Chronic carbon monoxide inhalation during pregnancy augments uterine artery blood flow and uteroplacental vascular growth in mice

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 8, 2013, Pages

  Venditti, Carolina C ^a   Casselman, Richard ^a   Murphy, Malia S Q ^a   Adamson, S Lee ^c,d   Sled, John G ^b,c   Smith, Graeme N ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d MOUNT SINAI HOSPITAL   (Canada)

Author keywords

Carbon monoxide; Placenta; Preeclampsia; Pregnancy; sFLT1; Vascular endothelial growth factor

Indexed keywords

CARBON MONOXIDE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1;

ANGIOGENESIS; ANIMAL EXPERIMENT; ARTERY BLOOD FLOW; ARTICLE; BLOOD FLOW VELOCITY; BLOOD VESSEL DIAMETER; CONTROLLED STUDY; DOPPLER FLOWMETRY; ENVIRONMENTAL EXPOSURE; FEMALE; GROWTH; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; PLACENTA; PREGNANCY; PRIORITY JOURNAL; UMBILICAL ARTERY; UTERINE ARTERY; UTEROPLACENTAL VASCULAR GROWTH; UTERUS BLOOD FLOW; VASCULARIZATION;

CARBON MONOXIDE; PLACENTA; PREECLAMPSIA; PREGNANCY; SFLT1; VASCULAR ENDOTHELIAL GROWTH FACTOR;

ANIMALS; CARBON MONOXIDE; FEMALE; MICE; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; REGIONAL BLOOD FLOW; UTERINE ARTERY; UTERUS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84885656038     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00204.2013     Document Type: Article

References (62)

1. Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C, Cross JC. Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev Biol 250: 358-373, 2002.
2. Akamatsu Y, Haga M, Tyagi S, Yamashita K, Graça-Souza AV, Ollinger R, Czismadia E, May GA, Ifedigbo E, Otterbein LE. Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. FASEB J 18: 771-772, 2004.
3. Albuquerque CA, Smith KR, Johnson C, Chao R, Harding R. Influence of maternal tobacco smoking during pregnancy on uterine, umbilical and fetal cerebral artery blood flows. Early Hum Dev 80: 31-42, 2004.
4. Arbeille P, Fignon A, Bosc M, Bodart S. Changes in the utero-placental and fetal cerebral circulations induced by nicotine in the ovine fetus. J Gynecol Obstet Biol Reprod (Paris) 23: 51, 1994.
5. Bainbridge SA, Belkacemi L, Dickinson M, Graham CH, Smith GN. Carbon monoxide inhibits hypoxia/reoxygenation-induced apoptosis and secondary necrosis in syncytiotrophoblast. Am J Pathol 169: 774-783, 2006.
6. Bainbridge SA, Farley AE, McLaughlin BE, Graham CH, Marks GS, Nakatsu K, Brien JF, Smith GN. Carbon monoxide decreases perfusion pressure in isolated human placenta. Placenta 23: 563-569, 2002.
7. Bainbridge SA, Sidle EH, Smith GN. Direct placental effects of cigarette smoke protect women from pre-eclampsia: the specific roles of carbon monoxide and antioxidant systems in the placenta. Med Hypotheses 64: 17-27, 2005.
8. Baum M, Schiff E, Kreiser D, Dennery PA, Stevenson DK, Rosenthal T, Seidman DS. End-tidal carbon monoxide measurements in women with pregnancy-induced hypertension and preeclampsia. Am J Obstet Gynecol 183: 900-903, 2000.
9. Becker R, Vonk R, Vollert W, Entezami M. Doppler sonography of uterine arteries at 20-23 weeks: risk assessment of adverse pregnancy outcome by quantification of impedance and notch. J Perinat Med 30: 388-394, 2002.
10. Burke SD, Barrette VF, Bianco J, Thorne JG, Yamada AT, Pang SC, Adams MA, Croy BA. Spiral arterial remodeling is not essential for normal blood pressure regulation in pregnant mice. Hypertension 55: 729-737, 2010.
11. Campbell S, Griffin DR, Pearce JM, Diaz-Recasens J, Cohen-Over-beek TE, Willson K, Teague MJ. New Doppler technique for assessing uteroplacental blood flow. Lancet 321: 675-677, 1983.
12. Chen B, Guo L, Fan C, Bolisetty S, Joseph R, Wright MM, Agarwal A, George JF. Carbon monoxide rescues heme oxygenase-1-deficient mice from arterial thrombosis in allogeneic aortic transplantation. Am J Pathol 175: 422-429, 2009.
13. Clark JE, Naughton P, Shurey S, Green CJ, Johnson TR, Mann BE, Foresti R, Motterlini R. Cardioprotective actions by a water-soluble carbon monoxide-releasing molecule. Circ Res 93: e2-e8, 2003.
14. Cnattingius S, Mills JL, Yuen J, Eriksson O, Salonen H. The paradoxical effect of smoking in preeclamptic pregnancies: smoking reduces the incidence but increases the rates of perinatal mortality, abruptio placentae, and intrauterine growth restriction. Am J Obstet Gynecol 177: 156-161, 1997.
15. Coan PM, Ferguson-Smith AC, Burton GJ. Developmental dynamics of the definitive mouse placenta assessed by stereology. Biol Reprod 70: 1806-1813, 2004.
16. Conde-Agudelo A, Althabe F, Belizán JM, Kafury-Goeta AC. Cigarette smoking during pregnancy and risk of preeclampsia: a systematic review. Am J Obstet Gynecol 181: 1026-1035, 1999.
17. Cudmore M, Ahmad S, Al-Ani B, Fujisawa T, Coxall H, Chudasama K, Devey LR, Wigmore SJ, Abbas A, Hewett PW. Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation 115: 1789-1797, 2007.
18. Duley L. Maternal mortality associated with hypertensive disorders of pregnancy in Africa, Asia, Latin America and the Caribbean. Br J Obstet Gynecol 99: 547-553, 1992.
19. El-Mousleh T, Casalis PA, Wollenberg I, Zenclussen ML, Volk HD, Langwisch S, Jensen F, Zenclussen AC. Exploring the potential of low doses carbon monoxide as therapy in pregnancy complications. Med Gas Res 2: 4, 2012.
20. George EM, Cockrell K, Aranay M, Csongradi E, Stec DE, Granger JP. Induction of heme oxygenase 1 attenuates placental ischemia CO-induced hypertension. Hypertension 57: 941-948, 2011.
21. George EM, Colson D, Dixon J, Palei AC, Granger JP. Heme oxygen-ase-1 attenuates hypoxia-induced sFlt-1 and oxidative stress in placental villi through its metabolic products CO and bilirubin. Int J Hypertens 2012: 2012, 486053.
22. Hammoud AO, Bujold E, Sorokin Y, Schild C, Krapp M, Baumann P. Smoking in pregnancy revisited: findings from a large population-based study. Am J Obstet Gynecol 192: 1856-1862, 2005.
23. Harrington K, Carpenter RG, Goldfrad C, Campbell S. Transvaginal Doppler ultrasound of the uteroplacental circulation in the early prediction of preeclampsia and intrauterine growth retardation. Br J Obstet Gynecol 104: 674-681, 1997.
24. Hunter A, Aitkenhead M, Caldwell C, McCracken G, Wilson D, McClure N. Serum levels of vascular endothelial growth factor in pre-eclamptic and normotensive pregnancy. Hypertension 36: 965-969, 2000.
25. Kahn S, Almeida N, McNamara H, Koren G, Genest J, Dahhou M, Platt R, Kramer M. Smoking in preeclamptic women is associated with higher birthweight for gestational age and lower soluble fms-like tyrosine kinase-1 levels: a nested case control study. BMC Pregnancy Childbirth 11: 91, 2011.
26. Karumanchi SA, Bdolah Y. Hypoxia and sFlt-1 in preeclampsia: the chicken-and-egg question. Endocrinology 145: 4835-4837, 2004.
27. Karumanchi SA, Levine RJ. How does smoking reduce the risk of preeclampsia? Hypertension 55: 1100-1101, 2010.
28. Krauss T, Pauer HU, Augustin HG. Prospective analysis of placenta growth factor (PlGF) concentrations in the plasma of women with normal pregnancy and pregnancies complicated by preeclampsia. Hypertens Pregnancy 23: 101-111, 2004.
29. Kreiser D, Baum M, Seidman DS, Fanaroff A, Shah D, Hendler I, Stevenson DK, Schiff E, Druzin ML. End tidal carbon monoxide levels are lower in women with gestational hypertension and pre-eclampsia. J Perinatol 24: 213-217, 2004.
30. Lindqvist PG, Marsal K. Moderate smoking during pregnancy is associated with a reduced risk of preeclampsia. Acta Obstet Gynecol Scand 78: 693-697, 1999.
31. Longo LD. Carbon monoxide in the pregnant mother and fetus and its exchange across the placenta. Ann NY Acad Sci 174: 313-341, 1970.
32. Longo LD. The biological effects of carbon monoxide on the pregnant woman, fetus, and newborn infant. Am J Obstet Gynecol 129: 69, 1977.
33. Lu F, Longo M, Tamayo E, Maner W, Al-Hendy A, Anderson GD, Hankins GDV, Saade GR. The effect of over-expression of sFlt-1 on blood pressure and the occurrence of other manifestations of preeclampsia in unrestrained conscious pregnant mice. Am J Obstet Gynecol 196: 396-397, 2007.
34. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Liber-mann TA, Morgan JP, Sellke FW, Stillman IE. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111: 649-658, 2003.
35. Maynard SE, Venkatesha S, Thadhani R, Karumanchi SA. Soluble Fms-like tyrosine kinase 1 and endothelial dysfunction in the pathogenesis of preeclampsia. Pediatr Res 57: 1R-7R, 2005.
36. McLaughlin BE, Hutchinson JM, Graham CH, Smith GN, Marks GS, Nakatsu K, Brien JF. Heme oxygenase activity in term human placenta. Placenta 21: 870-873, 2000.
37. Miller EC, Cao H, Wen SW, Yang Q, Lafleche J, Walker M. The risk of adverse pregnancy outcomes is increased in preeclamptic women who smoke compared with nonpreeclamptic women who do not smoke. Am J Obstet Gynecol 203: 334-338, 2010.
38. Motterlini R, Otterbein LE. The therapeutic potential of carbon monoxide. Nat Rev Drug Disc 9: 728-743, 2010.
39. Mu J, Adamson SL. Developmental changes in hemodynamics of uterine artery, utero-and umbilicoplacental, and vitelline circulations in mouse throughout gestation. Am J Physiol Heart Circ Physiol 291: H1421-H1428, 2006.
40. Odrcich MJ, Graham CH, Kimura KA, McLaughlin BE, Marks GS, Nakatsu K, Brien JF. Heme oxygenase and nitric oxide synthase in the placenta of the guinea-pig during gestation. Placenta 19: 509-516, 1998.
41. Otterbein LE, Bach FH, Alam J, Soares M, Lu HT, Wysk M, Davis RJ, Flavell RA, Choi AM. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6: 422-428, 2000.
42. Pfarrer C, Macara L, Leiser R. Adaptive angiogenesis in placentas of heavy smokers. Lancet 354: 303, 1999.
43. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science's STKE 308: 1592, 2005.
44. Rennie MY, Detmar J, Whiteley KJ, Yang J, Jurisicova A, Adamson SL, Sled JG. Vessel tortuousity and reduced vascularization in the fetoplacental arterial tree after maternal exposure to polycyclic aromatic hydrocarbons. Am J Physiol Heart Circ Physiol 300: H675-H684, 2011.
45. Rennie MY, Whiteley KJ, Kulandavelu S, Adamson SL, Sled JG. 3D visualization and quantification by microcomputed tomography of late gestational changes in the arterial and venous feto-placental vasculature of the mouse. Placenta 28: 833-840, 2007.
46. Roberts JM, Cooper DW. Pathogenesis and genetics of pre-eclampsia. Lancet 357: 53-56, 2001.
47. Rossant J, Cross JC. Placental development: lessons from mouse mutants. Nat Rev Genet 2: 538-548, 2001.
48. Sarady JK, Zuckerbraun BS, Bilban M, Wagner O, Usheva A, Liu F, Ifedigbo E, Zamora R, Choi AM, Otterbein LE. Carbon monoxide protection against endotoxic shock involves reciprocal effects on iNOS in the lung and liver. FASEB J 18: 854-856, 2004.
49. Shibuya M. Structure and function of VEGF/VEGF-receptor system involved in angiogenesis. Cell Struct Funct 26: 25, 2001.
50. Sidle EH, Casselman R, Smith GN. Effect of cigarette smoke on placental antioxidant enzyme expression. Am J Physiol Regul Integr Comp Physiol 293: R754-R758, 2007.
51. Venditti CC, Casselman R, Smith GN. Effects of chronic carbon monoxide exposure on fetal growth and development in mice. BMC Pregnancy Childbirth 11: 101, 2011.
52. Venditti CC, Smith GN. Self-reported cigarette smoking status imprecisely quantifies exposure in pregnancy. Open J Obstet Gynecol 2: 56-61, 2012.
53. Volti GL, Sacerdoti D, Sangras B, Vanella A, Mezentsev A, Scapag-nini G, Falck JR, Abraham NG. Carbon monoxide signaling in promoting angiogenesis in human microvessel endothelial cells. Antioxid Redox Signal 7: 704-710, 2005.
54. Whiteley KJ, Pfarrer CD, Adamson SL. Vascular corrosion casting of the uteroplacental and fetoplacental vasculature in mice. Methods Mol Med 121: 371, 2005.
55. Wikstrom AK, Stephansson O, Cnattingius S. Tobacco use during pregnancy and preeclampsia risk. Hypertension 55: 1254-1259, 2010.
56. Woods AK, Hoffmann DS, Weydert CJ, Butler SD, Zhou Y, Sharma RV, Davisson RL. Adenoviral delivery of VEGF121 early in pregnancy prevents spontaneous development of preeclampsia in BPH/5 mice. Hypertension 57: 94-102, 2011.
57. Xiong X, Wang FL, Davidge ST, Demianczuk NN, Mayes DC, Olson DM, Saunders LD. Maternal smoking and preeclampsia. J Reprod Med 45: 727-732, 2000.
58. Yang Q, Wen SW, Smith GN, Chen Y, Krewski D, Chen XK, Walker MC. Maternal cigarette smoking and the risk of pregnancy-induced hypertension and eclampsia. Int J Epidemiol 35: 288-293, 2006.
59. Zenclussen ML, Casalis PA, El Mousleh T, Rebelo S, Langwisch S, Linzke N, Volk HD, Fest S, Soares MP, Zenclussen AC. Haem oxygenase-1 dictates intrauterine fetal survival in mice via carbon monoxide. J Pathol 225: 293-304, 2011.
60. Zhai D, Guo Y, Smith G, Krewski D, Walker M, Wen SW. Maternal exposure to moderate ambient level of carbon monoxide is associated with decreased risk of preeclampsia. Am J Obstet Gynecol 207: 57, e1-9, 2012.
61. Zhang J, Klebanoff MA, Levine RJ, Puri M, Moyer P. The puzzling association between smoking and hypertension during pregnancy. Am J Obstet Gynecol 181: 1407-1413, 1999.
62. Zuckerbraun BS, Chin BY, Bilban M, dvila JC, Rao J, Billiar TR, Otterbein LE. Carbon monoxide signals via inhibition of cytochrome coxidase and generation of mitochondrial reactive oxygen species. FASEB J 21: 1099-1106, 2007.