Fetal loss and hyposulfataemia in pregnant NaS1 transporter null mice

Journal of Reproduction and Development

Volumn 57, Issue 4, 2011, Pages 444-449

  Dawson, Paul Anthony ^a   Sim, Pearl ^a   Simmons, David Gordon ^a   Markovich, Daniel ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Placenta; Pregnancy; Sulfate

Indexed keywords

CATION TRANSPORT PROTEIN; COTRANSPORTER; SODIUM SULFATE COTRANSPORTER; SULFATE;

AMNION FLUID; ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BREEDING; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; MALE; METABOLISM; METHODOLOGY; MOUSE; PLACENTA; PREGNANCY; REAL TIME POLYMERASE CHAIN REACTION; STATISTICAL MODEL; TIME; TRANSGENIC MOUSE;

AMNIOTIC FLUID; ANIMALS; BEHAVIOR, ANIMAL; CATION TRANSPORT PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MALE; MICE; MICE, TRANSGENIC; MODELS, STATISTICAL; PLACENTA; PREGNANCY; PREGNANCY, ANIMAL; REAL-TIME POLYMERASE CHAIN REACTION; SULFATES; SYMPORTERS; TIME FACTORS;

MUS;

EID: 80052587122     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.10-173K     Document Type: Article

References (46)

1. Falany CN. Enzymology of human cytosolic sulfotransferases. FASEB J 1997; 11: 206-216.
2. Klassen CD, Boles J. The importance of 3'-phosphoadenosine 5'-phosphosulfate (PAPS) in the regulation of sulfation. FASEB J 1997; 11: 404-418.
3. Strott CA. Sulfonation and molecular action. Endocr Rev 2002; 23: 703-732.
4. Strott CA. Steroid sulfotransferases. Endocr Rev 1996; 17: 670-697.
5. Wood CE. Estrogen/hypothalamus-pituitary-adrenal axis interactions in the fetus: The interplay between placenta and fetal brain. J Soc Gynecol Investig 2005; 12: 67-76.
6. Mulder GJ, Jakoby WB. Sulfation. In: Mulder GJ (ed.), Conjugation Reactions in Drug Metabolism: An Integrated Approach: Substrates, Co-substrates, Enzymes and Their Interactions In Vivo and In Vitro. Taylor and Francis, London; 1990: 107-161.
7. Lee A, Beck L, Markovich D. The human renal sodium sulfate cotransporter (SLC13A1; hNaSi-1) cDNA and gene: organisation, chromosomal localization, and functional characterization. Genomics 2000; 70: 354-363.
8. Cole DE, Baldwin LS, Stirk LJ. Increased inorganic sulfate in mother and fetus at parturition: evidence for a fetal-to-maternal gradient. Am J Obstet Gynecol 1984; 148: 596-599.
9. Cole DE, Baldwin LS, Stirk LJ. Increased renal reabsorption of inorganic sulfate in third-trimester high-risk pregnancies. Obstet Gynecol 1985; 66: 485-490.
10. Morris ME, Levy G. Plasma inorganic sulfate concentrations in pregnant women. J Pharm Sci 1983; 72: 715-716.
11. Tallgren LG. Inorganic sulphate in relation to the serum thyroxine level and in renal failure. Acta Med Scand 1980; Suppl 640: 1-100.
12. Lee HJ, Balasubramanian SV, Morris ME. Effect of pregnancy, postnatal growth, and gender on renal sulfate transport. Proc Soc Exp Biol Med 1999; 221: 336-344.
13. Gaull G, Sturman JA, Raiha NC. Development of mammalian sulfur metabolism: absence of cystathionase in human fetal tissues. Pediatr Res 1972; 6: 538-547.
14. Loriette C, Chatagner F. Cysteine oxidase and cysteine sulfinic acid decarboxylase in developing rat liver. Experientia 1978; 34: 981-982.
15. Dawson PA, Beck L, Markovich D. Hyposulfatemia, growth retardation, reduced fertility and seizures in mice lacking a functional NaSi-1 gene. Proc Natl Acad Sci USA 2003; 100: 13704-13709.
16. de Agostini A. An unexpected role for anticoagulant heparan sulfate proteoglycans in reproduction. Swiss Med Wkly 2006; 136: 583-590.
17. Tong MH, Jiang H, Liu P, Lawson JA, Brass LF, Song WC. Spontaneous fetal loss caused by placental thrombosis in estrogen sulfotransferase-deficient mice. Nat Med 2005; 11: 153-159.
18. Stuart RO, Bush KT, Nigam SK. Changes in global gene expression patterns during development and maturation of the rat kidney. Proc Natl Acad Sci USA 2001; 98: 5649-5654.
19. Lee S, Dawson PA, Hewavitharana AK, Shaw PN, Markovich D. Disruption of NaS1 sulfate transport function in mice leads to enhanced acetaminophen-induced hepatotoxicity. Hepatology 2006; 43: 1241-1247.
20. Simmons DG, Rawn S, Davies A, Hughes M, Cross JC. Spatial and temporal expression of the 23 murine Prolactin/Placental Lactogen-related genes is not associated with their position in the locus. BMC Genomics 2008; 9: 352.
21. Dawson PA, Steane SE, Markovich D. Behavioural abnormalities of the hyposulfataemic Nas1 knock-out mouse. Behav Brain Res 2004; 154: 457-463.
22. Superti-Furga A, Hastbacka J, Wilcox WR, Cohn DH, van der Harten HJ, Rossi A, Blau N, Rimoin DL, Steinmann B, Lander ES, Gitzelmann R. Achondrogenesis type IB is caused by mutations in the diastrophic dysplasia sulphate transporter gene. Nat Genet 1996; 12: 100-102.
23. Dawson PA, Gardiner B, Grimmond S, Markovich D. Transcriptional profile reveals altered hepatic lipid and cholesterol metabolism in hyposulfatemic NaS1 null mice. Physiol Genomics 2006; 26: 116-124.
24. Dawson PA, Pirlo KJ, Steane SE, Kunzelmann K, Chien YJ, Markovich D. Molecular cloning and characterization of the mouse Na+ sulfate cotransporter gene (Slc13a4): Structure and expression. Genes Genet Syst 2006; 81: 265-272.
25. Haila S, Hastbacka J, Bohling T, Karjalainen-Lindsberg ML, Kere J, Saarialho-Kere U. SLC26A2 (diastrophic dysplasia sulfate transporter) is expressed in developing and mature cartilage but also in other tissues and cell types. J Histochem Cytochem 2001; 49: 973-982.
26. Cross JC, Simmons DG, Watson ED. Chorioallantoic morphogenesis and formation of the placental villous tree. Ann NY Acad Sci 2003; 995: 84-93.
27. Renfree MB, Hensleigh HC, McLaren A. Developmental changes in the composition and amount of mouse fetal fluids. J Embryol Exp Morphol 1975; 33: 435-446.
28. Cowley DE, Pomp D, Atchley WR, Eisen EJ, Hawkins-Brown D. The impact of maternal uterine genotype on postnatal growth and adult body size in mice. Genetics 1989; 122: 193-203.
29. Romero A, Villamayor F, Grau MT, Sacristán A, Ortiz JA. Relationship between fetal weight and litter size in rats: application to reproductive toxicology studies. Reprod Toxicol 1992; 6: 453-456.
30. 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: 411-418.
31. Roberts CT, Owens JA, Sferruzzi-Perri AN. Distinct actions of insulin-like growth factors (IGFs) on placental development and fetal growth: lessons from mice and guinea pigs. Placenta 2008; 29: S42-S47.
32. Dackor J, Li M, Threadgill DW. Placental overgrowth and fertility defects in mice with a hypermorphic allele of epidermal growth factor receptor. Mamm Genome 2009; 20: 339-349.
33. Hirning-Folz U, Winking H, Hameister H. Aberrant Myc expression in the murine trisomy 15 syndrome is correlated with prolonged proliferation in spongiotrophoblast cells of the placenta. Cytogenet Cell Genet 1992; 61: 289-294.
34. Rantakari P, Strauss L, Kiviranta R, Lagerbohm H, Paviala J, Holopainen I, Vainio S, Pakarinen P, Poutanen M. Placenta defects and embryonic lethality resulting from disruption of mouse hydroxysteroid (17-beta) dehydrogenase 2 gene. Mol Endocrinol 2008; 22: 665-675.
35. Soares MJ. The prolactin and growth hormone families: pregnancy-specific hormones/cytokines at the maternal-fetal interface. Reprod Biol Endocrinol 2004; 2: 51.
36. Bowen JM, Chamley L, Mitchell MD, Keelan JA. Cytokines of the placenta and extra-placental membranes: biosynthesis, secretion and roles in establishment of pregnancy in women. Placenta 2002; 23: 239-256.
37. Mitchell MD, Trautman MS, Dudley DJ. Cytokine networking in the placenta. Placenta 1993; 14: 249-275.
38. Soares MJ, Müller H, Orwig KE, Peters TJ, Dai G. The uteroplacental prolactin family and pregnancy. Biol Reprod 1998; 58: 273-284.
39. Ouyang YB, Crawley JT, Aston CE, Moore KL. Reduced body weight and increased postimplantation fetal death in tyrosylprotein sulfotransferase-1-deficient mice. J Biol Chem 2002; 277: 23781-23787.
40. Langley-Evans SC, Gardner DS, Jackson AA. Association of disproportionate growth of fetal rats in late gestation with raised systolic blood pressure in later life. J. Reprod Fertil 1996; 106: 307-312.
41. Langley SC, Jackson AA. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci (Lond) 1994; 86: 217-222.
42. Misra DP, Salafia CM, Miller RK, Charles AK. Non-linear and gender-specific relationships among placental growth measures and the fetoplacental weight ratio. Placenta 2009; 30: 1052-1057.
43. Carola V, D'Olimpio F, Brnamonti E, Mangia F, Renzi P. Evaluation of the elevated plus-maze and open field tests for the assessment of anxiety-related behaviour in inbred mice. Behav Brain Res 2002; 134: 49-57.
44. Njung'e K, Handley SL. Evaluation of marble-burying behavior as a model of anxiety. Pharmacol Biochem Behav 1991; 38: 63-67.
45. Rodgers RJ, Johnson JT. Factor analysis of spatiotemporal and ethological measures in the murine elevated-plus maze test of anxiety. Pharmacol Biochem Behav 1995; 52: 297-303.
46. Markovich D. Physiological roles and regulation of mammalian sulfate transporters. Physiol Rev 2001; 81: 1499-1534.