomarkers for systemic lupus erythematosus. Biomolecules 11(7):928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Mak A, Kow NY, Schwarz H, Gong L, Tay SH, Ling LH (2017) Endothelial dysfunction in systemic lupus erythematosus – a case-control study and an updated meta-analysis and meta-regression. Sci Rep 7(1):7320

    Article  PubMed  PubMed Central  Google Scholar 

  6. Taraborelli M, Sciatti E, Bonadei I, Terlizzi V, Fredi M, Zani R, Cancarini G, Tincani A, Franceschini F, Vizzardi E, Cavazzana I (2018) Endothelial dysfunction in early systemic lupus erythematosus patients and controls without previous cardiovascular events. Arthritis Care Res (Hoboken) 70(9):1277–1283

    Article  CAS  PubMed  Google Scholar 

  7. Ozelius LJ, Page CE, Klein C, Hewett JW, Mineta M, Leung J, Shalish C, Bressman SB, de Leon D, Brin MF, Fahn S, Corey DP, Breakefield XO (1999) The TOR1A (DYT1) gene family and its role in early onset torsion dystonia. Genomics 62(3):377–384

    Article  CAS  PubMed  Google Scholar 

  8. Shichiri M, Ishimaru S, Ota T, Nishikawa T, Isogai T, Hirata Y (2003) Salusins: newly identified bioactive peptides with hemodynamic and mitogenic activities. Nat Med 9(9):1166–1172

    Article  CAS  PubMed  Google Scholar 

  9. Sato K, Watanabe R, Itoh F, Shichiri M, Watanabe T (2013) Salusins: potential use as a biomarker for atherosclerotic cardiovascular diseases. Int J Hypertens 2013:965140

    Article  PubMed  PubMed Central  Google Scholar 

  10. Erden I, Demir B, Uçak H, Cicek D, Dertlioğlu SB, Aydin S (2014) Serum salusin-α and salusin-β levels in patients with Behcet’s disease. Eur J Dermatol 24(5):577–582

    Article  PubMed  Google Scholar 

  11. Ozgen M, Koca SS, Dagli N, Balin M, Ustundag B, Isik A (2011) Serum salusin-alpha level in rheumatoid arthritis. Regul Pept 167(1):125–128

    Article  CAS  PubMed  Google Scholar 

  12. Koca SS, Özgen M, Işık B, Dağlı MN, Üstündağ B, Işık A (2014) Serum salusin-α levels in systemic lupus erythematosus and systemic sclerosis. Eur J Rheumatol 1(1):14–17

    Article  PubMed  PubMed Central  Google Scholar 

  13. Nowaczyk J, Blicharz L, Zawistowski M, Sikora M, Zaremba M, Czuwara J, Rudnicka L (2023) The clinical significance of salusins in systemic sclerosis-a cross-sectional study. Diagnostics (Basel) 13(5):848

    Article  PubMed  Google Scholar 

  14. Kobak S, Atabay T, Akyildiz M, Gokduman A, Vural H (2022) Serum salusin-α and salusin-β levels in patients with psoriatic arthritis. Reumatologia 60(5):306–310

    Article  PubMed  PubMed Central  Google Scholar 

  15. Aringer M, Costenbader K, Daikh D, Brinks R, Mosca M, Ramsey-Goldman R, Smolen JS, Wofsy D, Boumpas DT, Kamen DL, Jayne D, Cervera R, Costedoat-Chalumeau N, Diamond B, Gladman DD, Hahn B, Hiepe F, Jacobsen S, Khanna D, Lerstrøm K, Massarotti E, McCune J, Ruiz-Irastorza G, Sanchez-Guerrero J, Schneider M, Urowitz M, Bertsias G, Hoyer BF, Leuchten N, Tani C, Tedeschi SK, Touma Z, Schmajuk G, Anic B, Assan F, Chan TM, Clarke AE, Crow MK, Czirják L, Doria A, Graninger W, Halda-Kiss B, Hasni S, Izmirly PM, Jung M, Kumánovics G, Mariette X, Padjen I, Pego-Reigosa JM, Romero-Diaz J, Rúa-Figueroa Fernández Í, Seror R, Stummvoll GH, Tanaka Y, Tektonidou MG, Vasconcelos C, Vital EM, Wallace DJ, Yavuz S, Meroni PL, Fritzler MJ, Naden R, Dörner T, Johnson SR (2019) 2019 European League Against Rheumatism/American College of Rheumatology Classification Criteria for Systemic Lupus Erythematosus. Arthritis Rheumatol 71(9):1400–1412

    Article  PubMed  PubMed Central  Google Scholar 

  16. Gladman DD, Ibanez D, Urowitz MB (2002) Systemic lupus erythematosus disease activity index 2000. J Rheumatol 29(2):288–291

    PubMed  Google Scholar 

  17. Sato K, Fujimoto K, Koyama T, Shichiri M (2010) Release of salusin-beta from human monocytes/macrophages. Regul Pept 162(1–3):68–72

    Article  CAS  PubMed  Google Scholar 

  18. Sato K, Sato T, Susumu T, Koyama T, Shichiri M (2009) Presence of immunoreactive salusin-beta in human plasma and urine. Regul Pept 158(1–3):63–67

    Article  CAS  PubMed  Google Scholar 

  19. Izumiyama H, Tanaka H, Egi K, Sunamori M, Hirata Y, Shichiri M (2005) Synthetic salusins as cardiac depressors in rat. Hypertension 45(3):419–425

    Article  CAS  PubMed  Google Scholar 

  20. Sun HJ, Liu TY, Zhang F, Xiong XQ, Wang JJ, Chen Q, Li YH, Kang YM, Zhou YB, Han Y, Gao XY, Zhu GQ (2015) Salusin- β contributes to vascular remodeling associated with hypertension via promoting vascular smooth muscle cell proliferation and vascular fibrosis. Biochim Biophys Acta 1852(9):1709–1718

    Article  CAS  PubMed  Google Scholar 

  21. Fujimoto K, Hayashi A, Kamata Y, Ogawa A, Watanabe T, Ichikawa R, Iso Y, Koba S, Kobayashi Y, Koyama T, Shichiri M (2013) Circulating levels of human salusin-β, a potent hemodynamic and atherogenesis regulator. PLoS One 8(10):e76714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Wang Y, Wang S, Zhang J, Zhang M, Zhang H, Gong G, Luo M, Wang T, Mao X (2020) Salusin- β is superior to salusin-α as a marker for evaluating coronary atherosclerosis. J Int Med Res 48(2):300060520903868

    Article  CAS  PubMed  Google Scholar 

  23. Koya T, Miyazaki T, Watanabe T, Shichiri M, Atsumi T, Kim-Kaneyama JR, Miyazaki A (2012) Salusin-β accelerates inflammatory responses in vascular endothelial cells via NF-κB signaling in LDL receptor-deficient mice in vivo and HUVECs in vitro. Am J Physiol Heart Circ Physiol 303(1):H96-105

    Article  CAS  PubMed  Google Scholar 

  24. Gabay C, Cakir N, Moral F, Roux-Lombard P, Meyer O, Dayer JM, Vischer T, Yazici H, Guerne PA (1997) Circulating levels of tumor necrosis factor soluble receptors in systemic lupus erythematosus are significantly higher than in other rheumatic diseases and correlate with disease activity. J Rheumatol 24(2):303–308

    CAS  PubMed  Google Scholar 

  25. Chen H, Jin G (2021) Downregulation of salusin-β protects renal tubular epithelial cells against high glucose-induced inflammation, oxidative stress, apoptosis and lipid accumulation via suppressing miR-155-5p. Bioengineered 12(1):6155–6165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. de Groot PG, de Laat B (2017) Mechanisms of thrombosis in systemic lupus erythematosus and antiphospholipid syndrome. Best Pract Res Clin Rheumatol 31(3):334–341

    Article  PubMed  Google Scholar 

  27. Lu QB, Du Q, Wang HP, Tang ZH, Wang YB, Sun HJ (2020) Salusin-β mediates tubular cell apoptosis in acute kidney injury: involvement of the PKC/ROS signaling pathway. Redox Biol 30:101411

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research was funded by the Connective Tissue Diseases Research Center of Tabriz University of Medical Sciences, Tabriz, Iran (Grant No. 63897).

Author information

Authors and Affiliations

  1. Connective Tissue Diseases Research Center, Tabriz University of Medical Sciences, Golgasht St, P.O Box 5166614756, Tabriz, Iran

    Mehrzad Hajialilo, Razieh Jorjani, Mehran Rahimi, Aida Malek Mahdavi & Alireza Khabbazi

  2. Biotechnology Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

    Amir Ghorbanihaghjo

  3. Tuberculosis and Lung Disease Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

    Aida Malek Mahdavi

  4. Rahat Breathe and Sleep Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

    Aida Malek Mahdavi

  5. Research Center for Evidence-Based Medicine, A Joanna Briggs Institute Affiliated Group, Health Management and Safety Promotion Research Institute, Tabriz University of Medical Sciences, Tabriz, Iran

    Morteza Ghojazadeh

Authors
  1. Mehrzad Hajialilo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Razieh Jorjani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mehran Rahimi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amir Ghorbanihaghjo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aida Malek Mahdavi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Morteza Ghojazadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alireza Khabbazi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MH, RJ, and AKH designed the study; MH, RJ, MR, AG, and AKH were involved in the data acquisition and/or management; AMM, MG, and AKH analyzed the data and critically interpreted the results; MR, AMM, and AKH were involved in drafting the manuscript. All authors revised the manuscript critically for important intellectual content and approved the final manuscript.

Corresponding author

Correspondence to Alireza Khabbazi.

Ethics declarations

Disclosures

None.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hajialilo, M., Jorjani, R., Rahimi, M. et al. Serum salusin-β levels in patients with systemic lupus erythematosus. Clin Rheumatol 42, 2097–2103 (2023). https://doi.org/10.1007/s10067-023-06610-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-023-06610-y

Keywords

Search

Navigation