Proteomic identification of S-nitrosylated Golgi proteins: New insights into endothelial cell regulation by eNOS-derived NO

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Sangwung, Panjamaporn ^a   Greco, Todd M ^b,c   Wang, Yanzhuang ^d   Ischiropoulos, Harry ^b   Sessa, William C ^a   Iwakiri, Yasuko ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c PRINCETON UNIVERSITY   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTIN; CD147 ANTIGEN; CYSTEINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GOLGI PHOSPHOPROTEIN 3; ONCOPROTEIN; UNCLASSIFIED DRUG; GOLPH3 PROTEIN, HUMAN; MEMBRANE PROTEIN; NITRIC OXIDE; NITRIC OXIDE DONOR;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; AORTA; ARTICLE; CELL COMPARTMENTALIZATION; CELL LYSATE; CONTROLLED STUDY; ENDOTHELIUM CELL; GOLGI COMPLEX; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; ISOLATED LIVER; MALE; MASS SPECTROMETRY; NITROSYLATION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; RAT; RESIDUE ANALYSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CATTLE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; ENDOPLASMIC RETICULUM; ENZYMOLOGY; HUMAN; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; NITROSATION; PATHOLOGY; PROTEOMICS; SPRAGUE DAWLEY RAT;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD147; AORTA; CATTLE; ENDOPLASMIC RETICULUM; ENDOTHELIAL CELLS; GOLGI APPARATUS; HUMANS; MALE; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE III; NITROSATION; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84857418728     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031564     Document Type: Article

References (35)

1. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS, (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6: 150-166.
2. Stamler JS, Simon DI, Osborne JA, Mullins ME, Jaraki O, et al. (1992) S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc Natl Acad Sci U S A 89: 444-448.
3. Stamler JS, (1994) Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78: 931-936.
4. Garcia-Cardena G, Martasek P, Masters BS, Skidd PM, Couet J, et al. (1997) Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J Biol Chem 272: 25437-25440.
5. Garcia-Cardena G, Oh P, Liu J, Schnitzer JE, Sessa WC, (1996) Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc Natl Acad Sci U S A 93: 6448-6453.
6. Sessa WC, Garcia-Cardena G, Liu J, Keh A, Pollock JS, et al. (1995) The Golgi association of endothelial nitric oxide synthase is necessary for the efficient synthesis of nitric oxide. J Biol Chem 270: 17641-17644.
7. Iwakiri Y, Satoh A, Chatterjee S, Toomre DK, Chalouni CM, et al. (2006) Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking. Proc Natl Acad Sci U S A 103: 19777-19782.
8. Iwakiri Y, (2011) S-nitrosylation of proteins: a new insight into endothelial cell function regulated by eNOS-derived NO. Nitric Oxide 25: 95-101.
9. Greco TM, Hodara R, Parastatidis I, Heijnen HF, Dennehy MK, et al. (2006) Identification of S-nitrosylation motifs by site-specific mapping of the S-nitrosocysteine proteome in human vascular smooth muscle cells. Proc Natl Acad Sci U S A 103: 7420-7425.
10. Wilson MC, Meredith D, Halestrap AP, (2002) Fluorescence resonance energy transfer studies on the interaction between the lactate transporter MCT1 and CD147 provide information on the topology and stoichiometry of the complex in situ. J Biol Chem 277: 3666-3672.
11. Wang Y, Taguchi T, Warren G, (2006) Purification of rat liver Golgi stacks. In: Celis J, editors. San Diego Elsevier Science (USA) pp. 33-39.
12. Jaffrey SR, Snyder SH, (2001) The biotin switch method for the detection of S-nitrosylated proteins. Sci STKE 2001: PL1.
13. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH, (2001) Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3: 193-197.
14. Bellinger AM, Reiken S, Carlson C, Mongillo M, Liu X, et al. (2009) Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat Med 15: 325-330.
15. Loureiro-Silva MR, Iwakiri Y, Abraldes JG, Haq O, Groszmann RJ, (2006) Increased phosphodiesterase-5 expression is involved in the decreased vasodilator response to nitric oxide in cirrhotic rat livers. J Hepatol 44: 886-893.
16. Biswas C, Zhang Y, DeCastro R, Guo H, Nakamura T, et al. (1995) The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res 55: 434-439.
17. Guo H, Zucker S, Gordon MK, Toole BP, Biswas C, (1997) Stimulation of matrix metalloproteinase production by recombinant extracellular matrix metalloproteinase inducer from transfected Chinese hamster ovary cells. J Biol Chem 272: 24-27.
18. Sun J, Hemler ME, (2001) Regulation of MMP-1 and MMP-2 production through CD147/extracellular matrix metalloproteinase inducer interactions. Cancer Res 61: 2276-2281.
19. Dippold HC, Ng MM, Farber-Katz SE, Lee SK, Kerr ML, et al. (2009) GOLPH3 bridges phosphatidylinositol-4- phosphate and actomyosin to stretch and shape the Golgi to promote budding. Cell 139: 337-351.
20. Fernandez-Varo G, Ros J, Morales-Ruiz M, Cejudo-Martin P, Arroyo V, et al. (2003) Nitric oxide synthase 3-dependent vascular remodeling and circulatory dysfunction in cirrhosis. Am J Pathol 162: 1985-1993.
21. Capitani M, Sallese M, (2009) The KDEL receptor: new functions for an old protein. FEBS Lett 583: 3863-3871.
22. Wu CC, MacCoss MJ, Mardones G, Finnigan C, Mogelsvang S, et al. (2004) Organellar proteomics reveals golgi arginine dimethylation. Mol Biol Cell 15: 2907-2919.
23. Tang W, Chang SB, Hemler ME, (2004) Links between CD147 function, glycosylation, and caveolin-1. Mol Biol Cell 15: 4043-4050.
24. Kutateladze TG, (2010) Translation of the phosphoinositide code by PI effectors. Nat Chem Biol 6: 507-513.
25. Wood CS, Schmitz KR, Bessman NJ, Setty TG, Ferguson KM, et al. (2009) PtdIns4P recognition by Vps74/GOLPH3 links PtdIns 4-kinase signaling to retrograde Golgi trafficking. J Cell Biol 187: 967-975.
26. Iwakiri Y, Cadelina G, Sessa WC, Groszmann RJ, (2002) Mice with targeted deletion of eNOS develop hyperdynamic circulation associated with portal hypertension. Am J Physiol Gastrointest Liver Physiol 283: G1074-1081.
27. Iwakiri Y, Groszmann RJ, (2006) The hyperdynamic circulation of chronic liver diseases: from the patient to the molecule. Hepatology 43: S121-131.
28. Tazi KA, Barriere E, Moreau R, Heller J, Sogni P, et al. (2002) Role of shear stress in aortic eNOS up-regulation in rats with biliary cirrhosis. Gastroenterology 122: 1869-1877.
29. Doulias PT, Greene JL, Greco TM, Tenopoulou M, Seeholzer SH, et al. (2010) Structural profiling of endogenous S-nitrosocysteine residues reveals unique features that accommodate diverse mechanisms for protein S-nitrosylation. Proc Natl Acad Sci U S A 107: 16958-16963.
30. Aguilera-Romero A, Kaminska J, Spang A, Riezman H, Muniz M, (2008) The yeast p24 complex is required for the formation of COPI retrograde transport vesicles from the Golgi apparatus. J Cell Biol 180: 713-720.
31. Nichols WC, Seligsohn U, Zivelin A, Terry VH, Hertel CE, et al. (1998) Mutations in the ER-Golgi intermediate compartment protein ERGIC-53 cause combined deficiency of coagulation factors V and VIII. Cell 93: 61-70.
32. Strating JR, Martens GJ, (2009) The p24 family and selective transport processes at the ER-Golgi interface. Biol Cell 101: 495-509.
33. Sohda M, Misumi Y, Fujiwara T, Nishioka M, Ikehara Y, (1994) Molecular cloning and sequence analysis of a human 372-kDA protein localized in the Golgi complex. Biochem Biophys Res Commun 205: 1399-1408.
34. Toki C, Fujiwara T, Sohda M, Hong HS, Misumi Y, et al. (1997) Identification and characterization of rat 364-kDa Golgi-associated protein recognized by autoantibodies from a patient with rheumatoid arthritis. Cell Struct Funct 22: 565-577.
35. Renna M, Faraonio R, Bonatti S, De Stefano D, Carnuccio R, et al. (2006) Nitric oxide-induced endoplasmic reticulum stress activates the expression of cargo receptor proteins and alters the glycoprotein transport to the Golgi complex. Int J Biochem Cell Biol 38: 2040-2048.