Insulin inhibits low oxygen-induced ATP release from human erythrocytes: Implication for vascular control

Microcirculation

Volumn 16, Issue 5, 2009, Pages 424-433

  Hanson, Madelyn S ^a   Ellsworth, Mary L ^a   Achilleus, David ^a   Stephenson, Alan H ^a   Bowles, Elizabeth A ^a   Sridharan, Meera ^a   Adderley, Shaquria ^a   Sprague, Randy S ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ATP; Erythrocyte; Hyperinsulinemia; Insulin; Prediabetes

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYCLIC AMP DEPENDENT PROTEIN KINASE; HEMOGLOBIN; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; INSULIN; MASTOPARAN; OXYGEN; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIAL OXYGEN TENSION; ARTERIOLE; ARTERY DILATATION; ARTICLE; BLOOD SAMPLING; BLOOD VESSEL DIAMETER; CONTROLLED STUDY; ENZYME RELEASE; ERYTHROCYTE; HAMSTER; HEMOLYSIS; HUMAN; HYPERINSULINEMIA; INCUBATION TIME; MALE; MUSCLE BLOOD VESSEL; NONHUMAN; OXYGEN SUPPLY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VASODILATATION;

ADENOSINE TRIPHOSPHATE; ADULT; ANIMALS; ARTERIOLES; BLOOD FLOW VELOCITY; CRICETINAE; ERYTHROCYTES; HUMANS; HYPERINSULINISM; HYPOGLYCEMIC AGENTS; INSULIN; MALE; MESOCRICETUS; MIDDLE AGED; MUSCLE, SKELETAL; OXYGEN; PEPTIDES;

EID: 68249155049     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1080/10739680902855218     Document Type: Article

References (57)

1. Ardigo D, Franzini L, Valtuena S, Monti LD, Reaven GM, Zavaroni I. (2006). Relation of plasma insulin levels to forearm flow-mediated dilatation in healthy volunteers. Am J Cardiol 97:1250-1254.
2. Bakker W, Sipkema P, Stehouwer CD, Serne EH, Smulders YM, et al. (2008). Protein kinase C theta activation induces insulin-mediated constriction of muscle resistance arteries. Diabetes 57:706-713.
3. 2 difference in type 2 diabetes. J Appl Physiol 94:1033-1038.
4. Bartels DW, Davidson MH, Gong WC. (2007). Type 2 diabetes and cardiovascular disease: Reducing the risk. J Manag Care Pharm 13:S2-S15; quiz, S6-S7.
5. Benjamin SM, Valdez R, Geiss LS, Rolka DB, Narayan KM. (2003). Estimated number of adults with prediabetes in the US in 2000: Opportunities for prevention. Diab Care 26:645-649.
6. Bergfeld GR, Forrester T. (1992). Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia. Cardiovasc Res 26: 40-47.
7. Boyle PJ. (2007). Diabetes mellitus and macrovascular disease: mechanisms and mediators. Am J Med 120:S12-S17.
8. Bylund-Fellenius AC, Idstrom JP, Holm S. (1984). Muscle respiration during exercise. Am Rev Respir Dis 129:S10-S12.
9. Bylund-Fellenius AC, Walker PM, Elander A, Holm S, Holm J, Schersten T. (1981). Energy metabolism in relation to oxygen partial pressure in human skeletal muscle during exercise. Biochem J 200: 247-255.
10. Dietrich HH, Ellsworth ML, Sprague RS, Dacey RG, Jr. (2000). Red blood cell regulation of microvascular tone through adenosine triphosphate. Am J Physiol Heart Circ Physiol 278:H1294-H1298.
11. Duling BR. (1974). Oxygen sensitivity of vascular smooth muscle. II. In vivo studies. Am J Physiol 227:42-49.
12. Ellsworth ML. (2000). The red blood cell as an oxygen sensor: What is the evidence? Acta Physiol Scand 168:551-559.
13. Ellsworth ML. (2004). Red blood cell-derived ATP as a regulator of skeletal muscle perfusion. Med Sci Sports Exerc 36:35-41.
14. Ellsworth ML, Forrester T, Ellis CG, Dietrich HH. (1995). The erythrocyte as a regulator of vascular tone. Am J Physiol 269:H2155-H2161.
15. Eringa EC, Stehouwer CD, Merlijn T, Westerhof N, Sipkema P. (2002). Physiological concentrations of insulin induce endothelin-mediated vasoconstriction during inhibition of NOS or PI3-kinase in skeletal muscle arterioles. Cardiovasc Res 56:464-471.
16. Eringa EC, Stehouwer CD, van Nieuw Amerongen GP, Ouwehand L, Westerhof N, Sipkema P. (2004). Vasoconstrictor effects of insulin in skeletal muscle arterioles are mediated by ERK1/2 activation in endothelium. Am J Physiol Heart Circ Physiol 287:H2043-H2048.
17. Hanson MS, Stephenson AH, Bowles EA, Sridharan M, Adderley S, Sprague RS. (2008). Phosphodiesterase 3 is present in rabbit and human erythrocytes and its inhibition potentiates iloprost-induced increases in cAMP. Am J Physiol Heart Circ Physiol 295:H786- H793.
18. Hester RL. (1993). Uptake of metabolites by postcapillary venules: mechanism for the control of arteriolar diameter. Microvasc Res 46:254-261.
19. Higashijima T, Burnier J, Ross EM. (1990). Regulation of Gi and Go by mastoparan, related amphiphilic peptides, and hydrophobic amines. Mechanism and structural determinants of activity. J Biol Chem 265:14176-14186.
20. Jaap AJ, Hammersley MS, Shore AC, Tooke JE. (1994). Reduced microvascular hyperaemia in subjects at risk of developing type 2 (non-insulindependent) diabetes mellitus. Diabetologia 37: 214-216.
21. Jaap AJ, Shore AC, Tooke JE. (1997). Relationship of insulin resistance to microvascular dysfunction in subjects with fasting hyperglycaemia. Diabetologia 40:238-243.
22. Jagger JE, Bateman RM, Ellsworth ML, Ellis CG. (2001). Role of erythrocyte in regulating local O2 delivery mediated by hemoglobin oxygenation. Am J Physiol Heart Circ Physiol 280:H2833-H2839.
23. Jung F, Kessler H, Pindur G, Sternitzky R, Franke RP. (1999). Intramuscular oxygen partial pressure in the healthy during exercise. Clin Hemorheol Microcirc 21:25-33.
24. Kawano H, Motoyama T, Hirashima O, Hirai N, Miyao Y, et al. (1999). Hyperglycemia rapidly suppresses flow-mediated endothelium-dependent vasodilation of brachial artery. J Am Coll Cardiol 34:146-154.
25. Kim SH, Reaven GM. (2008). Isolated impaired fasting glucose and peripheral insulin sensitivity: Not a simple relationship. Diab Care 31:347-352.
26. Lalande S, Gusso S, Hofman PL, Baldi JC. (2008). Reduced leg blood flow during submaximal exercise in type 2 diabetes. Med Sci Sports Exerc 40:612-617.
27. Lim SC, Tan HH, Goh SK, Subramaniam T, Sum CF, et al. (2006). Oxidative burden in prediabetic and diabetic individuals: Evidence from plasma coenzyme Q(10). Diab Med 23:1344-1349.
28. Lteif A, Vaishnava P, Baron AD, Mather KJ. (2007). Endothelin limits insulin action in obese/insulinresistant humans. Diabetes 56:728-734.
29. Lyssenko V, Almgren P, Anevski D, Perfekt R, Lahti K, et al. (2005). Predictors of and longitudinal changes in insulin sensitivity and secretion preceding onset of type 2 diabetes. Diabetes 54:166-174.
30. McVeigh GE, Brennan GM, Johnston GD, McDermott BJ, McGrath LT, et al. (1992). Impaired endothelium- dependent and -independent vasodilation in patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 35:771-776.
31. 2+ but requires phosphorylation by Akt at Ser(1179). J Biol Chem 276:30392-30398.
32. Mori Y, Hoshino K, Yokota K, Itoh Y, Tajima N. (2006). Japanese IGT subjects with high insulin response are far more frequently associated with the metabolic syndrome than those with low insulin response. Endocrine 29:351-355.
33. Olearczyk JJ, Stephenson AH, Lonigro AJ, Sprague RS. (2004). Heterotrimeric G protein Gi is involved in a signal transduction pathway for ATP release from erythrocytes. Am J Physiol Heart Circ Physiol 286:H940-H945.
34. Olearczyk JJ, Stephenson AH, Lonigro AJ, Sprague RS. (2004). NO inhibits signal transduction pathway for ATP release from erythrocytes via its action on heterotrimeric G protein Gi. Am J Physiol Heart Circ Physiol 287:H748-H754.
35. Psyrogiannis A, Habeos I, Kyriazopoulou V. (2003). Insulin sensitivity and Lp(alpha) concentrations in normoglycemic offspring of type 2 diabetic parents. Lipids Health Dis 2:8.
36. Rothermel JD, Parker Botelho LH. (1988). A mechanistic and kinetic analysis of the interactions of the diastereoisomers of adenosine 3′,5′-(cyclic)phosphorothioate with purified cyclic AMP-dependent protein kinase. Biochem J 251:757-762.
37. Sandeman DD, Pym CA, Green EM, Seamark C, Shore AC, Tooke JE. (1991). Microvascular vasodilatation in feet of newly diagnosed non-insulindependent diabetic patients. BMJ 302:1122-1123.
38. Schaap P, van Ments-Cohen M, Soede RD, Brandt R, Firtel RA, et al. (1993). Cell-permeable non-hydrolyzable cAMP derivatives as tools for analysis of signaling pathways controlling gene regulation in Dictyostelium. J Biol Chem 268:6323-6331.
39. Segura J, Campo C, Ruilope LM, Rodicio JL. (2005). Do we need to target "prediabetic" hypertensive patients? J Hypertens 23:2119-2125.
40. Shrot P, Sahebzamani FM, Brownlee, Jr HJ. (2004). Case study: Screening and treatment of pre-diabetes in primary care. Clin Diab 22:98-100.
41. Sprague R, Bowles E, Stumpf M, Ricketts G, Freidman A, et al. (2005). Rabbit erythrocytes possess adenylyl cyclase type II that is activated by the heterotrimeric G proteins Gs and Gi. Pharmacol Rep 57 (Suppl):222-228.
42. Sprague RS, Ellsworth ML, Stephenson AH, Kleinhenz ME, Lonigro AJ. (1998). Deformation-induced ATP release from red blood cells requires CFTR activity. Am J Physiol 275:H1726-H1732.
43. Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AJ. (1996). ATP: The red blood cell link to NO and local control of the pulmonary circulation. Am J Physiol 271:H2717--H2722.
44. Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AJ. (2001). Participation of cAMP in a signaltransduction pathway relating erythrocyte deformation to ATP release. Am J Physiol Cell Physiol 281:C1158-C1164.
45. Sprague RS, Olearczyk JJ, Spence DM, Stephenson AH, Sprung RW, Lonigro AJ. (2003). Extracellular ATP signaling in the rabbit lung: Erythrocytes as determinants of vascular resistance. Am J Physiol Heart Circ Physiol 285:H693-H700.
46. Sprague RS, Stephenson AH, Bowles EA, Stumpf MS, Lonigro AJ. (2006). Reduced expression of G(i) in erythrocytes of humans with type 2 diabetes is associated with impairment of both cAMP generation and ATP release. Diabetes 55:3588-3593.
47. Sprague RS, Stephenson AH, Ellsworth ML. (2007). Red not dead: Signaling in and from erythrocytes. Trends Endocrinol Metab 18:350-355.
48. Steinberg HO, Brechtel G, Johnson A, Fineberg N, Baron AD. (1994). Insulin-mediated skeletal muscle vasodilation is nitric oxide dependent. A novel action of insulin to increase nitric oxide release. J Clin Invest 94:1172-1179.
49. Strehler B, McElroy W. (1957). Assay of adenosine triphosphate. In: Colowick S, Kaplan N, eds. Methods in Ezymology (pp. 871-873). New York: Academic Press.
50. Su Y, Liu XM, Sun YM, Jin HB, Fu R, et al. (2008). The relationship between endothelial dysfunction and oxidative stress in diabetes and prediabetes. Int J Clin Pract 62:877-882.
51. Sullivan SM, Pittman RN. (1982). Hamster retractor muscle: A new preparation for intravital microscopy. Microvasc Res 23:329-335.
52. Tigno XT, Ding SY, Hansen BC. (2006). Paradoxical increase in dermal microvascular flow in pre-diabetes associated with elevated levels of CRP. Clin Hemorheol Microcirc 34:273-282.
53. Tooke JE. (1995). Microvascular function in human diabetes. A physiological perspective. Diabetes 44:721-726.
54. Vincent MA, Barrett EJ, Lindner JR, Clark MG, Rattigan S. (2003). Inhibiting NOS blocks microvascular recruitment and blunts muscle glucose uptake in response to insulin. Am J Physiol Endocrinol Metab 285:E123-E129.
55. Walsh DA. (1978). Role of the cAMP-dependent protein kinase as the transducer of cAMP action. Biochem Pharmacol 27:1801-1804.
56. Wiernsperger N. (2000). Defects in microvascular haemodynamics during prediabetes: Contributor or epiphenomenon? Diabetologia 43:1439-1448.
57. Williams SB, Cusco JA, Roddy MA, Johnstone MT, Creager MA. (1996). Impaired nitric oxide-mediated vasodilation in patients with non-insulin-dependent diabetes mellitus. J Am Coll Cardiol 27:567-574.