Sorbitol, Phosphoinositides, and Sodium-Potassium-ATPase in the Pathogenesis of Diabetic Complications

New England Journal of Medicine

Volumn 316, Issue 10, 1987, Pages 599-606

  Flier, Jeffrey S ^a,b   Underhill, Lisa H ^a,b   Greene, Douglas A ^a,b   Lattimer, Sarah A ^a,b   Sima, Anders A f ^a,b  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ALDOSE REDUCTASE INHIBITOR; SORBITOL;

ADULT; COMPLICATION; DIABETES MELLITUS; DIABETIC ANGIOPATHY; DIABETIC NEUROPATHY; ENDOCRINE SYSTEM; ETIOLOGY; HUMAN; PERIPHERAL NERVOUS SYSTEM; PERIPHERAL VASCULAR SYSTEM; PRIORITY JOURNAL; RAT; REVIEW;

ANIMAL; DIABETES MELLITUS; HUMAN; INOSITOL; NA(+)-K(+)-EXCHANGING ATPASE; PHOSPHATIDYLINOSITOLS; PROTEIN KINASE C; RATS; SORBITOL; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.;

EID: 0023116890     PISSN: 00284793     EISSN: 15334406     Source Type: Journal    
DOI: 10.1056/NEJM198703053161007     Document Type: Review

References (65)

1. Winegrad AI, Greene DA. Diabetic polyneuropathy: the importance of insulin deficiency, hyperglycemia and alterations in myoinositol metabolism in its pathogenesis. N Engl J Med 1976; 295: 1416–21.
2. Berridge MJ. Inositol triphosphate and diacylglycerol as second messengers. Biochem J 1984; 220: 345–60.
3. Greene DA, Lattimer S, Ulbrecht J, Carroll P. Glucose-induced alterations in nerve metabolism: current perspective on the pathogenesis of diabetic neuropathy and future directions for research and therapy. Diabetes Care 1985; 8: 290–9.
4. Greene DA, Lattimer SA. Protein kinase C agonists acutely normalize decreased ouabain-inhibitable respiration in diabetic rabbit nerve: implications for (Na,K)-ATPase regulation and diabetic complications. Diabetes 1986; 35: 242–5.
5. MacGregor LC, Rosecan LR, Laties AM, Matschinsky FM. Altered retinal metabolism in diabetes. I. Microanalysis of lipid, glucose, sorbitol, and myo-inositol in the choroid and in the individual layers of the rabbit retina. J Biol Chem 1986; 261: 4046–51.
6. Cohen MP, Dasmahapatra A, Shapiro E. Reduced glomerular sodium/potassium adenosine triphosphatase activity in acute streptozocin diabetes and its prevention by oral sorbinil. Diabetes 1985; 34: 1071–4.
7. Simmons DA, Kern EF, Winegrad AI, Martin DB. Basal phosphatidylinositol turnover controls aortic Na+/K+ ATPase activity. J Clin Invest 1986; 77: 503–13.
8. Stewart MA, Sherman WR, Kurien MM, Moonsammy GI, Wisgerhof M. Polyol accumulations in nervous tissue of rats with experimental diabetes and galactosaemia. J Neurochem 1967; 14: 1057–66.
9. Dawson RMC, Freinkel N. The distribution of free mesoinositol in mammalian tissues, including some observations on the lactating rat. Biochem J 1961; 78: 606–10.
10. Daughaday WH, Lamer J. The renal excretion of inositol in normal and diabetic human beings. J Clin Invest 1954; 33: 326–32.
11. Palmano KP, Whiting PH, Hawthorne JN. Free and lipid myo-inositol in tissues from rats with acute and less severe streptozotocin-induced diabetes. Biochem J 1977; 167: 229–35.
12. Mayhew JA, Gillon KRW, Hawthorne JN. Free and lipid inositol, sorbitol and sugars in sciatic nerve obtained post-mortem from diabetic patients and control subjects. Diabetologia 1983; 24: 13–5.
13. Pirie A, van Heyningen R. The effect of diabetes on the content of sorbitol, glucose, fructose and inositol in the human lens. Exp Eye Res 1964; 3: 124–31.
14. Greene DA, Yagihashi S, Lattimer SA, Sima AAF. Nerve Na+-K+ATPase, conduction, and myo-inositol in the insulin-deficient BB rat. Am J Physiol 1984; 247: E534–E539.
15. Greene DA, Lattimer SA. Impaired rat sciatic nerve sodium-potassium adenosine triphosphatase in acute streptozocin diabetes and its correction by dietary myo-inositol supplementation. J Clin Invest 1983; 72: 1058–63.
16. Finegold D, Lattimer SA, Nolle S, Bernstein M, Greene DA. Polyol pathway activity and myo-inositol metabolism: a suggested relationship in the pathogenesis of diabetic neuropathy. Diabetes 1983; 32: 988–92.
17. Gillon KRW, Hawthorne JN. Sorbitol, inositol and nerve conduction in diabetes. Life Sci 1983; 32: 1943–7.
18. Mayer JH, Tomlinson DR. Prevention of defects of axonal transport and nerve conduction velocity by oral administration of myo-inositol or an aldose reductase inhibitor in streptozotocin-diabetic rats. Diabetologia 1983; 25: 433–8.
19. Greene DA, Lattimer SA. Action of sorbinil in diabetic peripheral nerve: relationship of polyol (sorbitol) pathway inhibition to a myo-inositol-mediated defect in sodium-potassium ATPase activity. Diabetes 1984; 33: 712–6.
20. Gillon KRW, Hawthorne JN. Transport of myo-inositol into endoneurial preparations of sciatic nerve from normal and streptozotocin-diabetic rats. Biochem J 1983; 210: 775–81.
21. Greene DA, Winegrad AI. Effects of acute experimental diabetes on composite energy metabolism in peripheral nerve axons and Schwann cells. Diabetes 1981; 30: 967–74.
22. Greene DA, Lattimer SA. Sodium- and energy-dependent uptake of myo-inositol by rabbit peripheral nerve: competitive inhibition by glucose and lack of an insulin effect. J Clin Invest 1982; 70: 1009–18.
23. Greene DA, Mackway AM. Decreased myo-inositol content and Na+-K+ ATPase activity in the superior cervical ganglion of STZ diabetic rat, and prevention by aldose reductase inhibition. Diabetes 1986; 35: 1106–8.
24. Beyer-Mears A, Ku L, Cohen MP. Glomerular polyol accumulation in diabetes and its prevention by oral sorbinil. Diabetes 1984; 33: 604–7.
25. Ulbrecht JS, Bensen JT, Greene DA. Sodium-dependent myo-inositol uptake in isolated renal glomeruli: possible inhibition by glucose. Diabetes 1985; 34: Suppl 1: 13A. abstract.
26. Hammerman MR, Sacktor B, Daughaday WH. Myo-inositol transport in renal brush border vesicles and its inhibition by D-glucose. Am J Physiol 1980; 239: F113–F120.
27. Caspary WF, Crane RK. Active transport of myo-inositol and its relation to the sugar transport system in hamster small intestine. Biochim Biophys Acta 1970; 203: 308–16.
28. Gabbay KH. The sorbitol pathway and the complications of diabetes. N Engl J Med 1973; 288: 831–6.
29. Cogan DG, Kinoshita JH, Kador PF, et al. Aldose reductase and complications of diabetes. Ann Intern Med 1984; 101: 82–91.
30. Judzewitsch RG, Jaspan JB, Polonsky KS, et al. Aldose reductase inhibition improves nerve conduction velocity in diabetic patients. N Engl J Med 1983; 308: 119–25.
31. Cohen MP, Klepser H. Binding of an aldose reductase inhibitor to renal glomeruli. Biochem Biophys Res Commun 1980; 129: 530–5.
32. Charalampous FC. Metabolic functions of myo-inositol. VIII. Role of inositol in Na+-K+ transport and in NA+- and K+-activated adenosine triphosphatase of KB cells. J Biol Chem 1971; 246: 455–60.
33. Mandersloot JG, Roelofsen B, DeGier J. Phosphatidylinositol as the endogenous activator of the (Na+ + K+)-ATPase in microsomes of rabbit kidney. Biochem Biophys Acta 1978; 508: 478–85.
34. Roelofsen B. The (non)specificity in the lipid-requirement of calcium- and (sodium plus potassium)-transporting adenosine triphosphatases. Life Sci 1981; 29: 2235–47.
35. Das PK, Bray GM, Aguayo AJ, Rasminsky M. Diminished ouabain-sensitive, sodium-potassium ATPase activity in sciatic nerves of rats with streptozotocin-induced diabetes. Exp Neurol 1976; 53: 285–8.
36. Clements RS Jr. Diabetic neuropathy: new concepts of its etiology. Diabetes 1979; 28: 604–11.
37. Greene DA, Lattimer SA. Impaired energy utilization and Na-K-ATPase in diabetic peripheral nerve. Am J Physiol 1984; 246: E311–E318.
38. Brismar T, Sima AAF. Changes in nodal function in nerve fibers of the spontaneously diabetic BB-Wistar rat. Potential clamp analysis. Acta Physiol Scand 1981; 113: 499–506.
39. Simmons DA, Winegrad AI, Martin DB. Significance of tissue myo-inositol concentrations in metabolic regulation in nerve. Science 1982; 217: 848–51.
40. MacGregor LC, Matschinsky FM. Altered retinal metabolism in diabetes. II. Measurement of sodium-potassium ATPase and total sodium and potassium in individual retinal layers. J Biol Chem 1986; 261: 4052–8.
41. Dixon FJ, Hokin LE. The formation of inositol-1–2-cyclic phosphate on agonist stimulation of phosphoinositide breakdown in mouse pancreatic minilobules. Evidence for direct phosphodiesteratic cleavage of phosphatidylinositol. J Biol Chem 1985; 260: 16068–71.
42. Batty IR, Nahorski SR, Irvine RF. Rapid formation of inositol 1,3,4,5-tetrakisphosphate following muscarinic receptor stimulation of rat cerebral cortical slices. Biochem J 1985; 232: 211–5.
43. Kikkawa U, Nishizuka Y. Protein kinase C. In: Krebs EG, Boyer PD, eds. The enzymes. New York: Academic Press, 1986:167–89.
44. Hawthorne JN, Pickard MR, Griffin HD. Phosphatidylinositol, triphosphoinositide and synaptic transmission. In: Wells WW, Eisenberg F Jr, eds. Cyclitols and phosphoinositides. New York: Academic Press. 1978: 145–51.
45. Ling L, Cantley L. The (Na,K)-ATPase of Friend erythroleukemia cells is phosphorylated near the ATP hydrolysis by an endogenous membrane-bound kinase. J Biol Chem 1984; 259: 4089–95.
46. Vorbrodt AW, Lossinsky AS, Wisniewski HM. Cytochemical localization of ouabain-sensitive, K+-dependent p-nitro-phenylphosphatase (transport ATPase) in the mouse central and peripheral nervous system. Brain Res 1982; 243: 225–34.
47. Brismar T. Neuropathy-functional abnormalities in the BB rat. Metabolism 1983; 32: 112–7.
48. Sima AAF, Brismar T. Reversible diabetic nerve dysfunction: structural correlates to electrophysiological abnormalities. Ann Neurol 1985; 18: 21–9.
49. Sima AAF. Annotation: can the BB-rat help to unravel diabetic neuropathy? Neuropathol Appl Neurobiol 1985; 11: 253–64.
50. Sima AA, Lattimer SA, Yagihashi S, Greene DA. Axo-glial dysjunction: a novel structural lesion that accounts for poorly reversible slowing of nerve conduction in the spontaneously diabetic Bio-breeding rat. J Clin Invest 1986; 77: 474–84.
51. Sima AAF, Bril V, Greene DA. A new characteristic ultrastructural abnormality and morphological evidence for pathogenic heterogeneity in human diabetic neuropathy. Clin Res 1986; 34: 688A. abstract.
52. Robison WG Jr, Kador PF, Kinoshita JH. Retinal capillaries: basement membrane thickening by galactosemia prevented with aldose reductase inhibitor. Science 1983; 221: 1177–9.
53. Goldfarb S, Simmons DA, Kern E. Amelioration of glomerular hyperfiltration in acute experimental diabetes by dietary myo-inositol and by an aldose reductase inhibitor. Clin Res 1986; 34: 725A. abstract.
54. Greene DA, Brown M, Cleary P, Gilbert P, Nielsen VK, Pfeifer M. Age and gender as a factor in the development of diabetic neuropathy: baseline neurological assessment in the Diabetes Control and Complications Trial. Diabetes 1986; 35: Suppl 1: 12A. abstract.
55. Klein R, Klein BEK, Moss SE, David MD, DeMets DL. Retinopathy in young-onset diabetic patients. Diabetes Care 1985; 8: 311–5.
56. Williamson JR, Rowold E, Chang K, et al. Sex steroid dependency of diabetes-induced changes in polyol metabolism, vascular permeability, and collagen cross-linking. Diabetes 1986; 35: 20–7.
57. Sugimura K, Dyck PJ. Multifocal fiber loss in proximal sciatic nerve in symmetric distal diabetic neuropathy. J Neurol Sci 1982; 53: 501–9.
58. Tuck RR, Schmelzer JD, Low PA. Endoneurial blood flow and oxygen tension in the sciatic nerves of rats with experimental diabetic neuropathy. Brain 1984; 107: 935–50.
59. Young RJ, Ewing DJ, Clarke BF. A controlled trial of sorbinil, an aldose reductase inhibitor, in chronic painful diabetic neuropathy. Diabetes 1983; 32: 938–42.
60. Fagius J, Brattberg A, Jameson S, Berne C. Limited benefit of treatment of diabetic polyneuropathy with an aldose reductase inhibitor: a 24-week controlled trial. Diabetologia 1985; 28: 323–9.
61. Greene DA, Brown MJ, Braunstein SN, Schwartz SS, Asbury AK, Winegrad AI. Comparison of clinical course and sequential electrophysiological tests in diabetics with symptomatic polyneuropathy and its implications for clinical trials. Diabetes 1981; 30: 139–47.
62. Clements RS Jr, Vourganti B, Kuba T, Oh SJ, Darnell B. Dietary myo-inositol intake and peripheral nerve function in diabetic neuropathy. Metabolism 1979; 28: 477–83.
63. Gregersen G, Børsting H, Theil P, Servo C. Myoinositol and function of peripheral nerves in human diabetics: a controlled clinical trial. Acta Neurol Scand 1978; 58: 241–8.
64. Gregersen G, Bertelsen B, Harbo H, et al. Oral supplementation of myo-inositol: effects on peripheral nerve function in human diabetics and on the concentration in plasma, erythrocytes, urine and muscle tissue in human diabetics and normals. Acta Neurol Scand 1983; 67: 164–72.
65. Ishii DN, Recio-Pinto E, Spinelli W, Mill JF, Sonnenfeld KH. Neurite formation modulated by nerve growth factor, insulin, and tumor promoter receptors. Int J Neurosci 1985; 26: 109–27.