Analysis of Nitroso-proteomes in Normotensive and severe preeclamptic human placentas

Biology of Reproduction

Volumn 84, Issue 5, 2011, Pages 966-975

  Zhang, Hong Hai ^a   Wang, Yu Ping ^c   Chen, Dong Bao ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Louisiana State University School of Medicine Shreveport   (United States)

Author keywords

Nitric oxide; Placenta; Preeclampsia; Proteomics; S nitrosylation

Indexed keywords

BIOTIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEAT SHOCK PROTEIN 90; NITRATE; NITRITE; PLACENTA PROTEIN; PROTEOME;

ADULT; ARTICLE; BLOOD PRESSURE; CELL METABOLISM; CELL MOTION; FEMALE; HUMAN; HUMAN TISSUE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NITROSYLATION; PLACENTA; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN SYNTHESIS; S NITROSYLATION; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

ADOLESCENT; ADULT; DOWN-REGULATION; FEMALE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; NITRATES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; NITRITES; NITROSATION; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY PROTEINS; PROTEOME; PROTEOMICS; SEVERITY OF ILLNESS INDEX; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TWO-DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UP-REGULATION; YOUNG ADULT;

EID: 79956259342     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.090688     Document Type: Article

References (64)

1. Roberts JM, Cooper DW. Pathogenesis and genetics of pre-eclampsia. Lancet 2001; 357:53-56.
2. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science 2005; 308:1592-1594.
3. Roberts JM, Hubel CA, Taylor RN. Endothelial dysfunction yes, cytotoxicity no! Am J Obstet Gynecol 1995; 173:978-979.
4. Sladek SM, Magness RR, Conrad KP. Nitric oxide and pregnancy. Am J Physiol 1997; 272:R441-R463.
5. Sanyal M, Nag TC, Das C. Localization of nitric oxide synthase in human trophoblast cells: role of nitric oxide in trophoblast proliferation and differentiation. Am J Reprod Immunol 2000; 43:70-77.
6. Buhimschi I, Yallampalli C, Chwalisz K, Garfield RE. Pre-eclampsia-like conditions produced by nitric oxide inhibition: effects of L-arginine, Darginine and steroid hormones. Hum Reprod 1995; 10:2723-2730.
7. van der Heijden OW, Essers YP, Fazzi G, Peeters LL, De Mey JG, van Eys GJ. Uterine artery remodeling and reproductive performance are impaired in endothelial nitric oxide synthase-deficient mice. Biol Reprod 2005; 72:1161-1168.
8. Denninger JW, Marletta MA. Guanylate cyclase and the NO/cGMP signaling pathway. Biochim Biophys Acta 1999; 1411:334-350.
9. Wanstall JC, Homer KL, Doggrell SA. Evidence for, and importance of, cGMP-independent mechanisms with NO and NO donors on blood vessels and platelets. Curr Vasc Pharmacol 2005; 3:41-53.
10. Smith KM, Moore LC, Layton HE. Advective transport of nitric oxide in a mathematical model of the afferent arteriole. Am J Physiol Renal Physiol 2003; 284:F1080-F1096.
11. Radi R, Peluffo G, Alvarez MN, Naviliat M, Cayota A. Unraveling peroxynitrite formation in biological systems. Free Radic Biol Med 2001; 30:463-488.
12. Webster RP, Brockman D, Myatt L. Nitration of p38 MAPK in the placenta: association of nitration with reduced catalytic activity of p38 MAPK in pre-eclampsia. Mol Hum Reprod 2006; 12:677-685.
13. Webster RP, Roberts VH, Myatt L. Protein nitration in placenta- functional significance. Placenta 2008; 29:985-994.
14. Stamler JS, Lamas S, Fang FC. Nitrosylation. The prototypic redox-based signaling mechanism. Cell 2001; 106:675-683.
15. Boehning D, Snyder SH. Novel neural modulators. Annu Rev Neurosci 2003; 26:105-131.
16. Foster MW, McMahon TJ, Stamler JS. S-nitrosylation in health and disease. Trends Mol Med 2003; 9:160-168.
17. Stamler JS, Simon DI, Osborne JA, Mullins ME, Jaraki O, Michel T, Singel DJ, Loscalzo J. S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc Natl Acad Sci U S A 1992; 89:444-448.
18. Keaney JF Jr, Simon DI, Stamler JS, Jaraki O, Scharfstein J, Vita JA, Loscalzo J. NO forms an adduct with serum albumin that has endotheliumderived relaxing factor-like properties. J Clin Invest 1993; 91:1582-1589.
19. Reynaert NL, Ckless K, Wouters EF, van der Vliet A, Janssen-Heininger YM. Nitric oxide and redox signaling in allergic airway inflammation. Antioxid Redox Signal 2005; 7:129-143.
20. Liu L, Yan Y, Zeng M, Zhang J, Hanes MA, Ahearn G, McMahon TJ, Dickfeld T, Marshall HE, Que LG, Stamler JS. Essential roles of Snitrosothiols in vascular homeostasis and endotoxic shock. Cell 2004; 116: 617-628.
21. Lima B, Forrester MT, Hess DT, Stamler JS. S-nitrosylation in cardiovascular signaling. Circ Res 2010; 106:633-646.
22. Lima B, Lam GK, Xie L, Diesen DL, Villamizar N, Nienaber J, Messina E, Bowles D, Kontos CD, Hare JM, Stamler JS, Rockman HA. Endogenous S-nitrosothiols protect against myocardial injury. Proc Natl Acad Sci U S A 2009; 106:6297-6302.
23. Mannick JB, Hausladen A, Liu L, Hess DT, Zeng M, Miao QX, Kane LS, Gow AJ, Stamler JS. Fas-induced caspase denitrosylation. Science 1999; 284:651-654.
24. Dash PR, Cartwright JE, Baker PN, Johnstone AP, Whitley GS. Nitric oxide protects human extravillous trophoblast cells from apoptosis by a cyclic GMP-dependent mechanism and independently of caspase 3 nitrosylation. Exp Cell Res 2003; 287:314-324.
25. Harris LK, McCormick J, Cartwright JE, Whitley GS, Dash PR. Snitrosylation of proteins at the leading edge of migrating trophoblasts by inducible nitric oxide synthase promotes trophoblast invasion. Exp Cell Res 2008; 314:1765-1776.
26. Pruitt KD, Tatusova T, Maglott DR. NCBI reference sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 2007; 35:D61-D65.
27. Lauer T, Preik M, Rassaf T, Strauer BE, Deussen A, Feelisch M, Kelm M. Plasma nitrite rather than nitrate reflects regional endothelial nitric oxide synthase activity but lacks intrinsic vasodilator action. Proc Natl Acad Sci U S A 2001; 98:12814-12819.
28. Lane P, Hao G, Gross SS. S-nitrosylation is emerging as a specific and fundamental posttranslational protein modification: head-to-head comparison with O-phosphorylation. Sci STKE 2001; (86):re1.
29. Ravi K, Brennan LA, Levic S, Ross PA, Black SM. S-nitrosylation of endothelial nitric oxide synthase is associated with monomerization and decreased enzyme activity. Proc Natl Acad Sci U S A 2004; 101:2619-2624.
30. Jaffrey SR, Snyder SH. The biotin switch method for the detection of Snitrosylated proteins. Sci STKE 2001;(86):pl1.
31. Zhang HH, Feng L, Livnat I, Hoh JK, Shim JY, Liao WX, Chen DB. Estradiol-17(beta) stimulates specific receptor and endogenous nitric oxide-dependent dynamic endothelial protein S-nitrosylation: analysis of endothelial nitrosyl-proteome. Endocrinology 2010; 151:3874-3887.
32. Giustarini D, Dalle-Donne I, Colombo R, Milzani A, Rossi R. Is ascorbate able to reduce disulfide bridges? A cautionary note. Nitric Oxide 2008; 19: 252-258.
33. Huang B, Chen SC, Wang DL. Shear flow increases S-nitrosylation of proteins in endothelial cells. Cardiovasc Res 2009; 83:536-546.
34. Norris LA, Higgins JR, Darling MR, Walshe JJ, Bonnar J. Nitric oxide in the uteroplacental, fetoplacental, and peripheral circulations in preeclampsia. Obstet Gynecol 1999; 93:958-963.
35. Nobunaga T, Tokugawa Y, Hashimoto K, Kimura T, Matsuzaki N, Nitta Y, Fujita T, Kidoguchi KI, Azuma C, Saji F. Plasma nitric oxide levels in pregnant patients with preeclampsia and essential hypertension. Gynecol Obstet Invest 1996; 41:189-193.
36. Smarason AK, Allman KG, Young D, Redman CW. Elevated levels of serum nitrate, a stable end product of nitric oxide, in women with preeclampsia. Br J Obstet Gynaecol 1997; 104:538-543.
37. Bartha JL, Comino-Delgado R, Bedoya FJ, Barahona M, Lubian D, Garcia-Benasach F. Maternal serum nitric oxide levels associated with biochemical and clinical parameters in hypertension in pregnancy. Eur J Obstet Gynecol Reprod Biol 1999; 82:201-207.
38. Pathak N, Sawhney H, Vasishta K, Majumdar S. Estimation of oxidative products of nitric oxide (nitrates, nitrites) in preeclampsia. Aust N Z J Obstet Gynaecol 1999; 39:484-487.
39. Shaamash AH, Elsnosy ED, Makhlouf AM, Zakhari MM, Ibrahim OA, EL-dien HM. Maternal and fetal serum nitric oxide (NO) concentrations in normal pregnancy, pre-eclampsia and eclampsia. Int J Gynaecol Obstet 2000; 68:207-214.
40. Salas SP. Role of nitric oxide in maternal hemodynamics and hormonal changes in pregnant rats. Biol Res 1998; 31:243-250.
41. Mutlu-Turkoglu U, Aykac-Toker G, Ibrahimoglu L, Ademoglu E, Uysal M. Plasma nitric oxide metabolites and lipid peroxide levels in preeclamptic pregnant women before and after delivery. Gynecol Obstet Invest 1999; 48:247-250.
42. Silver RK, Kupferminc MJ, Russell TL, Adler L, Mullen TA, Caplan MS. Evaluation of nitric oxide as a mediator of severe preeclampsia. Am J Obstet Gynecol 1996; 175:1013-1017.
43. Egerman RS, Andersen RN, Manejwala FM, Sibai BM. Neuropeptide Y and nitrite levels in preeclamptic and normotensive gravid women. Am J Obstet Gynecol 1999; 181:921-923.
44. Messmer UK, Lapetina EG, Brune B. Nitric oxide-induced apoptosis in RAW 264.7 macrophages is antagonized by protein kinase C- and protein kinase A-activating compounds. Mol Pharmacol 1995; 47:757-765.
45. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein Snitrosylation: purview and parameters. Nat Rev Mol Cell Biol 2005; 6: 150-166.
46. Forrester MT, Foster MW, Stamler JS. Assessment and application of the biotin switch technique for examining protein S-nitrosylation under conditions of pharmacologically induced oxidative stress. J Biol Chem 2007; 282:13977-13983.
47. Myatt L, Cui X. Oxidative stress in the placenta. Histochem Cell Biol 2004; 122:369-382.
48. Sun J, Morgan M, Shen RF, Steenbergen C, Murphy E. Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ Res 2007; 101:1155-1163.
49. Torta F, Usuelli V, Malgaroli A, Bachi A. Proteomic analysis of protein Snitrosylation. Proteomics 2008; 8:4484-4494.
50. Yang Y, Loscalzo J. S-nitrosoprotein formation and localization in endothelial cells. Proc Natl Acad Sci U S A 2005; 102:117-122.
51. Santhanam L, Gucek M, Brown TR, Mansharamani M, Ryoo S, Lemmon CA, Romer L, Shoukas AA, Berkowitz DE, Cole RN. Selective fluorescent labeling of S-nitrosothiols (S-FLOS): a novel method for studying S-nitrosation. Nitric Oxide 2008; 19:295-302.
52. Martinez-Ruiz A, Villanueva L, Gonzalez de Orduna C, Lopez-Ferrer D, Higueras MA, Tarin C, Rodriguez-Crespo I, Vazquez J, Lamas S. Snitrosylation of Hsp90 promotes the inhibition of its ATPase and endothelial nitric oxide synthase regulatory activities. Proc Natl Acad Sci U S A 2005; 102:8525-8530.
53. Rhee SG, Chae HZ, Kim K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med 2005; 38:1543-1552.
54. Fang J, Nakamura T, Cho DH, Gu Z, Lipton SA. S-nitrosylation of peroxiredoxin 2 promotes oxidative stress-induced neuronal cell death in Parkinson's disease. Proc Natl Acad Sci U S A 2007; 104:18742-18747.
55. Hara MR, Agrawal N, Kim SF, Cascio MB, Fujimuro M, Ozeki Y, Takahashi M, Cheah JH, Tankou SK, Hester LD, Ferris CD, Hayward SD, et al. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 2005; 7:665-674.
56. Goldman-Wohl D, Yagel S. Regulation of trophoblast invasion: from normal implantation to pre-eclampsia. Mol Cell Endocrinol 2002; 187: 233-238.
57. Brouillette CG, Anantharamaiah GM, Engler JA, Borhani DW. Structural models of human apolipoprotein A-I: a critical analysis and review. Biochim Biophys Acta 2001; 1531:4-46.
58. Huang Y, Wang KK. The calpain family and human disease. Trends Mol Med 2001; 7:355-362.
59. Strobl JS, Thomas MJ. Human growth hormone. Pharmacol Rev 1994; 46: 1-34.
60. Tamatani M, Matsuyama T, Yamaguchi A, Mitsuda N, Tsukamoto Y, Taniguchi M, Che YH, Ozawa K, Hori O, Nishimura H, Yamashita A, Okabe M, et al. ORP150 protects against hypoxia/ischemia-induced neuronal death. Nat Med 2001; 7:317-323.
61. Thauer RK. Citric-acid cycle, 50 years on. Modifications and an alternative pathway in anaerobic bacteria. Eur J Biochem 1988; 176:497-508.
62. Schmid SL. Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu Rev Biochem 1997; 66:511-548.
63. Drenth JP, Tahvanainen E, te Morsche RH, Tahvanainen P, Kaariainen H, Hockerstedt K, van de Kamp JM, Breuning MH, Jansen JB. Abnormal hepatocystin caused by truncating PRKCSH mutations leads to autosomal dominant polycystic liver disease. Hepatology 2004; 39: 924-931.
64. Towbin H, Ozbey O, Zingel O. An immunoblotting method for highresolution isoelectric focusing of protein isoforms on immobilized pH gradients. Electrophoresis 2001; 22:1887-1893.