Antidiabetic Role of High Density Lipoproteins

  • O. N. PoteryaevaEmail author
  • I. F. Usynin


Disturbance in lipid metabolism can be both a cause and a consequence of the development of diabetes mellitus (DM). One of the most informative parameters of lipid metabolism is the ratio of atherogenic and antiatherogenic fractions of lipoproteins and their protein components. The review summarizes literature data and own results indicating an important role of high-density lipoprotein (HDL) and their main protein component, apolipoprotein A-I (apoA-I), in the pathogenesis of type 2 DM. On the one hand, HDL are involved in the regulation of insulin secretion by β-cells and insulin-independent absorption of glucose. On the other hand, insulin resistance and hyperglycemia lead to a decrease in HDL levels and cause modification of their protein component. In addition, HDL, possessing anti-inflammatory and mitogenic properties, provide anti-diabetic protection via systemic mechanisms. Thus, maintenance of a high concentration of HDL and apoA-I in blood plasma and prevention of their modification are important issues in the context of prevention and treatment of diabetes.


type 2 diabetes mellitus dyslipidemia insulin resistance high-density lipoproteins apolipoprotein A-I matrix metalloproteinases 



  1. 1.
    Dedov, I.I. and Shestakova, M.V. (Eds), Sakharnyi Diabet, 2015, vol. 18, no. 1, pp. 1–112.
  2. 2.
    Urazgil’dieva, S.A. and Malygina, O.F., Meditsinskii Sovet, 2016, vol. 3, pp. 48–53.Google Scholar
  3. 3.
    Rye, K.-A., Barter, P.J., and Cochran, B.J., Curr. Opion Lipidol., 2016, vol. 27, no. 1, pp. 8–13. CrossRefGoogle Scholar
  4. 4.
    Wu, X., Yu, Z., Su, W., Isquith, D.A., Neradilek, M.B., Lu, N., Gu, F., Li, H., and Zhao, X.Q., J. Clin. Lipidol., 2017, vol. 11, vol. 2, pp. 362–368.
  5. 5.
    Balabolkin, M.I., Vvedenie v diabetologiyu (Introduction to Daibetology), Moscow: Nauka, 1994.Google Scholar
  6. 6.
    Dedov, I.I., Sakharnyi Diabet, 1998, vol. 1, pp. 7–18.Google Scholar
  7. 7.
    Kontush, A. and Chapman, M.J., Pharmacological Reviews, 2006, vol. 58, pp. 342–347. CrossRefGoogle Scholar
  8. 8.
    Tall, A.R., J. Int. Med., 2008, vol. 263, no. 3, pp. 256–273. CrossRefGoogle Scholar
  9. 9.
    Huang, Y., Zhu, Y., Langer, C., Raabe, M., Wu, S., Wiesenhutter, B., Seedorf, U., Maeda, N., Assmann, G., and von Eckardstein, A., Arterioscler. Thromb. Vasc. Biol., 1997, vol. 17, no. 10, pp. 2010–2019.CrossRefGoogle Scholar
  10. 10.
    Ross, R., N. Eng. J. Med., 1999, vol. 340, no. 2, pp. 115–126.CrossRefGoogle Scholar
  11. 11.
    Hu, Y.W., Zheng, L., and Wang, Q., Biochim. Biophys. Acta—Molecular and Cell Biology of Lipids, 2010, vol. 1801, no. 2, pp. 100–105.
  12. 12.
    Vanhollebeke, B. and Pays, E., Cellular Molecular Life Sci., 2006, vol. 63, no. 17, pp. 1937–1944. CrossRefGoogle Scholar
  13. 13.
    Srivastava, R.A.K. and Srivastava, N., Molecular Cellular Biochem., 2000, vol. 209, pp. 131–144.CrossRefGoogle Scholar
  14. 14.
    Schultz, J.R., Verstuyft, J.G., Gong, E.L., Nichols, A.V., and Rubin, E.M., Nature, 1993, vol. 365, no. 6448, pp. 762–764.CrossRefGoogle Scholar
  15. 15.
    Gordon, S.M., Hofmann, S., Askew, D.S., and Davidson, W.S., Trends Endocrinol. Metabol., 2011, vol. 22, pp. 9–15. CrossRefGoogle Scholar
  16. 16.
    Grebennikov, I.N. and Kulikov, V.A., Vestnik VGMU, 2011, vol. 12, no. 2, pp. 12–19.Google Scholar
  17. 17.
    Vergès, B., Duvillard, L., Lagrost, L., Vachoux, C., Garret, C., Bouyer, K., Courtney, M., Pomié, C., and Burcelin, R., J. Clin. Endocrinol. Metab., 2014, vol. 99, no. 7, pp. 1245–1253. CrossRefGoogle Scholar
  18. 18.
    Drew, B.G., Fidge, N.H., Gallon-Beaumier, G., Kemp, B.E., and Kingwell, B.A., Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 6999–7004. CrossRefGoogle Scholar
  19. 19.
    Maedler, K., Spinas, G.A., Lehmann, R., Sergeev, P., Weber, M., Fontana, A., Kaiser, N., and Donath, M.Y., Diabetes, 2001, vol. 50, pp. 1683–1690.CrossRefGoogle Scholar
  20. 20.
    Rütti, S., Ehses, J.A., Sibler, R.A., Prazak, R., Rohrer, L., Georgopoulos, S., Meier, D.T., Niclauss, N., Berney, T., Donath, M.Y., and von Eckardstein, A., Endocrinology, 2009, vol. 150, no. 10, pp. 4521–4530. CrossRefGoogle Scholar
  21. 21.
    von Eckardstein, A. and Widmann, C., Cardiovascular Res., 2014, vol. 103, pp. 384–394. CrossRefGoogle Scholar
  22. 22.
    Volchuk, A. and Ron, D., Diabetes Obes. Metab., 2010, vol. 12, no. 2, pp. 48–57. CrossRefGoogle Scholar
  23. 23.
    Petremand, J., Puyal, J., Chatton, J.-Y., Duprez, J., Allagnat, F., Frias, M., James, R.W., Waeber, G., Jonas, J.-C., and Widmann1, C., Diabetes, 2012, vol. 61, pp. 1100–1111. CrossRefGoogle Scholar
  24. 24.
    Engin, F. and Hotamisligil, G.S., Diabetes Obes. Metab., 2010, vol. 12, suppl. 2, pp. 108–115. CrossRefGoogle Scholar
  25. 25.
    Panin, L.E., Russkikh, G.S., and Filatova, T.G., Vopr. Med. Khim., 1986, vol. 32, no. 3, pp. 61–65.Google Scholar
  26. 26.
    Polyakov, L.M. and Panin, L.E., Ateroskleroz, 2013, vol. 9, no. 1, pp. 42–53.Google Scholar
  27. 27.
    Usynin, I.F. and Panin, L.E., Biochemistry (Moscow), 2008, vol. 73, no. 4, pp. 453–468.Google Scholar
  28. 28.
    Panin, L.E., Kovalenko, G.A., Polyakov, L.M., Tuzikov, F.V., Tuzikova, N.A., and Knyazev, R.A., Bulleten’ SO RAMN, 2012, vol. 32, no. 1, pp. 38–42.Google Scholar
  29. 29.
    Vollenweider, P., von Eckardstein, A., and Widmann, C., in From Biological Understanding to Clinical Exploitation, Berlin-Heidelberg-New York: Springer, 2015, pp. 405–421.Google Scholar
  30. 30.
    Gatti, A., Maranghi, M., Bacci, S., Carallo, C., Ginasso, A., Mandosi, E., Fallarino, M., Morano, S., Trischitta, V., and Filetti, S., Diabetes Care, 2009, vol. 32, pp. 1550–1552. CrossRefGoogle Scholar
  31. 31.
    Montonen, J., Grogan, D., Joost, H.G., Boeing, H., Fritsche, A., Schleicher, E., Schulze, M.B., and Pischon, T., Eur. J. Epidemiol., 2011, vol. 26, pp. 29–38. CrossRefGoogle Scholar
  32. 32.
    Hwang, Y.-C., Ahn, H.-Y., Park, S.-W., and Park, C.-Y., Eur. J. Endocrinol., 2014, vol. 171, pp. 137–142. CrossRefGoogle Scholar
  33. 33.
    Jian, Z.-H., Lung, C.-C., Ko, P.-C., Sun, Y.-H., Huang, J.-Y., Ho, C.-C., Ho, C.-Y., Chiang, Y.-C., Chen, C.-J., and Liaw, Y.-P., BMC Endocrine Disorders, 2013, vol. 13, pp. 42–49. CrossRefGoogle Scholar
  34. 34.
    Barter, P.J., Rye, K.-A., Tardif, J.C., Waters, D.D., Boekholdt, S.M., Breazna, A., and Kastelein, J.J., Circulation, 2011, vol. 124, pp. 555–562. CrossRefGoogle Scholar
  35. 35.
    Waldman, B., Jenkins, A.J., Davis, T.M., Taskinen, M.R., Scott, R., O’Connell, R.L., Gebski, V.J., Ng, M.K., and Keech, A.C., Diabetes Care, 2014, vol. 37, pp. 2351–2358. CrossRefGoogle Scholar
  36. 36.
    Siebel, A.L., Natoli, A.K., Yap, F.Y. Carey, A.L., Reddy-Luthmoodoo, M., Sviridov, D., Weber, C.I., Meneses-Lorente, G., Maugeais, C., Forbes, J.M., and Kingwell, B.A., Circ. Res, 2013, vol. 113, pp. 167–175. CrossRefGoogle Scholar
  37. 37.
    Sasongko, M.B., Wong, T.Y., Nguyen, T.T., Kawasaki, R., Jenkins, A., Shaw, J., and Wang, J.J., Diabetes Care, 2011, vol. 34, no. 2, pp. 474–479. CrossRefGoogle Scholar
  38. 38.
    Nieuwdorp, M., Vergeer, M., Bisoendial, R.J., op’t Roodt, J., Levels, H., Birjmohum, R.S., Kuivenhoven, J.A., Basse, R., Rabelink, T.J., Kastelein, J.J., and Stroes, E.S., Diabetologia, 2008, vol. 51, pp. 1081–1084. CrossRefGoogle Scholar
  39. 39.
    Kahn, B.B., Alquier, T., Carling, D., and Hardie, D.G., Cell. Metab., 2005, vol. 1, no. 1, pp. 15–25.CrossRefGoogle Scholar
  40. 40.
    Drew, B.G., Duffy, S.J., Formosa, M.F., Natoli, A.K., Henstridge, D.C., Penfold, S.A., Thomas, W.G., Mukhamedova, N., de Courten, B., Forbes, J.M., Yap, F.Y., Kaye, D.M., van Hall, G., Febbraio, M.A., Kemp, B.E., Sviridov, D., Steinberg, G.R., and Kingwell, B.A., Circulation, 2009, vol. 119, no. 15, pp. 2103–2111. CrossRefGoogle Scholar
  41. 41.
    Brunham, L.R., Kruit, J.K., Pape, T.D., Timmins, J.M., Reuwer, A.Q., Vasanji, Z., Marsh, B.J., Rodrigues, B., Johnson, J.D., Parks, J.S., Verchere, C.B., and Hayden, M.R., Nat. Med., 2007, vol. 13, pp. 340–347. CrossRefGoogle Scholar
  42. 42.
    Bardini, G., Dicembrini, I., Rotella, C.M., and Giannini, S., Acta Diabetol., 2013, vol. 50, pp. 277–281. CrossRefGoogle Scholar
  43. 43.
    Han, R., Lai, R., Ding, Q., Wang, Z., Luo, X., Zhang, Y., Cui, G., He, J., Liu, W., and Chen, Y., Diabetologia, 2007, vol. 50, pp. 1960–1968. CrossRefGoogle Scholar
  44. 44.
    Ruan, X., Li, Z., Zhang, I., Pan, Y., Wang, Z., Feng, G.S., and Chen, Y., J. Cell. Mol. Med., 2011, vol. 15, pp. 763–772. CrossRefGoogle Scholar
  45. 45.
    Stenkula, K.G., Lindahl, M., Petrlova, J., Dalla-Riva, J., Göransson, O., Cushman, S.W., Krupinska, E., Jones, H.A., and Lagerstedt, J.O., Diabetologia, 2014, vol. 57, pp. 797–800. CrossRefGoogle Scholar
  46. 46.
    Cochran, B.J., Bisoendial, R.J., Hou, L., Glaros, E.N., Rossy, J., Thomas, S.R., Barter, P.J., and Rye, K.-A., Arterioscler. Thromb. Vasc. Biol., 2014, vol. 34, pp. 2261–2267. CrossRefGoogle Scholar
  47. 47.
    Drucker, D.J., Philippe, J., Mojsov, S., Chick, W.L., and Habener, J.F., Proc. Natl. Acad. Sci. USA, 1987, vol. 84, pp. 3434–3438.CrossRefGoogle Scholar
  48. 48.
    Skoglund, G., Hussain, M.A. and Holz, G.G., Diabetes, 2000, vol. 49, pp. 1156–1164.CrossRefGoogle Scholar
  49. 49.
    Fryirs, M.A., Barter, P.J., Appavoo, M., Tuch, B.E., Tabet, F., Heather, A.K., and Rye, K.A., Arterioscler. Thromb. Vasc. Biol., 2010, vol. 30, pp. 1642–1648.CrossRefGoogle Scholar
  50. 50.
    Abderrahmani, A., Niederhauser, G., Favre, D., Ab-delli, S., Ferdaoussi, M., Yang, J.-Y., Regazzi, R., Widmann, C., and Waeber, G., Diabetologia, 2007, vol. 50, pp. 1304–1314. CrossRefGoogle Scholar
  51. 51.
    Wang, F., Kohan, A.B., Kindel, T.L., Corbin, K.L., Nunemaker, C.S., Obici, S., and Woods, S.C., Proc. Natl. Acad. Sci. USA, 2012, vol. 109, pp. 9641–9646. CrossRefGoogle Scholar
  52. 52.
    Panin, L.E., Poteryaeva, O.N., and Russkikh, G.S., Byull. SO RAMN, 2010, vol. 30, no. 2, pp. 28–32.Google Scholar
  53. 53.
    Cnop, M., Hannaert, J.C., Grupping, A.Y., and Pipeleers, D.G., Endocrinology, 2002, vol. 143, pp. 3449–3453. CrossRefGoogle Scholar
  54. 54.
    Kulikov, V.A., Vestnik VGMU, 2011, vol. 10, no. 1, pp. 33–40.Google Scholar
  55. 55.
    Haidar, B., Denis, M., Marcil, M., Krimbou, L., and Genest, J., Jr., J. Biol. Chem., 2004, vol. 279, no. 11, pp. 9963–9969. CrossRefGoogle Scholar
  56. 56.
    Karwatsky, J., Ma, L., Dong, F., and Zha, X., J. Lipid. Res., 2010, vol. 51, pp. 1144–1156. CrossRefGoogle Scholar
  57. 57.
    Miralles, F., Battelino, T., Czernichow, P., and Scharfmann, R., J. Cell Biology, 1998, vol. 143, no. 3, pp. 827–836.CrossRefGoogle Scholar
  58. 58.
    Poteryaeva, O.N., Russkikh, G.S., and Panin, L.E., Byull. Eksper. Biol. Med., 2011, vol. 152, no. 11, pp. 509–510.Google Scholar
  59. 59.
    Poteryaeva, O.N., Russkikh, G.S., Zubova, A.V., Gevorgyan, M.M., and Usynin, I.F., Byull. Eksper. Biol. Med., 2017, vol. 158, no. 12, pp. 697–701. Google Scholar
  60. 60.
    Usynin, I.F., Poteryaeva, O.N., Russkikh, G.S., Zubova, A.V., Boiko, K.A., and Polyakov, L.M., Biomed. Khim., 2018, vol. 64, pp. 195–200. CrossRefGoogle Scholar
  61. 61.
    Christoffersson, G., Waldén, T., Sandberg, M., Opdenakker, G., Carlsson, P.-O., and Phillipson, M., Am. J. Pathol., 2015, vol. 185, no. 4, pp. 1094–1103. CrossRefGoogle Scholar
  62. 62.
    Perez, S.E., Cano, D.A., Dao-Pick, T., Rougier, J.-P., Werb, Z., and Hebrok, M., Diabetes, 2005, vol. 54, no. 3, pp. 694–701.CrossRefGoogle Scholar
  63. 63.
    McLennan, S.V., Kelly, D.J., Schache, M., Waltham, M., Dy, V., Langham, R.G., Yue, D.K., and Gilbert, R.E., Kidney Int., 2007, vol. 72, no. 4, pp. 481–488. CrossRefGoogle Scholar
  64. 64.
    Aston-Mourney, K., Zraika, S., Udayasankar, J., Subramanian, S.L., Green, P.S., Kahn, S.E., and Hull, R.L., J. Biol. Chem., 2013, vol. 288, no. 5, pp. 3553–3559. CrossRefGoogle Scholar
  65. 65.
    Anderson, S.S., Wu, K., Nagase, H., Stettler-Stevenson, W.G., Kim, Y., and Tsilibary, E.C., Cell. Adhes. Commun., 1996, vol. 4, no. 2, pp. 89–101.CrossRefGoogle Scholar
  66. 66.
    Khasigov, P.Z., Ktsoeva, S.A., Gatagonova, T.M., Grachev, S.V., Tareeva, I.E., Grachev, S.V., and Berezov, T.T., Biochemistry (Moscow), 2000, vol. 65, no. 5, pp. 613–619.Google Scholar
  67. 67.
    Portik-Dobos, V., Anstadt, M.P., Hutchinson, J., Bannan, M., and Erqul, A., Diabetes, 2002, vol. 51, no. 10, pp. 3063–3068. CrossRefGoogle Scholar
  68. 68.
    Rittie, L., Berton, A., Monboisse, J.C., Hornebeck, W., and Gillery, P., Biochem. Biophys. Res. Commun., 1999, vol. 264, no. 2, pp. 488–492.CrossRefGoogle Scholar
  69. 69.
    Lan, C.C., Liu, I.H., Fang, A.H., Wen, C.H., and Wu, C.S., Br. J. Dermatol., 2008, vol. 159, no. 5, pp. 1103–1115. Google Scholar
  70. 70.
    Rysz, J., Banach, M., Stolarek, R.A., Pasnik, J., Cialkowska-Rysz, A., Koktysz, R., Piechota, M., and Baj, Z., J. Nephrol., 2007, vol. 20, no. 4, pp. 444–452.Google Scholar
  71. 71.
    Usynin, I.F., Dudarev, A.N., Gorodetskaya, A.Yu., Miroshnichenko, S.M., Tkachenko, T.A., and Tkachenko, V.I., Byull. Eksper. Biol. Med., 2017, vol. 164, no. 9, pp. 285–288.Google Scholar
  72. 72.
    Panin, L.E., Poteryaeva, O.N., Shevkoplyas, O.P., Voronova, O.S., and Kostina, N.E., Probl. Endokrinol., 2003, vol. 49, no. 4, pp. 4–8.Google Scholar
  73. 73.
    Hu, Z., Lu, Y., and Mao, T., J. Chung Hua Nei Ko Tsa Chih., 1997, vol. 36, no. 3, pp. 173–176.Google Scholar
  74. 74.
    Kurashvili, L.V., Semechkina, E.A., Adonina, T.S., Zueva, G.F., and Zakharova, I.R., Probl. Endocrinol., 1998, vol. 44, no. 3, pp. 10–12.Google Scholar
  75. 75.
    Kaseta, J.R., Skafar, D.F., Ram, J.L., and Jacber, S.J., J. Clin. Endocrin. Metab., 1999, vol. 84, no. 6, pp. 124–132.CrossRefGoogle Scholar
  76. 76.
    Verges, B.L., Diabetes Metab., 1999, vol. 25, no. 3, pp. 32–40.Google Scholar
  77. 77.
    Glinkina, I.V., Lechashchii Vrach, 2002, vol. 6, pp. 6–8.Google Scholar
  78. 78.
    Sniderman, A.D., Lamarche, B., Tilley, J., Seccombe, D., and Frohlich, J., Diabetes Care, 2002, 25, no. 3, pp. 579–582.CrossRefGoogle Scholar
  79. 79.
    Protasov, K.V., Sibirskyi Meditsinskyi Zhurnal, 2012, vol. 5, pp. 5–9.Google Scholar
  80. 80.
    Forte, T., Obrazovanie i struktura lipoproteidov vysokoi plotnosti (Formation and Structure of High Density Lipoproteins). Materials of the First Soviet American Symposium, Leningrad, 1983, p. 320.Google Scholar
  81. 81.
    Ducobu, J., Diabetographia, 1997, vol. 10, pp. 8–12.Google Scholar
  82. 82.
    Gowri, M.S., Van der Westhuyzen, D.R., Bridges, S.R., and Anderson, J.W., Arterioscler. Thromb. Vasc. Biol., 1999, vol. 19, no. 9, pp. 2226–2233.CrossRefGoogle Scholar
  83. 83.
    Kontush, A., Cardiovascular. Res., 2014, vol. 103, pp. 341–349. CrossRefGoogle Scholar
  84. 84.
    Smith, J.D., Arterioscler. Thromb. Vasc. Biol., 2010, vol. 30, pp. 151–155. CrossRefGoogle Scholar
  85. 85.
    Hwang, Y.-C., Ahn, H.-Y., Park, S.-W., and Park, C.-Y., Eur. J. Endocrinol., 2014, vol. 171, pp. 137–142. CrossRefGoogle Scholar
  86. 86.
    Verges, B.L., Diabetes Metab., 1999, vol. 25, no. 3, pp. 32–40.Google Scholar
  87. 87.
    Salem, M., Kamadan, L., and Bahgat, N., J. Egypt. Med. Assoc., 1988, vol. 71, no. 1, pp. 149–157.Google Scholar
  88. 88.
    Onat, A., Hergenc, G., Bulur, S., Ugur, M., Kucukdurmaz, Z., and Can, G., Int. J. Cardiol., 2010, vol. 142, pp. 72–79. CrossRefGoogle Scholar
  89. 89.
    Nobecourt, E., Davies, M.J., Brown, B.E., Curtiss, L.K., Bonnet, D.J., Charlton, F., Januszew-ski, A.S., Jenkins, A.J., Barter, P.J., and Rye, K.A., Diabetologia, 2007, vol. 50, pp. 643–653. CrossRefGoogle Scholar
  90. 90.
    Tabel, F., Lambert, G., Cuesta Torres, L.F., Hou, L., Sotirchos, I., Touyz, R.M., Jenkins, A.J., Barter, P.J., and Rye, K.A., Arterioscler. Tromb. Vasc. Biol., 2011, vol. 31, pp. 1192–1200. CrossRefGoogle Scholar
  91. 91.
    Pan, B., Ren, H., He, Y., Lv, X., Ma, Y., Li, J., Huang, L., Yu, B., Kong, J., Niu, C., Zhang, Y., Sun, W., and Zheng, L., Clin. Cancer Res., 2012, vol. 7, no. 11, pp. 48 530–48 542. Google Scholar
  92. 92.
    Pan, B., Ren, H., He, Y., Lv, X., Ma, Y., Li, J., Huang, L., Yu, B., Kong, J., Niu, C., Zhang, Y., Sun, W., and Zheng, L., Int. J. Cancer., 2012, vol. 131, no. 1, pp. 70–82. CrossRefGoogle Scholar
  93. 93.
    Feng, H., Curr. Opin. Endocrinol. Diabetes Obes., 2009, vol. 16, pp. 156–162.CrossRefGoogle Scholar

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© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  1. 1.Institute of Biochemistry, Federal Research Center of Fundamental and Translation MedicineNovosibirskRussia

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