Electrospray ionization mass spectrometric analyses of phospholipids from INS-1 insulinoma cells: Comparison to pancreatic islets and effects of fatty acid supplementation on phospholipid composition and insulin secretion

Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids

Volumn 1484, Issue 2-3, 2000, Pages 251-266

  Ramanadham, Sasanka ^a   Hsu, Fong Fu ^a   Zhang, Sheng ^a   Bohrer, Alan ^a   Ma, Zhongmin ^a   Turk, John ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Arachidonic acid; Insulin secretagogue; Plasmenylethanolamine

Indexed keywords

ARACHIDONIC ACID; FATTY ACID; GLYCEROPHOSPHOETHANOLAMINE; GLYCEROPHOSPHORYLCHOLINE; INSULIN; LINOLEIC ACID; OLEIC ACID; PALMITIC ACID; PHOSPHOLIPID; POLYUNSATURATED FATTY ACID;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DIABETES MELLITUS; EXOCYTOSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INSULIN RELEASE; INSULINOMA; IONIZATION; LIPID COMPOSITION; MALE; MASS SPECTROMETRY; MEMBRANE FUSION; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT;

ANIMALS; FATTY ACIDS; INSULIN; INSULINOMA; ISLETS OF LANGERHANS; MASS SPECTROMETRY; PANCREATIC NEOPLASMS; PHOSPHOLIPIDS; RATS; TUMOR CELLS, CULTURED;

EID: 0034630397     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1388-1981(00)00022-6     Document Type: Article

References (73)

1. Porte D. Banting lecture 1990. Beta-cells in type II diabetes mellitus. Diabetes. 40:1991;166-180.
2. Meglasson M.D., Matschinsky F.M. Pancreatic islet glucose metabolism and regulation of insulin secretion. Diabetes/Metabol. Rev. 2:1986;163-214.
3. Matschinsky F.M. Glucokinase as glucose sensor and metabolic signal generator in pancreatic beta-cells and hepatocytes. Diabetes. 39:1990;647-652.
4. + channels in pancreatic B-cells. Nature. 311:1984;271-273.
5. 2+ concentration in pancreatic beta-cells. J. Biol. Chem. 262:1987;5448-5454.
6. Gylfe E. Glucose-induced early changes in cytoplasmic calcium of pancreatic beta-cells studied with time-sharing dual-wavelength fluorometry. J. Biol. Chem. 263:1988;5044-5048.
7. Misler S., Barnett D.W., Gillis K.D., Pressel D.M. Electrophysiology of stimulus-secretion coupling in human beta-cells. Diabetes. 41:1992;1221-1228.
8. 2+ entry. Diabetes. 41:1992;662-670.
9. 2+ mobilization by arachidonic acid. Comparison with myo-inositol 1,4,5-trisphosphate in isolated pancreatic islets. J. Biol. Chem. 261:1986;3501-3511.
10. Wolf B.A., Pasqualea S.M., Turk J. Free fatty acid accumulation in secretagogue-stimulated pancreatic islets and effects of arachidonic acid on depolarization-induced insulin secretion. Biochemistry. 30:1991;6371-6379.
11. Metz S.A. The pancreatic islet as Rubik's Cube. Is phospholipid hydrolysis a piece of the puzzle? Diabetes. 40:1991;1565-1573.
12. Turk J., Gross R.W., Ramanadham S. Amplification of insulin secretion by lipid messengers. Diabetes. 42:1993;367-374.
13. Ramanadham S., Gross R.W., Turk J. Arachidonic acid induces an increase in the cytosolic calcium concentration in single pancreatic islet beta cells. Biochem. Biophys. Res. Commun. 184:1992;647-653.
14. Metz S.A., Draznin B., Sussman K.E., Leitner J.W. Unmasking of arachidonic acid-induced insulin release by removal of extracellular calcium. Arachidonic acid mobilizes cellular calcium in rat islets of Langerhans. Biochem. Biophys. Res. Commun. 142:1987;251-258.
15. Konrad R.J., Jolly Y.C., Major C., Wolf B.A. Inhibition of phospholipase A2 and insulin secretion in pancreatic islets. Biochim. Biophys. Acta. 1135:1992;215-220.
16. Ramanadham S., Gross R.W., Han X., Turk J. Inhibition of arachidonic acid release by secretagogue-stimulated pancreatic islets suppresses both insulin secretion and the rise in beta-cell cytosolic calcium ion concentration. Biochemistry. 32:1993;337-346.
17. Loweth A.C., Scarpello J.H.B., Morgan N.G. A specific inhibitor of cytosolic phospholipase A2 activity, AACOCF3, inhibits glucose-induced insulin secretion from isolated rat islets. Biochem. Biophys. Res. Commun. 218:1996;423-427.
18. + permeability without diminution by exogenous arachidonic acid. Biochem. Pharmacol. 53:1997;1077-1086.
19. Turk J., Mueller M., Bohrer A., Ramanadham S. Arachidonic acid metabolism in isolated pancreatic islets. VI. Carbohydrate insulin secretagogues must be metabolized to induce eicosanoid release. Biochim. Biophys. Acta. 1125:1992;280-291.
20. Ramanadham S., Hsu F.-F., Bohrer A., Ma Z., Turk J. Studies of the role of group VI Phospholipase A2 in fatty acid incorporation, phospholipid remodeling, lysophosphatidylcholine generation, and secretagogue-induced arachidonic acid release in pancreatic islets and insulinoma cells. J. Biol. Chem. 274:1999;13915-13927.
21. Hazen S.L., Zupan L.A., Weiss R.H., Getman D.P., Gross R.W. Suicide inhibition of canine myocardial cytosolic calcium-independent phospholipase A2. Mechanism-based discrimination between calcium-dependent and -independent phospholipases A2. J. Biol. Chem. 266:1991;7227-7232.
22. Zupan L.A., Weiss R.H., Hazen S.L., Parnas B.L., Aston K.W., Lennon P.J., Getman D.P., Gross R.W. Structural determinants of haloenol lactone-mediated suicide inhibition of canine myocardial calcium-independent phospholipase A2. J. Med. Chem. 36:1993;95-100.
23. Tang J., Kriz R.W., Wolfman N., Shaffer M., Seehra S., Jones S.A. A novel cytosolic calcium-independent phospholipase A2 contains eight ankyrin motifs. J. Biol. Chem. 272:1997;8567-8575.
24. 2+-independent phospholipase A2 enzymes from P388D1 macrophages and Chinese hamster ovary cells. J. Biol. Chem. 272:1997;8576-8590.
25. 2+-independent phospholipase A2 enzyme that contains a repeated structural motif homologous to the integral membrane protein binding domain of ankyrin. J. Biol. Chem. 272:1997;11118-11127.
26. Ma Z., Wang X., Nowatzke W., Ramanadham S., Turk J. Human pancreatic islets express mRNA species encoding two distinct catalytically active isoforms of group VI phospholipase A2 (iPLA2) that arise from an exon-skipping mechanism of alternative splicing of the transcript from the iPLA2 gene on chromosome 22q13.1. J. Biol. Chem. 274:1999;9607-9616.
27. Ramanadham S., Bohrer A., Mueller M., Jett P., Gross R.W., Turk J. Mass spectrometric identification and quantitation of arachidonic acid-containing phospholipids in pancreatic islets prominence of plasmenylethanolamine molecular species. Biochemistry. 32:1993;5339-5351.
28. Ramanadham S., Bohrer A., Gross R.W., Turk J. Mass spectrometric characterization of arachidonic acid-containing plasmalogens in human pancreatic islets and in rat islet beta-cells and subcellular membranes. Biochemistry. 32:1993;13499-13509.
29. Murphy R.C., Harrison K.A. Fast atom bombardment mass spectrometry of phospholipids. Mass Spectrom. Rev. 13:1994;57-76.
30. Han X., Gross R.W. Electrospray ionization mass spectroscopic analysis of human erythrocyte plasma membrane phospholipids. Proc. Natl. Acad. Sci. USA. 91:1994;10635-10639.
31. Han X., Gross R.W. Structural determination of picomole amounts of phospholipids via electrospray ionization tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 6:1995;1202-1210.
32. Han X., Gross R.W. Structural determination of lysophospholipid regioisomers by electrospray ionization tandem mass spectrometry. J. Am. Chem. Soc. 118:1996;451-457.
33. Han X., Gubitosi-Klug R.A., Collins B.J., Gross R.W. Alterations in individual molecular species of human platelet phospholipids during thrombin: stimulation electrospray ionization mass spectrometry-facilitated identification of the boundary conditions for the magnitude and selectivity of thrombin-induced platelet phospholipid hydrolysis. Biochemistry. 35:1996;5822-5832.
34. Ramanadham S., Hsu F.-F., Bohrer A., Nowatzke W., Ma Z., Turk J. Electrospray ionization mass spectrometric analyses of phospholipids from rat and human pancreatic islets and subcellular membranes: comparison to other tissues and implications for membrane fusion in insulin exocytosis. Biochemistry. 37:1998;4553-4567.
35. Glaser P.E., Gross R.W. Plasmenylethanolamine facilitates rapid membrane fusion: a stopped-flow kinetic investigation correlating the propensity of a major plasma membrane constituent to adopt an HII phase with its ability to promote membrane fusion. Biochemistry. 33:1994;5805-5812.
36. Glaser P.E., Gross R.W. Rapid plasmenylethanolamine-selective fusion of membrane bilayers catalyzed by an isoform of glyceraldehyde-3-phosphate dehydrogenase Discrimination between glycolytic and fusogenic roles of individual isoforms. Biochemistry. 34:1995;12193-12203.
37. Han X., Gross R.W. Plasmenylethanolamine facilitates rapid membrane fusion: a stopped-flow kinetic investigation correlating the propensity of a major plasma membrane constituent to adopt an HII phase with its ability to promote membrane fusion. Biophys. J. 63:1992;309-316.
38. P.R. Cullis, M.J. Hope, in: Biochemistry of Lipids, Lipoproteins, and Membranes, Elsevier, Amsterdam, 1991.
39. Asfari M., Janjic D., Meda P., Li G., Halban P.A., Wollheim C.B. Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology. 130:1992;167-178.
40. Noel R.J., Antonozzi P.A., McGarry J.D., Newgard C.B. Engineering of glycerol-stimulated insulin secretion in islet beta cells. Differential metabolic fates of glucose and glycerol provide insight into mechanisms of stimulus-secretion coupling. J. Biol. Chem. 272:1997;18621-18627.
41. Trinh K., Minassian C., Langerr A.J., O'Doherty R.M., Newgard C.B. Adenovirus-mediated expression of the catalytic subunit of glucose-6-phosphatase in INS-1 cells. Effects on glucose cycling, glucose usage, and insulin secretion. J. Biol. Chem. 272:1997;24837-24842.
42. McDaniel M.L., Colca J.R., Kotagal N., Lacy P.E. A subcellular fractionation approach for studying insulin release mechanisms and calcium metabolism in islets of Langerhans. Methods Enzymol. 98:1983;182-200.
43. Ricordi C., Lacy P.E., Finke E.H., Olack B.J., Scharp D.W. Automated method for isolation of human pancreatic islets. Diabetes. 37:1988;413-420.
44. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:1959;911-917.
45. Patton G.M., Fasulo J.M., Robins S.J. Separation of phospholipids and individual molecular species of phospholipids by high-performance liquid chromatography. J. Lipid Res. 23:1982;190-196.
46. Kayganich K.A., Murphy R.C. Fast atom bombardment tandem mass spectrometric identification of diacyl, alkylacyl, and alk-1-enylacyl molecular species of glycerophosphoethanolamine in human polymorphonuclear leukocytes. Anal. Chem. 64:1994;2965-2971.
47. Ramanadham S., Wolf M., Jett P.A., Gross R.W., Turk J. Characterization of an ATP-stimulatable Ca(2+)-independent phospholipase A2 from clonal insulin-secreting HIT cells and rat pancreatic islets a possible molecular component of the beta-cell fuel sensor. Biochemistry. 33:1994;7442-7452.
48. Gross R.W., Ramanadham S., Kruszka K., Han X., Turk J. Rat and human pancreatic islet cells contain a calcium ion independent phospholipase A2 activity selective for hydrolysis of arachidonate which is stimulated by adenosine triphosphate and is specifically localized to islet beta-cells. Biochemistry. 32:1993;327-336.
49. Hsu F.-F., Bohrer A., Turk J. Formation of lithiated adducts of glycerophosphocholine lipids facilitates their identification by electrospray ionization tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 9:1998;516-526.
50. 2+ concentration. Endocrinology. 139:1998;4073-4085.
51. Kuwae T., Schmid P.C., Schmid H.H.O. Assessment of phospholipid deacylation-reacylation cycles by a stable isotope technique. Biochem. Biophys. Res. Commun. 142:1987;86-91.
52. Kuwae T., Schmid P.C., Johnson S.B., Schmid H.H.O. Differential turnover of phospholipid acyl groups in mouse peritoneal macrophages. J. Biol. Chem. 265:1990;5002-5007.
53. Schmid P.C., Johnson S.B., Schmid H.H.O. Remodeling of rat hepatocyte phospholipids by selective acyl turnover. J. Biol. Chem. 266:1991;13690-13697.
54. Schmid P.C., Deli E., Schmid H.H.O. Generation and remodeling of phospholipid molecular species in rat hepatocytes. Arch. Biochem. Biophys. 319:1995;168-176.
55. Kuwae T., Schmid P.C., Schmid H.H.O. Alterations of fatty acyl turnover in macrophage lycerolipids induced by stimulation. Evidence for enhanced recycling of arachidonic acid. Biochim. Biophys. Acta. 1344:1997;74-86.
56. Ramanadham S., Wolf M.J., Li B., Bohrer A., Turk J. Glucose-responsitivity and expression of an ATP-stimulatable Ca-independent phospholipase A2 enzyme in clonal insulinoma cell lines. Biochim. Biophys. Acta. 1344:1997;153-164.
57. Michaelson L., Lazarus C.M., Griffiths G., Napier J.A., Stobart A.K. Isolation of a 5-fatty acid desaturase gene from Mortierella alpina. J. Biol. Chem. 273:1998;19055-19059.
58. Cho H.P., Nakamura M.T., Clarke S.D. Cloning, expression, and nutritional regulation of the mammalian-6 desaturase. J. Biol. Chem. 274:1999;471-477.
59. H.W. Cook, in: D.E. Vance, J. Vance (Eds.), Biochemistry of Lipids, Lipoproteins, and Membranes, Elsevier, New York, 1996, pp. 129-152.
60. Atouf F., Czernichow P., Scharfman R. Expression of neuronal traits in pancreatic beta cells, implication of neuron-restrictive silencing factor/repressor element silencing transcription factor, a neuron-restrictive silencer. J. Biol. Chem. 272:1997;1929-1934.
61. Karlsson O., Thor S., Norbert T., Ohlsson H., Edlund T. Insulin gene enhancer binding protein Isl-1 is a member of a novel class of proteins containing both a homeo- and a Cys-His domain. Nature. 344:1990;879-882.
62. Turque N., Plaza S., Radvanyi F., Carriere C., Saule S. Pax-QNR/Pax-6, a paired box- and homeobox-containing gene expressed in neurons, is also expressed in pancreatic endocrine cells. Mol. Endocrinol. 8:1994;928-929.
63. Naya F.J., Stellrecht C.M.M., Tsai M.-J. Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev. 9:1995;1009-1019.
64. Hsu F.F., Bohrer A., Turk J. Electrospray ionization tandem mass spectrometric analysis of sulfatide. Determination of fragmentation patterns and characterization of molecular species expressed in brain and in pancreatic islets. Biochim. Biophys. Acta. 1392:1998;202-216.
65. Ntambi J.M. The regulation of stearoyl-CoA desaturase (SCD). Prog. Lipid Res. 34:1995;139-150.
66. Shimabukuro M., Ohneda M., Lee Y., Unger R.H. Role of nitric oxide in obesity-induced beta-cell disease. J. Clin. Invest. 100:1997;290-295.
67. Shimabukuro M., Koyami K., Lee Y., Unger R.H. Leptin- or Troglitazone-induced lipopenia protects islets from interleukin 1 cytotoxicity. J. Clin. Invest. 100:1997;1750-1754.
68. Milburn J.L., Hirose H., Lee Y.H., Nagasawa Y., Ogawa A., Ohneda M., BeltrandelRio H., Newgard C.B., Johnson J.H., Unger R.H. Pancreatic beta-cells in obesity. Evidence for induction of functional, morphologic, and metabolic abnormalities by increase long chain fatty acids. J. Biol. Chem. 270:1995;1295-1299.
69. Hirose H., Lee Y.H., Inamn L.R., Nagasawa Y., Johnson J.H., Unger R.H. Defective fatty acid-mediated beta-cell compensation in Zucker diabetic fatty rats. Pathogenic implications for obesity-dependent diabetes. J. Biol. Chem. 271:1996;5633-5637.
70. Shimabukuro M., Zhou Y.-T., Levi M., Unger R.H. Fatty acid-induced beta cell apoptosis: a link between obesity and diabetes. Proc. Natl. Acad. Sci. USA. 95:1998;2498-2502.
71. Shimabukuro M., Higa M., Zhou Y.T., Wang M.Y., Newgard C.B., Unger R.H. Lipoapoptosis in beta-cells of obese prediabetic fa/fa rats. Role of serine palmitoyltransferase overexpression. J. Biol. Chem. 273:1998;32487-32490.
72. Zhou Y.-T., Shimabukuro M., Lee Y., Koyama K., Higa M., Ferguson T., Unger R.H. Enhanced de novo lipogenesis in the leptin-unresponsive pancreatic islets of prediabetic Zucker diabetic fatty rats role in the pathogenesis of lipotoxic diabetes. Diabetes. 47:1998;1904-1908.
73. Shimabukuro M., Zhou Y.-T., Lee Y., Unger R.H. Troglitazone lowers islet fat and restores beta cell function of Zucker diabetic fatty rats. J. Biol. Chem. 273:1998;3547-3550.