The effect of combined resistance aerobic exercise training on concentrations of asprosin and complement C1q tumor necrosis factor-related protein-1 in men with type 2 diabetes

Abstract

Aim

The present study aimed to investigate the effect of combined resistance aerobic exercise training on asprosin and complement C1q tumor necrosis factor-related protein-1 concentrations in men with type 2 diabetes.

Methods

Twenty four male patients with type 2 diabetes were randomized to two combined resistance aerobic exercise training group (n = 12) and control group (n = 12). The combined resistance aerobic exercise training was performed within three sessions per week for 12 weeks. Anthropometric measurements and blood samples were collected at baseline and after 12 weeks. Analysis of covariance was used to compare changes between the groups with pre-test values as covariates.

Results

After 12 weeks, asprosin concentration (p = 0.04), resistance insulin (p = 0.01), HbA1c (p = 0.001), fasting glucose (p = 0.01), weight (p = 0.04), body mass index (0.03), body fat percentage (0.001), total cholesterol (p = 0.04), Triglycerides (p = 0.03) significantly decreased in the exercise group compared to the control group. Significant changes were not observed at the complement C1q tumor necrosis factor-related protein-1 concentration (p = 0.52), WHR (p = 0.29), high-density lipoprotein cholesterol (p = 0.85), low-density lipoprotein cholesterol (p = 0.12), and fat free mass (p = 0.98) between the groups. After 12 weeks in the combined exercise group, low-density lipoprotein cholesterol (p = 0.007) decreased and high-density lipoprotein cholesterol (p = 0.01) increased significantly compared with the baseline. There was a significant positive correlation between asprosin changes with HbA1c(r = 0.44, p = 0.02) and resistance insulin (r = 0.43, p = 0.03) changes.

Conclusion

These findings suggest that combined resistance aerobic exercise training effectively decreases asprosin concentration and improves glycemic control in male patients with type 2 diabetes; however, it has no effect on complement C1q tumor necrosis factor-related protein-1 concentrations.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

Data accessibility

The data and materials used and/or analyzed in the current study are available from the corresponding author, upon reasonable request.

References

  1. 1.

    Association AD (2018) Classification and diagnosis of diabetes: standards of medical care in diabetes—2018. Diabetes Care 41 (Supplement 1):S13-S27

  2. 2.

    Liang W, dong Ye D (2019) The potential of adipokines as biomarkers and therapeutic agents for vascular complications in type 2 diabetes mellitus. Cytokine Growth Factor Rev

  3. 3.

    Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, Chasan-Taber L, Albright AL, Braun B (2010) Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement. Diabetes Care 33(12):e147–e167

    PubMed  PubMed Central  Article  Google Scholar 

  4. 4.

    Stefanyk LE, Dyck DJ (2010) The interaction between adipokines, diet and exercise on muscle insulin sensitivity. Curr Opin Clin Nutr Metab Care 13(3):255–259

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Berggren JR, Hulver MW, Houmard JA (2005) Fat as an endocrine organ: influence of exercise. J Appl Physiol 99(2):757–764

    CAS  PubMed  Article  Google Scholar 

  6. 6.

    Han S, Kim JD, Lee S, Jeong AL, Park JS, Yong HJ, Boldbaatar A, Ka HI, Rhee E-J, Lee W-Y (2016) Circulating CTRP1 levels in type 2 diabetes and their association with FGF21. Int J Endocrinol. 2016

  7. 7.

    Romere C, Duerrschmid C, Bournat J, Constable P, Jain M, Xia F, Saha PK, Del Solar M, Zhu B, York B (2016) Asprosin, a fasting-induced glucogenic protein hormone. Cell 165(3):566–579

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 8.

    Zhang X, Jiang H, Ma X, Wu H (2019) Increased serum level and impaired response to glucose fluctuation of asprosin is associated with type 2 diabetes mellitus. J Diabetes Invest

  9. 9.

    Duerrschmid C, He Y, Wang C, Li C, Bournat JC, Romere C, Saha PK, Lee ME, Phillips KJ, Jain M (2017) Asprosin is a centrally acting orexigenic hormone. Nat Med 23(12):1444

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Hosseini ZS, Heydari-Zarnagh H, Behmanesh M, Miri M (2020) Maternal exposure to air pollution and umbilical asprosin concentration, a novel insulin-resistant marker. Chemosphere:129228

  11. 11.

    Wang Y, Qu H, Xiong X, Qiu Y, Liao Y, Chen Y, Zheng Y, Zheng H (2018) Plasma asprosin concentrations are increased in individuals with glucose dysregulation and correlated with insulin resistance and first-phase insulin secretion. Med Inflam 2018

  12. 12.

    Li X, Liao M, Shen R, Zhang L, Hu H, Wu J, Wang X, Qu H, Guo S, Long M (2018) Plasma asprosin levels are associated with glucose metabolism, lipid, and sex hormone profiles in females with metabolic-related diseases. Med Inflam 2018

  13. 13.

    Yuan M, Li W, Zhu Y, Yu B, Wu J (2020) Asprosin: a novel player in metabolic diseases. Front Endocrinol 11:64

    Article  Google Scholar 

  14. 14.

    Zhang L, Chen C, Zhou N, Fu Y, Cheng X (2019) Circulating asprosin concentrations are increased in type 2 diabetes mellitus and independently associated with fasting glucose and triglyceride. Clin Chim Acta 489:183–188

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Naiemian S, Naeemipour M, Zarei M, Najafi ML, Gohari A, Behroozikhah MR, Heydari H, Miri M (2020) Serum concentration of asprosin in new-onset type 2 diabetes. Diabetol Metab Synd 12(1):1–8

    Article  Google Scholar 

  16. 16.

    Xin Y, Lyu X, Wang C, Fu Y, Zhang S, Tian C, Li Q, Zhang D (2014) Elevated circulating levels of CTRP1, a novel adipokine, in diabetic patients. Endocr J 61(9):841–847

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Xin Y, Zhang D, Fu Y, Wang C, Li Q, Tian C, Zhang S, Lyu X (2017) C1qtnf-related protein 1 improve insulin resistance by reducing phosphorylation of serine 1101 in insulin receptor substrate 1. Endocr J:EJ17–0128

  18. 18.

    Peterson JM, Aja S, Wei Z, Wong GW (2012) CTRP1 protein enhances fatty acid oxidation via AMP-activated protein kinase (AMPK) activation and acetyl-CoA carboxylase (ACC) inhibition. J Biol Chem 287(2):1576–1587

    CAS  PubMed  Article  Google Scholar 

  19. 19.

    Seldin MM, Tan SY, Wong GW (2014) Metabolic function of the CTRP family of hormones. Rev Endoc Metab Dis 15(2):111–123

    CAS  Article  Google Scholar 

  20. 20.

    Han S, Park JS, Lee S, Jeong AL, Oh KS, Ka HI, Choi H-J, Son W-C, Lee W-Y, Oh SJ (2016) CTRP1 protects against diet-induced hyperglycemia by enhancing glycolysis and fatty acid oxidation. J Nutri Biochem 27:43–52

    CAS  Article  Google Scholar 

  21. 21.

    Pan X, Lu T, Wu F, Jin L, Zhang Y, Shi L, Li X, Lin Z (2014) Circulating complement-C1q TNF-related protein 1 levels are increased in patients with type 2 diabetes and are associated with insulin sensitivity in Chinese subjects. PLoS One 9 (5)

  22. 22.

    Rodriguez S, Lei X, Petersen PS, Tan SY, Little HC, Wong GW (2016) Loss of CTRP1 disrupts glucose and lipid homeostasis. Am J Physiol Endocrinol Metab 311(4):E678–E697

    PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Han S, Yang Y (2018) A novel blood pressure modulator C1q/TNF-α–related protein 1 (CTRP1). BMB Rep 51(12):611

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. 24.

    Yagmur E, Buergerhausen D, Koek GH, Weiskirchen R, Trautwein C, Koch A, Tacke F (2019) Elevated CTRP1 plasma concentration is associated with sepsis and pre-existing type 2 diabetes mellitus in critically Ill patients. J Clin Med 8(5):661

    CAS  PubMed Central  Article  Google Scholar 

  25. 25.

    Colberg SR, Sigal RJ, Yardley JE, Riddell MC, Dunstan DW, Dempsey PC, Horton ES, Castorino K, Tate DF (2016) Physical activity/exercise and diabetes: a position statement of the American Diabetes Association. Diabetes Care 39(11):2065–2079

    PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Hansen D, Peeters S, Zwaenepoel B, Verleyen D, Wittebrood C, Timmerman N, Schotte M (2013) Exercise assessment and prescription in patients with type 2 diabetes in the private and home care setting: clinical recommendations from AXXON (Belgian Physical Therapy Association). Phys Ther 93(5):597–610

    PubMed  Article  Google Scholar 

  27. 27.

    Hordern MD, Dunstan DW, Prins JB, Baker MK, Singh MAF, Coombes JS (2012) Exercise prescription for patients with type 2 diabetes and pre-diabetes: a position statement from Exercise and Sport Science Australia. J Sci Med Sport 15(1):25–31

    PubMed  Article  Google Scholar 

  28. 28.

    Brzycki M (1993) Strength testing—predicting a one-rep max from reps-to-fatigue. J Phys Educ Recreat Dance 64(1):88–90

    Article  Google Scholar 

  29. 29.

    Sigal RJ, Armstrong MJ, Bacon SL, Boule NG, Dasgupta K, Kenny GP, Riddell MC (2018) Physical activity and diabetes. Can J Diabetes 42:S54–S63

    PubMed  Article  Google Scholar 

  30. 30.

    AminiLari Z, Fararouei M, Amanat S, Sinaei E, Dianatinasab S, AminiLari M, Daneshi N, Dianatinasab M (2017) The effect of 12 weeks aerobic, resistance, and combined exercises on omentin-1 levels and insulin resistance among type 2 diabetic middle-aged women. Diabetes Metab J 41(3):205–212

    PubMed  PubMed Central  Article  Google Scholar 

  31. 31.

    Jorge MLMP, de Oliveira VN, Resende NM, Paraiso LF, Calixto A, Diniz ALD, Resende ES, Ropelle ER, Carvalheira JB, Espindola FS (2011) The effects of aerobic, resistance, and combined exercise on metabolic control, inflammatory markers, adipocytokines, and muscle insulin signaling in patients with type 2 diabetes mellitus. Metabolism 60(9):1244–1252

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Church TS, Blair SN, Cocreham S, Johannsen N, Johnson W, Kramer K, Mikus CR, Myers V, Nauta M, Rodarte RQ (2010) Effects of aerobic and resistance training on hemoglobin A1c levels in patients with type 2 diabetes: a randomized controlled trial. JAMA 304(20):2253–2262

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. 33.

    Greenhill C (2016) Liver: asprosin—new hormone involved in hepatic glucose release. Nat Rev Endocrinol 12(6):312

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Ko JR, Seo DY, Kim TN, Park SH, Kwak H-B, Ko KS, Rhee BD, Han J (2019) Aerobic exercise training decreases hepatic asprosin in diabetic rats. J Clin Med 8(5):666

    CAS  PubMed Central  Article  Google Scholar 

  35. 35.

    Nakhaei H, Mogharnasi M, Fanaei H (2019) Effect of swimming training on levels of asprosin, lipid profile, glucose and insulin resistance in rats with metabolic syndrome. Obes Med 15:100111

    Article  Google Scholar 

  36. 36.

    Kajimura S (2017) Advances in the understanding of adipose tissue biology. Nat Rev Endocrinol 13(2):69–70

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. 37.

    Salminen A, Kaarniranta K, Kauppinen A (2016) Age-related changes in AMPK activation: role for AMPK phosphatases and inhibitory phosphorylation by upstream signaling pathways. Age Res Rev 28:15–26

    CAS  Article  Google Scholar 

  38. 38.

    Ferretti AC, Tonucci FM, Hidalgo F, Almada E, Larocca MC, Favre C (2016) AMPK and PKA interaction in the regulation of survival of liver cancer cells subjected to glucose starvation. Oncotarget 7(14):17815

    PubMed  PubMed Central  Article  Google Scholar 

  39. 39.

    Wang M, Yin C, Wang L, Liu Y, Li H, Li M, Yi X, Xiao Y (2019) Serum asprosin concentrations are increased and associated with insulin resistance in children with obesity. Ann Nutr Metab 75(4):205–212

    CAS  PubMed  Article  Google Scholar 

  40. 40.

    Wiecek M, Szymura J, Maciejczyk M, Kantorowicz M, Szygula Z (2018) Acute anaerobic exercise affects the secretion of Asprosin, Irisin, and other cytokines–a comparison between sexes. Front Physiol 9:1782

    PubMed  PubMed Central  Article  Google Scholar 

  41. 41.

    Schumann U, Qiu S, Enders K, Bosnyák E, Laszlo R, Machus K, Trájer E, Jaganathan S, Zügel M, Steinacker J (2017) Asprosin, a newly identified fasting-induced hormone is not elevated in obesity and is insensitive to acute exercise: 3592 board #39 June 3 8. Med Sci Sports Exerc 49:1023. https://doi.org/10.1249/01.mss.0000519807.24061.ca

    Article  Google Scholar 

  42. 42.

    Schäffler A, Buechler C (2012) CTRP family: linking immunity to metabolism. Trends Endocrinol Metab 23(4):194–204

    PubMed  Article  Google Scholar 

  43. 43.

    Shabani P, Emamgholipour S, Doosti M (2017) CTRP1 in liver disease. In: Advances in clinical chemistry, vol 79. Elsevier, pp 1–23

  44. 44.

    Kon M, Ebi Y, Nakagaki K (2019) Effects of a single bout of high-intensity interval exercise on C1q/TNF-related proteins. Appl Physiol Nutr Metab 44(1):47–51

    CAS  PubMed  Article  Google Scholar 

  45. 45.

    Kim KY, Kim HY, Kim JH, Lee CH, Kim DH, Lee YH, Han SH, Lim JS, Cho DH, Lee MS, Yoon S, Kim KI, Yoon DY, Yang Y (2006) Tumor necrosis factor-alpha and interleukin-1beta increases CTRP1 expression in adipose tissue. FEBS Lett 580(16):3953–3960. https://doi.org/10.1016/j.febslet.2006.06.034

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    Kadoglou NP, Iliadis F, Angelopoulou N, Perrea D, Ampatzidis G, Liapis CD, Alevizos M (2007) The anti-inflammatory effects of exercise training in patients with type 2 diabetes mellitus. Eur J Cardiovascu Prevent Rehabilit 14(6):837–843

    Article  Google Scholar 

  47. 47.

    Melo L, Dativo-Medeiros J, Menezes-Silva C, Barbosa F, Sousa-Rodrigues C, Rabelo L (2017) Physical exercise on inflammatory markers in type 2 diabetes patients: a systematic review of randomized controlled trials. Oxidat Med Cell Long 2017:1–10. https://doi.org/10.1155/2017/8523728

    Article  Google Scholar 

Download references

Acknowledgements

Thanks are owed to the patients and volunteers participated in this study.

Funding

The present study was financially supported by University of Neyshabur, Iran.

Author information

Affiliations

Authors

Contributions

All authors contributed to subject recruitment, data collection, review, and discussion of the trial report, and review and discussion of the manuscript.

Corresponding author

Correspondence to Mehdi Zarei.

Ethics declarations

Conflict of interest

The study authors declare no conflict of interest.

Ethical approval

The study protocol was carried out in compliance with the Declaration of Helsinki and was approved by the Ethics Committee of Sabzevar University of Medical Sciences and registered number IRCT20181006041252N15 in Iranian Registry of Clinical Trials (Primary Registry in the WHO Registry Network).

Informed consent

Written informed consent was obtained from all volunteers.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zarei, M., Nakhzari Khodakheyr, J., Rashidlamir, A. et al. The effect of combined resistance aerobic exercise training on concentrations of asprosin and complement C1q tumor necrosis factor-related protein-1 in men with type 2 diabetes. Sport Sci Health (2021). https://doi.org/10.1007/s11332-021-00738-7

Download citation

Keywords

  • Exercise
  • Asprosin protein
  • C1QTNF1 protein
  • Type 2 diabetes