Skip to main content

Advertisement

SpringerLink
Log in

The influence of ICAM1 rs5498 on diabetes mellitus risk: evidence from a meta-analysis

  • Original Research Paper
  • Published:
Inflammation Research Aims and scope Submit manuscript

Abstract

Objectives

Both type 1 diabetes (T1D) and type 2 diabetes (T2D) are classified as forms of diabetes mellitus (DM) and commonly considered inflammatory process. Intercellular adhesion molecule-1 (ICAM-1) is involved in the development and progression of diabetes mellitus. However, the genetic association between ICAM-1 rs5498, and T1D and T2D risk was inconclusive.

Materials and methods

A meta-analysis by searching the PubMed, Embase, Cochrane Library, and Chinese National Knowledge Infrastructure (CNKI) databases was performed out. The pooled odds ratio (OR) and 95% confidence interval (CI) were used to describe the strength of association of T1D and T2D risk.

Results

A total of 14 studies encompassing 3233 cases and 2884 controls were included in the present meta-analysis. Significant associations were found between the allele and recessive models of ICAM1 rs5498 and DM in Asian population (allele: OR 1.13; 95% CI 1.03–1.23, p = 0.008; recessive: OR 1.25; 95% CI 1.06–1.48, p = 0.008), but not in Caucasian population (p > 0.05). In addition, the allele model of rs5498 was found to be significantly associated with the increased risk of T2D (OR 1.10; 95% CI 1.01–1.21, p = 0.03), but not T1D (p > 0.05).

Conclusions

The ICAM1 rs5498 might be a susceptible factor for T2D, but not T1D. And the allele and recessive models of ICAM1 rs5498 might be a risk factor in Asian population.

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

Similar content being viewed by others

References

  1. Wong YCP. Need of integrated dietary therapy for persons with diabetes mellitus and “unhealthy” body constitution presentations. J Integr Med. 2016;14(4):255–68.

    Article  PubMed  Google Scholar 

  2. Chakraborty R, Roy S, Mandal V. Assessment of traditional knowledge of the antidiabetic plants of Darjeeling and Sikkim Himalayas in the context of recent phytochemical and pharmacological advances. J Integr Med. 2016;14(5):336–58.

    Article  PubMed  Google Scholar 

  3. Francés DE, Ingaramo PI, Ronco MT, Carnovale CE. Diabetes, an inflammatory process: oxidative stress and TNF-alpha involved in hepatic complication. J Biomed Sci Eng. 2013;06(6):645–53.

    Article  CAS  Google Scholar 

  4. Cho NH, Shaw JE, Karuranga S, Huang Y, da Rocha Fernandes JD, Ohlrogge AW, et al. IDF diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract. 2018;138:271–81.

    Article  PubMed  CAS  Google Scholar 

  5. Cade WT. Diabetes related microvascular and macrovascular diseases in the physical therapy setting. Phys Ther. 2008;88(11):1322–35.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Staeva-Vieira T, Peakman M. Von Herrath M. Translational mini-review series on type 1 diabetes: immune-based therapeutic approaches for type 1 diabetes. Clin Exp Immunol. 2010;148(1):17–31.

    Article  Google Scholar 

  7. Wu H, Deng X, Shi Y, Su Y, Wei J, Duan H. PGC-1α, glucose metabolism and type 2 diabetes mellitus. J Endocrinol. 2016;229(3):R99–115.

    Article  PubMed  CAS  Google Scholar 

  8. Laaksonen DE, Lakka HM, Niskanen LK, Kaplan GA, Salonen JT, Lakka TA. Metabolic syndrome and development of diabetes mellitus: application and validation of recently suggested definitions of the metabolic syndrome in a prospective cohort study. Am J Epidemiol. 2002;156(11):1070–77.

    Article  PubMed  Google Scholar 

  9. De Ferranti SD, Osganian SK. Epidemiology of paediatric metabolic syndrome and type 2 diabetes mellitus. Diabetes Vasc Dis Res. 2007;4(4):285–96.

    Article  Google Scholar 

  10. Åkerblom HK, Knip M, Hyöty H, Reijonen H, Virtanen S, Savilahti E, et al. Interaction of genetic and environmental factors in the pathogenesis of insulin-dependent diabetes mellitus. Clin Chim Acta. 1997;257(2):143–56.

    Article  PubMed  Google Scholar 

  11. Jae-Bung K, Mi-Hwa J, Je-Yeol C, Park JW, Suh JY, Lee JM. The influence of type 2 diabetes mellitus on the expression of inflammatory mediators and tissue inhibitor of metalloproteinases-2 in human chronic periodontitis. J Periodontal Implant Sci. 2011;41(3):109–16.

    Article  CAS  Google Scholar 

  12. Kolseth IBM, Reine TM, Parker K, Sudworth A, Witczak BJ, Jenssen TG, et al. Increased levels of inflammatory mediators and proinflammatory monocytes in patients with type I diabetes mellitus and nephropathy. J Diabetes Complic. 2017;31(1):245–52.

    Article  Google Scholar 

  13. Odawara M, Yamashita K. Genetic vs environmental factors in insulin-dependent diabetes mellitus. Lancet. 1997;349:956.

    Article  PubMed  CAS  Google Scholar 

  14. Lontchi-Yimagou E, Sobngwi E, Matsha TE, Kengne AP. Diabetes mellitus and inflammation. Curr Diabetes Rep. 2013;13(3):435–44.

    Article  CAS  Google Scholar 

  15. Wallet MA, Tisch R. Type 1 diabetes, inflammation and dendritic cells. Drug Discov Today Dis Mech. 2007;3(3):373–79.

    Article  Google Scholar 

  16. Bending D, Zaccone P, Cooke A. Inflammation and type one diabetes. Int Immunol. 2012;24(6):339–46.

    Article  PubMed  CAS  Google Scholar 

  17. Odegaard AO, Jacobs DR Jr, Sanchez OA, Goff DC Jr, Reiner AP, Gross MD. Oxidative stress, inflammation, endothelial dysfunction and incidence of type 2 diabetes. Cardiovasc Diabetol. 2016;15(51):1–12.

    Google Scholar 

  18. Esposito K, Nappo F, Marfella R, Giugliano G, Giugliano F, Ciotola M, et al. Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans. Circulation. 2002;106(16):2067–72.

    Article  PubMed  CAS  Google Scholar 

  19. Foss NT, Foss-Freitas MC, Ferreira MA, Cardili RN, Barbosa CM, Foss MC. Impaired cytokine production by peripheral blood mononuclear cells in type 1 diabetic patients. Diabetes Metab. 2007;33(6):439–43.

    Article  PubMed  CAS  Google Scholar 

  20. Navarro-GonzÃlez JF, Muros M, Mora-FernÃndez C, Herrera H, Meneses B, García J. Pentoxifylline for renoprotection in diabetic nephropathy: the PREDIAN study. Rationale and basal results. J Diabetes Complic. 2011;25(5):314–19.

    Article  Google Scholar 

  21. Tan S, Wang Y, Chen K, Long Z, Zou J. Ketamine alleviates depressive-like behaviors via down regulating inflammatory cytokines induced by chronic restraint stress in mice. Biol Pharm Bull. 2017;40:1260–7.

    Article  PubMed  CAS  Google Scholar 

  22. Kumari V, Sarangapani S, Krishnamurthy P, Vaitheeswaran K, Sathyabaarathi R, Rajesh M, et al. ICAM-1K469E polymorphism is a genetic determinant for the clinical risk factors of T2D subjects with retinopathy in Indians: a population-based case–control study. BMJ Open. 2012;2(4):e001036.

    Article  Google Scholar 

  23. Petrovic MG, Osredkar J, Saraga-Babić M, Petrovic D. K469E polymorphism of the intracellular adhesion molecule 1 gene is associated with proliferative diabetic retinopathy in Caucasians with type 2 diabetes. Clin Exp Ophthalmol. 2008;36(5):468–72.

    Article  PubMed  Google Scholar 

  24. Ceriello A, Falleti E, Bortolotti N. Increased circulating ICAM-1 levels in type-2 diabetic patients: the possible role of metabolic control and oxidative stress. Metab Clin Exp. 1996;45(4):498–501.

    Article  PubMed  CAS  Google Scholar 

  25. Sahakyan K, Klein BE, Lee KE, Tsai MY, Klein R. Inflammatory and endothelial dysfunction markers and proteinuria in persons with type 1 diabetes mellitus. Eur J Endocrinol. 2010;162(6):1101–05.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Sahakyan K, Klein BE, Myers CE, Tsai MY, Klein R. Novel risk factors in long-term hypertension incidence in type 1 diabetes mellitus. Am Heart J. 2010;159(6):1074–80.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Lv Z, Li Y, Wu Y, Qu Y. Association of ICAM-1 and HMGA1 gene variants with retinopathy in type 2 diabetes mellitus among Chinese individuals. Curr Eye Res. 2016;41(8):1–5.

    Article  CAS  Google Scholar 

  28. Ma J, Möllsten A, Prázny M, Falhammar H, Brismar K, Dahlquist G, et al. Genetic influences of the intercellular adhesion molecule 1 (ICAM-1) gene polymorphisms in development of type 1 diabetes and diabetic nephropathy. Diabetes Med. 2006;23(10):1093–99.

    Article  CAS  Google Scholar 

  29. Gu HF, Ma J, Gu KT, Brismar K. Association of intercellular adhesion molecule 1 (ICAM1) with diabetes and diabetic nephropathy. Front Endocrinol (Lausanne). 2013;3:179.

    Article  Google Scholar 

  30. Aminian B, Abdi Ardekani AR, Arandi N. ICAM-1 polymorphisms (G241R, K469E), in coronary artery disease and myocardial infarction. Iran J Immunol. 2007;4(4):227–35.

    PubMed  CAS  Google Scholar 

  31. Wei YS, Liu YG, Huang RYl. Intercellular adhesion molecule-1 gene K469E polymorphism an d genetic susceptibility of ischemic stroke in Chinese Zhuang populations. Chin J Med Genet. 2005;22(3):305–8.

    CAS  Google Scholar 

  32. Kamiuchi K, Hasegawa G, Obayashi H, Kitamura A, Ishii M, Yano M, et al. Intercellular adhesion molecule-1 (ICAM-1) polymorphism is associated with diabetic retinopathy in Type 2 diabetes mellitus. Diabetes Med. 2010;19(5):371–76.

    Article  Google Scholar 

  33. Sun H, Cong X, Sun R, Wang C, Wang X, Liu Y. Association between the ICAM-1 K469E polymorphism and diabetic retinopathy in type 2 diabetes mellitus: a meta-analysis. Diabetes Res Clin Pract. 2014;104(2):e46–9.

    Article  PubMed  CAS  Google Scholar 

  34. Ren Z, Ji N, Jia K, Wang L, Gu HF, Ma J. Association of the intercellular adhesion molecule-1 gene polymorphisms with type 2 diabetes and diabetic peripheral neuropathy in a Chinese Han population. Genes Genomics. 2015;37(1):69–75.

    Article  CAS  Google Scholar 

  35. Seman Abu N, Anderstam B, Wan MW, Östenson CG, Brismar K, Gu HF. Genetic, epigenetic and protein analyses of intercellular adhesion molecule 1 in Malaysian subjects with type 2 diabetes and diabetic nephropathy. J Diabetes Complic. 2015;29(8):1234–9.

    Article  Google Scholar 

  36. Popović D, Starčević JN, Letonja M, Makuc J, Vujkovac AC, Pleskovic RZ, et al. Polymorphism rs5498 of the ICAM-1 gene affects the progression of carotid atherosclerosis in patients with type 2 diabetes mellitus. Lipids Health Dis. 2016;15(1):1–7.

    Article  CAS  Google Scholar 

  37. Zhou Y, Ping FU. Study on the gene polymorphism of intercellular adhesion molecule-1 in type 2 diabetes mellitus patients with retinopathy. J Chin Pract Diagn Ther. 2010;24:29–31.

    Google Scholar 

  38. Nejentsev S, Laine AP, Simell O, Ilonen J. Intercellular adhesion molecule-1 (ICAM-1) K469E polymorphism: no association with type 1 diabetes among Finns. Tissue Antigens. 2010;55(6):568–70.

    Article  Google Scholar 

  39. Nishimura M, Obayashi H, Maruya E, Ohta M, Tegoshi H, Fukui M, et al. Association between type 1 diabetes age-at-onset and intercellular adhesion molecule-1 (ICAM-1) gene polymorphism. Hum Immunol. 2000;61(5):507–10.

    Article  PubMed  CAS  Google Scholar 

  40. Page MJ, Moher D. Evaluations of the uptake and impact of the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) statement and extensions: a scoping review. Syst Rev. 2017;6(1):263.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Wells GA, Shea BJ, O’Connell D. The Newcastle–Ottawa Scale (NOS) for assessing the quality of non-randomized studies in meta-analysis. Appl Eng Agric. 2014;18:727–34.

    Google Scholar 

  42. Zhu YP, Shen T, Lin YJ, Chen BD, Ruan Y, Cao Y, et al. Astragalus polysaccharides suppress ICAM-1 and VCAM-1 expression in TNF-α-treated human vascular endothelial cells by blocking NF-κB activation. Acta Pharmacol Sin. 2013;34(8):1036–42.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Zou J, Wu D, Liu Y, Tan S. Association of luteinizing hormone/choriogonadotropin receptor gene polymorphisms with polycystic ovary syndrome risk: a meta-analysis. Gynecol Endocrinol. 2018;5:1–5.

    Google Scholar 

  44. Textor S, Accardi R, Havlova T, Hussain I, Sylla BS, Gissmann L, et al. NF-κB-dependent upregulation of ICAM-1 by HPV16-E6/E7 facilitates NK cell/target cell interaction. Int J Cancer. 2011;128(5):1104–13.

    Article  PubMed  CAS  Google Scholar 

  45. Seventer GAV, Shimizu Y, Horgan KJ, Shaw S. The LFA-1 ligand ICAM-1 provides an important costimulatory signal for T cell receptor-mediated activation of resting T cells. J Immunol. 1990;144(12):4579–86.

    PubMed  Google Scholar 

  46. Driver JP, Chen YG, Mathews CE. Comparative genetics: synergizing human and NOD mouse studies for identifying genetic causation of type 1 diabetes. Rev Diabetes Stud. 2012;9(4):169–87.

    Article  Google Scholar 

  47. Amano K, Taki T, Hasegawa Y. Prevention of autoimmune IDDM in NOD mice by anti-LFA-1 and anti-ICAM-1 monoclonal-antibodies. Diabetologia. 1993;36:A10–0.

    Google Scholar 

  48. Martin S, Hibino T, Faust A, Kleemann R, Kolb H. Differential expression of ICAM-1 and LFA-1 versus l-selectin and VCAM-1 in autoimmune insulitis of NOD mice and association with both Th1- and Th2-type infiltrates. J Autoimmun. 1996;9(5):637–43.

    Article  PubMed  CAS  Google Scholar 

  49. Vudattu NK, Herold KC. Treatment of new onset type 1 diabetes with teplizumab: successes and pitfalls in development. Expert Opin Biol Ther. 2014;14(3):377–85.

    Article  PubMed  CAS  Google Scholar 

  50. Oh HM, Kwon MS, Kim HJ, Jeon BH, Kim HR, Choi HO, et al. Intermediate monomer–dimer equilibrium structure of native ICAM-1: implication for enhanced cell adhesion. Exp Cell Res. 2011;317(2):163–72.

    Article  PubMed  CAS  Google Scholar 

  51. Brorsson C, Hansen NT, Lage K, Bergholdt R, Brunak S, Pociot F, et al. Identification of T1D susceptibility genes within the MHC region by combining protein interaction networks and SNP genotyping data. Diabetes Obes Metab. 2010;11(s1):60–6.

    Google Scholar 

  52. Kristiansen OP, Nolsøe RL, Holst H, Reker S, Larsen ZM, Johannesen J, et al. The intercellular adhesion molecule-1 K469E polymorphism in type 1 diabetes. Immunogenetics. 2000; 52(1–2):107–11.

    Article  PubMed  CAS  Google Scholar 

  53. Vaag A, Brøns C, Gillberg L, Hansen NS, Hjort L, Arora GP, et al. Genetic, non-genetic and epigenetic risk determinants in developmental programming of type 2 diabetes. Acta Obstet Gynecol Scand. 2015;93(11):1099–108.

    Article  Google Scholar 

  54. Odegaard AO Jr, Sanchez JDR, Goff OA, Reiner DC Jr, Gross AP. MD. Oxidative stress, inflammation, endothelial dysfunction and incidence of type 2 diabetes. Cardiovasc Diabetol. 2016;15(1):51.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Ceriello A, Falleti E, Motz E, Taboga C, Tonutti L, Ezsol Z, et al. Hyperglycemia-induced circulating ICAM-1 increase in diabetes mellitus: the possible role of oxidative stress. Horm Metab Res. 1998;30(03):146–9.

    Article  PubMed  CAS  Google Scholar 

  56. Park CW, Kim JH, Lee JW, Kim YS, Ahn HJ, Shin YS, et al. High glucose-induced intercellular adhesion molecule-1 (ICAM-1) expression through an osmotic effect in rat mesangial cells is PKC-NF-ϰB-dependent. Diabetologia. 2000;43(12):1544–53.

    Article  PubMed  CAS  Google Scholar 

  57. Basile KJ, Guy VC, Schwartz S, Grant SFA. Overlap of genetic susceptibility to type 1 diabetes, type 2 diabetes, and latent autoimmune diabetes in adults. Curr Diabetes Rep. 2014;14(11):1–7.

    Article  CAS  Google Scholar 

  58. Leif G, Flemming P. Genetics of diabetes—are we missing the genes or the disease? Mol Cell Endocrinol. 2014;382(1):726–39.

    Article  CAS  Google Scholar 

  59. Dooley J, Tian L, Schonefeldt S, Delghingaro-Augusto V, Garcia-Perez JE, Pasciuto E, et al. Genetic predisposition for beta cell fragility underlies type 1 and type 2 diabetes. Nat Genet, 2016; 1–12.

Download references

Acknowledgements

This study was funded by the Youth Foundation of the Education Department of Hunan (17B035) and the construct program of the key discipline in Hunan province.

Author information

Authors and Affiliations

  1. Department of Pathophysiology, School of Basic Medical Science, Changsha Medical University, Changsha, 410219, People’s Republic of China

    Wensheng Mi, Yan Xia & Yanhui Bian

  2. Department of Human Anatomy, Histology and Embryology, Institute of Neuroscience, Changsha Medical University, Changsha, 410219, People’s Republic of China

    Wensheng Mi, Yan Xia & Yanhui Bian

Authors
  1. Wensheng Mi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yan Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yanhui Bian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yan Xia.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Responsible Editor: John Di Battista.

Publisher’s Note

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

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mi, W., Xia, Y. & Bian, Y. The influence of ICAM1 rs5498 on diabetes mellitus risk: evidence from a meta-analysis. Inflamm. Res. 68, 275–284 (2019). https://doi.org/10.1007/s00011-019-01220-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00011-019-01220-4

Keywords

Search

Navigation