Polyamines are present in mast cell secretory granules and are important for granule homeostasis

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  García Faroldi, Gianni ^a   Rodríguez, Carlos E ^a   Urdiales, JoséL ^a   Pérez Pomares, JoséM ^a   Dávila, JoséC ^a   Pejler, Gunnar ^b   Sánchez Jiménez, Francisca ^a   Fajardo, Ignacio ^a  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; HISTAMINE; POLYAMINE DERIVATIVE; SEROTONIN; SPERMIDINE; SPERMINE; CALCIMYCIN; CARRIER PROTEIN; IONOPHORE; POLYAMINE; TIP47 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BIOGENESIS; CELL DAMAGE; CELL ISOLATION; CELL METABOLISM; CELL ULTRASTRUCTURE; CONTROLLED STUDY; ENDOSOME; EXOCYTOSIS; FEMALE; FUNCTIONAL PROTEOMICS; MAST CELL; NONHUMAN; PROTEIN EXPRESSION; SECRETORY GRANULE; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DEGRANULATION; DRUG EFFECT; GENETICS; HOMEOSTASIS; METABOLISM; METHODOLOGY; MOUSE; PHYSIOLOGY; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETORY VESICLE; TRANSMISSION ELECTRON MICROSCOPY; TWO DIMENSIONAL GEL ELECTROPHORESIS; ULTRASTRUCTURE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BONE MARROW CELLS; CALCIMYCIN; CARRIER PROTEINS; CELL DEGRANULATION; CELLS, CULTURED; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; HOMEOSTASIS; IONOPHORES; MAST CELLS; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; POLYAMINES; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SECRETORY VESICLES; SPERMIDINE;

EID: 78649798116     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015071     Document Type: Article

References (60)

1. Galli SJ, Nakae S, Tsai M (2005) Mast cells in the development of adaptive immune responses. Nat Immunol 6: 135-142.
2. Yu M, Tsai M, Tam SY, Jones C, Zehnder J, et al. (2006) Mast cells can promote the development of multiple features of chronic asthma in mice. J Clin Invest 116: 1633-1641.
3. Sun J, Sukhova GK, Wolters PJ, Yang M, Kitamoto S, et al. (2007) Mast cells promote atherosclerosis by releasing proinflammatory cytokines. Nat Med 13: 719-724.
4. Lee DM, Friend DS, Gurish MF, Benoist C, Mathis D, et al. (2002) Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science 297: 1689-1692.
5. Secor VH, Secor WE, Gutekunst CA, Brown MA (2000) Mast cells are essential for early onset and severe disease in a murine model of multiple sclerosis. J Exp Med 191: 813-822.
6. Coussens LM, Raymond WW, Bergers G, Laig-Webster M, Behrendtsen O, et al. (1999) Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev 13: 1382-1397.
7. Soucek L, Lawlor ER, Soto D, Shchors K, Swigart LB, et al. (2007) Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors. Nat Med 13: 1211-1218.
8. Metcalfe DD, Baram D, Mekori YA (1997) Mast cells. Physiol Rev 77: 1033-1079.
9. Galli SJ, Kalesnikoff J, Grimbaldeston MA, Piliponsky AM, Williams CM, et al. (2005) Mast cells as "tunable" effector and immunoregulatory cells: recent advances. Annu Rev Immunol 23: 749-786.
10. Stevens RL, Austen KF (1989) Recent advances in the cellular and molecular biology of mast cells. Immunol Today 10: 381-386.
11. Abrink M, Grujic M, Pejler G (2004) Serglycin is essential for maturation of mast cell secretory granule. J Biol Chem 279: 40897-40905.
12. Braga T, Grujic M, Lukinius A, Hellman L, Abrink M, et al. (2007) Serglycin proteoglycan is required for secretory granule integrity in mucosal mast cells. Biochem J 403: 49-57.
13. Henningsson F, Hergeth S, Cortelius R, Abrink M, Pejler G (2006) A role for serglycin proteoglycan in granular retention and processing of mast cell secretory granule components. FEBS J 273: 4901-4912.
14. Ringvall M, Ronnberg E, Wernersson S, Duelli A, Henningsson F, et al. (2008) Serotonin and histamine storage in mast cell secretory granules is dependent on serglycin proteoglycan. J Allergy Clin Immunol 121: 1020-1026.
15. Pejler G, Abrink M, Wernersson S (2009) Serglycin proteoglycan: regulating the storage and activities of hematopoietic proteases. Biofactors 35: 61-68.
16. Forsberg E, Pejler G, Ringvall M, Lunderius C, Tomasini-Johansson B, et al. (1999) Abnormal mast cells in mice deficient in a heparin-synthesizing enzyme. Nature 400: 773-776.
17. Cohen SS (1998) A guide to the polyamines. New York: Oxford University Press. 624 p.
18. Medina MA, Urdiales JL, Rodriguez-Caso C, Ramirez FJ, Sanchez-Jimenez F (2003) Biogenic amines and polyamines: similar biochemistry for different physiological missions and biomedical applications. Crit Rev Biochem Mol Biol 38: 23-59.
19. Childs AC, Mehta DJ, Gerner EW (2003) Polyamine-dependent gene expression. Cell Mol Life Sci 60: 1394-1406.
20. Ruiz-Chica J, Medina MA, Sanchez-Jimenez F, Ramirez FJ (2001) Raman study of the interaction between polyamines and a GC oligonucleotide. Biochem Biophys Res Commun 285: 437-446.
21. Belting M, Havsmark B, Jonsson M, Persson S, Fransson LA (1996) Heparan sulphate/heparin glycosaminoglycans with strong affinity for the growthpromoter spermine have high antiproliferative activity. Glycobiology 6: 121-129.
22. Belting M, Borsig L, Fuster MM, Brown JR, Persson L, et al. (2002) Tumor attenuation by combined heparan sulfate and polyamine depletion. Proc Natl Acad Sci U S A 99: 371-376.
23. Belting M, Mani K, Jonsson M, Cheng F, Sandgren S, et al. (2003) Glypican-1 is a vehicle for polyamine uptake in mammalian cells: a pivital role for nitrosothiolderived nitric oxide. J Biol Chem 278: 47181-47189.
24. Henningsson F, Ledin J, Lunderius C, Wilen M, Hellman L, et al. (2002) Altered storage of proteases in mast cells from mice lacking heparin: a possible role for heparin in carboxypeptidase A processing. Biol Chem 383: 793-801.
25. Tchougounova E, Pejler G, Abrink M (2003) The chymase, mouse mast cell protease 4, constitutes the major chymotrypsin-like activity in peritoneum and ear tissue. A role for mouse mast cell protease 4 in thrombin regulation and fibronectin turnover. J Exp Med 198: 423-431.
26. Kruger PG, Lagunoff D, Wan H (1980) Isolation of rat mast cell granules with intact membranes. Exp Cell Res 129: 83-93.
27. Riederer MA, Soldati T, Shapiro AD, Lin J, Pfeffer SR (1994) Lysosome biogenesis requires Rab9 function and receptor recycling from endosomes to the trans-Golgi network. J Cell Biol 125: 573-582.
28. Garcia-Faroldi G, Correa-Fiz F, Abrighach H, Berdasco M, Fraga MF, et al. (2009) Polyamines affect histamine synthesis during early stages of IL-3-induced bone marrow cell differentiation. J Cell Biochem 108: 261-271.
29. Fajardo I, Urdiales JL, Medina MA, Sanchez-Jimenez F (2001) Effects of phorbol ester and dexamethasone treatment on histidine decarboxylase and ornithine decarboxylase in basophilic cells. Biochem Pharmacol 61: 1101-1106.
30. Liu W, Saint DA (2002) A new quantitative method of real time reverse transcription polymerase chain reaction assay based on simulation of polymerase chain reaction kinetics. Anal Biochem 302: 52-59.
31. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, et al. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45.
32. Spandidos A, Wang X, Wang H, Seed B (2010) PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 38: D792-799.
33. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
34. Gross B, Borggrefe T, Wabl M, Sivalenka RR, Bennett M, et al. (2002) SWAP- 70-deficient mast cells are impaired in development and IgE-mediated degranulation. Eur J Immunol 32: 1121-1128.
35. De Young MB, Nemeth EF, Scarpa A (1987) Measurement of the internal pH of mast cell granules using microvolumetric fluorescence and isotopic techniques. Arch Biochem Biophys 254: 222-233.
36. Kurosawa M, Okayama Y, Kobayashi S (1989) A diphosphoinositide kinase in rat mast cell granules. J Allergy Clin Immunol 84: 118-128.
37. Amende LM, Donlon MA (1985) Isolation of cellular membranes from rat mast cells. Biochim Biophys Acta 812: 713-720.
38. Metcalf BW, Bey P, Danzin C, Jung MJ, Casara P, et al. (1978) Catalytic Irreversible Inhibition of Mammalian Ornithine Decarboxylase (E.C.4.1.1.17) by Substrate and Product Analogs. J Am Chem Soc 100: 2551-2553.
39. Seiler N, Dezeure F (1990) Polyamine transport in mammalian cells. Int J Biochem 22: 211-218.
40. Blott EJ, Griffiths GM (2002) Secretory lysosomes. Nat Rev Mol Cell Biol 3: 122-131.
41. Sagi-Eisenberg R (2007) The mast cell: where endocytosis and regulated exocytosis meet. Immunol Rev 217: 292-303.
42. Humphries DE, Wong GW, Friend DS, Gurish MF, Qiu WT, et al. (1999) Heparin is essential for the storage of specific granule proteases in mast cells. Nature 400: 769-772.
43. Braga T, Ringvall M, Tveit H, Abrink M, Pejler G (2009) Reduction with dithiothreitol causes serglycin-specific defects in secretory granule integrity of bone marrow derived mast cells. Mol Immunol 46: 422-428.
44. Puri N, Roche PA (2008) Mast cells possess distinct secretory granule subsets whose exocytosis is regulated by different SNARE isoforms. Proc Natl Acad Sci U S A 105: 2580-2585.
45. Kanerva K, Lappalainen J, Makitie LT, Virolainen S, Kovanen PT, et al. (2009) Expression of antizyme inhibitor 2 in mast cells and role of polyamines as selective regulators of serotonin secretion. PLoS One 4: e6858.
46. Brand K (1987) Role of ornithine decarboxylase on glycolytic enzyme induction during thymocyte proliferation. J Biol Chem 262: 15232-15235.
47. Ryu H, Walker JK, Kim S, Koo N, Barak LS, et al. (2008) Regulation of M2-type pyruvate kinase mediated by the high-affinity IgE receptors is required for mast cell degranulation. Br J Pharmacol 154: 1035-1046.
48. Kim JY, Kim DY, Ro JY (2008) Granule formation in NGF-cultured mast cells is associated with expressions of pyruvate kinase type M2 and annexin I proteins. Int Arch Allergy Immunol 146: 287-297.
49. Bretscher A, Chambers D, Nguyen R, Reczek D (2000) ERM-Merlin and EBP50 protein families in plasma membrane organization and function. Annu Rev Cell Dev Biol 16: 113-143.
50. Cao TT, Deacon HW, Reczek D, Bretscher A, von Zastrow M (1999) A kinaseregulated PDZ-domain interaction controls endocytic sorting of the beta2-adrenergic receptor. Nature 401: 286-290.
51. Hryciw DH, Ekberg J, Ferguson C, Lee A, Wang D, et al. (2006) Regulation of albumin endocytosis by PSD95/Dlg/ZO-1 (PDZ) scaffolds. Interaction of Na+-H+ exchange regulatory factor-2 with ClC-5. J Biol Chem 281: 16068-16077.
52. Berger W, Steiner E, Grusch M, Elbling L, Micksche M (2009) Vaults and the major vault protein: novel roles in signal pathway regulation and immunity. Cell Mol Life Sci 66: 43-61.
53. Herlevsen M, Oxford G, Owens CR, Conaway M, Theodorescu D (2007) Depletion of major vault protein increases doxorubicin sensitivity and nuclear accumulation and disrupts its sequestration in lysosomes. Mol Cancer Ther 6: 1804-1813.
54. Kowalski MP, Dubouix-Bourandy A, Bajmoczi M, Golan DE, Zaidi T, et al. (2007) Host resistance to lung infection mediated by major vault protein in epithelial cells. Science 317: 130-132.
55. Hryciw DH, Wang Y, Devuyst O, Pollock CA, Poronnik P, et al. (2003) Cofilin interacts with ClC-5 and regulates albumin uptake in proximal tubule cell lines. J Biol Chem 278: 40169-40176.
56. Hryciw DH, Pollock CA, Poronnik P (2005) PKC-alpha-mediated remodeling of the actin cytoskeleton is involved in constitutive albumin uptake by proximal tubule cells. Am J Physiol Renal Physiol 288: F1227-1235.
57. Diaz E, Pfeffer SR (1998) TIP47: a cargo selection device for mannose 6- phosphate receptor trafficking. Cell 93: 433-443.
58. Espinosa EJ, Calero M, Sridevi K, Pfeffer SR (2009) RhoBTB3: a Rho GTPasefamily ATPase required for endosome to Golgi transport. Cell 137: 938-948.
59. Hyvonen MT, Merentie M, Uimari A, Keinanen TA, Janne J, et al. (2007) Mechanisms of polyamine catabolism-induced acute pancreatitis. Biochem Soc Trans 35: 326-330.
60. Kanerva K, Makitie LT, Back N, Andersson LC (2010) Ornithine decarboxylase antizyme inhibitor 2 regulates intracellular vesicle trafficking. Exp Cell Res 316: 1896-1906.