Xanthine oxidase and the fetal cardiovascular defence to hypoxia in late gestation ovine pregnancy

Journal of Physiology

Volumn 592, Issue 3, 2014, Pages 475-489

  Kane, Andrew D ^a   Hansell, Jeremy A ^a   Herrera, Emilio A ^b   Allison, Beth J ^a   Niu, Youguo ^a   Brain, Kirsty L ^a   Kaandorp, Joepe J ^c   Derks, Jan B ^c   Giussani, Dino A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CHILE   (Chile)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPURINOL; ANIMALS; BLOOD GLUCOSE; BLOOD PRESSURE; ENZYME INHIBITORS; FEMALE; FETAL HEART; FETAL HYPOXIA; GESTATIONAL AGE; HEART RATE; LACTIC ACID; NITRIC OXIDE; OXYGEN; OXYGEN CONSUMPTION; PREGNANCY; REACTIVE OXYGEN SPECIES; REGIONAL BLOOD FLOW; SHEEP; URIC ACID; VASOCONSTRICTION; XANTHINE OXIDASE;

EID: 84893387988     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.264275     Document Type: Article

References (43)

1. Apatu RS & Barnes RJ (1991). Release of glucose from the liver of fetal and postnatal sheep by portal vein infusion of catecholamines or glucagon. J Physiol 436, 449-468.
2. Bartelds B, van Bel F, Teitel D & Rudolph A (1993). Carotid, not aortic, chemoreceptors mediate the fetal cardiovascular response to acute hypoxemia in lambs. Pediatr Res 34, 51-55.
3. Benders M, Bos A, Rademaker C, Rijken M, Torrance H, Groenendaal F & van Bel F (2006). Early postnatal allopurinol does not improve short term outcome after severe birth asphyxia. Arch Dis Child Fetal Neonatal Ed 91, 163-165.
4. Berry C & Hare M (2004). Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms and pathophysiological implications. J Physiol 555, 589-606.
5. Boda D, Nemeth P, Kiss P & Orvos H (1999). Treatment of mothers with allopurinol to produce therapeutic blood levels in newborns. Prenat Neonat Med 4, 130-134.
6. Boyle D, Hirst K, Zerbe G, Meschia G & Wilkening R (1990). Fetal hind limb oxygen consumption and blood flow during acute graded hypoxia. Pediatr Res 28, 94-100.
7. Cappola TP, Kass DA, Nelson GS, Berger RD, Rosas GO, Kobeissi ZA, Marbán E & Hare JM (2001). Allopurinol improves myocardial efficiency in patients with idiopathic dilated cardiomyopathy. Circulation 104, 2407-2411.
8. Castelli P, Condemi A, Brambillasca C, Fundarò P, Botta M, Lemma M, Vanelli P, Santoli C, Gatti S & Riva E (1995). Improvement of cardiac function by allopurinol in patients undergoing cardiac surgery. J Cardiovasc Pharmacol 25, 119-125.
9. Clancy RR, McGaurn SA, Goin JE, Hirtz DG, Norwood WI, Gaynor JW, Jacobs ML, Wernovsky G, Mahle WT, Murphy JD, Nicolson SC, Steven JM & Spray TL (2001). Allopurinol neurocardiac protection trial in infants undergoing heart surgery using deep hypothermic circulatory arrest. Pediatrics 108, 61-70.
10. Coghlan J, Flitter W, Clutton S, Panda R, Daly R, Wright G, Ilsley C & Slater T (1994). Allopurinol pretreatment improves postoperative recovery and reduces lipid peroxidation in patients undergoing coronary artery bypass grafting. J Thorac Cardiovasc Surg 107, 248-256.
11. Cohn HE, Sacks EJ, Heymann MA & Rudolph AM (1974). Cardiovascular responses to hypoxemia and acidemia in fetal lambs. Am J Obstet Gynecol 120, 817-824.
12. Cowan F, Rutherford M, Groenendaal F, Eken P, Mercuri E, Bydder GM, Meiners LC, Dubowitz LM & de Vries LS (2003). Origin and timing of brain lesions in term infants with neonatal encephalopathy. Lancet 361, 736-742.
13. Derks J, Oudijk M, Torrance H, Rademaker C, Benders M, Rosen K, Cindrova-Davies T, Thakor A, Visser G, Burton G, van Bel F & Giussani D (2010). Allopurinol reduces oxidative stress in the ovine fetal cardiovascular system following repeated episodes of ischemia-reperfusion. Pediatr Res 68, 374-380.
14. Ekelund UEG, Harrison RW, Shokek O, Thakkar RN, Tunin RS, Senzaki H, Kass DA, Marbán E & Hare JM (1999). Intravenous allopurinol decreases myocardial oxygen consumption and increases mechanical efficiency in dogs with pacing-induced heart failure. Circ Res 85, 437-445.
15. Fletcher AJ, Edwards CM, Gardner DS, Fowden AL & Giussani DA (2000). Neuropeptide Y in the sheep fetus: effects of acute hypoxemia and dexamethasone during late gestation. Endocrinology 141, 3976-3982.
16. Gardner DS & Giussani DA (2003). Enhanced umbilical blood flow during acute hypoxemia after chronic umbilical cord compression: a role for nitric oxide. Circulation 108, 331-335.
17. Giussani DA & Davidge ST (2013). Developmental programming of cardiovascular disease by prenatal hypoxia. J Dev Orig Health Dis doi:10.1017/S204017441300010X, http://journals.cambridge.org/action/displayAbstract?fromPage=online&aid=8993851.
18. Giussani DA, Spencer JA, Moore PJ, Bennet L & Hanson MA (1993). Afferent and efferent components of the cardiovascular reflex responses to acute hypoxia in term fetal sheep. J Physiol 461, 431-449.
19. Herrera EA, Kane AD, Hansell JA, Thakor AS, Allison BJ, Niu Y & Giussani DA (2012). A role for xanthine oxidase in the control of fetal cardiovascular function in late gestation sheep. J Physiol 590, 1825-1837.
20. Iriyama K, Yoshiura M, Iwamoto T & Ozaki Y (1984). Simultaneous determination of uric and ascorbic acids in human serum by reversed-phase high-performance liquid chromatography with electrochemical detection. Anal Biochem 141, 238-243.
21. Johnson W, Kayser K, Brenowitz J & Saedi S (1991). A randomized controlled trial of allopurinol in coronary bypass surgery. Am Heart J 121, 20-24.
22. Jones C, Ritchie J & Walker D (1983). The effects of hypoxia on glucose turnover in the fetal sheep. J Dev Physiol 5, 223-235.
23. Jones CT (1977). The development of some metabolic responses to hypoxia in the foetal sheep. J Physiol 265, 743-762.
24. Jones CT & Ritchie J (1983). The effects of adrenergic blockade on fetal response to hypoxia. J Dev Physiol 5, 211-222.
25. Kaandorp J, Benders M, Rademaker C, Torrance H, Oudijk M, de Haan T, Bloemenkamp K, Rijken M, van Pampus M, Bos A, Porath M, Oetomo S, Willekes C, Gavilanes AD, Wouters M, van Elburg R, Huisjes A, Bakker S, van Meir C, von Lindern J, Boon J, de Boer I, Rijnders R, Jacobs C, Uiterwaal C, Mol BW, Visser G, van Bel F & Derks J (2010). Antenatal allopurinol for reduction of birth asphyxia induced brain damage (ALLO-Trial); a randomized double blind placebo controlled multicenter study. BMC Pregnancy Childbirth 10, 8.
26. Kaandorp JJ, Derks JB, Oudijk MA, Torrance HL, Harmsen MG, Nikkels PGJ, van Bel F, Visser GHA & Giussani DA (2013). Antenatal allopurinol reduces hippocampal brain damage after acute birth asphyxia in late gestation fetal sheep. Reprod Sci doi:10.1177/1933719113493516
27. Kaandorp JJ, van Bel F, Veen S, Derks JB, Groenendaal F, Rijken M, Roze E, Venema MMU, Rademaker CM, Bos AF & Benders MJ (2012). Long-term neuroprotective effects of allopurinol after moderate perinatal asphyxia: follow-up of two randomised controlled trials. Arch Dis Child Fetal Neonatal Ed 97, F162-F166.
28. Kane AD, Herrera EA, Hansell JA & Giussani DA (2012). Statin treatment depresses the fetal defence to acute hypoxia via increasing nitric oxide bioavailability. J Physiol 590, 323-334.
29. Kögler H, Fraser H, McCune S, Altschuld R & Marbán E (2003). Disproportionate enhancement of myocardial contractility by the xanthine oxidase inhibitor oxypurinol in failing rat myocardium. Cardiovasc Res 59, 582-592.
30. Lawrence GF, Brown VA, Parsons RJ & Cooke ID (1982). Feto-maternal consequences of high-dose glucose infusion during labour. Br J Obstet Gynaecol 89, 27-32.
31. Majmundar AJ, Wong WJ & Simon MC (2010). Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40, 294-309.
32. Masaoka N, Nakajima Y, Hayakawa Y, Ohgame S, Hamano S, Nagaishi M & Yamamoto T (2005). Transplacental effects of allopurinol on suppression of oxygen free radical production in chronically instrumented fetal lamb brains during intermittent umbilical cord occlusion. J Matern Fetal Neonatal Med 18, 1-7.
33. Matthews J, Altman D, Campbell M & Royston P (1990). Analysis of serial measurements in medical research. BMJ 300, 230-235
34. Morrison S, Gardner DS, Fletcher AJ, Bloomfield MR & Giussani DA (2003). Enhanced nitric oxide activity offsets peripheral vasoconstriction during acute hypoxaemia via chemoreflex and adrenomedullary actions in the sheep fetus. J Physiol 547, 283-291.
35. Peebles D (2012). Radical change for the fetus. J Physiol 590, 1773.
36. Primhak R, Jedeikin R, Ellis G, Makela S, Gillan J, Swyer P & Rowe R (1985). Myocardial ischaemia in asphyxia neonatorum. Electrocardiographic, enzymatic and histological correlations. Acta Paediatr Scand 74, 595-600.
37. Rudolph A (1985). Distribution and regulation of blood flow in the fetal and neonatal lamb. Circ Res 57, 811-821.
38. Salles M, Tabatabai M & Shahidi H (1972). Blood glucose levels in dogs pretreated with allopurinol during hemorrhagic shock. Am J Physiol 223, 679-681.
39. Thakor A & Giussani D (2009). Nitric oxide reduces vagal baroreflex sensitivity in the late gestation fetus. Pediatr Res 65, 269-273.
40. Thakor AS, Herrera EA, Serón-Ferré M & Giussani DA (2010a). Melatonin and vitamin C increase umbilical blood flow via nitric oxide-dependent mechanisms. J Pineal Res 49, 399-406.
41. Thakor AS, Richter HG, Kane AD, Dunster C, Kelly FJ, Poston L & Giussani DA (2010b). Redox modulation of the fetal cardiovascular defence to hypoxaemia. J Physiol 588, 4235-4247.
42. van Bel F, Shadid M, Moison R, Dorrepaal C, Fontijn J, Monteiro L, vande Bor & Berger H (1998). Effect of allopurinol on postasphyxial free radical formation, cerebral hemodynamics, and electrical brain activity. Pediatrics 101, 185-193.
43. van Dijk A, ParviziI N, Taverne M & Fink-Gremmels J (2008). Placental transfer and pharmacokinetics of allopurinol in late pregnant sows and their fetuses. J Vet Pharmacol Ther 31, 489-495.