Regulation of glucose homeostasis in humans with denervated livers

Journal of Clinical Investigation

Volumn 100, Issue 4, 1997, Pages 931-941

  Perseghin, Gianluca ^a   Regalia, Enrico ^b   Battezzati, Alberto ^a   Vergani, Sandro ^a   Pulvirenti, Andrea ^b   Terruzzi, Ileana ^a   Baratti, Dario ^b   Bozzetti, Federico ^b   Mazzaferro, Vincenzo ^b   Luzi, Livio ^a,c  

^a UNIVERSITY OF MILAN   (Italy)

^b NATIONAL CANCER INSTITUTE   (Italy)

^c SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

Autonomic innervation; Endogenous glucose production; Insulin; Insulin resistance; Liver transplantation

Indexed keywords

AZATHIOPRINE; C PEPTIDE; CYCLOSPORIN A; GLUCAGON; GLUCOSE; INSULIN; PREDNISONE;

ADULT; ARTICLE; CONTROLLED STUDY; GLUCONEOGENESIS; GLUCOSE CLAMP TECHNIQUE; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GRAFT REJECTION; HUMAN; HYPERGLYCEMIA; HYPERINSULINEMIA; HYPOGLYCEMIA; IMMUNOSUPPRESSIVE TREATMENT; INSULIN CLEARANCE; INSULIN RESISTANCE; LIVER CIRRHOSIS; LIVER TRANSPLANTATION; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; UVEITIS;

EID: 0030865881     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119609     Document Type: Article

References (58)

1. Bernard, C. 1849. Chiens rendus diabetiques. C.R. Seances Soc. Biol. Fil. 1:60-78.
2. Havel, P.J., and J.G. Taborsky. 1989. The contribution of autonomic nervous system to changes of glucagon and insulin secretion during hypoglycemic stress. Endocr. Rev. 10:332-350.
3. Rohner-Jeanrenaud, F., E. Bobbioni, E. Jonescu, J.F. Sauter, and B. Janrenaud. 1983. Central nervous system regulation of insulin secretion. II. CNS-integrated afferent and efferent signals that modulate insulin secretion during periods of plenty and scarcity. Adv. Metab. Disord. 10:198-201.
4. Shimazu, T. 1983. Reciprocal innervation of the liver: its significance in metabolic control. Adv. Metab. Disord. 10:355-384.
5. Miller, R.E. 1981. Pancreatic neuroendocrinology: peripheral neural mechanisms in the regulation of the islets of Langerhans. Endocr. Rev. 2:471-490.
6. Smith, G.P., J. Gibbs, A.J. Strohmayer, A.W. Root, and P.E. Stokes. 1973. Effect of 2-deoxy-D-glucose on insulin response to glucose in intact and adrenalectomized monkeys. Endocrinology. 92:750-758.
7. Benzo, C.A. 1983. The hypothalamus and blood glucose regulation. Life Sci. 32:2509-2515.
8. Shimazu, T., and A. Amakawa. 1968. Regulation of glycogen metabolism in liver by the autonomic nervous system. III. Differential effects of sympathetic nerve stimulation and of catecholamine on liver phosphorylase. Biochim. Biophys. Acta. 165:349-356.
9. Jarhult, J., B. Falck, S. Ingemansson, and A. Nobin. 1979. The functional importance of sympathetic nerves to the liver and endocrine pancreas. Ann. Surg. 189:96-100.
10. Pagano, G., P. Cavallo-Perin, M. Cassader, A. Bruno, A. Ozzello, P. Masciola, A.M. Dall'Olmo, and B. Imbimbo. 1983. An in vivo and in vitro study of the mechanism of prednisone-induced insulin resistance in healthy subjects. J. Clin. Invest. 72:1814-1820.
11. Nielsen, J.H., T. Mandrup-Poulsen, and J. Nerup. 1986. Direct effect of CyA on human pancreatic β-cell. Diabetes. 35:1049-1052.
12. Mazzaferro, V., E. Regalia, R. Doci, S. Andreola, A. Pulvirenti, F. Bozzetti, F. Montalto, M. Ammatuna, A. Morabito, and L. Gennari. 1996. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N. Engl. J. Med. 334:693-699.
13. Luzi, L., A. Secchi, F. Facchini, A. Battezzati, C. Staudacher, D. Spotti, R. Castoldi, G. Ferrari, V. Di Carlo, and G. Pozza. 1990. Reduction of insulin resistance by combined kidney-pancreas transplantation in type 1 (insulin-dependent) diabetic patients. Diabetologia. 33:549-556.
14. De Fronzo, R.A., J.D. Tobin, and R. Andres. 1979. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am. J. Physiol. 6:E214-E223.
15. Battezzati, A., L. Luzi, G. Perseghin, E. Bianchi, D. Spotti, A. Secchi, S. Vergani, V. Di Carlo, and G. Pozza. 1994. Persistence of counter-regulatory abnormalities in insulin-dependent diabetes mellitus after pancreas transplantation. Eur. J. Clin. Invest. 24:751-758.
16. Luzi, L., A. Battezzati, G. Perseghin, E. Bianchi, S. Vergani, A. Secchi, E. La Rocca, C. Staudacher, D. Spotti, G. Ferrari, et al. 1992. Lack of feed-back inhibition of insulin secretion in denervated human pancreas. Diabetes. 41:1632-1639.
17. Steele, R. 1959. Influence of glucose loading and of injected insulin on hepatic glucose output. Ann. NY Acad. Sci. 82:420-430.
18. Frayn, K.N. 1983. Calculation of substrate oxidation rates in vivo from gaseous exchange. J. Appl. Physiol. 55:628-634.
19. Lusk, G. 1924. Animal calorimetry: analysis of the oxidation of mixtures of carbohydrate and fat. J. Biol. Chem. 59:41-42.
20. Hawk, P.D. 1947. Kjedhal method. In Practical Physiological Chemistry. 12th ed. Blakiston, Toronto. 814-822.
21. Barbara, L., G. Benzi, S. Gaiani, F. Fusconi, G. Zironi, S. Siringo, A. Rigamonti, C. Barbara, W. Grigioni, and A. Mazziotti. 1992. Natural history of small untreated hepatocellular carcinoma in cirrhosis: a multivariate analysis of prognostic factors of tumor growth rate and patient survival. Hepatology. 16:132-137.
22. Ringe. B., R. Pichlmayr, C. Wittekind, and G. Tusch. 1991. Surgical treatment of hepatocellular carcinoma: experience with liver resection and transplantation in 198 patients. World J. Surg. 15:270-285.
23. Iwatsuki, S., T.E. Starzl, D.G. Sheahan, I. Yokoyama, A.J. Demetris, S. Todo, A.G. Tzakis, D.H. Van Thiel, B. Carr, R. Selby, and J. Madariaga. 1991. Hepatic resection versus transplantation for hepatocellular carcinoma. Ann. Surg. 214:221-228.
24. Luzi, L., G. Perseghin, E. Regalia, L. Piceni Sereni, A. Battezzati, D. Baratti, E. Blanchi, I. Terruzzi, H. Hilden, L.C. Groop, et al. 1997. Metabolic effects of liver transplantation in cirrhotic patients. J. Clin. Invest. 99:692-700.
25. Petrides, A.S., and R.A. De Fronzo. 1989. Glucose metabolism in cirrhosis: a review with some perspective for the future. Diabetes Metab. Rev. 5:691-709.
26. Selberg, O., W. Burchert, J. van der Hoff, G.J. Meyer, H. Hundeshagen, E. Radoch, H.-J. Balks, and M.J. Müller. 1993. Insulin resistance in liver cirrhosis. Positron-emission tomography scan analysis of skeletal muscle glucose metabolism. J. Clin. Invest. 91:1897-1902.
27. Cavallo-Perin, P., M. Cassader, C. Bozzo, A. Bruno, P. Nuccio, A.M. Dall'Olmo, M. Marucci, and G. Pagano. 1985. Mechanism of insulin resistance in human liver cirrhosis. Evidence of a combined receptor and postreceptor defect. J. Clin. Invest. 75:1659-1665.
28. Megyesi, C., E. Samols, and V. Marks. 1967. Glucose tolerance and diabetes in chronic liver disease. Lancet. 2:1055-1061.
29. Rizza, R., L.J. Mandarino, and E. Gerich. 1981. Dose-response characteristics for effects of insulin on production and utilization of glucose in man. Am. J. Physiol. 240:E630-E639.
30. De Fronzo, R.A., and E. Ferrannini. 1987. Regulation of hepatic glucose metabolism in humans. Diabetes Metab. Rev. 3:415-459.
31. De Fronzo, R.A., E. Ferrannini, R. Hendler, P. Felig, and J. Wharen. 1983. Regulation of splanchnic and peripheral glucose uptake by insulin and hyperglycemia in man. Diabetes. 32:35-45.
32. Roden, M., G. Perseghin, K.F. Petersen, J.-H. Hwang, G.W. Cline, K. Gerow, D.L. Rothman, and G.I. Shulman. 1996. The roles of insulin and glucagon in the regulation of hepatic glycogen synthesis and turnover in humans. J. Clin. Invest. 97:642-648.
33. Rossetti, L., D. Smith, G.I. Shulman, D. Papachristou, and R.A. De Fronzo. 1987. Correction of hyperglycemia with phlorizin normalizes tissue sensitivity to insulin in diabetic rats. J. Clin. Invest. 79:1510-1515.
34. Woods, S.C., and D. Porte Jr. 1977. Relationship between plasma and cerebrospinal fluid insulin levels in dogs. Am. J. Physiol. 233:E331-E334.
35. Grunstein, H.S., D.E. James, L.H. Storlien, G.A. Smythe, and E.W. Kraegen. 1985. Hyperinsulinemia suppresses glucose utilization in specific brain regions: in vivo studies using the euglycemic clamp in the rat. Endocrinology. 116:604-610.
36. Schwartz, M.W., D.P. Figlewicz, D.G. Baskin, S.C. Woods, and D. Porte Jr. 1992. Insulin in the brain: a hormonal regulator of energy balance. Endocr. Rev. 13:387-414.
37. Boon, A.P., S.G. Hubscher, J.A. Lee, J.E. Hines, and A.D. Burt. 1992. Hepatic re-innervation following orthotopic liver transplantation in man. J. Pathol. 167:217-222.
38. Kjaer, M., J. Jurlander, S. Keiding, H. Galbo, P. Kirkegaard, and E. Hage. 1994. No reinnervation of hepatic sympathetic nerves after liver transplantation in human subjects. J. Hepatol. 20:97-100.
39. Hansen, C.P., S. Boesby, and P. Kirkegaard. 1991. Glucose homeostasis after orthotopic liver transplantation in the pig. Transplantation (Baltimore). 51:587-589.
40. Lindfeldt, J., B. Ahren, and T. Holmin. 1993. Glucose homeostasis after peri-arterial hepatic denervation in partially hepatectomized rats. Res. Exp. Med. 193:397-405.
41. Wada, M., C.C. Connolly, C. Tarumi, D.W. Neal, and A.D. Cherrington. 1995. Hepatic denervation does not significantly change the response of the liver to glucagon in conscious dogs. Am. J. Physiol. 268:E194-E203.
42. Krentz, A.J., B. Dousset, D. Mayer, P. McMaster, J. Buckels, R. Cramb, J.M. Smith, and M. Nattrass. 1993. Metabolic effects of cyclosporin A and FK 506 in liver transplant recipients. Diabetes. 42:1753-1759.
43. Navasa, M., F. Feu, J.C. Garcia-Pagan, W. Jimenez, J. Llach, A. Rimola, J. Bosch, and J. Rodes. 1993. Hemodynamic and humoral changes after liver transplantation in patients with cirrhosis. Hepatology. 17:355-360.
44. Lautt, W.W. 1983. Afferent and efferent neural roles in liver function. Prog. Neurobiol. (Oxf.). 21:323-348.
45. Niijima, A. 1981. Visceral afferents and metabolic function. Diabetologia. 20(Suppl.):325-330.
46. Okazaki, H., K. Tanaka, H. Nagase, and S. Inoue. 1993. Modulation of insulin secretion by hepatic vagotomy in cirrhotic rats. Physiol. Behav. 53:521-525.
47. Tanaka, K., S. Inoue, S. Saito, H. Nagase, and Y. Takamura. 1993. Hepatic vagal amino acid sensors modulate amino acid induced insulin and glucagon secretion in the rat. J. Auton. Nerv. Syst. 42:225-231.
48. Carobi, C., and F. Magni. 1981. The afferent innervation of the liver: a horseradish peroxidase study in the rat. Neurosci. Lett. 23:269-274.
49. Lamarche, L., N. Yamaguchi, and F. Peronnet. 1995. Hepatic denervation reduces adrenal catecholamine secretion during insulin-induced hypoglycemia. Am. J. Physiol. 268:R50-R57.
50. Novin, D., D.A. Vanderweele, and M. Rezeck. 1973. Infusion of 2-deoxy-D-glucose into the hepatic-portal system causes eating: evidence for peripheral glucoreceptors. Science (Wash. DC). 181:858-860.
51. Russek, M. 1963. Participation of hepatic glucoreceptors in the control of food intake. Nature (Lond.). 197:79-80.
52. Schmitt, M. 1973. Influences of hepatic portal receptors on hypothalamic feeding and satiety centers. Am. J. Physiol. 225:1089-1095.
53. Sawchenko, P.E., and M.I. Friedman. 1979. Sensory function of the liver: a review. Am. J. Physiol. 236:R5-R20.
54. Donovan, C.M., M. Hamilton-Wessler, J.B. Halter, and R.N. Bergman. 1994. Primacy of liver glucosensors in the sympathetic response to progressive hypoglycemia. Proc. Natl. Acad. Sci. USA. 91:2863-2867.
55. Cuneo, R.C., P.E. Hickman, J.D. Wallace, B.T. Teh, G. Ward, J.D. Veldhuis, and M.J. Waters. 1995. Altered endogenous growth hormone secretory kinetics and diurnal GH-binding protein profiles in adults with chronic liver disease. Clin. Endocrinol. 43:265-275.
56. Chiasson, J.-L., J.E. Liljenquist, B.C. Sinclair-Smith, and W.W. Lacy. 1975. Gluconeogenesis from alanine in normal postabsorptive man: intrahepatic stimulatory effect of glucagon. Diabetes. 24:574-584.
57. Stevenson, R.W., K.E. Steiner, M.A. Davis, G.K. Hendrick, P.E. Williams, W.W. Lacy, L. Brown, P. Donahue, D.B. Lacy, and A.D. Cherrington. 1987. Similar dose responsiveness of hepatic glycogenolysis and gluconeogenesis to glucagon in vivo. Diabetes. 36:382-389.
58. Groen, A.K., R.C. Vervoorn, R. Van der Meer, and J.M. Tager. 1983. Control of gluconeogenesis in rat liver cells. I. Kinetics of the individual enzymes and the effect of glucagon. J. Biol. Chem. 258:14346-14353.