Lipid-modified proteins as biomarkers for cardiovascular disease: A review

Biomarkers

Volumn 10, Issue 4, 2005, Pages 219-237

  Ferri, N ^a   Paoletti, R ^a   Corsini, Alberto ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Atherosclerosis; Farnesol; Geranylgeraniol; Mevalonate pathway; Prenylated proteins; Statin

Indexed keywords

ACETYLCHOLINESTERASE; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ALKALINE PHOSPHATASE; BIOLOGICAL MARKER; CD14 ANTIGEN; CELL SURFACE PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYSTEINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FARNESOL; FOLATE RECEPTOR; GERANYLGERANIOL; GLYCINE; GLYCOPROTEIN IB; GLYCOSYLPHOSPHATIDYLINOSITOL; GUANINE NUCLEOTIDE BINDING PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; ISOPRENOID; LIPOPROTEIN LIPASE; NERVE CELL ADHESION MOLECULE; PRAVASTATIN; PROTEIN KINASE FYN; PROTEIN KINASE LYN; PROTEIN N MYRISTOYLTRANSFERASE; RAS PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; ROSUVASTATIN; SONIC HEDGEHOG PROTEIN; UNINDEXED DRUG;

AMINO TERMINAL SEQUENCE; ATHEROGENESIS; ATHEROSCLEROSIS; CARBOXY TERMINAL SEQUENCE; CARDIOVASCULAR DISEASE; CATALYSIS; CLINICAL TRIAL; COVALENT BOND; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; MYRISTYLATION; NONHUMAN; PALMITOYLATION; PLEIOTROPY; PRENYLATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; REVIEW;

ACYLTRANSFERASES; ARTERIOSCLEROSIS; BIOLOGICAL MARKERS; CARDIOVASCULAR DISEASES; CHOLESTEROL; CYSTEINE; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; MEMBRANE PROTEINS; MYRISTIC ACID; PALMITIC ACID; PROTEIN ISOPRENYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RAS PROTEINS;

EID: 26844473519     PISSN: 1354750X     EISSN: 13665804     Source Type: Journal    
DOI: 10.1080/13547500500216660     Document Type: Review

References (138)

1. Adjei AA, Davis JN, Erlichman C, Svingen PA, Kaufmann SH. 2000. Comparison of potential markers of farnesyltransferase inhibition. Clinical Cancer Research 6:2318-2325.
2. Ames JB, Tanaka T, Stryer L, Ikura M. 1994. Secondary structure of myristoylated recovering determined by three-dimensional heteronuclear NMR: implications for the calcium-myristoyl switch. Biochemistry 33:10743-10753.
3. Azim AC, Barkalow K, Chou J, Hartwig JH. 2000. Activation of the small GTPases, rac and cdc42, after ligation of the platelet PAR-1 receptor. Blood 95:959-964.
4. Baker AH, Edwards DR, Murphy G. 2002. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. Journal of Cell Science 115:3719-3727.
5. Bellosta S, Ferri N, Bernini F, Paoletti R, Corsini A. 2000. Non-lipid-related effects of statin. Annals of Medicine 32:164-176.
6. Bizzozero OA, Tetzloff SU, Bharadwaj M. 1994. Overview: protein palmitoylation in the nervous system: current views and unsolved problems. Neurochemistry Research 19:923-933.
7. Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, Wolfson MF, Castner BJ, Stocking KL, Reddy P, Srinivasan S, et al. 1997. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385:729-733.
8. Blair A, Shaul PW, Yuhanna IS, Conrad PA, Smart EJ. 1999. Oxidized low density lipoprotein displaces endothelial nitric-oxide synthase (eNOS) from plasmalemmal caveolae and impairs eNOS activation. Journal of Biological Chemistry 274:32512-32519.
9. Bonatti S, Migliaccio G, Simons K. 1989. Palmitylation of viral membrane glycoproteins takes place after exit from the endoplasmic reticulum. Journal of Biological Chemistry 264:12590-12595.
10. Briscoe J, Pierani A, Jessell TM, Ericson J. 2000. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101:435-445.
11. Busconi L, Michel T. 1993. N-terminal myristoylation determines subcellular localization. Journal of Biological Chemistry 268:8410-8413.
12. 2 terminus of Src. Biochemistry 33:13093-13101.
13. Canault M, Peiretti F, Mueller C, Kopp F, Morange P, Rihs S, Portugal H, Juhan-Vague I, Nalbone G. 2004. Exclusive expression of transmembrane TNF-alpha in mice reduces the inflammatory response in early lipid lesions of aortic sinus. Atherosclerosis 172:211-218.
14. Casey PJ. 1995. Protein lipidation in cell signaling. Science 268:221-225.
15. Casey PJ, Seabra MC. 1996. Protein prenyltransferases. Journal of Biological Chemistry 271:5289-5292.
16. Chatterjee S, Mayor. 2001. SCMLS cell. Molecular Life Sciences 58:1969-1987.
17. Chemla E, Castier Y, Julia P, Pirotski E, Carpentier A, Fabiani JN. 1997. Inhibition of intimal hyperplasia by an antisense oligonucleotide of farnesyl transferase delivered endoluminally during iliac angioplasty in a rabbit model. Annals of Vascular Surgery 11:581-587.
18. Chiang TM. 1997. Collagen-induced platelet aggregation and release reaction: role of ras protein. Thrombosis Research 88:205-213.
19. Cicha I, Schneiderhan-Marra N, Yilmaz A, Garlichs CD, Goppelt-Struebe M. 2004. Monitoring the cellular effects of HMG-CoA reductase inhibitors in vitro and ex vivo. Arteriosclerosis and Thrombosis Vascular Biology 24:2046-2050.
20. Cohen LH, Pieterman E, van Leeuwen RE, Du J, Negre-Aminou P, Valentijn AR, Overhand M, van der Marel GA, van Boom JH. 1999. Inhibition of human smooth muscle cell proliferation in culture by farnesyl pyrophosphate analogues, inhibitors of in vitro protein: farnesyl transferase. Biochemical Pharmacology 57:365-373.
21. Coleman ML, Marshall CJ, Olson MF. 2004. RAS and RHO GTPases in G1-phase cell-cycle regulation. Nature Reviews in Molecular Cell Biology 5:355-366.
22. Corsini A, Bellosta S, Baetta R, Fumagalli R, Paoletti R, Bernini F. 1999. New insights into the pharmacodynamic and pharmacokinetic properties of statins. Pharmacology Therapy 84:413-428.
23. Corsini A, Mazzotti M, Raiteri M, Soma MR, Gabbiam G, Fumagalli R, Paoletti R. 1993. Relationship between mevalonate pathway and arterial myocyte proliferation: in vitro studies with inhibitors of HMG-CoA reductase. Atherosclerosis 101:117-125.
24. Cross FR, Garber EA, Pellman D, Hanafusa H. 1984. A short sequence in the p60src N terminus is required for p60src myristylation and membrane association and for cell transformation. Molecular Cell Biology 4:1834-1842.
25. Dai Q, Choy E, Chin V, Romano J, Slivka SR, Steitz SA, Michaelis S, Philips MR. 1998. Mammalian prenylcysteine carboxyl methyltransferase is in the endoplasmic reticulum. Journal of Biological Chemistry 273:15030-15034.
26. Dorfleutner A, Ruf W. 2003. Regulation of tissue factor cytoplasmic domain phosphorylation by palmitoylation. Blood 102:3998-4005.
27. Drake TA, Cheng J, Chang A, Taylor FB Jr. 1993. Expression of tissue factor, thrombomodulin, and E-selectin in baboons with lethal Escherichia coli sepsis. American Journal of Pathology 142:1458-1470.
28. Dunphy JT, Greentree WK, Manahan CL, Linder ME. 1996. G-protein palmitoyltransferase activity is enriched in plasma membranes. Journal of Biological Chemistry 271:7154-7159.
29. Dunphy JT, Linder ME. 1998. Signalling functions of protein palmitoylation. Biochimica et Biophysica Acta 1436:245-261.
30. Eisenhaber B, Bork P, Eisenhaber F. 2001. Post-translational GPI lipid anchor modification of proteins in kingdoms of life: analysis of protein sequence data from complete genomes. Protein Engineering 14:17-25.
31. Englund PT. 1993. The structure and biosynthesis of glycosyl phosphatidylinositol protein anchors. Annual Reviews in Biochemistry 62:121-138.
32. Farnsworth CC, Seabra MC, Ericsson LH, Gelb MH, Glomset JA. 1994. Rab geranylgeranyl transferase catalyzes the geranylgeranylation of adjacent cysteines in the small GTPases Rab 1A, Rab3A, and Rab5A. Proceedings of the National Academy of Sciences USA 91:11963-11967.
33. Feron O, Michel JB, Sase K, Michel T. 1998. Dynamic regulation of endothelial nitric oxide synthase: complementary roles of dual acylation and caveolin interactions. Biochemistry 37:193-200.
34. Ferri N, Arnaboldi L, Orlandi A, Yokoyama K, Gree R, Granata A, Hachem A, Paoletti R, Gelb MH, Corsini A. 2001. Effect of S(-) perillic acid on protein prenylation and arterial smooth muscle cell proliferation. Biochemical Pharmacology 62:1637-1645.
35. Ferri N, Yokoyama K, Sadilek M, Paoletti R, Apitz-Castro R, Gelb MH, Corsini A. 2003. Ajoene, a garlic compound, inhibits protein prenylation and arterial smooth muscle cell proliferation. British Journal of Pharmacology 138:811-818.
36. Galis ZS, Sukhova GK, Lark MW, Libby P. 1994. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. Journal of Clinical Investigation 94:2493-2503.
37. Gauthier MC, Racine C, Ferland C, Flamand N, Chakir J, Tremblay GM, Laviolette M. 2003. Expression of membrane type-4 matrix metalloproteinase (metalloproteinase-17) by human eosinophils. International Journal of Biochemistry and Cell Biology 35:1667-1673.
38. George J, Afek A, Keren P, Herz I, Goldberg I, Haklai R, Kloog Y, Keren G. 2002. Functional inhibition of Ras by S-trans, trans-farnesyl thiosalicylic acid attenuates atherosclerosis in apolipoprotein E knockout mice. Circulation 105:2416-2422.
39. Ghosh S, Gachhui R, Crooks C, Wu C, Lisanti MP, Stuehr DJ. 1998. Interaction between caveolin-1 and the reductase domain of endothelial nitric-oxide synthase: Consequences for catalysis. Journal of Biological Chemistry 273:22267-22271.
40. Hallak H, Muszbek L, Laposata M, Belmonte E, Brass LF, Manning DR. 1994. Covalent binding of arachidonate to G protein alpha subunits of human platelets. Journal of Biological Chemistry 269:4713-4716.
41. Hancock JF, Cadwallader K, Marshall CJ. 1991a. Methylation and proteolysis are essential for efficient membrane binding of prenylated p21K-ras(B). EMBO Journal 10:641-646.
42. Hancock JF, Cadwallader K, Paterson H, Marshall CJ. 1991b. A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. EMBO Journal 10:4033-4039.
43. Hancock JF, Paterson H, Marshall CJ. 1990. A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell 63:133-139.
44. Hayes JS, Lawler OA, Walsh MT, Kinsella BT. 1999. The prostacyclin receptor is isoprenylated. Isoprenylation is required for efficient receptor-effector coupling. Journal of Biological Chemistry 274:23707-23718.
45. Ignarro LJ. 1990. Nitric oxide: a novel signal transduction mechanism for transcellular communication. Hypertension 16:477-483.
46. Ikezawa H. 2002. Glycosylphosphatidylinositol (GPI)-anchored proteins. Biology and Pharmacology Bulletin 25:409-417.
47. Indolfi C, Avvedimento EV, Rapacciuolo A, Di Lorenzo E, Esposito G, Stabile E, Feliciello A, Mele E, Giuliano P, Condorelli G, et al. 1995. Inhibition of cellular ras prevents smooth muscle cell proliferation after vascular injury in vivo. Nature Medicine 1:541-545.
48. Irani K, Herzlinger S, Finkel T. 1994. Ras proteins regulate multiple mitogenic pathways in A10 vascular smooth muscle cells. Biochemistry and Biophysics Research Communications 202:1252-1258.
49. Ishibashi T, Sakamoto T, Ohkawara H, Nagata K, Sugimoto K, Sakurada S, Sugimoto N, Watanabe A, Yokoyama K, Sakamoto N, et al. 2003. Integral role of RhoA activation in monocyte adhesion-triggered tissue factor expression in endothelial cells. Arteriosclerosis and Thrombosis Vascular Biology 23:681-687.
50. Itoh Y, Kajita M, Kinoh H, Mori H, Okada A, Seiki M. 1999. Membrane type 4 matrix metalloproteinase (MT4-MMP, MMP-17) is a glycosylphosphatidylinositol-anchored proteinase. Journal of Biological Chemistry 274:34260-34266.
51. Jeromin A, Muralidhar D, Parameswaran MN, Roder J, Fairwell T, Scarlata S, Dowal L, Mustafi SM, Chary KV, Sharma Y. 2004. N-terminal myristoylation regulates calcium-induced conformational changes in neuronal calcium sensor-1. Journal of Biological Chemistry 279:27158-27167.
52. Johnson DR, Bhatnagar RS, Knoll LJ, Gordon JI. 1994. Genetic and biochemical studies of protein N-myristoylation. Annual Reviews in Biochemistry 63:869-914.
53. Kamps MP, Buss JE, Sefton BM. 1985. Mutation of NH2-terminal glycine of p60sre prevents both myristoylation and morphological transformation. Proceedings of the National Academy of Sciences USA 82:4625-4628.
54. Kojima S, Itoh Y, Matsumoto S, Masuho Y, Seiki M. 2000. Membrane-type 6 matrix metalloproteinase (MT6-MMP, MMP-25) is the second glycosyl-phosphatidyl inositol (GPI)-anchored MMP. FEBS Letters 480:142-146.
55. Ledoux S, Laouari D, Essig M, Runembert I, Trugnan G, Michel JB, Friedlander G. 2002. Lovastatin enhances ecto-5′-nucleotidase activity and cell surface expression in endothelial cells: implication of rho-family GTPases. Circulation Research 90:420-427.
56. Liang X, Lu Y, Neubert TA, Resh MD. 2002. Mass spectrometric analysis of GAP-43/neuromodulin reveals the presence of a variety of fatty acylated species. Journal of Biological Chemistry 277:33032-33040.
57. Liang X, Lu Y, Wilkes M, Neubert TA, Resh MD. 2004. The N-terminal SH4 region of the Ste family kinase Fyn is modified by methylation and heterogeneous fatty acylation: role in membrane targeting, cell adhesion, and spreading. Journal of Biological Chemistry 279:8133-8139.
58. Liao JK. 2002. Isoprenoids as mediators of the biological effects of statins. Journal of Clinical Investigation 110:285-288.
59. Lobell RB, Liu D, Buser CA, Davide JP, DePuy E, Hamilton K, Koblan KS, Lee Y, Mosser S, Motzel SL, et al. 2002. Preclinical and clinical pharmacodynamic assessment of L-778,123, a dual inhibitor of farnesyl:protein transferase and geranylgeranyl:protein transferase type-I. Molecular Cancer Therapy 1:747-758.
60. Long SB, Casey PJ, Beese LS. 1998. Cocrystal structure of protein farnesyltransferase complexed with a farnesyl diphosphate substrate. Biochemistry 37:9612-9618.
61. Mann M, Talbo G. 1996. Developments in matrix-assisted laser desorption/ionization peptide mass spectrometry. Current Opinions in Biotechnology 7:11-19.
62. Marcus AJ, Brockman MJ, Drosopoulos JH, Islam N, Alyonycheva TN, Safier LB, Hajjar KA, Posnett DN, Schoenborn MA, Schooley KA, et al. 1997. The endothelial cell ecto-ADPase responsible for inhibition of platelet function is C39. Journal of Clinical Investigation 99:1351-1360.
63. Matsubara M, Titani K, Taniguchi H, Hayashi N. 2003. Direct involvement of protein myristoylation in myristoylated alanine-rich C kinase substrate (MARCKS)-calmodulin interaction. Journal of Biological Chemistry 278:48898-48902.
64. Mayor S, Riezman H. 2004. Sorting GPI-anchored proteins. Nature Reviews in Molecular Cell Biology 5:110-120.
65. Miggin SM, Lawler OA, Kinsella BT. 2003. Palmitoylation of the human prostacyclin receptor. Functional implications of palmitoylation and isoprenylation. Journal of Biological Chemistry 278:6947-6958.
66. Misumi Y, Ogata S, Ohkubo K, Hirose S, Ikehara Y. 1990. Primary structure of human placental 5′-nucleotidase and identification of the glycolipid anchor in the mature form. European Journal of Biochemistry 191:563-569.
67. Miyata T, Takeda J, Iida Y, Yamada N, Inoue N, Takahashi M, Maeda K, Kitani T, Kinoshita T. 1993. The cloning of PIG-A, a component in the early step of GPI-anchor biosynthesis. Science 259:1318-1320.
68. Moncada S. 1982. Eighth Gaddum Memorial Lecture. University of London Institute of Education, December 1980, Biological importance of prostacyclin. British Journal of Pharmacology 76:3-31.
69. Moores SL, Schaber MD, Mosser SD, Rands E, O'Hara MB, Garsky VM, Marshall MS, Pompliano DL, Gibbs JB. 1991. Sequence dependence of protein isoprenylation. Journal of Biological Chemistry 266:14603-14610.
70. Moss ML, Jin SL, Milla ME, Bickett DM, Burkhart W, Carter HL, Chen WJ, Clay WC, Didsbury JR, Hassler D, et al. 1997. Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-alpha. Nature 385:733-736.
71. Mullor JL, Sanchez P, Altaba AR. 2002. Pathways and consequences: Hedgehog signaling in human disease. Trends in Cell Biology 12:562-569.
72. Mumby SM. 1997. Reversible palmitoylation of signaling proteins. Current Opinions in Cell Biology 9:148-154.
73. Murray D, Hermida-Matsumoto L, Buser CA, Tsang J, Sigal CT, Ben-Tal N, Honig B, Resh MD, McLaughlin S. 1998. Electrostatics and the membrane association of Src: theory and experiment. Biochemistry 37:2145-2159.
74. Muszbek L, Laposata M. 1989. Glycoprotein Ib and glycoprotein IX in human platelets are acylated with palmitic acid through thioester linkages. Journal of Biological Chemistry 264:9716-9719.
75. O'Brien KD, Pineda C, Chiu WS, Bowen R, Deeg MA. 1999. Glycosylphosphatidylinositol-specific phospholipase D is expressed by macrophages in human atherosclerosis and colocalizes with oxidation epitopes. Circulation 99:2876-2882.
76. Oh J, Takahashi R, Kondo S, Mizoguchi A, Adachi E, Sasahara RM, Nishimura S, Imamura Y, Kitayama H, Alexander DB, et al. 2001. The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 107:789-800.
77. Oida H, Namba T, Sugimoto Y, Ushikubi F, Ohishi H, Ichikawa A, Narumiya S. 1995. In situ hybridization studies of prostacychn receptor mRNA expression in various mouse organs. British Journal of Pharmacology 116:2828-2837.
78. Olson MF, Ashworth A, Hall A. 1995. An essential role for Rho, Rac, and Cdc42 GTPases in cell cycle progression through G1. Science 269:1270-1272.
79. Park HW, Boduluri SR, Moomaw JF, Casey PJ, Beese LS. 1997. Crystal structure of protein farnesyltransferase at 2.25 angstrom resolution. Science 275:1800-1804.
80. Peters C, Wolf A, Wagner M, Kuhlmann J, Waldmann H. 2004. The cholesterol membrane anchor of the Hedgehog protein confers stable membrane association to lipid-modified proteins. Proceedings of the National Academy of Sciences USA 101:8531-8536.
81. Peterson SN, Lapetina EG. 1994. Platelet activation and inhibition. Novel signal transduction mechanisms. Annals of the New York Academy of Sciences 714:53-63.
82. Porter JA, Von Kessler DP, Ekker SC, Young KE, Lee JJ, Moses K, Beachy PA. 1995. The product of hedgehog autoproteolytic cleavage active in local and long-range signalling. Nature 374:363-366.
83. Porter JA, Young KE, Beachy PA. 1996. Cholesterol modification of hedgehog signaling proteins in animal development. Science 274:255-259.
84. Raiteri M, Arnaboldi L, McGeady P, Gelb MH, Verri D, Tagliabue C, Quarato P, Ferraboschi P, Santaniello E, Paoletti R, et al. 1997. Pharmacological control of the mevalonate pathway: effect on arterial smooth muscle cell proliferation. Journal of Pharmacology and Experimental Therapy 281:1144-1153.
85. Reid TS, Terry KL, Casey PJ, Beese LS. 2004. Crystallographic analysis of CaaX prenyltransferases complexed with substrates defines rules of protein substrate selectivity. Journal of Molecular Biology 343:417-433.
86. Reiss Y, Stradley SJ, Gierasch LM, Brown MS, Goldstein JL. 1991. Sequence requirement for peptide recognition by rat brain p21ras protein farnesyltransferase. Proceedings of the National Academy of Sciences USA 88:732-736.
87. Resh MD. 1994. Myristylation and palmitylation of Src family members: the fats of the matter. Cell 76:411-413.
88. Resh MD. 1999. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochimica et Biophysica Acta 1451:1-16.
89. Resta R, Hooker SW, Hansen KR, Laurent AB, Park JL, Blackburn MR, Knudsen TB, Thompson LF. 1993. Murine ecto-5′-nucleotidase (CD73): cDNA cloning and tissue distribution. Gene 133:171-177.
90. Ridker PM, Brown NJ, Vaughan DE, Harrison DG, Mehta JL. 2004. Established and emerging plasma biomarkers in the prediction of first atherothrombotic events. Circulation 109:IV6-IV19.
91. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. 2003. Cell migration: integrating signals from front to back. Science 302:1704-1709.
92. Robinson LJ, Busconi L, Michel T. 1995. Agonist-modulated palmitoylation of endothelial nitric oxide synthase. Journal of Biological Chemistry 270:995-998.
93. Robinson LJ, Michel T. 1995. Mutagenesis of palmitoylation sites in endothelial nitric oxide synthase identifies a novel motif for dual acylation and subcellular targeting. Proceedings of the National Academy of Sciences USA 92:11776-11780.
94. Robinson PJ. 1991. Phosphatidylinositol membrane anchors and T-cell activation. Immunology Today 12:35-41.
95. Robinson PJ. 1997. Signal transduction via GPI-anchored membrane proteins. Advances in Experimental Medicine and Biology 419:365-370.
96. Roelink H, Porter JA, Chiang C, Tanabe Y, Chang DT, Beachy PA, Jessell TM. 1995. Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81:445-455.
97. Roepstorff P. 1997. Mass spectrometry in protein studies from genome to function. Current Opinions in Biotechnology 8:6-13.
98. Roskoski R Jr, Ritchie P. 1998. Role of the carboxyterminal residue in peptide binding to protein farnesyltransferase and protein geranylgeranyltransferase. Archives in Biochemistry and Biophysics 356:167-176.
99. Ross R. 1999. Atherosclerosis - an inflammatory disease. New England Journal of Medicine 340:115-126.
100. Roth AF, Feng Y, Chen L, Davis NG. 2002. The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. Journal of Cell Biology 159:23-28.
101. Saisho Y, Morimoto A, Umeda T. 1997. Determination of farnesyl pyrophosphate in dog and human plasma by high-performance liquid chromatography with fluorescence detection. Annals in Biochemistry 252:89-95.
102. Sanchez JC, Rouge V, Pisteur M, Ravier F, Tonella L, Moosmayer M, Wilkins MR, Hochstrasser DF. 1997. Improved and simplified in-gel sample application using reswelling of dry immobilized pH gradients. Electrophoresis 18:324-327.
103. Sase K, Michel T. 1995. Expression of constitutive endothelial nitric oxide synthase in human blood platelets. Life Science 57:2049-2055.
104. Scandinavian Simvastatin Survival Study Group. 1994. Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Simvastatin Survival Study (4S). Lancet 344:1383-1389.
105. Schafer HF, Kattermann R. 1992. Fatty acid modulation of HcpG2 cell cholesterol biosynthesis and esterification. Clinical Biochemistry 25:325-330.
106. Schick PK, Walker J. 1996. The acylation of megakaryocyte, proteins: glycoprotein IX is primarily myristoylated while glycoprotein Ib is palmitoylated. Blood 87:1377-1384.
107. Schoenwaelder SM, Hughan SC, Boniface K, Fernando S, Holdsworth M, Thompson PE, Salem HH, Jackson SP. 2002. RhoA sustains integrin alpha IIbbeta 3 adhesion contacts under high shear. Journal of Biological Chemistry 277:14738-14746.
108. Seabra MC, Goldstein JL, Sudhof TC, Brown MS. 1992. Rab geranylgeranyl transferase: A multisubunit enzyme that prenylates GTP-binding proteins terminating in Cys-X-Cys or Cys-Cys. Journal of Biological Chemistry 267:14497-14503.
109. Shahinian S, Silvius JR. 1995. Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membranes. Biochemistry 34:3813-3822.
110. Shaul PW, Smart EJ, Robinson LJ, German Z, Yuhanna IS, Ying Y, Anderson RG, Michel T. 1996. Acylation targets emdothelial nitric-oxide synthase to plasmalemmal caveolae. Journal of Biological Chemistry 271:6518-6522.
111. 2+-induced alpha-granule secretion in platelets. Journal of Biological Chemistry 275:33844-33849.
112. Sigal CT, Zhou W, Buser CA, McLaughlin S, Resh MD. 1994. Amino-terminal basic residues of Src mediate membrane binding through electrostatic interaction with acidic phospholipids. Proceedings of the National Academy of Sciences USA 91:12253-12257.
113. Sinensky M. 2000. Recent advances in the study of prenylated proteins. Biochimica et Biophysica Acta 1484:93-106.
114. Smotrys JE, Linder ME. 2004. Palmitoylation of intracellular signaling proteins: regulation and function. Annual Reviews in Biochemistry 73:559-587.
115. Sobering AK, Watanabe R, Romeo MJ, Yan BC, Specht CA, Orlean P, Riezman H, Levin DE. 2004. Yeast Ras regulates the complex that catalyzes the first step in GPI-anchor biosynthesis at the ER. Cell 117:637-648.
116. Stark WW Jr, Blaskovich MA, Johnson BA, Qian Y, Vasudevan A, Pitt B, Hamilton AD, Sebti SM, Davies P. 1998. Inhibiting geranylgeranylation blocks growth and promotes apoptosis in pulmonary vascular smooth muscle cells. American Journal of Physiol 275:L55-L63.
117. Sternlicht MD, Werb Z. 2001. How matrix metalloproteinases regulate cell behavior. Annual Reviews in Cell Development and Biology 17:463-516.
118. Stevenson FT, Bursten SL, Locksley RM, Lovett DH. 1992. Myristyl acylation of the tumor necrosis factor alpha precursor on specific lysine residues. Journal of Experimental Medicine 176:1053-1062.
119. Strickland CL, Windsor WT, Syto R, Wang L, Bond R, Wu Z, Schwartz J, Le HV, Beese LS, Weber PC. 1998. Crystal structure of farnesyl protein transferase complexed with a CaaX peptide and famesyl. diphosphate analogue. Biochemistry 37:16601-16611.
120. Sukhova GK, Schonbeck U, Rabkin E, Schoen FJ, Poole AR, Billinghurst RC, Libby P. 1999. Evidence for increased collagenolysis by interstitial collagenases-1 and -3 in vulnerable human atheromatous plaques. Circulation 99:2503-2509.
121. Takahashi C, Sheng Z, Horan TP, Kitayama H, Maki M, Hitomi K, Kitaura Y, Takai S, Sasahara RM, Horimoto A, et al. 1998. Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK. Proceedings of the National Academy of Sciences USA 95:13221-13226.
122. Taniguchi H, Suzuki M, Manenti S, Titani K. 1994. A mass spectrometric study on the in vivo posttranslational modification of GAP-43. Journal of Biological Chemistry 269:22481-22484.
123. Terry RW, Kwee L, Levine JF, Labow MA. 1993. Cytokine induction of an alternatively spliced murine vascular cell adhesion molecule (VCAM) mRNA encoding a glycosylphosphatidylinositol-anchored VCAM protein. Proceedings of the National Academy of Sciences USA 90:5919-5923.
124. Traini M, Gooley AA, Ou K, Wilkins MR, Tonella L, Sanchez JC, Hochstrasser DF, Williams KL. 1998. Towards an automated approach for protein identification in proteome projects. Electrophoresis 19:1941-1949.
125. Uno F, Sasaki J, Nishizaki M, Carboni G, Xu K, Atkinson EN, Kondo M, Minna JD, Roth JA, Ji L. 2004. Myristoylation of the fus1 protein is required for tumor suppression in human lung cancer cells. Cancer Research 64:2969-2976.
126. Utsumi T, Takeshige T, Tanaka K, Takami K, Kira Y, Klostergaard J, Ishisaka R. 2001. Transmembrane TNF (pro-TNF) is palmitoylated. FEBS Letters 500:1-6.
127. Van Lent PL, Span PN, Sloetjes AW, Radstake TR, Van Lieshout AW, Heuvel JJ, Sweep CG, Van den Berg WB. 2005. Expression and localisation of the new metalloproteinase inhibitor RECK (reversion inducing cysteine-rich protein with Kazal motifs) in inflamed synovial membranes of patients with rheumatoid arthritis. Annals of Rheumatism Disease 64:368-374.
128. Vidugiriene J, Menon AK. 1994. The GPI anchor of cell-surface proteins is synthesized on the cytoplasmic face of the endoplasmic reticulum. Journal of Cell Biology 127:333-341.
129. Walther DJ, Peter JU, Winter S, Holtje M, Paulmann N, Grohmann M, Vowinckel J, Alamo-Bethencourt V, Wilhelm CS, Ahnert-Hilger G, Bader M. 2003. Serotonylation of small GTPases is a signal transduction pathway that triggers platelet alpha-granule release. Cell 115:851-862.
130. West of Scotland Coronary Prevention Group. 1996. West of Scotland Coronary identification of high-risk groups and comparison with other cardiovascular intervention trials. Lancet 348:1339-1342.
131. Wolven A, Okamura H, Rosenblatt Y, Resh M.D. 1997. Palmitoylation of p59fyn is reversible and sufficient for plasma membrane association. Molecular Biology of the Cell 8:1159-1173.
132. Work LM. McPhaden AR, Pyne NJ, Pyne S, Wadsworth RM, Wainwright OL. 2001. Short-term local delivery of an inhibitor of Ras farnesyltransferase prevents neointima formation in vivo after porcine coronary balloon angioplasty. Circulation 104:1538-1543.
133. Yokoyama K, Goodwin GW, Ghomashchi F, Glomset JA, Gelb MH. 1991. A protein geranylgeranyl-transferase from bovine brain: implications for protein prenylation specificity. Proceedings of the National Academy of Sciences USA 88:5302-5306.
134. Zhang S, Ren J, Khan MF, Cheng AM, Abendschein D, Muslin AJ. 2003. Grb2 is required for the development of neointima in response to vascular injury. Arteriosclerosis and Thrombosis Vascular Biology 23:1788-1793.
135. Zheng J, Knighton DR, Xuong NH, Taylor SS, Sowadski JM, Ten Eyck LF. 1993. Crystal structures of the myristylated catalytic subunit of cAMP-dependent protein kinase reveal open and closed conformations. Protein Science 2:1559-1573.
136. Zhou W, Parent LJ, Wills JW, Resh MD. 1994. Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids. Journal of Virology 68:2556-2569.
137. Zimmermann H. 1992, 5′-Nucleotidase: molecular structure and functional aspects. Biochemistry Journal 285:345-365.
138. Zimmermann H. 1996. Biochemistry, localization and functional roles of ecto-nucleotidases in the nervous system. Progress in Neurobiology 49:589-618.