Table of Contents Author Guidelines Submit a Manuscript
International Journal of Endocrinology
Volume 2014, Article ID 607924, 9 pages
http://dx.doi.org/10.1155/2014/607924
Research Article

Markers of Systemic Inflammation and Apo-AI Containing HDL Subpopulations in Women with and without Diabetes

1Department of Clinical and Experimental Medicine, University of Messina, Via C. Valeria, 98124 Messina, Italy
2Department of Economical, Business and Environmental Sciences and Quantitative Methods, University of Messina, Piazza Pugliatti 1, 98122 Messina, Italy
3Lipid Metabolism Laboratory, JM-USDA-Human Nutrition Research Center on Aging, Tufts University, 711 Washington Street, Boston, MA 02111, USA

Received 4 July 2014; Accepted 19 August 2014; Published 2 September 2014

Academic Editor: Maria Chiara Rossi

Copyright © 2014 Giuseppina T. Russo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. A. Raza, R. A. Reinhart, and A. Movahed, “Ischemic heart disease in women and the role of hormone therapy,” International Journal of Cardiology, vol. 96, no. 1, pp. 7–19, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. E. Barrett-Connor, “Sex differences in coronary heart disease: why are women so superior? The 1995 Ancel Keys Lecture,” Circulation, vol. 95, no. 1, pp. 252–264, 1997. View at Publisher · View at Google Scholar · View at Scopus
  3. J. R. Sowers, “Diabetes mellitus and cardiovascular disease in women,” Archives of Internal Medicine, vol. 158, no. 6, pp. 617–621, 1998. View at Publisher · View at Google Scholar · View at Scopus
  4. W. B. Kannel and P. W. F. Wilson, “Risk factors that attenuate the female coronary disease advantage,” Archives of Internal Medicine, vol. 155, no. 1, pp. 57–61, 1995. View at Publisher · View at Google Scholar · View at Scopus
  5. B. F. Asztalos, C. H. Sloop, L. Wong, and P. S. Roheim, “Two-dimensional electrophoresis of plasma lipoproteins: recognition of new apo A-I-containing subpopulations,” Biochimica et Biophysica Acta, vol. 1169, no. 3, pp. 291–300, 1993. View at Publisher · View at Google Scholar · View at Scopus
  6. D. J. Gordon, J. L. Probstfield, R. J. Garrison et al., “High-density lipoprotein cholesterol and cardiovascular disease. Four prospective American studies,” Circulation, vol. 79, no. 1, pp. 8–15, 1989. View at Publisher · View at Google Scholar · View at Scopus
  7. M.-R. Taskinen, “Diabetic dyslipidaemia: from basic research to clinical practice,” Diabetologia, vol. 46, no. 6, pp. 733–749, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. R. Barbaras, P. Puchois, J.-C. Fruchart, and G. Ailhaud, “Cholesterol efflux from cultured adipose cells is mediated by LpA-I particles but not by LpA-IA-II particles,” Biochemical and Biophysical Research Communications, vol. 142, no. 1, pp. 63–69, 1987. View at Publisher · View at Google Scholar · View at Scopus
  9. B. F. Asztalos and E. J. Schaefer, “HDL in atherosclerosis: actor or bystander?” Atherosclerosis Supplements, vol. 4, no. 1, pp. 21–29, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. B. F. Asztalos, P. S. Roheim, R. L. Milani et al., “Distribution of apoA-I-containing HDL subpopulations in patients with coronary heart disease,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 20, no. 12, pp. 2670–2676, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. M. C. Cheung, B. G. Brown, A. C. Wolf, and J. J. Albers, “Altered particle size distribution of apolipoprotein A-I-containing lipoproteins in subjects with coronary artery disease,” Journal of Lipid Research, vol. 32, no. 3, pp. 383–394, 1991. View at Google Scholar · View at Scopus
  12. B. F. Asztalos, L. A. Cupples, S. Demissie et al., “High-density lipoprotein subpopulation profile and coronary heart disease prevalence in male participants of the Framingham Offspring Study,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 24, no. 11, pp. 2181–2187, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. M. E. Brousseau, M. R. Diffenderfer, J. S. Millar et al., “Effects of cholesteryl ester transfer protein inhibition on high-density lipoprotein subspecies, apolipoprotein A-I metabolism, and fecal sterol excretion,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 5, pp. 1057–1064, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. G. T. Russo, K. V. Horvath, A. Di Benedetto, A. Giandalia, D. Cucinotta, and B. Asztalos, “Influence of menopause and cholesteryl ester transfer protein (CETP) TaqIB polymorphism on lipid profile and HDL subpopulations distribution in women with and without type 2 diabetes,” Atherosclerosis, vol. 210, no. 1, pp. 294–301, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. B. F. Asztalos, M. Tani, and E. J. Schaefer, “Metabolic and functional relevance of HDL subspecies,” Current Opinion in Lipidology, vol. 22, no. 3, pp. 176–185, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. E. J. Schaefer and B. F. Asztalos, “Increasing high-density lipoprotein cholesterol, inhibition of cholesteryl ester transfer protein, and heart disease risk reduction,” The American Journal of Cardiology, vol. 100, no. 11, pp. S25–S31, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. B. F. Asztalos, M. De La Llera-Moya, G. E. Dallal, K. V. Horvath, E. J. Schaefer, and G. H. Rothblat, “Differential effects of HDL subpopulations on cellular ABCA1- and SR-BI-mediated cholesterol efflux,” Journal of Lipid Research, vol. 46, no. 10, pp. 2246–2253, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. B. F. Asztalos, E. J. Schaefer, K. V. Horvath et al., “Role of LCAT in HDL remodeling: Investigation of LCAT deficiency states,” Journal of Lipid Research, vol. 48, no. 3, pp. 592–599, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Di Benedetto, G. T. Russo, F. Corrado et al., “Inflammatory markers in women with a recent history of gestational diabetes mellitus,” Journal of Endocrinological Investigation, vol. 28, no. 1, pp. 34–38, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. P. M. Ridker, C. H. Hennekens, J. E. Buring, and N. Rifai, “C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women,” The New England Journal of Medicine, vol. 342, no. 12, pp. 836–843, 2000. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Genest, “C-reactive protein: risk factor, biomarker and/or therapeutic target?” Canadian Journal of Cardiology, vol. 26, supplement A, pp. 41A–44A, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Corrado, M. Rizzo, G. Coppola et al., “An update on the role of markers of inflammation in atherosclerosis,” Journal of Atherosclerosis and Thrombosis, vol. 17, no. 1, pp. 1–11, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. A. M. Bennet, J. A. Prince, G.-Z. Fei et al., “Interleukin-6 serum levels and genotypes influence the risk for myocardial infarction,” Atherosclerosis, vol. 171, no. 2, pp. 359–367, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. P. J. Klover, T. A. Zimmers, L. G. Koniaris, and R. A. Mooney, “Chronic exposure to Interleukin-6 causes hepatic insulin resistance in mice,” Diabetes, vol. 52, no. 11, pp. 2784–2789, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Chrysohoou, C. Pitsavos, J. Skoumas et al., “The emerging anti-inflammatory role of HDL-cholesterol, illustrated in cardiovascular disease free population; the ATTICA study,” International Journal of Cardiology, vol. 122, no. 1, pp. 29–33, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. “The expert committee on the diagnosis and classification of diabetes mellitus report of the expert committee on the diagnosis and classification of diabetes mellitus,” Diabetes Care, vol. 20, pp. 1183–1197, 1997.
  27. J. R. McNamara and E. J. Schaefer, “Automated enzymatic standardized lipid analyses for plasma and lipoprotein fractions,” Clinica Chimica Acta, vol. 166, no. 1, pp. 1–8, 1987. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Gordon, W. P. Castelli, M. C. Hjortland, W. B. Kannel, and T. R. Dawber, “High density lipoprotein as a protective factor against coronary heart disease. The Framingham study,” The American Journal of Medicine, vol. 62, no. 5, pp. 707–714, 1977. View at Publisher · View at Google Scholar · View at Scopus
  29. G. Assmann, P. Cullen, and H. Schulte, “The munster heart study (PROCAM). Results of follow-up at 8 years,” European Heart Journal, vol. 19, pp. A2–A11, 1998. View at Google Scholar · View at Scopus
  30. P. P. Toth, M. Barylski, D. Nikolic et al., “Should low high-density lipoprotein cholesterol (HDL-C) be treated,” Best Practice and Research Clinical Endocrinology Metabolism, vol. 28, no. 3, pp. 353–368, 2014. View at Publisher · View at Google Scholar
  31. S. J. Robins, A. Lyass, J. P. Zachariah, J. M. Massaro, and R. S. Vasan, “Insulin resistance and the relationship of a dyslipidemia to coronary heart disease: the framingham heart study,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 5, pp. 1208–1214, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. Y.-X. Meng, E. S. Ford, C. Li et al., “Association of C-reactive protein with surrogate measures of insulin resistance among nondiabetic US adults: findings from national health and nutrition examination survey 1999–2002,” Clinical Chemistry, vol. 53, no. 12, pp. 2152–2159, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Luc, J.-M. Bard, I. Juhan-Vague et al., “C-reactive protein, interleukin-6, and fibrinogen as predictors of coronary heart disease: the PRIME study,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 23, no. 7, pp. 1255–1261, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. S. G. Lakoski, M. Cushman, M. Criqui et al., “Gender and C-reactive protein: data from the Multiethnic Study of Atherosclerosis (MESA) cohort,” The American Heart Journal, vol. 152, no. 3, pp. 593–598, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. M.-M. Lai, C.-I. Li, S. L. Kardia et al., “Sex difference in the association of metabolic syndrome with high sensitivity C-reactive protein in a Taiwanese population,” BMC Public Health, vol. 10, article 429, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Daniele, R. Guardado Mendoza, D. Winnier et al., “The inflammatory status score including IL-6, TNF-α, osteopontin, fractalkine, MCP-1 and adiponectin underlies whole-body insulin resistance and hyperglycemia in type 2 diabetes mellitus,” Acta Diabetologica, vol. 51, no. 1, pp. 123–131, 2014. View at Google Scholar
  37. T. S. Han, N. Sattar, K. Williams, C. Gonzalez-Villalpando, M. E. J. Lean, and S. M. Haffner, “Prospective study of C-reactive protein in relation to the development of diabetes and metabolic syndrome in the Mexico City diabetes study,” Diabetes Care, vol. 25, no. 11, pp. 2016–2021, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Thorand, J. Baumert, H. Kolb et al., “Sex differences in the prediction of type 2 diabetes by inflammatory markers: results from the MONICA/KORA Augsburg case-cohort study, 1984–2002,” Diabetes Care, vol. 30, no. 4, pp. 854–860, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. R.-C. Huang, T. A. Mori, V. Burke et al., “Synergy between adiposity, insulin resistance, metabolic risk factors, and inflammation in adolescents,” Diabetes Care, vol. 32, no. 4, pp. 695–701, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. E. M. Tsompanidi, M. S. Brinkmeier, E. H. Fotiadou, S. M. Giakoumi, and K. E. Kypreos, “HDL biogenesis and functions: role of HDL quality and quantity in atherosclerosis,” Atherosclerosis, vol. 208, no. 1, pp. 3–9, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Besler, T. F. Lüscher, and U. Landmesser, “Molecular mechanisms of vascular effects of High-density lipoprotein: alterations in cardiovascular disease,” EMBO Molecular Medicine, vol. 4, no. 4, pp. 251–268, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. J. R. Nofer, B. Kehrel, M. Fobker, B. Levkau, G. Assmann, and A. V. Eckardstein, “HDL and arteriosclerosis: beyond reverse cholesterol transport,” Atherosclerosis, vol. 161, no. 1, pp. 1–16, 2002. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Radojkovic, A. Genoux, V. Pons et al., “Stimulation of cell surface F1-ATPase activity by apolipoprotein A-I inhibits endothelial cell apoptosis and promotes proliferation,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 29, no. 7, pp. 1125–1130, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. G. D. Norata, A. Pirillo, E. Ammirati, and A. L. Catapano, “Emerging role of high density lipoproteins as a player in the immune system,” Atherosclerosis, vol. 220, no. 1, pp. 11–21, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Camont, M. J. Chapman, and A. Kontush, “Biological activities of HDL subpopulations and their relevance to cardiovascular disease,” Trends in Molecular Medicine, vol. 17, no. 10, pp. 594–603, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. D. M. Tehrani, J. M. Gardin, D. Yanez et al., “Impact of inflammatory biomarkers on relation of high density lipoprotein-cholesterol with incident coronary heart disease: cardiovascular health study,” Atherosclerosis, vol. 231, no. 2, pp. 246–251, 2013. View at Publisher · View at Google Scholar
  47. B. J. Ansell, M. Navab, S. Hama et al., “Inflammatory/antiinflammatory properties of high-density lipoprotein distinguish patients from control subjects better than high-density lipoprotein cholesterol levels and are favorably affected by simvastatin treatment,” Circulation, vol. 108, no. 22, pp. 2751–2756, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. G. K. Hansson, “Mechanisms of disease: inflammation, atherosclerosis, and coronary artery disease,” The New England Journal of Medicine, vol. 352, no. 16, pp. 1685–1695, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. K. Alwaili, D. Bailey, Z. Awan et al., “The HDL proteome in acute coronary syndromes shifts to an inflammatory profile,” Biochimica et Biophysica Acta: Molecular and Cell Biology of Lipids, vol. 1821, no. 3, pp. 405–415, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Kisilevsky and L. Subrahmanyan, “Serum amyloid A changes high density lipoprotein's cellular affinity: a clue to serum amyloid A's principal function,” Laboratory Investigation, vol. 66, no. 6, pp. 778–785, 1992. View at Google Scholar · View at Scopus
  51. A. Kontush and M. J. Chapman, “Functionally defective high-density lipoprotein: A new therapeutic target at the crossroads of dyslipidemia, inflammation, and atherosclerosis,” Pharmacological Reviews, vol. 58, no. 3, pp. 342–374, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. M. McMahon, J. Grossman, J. FitzGerald et al., “Proinflammatory high-density lipoprotein as a biomarker for atherosclerosis in patients with systemic lupus erythematosus and rheumatoid arthritis,” Arthritis and Rheumatism, vol. 54, no. 8, pp. 2541–2549, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Navab, G. M. Anantharamaiah, S. T. Reddy, B. J. van Lenten, B. J. Ansell, and A. M. Fogelman, “Mechanisms of disease: proatherogenic HDL—An evolving field,” Nature Clinical Practice Endocrinology and Metabolism, vol. 2, no. 9, pp. 504–511, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. H. Bindu G, V. S. Rao, and V. V. Kakkar, “Friend turns foe: transformation of anti-inflammatory hdl to proinflammatory HDL during acute-phase response,” Cholesterol, vol. 2011, Article ID 274629, 7 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Von Eckardstein, Y. Huang, and G. Assmann, “Physiological role and clinical relevance of high-density lipoprotein subclasses,” Current Opinion in Lipidology, vol. 5, no. 6, pp. 404–416, 1994. View at Publisher · View at Google Scholar · View at Scopus
  56. B. J. Ansell, G. C. Fonarow, and A. M. Fogelman, “The paradox of dysfunctional high-density lipoprotein,” Current Opinion in Lipidology, vol. 18, no. 4, pp. 427–434, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. T. Kelesidis, J. S. Currier, D. Huynh et al., “A biochemical fluorometric method for assessing the oxidative properties of HDL,” Journal of Lipid Research, vol. 52, no. 12, pp. 2341–2351, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. Y. L. Marcel, P. K. Weech, T. D. Nguyen, R. W. Milne, and W. J. McConathy, “Apolipoproteins as the basis for heterogeneity in high-density lipoprotein2 and high-density lipoprotein3. Studies by isoelectric focusing on agarose films,” European Journal of Biochemistry, vol. 143, no. 3, pp. 467–476, 1984. View at Publisher · View at Google Scholar · View at Scopus
  59. B. F. Asztalos, D. Collins, L. A. Cupples et al., “Value of high-density lipoprotein (HDL) subpopulations in predicting recurrent cardiovascular events in the veterans affairs HDL intervention trial,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 10, pp. 2185–2191, 2005. View at Publisher · View at Google Scholar · View at Scopus