Nitric oxide-mediated cutaneous microvascular function is impaired in polycystic ovary sydrome but can be improved by exercise training

Journal of Physiology

Volumn 591, Issue 6, 2013, Pages 1475-1487

  Sprung, V S ^a   Cuthbertson, D J ^b   Pugh, C J A ^a   Daousi, C ^b   Atkinson, G ^c   Aziz, N F ^d   Kemp, G J ^e   Green, D J ^a,f   Cable, N T ^a   Jones, H ^a  

^a LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^b UNIVERSITY HOSPITAL AINTREE   (United Kingdom)

^c TEESSIDE UNIVERSITY   (United Kingdom)

^d LIVERPOOL WOMEN S HOSPITAL   (United Kingdom)

^e UNIVERSITY OF LIVERPOOL   (United Kingdom)

^f UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

N(G) METHYLARGININE; NITRIC OXIDE;

ADULT; AEROBIC EXERCISE; ARTICLE; BIOAVAILABILITY; CARDIOPULMONARY FUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; EXERCISE INTENSITY; FEMALE; HOMEOSTASIS; HUMAN; INSULIN RESISTANCE; KINESIOTHERAPY; LASER DOPPLER FLOWMETRY; MICROANGIOPATHY; MICRODIALYSIS; OBESITY; OVARY POLYCYSTIC DISEASE; PRIORITY JOURNAL; TREATMENT OUTCOME; VASODILATATION;

ADULT; CASE-CONTROL STUDIES; ENZYME INHIBITORS; EXERCISE; EXERCISE THERAPY; FEMALE; HEART DISEASES; HEART FUNCTION TESTS; HOT TEMPERATURE; HUMANS; INSULIN RESISTANCE; LASER-DOPPLER FLOWMETRY; LIPOPROTEINS, LDL; MICRODIALYSIS; MICROVESSELS; NITRIC OXIDE; OMEGA-N-METHYLARGININE; POLYCYSTIC OVARY SYNDROME; REGIONAL BLOOD FLOW; SKIN; VASODILATION;

EID: 84875059486     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.246918     Document Type: Article

References (51)

1. Abdul-Ghani MA, Matsuda M, Balas B & DeFronzo RA (2007). Muscle and liver insulin resistance indexes derived from the oral glucose tolerance test. Diabetes Care 30, 89-94.
2. Alexandraki K, Protogerou AD, Papaioannou TG, Piperi C, Mastorakos G, Lekakis J, Panidis D & Diamanti-Kandarakis E (2006). Early microvascular and macrovascular dysfunction is not accompanied by structural arterial injury in polycystic ovary syndrome. Hormones (Athens) 5, 126-136.
3. Atkinson G & Batterham AM (2012). The use of ratios and percentage changes in sports medicine: time for a rethink Int J Sports Med 33, 505-506.
4. Atkinson G, Pugh C & Scott MA (2010). Exploring data distribution prior to analysis: benefits and pitfalls. Int J Sports Med 31, 841-842.
5. Azziz R, Carmina E, Dewailly D, Diamanti-Kandarakis E, Escobar-Morreale HF, Futterweit W, Janssen OE, Legro RS, Norman RJ, Taylor AE & Witchel SF; Androgen Excess Society (2006). Positions statement: criteria for defining polycystic ovary syndrome as a predominantly hyperandrogenic syndrome: an Androgen Excess Society guideline. J Clin Endocrinol Metab 91, 4237-4245.
6. Azziz R, Woods KS, Reyna R, Key TJ, Knochenhauer ES & Yildiz BO (2004). The prevalence and features of the polycystic ovary syndrome in an unselected population. J Clin Endocrinol Metab 89, 2745-2749.
7. Black MA, Green DJ & Cable NT (2008). Exercise prevents age-related decline in nitric-oxide-mediated vasodilator function in cutaneous microvessels. J Physiol 586, 3511-3524.
8. Borg G (1998). Borg's Perceived Exertion and Pain Scales Human Kinetics Publishers, Champaign, Illinois
9. Broekmans FJ, Knauff EA, Valkenburg O, Laven JS, Eijkemans MJ & Fauser BC (2006). PCOS according to the Rotterdam consensus criteria: change in prevalence among WHO-II anovulation and association with metabolic factors. BJOG 113, 1210-1217.
10. Bruce RA, Kusumi F & Hosmer D (1973). Maximal oxygen intake and nomographic assessment of functional aerobic impairment in cardiovascular disease. Am Heart J 85, 546-562.
11. Burkhalter N (1996). Evaluation of Borg's perceived exertion scale in cardiac rehabilitation. [Article in Portuguese.] Rev Lat Am Enfermagem 4, 65-73.
12. Carmina E, Bucchieri S, Mansueto P, Rini G, Ferin M & Lobo RA (2009). Circulating levels of adipose products and differences in fat distribution in the ovulatory and anovulatory phenotypes of polycystic ovary syndrome. Fertil Steril 91, 1332-1335.
13. Carmina E, Orio F, Palomba S, Longo RA, Cascella T, Colao A, Lombardi G, Rini GB & Lobo RA (2006). Endothelial dysfunction in PCOS: role of obesity and adipose hormones. Am J Med 119, 356.e1-356.e6.
14. Cracowski JL, Minson CT, Salvat-Melis M & Halliwill JR (2006). Methodological issues in the assessment of skin microvascular endothelial function in humans. Trends Pharmacol Sci 27, 503-508.
15. Dietz NM, Rivera JM, Warner DO & Joyner MJ (1994). Is nitric oxide involved in cutaneous vasodilation during body heating in humans J Appl Physiol 76, 2047-2053.
16. Frangos JA, Eskin SG, McIntire LV & Ives CL (1985). Flow effects on prostacyclin production by cultured human endothelial cells. Science 227, 1477-1479.
17. Giles TD, Sander GE, Nossaman BD & Kadowitz PJ (2012). Impaired vasodilation in the pathogenesis of hypertension: focus on nitric oxide, endothelial-derived hyperpolarizing factors, and prostaglandins. J Clin Hypertens (Greenwich) 14, 198-205.
18. Goldsmith PC, Leslie TA, Hayes NA, Levell NJ, Dowd PM & Foreman JC (1996). Inhibitors of nitric oxide synthase in human skin. J Invest Dermatol 106, 113-118.
19. Goodarzi MO, Dumesic DA, Chazenbalk G & Azziz R (2011). Polycystic ovary syndrome: etiology, pathogenesis and diagnosis. Nat Rev Endocrinol 7, 219-231.
20. Goto C, Higashi Y, Kimura M, Noma K, Hara K, Nakagawa K, Kawamura M, Chayama K, Yoshizumi M & Nara I (2003). Effect of different intensities of exercise on endothelium-dependent vasodilation in humans: role of endothelium-dependent nitric oxide and oxidative stress. Circulation 108, 530-535.
21. Green DJ (2009). Exercise training as vascular medicine: direct impacts on the vasculature in humans. Exerc Sport Sci Rev 37, 196-202.
22. Green DJ, Carter HH, Fitzsimons MG, Cable NT, Thijssen DH & Naylor LH (2010). Obligatory role of hyperaemia and shear stress in microvascular adaptation to repeated heating in humans. J Physiol 588, 1571-1577.
23. Green DJ, Jones H, Thijssen D, Cable NT & Atkinson G (2011). Flow-mediated dilation and cardiovascular event prediction: does nitric oxide matter Hypertension 57, 363-369.
24. Green DJ, O'Driscoll G, Joyner MJ & Cable NT (2008). Exercise and cardiovascular risk reduction: time to update the rationale for exercise J Appl Physiol 105, 766-768.
25. Hambrecht R, Adams V, Erbs S, Linke A, Krankel N, Shu Y, Baither Y, Gielen S, Thiele H, Gummert JF, Mohr FW & Schuler G (2003). Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation 107, 3152-3158.
26. Herman SM, Robinson JT, McCredie RJ, Adams MR, Boyer MJ & Celermajer DS (1997). Androgen deprivation is associated with enhanced endothelium-dependent dilatation in adult men. Arterioscler Thromb Vasc Biol 17, 2004-2009.
27. Holowatz LA, Thompson CS, Minson CT & Kenney WL (2005). Mechanisms of acetylcholine-mediated vasodilatation in young and aged human skin. J Physiol 563, 965-973.
28. Holowatz LA, Thompson-Torgerson CS & Kenney WL (2008). The human cutaneous circulation as a model of generalized microvascular function. J Appl Physiol 105, 370-372.
29. Houghton BL, Meendering JR, Wong BJ & Minson CT (2006). Nitric oxide and noradrenaline contribute to the temperature threshold of the axon reflex response to gradual local heating in human skin. J Physiol 572, 811-820.
30. Jones H, Sprung VS, Pugh CJ, Daousi C, Irwin A, Aziz N, Adams VL, Thomas EL, Bell JD, Kemp GJ & Cuthbertson DJ (2012). Polycystic ovary syndrome with hyperandrogenism is characterized by an increased risk of hepatic steatosis compared to nonhyperandrogenic PCOS phenotypes and healthy controls, independent of obesity and insulin resistance. J Clin Endocrinol Metab 97, 3709-3716.
31. Ketel IJ, Stehouwer CD, Serné EH, Korsen TJ, Hompes PG, Smulders YM, de Jongh RT, Homburg R & Lambalk CB (2008). Obese but not normal-weight women with polycystic ovary syndrome are characterized by metabolic and microvascular insulin resistance. J Clin Endocrinol Metab 93, 3365-3372.
32. Khan F, Davidson NC, Littleford RC, Litchfield SJ, Struthers AD & Belch JJ (1997). Cutaneous vascular responses to acetylcholine are mediated by a prostanoid-dependent mechanism in man. Vasc Med 2, 82-86.
33. Khan F, Litchfield SJ, Stonebridge PA & Belch JJ (1999). Lipid-lowering and skin vascular responses in patients with hypercholesterolaemia and peripheral arterial obstructive disease. Vasc Med 4, 233-238.
34. Khan F, Patterson D, Belch JJ, Hirata K & Lang CC (2008). Relationship between peripheral and coronary function using laser Doppler imaging and transthoracic echocardiography. Clin Sci (Lond) 115, 295-300.
35. Lakhani K, Leonard A, Seifalian AM & Hardiman P (2005). Microvascular dysfunction in women with polycystic ovary syndrome. Hum Reprod 20, 3219-3224.
36. Mathur RS, Moody LO, Landgrebe S & Williamson HO (1981). Plasma androgens and sex hormone-binding globulin in the evaluation of hirsute females. Fertil Steril 35, 29-35.
37. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF & Turner RC (1985). Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412-419.
38. Middlebrooke AR, Elston LM, Macleod KM, Mawson DM, Ball CI, Shore AC & Tooke JE (2006). Six months of aerobic exercise does not improve microvascular function in type 2 diabetes mellitus. Diabetologia 49, 2263-2271.
39. Minson CT, Berry LT & Joyner MJ (2001). Nitric oxide and neurally mediated regulation of skin blood flow during local heating. J Appl Physiol 91, 1619-1626.
40. Minson CT, Holowatz LA, Wong BJ, Kenney WL & Wilkins BW (2002). Decreased nitric oxide- and axon reflex-mediated cutaneous vasodilation with age during local heating. J Appl Physiol 93, 1644-1649.
41. Moran LJ, Misso ML, Wild RA & Norman RJ (2010). Impaired glucose tolerance, type 2 diabetes and metabolic syndrome in polycystic ovary syndrome: a systematic review and meta-analysis. Hum Reprod Update 16, 347-363.
42. Perneger TV (1998). What's wrong with Bonferroni adjustments. BMJ 316, 1236-1238.
43. Rizzoni D, Porteri E, Boari GE, De Ciuceis C, Sleiman I, Muiesan ML, Castellano M, Miclini M & Agabiti-Rosei E (2003). Prognostic significance of small-artery structure in hypertension. Circulation 108, 2230-2235.
44. Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group (2004). Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil Steril 81, 19-25.
45. Shojaee-Moradie F, Baynes KC, Pentecost C, Bell JD, Thomas EL, Jackson NC, Stolinski M, Whyte M, Lovell D, Bowes SB, Gibney J, Jones RH & Umpleby AM (2007). Exercise training reduces fatty acid availability and improves the insulin sensitivity of glucose metabolism. Diabetologia 50, 404-413.
46. Simmons GH, Wong BJ, Holowatz LA & Kenney WL (2011). Changes in the control of skin blood flow with exercise training: where do cutaneous vascular adaptations fit in Exp Physiol 96, 822-828.
47. Sokolnicki LA, Khosla S & Charkoudian N (2007a). Effects of testosterone and estradiol on cutaneous vasodilation during local warming in older men. Am J Physiol Endocrinol Metab 293, E1426-E1429.
48. Sokolnicki LA, Roberts SK, Wilkins BW, Basu A & Charkoudian N (2007b). Contribution of nitric oxide to cutaneous microvascular dilation in individuals with type 2 diabetes mellitus. Am J Physiol Endocrinol Metab 292, E314-E318.
49. Sprung VS, Atkinson G, Cuthbertson DJ, Pugh CJ, Aziz N, Green DJ, Cable NT & Jones H (2013). Endothelial function measured using flow mediated dilation in polycystic ovarian syndrome: a meta-analysis of the observational studies. Clin Endocrinol (Oxf) 78, 438-446.
50. Wenner MM, Taylor HS & Stachenfeld NS (2011). Endothelin B receptor contribution to peripheral microvascular function in women with polycystic ovary syndrome. J Physiol 589, 4671-4679.
51. Wild RA, Carmina E, Diamanti-Kandarakis E, Dokras A, Escobar-Morreale HF, Futterweit W, Lobo R, Norman RJ, Talbott E & Dumesic DA (2010). Assessment of cardiovascular risk and prevention of cardiovascular disease in women with the polycystic ovary syndrome: a consensus statement by the Androgen Excess and Polycystic Ovary Syndrome (AE-PCOS) Society. J Clin Endocrinol Metab 95, 2038-2049.