Type 4A cAMP-specific phosphodiesterase is stored in granules of human neutrophils and eosinophils

Cell and Tissue Research

Volumn 312, Issue 3, 2003, Pages 301-311

  Pryzwansky, Katherine B ^a   Madden, Victoria J ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

cAMP dependent protein kinase; fMLP; Human; Immunogold; Lactoferrin; Myeloperoxidase

Indexed keywords

CYCLIC AMP; PHOSPHODIESTERASE; PROTEIN KINASE;

ARTICLE; CELL FUNCTION; CELL LABELING; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ENZYME REGULATION; EOSINOPHIL; GENE TARGETING; GRANULOCYTE FUNCTION; HUMAN; HUMAN CELL; IMMUNOGOLD STAINING; MORPHOMETRICS; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

3',5'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASE; CYCLIC AMP; CYTOPLASMIC GRANULES; EOSINOPHILS; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, IMMUNOELECTRON; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEUTROPHILS; PEROXIDASE; PROTEIN ISOFORMS;

EID: 0037560262     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-003-0728-y     Document Type: Article

References (67)

1. Agwu DE, McCall CE, McPhail LC (1991) Regulation of phospholipase D-induced hydrolysis of choline-containing phosphoglycerides by cyclic AMP in human neutrophils. J Immunol 146:3895-3903
2. 2+-triggered membrane association with selectivity for interaction with phosphatidic acid. J Biol Chem 277:28298-22002
3. Bainton DF, Miller LJ, Kishimoto TK, Springer TA (1987) Leukocyte adhesion receptors are stored in peroxidase-negative granules of human neutrophils. J Exp Med 166:1641-1653
4. Beard MB, Huston E, Campbell L, Gall I, McPhee I, Yarwood S, Scotland G, Houslay MD (2002) In addition to the SH3 binding region, multiple regions within the N-terminal noncatalytic portion of the cAMP-specific phosphodiesterase, PDE4A5, contribute to its intracellular targeting. Cell Signal 14:453-465
5. Beil WJ, Weller PF, Tzizik DM, Galli SJ, Dvorak AM (1993) Ultrastructural immunogold localization of tumor necrosis factor-α to the matrix compartment of eosinophil secondary granules in patients with idiopathic hypereosinophilic syndrome. J Histochem Cytochem 41:1611
6. Bengis-Garber C, Gruener N (1996) Protein kinase A down-regulates the phosphorylation of p46 Phox in human neutrophils: a possible pathway for inhibition of the respiratory burst. Cell Signal 8:291-296
7. Borregaard N, Cowland JB (1997) Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89:3503-3521
8. Coffey RG (1992) Effects of cyclic nucleotides on granulocytes. In: Coffey RG (ed) Granulocyte responses to cytokines: basic and clinical research, vol. Marcel Dekker, New York, pp 301-338
9. Damiano VV, Kucich U, Murer E, Laudenslager N, Weinbaum G (1988) Ultrastructural quantitation of peroxidase- and elastase-containing granules in human neutrophils. Am J Pathol 131:235-245
10. Dent G, Giembycz MA, Rabe KF, Barnes PJ (1991) Inhibition of eosinophil cyclic nucleotide PDE activity and opsonized zymosan-stimulated respiratory burst by "type IV"-selective PDE inhibitors. Br J Pharmacol 103:1339-1346
11. Derian CK, Santulli RJ, Rao PE, Solomon HF, Barret JA (1995) Inhibition of chemotactic peptide-induced neutrophil adhesion to vascular endothelium by cAMP modulators. J Immunol 154:308-317
12. Dubucquoi S, Desreumaux P, Janin A, Klein O, Goldman M, Tavernier J, Capron A, Capron M (1994) Interleukin 5 synthesis by eosinophils: association with granules and immunoglobulin-dependent secretion. J Exp Med 179:703-708
13. Dubyak GR, Cowen DS, Lazarus HN (1990) Activation of the inositol phospholipid signaling system by receptors for extracellular ATP in human neutrophils, monocytes, and neutrophil/monocyte progenitor cells. Ann N Y Acad Sci 603:218-238
14. Dusenbery KE, Mendiola JR, Skubitz KM (1988) Evidence for ecto-protein kinase activity on the surface of human neutrophils. Biochem Biophys Res Comm 153:7-13
15. Egesten A, Breton-Gorius J, Guichard J, Gullberg U, Olsson I (1994) The heterogeneity of azurophil granules in neutrophil promyelocytes: immunogold localization of myeloperoxidase, cathepsin G, elastase, proteinase 3, and bactericidal/permeability increasing protein. Blood 83:2985-2994
16. Ehrlich YH, Hogan MV, Pawlowska Z, Naik U, Kornecki E (1990) Ectoprotein kinase in the regulation of cellular responsiveness to extracellular ATP. Ann N Y Acad Sci 603:401-416
17. Emes CH, Crawford N (1982) Ecto-protein kinase activity in rabbit peritoneal polymorphonuclear leukocytes. Biochim Biophys Acta 717:98-104
18. Goding JW (2000) Ecto-enzymes: physiology meets pathology. J Leukoc Biol 67:285-311
19. Gordon JL (1986) Extracellular ATP: effects, sources and fate. Biochem J 233:309-319
20. Grady PG, Thomas LL (1986) Characterization of cyclic-nucleotide phosphodiesterase activities in resting and N-formylmethionylleucylphenylalanine-stimulated human neutrophils. Biochim Biophys Acta 885:282-293
21. Harvath L, Robbins JD, Russell AA, Seamon KB (1991) cAMP and human neutrophil chemotaxis. J Immunol 146:224-232
22. Hatmi M, Gavaret JM, Elalamy I, Vargaftig BB, Jacquemin C (1996) Evidence for cAMP-dependent platelet ectoprotein kinase activity that phosphorylates platelet glycoprotein IV (CD36). J Biol Chem 271:24776-24780
23. Houslay MD, Scotland G, Erdogan S, Huston E, Mackenzie S, McCallum JF, McPhee I, Pooley L, Rena G, Ross A, Beard M, Peder A, Begg F, Wilkinson I, Yarwood S, Ackerman C, Houslay ES, Hoffman R, Engels P, Sullivan M, Bolger G (1997) Intracellular targeting, interaction with Src homology 3 (SH3) domains and rolipram-detected conformational switches in cAMP-specific PDE4A phosphodiesterase. Biochem Soc Trans 25:374-381
24. Iannone MA, Wolberg G, Zimmerman TP (1989) Chemotactic peptide induces cAMP elevation in human neutrophils by amplification of the adenylate cyclase response to endogenously produced adenosine. J Biol Chem 264:20177-20180
25. Kubler D, Pyerin W, Bill O, Hotz A, Sonka J, Kinzel V (1989) Evidence for ecto-protein kinase activity that phosphorylates kemptide in a cyclic AMP-dependent mode. J Biol Chem 264:14549-14555
26. Levi-Schaffer F, Lacy P, Severs NJ, Newman TM, North J, Gomperts B, Kay AB, Moqbel R (1995) Association of granulocyte-macrophage colony-stimulating factor with the crystalloid granules of human eosinophils. Blood 85:2579-2586
27. Madden VJ (1998) Microwave processing of cell monolayers in situ for post-embedding immunocytochemistry with retention of ultrastructure and antigenicity. Microsc Microanal 4:854-855
28. Manning CD, McLaughlin MM, Livi GP, Cieslinski LB, Torphy TJ, Barnette MS (1996) Prolonged beta adrenoreceptor stimulation up-regulates cAMP phosphodiesterase activity in human monocytes by increasing mRNA and protein for phosphodiesterases 4A and 4B. J Pharmacol Exp Ther 276:810-818
29. Michel JJ, Scott JD (2002) AKAP mediated signal transduction. Annu Rev Pharmacol Toxicol 42:235-257
30. Newsholme SJ, Schwartz L (1993) cAMP-specific phosphodiesterase inhibitor, rolipram, reduces eosinophil infiltration evoked by leukotrienes or by histamine in guinea pig conjunctiva. Inflammation 17:25-31
31. Nielson CP, Vestal RE, Sturm RJ, Heaslip R (1990) Effects of selective phosphodiesterase inhibitors on the polymorphonuclear leukocyte respiratory burst. J Allergy Clin Immunol 86:801-808
32. Nourshargh S, Hoult JRS (1986) Inhibition of human neutrophil degranulation by forskolin in the presence of phosphodiesterase inhibitors. Eur J Pharmacol 122:205-212
33. O'Connell JC, McCallum JF, McPhee I, Wakefield J, Houslay ES, Wishart W, Bolger G, Frame M, Houslay MD (1996) The SH3 domain of Src tyrosyl protein kinase interacts with the N-terminal splice region of the PDE4A cAMP-specific phosphodiesterase RPDE-6 (RNPDE4A5). Biochem J 318:255-262
34. Ottonello L, Morone MP, Dapino P, Dallegri F (1995a) Cyclic AMP-elevating agents down-regulate the oxidative burst induced by granulocyte-macrophage colony-stimulating factor (GM-CSF) in adherent neutrophils. Clin Exp Immunol 101:502-506
35. Ottonello L, Morone MP, Dapino P, Dallegri F (1995b) Tumour necrosis factor alpha-induced oxidative burst in neutrophils adherent to fibronectin: effects of cyclic AMP-elevating agents. Br J Haematol 91:566-570
36. Peachell PT, Undem BJ, Schleimer RP, R. W. MacGlashan J, Lichtenstein LM, Cieslinski LB, Torphy TJ (1992) Preliminary identification and role of phosphodiesterase isozymes in human basophils. J Immunol 148:2503-2510
37. Plaut M, Marone G, Thomas LL, Lichtenstein LM (1980) Cyclic nucleotides in immune responses and allergy. Adv Cyclic Nucleotide Res 12:161-171
38. Pryzwansky KB (1987) Human leukocytes as viewed by stereo high voltage electron microscopy. Blood Cells 12:505-530
39. Pryzwansky KB, Breton-Gorius J (1985) Identification of a subpopulation of primary granules in human neutrophils based upon maturation and distribution. Lab Invest 53:664-671
40. Pryzwansky KB, Merricks EP (1998) Chemotactic peptide-induced changes of intermediate filament organization in neutrophils during granule secretion: role of cyclic guanosine monophosphate. Mol Biol Cell 9:2933-2947
41. Pryzwansky KB, Steiner AL, Spitznagel JK, Kapoor CL (1981) Compartmentalization of cyclic AMP during phagocytosis by human neutrophilic granulocytes. Science 211:407-410
42. Pryzwansky KB, Wyatt TA, Reed W, Ross GD (1991) Phorbol ester induces transient focal concentrations of functional, newly expressed CR3 in neutrophils at sites of specific granule exocytosis. Eur J Cell Biol 54:61-75
43. Pryzwansky KB, Kidao S, Merricks EP (1998) Compartmentalization of PDE-4 and cAMP-dependent protein kinase in neutrophils and macrophages during phagocytosis. Cell Biochem Biophys 28:251-275
44. Pryzwansky K, Madden VJ, Jones SK (2001) Type 4A cAMP-specific phosphodiesterase (PDE-4A) is localized within granules of human granulocytes and is exocytosed during fMLP stimulation. FASEB J 15:A1172
45. Rice WG, J. M. Kinkade J, Parmley RT (1986) High resolution of heterogeneity among human neutrophil granules: physical, biochemical, and ultrastructural properties of isolated fractions. Blood 68:541-555
46. Rice WG, Ganz T, Kinkade JM, Selsted ME, Lehrer RI, Parmley RT (1987) Defensin-rich granules of human neutrophils. Blood 70:757-765
47. Santamaria LF, Palacios JM, Belta J (1997) Inhibition of eotaxin-mediated human eosinophil activation and migration by the selective cyclic nucleotide phosphodiesterase type 4 inhibitor rolipram. Br J Pharmacol 121:1150-1154
48. Scotland G, Houslay MD (1995) Chimeric constructs show that the unique N-terminal domain of the cyclic AMP phosphodiesterase RD1 (RNPDE4A1A; rPDE-IVA1) can confer membrane association upon the normally cytosolic protein chloramphenicol acetyltransferase. Biochem J 308:673-681
49. Shakur Y, Wilson M, Pooley L, Lobban M, Griffiths SL, Campbell AM, Beattie J, Daly C, Houslay MD (1995) Identification and characterization of the type IVA cyclic AMP-specific phosphodiesterase RD1 as a membrane-bound protein expressed in cerebellum. Biochem J 306:801-809
50. Simchowitz L, Fischbein LC, Spilberg I, Atkinson JP (1980) Induction of a transient elevation in intracellular levels of adenosine-3′-5′-cyclic monophosphate by chemotactic factors: an early event in human neutrophil activation. J Immunol 125:1482-1491
51. Skubitz KM, Goueli SA (1991) Basic fibroblast growth factor is a substrate for phosphorylation by human neutrophil ecto-protein kinase activity. Biochem Biophys Res Comm 174:49-55
52. Skubitz KM, Ehresmann DD, Ducker TP (1991) Characterization of human neutrophil ecto-protein kinase activity released by kinase substrates. J Immunol 147:638-650
53. Smith KJ, Scotland G, Beattie J, Trayer IP, Houslay MD (1996) Determination of the structure of the N-terminal splice region of the cyclic AMP-specific phosphodiesterase RD1 (RN-PDE4A1) by H NMR and identification of the membrane association domain using chimeric constructs. J Biol Chem 271:16703-16711
54. Smolen JE, Geosits SJ (1984) Human neutrophil phosphodiesterase. Inflammation 2:193-199
55. Smolen JE, Weissmann G (1981) Stimuli which provoke secretion of azurophil enzymes from human neutrophils induce increments in adenosine cyclic 3′-5′-monophosphate. Biochim Biophys Acta 672:197-206
56. Souness JE, Carter CM, Diocee BK, Hassall GA, Wood LJ, Turner NC (1991) Characterization of guinea-pig eosinophil phosphodiesterase activity. Biochem Pharmacol 42:937-945
57. Takenawa T, Ishitoya J, Nagai Y (1986) Inhibitory effect of prostaglandin E2, forskolin, and dibutyryl cAMP on arachidonic acid release and inositol phospholipid metabolism in guinea pig neutrophils. J Biol Chem 261:1092-1098
58. 2+ signals of RBL-2H3 cells and human basophils. J Immunol 159:964-969
59. Underwood DC, Osborn RR, Novak LB, Matthews JK, Newsholme SJ, Undem BJ, Hand JM, Torphy TJ (1993) Inhibition of antigen-induced bronchoconstriction and eosinophil infiltration in the guinea pig by the cyclic AMP-specific phosphodiesterase inhibitor, rolipram. J Pharmacol Exp Ther 266:306-313
60. 2+-dependent mechanism which is independent of transmembrane activation of adenylate cyclase. J Biol Chem 260:6769-6775
61. Verghese MW, McConnell RT, Lenhard JM, Hamacher L, Jin S-LC (1995a) Regulation of distinct cyclic AMP-specific phosphodiesterase (phosphodiesterase type 4) isozymes in human monocytic cells. Mol Pharmacol 47:1164-1171
62. Verghese MW, McConnell RT, Strickland AB, Gooding RC, Stimpson SA, Yarnall DP, Taylor JD, Furdon PJ (1995b) Differential regulation of human monocyte-derived TNFα and IL-1β by Type IV cAMP-phosphodiesterase (cAMP-PDE) inhibitors. J Pharmacol Exp Ther 272:1313-1320
63. Wang P, Wu P, Ohleth KM, Egan RW, Billah MM (1999) Phosphodiesterase 4B2 is the predominant phosphodiesterase species and undergoes differential regulation of gene expression in human monocytes and neutrophils. Mol Pharmacol 56:170-174
64. Ward PA, Walker BAM, Hagenlocker BE (1990) Functional consequences of interactions between human neutrophils and ATP, ATPγS, and adenosine. Ann N Y Acad Sci 603:108-119
65. Wright CD, Kuipers PJ, Kobylarz-Singer D, Devall LJ, Klinkefus BA, Weishaar RE (1990) Differential inhibition of human neutrophil functions. Biochem Pharmacol 40:699-707
66. Wyatt TA, Lincoln TM, Pryzwansky KB (1993) Regulation of human neutrophil degranulation by LY83583 and L-arginine: role of cGMP-dependent protein kinase. Am J Physiol Cell Physiol 34:C201-C211
67. Ydrenius L, Majeed M, Rasmusson BJ, Stendahl O, Sarndahl E (2000) Activation of cAMP-dependent protein kinase is necessary for actin rearrangements in human neutrophils during phagocytosis. J Leukoc Biol 67:520-528