Protective effect of N-acetylcysteine on liver damage during chronic intrauterine hypoxia in fetal guinea pig

Reproductive Sciences

Volumn 19, Issue 9, 2012, Pages 1001-1009

  Hashimoto, Kazumasa ^a   Pinkas, Gerard ^a   Evans, Lashauna ^a   Liu, Hongshan ^a   Al Hasan, Yazan ^a   Thompson, Loren P ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

fetal hypoxia; fetal liver; guinea pig; N acetylcysteine; oxidative stress

Indexed keywords

ACETYLCYSTEINE; MALONALDEHYDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL DEATH; CONTROLLED STUDY; DNA FRAGMENTATION; ERYTHROID CELL; FEMALE; FETUS; FETUS HYPOXIA; FETUS LIVER; GUINEA PIG; HISTOPATHOLOGY; LIPID PEROXIDATION; LIVER INJURY; NONHUMAN; ORGAN WEIGHT; OXIDATIVE STRESS; PRIORITY JOURNAL;

ACETYLCYSTEINE; ANIMALS; ANTIOXIDANTS; FEMALE; FETAL HYPOXIA; GUINEA PIGS; LIVER DISEASES; ORGAN SIZE; OXIDATIVE STRESS; PREGNANCY; PROTECTIVE AGENTS;

EID: 84865034009     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719112440052     Document Type: Article

References (64)

1. Neerhof MG, Thaete LG. The fetal response to chronic placental insufficiency. Semin Perinatol. 2008 ; 32 (3). 201-205
2. Burton GJ. Oxygen, the Janus gas; its effects on human placental development and function. J Anat. 2009 ; 215 (1). 27-35
3. Hutter D, Kingdom J, Jaeggi E. Causes and mechanisms of intrauterine hypoxia and its impact on the fetal cardiovascular system: a review. Int J Pediatr. 2010 ; 2010: 401323
4. Nathanielsz PW, Hanson MA. The fetal dilemma: spare the brain and spoil the liver. J Physiol. 2003 ; 548 (pt 2). 333
5. Kiserud T, Kessler J, Ebbing C, Rasmussen S. Ductus venosus shunting in growth-restricted fetuses and the effect of umbilical circulatory compromise. Ultrasound Obstet Gynecol. 2006 ; 28 (2). 143-149
6. Tchirikov M, Schroder HJ, Hecher K. Ductus venosus shunting in the fetal venous circulation: regulatory mechanisms, diagnostic methods and medical importance. Ultrasound Obstet Gynecol. 2006 ; 27 (4). 452-461
7. Kung JW, Currie IS, Forbes SJ, Ross JA. Liver development, regeneration, and carcinogenesis. J Biomed Biotechnol. 2010 ; 2010: 984-248
8. Si-Tayeb K, Lemaigre FP, Duncan SA. Organogenesis and development of the liver. Dev Cell. 2010 ; 18 (2). 175-189
9. Koury ST, Bondurant MC, Koury MJ, Semenza GL. Localization of cells producing erythropoietin in murine liver by in situ hybridization. Blood. 1991 ; 77 (11). 2497-2503
10. Maxwell PH, Ferguson DJ, Osmond MK, Pugh CW, Heryet A, Doe BG, et al. Expression of a homologously recombined erythopoietin-SV40 T antigen fusion gene in mouse liver: evidence for erythropoietin production by Ito cells. Blood. 1994 ; 84 (6). 1823-1830
11. Regnault TR, Teng C, de Vrijer B, Galan HL, Wilkening RB, Battaglia FC, et al. The tissue and plasma concentration of polyols and sugars in sheep intrauterine growth retardation. Exp Biol Med. 2010 ; 235 (8). 999-1006
12. Fernandez ML. Guinea pigs as models for cholesterol and lipoprotein metabolism. J Nutr. 2001 ; 131 (1). 10-20
13. Seferovic MD, Chen S, Pinto DM, Gupta MB. Altered liver secretion of vascular regulatory proteins in hypoxic pregnancies stimulate angiogenesis in vitro. J Proteome Res. 2011 ; 10 (4). 1495-1504
14. Watson CS, Bialek P, Anzo M, Khosravi J, Yee SP, Han VK, et al. Elevated circulating insulin-like growth factor binding protein-1 is sufficient to cause fetal growth restriction. Endocrinology. 2006 ; 147 (3). 1175-1186
15. Tazuke SI, Mazure NM, Sugawara J, Carland G, Faessen GH, Suen LF, et al. Hypoxia stimulates insulin-like growth factor binding protein 1 (IGFBP-1) gene expression in HepG2 cells: a possible model for IGFBP-1 expression in fetal hypoxia. Proc Natl Acad Sci USA. 1998 ; 95 (17). 10188-10193
16. Crossey PA, Pillai CC, Miell JP. Altered placental development and intrauterine growth restriction in IGF binding protein-1 transgenic mice. J Clin Invest. 2002 ; 110 (3). 411-418
17. Maulik D, Numagami Y, Ohnishi ST, Mishra OP, Delivoria-Papadopoulos M. Direct measurement of oxygen free radicals during in utero hypoxia in the fetal guinea pig brain. Brain Res. 1998 ; 798 (1-2). 166-172
18. Clanton TL. Hypoxia-induced reactive oxygen species formation in skeletal muscle. J Appl Physiol. 2007 ; 102 (6). 2379-2388
19. Maiti P, Singh SB, Sharma AK, Muthuraju S, Banerjee PK, Ilavazhagan G. Hypobaric hypoxia induces oxidative stress in rat brain. Neurochem Int. 2006 ; 49 (8). 709-716
20. Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest. 2005 ; 115 (3). 500-508
21. Abdel-Naim AB, Nagy AA, Mohamadin AM, El-Mazar HM, Ahmed AE. Chloroacetonitrile induces oxidative stress and apoptosis in mouse fetal liver. Toxicol Lett. 2009 ; 190 (2). 123-127
22. Behn C, Araneda OF, Llanos AJ, Celedon G, Gonzalez G. Hypoxia-related lipid peroxidation: evidences, implications and approaches. Respir Physiol Neurobiol. 2007 ; 158 (2-3). 143-150
23. Thorn SR, Regnault TR, Brown LD, Rozance PJ, Keng J, Roper M, et al. Intrauterine growth restriction increases fetal hepatic gluconeogenic capacity and reduces messenger ribonucleic acid translation initiation and nutrient sensing in fetal liver and skeletal muscle. Endocrinology. 2009 ; 150 (7). 3021-3030
24. Camm EJ, Martin-Gronert MS, Wright NL, Hansell JA, Ozanne SE, Giussani DA. Prenatal hypoxia independent of undernutrition promotes molecular markers of insulin resistance in adult offspring. FASEB J. 2011 ; 25 (1). 420-427
25. Thompson LP, Dong Y. Chronic hypoxia decreases endothelial nitric oxide synthase protein expression in fetal guinea pig hearts. J Soc Gynecol Investig. 2005 ; 12 (6). 388-395
26. Dong Y, Thompson LP. Differential expression of endothelial nitric oxide synthase in coronary and cardiac tissue in hypoxic fetal guinea pig hearts. J Soc Gynecol Investig. 2006 ; 13 (7). 483-490
27. Sparks JW, Girard JR, Callikan S, Battaglia FC. Growth of fetal guinea pig: physical and chemical characteristics. Am J Physiol. 1985 ; 248 (1 pt1). E132 - E139
28. Thompson LP, Aguan K, Zhou H. Chronic hypoxia inhibits contraction of fetal arteries by increased endothelium-derived nitric oxide and prostaglandin synthesis. Soc Gynecol Investig. 2004 ; 11 (8). 511-520
29. Thompson L, Dong Y, Evans L. Chronic hypoxia increases inducible NOS-derived nitric oxide in fetal guinea pig hearts. Ped Res. 2009 ; 65 (2). 188-192
30. Oh C, Dong Y, Harman C, Mighty HE, Kopelman J, Thompson LP. Chronic hypoxia differentially increases glutathione content and γ-glytamyl cysteine synthetase expression in fetal guinea pig organs. Early Hum Dev. 2008 ; 84 (2). 121-127
31. Beloosesky R, Gayle DA, Amidid F, Nunez SE, Babu J, Desai M, et al. N-acetylcysteine suppresses amniotic fluid and placenta inflammatory cytokine response to lipopolysaccharide in rats. Am J Obstet Gynecol. 2006 ; 194 (1). 268-273
32. Wang BJ, Guo YL, Chang HY, Sheu HM, Pan MH, Lee YH, et al. N-acetylcysteine inhibits chromium hypersensitivity in coadjuvant chromium-sensitized albino guinea pigs by suppressing the effects of reactive oxygen species. Exp Dermatol. 2010 ; 19 (8). e191 - e200
33. Evans LE, Liu H, Pinkas G, Thompson LP. Chronic hypoxia increases peroxynitrite, MMP9 expression, and collagen accumulation in guinea pig hearts. Ped Res. 2012 ; 71 (1). 25-31
34. Ross M, Pawlina W, Barnash T Atlas of Descriptive Histology. Ross M Pawlina W Barnash T, ed. Sunderland, MA: Sinauer Assoc. Inc ; 2009: 218-221.
35. Seferovic MD, Ali R, Kamei H, Liu S, Khosravi JM, Nazarian S, et al. Hypoxia and leucine deprivation induce human insulin-like growth factor binding protein-1 hyperphosphorylation and increase its biological activity. Endocrinology. 2009 ; 150 (1). 220-231
36. Tchirikov M, Kertschanska S, Sturenberg HJ, Schroder HJ. Liver blood perfusion as a possible instrument for fetal growth regulation. Placenta. 2002 ; 23 (suppl A). S153 - S158
37. Kessler J, Rasmussen S, Kiserud T. The fetal portal vein: normal blood flow development during the second half of human pregnancy. Ultrasound Obstet Gynecol. 2007 ; 30 (1). 52-60
38. Silver M, Barnes RJ, Fowden AL, Comline RS. Preferential oxygen supply to the brain and upper body in the fetal pig. Adv Exp Med Biol. 1988 ; 222: 683-687
39. Jensen A, Hohmann M, Kunzel W. Redistribution of fetal circulation during repeated asphyxia in sheep: effects on skin blood flow, transcutaneous PO2, and plasma catecholamines. J Dev Physiol. 1987 ; 9 (1). 41-55
40. Salihagic-Kadic A, Medic M, Jugovic D, Kos M, Latin V, Kusan Jukić M, et al. Fetal cerebrovascular response to chronic hypoxia - implications for the prevention of brain damage. J Matern Fetal Neonatal Med. 2006 ; 19 (7). 387-396
41. Tchirikov M, Buchert R, Wilke F, Brenner W. Glucose uptake in the placenta, fetal brain, heart and liver related to blood flow redistribution during acute hypoxia. J Obstet Gynaecol Res. 2011 ; 37 (8). 979-985
42. Carter AM. The blood supply to the abdominal organs of the fetal guinea-pig. J Dev Physiol. 1984 ; 6 (5). 407-416
43. Carter AM, Detmer A, Egund N. Contribution of the umbilical and portal veins to the hepatic blood supply of guinea pig fetuses - an angiographic study. Lab Anim Sci. 1992 ; 42 (2). 174-179
44. Carter AM, Detmer A. Blood flow to the placenta and lower body in the growth-retarded guinea pig fetus. J Dev Physiol. 1990 ; 13 (5). 261-269
45. McGrath KE, Palis J. Hematopoiesis in the yolk sac: more than meets the eye. Exp Hematol. 2005 ; 33 (9). 1021-1028
46. Porayette P, Paulson RF. BMP4/Smad5 dependent stress erythropoiesis is required for the expansion of erythroid progenitors during fetal development. Dev Biol. 2008 ; 317 (1). 24-35
47. Stockmann C, Fandrey J. Hypoxia-induced erythropoietin production: a paradigm for oxygen-regulated gene expression. Clin Exp Pharmacol Physiol. 2006 ; 33 (10). 968-979
48. Avery SV. Molecular targets of oxidative stress. Biochem J. 2011 ; 434 (2). 201-210
49. Hagar H, Ueda N, Shah SV. Role of reactive oxygen metabolites in DNA damage and cell death in chemical hypoxic injury to LLC-PK1 cells. Am J Physiol. 1996 ; 271 (1 pt 2). F209 - F215
50. Yoshioka T, Utsumi K, Sekiba K. Superoxide dismutase activity and lipid peroxidation of the rat liver during development. Biol Neonate. 1977 ; 32 (3-4). 47-53
51. Yoshioka T, Takehara Y, Shimatani M, Abe K, Utsumi K. Lipid peroxidation and antioxidants in rat liver during development. Tohoku J Exp Med. 1982 ; 137 (4). 391-400
52. Konstantinova SG, Russanov EM. Effect of pregnancy and fetal development on sheep liver superoxide dismutase activity. Res Vet Sci. 1988 ; 45 (3). 287-290
53. Rickett GM, Kelly FJ. Developmental expression of antioxidant enzymes in guinea pig lung and liver. Development. 1990 ; 108 (2). 331-336
54. Sato EF, Nakagawa E, Hiramoto K, Yamamasu S, Moriyama-Shimamoto I, Inoue M. Oxidative stress promotes the regression of fetal liver hemopoiesis. Biochemistry (Mosc). 2004 ; 69 (1). 18-22
55. Yamamasu S, Sato EF, Ogita S. Role of glutathione metabolism and apoptosis in the regression of liver hemopoiesis. Free Radic Biol Med. 1997 ; 23 (1). 100-109
56. Riggs BS, Bronstein AC, Kulig K, Archer PG, Rumack BH. Acute acetaminophen overdose during pregnancy. Obstet Gynecol. 1989 ; 74 (2). 247-253
57. Horowitz RS, Dart RC, Jarvie DR, Bearer CF, Gupta U. Placental transfer of N-acetylcysteine following human maternal acetaminophen toxicity. J Toxicol Clin Toxicol. 1997 ; 35 (5). 447-451
58. Buhimschi IA, Buhimschi CS, Weiner CP. Protective effect of N-acetylcysteine against fetal death and preterm labor induced by maternal inflammation. Am J Obstet Gynecol. 2003 ; 188 (1). 203-208
59. Basyigit I, Tugay M, Dilioglugil MO, Yildiz F, Maral H, Sozubir S. Protective effects of N-acetylcysteine on peroxidative changes of the fetal rat lungs whose mothers were exposed to cigarette smoke. Hum Exp Toxicol. 2007 ; 26 (2). 99-103
60. Parnell SE, Sulik KK, Dehart DB, Chen SY. Reduction of ethanol-induced ocular abnormalities in mice through dietary administration of N-acetylcysteine. Alcohol. 2010 ; 44 (7-8). 699-705
61. Ameri K, Hammond EM, Culmsee C, Raida M, Katschinski DM, Wenger RH, et al. Induction of activating transcription factor 3 by anoxia is independent of p53 and the hypoxic HIF signalling pathway. Oncogene. 2007 ; 26 (2). 284-289
62. Tacchini L, Dansi P, Matteucci E, Desiderio MA. Hepatocyte growth factor signalling stimulates hypoxia inducible factor-1 (HIF-1) activity in HepG2 hepatoma cells. Carcinogenesis. 2001 ; 22 (9). 1363-1371
63. Sanz-Alfayate G, Obeso A, Agapito MT, Gonzalez C. Reduced to oxidized glutathione ratios and oxygen sensing in calf and rabbit carotid body chemoreceptor cells. J Physiol. 2001 ; 537 (pt 1). 209-220
64. Martinez J, Canas PE, Minguell JJ. The effect of androgens on DNA synthesis by fetal hemopoietic stromal cells. Growth. 1983 ; 47 (2). 201-206