Marinobufagenin is an upstream modulator of Gadd45a stress signaling in preeclampsia

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1812, Issue 1, 2011, Pages 49-58

  Uddin, Mohammad N ^a   Horvat, Darijana ^a   DeMorrow, Sharon ^a   Agunanne, Enoch ^a   Puschett, Jules B ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

Apoptosis; Cellular regulation; Gadd45a; MBG; Preeclampsia; RBG

Indexed keywords

BUFOGENIN; CASPASE 3; DEOXYCORTICOSTERONE ACETATE; DRINKING WATER; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; MARINOBUFAGENIN; PROTEIN SFLT1; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOTROPHOBLAST; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; NONHUMAN; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RNA INTERFERENCE;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BUFANOLIDES; CASPASE 3; CASPASE 8; CELL CYCLE; CELL CYCLE PROTEINS; CELLS, CULTURED; FEMALE; HUMANS; MALE; NUCLEAR PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TROPHOBLASTS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASOCONSTRICTOR AGENTS;

LAKE VICTORIA MARBURGVIRUS; RATTUS;

EID: 78650293011     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2010.09.006     Document Type: Article

References (69)

1. Schoner W. Endogenous cardiac glycosides, a new class of steroid hormones. Eur. J. Biochem. 2002, 269:2440-24488.
2. +-pump in human mesenteric arteries. J. Hypertens. 1998, 16:1953-1958.
3. Fedorova O.V., Kolodkin N.I., Agalakova N.I., Lakatta E.G., Bagrov A.Y. Marinobufagenin, an endogenous alpha-1 sodium pump ligand, in hypertensive dahl salt-sensitive rats. Hypertension 2001, 37:2440-2448.
4. Pamnani M.B., Chen S., Yuan C.M., Haddy F.J. Chronic blood pressure effects of bufalin, a sodium-potassium ATPase inhibitor, in rats. Hypertension 1994, 23:I106-I109.
5. Lopatin D.A., Ailamazian E.K., Dmitrieva R.I., Shpen V.M., Fedorova O.V., Doris P.A., Bagrov A.Y. Circulating bufodienolide and cardenolide sodium pump inhibitors in preeclampsia. J. Hypertens. 1999, 17:1179-1187.
6. Gonick H.C., Ding Y., Vaziri N.D., Bagrov A.Y., Fedorova O.V. Simultaneous measurement of marinobufagenin, ouabain, and hypertension-associated protein in various disease states. Clin. Exp. Hypertens. 1998, 20(5-6):617-627.
7. Vu H.V., Ianosi-Irimie M.R., Pridjian C.A., Whitbred J.M., Durst J.M., Bagrov A.Y., Fedorova O.V., Pridjian G., Puschett J.B. Involvement of marinobufagenin in a rat model of human preeclampsia. Am. J. Nephrol. 2005, 25:520-528.
8. Durst J., Vu H.V., Ianosi-Irimie M.R., Pridjian C.A., Bagrov A., Fedorova O.V., Pridjian G., Puschett J.B. Antibodies to marinobufagenin reduce blood pressure in a rat model of preeclampsia. J. Invest. Med. 2004, 52:S318.
9. Pridjian G., Puschett J.B. Preeclampsia, part I: clinical and pathophysiological considerations. Obstet. Gynecol. Surv. 2002, 57(9):598-618.
10. Pridjian G., Puschett J.B. Preeclampsia, part II: experimental and genetic considerations. Obstet. Gynecol. Surv. 2002, 57(9):619-640.
11. Berg C.J., Atrash H.K., Koonin L.M., Tucker M. Pregnancy-related mortality in the United States, 1987-1990. Obstet. Gynecol. 1996, 88:161-167.
12. Roberts J.M., Redman C.W.G. Pre-eclampsia: more than pregnancy-induced hypertension. Lancet 1993, 341:1447-1451.
13. Ianosi-Irimie M., Vu H.V., Whitbred J.M., Pridjian C.A., Nadig J.D., Williams M.Y., Wrenn D.C., Pridjian G., Puschett J.B. A rat model of preeclampsia. Clin. Exp. Hypertens. 2005, 27:605-617.
14. Uddin M.N., Horvat D., Glaser S.S., Mitchell B.M., Puschett J.B. Examination of the cellular mechanisms by which marinobufagenin inhibits cytotrophoblast function. J. Biol. Chem. 2008, 283(26):17946-17953.
15. Uddin M.N., Horvat D., Glaser S.S., Danchuk S., Mitchell B.M., Sullivan D.E., Morris C.A., Puschett J.B. Marinobufagenin inhibits proliferation and migration of cytotrophoblast and CHO cells. Placenta 2008, 29:266-273.
16. LaMarca H.L., Morris C.A., Pettit G.R., Nagowa T., Puschett J.B. Marinobufagenin impairs first trimester cytotrophoblast differentiation. Placenta 2006, 27:984-988.
17. Uddin M.N., McLean L.B., Hunter F.A., Horvat D., Severson J., Tharakan B., Childs E.W., Puschett J.B. Vascular leak in a rat model of preeclampsia. Am. J. Nephrol. 2009, 30:26-33.
18. Hays P.M., Cruikshank D.P., Dunn L.J. Plasma volume determination in normal and preeclamptic pregnancies. Obstet. Gynecol. 1985, 151:958-966.
19. Gallery E.D.M., Hunyor S.N., Györy A.Z. Plasma volume contraction: a significant factor in both pregnancy-associated hypertension (pre-eclampsia) and chronic hypertension in pregnancy. Q. J. Med. 1979, 48:593-602.
20. Vu H., Ianosi-Irimie M., Danchuk S., Rabon E., Nogawa T., Kamano Y., Pettit G.R., Wiese T., Puschett J.B. Resibufogenin corrects hypertension in a rat model of human preeclampsia. Exp. Biol. Med. 2006, 231:215-220.
21. Danchuk S., Sukhanov S., Horvat D., Uddin M.N., Puschett J.B. Effects of resibufogenin in experimental hypertension. Am. J. Nephrol. 2008, 28:8-13.
22. Horvat D., Severson J., Uddin M.N., Mitchell B., Puschett J.B. Resibufogenin prevents the manifestations of preeclampsia in an animal model of the syndrome. Hypertens. Pregnancy 2009, 25:1-9.
23. Chelbi S.T., Mondon F., Jammes H., Buffat C., Mignot T.M., Tost J., Busato F., Gut I., Rebourcet R., Laissue P., Tsatsaris V., Goffinet F., Rigourd V., Carbonne B., Ferré F., Vaiman D. Expressional and epigenetic alterations of placental serine protease inhibitors: SERPINA3 is a potential marker of preeclampsia. Hypertension 2007, 49:76-83.
24. Savvidou M.D., Hingorani A.D., Tsikas D., Frölich J.C., Vallance P., Nicolaides K.H. Endothelial dysfunction and raised plasma concentrations of asymmetric dimethylarginine in pregnant women who subsequently develop pre-eclampsia. Lancet 2003, 361:1511-1517.
25. Maynard S.E., Min J.Y., Merchan J., Lim K.H., Li J., Mondal S., Libermann T.A., Morgan J.P., Sellke F.W., Stillman I.E., Epstein F.H., Sukhatme V.P., Karumanchi S.A. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J. Clin. Invest. 2003, 111:649-658.
26. Kirsten G.F., van Zyl N., Smith M., Odendaal H. Necrotizing enterocolitis in infants born to women with severe early preeclampsia and absent end-diastolic umbilical artery Doppler flow velocity waveforms. Am. J. Perinatol. 1999, 16:309-314.
27. Ito M., Itakura A., Ohno Y., Nomura M., Senga T., Nagasaka T., Mizutani S. Possible activation of the renin-angiotensin system in the feto-placental unit in preeclampsia. J. Clin. Endocrinol. Metab. 2002, 87:1871-1878.
28. Redman C.W., Sargent I.L. Latest advances in understanding preeclampsia. Science. 2005, 308:1592-1594.
29. A. Amanullah, N. Azam, A. Balliet, C. Hollander, B. Hoffman, A. Fornace, D. Liebermann. Cell signalling: cell survival and a Gadd45-factor deficiency. Nature. 14 (2003) 424(6950):741;discussion 742.
30. Abdollahi A., Lord K.A., Hoffman-Liebermann B., Liebermann D.A. Sequence and expression of a cDNA encoding MyD118: a novel myeloid differentiation primary response gene induced by multiple cytokines. Oncogene 1991, 6(1):165-167.
31. Liebermann D.A., Hoffman B. Gadd45 in stress signaling. J. Mol. Signal. 2008, 3:15.
32. Fornace A.J., Jackman J., Hollander M.C., Hoffman-Liebermann B., Liebermann D.A. Genotoxic-stress-response genes and growth-arrest genes. gadd, MyD, and other genes induced by treatments eliciting growth arrest. Ann. NY Acad. Sci. 1992, 663:139-153.
33. Liebermann D.A., Hoffman B. Myeloid differentiation (MyD)/growth arrest DNA damage (GADD) genes in tumor suppression, immunity and inflammation. Leukemia 2002, 16(4):527-541.
34. Gupta S.K., Gupta M., Hoffman B., Liebermann D.A. Hematopoietic cells from gadd45a-deficient and gadd45b-deficient mice exhibit impaired stress responses to acute stimulation with cytokines, myeloablation and inflammation. Oncogene 2006, 25(40):5537-5546.
35. Lu B., Ferrandino A.F., Flavell R.A. Gadd45beta is important for perpetuating cognate and inflammatory signals in T cells. Nat. Immunol. 2004, 5(1):38-44.
36. Salvador J.M., Mittelstadt P.R., Belova G.I., Fornace A.J., Ashwell J.D. The autoimmune suppressor Gadd45alpha inhibits the T cell alternative p38 activation pathway. Nat. Immunol. 2005, 6(4):396-402.
37. Takekawa M., Saito H. A family of stress-inducible GADD45-like proteins mediate activation of the stress-responsive MTK1/MEKK4 MAPKKK. Cell 1998, 95(4):521-530.
38. Zhang W., Bae I., Krishnaraju K., Azam N., Fan W., Smith K., Hoffman B., Liebermann D.A. CR6: a third member in the MyD118 and Gadd45 gene family which functions in negative growth control. Oncogene 1999, 18(35):4899-4907.
39. Gupta M., Gupta S.K., Balliet A.G., Hollander M.C., Fornace A.J., Hoffman B., Liebermann D.A. Hematopoietic cells from Gadd45a- and Gadd45b-deficient mice are sensitized to genotoxic-stress-induced apoptosis. Oncogene 2005, 24(48):7170-7179.
40. Tsuchimochi K., Otero M., Dragomir C.L., Plumb D.A., Zerbini L.F., Libermann T.A., Marcu K.B., Komiya S., Ijiri K., Goldring MB M.B. GADD45 beta enhances Col10a1 transcription via the MTK1/MKK3/6/p38 axis and activation of C/EBP {beta}-TAD4 in terminally differentiating chondrocytes. J. Biol. Chem. 2010, 285(11):8395-8407.
41. Xiong Y., Liebermann D.A., Tront J.S., Holtzman E.J., Huang Y., Hoffman B., Geifman-Holtzman O. Gadd45a stress signaling regulates sFlt-1 expression in preeclampsia. J. Cell. Physiol. 2009, 220(3):632-639.
42. Puschett J.B. The role of excessive volume expansion in the pathogenesis of preeclampsia. Med. Hypotheses 2006, 67(5):1125-1132.
43. Kalenga M.K., Thomas K., de Gasparo M., De Hertogh R. Determination of renin, angiotensin converting enzyme and angiotensin II levels in human placenta, chorion and amnion from women with pregnancy-induced hypertension. Clin. Endocrinol. 1964, 4:429-433.
44. Xie Z., Askari A. Na(+)/K(+)-ATPase as a signal transducer. Eur. J. Biochem. 2002, 269:2434-2439.
45. Choy M.Y., Manyonda I.T. The phagocytic activity of human first trimester extravillous trophoblast. Hum. Reprod. 1998, 13:2941-2949.
46. Choy M.Y., Whitley G.S., Manyonda I.T. Efficient, rapid and reliable establishment of human trophoblast cell lines using poly-l-ornithine. Early Pregnancy 2000, 4(2):124-143.
47. Cartwright J.E., Kenny L.C., Dash P.R., Crocker I.P., Aplin J.D., Baker P.N., Whitley G.S. Trophoblast invasion of spiral arteries: a novel in vitro model. Placenta 2002, 23:232-235.
48. Cartwright J.E., Holden D.P., Whitley G.S. Hepatocyte growth factor regulates human trophoblast motility and invasion: a role for nitric oxide. Br. J. Pharmacol. 1999, 128:181-189.
49. Chard T. An introduction to radioimmunoassay and related techniques, 4th ed. Laboratory Techniques in Biochemistry and Molecular Biology, Vol. 6, Part II 1990, Elsevier, Amsterdam. R.H. Burdon, P.H. van Knippenberg (Eds.).
50. Tijssen P. Practice and theory of enzyme immunoassays. Laboratory Techniques in Biochemistry and Molecular Biology 1985, vol. 15. Elsevier, Amsterdam.
51. Brown M.A., Gallery E.D., Ross M.R., Esber R.P. Am. J. Obstet. Gynecol. 1988, 159:297-307.
52. Whitley G.S., Cartwright J.E. Trophoblast-mediated spiral artery remodeling: a role for apoptosis. J. Anat. 2009, 215:21-26.
53. Roberts J.M., Taylor R.N., Musci T.J., Rodgers G.M., Hubel C.A., McLaughlin M.K. Preeclampsia: an endothelial cell disorder. Am. J. Obstet. Gynecol. 1989, 161(5):1200-1204.
54. Agunanne E., Horvat D., Uddin M.N., Puschett J.B. The treatment of preeclampsia in a rat model employing Digibind®. Am. J. Perinatol. 2010, 27(4):299-305.
55. Levy R. The role of apoptosis in preeclampsia. Isr. Med. Assoc. J. 2005, 7:178-181.
56. Leung D.N., Smith S.C., To K.F., Sahota D.S., Baker P.N. Increased placental apoptosis in pregnancies complicated by preeclampsia. Am. J. Obstet. Gynecol. 2001, 184:1249-1250.
57. Smith S.C., Baker P.N., Symonds E.M. Increased placental apoptosis in intrauterine growth restriction. Am. J. Obstet. Gynecol. 1997, 177:1395-1401.
58. DiFederico E., Genbacev O., Fisher S.J. Preeclampsia is associated with widespread apoptosis of placental cytotrophoblasts within the uterine wall. Am. J. Pathol. 1999, 155:293-301.
59. Zhou C.C., Zhang Y., Irani R.A., Zhang H., Mi T., Popek E.J., Hicks M.J., Ramin S.M., Kellems R.E., Xia Y. Angiotensin receptor agonistic autoantibodies induce pre-eclampsia in pregnant mice. Nat. Med. 2008, 14:855-862.
60. Uddin M.N., Agunanne E., Horvat D., Puschett J.B. Alterations in the renin-angiotensin system in a rat model of human preeclampsia. Am. J. Nephrol. 2010, 31:171-177.
61. Liebermann D.A., Hoffman B. MyD genes in negative growth control. Oncogene 1998, 17:3319-3330.
62. Wang X., Gorospe M., Holbrook N.J. Gadd45 is not required for activation of c-Jun N-terminal kinase or p38 during acute stress. J. Biol. Chem. 1999, 274:29599-29602.
63. Vairapandi M., Azam N., Balliet A.G., Hoffman B., Liebermann D.A. Characterization of MyD118, Gadd45, PCNA interacting domains: PCNA impedes MyD/Gadd mediated negative growth control. J. Biol. Chem. 2000, 275:16810-16819.
64. Hildesheim J., Bulavin D.V., Anver M.R., Alvord W.G., Hollander M.C., Vardanian L., Fornace A.J. Jr Gadd45a protects against UV irradiation-induced skin tumors, promotes apoptosis and stress signaling via MAPK and p53. Cancer Res. 2002, 62:7305-7315.
65. Chang L., Karin M. Mammalian MAP kinase signalling cascades. Nature 2001, 410:37-40.
66. Whitmarsh A.J., Davis R.J. Signal transduction: a central control for cell growth. Nature 2000, 403:255-256.
67. Takacs P., Green K.L., Nikaeo A., Kauma S.W. Increased vascular endothelial cell production of interleukin-6 in severe preeclampsia. Am. J. Obstet. Gynecol. 2003, 188:740-744.
68. Tinsley J.H., Chiasson V.L., South S., Mahajan A., Mitchell B.M. Immunosuppression improves blood pressure and endothelial function in a rat model of pregnancy-induced hypertension. Am. J. Hypertens. 2009, 22:1107-1114.
69. Uddin M., Horvat D., Childs E.W., Puschett J.B. Marinobufagenin causes endothelial cell monolayer hyperpermeability by altering apoptotic signaling. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296:R1726-R1734.