Portal vein hypoglycemia is essential for full induction of hypoglycemia-associated autonomic failure with slow-onset hypoglycemia

American Journal of Physiology - Endocrinology and Metabolism

Volumn 293, Issue 3, 2007, Pages

  Matveyenko, Aleksey V ^a,b   Bohland, MaryAnn ^a   Saberi, Maziyar ^a   Donovan, Casey M ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Counterregulation; Glucose sensor; Sympathoadrenal

Indexed keywords

ADRENALIN; GLUCAGON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTONOMIC DYSFUNCTION; CONTROLLED STUDY; DISEASE ASSOCIATION; GLUCOSE BLOOD LEVEL; GLUCOSE INFUSION; HORMONE RESPONSE; HYPOGLYCEMIA; INSULIN INFUSION; NONHUMAN; PORTAL VEIN; PRIORITY JOURNAL; RAT;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; GLUCOSE; HYPOGLYCEMIA; MALE; PORTAL VEIN; RATS; RATS, WISTAR;

EID: 34548420968     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00283.2007     Document Type: Article

References (51)

1. Amiel SA, Sherwin RS, Simonson DC, Tamborlane WV. Effect of intensive insulin therapy on glycemic thresholds for counterregulatory hormone release. Diabetes 37: 901-907, 1988.
2. Bohland MA, Watts AG, Donovan CM. Celiac-superior mesenteric ganglionectomy attenuates hypoglycemic activation of hindbrain neurons (Abstract). Diabetes 55S1: A16, 2006.
3. Boyle PJ. Alteration in brain glucose metabolism induced by hypoglycaemia in man. Diabetologia 40, Suppl 2: S69-S74, 1997.
4. Boyle PJ, Nagy RJ, O'Connor AM, Kempers SF, Yeo RA, Qualls C. Adaptation in brain glucose uptake following recurrent hypoglycemia. Proc Natl Acad Sci USA 91: 9352-9356, 1994.
5. Burcelin R, Dolci W, Thorens B. Glucose sensing by the hepatoportal sensor is GLUT2-dependent: in vivo analysis in GLUT2-null mice. Diabetes 49: 1643-1648, 2000.
6. Cryer PE. Banting Lecture Hypoglycemia: the limiting factor in the management of IDDM. Diabetes 43: 1378-1389, 1994.
7. Cryer PE. Hypoglycaemia: the limiting factor in the glycaemic management of Type I and Type II Diabetes. Diabetologia 45: 937-948, 2002.
8. Cryer PE. Hypoglycemia-associated autonomic failure in diabetes. Am J Physiol Endocrinol Metab 281: E1115-E1121, 2001.
9. Cryer PE. Mechanisms of hypoglycemia-associated autonomic failure and its component syndromes in diabetes. Diabetes 54: 3592-3601, 2005.
10. Cryer PE, Davis SN, Shamoon H. Hypoglycemia in diabetes. Diabetes Care 26: 1902-1912, 2003.
11. Davis SN, Mann S, Galassetti P, Neill RA, Tate D, Ertl AC, Costa F. Effects of differing durations of antecedent hypoglycemia on counterregulatory responses to subsequent hypoglycemia in normal humans. Diabetes 49: 1897-1903, 2000.
12. Davis SN, Shavers C, Costa F, Mosqueda-Garcia R. Role of cortisol in the pathogenesis of deficient counterregulation after antecedent hypoglycemia in normal humans. J Clin Invest 98: 680-691, 1996.
13. Davis SN, Shavers C, Davis B, Costa F. Prevention of an increase in plasma cortisol during hypoglycemia preserves subsequent counterregulatory responses. J Clin Invest 100: 429-438, 1997.
14. DCCT. Hypoglycemia in the Diabetes Control and Complications Trial. Diabetes 46: 271-286, 1997.
15. Donovan CM, Halter JB, Bergman RN. Importance of hepatic glucoreceptors in sympathoadrenal response to hypoglycemia. Diabetes 40: 155-158, 1991.
16. Donovan CM, Hamilton-Wessler M, Halter JB, Bergman RN. Primacy of liver glucosensors in the sympathetic response to progressive hypoglycemia. Proc Natl Acad Sci USA 91: 2863-2867, 1994.
17. Dunn-Meynell AA, Routh VH, Kang L, Gaspers L, Levin BE. Glucokinase is the likely mediator of glucosensing in both glucose-excited and glucose-inhibited central neurons. Diabetes 51: 2056-2065, 2002.
18. Evans SB, Wilkinson CW, Bentson K, Gronbeck P, Zavosh A, Figlewicz DP. PVN activation is suppressed by repeated hypoglycemia but not antecedent corticosterone in the rat. Am J Physiol Regul Integr Comp Physiol 281: R1426-R1436, 2001.
19. Fanelli CG, Epifano L, Rambotti AM, Pampanelli S, Di Vincenzo A, Modarelli F, Lepore M, Annibale B, Ciofetta M, Bottini P, Porcellati F, Scionti L, Santeusanio F. Meticulous prevention of hypoglycemia normalizes the glycemic thresholds and magnitude of most of neuroendocrine responses to, symptoms of, and cognitive function during hypoglycemia in intensively treated patients with short-term IDDM. Diabetes 42: 1683-1689, 1993.
20. Flanagan DE, Keshavarz T, Evans ML, Flanagan S, Fan X, Jacob RJ, Sherwin RS. Role of corticotrophin-releasing hormone in the impairment of counterregulatory responses to hypoglycemia. Diabetes 52: 605-613, 2003.
21. Fujita S, Donovan CM. Celiac-superior mesenteric ganglionectomy, but not vagotomy, suppresses the sympathoadrenal response to insulin-induced hypoglycemia. Diabetes 54: 3258-3264, 2005.
22. Heller SR, Cryer PE. Reduced neuroendocrine and symptomatic responses to subsequent hypoglycemia after 1 episode of hypoglycemia in nondiabetic humans. Diabetes 40: 223-226, 1991.
23. Hevener AL, Bergman RN, Donovan CM. Novel glucosensor for hypoglycemic detection localized to the portal vein. Diabetes 46: 1521-1525, 1997.
24. Hevener AL, Bergman RN, Donovan CM. Portal vein afferents are critical for the sympathoadrenal response to hypoglycemia. Diabetes 49: 8-12, 2000.
25. Inouye KE, Yue JT, Chan O, Kim T, Akirav EM, Park E, Riddell MC, Burdett E, Matthews SG, Vranic M. Effects of insulin treatment without and with recurrent hypoglycemia on hypoglycemic counterregulation and adrenal catecholamine-synthesizing enzymes in diabetic rats. Endocrinology 147: 1860-1870, 2006.
26. Ishise S, Pegram BL, Yamamoto J, Kitamura Y, Frohlich ED. Reference sample microsphere method: cardiac output and blood flows in conscious rat. Am J Physiol Heart Circ Physiol 239: H443-H449, 1980.
27. Jetton TL, Liang Y, Pettepher CC, Zimmerman EC, Cox FG, Horvath K, Matschinsky FM, Magnuson MA. Analysis of upstream glucokinase promoter activity in transgenic mice and identification of glucokinase in rare neuroendocrine cells in the brain and gut. J Biol Chem 269: 3641-3654, 1994.
28. Kale AY, Paranjape SA, Briski KPI. Administration of the nonsteroidal glucocorticoid receptor antagonist, CP-472555, prevents exacerbated hypoglycemia during repeated insulin administration. Neuroscience 140: 555-565, 2006.
29. Lamarche L, Yamaguchi N, Peronnet F. Hepatic denervation reduces adrenal catecholamine secretion during insulin-induced hypoglycemia. Am J Physiol Regul Integr Comp Physiol 268: R50-R57, 1995.
30. Levin BE, Routh VH, Kang L, Sanders NM, Dunn-Meynell AA. Neuronal glucosensing: What do we know after 50 years? Diabetes 53: 2521-2528, 2004.
31. Matveyenko AV, Donovan CM. Metabolic sensors mediate hypoglycemic detection at the portal vein. Diabetes 55: 1276-1282, 2006.
32. McCrimmon RJ, Song Z, Cheng H, McNay EC, Weikart-Yeckel C, Fan X, Routh VH, Sherwin RS. Corticotrophin-releasing factor receptors within the ventromedial hypothalamus regulate hypoglycemia-induced hormonal counterregulation. J Clin Invest 116: 1723-1730, 2006.
33. Morrison SF, Cao WH. Different adrenal sympathetic preganglionic neurons regulate epinephrine and norepinephrine secretion. Am J Physiol Regul Integr Comp Physiol 279: R1763-R1775, 2000.
34. Ohkubo Y, Kishikawa H, Araki E, Miyata T, Isami S, Motoyoshi S, Kojima Y, Furuyoshi N, Shichiri M. Intensive insulin therapy prevents the progression of diabetic microvascular complications in Japanese patients with non-insulin-dependent diabetes mellitus: a randomized prospective 6-year study. Diabetes Res Clin Pract 28: 103-117, 1995.
35. Paramore DS, Fanelli CG, Shah SD, Cryer PE. Hypoglycemia per se stimulates sympathetic neural as well as adrenomedullary activity, but, unlike the adrenomedullary response, the forearm sympathetic neural response is not reduced after recent hypoglycemia. Diabetes 48: 1429-1436, 1999.
36. Paranjape SA, Briski KP. Recurrent insulin-induced hypoglycemia causes site-specific patterns of habituation or amplification of CNS neuronal genomic activation. Neuroscience 130: 957-970, 2005.
37. Peuler JD, Johnson GA. Simultaneous single isotope radioenzymatic assay of plasma norepinephrine, epinephrine and dopamine. Life Sci 21: 625-636, 1977.
38. Powell AM, Sherwin RS, Shulman GI. Impaired hormonal responses to hypoglycemia in spontaneously diabetic and recurrently hypoglycemic rats. Reversibility and stimulus specificity of the deficits. J Clin Invest 92: 2667-2674, 1993.
39. Rattarasarn C, Dagogo-Jack S, Zachwieja JJ, Cryer PE. Hypoglycemia-induced autonomic failure in IDDM is specific for stimulus of hypoglycemia and is not attributable to prior autonomic activation. Diabetes 43: 809-818, 1994.
40. Sanders NM, Dunn-Meynell AA, Levin BE. Third ventricular alloxan reversibly impairs glucose counterregulatory responses. Diabetes 53: 1230-1236, 2004.
41. Sanders NM, Figlewicz DP, Taborsky GJ Jr, Wilkinson CW, Daumen W, Levin BE. Feeding and neuroendocrine responses after recurrent insulin-induced hypoglycemia. Physiol Behav 87: 700-706, 2006.
42. Sanders NM, Ritter S. Repeated 2-deoxy-D-glucose-induced glucoprivation attenuates Fos expression and glucoregulatory responses during subsequent glucoprivation. Diabetes 49: 1865-1874, 2000.
43. Sandoval DA, Ping L, Neill AR, Morrey S, Davis SN. Cortisol acts through central mechanisms to blunt counterregulatory responses to hypoglycemia in conscious rats. Diabetes 52: 2198-2204, 2003.
44. Schmitt M. Influences of hepatic portal receptors on hypothalamic feeding and satiety centers. Am J Physiol 225: 1089-1095, 1973.
45. Shimizu N, Oomura Y, Novin D, Grijalva CV, Cooper PH. Functional correlations between lateral hypothalamic glucose-sensitive neurons and hepatic portal glucose-sensitive units in rat. Brain Res 265: 49-54, 1983.
46. Smith D, Pernet A, Reid H, Bingham E, Rosenthal JM, Macdonald IA, Umpleby AM, Amiel SA. The role of hepatic portal glucose sensing in modulating responses to hypoglycaemia in man. Diabetologia 45: 1416-1424, 2002.
47. Song Z, Routh VH. Differential effects of glucose and lactate on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 54: 15-22, 2005.
48. Song Z, Routh VH. Recurrent hypoglycemia reduces the glucose sensitivity of glucose-inhibited neurons in the ventromedial hypothalamus nucleus. Am J Physiol Regul Integr Comp Physiol 291: R1283-R1287, 2006.
49. Vollmer RR, Baruchin A, Kolibal-Pegher SS, Corey SP, Stricker EM, Kaplan BB. Selective activation of norepinephrine- and epinephrine-secreting chromaffin cells in rat adrenal medulla. Am J Physiol Regul Integr Comp Physiol 263: R716-R721, 1992.
50. White NH, Skor DA, Cryer PE, Levandoski LA, Bier DM, Santiago JV. Identification of type I diabetic patients at increased risk for hypoglycemia during intensive therapy. N Engl J Med 308: 485-491, 1983.
51. Young JB, Rosa RM, Landsberg L. Dissociation of sympathetic nervous system and adrenal medullary responses. Am J Physiol Endocrinol Metab 247: E35-E40, 1984.