Na+, K+-ATPase activity and subunit isoform protein abundance: Effects of antenatal glucocorticoids in the frontal cerebral cortex and renal cortex of ovine fetuses

Reproductive Sciences

Volumn 16, Issue 3, 2009, Pages 294-307

  Mehter, Najma S ^a,b   Sadowska, Grazyna B ^a   Malaeb, Shadi N ^a   Stonestreet, Barbara S ^a  

^a BROWN UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Brain; Development; Dexamethasone; Kidney; Sheep; Steroids

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); DEXAMETHASONE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CONTROLLED STUDY; FETUS; KIDNEY CORTEX; NONHUMAN; PRENATAL PERIOD; PRIORITY JOURNAL; SHEEP; WESTERN BLOTTING;

ANIMALS; CELL COUNT; CEREBRAL CORTEX; DEXAMETHASONE; DRUG ADMINISTRATION SCHEDULE; FEMALE; GLUCOCORTICOIDS; INJECTIONS, INTRAMUSCULAR; KIDNEY CORTEX; MATERNAL-FETAL EXCHANGE; NEURONS; PREGNANCY; PROTEIN SUBUNITS; SHEEP; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 60049084222     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719108325507     Document Type: Article

References (70)

1. Skou JC The Na,K-pump. Methods Enzymol. 1988 ; 156: 1-25.
2. Therien AG, Blostein R. Mechanisms of sodium pump regulation. Am J Physiol Cell Physiol. 2000 ; 279: C541 - C566.
3. Malik N., Canfield VA, Beckers MC, Gros P., Levenson R. Identification of the mammalian Na,K-ATPase 3 subunit. J Biol Chem. 1996 ; 271: 22754-22758.
4. Mobasheri A., Avila J., Cozar-Castellano I., et al. Na+, K+-ATPase isozyme diversity; comparative biochemistry and physiological implications of novel functional interactions. Biosci Rep. 2000 ; 20: 51-91.
5. Chow DC, Forte JG Functional significance of the beta-subunit for heterodimeric P-type ATPases. J Exp Biol. 1995 ; 198 (pt 1). 1-17.
6. Horisberger JD, Lemas V., Kraehenbuhl JP, Rossier BC Structure-function relationship of Na,K-ATPase. Annu Rev Physiol. 1991 ; 53: 565-584.
7. Hieber V., Siegel GJ, Fink DJ, Beaty MW, Mata M. Differential distribution of (Na, K)-ATPase alpha isoforms in the central nervous system. Cell Mol Neurobiol. 1991 ; 11: 253-262.
8. Shull GE, Greeb J., Lingrel JB Molecular cloning of three distinct forms of the Na+,K+-ATPase alpha-subunit from rat brain. Biochemistry. 1986 ; 25: 8125-8132.
9. Herrera VL, Cova T., Sassoon D., Ruiz-Opazo. Developmental cell-specific regulation of Na(+)-K(+)-ATPase alpha 1-, alpha 2-, and alpha 3-isoform gene expression. Am J Physiol. 1994 ; 266 (5 pt 1). C1301 - C1312.
10. Lucking K., Nielsen JM, Pedersen PA, Jorgensen PL Na-K-ATPase isoform (alpha 3, alpha 2, alpha 1) abundance in rat kidney estimated by competitive RT-PCR and ouabain binding. Am J Physiol. 1996 ; 271 (2) Pt 2: F253-60.
11. Orlowski J., Lingrel JB Tissue-specific and developmental regulation of rat Na,K-ATPase catalytic alpha isoform and beta subunit mRNAs. J Biol Chem. 1988 ; 263: 10436-10442.
12. Jaisser F., Jaunin P., Geering K., Rossier BC, Horisberger JD Modulation of the Na,K-pump function by beta subunit isoforms. J Gen Physiol. 1994 ; 103: 605-623.
13. Aperia A., Larsson L., Zetterstrom R. Hormonal induction of Na-K-ATPase in developing proximal tubular cells. Am J Physiol. 1981 ; 241: F356 - F360.
14. Celsi G., Wang ZM, Akusjarvi G., Aperia A. Sensitive periods for glucocorticoids' regulation of Na+,K(+)-ATPase mRNA in the developing lung and kidney. Pediatr Res. 1993 ; 33: 5-9.
15. Petershack JA, Nagaraja SC, Guillery EN Role of glucocorticoids in the maturation of renal cortical Na+-K+-ATPase during fetal life in sheep. Am J Physiol. 1999 ; 276 (6 pt 2). R1825 - R1832.
16. Devarajan P., Benz EJ, Jr. Translational regulation of Na-K-ATPase subunit mRNAs by glucocorticoids. Am J Physiol Renal Physiol. 2000 ; 279: F1132 - F1138.
17. Crowley PA Antenatal corticosteroid therapy: a meta-analysis of the randomized trials, 1972 to 1994. Am J Obstet Gynecol. 1995 ; 173: 322-335.
18. Doyle LW, Kitchen WH, Ford GW, Rickards AL, Lissenden JV, Ryan MM Effects of antenatal steroid therapy on mortality and morbidity in very low birth weight infants. J Pediatr. 1986 ; 108: 287-292.
19. Liggins GC, Howie RN A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants. Pediatrics. 1972 ; 50: 515-525.
20. National Institutes of Health Consensus Development Panel. NIH consensus development panel on the effect of corticosteroids for fetal maturation on perinatal outcomes. JAMA. 1995 ; 273: 413-418.
21. Crowther CA, Harding JE Repeat doses of prenatal corticosteroids for women at risk of preterm birth for preventing neonatal respiratory disease. Cochrane Database Syst Rev. CD003935.
22. Stiles AD Prenatal corticosteroids-early gain, long-term questions. N Engl J Med. 2007 ; 357: 1248-1250.
23. National Institutes of Health Consensus Development Panel. Antenatal Corticosteroids Revisited: Repeat Courses. 2000 ; 17: 1-18.
24. Crowther CA, Haslam RR, Hiller JE, Doyle LW, Robinson JS, and the Australasian Collaborative Trial of Repeat Doses of Steroids (ACTORDS) Study Group. Neonatal respiratory distress syndrome after repeat exposure to antenatal corticosteroids: a randomised controlled trial. Lancet. 2006 ; 367: 1913-1919.
25. Wapner RJ, Sorokin Y., Thom EA, et al. Single versus weekly courses of antenatal corticosteroids: evaluation of safety and efficacy. Am J Obstet Gynecol. 2006 ; 195: 633-642.
26. Wapner RJ, Sorokin Y., Mele L., et al. Long-term outcomes after repeat doses of antenatal corticosteroids. N Engl J Med. 2007 ; 357: 1190-1198.
27. Berry LM, Polk DH, Ikegami M., Jobe AH, Padbury JF, Ervin MG Preterm newborn lamb renal and cardiovascular responses after fetal or maternal antenatal betamethasone. Am J Physiol. 1997 ; 272 (6 pt 2). R1972 - R1979.
28. Okah FA, Pickens WL, Hoath SB Effect of prenatal steroids on skin surface hydrophobicity in the premature rat. Pediatr Res. 1995 ; 37 (4 pt 1). 402-408.
29. Stonestreet BS, Hansen NB, Laptook AR, Oh W. Glucocorticoid accelerates renal functional maturation in fetal lambs. Early Hum Dev. 1983 ; 8: 331-341.
30. Stonestreet BS, Petersson KH, Sadowska GB, Pettigrew KD, Patlak CS Antenatal steroids decrease blood-brain barrier permeability in the ovine fetus. Am J Physiol. 1999 ; 276 (2 pt 2). R283 - R289.
31. Adams DF, Ment LR, Vohr B. Antenatal therapies and the developing brain. Semin Neonatol. 2001 ; 6: 173-183.
32. Schwab M., Antonow-Schlorke I., Kuhn B., et al. Effect of antenatal betamethasone treatment on microtubuleassociated proteins MAP1B and MAP2 in fetal sheep. J Physiol. 2001 ; 530 (pt 3). 497-506.
33. Schwab M., Roedel M., Anwar MA, et al. Effects of betamethasone administration to the fetal sheep in late gestation on fetal cerebral blood flow. J Physiol. 2000 ; 528 (pt 3). 619-632.
34. Schwab M., Schmidt K., Roedel M., et al. Non-linear changes of electrocortical activity after antenatal betamethasone treatment in fetal sheep. J Physiol. 2001 ; 531 (pt 2). 535-543.
35. Stonestreet BS, Elitt CM, Markowitz J., Petersson KH, Sadowska GB Effects of antenatal corticosteroids on regional brain and non-neural tissue water content in the ovine fetus. J Soc Gynecol Investig. 2003 ; 10: 59-66.
36. Stonestreet BS, Sadowska GB, McKnight AJ, Patlak C., Petersson KH Exogenous and endogenous corticosteroids modulate blood-brain barrier development in the ovine fetus. Am J Physiol Regul Integr Comp Physiol. 2000 ; 279: R468 - R477.
37. Dunlop SA, Archer MA, Quinlivan JA, Beazley LD, Newnham JP Repeated prenatal corticosteroids delay myelination in the ovine central nervous system. J Matern Fetal Med. 1997 ; 6: 309-313.
38. Huang WL, Harper CG, Evans SF, Newnham JP, Dunlop SA Repeated prenatal corticosteroid administration delays myelination of the corpus callosum in fetal sheep. Int J Dev Neurosci. 2001 ; 19: 415-425.
39. Dodic M., Wintour EM Effects of prolonged (48 h) infusion of cortisol on blood pressure, renal function and fetal fluids in the immature ovine foetus. Clin Exp Pharmacol Physiol. 1994 ; 21: 971-980.
40. Wintour EM, Alcorn D., McFarlane A., Moritz K., Potocnik SJ, Tanqalakis K. Effect of maternal glucocorticoid treatment on fetal fluids in sheep at 0.4 gestation. Am J Physiol. 1994 ; 266 (4 pt 2). R1174 - R1181.
41. Dickinson H., Walker DW, Wintour EM, Moritz K. Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse. Am J Physiol Regul Integr Comp Physiol. 2007 ; 292: R453 - R461. Epub 2006 Aug 31.
42. al-Dahan J., Stimmler L., Chantler C., Haycock GB The effect of antenatal dexamethasone administration on glomerular filtration rate and renal sodium excretion in premature infants. Pediatr Nephrol. 1987 ; 1: 131-135.
43. Omar SA, DeCristofaro JD, Agarwal BI, La Gamma EF Effects of prenatal steroids on water and sodium homeostasis in extremely low birth weight neonates. Pediatrics. 1999 ; 104 (3 pt 1). 482-488.
44. Sadowska GB, Patlak CS, Petersson KH, Stonestreet BS Effects of multiple courses of antenatal corticosteroids on blood-brain barrier permeability in the ovine fetus. J Soc Gynecol Investig. 2006 ; 13 (4). 248-255.
45. Stonestreet BS, Watkins S., Petersson KH, Sadowska GB Effects of multiple courses of antenatal corticosteroids on regional brain and somatic tissue water content in ovine fetuses. J Soc Gynecol Investig. 2004 ; 11: 166-174.
46. Jorgensen PL Purification and characterization of (Na+ plus K+)-ATPase. 3. Purification from the outer medulla of mammalian kidney after selective removal of membrane components by sodium dodecylsulphate. Biochim Biophys Acta. 1974 ; 356: 36-52.
47. Lo SC, August TR, Liberman UA, Edelman IS Dependence of renal (Na+ + k+)-adenosine triphosphatase activity on thyroid status. J Biol Chem. 1976 ; 251: 7826-7833.
48. Schmitt CA, McDonough AA Developmental and thyroid hormone regulation of two molecular forms of Na+-K+-ATPase in brain. J Biol Chem. 1986 ; 261: 10439-10444.
49. Fiske CR, Subbarow Y. The colorimetric determination of phosphorus. J Biol Chem. 1925 ; 66: 375-400.
50. Kim CR, Sadowska GB, Petersson KH, Merino M., Sysyn GD, Padbury JF, Stonestreet BS Effects of postnatal steroids on Na+/K+-ATPase activity and alpha1- and beta1-subunit protein expression in the cerebral cortex and renal cortex of newborn lambs. Reprod Fertil Dev. 2006 ; 18: 413-423.
51. Martin-Vasallo P., Wetzel RK, Garcia-Segura LM, Molina-Holgado E., Aryarkhova E., Sweadner KJ Oligodendrocytes in brain and optic nerve express the beta3 subunit isoform of Na,K-ATPase. Glia. 2000 ; 31: 206-218.
52. Arystarkhova E., Sweadner KJ Tissue-specific expression of the Na,K-ATPase beta3 subunit. The presence of beta3 in lung and liver addresses the problem of the missing subunit. J Biol Chem. 1997 ; 272: 22405-22408.
53. Malaeb SN, Sadowska GB, Stonestreet BS Effects of maternal treatment with corticosteroids on tight junction protein expression in the cerebral cortex of the ovine fetus with and without exposure to in utero brain ischemia. Brain Res. 2007 ; 1160: 11-19.
54. Ron NP, Kazianis JA, Padbury JF, Brown CM, McGonnigal BG, Sysyn GD, Sadowska GB, Stonestreet BS Ontogeny and the effects of corticosteroid pretreatment on aquaporin water channels in the ovine cerebral cortex. Reprod Fertil Dev. 2005 ; 17: 535-542.
55. Uno H., Lohmiller L., Thieme C., Kemnitz JW, Engle MJ, Roecker EB, Farrell PM Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus. Brain Res Dev Brain Res. 1990 ; 53: 157-167.
56. Mullen RJ, Buck CR, Smith AM NeuN, a neuronal specific nuclear protein in vertebrates. Development. 1992 ; 116: 201-211.
57. Sliwowska JH, Billings HJ, Goodman RL, Coolen LM, Lehman MN The premammillary hypothalamic area of the ewe: anatomical characterization of a melatonin target area mediating seasonal reproduction. Biol Reprod. 2004 ; 70: 1768-1775.
58. Feraille E., Doucet A. Sodium-potassiumadenosinetriphosphatase-dependent sodium transport in the kidney: hormonal control. Physiol Rev. 2001 ; 81: 345-418.
59. Patrick J., Hilton PJ Characterization of sodium-transport disorders in disease: different effects upon sodium and potassium of changes in the sodium pump and in membrane permeability. Clin Sci (Lond). 1979 ; 57: 289-293.
60. Rose AM, Valdes R. Jr. Understanding the sodium pump and its relevance to disease. Clin Chem. 1994 ; 40: 1674-1685.
61. Jamme I., Petit E., Gerbi A., Maxient JM, MacKenzie ET, Nouvelot A. Changes in ouabain affinity of Na+, K+-ATPase during focal cerebral ischaemia in the mouse. Brain Res. 1997 ; 774: 123-130.
62. Chauhan NB, Lee JM, Siegel GJ Na,K-ATPase mRNA levels and plaque load in Alzheimer's disease. J Mol Neurosci. 1997 ; 9: 151-66.
63. Hieber V., Siegel GJ, Fink DJ, Beaty MW, Mata M. Differential distribution of (Na, K)-ATPase alpha isoforms in the central nervous system. Cell Mol Neurobiol. 1991 ; 11: 253-262.
64. Shyjan AW, Levenson R. Antisera specific for the alpha 1, alpha 2, alpha 3, and beta subunits of the Na,K-ATPase: differential expression of alpha and beta subunits in rat tissue membranes. Biochemistry. 1989 ; 28: 4531-4535.
65. Watts AG, Sanchez-Watts G., Emanuel JR, Levenson R. Cell-specific expression of mRNAs encoding Na+,K(+)-ATPase alpha- and beta-subunit isoforms within the rat central nervous system. Proc Natl Acad Sci U S A. 1991 ; 88: 7425-7429.
66. Jobe AH, Polk DH, Ervin MG, Padbury JF, Rebello CM, Ikegami M. Preterm betamethasone treatment of fetal sheep: outcome after term delivery. J Soc Gynecol Investig. 1996 ; 3: 250-258.
67. Smith LM, Altamirano AK, Ervin MG, Seidner SR, Jobe AH Prenatal glucocorticoid exposure and postnatal adaptation in premature newborn baboons ventilated for six days. Am J Obstet Gynecol. 2004 ; 191: 1688-1694.
68. Horvath K., Blochin B., Hill I., Verma R., Lu RB, Lebenthal E. The pre- and postnatal development of Na+/K(+)-ATPase in gastrointestinal organs of the rat: effect of betamethasone treatment. J Pediatr Gastroenterol Nutr. 1993 ; 16: 412-418.
69. Lyoussi B., Crabbe J. Effects of dexamethasone on (Na+ + K+)-ATPase and other parameters related to transepithelial Na+ transport by amphibian renal distal cells (A6) in culture. J Steroid Biochem Mol Biol. 1996 ; 59: 333-338.
70. Smith LM, Ervin MG, Wada N., Ikagami M., Polk DH, Jobe AH Antenatal glucocorticoids alter postnatal preterm lamb renal and cardiovascular responses to intravascular volume expansion. Pediatr Res. 2000 ; 47: 622-627.