Bilirubin has widespread inhibitory effects on protein phosphorylation

Pediatric Research

Volumn 39, Issue 6, 1996, Pages 1072-1077

  Hansen, Thor Willy Ruud ^a,b   Mathiesen, Siri B W ^a   Walaas, S Ivar ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BILIRUBIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; GLYCOGEN SYNTHASE; HISTONE H1; HISTONE H2A; MYOSIN; NERVE PROTEIN; PHOSPHOPROTEIN DARPP 32; PROTEIN KINASE; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE C; SYNAPSIN I; SYNTHETIC PEPTIDE;

ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME SUBSTRATE; INHIBITION KINETICS; NEUROTOXICITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 0029954653     PISSN: 00313998     EISSN: None     Source Type: Journal    
DOI: 10.1203/00006450-199606000-00023     Document Type: Article

References (60)

1. Orth J 1875 Ueber das Vorkommen von Bilirubinkrystallen bei neugeborenen Kindern. Virchows Arch Pathol Anat 63:447-462
2. Schmorl G 1904 Zur Kenntnis des Ikterus Neonatorum. Verh Dtsch Pathol Ges 6:109-115
3. Day RL 1954 Inhibition of brain respiration in vitro by bilirubin: Reversal of inhibition by various means. Am J Dis Child 504:506
4. Hansen TWR, Bratlid D 1986 Bilirubin and brain toxicity. Acta Paediatr Scand 75:513-522
5. Walaas SI, Greengard P 1991 Protein phosphorylation and neuronal function. Pharmacol Rev 43:299-349
6. Hansen TWR, Bratlid D, Walaas SI 1988 Bilirubin decreases phosphorylation of synapsin I, a synaptic vesicle-associated neuronal phosphoprotein, in intact synaptosomes from rat cerebral cortex. Pediatr Res 23:219-223
7. Greengard P, Valtorta F, Czemik AJ, Benfenati F 1993 Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259:780-785
8. Hansen TWR, Paulsen O, Gjerstad L, Bratlid D 1988 Short-term exposure to bilirubin reduces synaptic activation in rat transverse hippocampal slices. Pediatr Res 23:453-456
9. Constantopoulos A, Matsaniotis N 1976 Bilirubin inhibition of protein kinase: its prevention by cyclic AMP. Cytobios 17:17-20
10. Morphis L, Constantopoulos A, Matsaniotis N 1982 Bilirubin-induced modulation of cerebral protein phosphorylation in neonate rabbits in vivo. Science 218:156-158
11. Sano K, Nakamura H, Matsuo T 1985 Mode of inhibitory action of bilirubin on protein kinase C. Pediatr Res 19:587-590
12. Zetterström R, Ernster L 1956 Bilirubin, an uncoupler of oxidative phosphorylation in isolated mitochondria. Nature 178:1335-1337
13. Palmer CJ, Scott BT, Jones LR 1991 Purification and complete sequence determination of the major plasma membrane substrate for cAMP-dependent protein kinase and protein kinase C in myocardium. J Biol Chem 266:11126-11130
14. Hansen TWR, Walaas SI 1988 Concentration-dependent inhibitory effect of bilirubin (B) on phosphorylation of some proteins. Pediatr Res 24:264A(abstr)
15. Hansen TWR, Mathiesen SBW, Walaas SI 1994 Bilirubin inhibits cyclic AMP-dependent protein kinase (PKA) by a non-competitive mechanism. Pediatr Res 35:229A(abstr)
16. Woodgett J, Hunter T 1987 Isolation and characterization of two distinct forms of protein kinase C. J Biol Chem 262:4836-4843
17. Walaas SI, Nairn AC 1989 Multisite phosphorylation of microtubule-associated protein 2 (MAP-2) in rat brain: Peptide mapping distinguishes between cyclic AMP-, calcium/calmodulin- and calcium/phospholipid-regulated phosphorylation mechanisms. J Mol Neurosci 1:117-127
18. Laemmli UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
19. Walaas SI, Czernik AJ, Olstad OK, Sletten K, Walaas O 1994 Protein kinase C and cyclic AMP-dependent protein kinase phosphorylate phospholemman, an insulin and adrenaline-regulated membrane phosphoprotein, at specific sites in the carboxyterminal domain. Biochem J 304:635-640
20. Kemp BE, Benjamini E, Krebs EG 1976 Synthetic hexapeptide substrates and inhibitors of 3́:5́-cyclic AMP-dependent protein kinase. Proc Natl Acad Sci USA 73:1038-1042
21. Segel IH 1976 Biochemical Calculations, 2nd Ed., J Wiley & Sons New York, pp 234-236
22. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC 1985 Measurement of protein using bicinchoninic acid. Anal Biochem 150:76-85
23. Hanks SK, Quinn AM, Hunter T 1988 The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52
24. Amit Y, Bonch A 1993 Bilirubin inhibits protein kinase C and protein kinase C-mediated phosphorylation of endogenous substrates in human skin fibroblasts. Clin Chim Acta 223:103-111
25. Menken M, Waggoner JG, Berlin NI 1966 The influence of bilirubin on oxidative phosphorylation and related reactions in brain and liver mitochondria: effects of protein binding. J Neurochem 13:1241-1248
26. 31P nuclear magnetic resonance spectroscopy. Pediatr Res 23:569-573
27. Wennberg RP, Johanson BB, Folbergová J, Siesjö BK 1991 Bilirubin-induced changes in brain energy metabolism after osmotic opening of the blood-brain barrier. Pediatr Res 30:473-478
28. Kashiwamata S, Niwa F, Katoh R, Higashida H 1975 Malate dehydrogenase of bovine cerebrum: inhibition by bilirubin. J Neurochem 24:189-191
29. +-linked isocitrate dehydrogenase. Biochim Biophys Acta 327:233-237
30. +-activated p-nitrophenylphosphatase activities of NaI-treated microsomes from young rat cerebrum. J Biol Chem 254:4577-4588
31. McLoughlin DJ, Howell ML 1987 Bilirubin inhibition of enzymes involved in the mitochondrial malate-aspartate shuttle. Biochim Biophys Acta 893:7-12
32. Ahmad H, Singh SV, Awashti YC 1991 Inhibition of bovine lens glutathione S-transferases by hematin, bilirubin, and bromosulfophthalein. Lens Eye Toxic Res 8:431-440
33. Sjöberg P, Egestad B, Klasson-Wehler E, Gustafsson J 1991 Glucuronidation of mono(2-ethylhexyl)phthaleate. Some enzyme characteristics and inhibition by bilirubin. Biochem Pharmacol 41:1493-1496
34. Ivanetich KM, Thumser AE, Phillips SE, Sikakana CN 1990 Reversible inhibition of rat hepatic glutathione S-transferase 1:2 by bilirubin. Biochem Pharmacol 40:1563-1568
35. Ferreira GC, Dailey HA 1988 Mouse protoporphyrinogen oxidase: kinetic parameters and demonstration of inhibition by bilirubin. Biochem J 250:597-603
36. Katoh-Semba R 1976 Studies on cellular toxicity of bilirubin: effect on brain glycolysis in the young rat. Brain Res 113:339-348
37. Katoh-Semba R, Kashiwamata S 1980 Interaction of bilirubin with brain capillaries and its toxicity. Biochim Biophys Acta 632:290-297
38. Roger C, Koziel V, Vert P, Nehlig A 1993 Effects of bilirubin infusion on local cerebral glucose utilization in the immature rat. Brain Res Dev Brain Res 76:115-130
39. Mayor F Jr, Diez-Guerra J, Valdivieso F, Mayor F 1986 Effect of bilirubin on the membrane potential of rat brain synaptosomes. J Neurochem 47:363-369
40. Stumpf DA, Eguren LA, Parks JK 1985 Bilirubin increases mitochondrial inner membrane conductance. Biochem Med 34:226-229
41. Chantoux F, Chuniaud L, Dessante M, Trivin F, Blondeau JP, Francon J 1993 Competitive inhibition of thyroid hormone uptake into cultured rat brain astrocytes by bilirubin and bilirubin conjugates. Mol Cell Endocrinol 97:145-151
42. Ookhtens M, Lyon I, Fernandez-Checa J, Kaplowitz N 1988 Inhibition of glutathione efflux in the perfused rat liver and isolated hepatocytes by organic anions and bilirubin. Kinetics, sidedness, and molecular forms. J Clin Invest 82:608-616
43. Ochoa ELM, Wennberg RP, An Y, Tandon T, Takashima T, Nguyen T, Chui A 1993 Interactions of bilirubin with isolated presynaptic nerve terminals: functional effects on the uptake and release of neurotransmitters. Cell Mol Neurobiol 13:69-86
44. Gurba PE, Zand R 1974 Bilirubin binding to myelin basic protein, histones and its inhibition in vitro of cerebellar protein synthesis. Biochem Biophys Res Commun 58:1142-1147
45. 35S]methionine incorporation, and mitochondrial function. Pediatr Res 25:364-368
46. Majumdar AP 1974 Bilirubin encephalopathy: effect on RNA polymerase activity and chromatin template activity in the brain of the Gunn rat. Neurobiology 4:425-431
47. Yamada N, Sawasaki Y, Nakajima H 1977 Impairment of DNA synthesis in Gunn rat cerebellum. Brain Res 126:295-307
48. Vetvicka V, Miler I, Sima P, Taborsky L, Fornuser L 1985 The effect of bilirubin on the Fc receptor expression and phagocytic activity of mouse peritoneal macrophages. Folia Microbiol 30:373-380
49. Vetvicka V, Sima P, Miler I, Bilej M 1991 The immunosuppressive effects of bilirubin. Folia Microbiol 36:112-119
50. Meisel P, Jahr H 1991 Influence of albumin-bound bilirubin on the antibody-dependent cellular cytotoxicity of human cells in vitro. Biol Neonate 60:308-313
51. Claireaux AE, Cole PG, Lathe GH 1953 Icterus of the brain in the newborn. Lancet 2:1226-1230
52. Karplus M, Lee C, Cashore WJ, Oh W 1988 The effects of brain bilirubin deposition on auditory brain stem evoked responses in rats. Early Hum Dev 16:185-194
53. Hansen TWR, Cashore WJ, Oh W 1992 Changes in piglet auditory brainstem response amplitudes without increases in serum or cerebrospinal fluid neuron-specific enolase. Pediatr Res 32:524-529
54. Vasquez J, Ortega G, Valdivieso F, Mayor F Jr 1989 Interaction of bilirubin with gangliosides. J Biochem 106:139-142
55. Leonard M, Noy N, Zakim D 1989 The interactions of bilirubin with model and biological membranes. J Biol Chem 264:5648-5652
56. Amit Y, Poznansky MJ, Schiff D 1989 Bilirubin toxicity in a neuroblastoma cell line N-115. II. Delayed effects and recovery. Pediatr Res 25:369-372
57. Jacobsen C 1978 Lysine residue 240 of human serum albumin is involved in high-affinity binding of bilirubin. Biochem J 171:453-459
58. Lo Bello M, Pastore A, Petruzelli R, Parker MW, Wilce MCJ, Federici G, Ricci G 1993 Conformational states of human placental glutathione transferase as probed by limited proteolysis. Biochem Biophys Res Commun 194:804-810
59. Xia C, Meyer DJ, Chen H, Reinemer P, Huber R, Ketterer B 1993 Chemical modification of GSH transferase P 1-1 confirms the presence of Arg-13, Lys-44 and one carboxylate group in the GSH binding domain of the active site. Biochem J 293:357-362
60. Hinz HR, Kirley TL 1990 Lysine 480 is an essential residue in the putative ATP site of lamb kidney (Na,K)-ATPase. Identification of the pyridoxal 5′-diphospho-5′-adenosine and pyridoxal phosphate reactive residue. J Biol Chem 265:10260-10265