Hypothalamic S-Nitrosylation Contributes to the Counter-Regulatory Response Impairment following Recurrent Hypoglycemia

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Fioramonti, Xavier ^a,b   Deak, Adam ^a   Deshpande, Srinidhi ^a   Carneiro, Lionel ^b   Zhou, Chunxue ^a   Sayed, Nazish ^a   Orban, Branly ^a   Berlin, Joshua R ^a   Pénicaud, Luc ^b   Leloup, Corinne ^b   Beuve, Annie ^a   Routh, Vanessa H ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ADRENALIN; CATECHOLAMINE; DRINKING WATER; GLUCAGON; GUANYLATE CYCLASE; NITRIC OXIDE; NITROSO CYSTEINE; NITROSO DERIVATIVE; PIG INSULIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DESENSITIZATION; GLUCAGON BLOOD LEVEL; HYPERINSULINEMIA; HYPOGLYCEMIA; MALE; MEMBRANE POTENTIAL; NITROSYLATION; NONHUMAN; PROTEIN DEFECT; PROTEIN FUNCTION; PROTEIN INTERACTION; RAT; RECURRENT DISEASE; REGULATORY MECHANISM; ZONA INCERTA;

ACETYLCYSTEINE; ANIMALS; GLUCOSE; HYPOGLYCEMIA; HYPOTHALAMUS; INSULIN; MALE; NEURONS; RATS; REACTIVE OXYGEN SPECIES;

EID: 84880427635     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068709     Document Type: Article

References (40)

1. Cryer PE, (1981) Glucose counterregulation in man. Diabetes 30: 261-264.
2. Amiel SA, Tamborlane WV, Simonson DC, Sherwin RS, (1987) Defective glucose counterregulation after strict glycemic control of insulin-dependent diabetes mellitus. New EngJMed 316: 1376-1383.
3. Cryer PE, (2008) The barrier of hypoglycemia in diabetes. Diabetes 57: 3169-3176.
4. Borg MA, Sherwin RS, Borg WP, Tamborlane WV, Shulman GI, (1997) Local ventromedial hypothalamus glucose perfusion blocks counterregulation during systemic hypoglycemia in awake rats. J Clin Invest 99: 361-365.
5. Borg WP, During MJ, Sherwin RS, Borg MA, Brines ML, et al. (1994) Ventromedial hypothalamic lesions in rats suppress counterregulatory responses to hypoglycemia. J Clin Invest 93: 1677-1682.
6. Borg WP, Sherwin RS, During MJ, Borg MA, Shulman GI, (1995) Local ventromedial hypothalamus glucopenia triggers counterregulatory hormone release. Diabetes 44: 180-184.
7. Routh VH, (2002) Glucose-sensing neurons: are they physiologically relevant? Physiol Behav 76: 403-413.
8. Fioramonti X, Contie S, Song Z, Routh VH, Lorsignol A, et al. (2007) Characterization of glucosensing neuron subpopulations in the arcuate nucleus: integration in neuropeptide Y and pro-opio melanocortin networks? Diabetes 56: 1219-1227.
9. Song Z, Levin BE, McArdle JJ, Bakhos N, Routh VH, (2001) Convergence of pre- and postsynaptic influences on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 50: 2673-2681.
10. Wang R, Ingoglia NA, Routh VH, (2001) Arcuate (ARC) glucosensing neurons respond to physiologic changes in extracellular glucose. AbstrSocNeurosci 31: 947.
11. Song Z, Routh VH, (2006) Recurrent hypoglycemia reduces the glucose sensitivity of glucose-inhibited neurons in the ventromedial hypothalamus nucleus. Am J Physiol Regul Integr Comp Physiol 291: R1283-1287.
12. Fioramonti X, Marsollier N, Song Z, Fakira KA, Patel RM, et al. (2010) Ventromedial hypothalamic nitric oxide production is necessary for hypoglycemia detection and counterregulation. Diabetes 59: 519-528.
13. Murphy BA, Fakira KA, Song Z, Beuve A, Routh VH (2009) AMP-activated Protein Kinase (AMPK) and Nitric Oxide (NO) regulate the glucose sensitivity of ventromedial hypothalamic (VMH) glucose-inhibited (GI) neurons. Am J Physiol Cell Physiol.
14. Canabal DD, Song Z, Potian JG, Beuve A, McArdle JJ, et al. (2007) Glucose, insulin, and leptin signaling pathways modulate nitric oxide synthesis in glucose-inhibited neurons in the ventromedial hypothalamus. Am J Physiol Regul Integr Comp Physiol 292: R1418-1428.
15. Stamler JS, (2004) S-nitrosothiols in the blood: roles, amounts, and methods of analysis. Circ Res 94: 414-417.
16. Sayed N, Baskaran P, Ma X, van den Akker F, Beuve A, (2007) Desensitization of soluble guanylyl cyclase, the NO receptor, by S-nitrosylation. Proc Natl Acad Sci U S A 104: 12312-12317.
17. Singh P, Jain A, Kaur G, (2004) Impact of hypoglycemia and diabetes on CNS: correlation of mitochondrial oxidative stress with DNA damage. Mol Cell Biochem 260: 153-159.
18. De Groote J, Van Steenbergen W, (1995) Paracetamol intoxication and N-acetyl-cysteine treatment. Acta Gastroenterol Belg 58: 326-334.
19. Kamboj SS, Chopra K, Sandhir R, (2008) Neuroprotective effect of N-acetylcysteine in the development of diabetic encephalopathy in streptozotocin-induced diabetes. Metab Brain Dis 23: 427-443.
20. Carneiro L, Allard C, Guissard C, Fioramonti X, Tourrel-Cuzin C, et al. (2012) Importance of mitochondrial dynamin-related protein 1 in hypothalamic glucose sensitivity in rats. Antioxid Redox Signal 17: 433-444.
21. Szabados E, Fischer GM, Toth K, Csete B, Nemeti B, et al. (1999) Role of reactive oxygen species and poly-ADP-ribose polymerase in the development of AZT-induced cardiomyopathy in rat. Free Radic Biol Med 26: 309-317.
22. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH, (2001) Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3: 193-197.
23. Saberi M, Bohland M, Donovan CM, (2008) The locus for hypoglycemic detection shifts with the rate of fall in glycemia: the role of portal-superior mesenteric vein glucose sensing. Diabetes 57: 1380-1386.
24. Sayed N, Kim DD, Fioramonti X, Iwahashi T, Duran WN, et al. (2008) Nitroglycerin-induced S-nitrosylation and desensitization of soluble guanylyl cyclase contribute to nitrate tolerance. Circ Res 103: 606-614.
25. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS, (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6: 150-166.
26. Monteiro HP, Arai RJ, Travassos LR, (2008) Protein tyrosine phosphorylation and protein tyrosine nitration in redox signaling. Antioxid Redox Signal 10: 843-889.
27. McCrimmon RJ, Song Z, Cheng H, McNay EC, Weikart-Yeckel C, et al. (2006) Corticotrophin-releasing factor receptors within the ventromedial hypothalamus regulate hypoglycemia-induced hormonal counterregulation. J Clin Invest 116: 1723-1730.
28. Song Z, Routh VH, (2005) Differential effects of glucose and lactate on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 54: 15-22.
29. Shinozaki S, Choi CS, Shimizu N, Yamada M, Kim M, et al. (2011) Liver-specific inducible nitric-oxide synthase expression is sufficient to cause hepatic insulin resistance and mild hyperglycemia in mice. J Biol Chem 286: 34959-34975.
30. Fioramonti X, Song Z, Vazirani RP, Beuve A, Routh VH, (2011) Hypothalamic nitric oxide in hypoglycemia detection and counterregulation: a two-edged sword. Antioxid Redox Signal 14: 505-517.
31. Ridnour LA, Thomas DD, Mancardi D, Espey MG, Miranda KM, et al. (2004) The chemistry of nitrosative stress induced by nitric oxide and reactive nitrogen oxide species. Putting perspective on stressful biological situations. Biol Chem 385: 1-10.
32. Zafarullah M, Li WQ, Sylvester J, Ahmad M, (2003) Molecular mechanisms of N-acetylcysteine actions. Cell Mol Life Sci 60: 6-20.
33. Abrams J, (1991) Interactions between organic nitrates and thiol groups. Am J Med 91: 106S-112S.
34. De Vries N, De Flora S (1993) N-acetyl-l-cysteine. J Cell Biochem Suppl 17F: 270-277.
35. Song D, Hutchings S, Pang CC, (2005) Chronic N-acetylcysteine prevents fructose-induced insulin resistance and hypertension in rats. Eur J Pharmacol 508: 205-210.
36. Cooper CE, (2003) Competitive, reversible, physiological? Inhibition of mitochondrial cytochrome oxidase by nitric oxide. IUBMB Life 55: 591-597.
37. Suh SW, Hamby AM, Gum ET, Shin BS, Won SJ, et al. (2008) Sequential release of nitric oxide, zinc, and superoxide in hypoglycemic neuronal death. J Cereb Blood Flow Metab 28: 1697-1706.
38. Jaillard T, Roger M, Galinier A, Guillou P, Benani A, et al. (2009) Hypothalamic reactive oxygen species are required for insulin-induced food intake inhibition: an NADPH oxidase-dependent mechanism. Diabetes 58: 1544-1549.
39. Barglow KT, Knutson CG, Wishnok JS, Tannenbaum SR, Marletta MA, (2011) Site-specific and redox-controlled S-nitrosation of thioredoxin. Proc Natl Acad Sci U S A 108: E600-606.
40. Stamler JS, Hess DT, (2010) Nascent nitrosylases. Nat Cell Biol 12: 1024-1026.