Successful intensive insulin treatment of type 1 diabetic dogs leads to restoration of peripheral leukocyte insulin signaling gene expression and enzyme activities

Journal of Veterinary Medical Science

Volumn 71, Issue 8, 2009, Pages 1017-1026

  Mori, Akihiro ^a   Lee, Peter ^b   Sako, Toshinori ^a   Mizutani, Hisashi ^b   Arai, Toshiro ^b  

^a School of Veterinary Nursing and Technology   (Japan)

^b NIPPON VETERINARY AND LIFE SCIENCE UNIVERSITY   (Japan)

Author keywords

Diabetes mellitus; Dogs; Insulin receptor substrate; Intensive glycemic control; Leukocytes

Indexed keywords

ANTIDIABETIC AGENT; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; INSULIN; INSULIN RECEPTOR SUBSTRATE; MALATE DEHYDROGENASE; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; RNA;

ANIMAL; ANIMAL DISEASE; ARTICLE; DOG; DOG DISEASE; DRUG EFFECT; ENERGY METABOLISM; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GLUCOSE BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; ISOLATION AND PURIFICATION; LEUKOCYTE; MALE; METABOLISM; PHYSIOLOGY; REFERENCE VALUE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 1; DOG DISEASES; DOGS; ENERGY METABOLISM; FEMALE; GENE EXPRESSION REGULATION; GLUCOSEPHOSPHATE DEHYDROGENASE; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; LEUKOCYTES; MALATE DEHYDROGENASE; MALE; REFERENCE VALUES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; RNA, MESSENGER;

CANIS FAMILIARIS;

EID: 70349448505     PISSN: 09167250     EISSN: 13477439     Source Type: Journal    
DOI: 10.1292/jvms.71.1017     Document Type: Article

References (60)

1. Ainscow, E.K., Zhao, C. and Rutter, G.A. 2000. Acute overexpression of lactate dehydrogenase-A perturbs β-cell mitochondrial metabolism and insulin secretion. Diabetes 49: 1149-1155.
2. Alba-Loureiro, T.C., Hirabara, S.M., Mendonça, J.R., Curi, R. and Pithon-Curi, T.C. 2006. Diabetes causes marked changes in function and metabolism of rat neutrophils. J. Endocrinol. 188: 295-303.
3. Alcazar, O., Tiedge, M. and Lenzen, S. 2000. Importance of lactate dehydrogenase for the regulation of lgycolytic flux and insulin secretion in insulin-producing cells. Biochem. J. 352: 373-380.
4. Ardawi, M.S. 1988. Glutamine and glucose metabolism in human peripheral lymphocytes. Metabolism 37: 99-103.
5. Beck, W.S. and Valentine, W.N. 1952. The aerobic carbohydrate metabolism of leukocytes in health and leukemia. II. The effect of various substrates and coenzymes on glycolysis and respiration. Cancer. Res. 12: 823-828.
6. Beck-Nielsen, H., Pedersen, O., Kragballe, K. and Sorensen, N.S. 1977. The monocyte as a model for the study of insulin receptors in man. Diabetologia 13: 563-569.
7. Bergmeyer, H.U. and Bernt, E. 1974a. Malate dehydrogenase UV-assay. pp. 613-617. In: Methods of Enzymatic Analysis, vol. 2 (Bergmeyer, H.U. ed.), Verlag Chemie, New York.
8. Bergmeyer, H.U., Gawehn, K. and Grassl, M. 1974b. Hexokinase from yeast. pp. 473-474. In: Methods of Enzymatic Analysis, vol. 1 (Bergmeyer, H.U. ed.), Verlag Chemie, New York.
9. Bergmeyer, H.U., Gawehn, K. and Grassl, M. 1974c. Glucose-6-phosphate dehydrogenase from yeast. pp. 458-459. In: Methods of Enzymatic Analysis, vol. 1 (Bergmeyer, H.U. ed.), Verlag Chemie, New York.
10. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
11. Cavalot, F., Anfossi, G., Russo, I., Mularoni, E., Massucco, P., Burzacca, S., Mattiello, L. and Trovati, M. 1992. Insulin, at physiological concentrations, enhances the polymorphonuclear leukocyte chemotactic properties. Horm. Metab. Res. 24: 225-228.
12. Cheatham, B. and Kahn, C.R. 1995. Insulin action and the insulin signaling network. Endocr. Rev. 16: 117-142.
13. Crofford, O.B. 1995. Diabetes control and complications. Annu. Rev. Med. 46: 267-279.
14. DCTT Research Group. 1993. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial (DCTT) Research Group. N. Engl. J. Med. 329: 977-986.
15. Esmann, V. 1972. The diabetic leukocyte. Enzyme 13: 32-55.
16. Estrada, D.E., Elliott, E., Zinman, B., Poon, I., Liu, Z., Klip, A. and Daneman, D. 1994. Regulation of glucose transport and expression of GLUT3 transporters in human circulating mono-nuclear cells: studies in cells from insulin-dependent diabetic and nondiabetic individuals. Metabolism 43: 591-598.
17. Feldman, E.C. and Nelson, R.W. 2004. Diabetes mellitus. pp. 486-538. In: Canine and Feline Endocrinology and Reproduction, 3rd., ed. W.B. Saunders, Philadelphia.
18. Fujita, Y., Fukushima, M., Suzuki, H., Taniguchi, A., Nakai, Y., Kuroe, A., Yasuda, K., Hosokawa, M., Yamada, Y., Inagaki, N. and Seino, Y. 2008. Short-term intensive glycemic control improves vibratory sensation in type 2 diabetes. Diabetes Res. Clin. Pract. 80: 16-19.
19. Fussganger, R.D., Kahn, C.R., Roth, J. and De Meyts, P. 1976. Binding and degradation of insulin by human peripheral granulocytes. Demonstration of specific receptors with high affinity. J. Biol. Chem. 251: 2761-2769.
20. Gould, G.W. and Holman, G.D. 1993. The glucose transporter family: structure, function and tissue-specific expression. Biochem. J. 295: 329-341.
21. Guimarães, A.R., Costa-Rosa, L.F., Safi, D.A. and Curi, R. 1993. Effects of a polyunsaturated fatty-acid rich diet on macrophage and lymphocyte metabolism of diabetic rats. Braz. J. Med. Biol. Res. 26: 813-818.
22. Hashimoto, H., Arai, T., Takeguchi, A., Hioki, K., Ohnishi, Y., Kawai, K., Ito, M., Suzuki, R., Yamauchi, T., Ohsugi, M., Saito, M., Ueyama, Y., Tobe, K., Kadowaki, T., Tamaoki, N. and Kosaka, K. 2006. Ontogenetic characteristics of enzyme activities and plasma metabolites in C57BL/6J:Jcl mice deficient in insulin receptor substrate 2. Comp. Med. 56: 176-187.
23. Helderman, J.H. and Strom, T.B. 1977. Emergence of insulin receptors upon alloimmune T cells in the rat. J. Clin. Invest. 59: 338-344.
24. Helderman, J.H. 1981. Role of insulin in the intermediary metabolism of the activated thymic-derived lymphocyte. J. Clin. Invest. 67: 1636-1642.
25. Hess, B. and Wieker, H-J. 1974. Pyruvate kinase from yeast. pp 778-783. In: Methods of Enzymatic Analysis, vol. 2 (Bergmeyer, H.U. ed.), Verlag Chemie, New York.
26. Joshi, N., Caputo, G.M., Weitekamp, M.R. and Karchmer, A.W. 1999. Infections in patients with diabetes mellitus. N. Engl. J. Med. 341: 1906-1912.
27. Kaloustian, H.D., Stolzenbach, F.E., Everse, J. and Kaplan, N.O. 1969. Lactate dehydrogenase of lobster (Hornarus americanus) tail muscle. I. Physical and chemical properties. J. Biol. Chem. 244: 2891-2901.
28. Kerouz, N.J., Horsch, D., Pons, S. and Kahn, C.R. 1997. Differential regulation of insulin receptor substrates-1 and -2 (IRS-1 and IRS-2) and phosphatidylinositol 3-kinase isoforms in liver and muscle of the obese diabetic (ob/ob) mouse. J. Clin. Invest. 100: 3164-3172.
29. Kosicki, G.W. and Srere, P.A. 1961. Kinetic studies on the citrate-condensing enzyme. J. Biol. Chem. 236: 2560-2565.
30. Kumagai, J., Akiyama, H., Iwashita, S., Iida, H. and Yahara, I. 1981. In vitro regeneration of resting lymphocytes from stimulated lymphocytes and its inhibition by insulin. J. Immunol. 126: 1249-1254.
31. Longo, N. and Elsas, L.J. 1998. Human glucose transporters. Adv. Pediatr. 45: 293-313.
32. Maratou, E., Dimitriadis, G., Kollias, A., Boutati, E., Lambadiari, V., Mitrou, P. and Raptis, S.A. 2007. Glucose transporter expression on the plasma membrane of resting and activated white blood cells. Eur. J. Clin. Invest. 37: 282-290.
33. Mori, A., Lee, P., Takemitsu, H., Iwasaki, E., Kimura, N., Yagishita, M., Hayasaka, M. and Arai, T. 2009. Decreased gene expression of insulin signaling genes in insulin sensitive tissues of obese cats. Vet. Res. Commun. 33: 315-329.
34. Mori, A., Lee, P., Takemitsu, H., Sako, T. and Arai, T. 2009. Comparison of insulin signaling gene expression in insulin sensitive tissues between cats and dogs. Vet. Res. Commun. 33: 211-226.
35. Mori, A., Sagara, F., Shimizu, S., Mizutani, H., Sako, T., Hirose, H., Yoshimura, I., Uematsu, Y., Yamaguchi, T. and Arai, T. 2008. Changes in peripheral lymphocyte subsets in the type 1 diabetic dogs treated with insulin injections. J. Vet. Med. Sci. 70: 185-187.
36. Mori, A., Sako, T., Lee, P., Motoike, T., Iwase, K., Kanaya, Y., Fukuta, H., Mizutani, H. and Arai, T. 2008. Comparison of time-action profiles of insulin Glargine and NPH insulin in normal and diabetic dogs. Vet. Res. Commun. 32: 563-573.
37. Mowat, A. and Baum, J. 1971. Chemotaxis of polymorphonuclear leukocytes from patients with diabetes mellitus. N. Engl. J. Med. 284: 621-627.
38. Muggeo, M., Moghetti, P., Querena, M., Cacciatori, V., Zoppini, G., Zenere, M., Tosi, F., Travia, D. and Bonora, E. 1993. Monnonuclear leukocytes from obese patients with type II diabetes have reduced activity of hexokinase, 6-phosphofructokinase and glucose-6-phosphate dehydrogenase. Horm. Metab. Res. 25: 160-164.
39. Newsholme, E.A. and Dimitriadis, G. 2001. Integration of biochemical and physiologic effects of insulin on glucose metabolism. Exp. Clin. Endocrinol. Diabetes. 109: S122-134.
40. Newsholme, E.A., Newsholme, P. and Curi, R. 1987. The role of the citric acid cycle in cells of the immune system and its importance in sepsis, trauma and burns. Biochem. Soc. Symp. 54: 145-162.
41. Okuno, Y. and Gliemann, J. 1988. Effect of chemotactic factors on hexose transport in polymorphonuclear leucocytes. Biochim. Biophys. Acta. 941: 157-164.
42. Oldenborg, P.A. and Sehlin, J. 1998. Insulin-stimulated chemokinesis in normal human neutrophils is dependent on Dglucose concentration and sensitive to inhibitors of tyrosine kinase and phosphatidylinositol 3-kinase. J. Leukoc. Biol. 63: 203-208.
43. Piatkiewicz, P., Czech, A. and Tatoń, J. 2007. Glucose transport in human peripheral blood lymphocytes influenced by type 2 diabetes mellitus. Arch. Immunol. Ther. Exp. (Warsz). 55: 119-126.
44. Powers, A.C., Solomon, S.S. and Duckworth, W.C. 1980. Insulin Degradation by mononuclear cells. Diabetes 29: 27-32.
45. Rand, J.S., Fleeman, L.M., Farrow, H.A., Appleton, D.J. and Lederer, R. 2004. Canine and feline diabetes mellitus: nature or nurture? J. Nutr. 134: 2072S-2080S.
46. Rej, R. and Horder, M. 1983. Aspartate aminotransferase (glutamate oxaloacetate transaminase). pp. 416-433. In: Methods of Enzymatic Analysis, vol. 3 (Bergmeyer, H.U. ed.), Verlag Chemie, New York.
47. Roep, B.O. 2003. The role of T cells in the pathogenesis of Type 1 diabetes: from cause to cure. Diabetologia 46: 305-321.
48. Rondinone, C.M., Wang, L.M., Lonnroth, P., Wesslau, C., Pierce, J.H. and Smith, U. 1997. Insulin receptor substrate (IRS) 1 is reduced and IRS-2 is the main docking protein for phosphatidylinositol 3-kinase in adipocytes from subjects with non-insulin-dependent diabetes mellitus. Proc. Natl. Acad. Sci. U.S.A. 94: 4171-4175.
49. Sako, T., Mori, A., Lee, P., Takahashi, T., Izawa, T., Karasawa, S., Furuuchi, M., Azakami, D., Mizukoshi, M., Mizutani, H., Kiyosawa, Y. and Arai, T. 2008.Diagnostic significance of serum glycated albumin in diabetic dogs. J. Vet. Diagn. Invest. 20: 634-638.
50. Schmidt, E. 1974. Glutamate dehydrogenase UV-assay. pp. 650-656. In: Methods of Enzymatic Analysis, vol. 2 (Bergmeyer, H.U. ed.), Verlag Chemie, New York.
51. Scrutton, M.C., Olmsted, M.R. and Utter, M.F. 1969. Pyruvate carboxylase from chicken liver. pp. 235-250. In: Methods of Enzymology, vol. 13 (Lowenstein, J.M. ed.), Academic Press, New York.
52. Shimomura, I., Matsuda, M., Hammer, R.E., Bashmakov, Y., Brown, M.S. and Goldstein, J.L. 2000. Decreased IRS-2 and increased SREBP-1c lead to mixed insulin resistance and sensitivity in livers of lipodystrophic and ob/ob mice. Mol. Cell. 6: 77-86.
53. Strom, T.B., Bear, R.A. and Carpenter, C.B. 1975. Insulininduced augmentation of lymphocyte-mediated cytotoxicity. Science 187: 1206-1208.
54. Sun, Y., Liu, S., Ferguson, S., Wang, L., Klepcyk, P., Yun, J.S. and Friedman, J.E. 2002. Phosphoenolpyruvate carboxykinase overexpression selectively attenuates insulin signaling and hepatic insulin sensitivity in transgenic mice. J. Biol. Chem. 277: 23301-23307.
55. Takeguchi, A., Urabe, S., Tanaka, A., Sako, T., Washizu, T., Morinaga, N., Kimura, N. and Arai, T. 2005. Activities of enzymes in some types of peripheral leucocytes may reflect the differences in nutrient metabolism between dogs and cats. Res. Vet. Sci. 78: 21-24.
56. Walrand, S., Guillet, C., Boirie, Y. and Vasson, M.P. 2004. In vivo evidences that insulin regulates human polymorphonuclear neutrophil functions. J. Leukoc. Biol. 76: 1104-1110.
57. Washizu, T., Kuramoto, E., Abe, M., Sako, T. and Arai, T. 1998. A comparison of the activities of certain enzymes related to energy metabolism in leukocytes in dogs and cats. Vet. Res. Commun. 22: 187-192.
58. Washizu, T., Takahashi, M., Azakami, D., Ikeda, M. and Arai, T. 2001. Activities of enzymes in the malate-aspartate shuttle in the peripheral leukocytes of dogs and cats. Vet. Res. Commun. 25: 623-629.
59. White, M.F. 1998. The IRS signaling system: a network of docking proteins that mediate insulin and cytokine action. Recent. Prog. Horm. Res. 53: 119-138.
60. Wu, G. and Greene, L.W., 1992. Glutamine and glucose metabolism in bovine blood lymphocytes. Comp. Biochem. Physiol. B 103: 821-825.