A heparan sulfate-facilitated and raft-dependent macropinocytosis of eosinophil cationic protein

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Volumn 8, Issue 12, 2007, Pages 1778-1795

  Fan, Tan Chi ^a   Chang, Hao Teng ^a   Chen, I Wen ^a   Wang, Hsiu Yiu ^a   Chang, Margaret Dah Tsyr ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

ECP; Heparan sulfate; Lipid rafr; Macropinocytosis

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CAVEOLIN; CHLORATE; CHOLESTEROL; CLATHRIN; EOSINOPHIL CATIONIC PROTEIN; GLYCAN; GLYCOSAMINOGLYCAN; GUANOSINE TRIPHOSPHATASE; HEPARAN SULFATE; HEPARIN LYASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEOHEPARAN SULFATE; RAC1 PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; BRONCHUS MUCOSA; CONTROLLED STUDY; CYTOTOXICITY; ENDOCYTOSIS; ENZYME ACTIVITY; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; INTERNALIZATION; LIPID RAFT; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN TRANSPORT; SULFATION; WILD TYPE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BIOLOGICAL TRANSPORT; BRONCHI; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; ENDOCYTOSIS; EOSINOPHIL CATIONIC PROTEIN; EOSINOPHILS; EPITHELIAL CELLS; HEPARITIN SULFATE; HUMANS; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; PINOCYTOSIS;

EID: 35948950217     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2007.00650.x     Document Type: Article

References (68)

1. Makarov AA, Ilinskaya ON. Cytotoxic ribonucleases: Molecular weapons and their targets. FEBS Lett 2003; 540: 15-20.
2. Bracale A, Spalletti-Cernia D, Mastronicola M, Castaldi F, Mannucci R, Nitsch L, D'Alessio G. Essential stations in the intracellular pathway of cytotoxic bovine seminal ribonuclease. Biochem J 2002; 362: 553-560.
3. Maeda T, Kitazoe M, Tada H, Llorens Rd, Salomon DS, Ueda M, Yamada H, Seno M. Growth inhibition of mammalian cells by eosinophil cationic protein. Eur J Biochem 2002; 269: 307-316.
4. Leland PA, Staniszewski KE, Kim B, Raines RT. A synapomorphic disulfide bond is critical for the conformational stability and cytotoxicity of an amphibian ribonuclease. FEBS Lett 2000; 477: 203-207.
5. Leland PA, Staniszewski KE, Kim BM, Raines RT. Endowing human pancreatic ribonuclease with toxicity for cancer cells. J Biol Chem 2001; 276: 43095-43102.
6. Rosenberg H. The eosinophil ribonucleases. Cell Mol Life Sci 1998; 54: 795-803.
7. Barker R, Loegering D, Ten R, Hamann K, Pease L, Gleich G. Eosinophil cationic protein cDNA. Comparison with other toxic cationic proteins and ribonucleases. J Immunol 1989; 143: 952-955.
8. Giembycz MA, Lindsay MA. Pharmacology of the eosinophil. Pharmacol Rev 1999; 51: 213-340.
9. Gleich GJ. Mechanisms of eosinophil-associated inflammation. J Allergy Clin Immunol 2000; 105: 651-663.
10. Young J, Peterson C, Venge P, Cohn Z. Mechanism of membrane damage mediated by human eosinophil cationic protein. Nature 1986; 321: 613-616.
11. Carreras E, Boix E, Navarro S, Rosenberg HF, Cuchillo CM, Nogues MV. Surface-exposed amino acids of eosinophil cationic protein play a critical role in the inhibition of mammalian cell proliferation. Mol Cell Biochem 2005; 272: 1-7.
12. Carreras E, Boix E, Rosenberg HF, Cuchillo CM, Nogues MV. Both aromatic and cationic residues contribute to the membrane-lytic and bactericidal activity of eosinophil cationic protein. Biochemistry 2003; 42: 6636-6644.
13. Gleich GJ, Loegering DA, Bell MP, Checkel JL, Ackerman SJ, McKean DJ. Biochemical and functional similarities between human eosinophil-derived neurotoxin and eosinophil cationic protein: Homology with ribonuclease. Proc Natl Acad Sci U S A 1986; 83: 3146-3150.
14. Prydz K, Dalen KT. Synthesis and sorting of proteoglycans. J Cell Sci 2000; 113: 193-205.
15. Whitelock JM, Iozzo RV. Heparan sulfate: A complex polymer charged with biological activity. Chem Rev 2005; 105: 2745-2754.
16. Park PW, Reizes O, Bernfield M. Cell surface heparan sulfate proteoglycans: Selective regulators of ligand-receptor encounters. J Biol Chem 2000; 275: 29923-29926.
17. Perrimon N, Bernfield M. Specificities of heparan sulfate proteoglycans in developmental processes. Nature 2000; 404: 725-728.
18. Yanagishita M. Cellular catabolism of heparan sulfate proteoglycans. Trends Glycosci Glycotechnol 1998; 10: 57-63.
19. Tkachenko E, Simons M. Clustering induces redistribution of syndecan-4 core protein into raft membrane domains. J Biol Chem 2002; 277: 19946-19951.
20. Simons A, Ikonen E. Functional rafts in cell membranes. Nature 1997; 387: 569-572.
21. Nichols B. Caveosomes and endocytosis of lipid rafts. J Cell Sci 2003; 116: 4707-4714.
22. Parton R. Caveolae and caveolins. Curr Opin Cell Biol 1996; 8: 542-548.
23. Gauthier NC, Monzo P, Kaddai V, Doye A, Ricci V, Boquet P. Helicobacter pylori VacA cytotoxin: A probe for a clathrin-independent and Cdc42-dependent pinocytic pathway routed to late endosomes. Mol Biol Cell 2005; 16: 4852-4866.
24. Grimmer S, van Deurs B, Sandvig K. Membrane ruffling and macropinocytosis in A431 cells require cholesterol. J Cell Sci 2002; 115: 2953-2962.
25. Nhieu GT, Sansonetti PJ. Mechanism of Shigella entry into epithelial cells. Curr Opin Microbiol 1999; 2: 51-55.
26. Nakase I, Niwa M, Takeuchi T, Sonomura K, Kawabata N, Koike Y, Takehashi M, Tanaka S, Ueda K, Simpson JC, Jones AT, Sugiura Y, Futaki S. Cellular uptake of arginine-rich peptides: Roles for macropinocytosis and actin rearrangement. Mol Ther 2004; 10: 1011-1022.
27. Wadia JS, Stan RV, Dowdy SF. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 2004; 10: 310-315.
28. Sieczkarski SB, Whittaker GR. Dissecting virus entry via endocytosis. J Gen Virol 2002; 83: 1535-1545.
29. Brown FD, Rozelle AL, Yin HL, Balla T, Donaldson JG. Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J Cell Biol 2001; 154: 1007-1017.
30. D'Souza-Schorey C, Chavrier P. ARF proteins: Roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 2006; 7: 347-358.
31. Naslavsky N, Weigert R, Donaldson JG. Convergence of non-clathrin- and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol Biol Cell 2003; 14: 417-431.
32. Farley J, Nakayama G, Cryns D, Segel I. Adenosine triphosphate sulfurylase from Penicillium chrysogenum equilibrium binding, substrate hydrolysis, and isotope exchange studies. Arch Biochem Biophys 1978; 185: 376-390.
33. Noel GJ, Love DC, Mosser DM. High-molecular-weight proteins of nontypeable Haemophilus influenzae mediate bacterial adhesion to cellular proteoglycans. Infect Immun 1994; 62: 4028-4033.
34. Wang LH, Rothberg KG, Anderson RG. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 1993; 123: 1107-1117.
35. Anderson HA, Chen Y, Norkin LC. Bound simian virus 40 translocates to caveolin enriched membrane domains and its entry is inhibited by drugs that selectively disrupt caveolae. Mol Biol Cell 1996; 7: 1825-1834.
36. Puri V, Watanabe R, Singh RD, Dominguez M, Brown JC, Wheatley CL, Marks DL, Pagano RE. Clathrin-dependent and -independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways. J Cell Biol 2001; 154: 535-547.
37. Benmerah A, Bayrou M, Cerf-Bensussan N, Dautry-Varsat A. Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J Cell Sci 1999; 112: 1303-1311.
38. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 2003; 422: 37-44.
39. Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 1994; 127: 915-934.
40. Soldati T, Schliwa M. Powering membrane traffic in endocytosis and recycling. Nat Rev Mol Cell Biol 2006; 7: 897-908.
41. Sampath P, Pollard TD. Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments. Biochemistry 1991; 30: 1973-1980.
42. West MA, Bretscher MS, Watts C. Distinct endocytotic pathways in EGF-stimulated human carcinoma A431 cells. J Cell Biol 1989; 109: 2731-2739.
43. Araki N, Johnson MT, Swanson JA. A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol 1996; 135: 1249-1260.
44. Murray J, Wilson L, Kellie S. Phosphatidylinositol-3′ kinase-dependent vesicle formation in macrophages in response to macrophage colony stimulating factor. J Cell Biol 2000; 113: 337-348.
45. West MA, Prescott AR, Eskelinen E, Ridley AJ, Watts C. Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr Biol 2000; 10: 839-848.
46. Johannes L, Lamaze C. Clathrin-dependent or not: Is it still the question? Traffic 2002; 3: 443-451.
47. Sabharanjak S, Sharma P, Parton RG, Mayor S. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2002; 2: 411-423.
48. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, Sharma DK, Pagano RE, Hancock JF, Mayor S, Parton RG. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 2005; 168: 465-476.
49. Lamaze C, Dujeancourt A, Baba T, Lo CG, Benmerah A, Dautry-Varsat A. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol Cell 2001; 7: 661-671.
50. Manes S, Ana Lacalle R, Gomez-Mouton C, Martinez - AC. From rafts to crafts: Membrane asymmetry in moving cells. Trends Immunol 2003; 24: 320-326.
51. Kirkham M, Parton RG. Clathrin-independent endocytosis: New insights into caveolae and non-caveolar lipid raft carriers. Biochim Biophys Acta 2005; 1746: 349-363.
52. Naslavsky N, Weigert R, Donaldson JG. Characterization of a nonclathrin endocytic pathway: Membrane cargo and lipid requirements. Mol Biol Cell 2004; 15: 3542-3552.
53. Swanson JA, Watts C. Macropinosytosis. Trends Cell Biol 1995; 5: 424-428.
54. Racoosin EL, Swanson JA. Macropinosome maturation and fusion with tubular lysosomes in macrophages. J Cell Biol 1993; 121: 1011-1020.
55. Hewlett LJ, Prescott AR, Watts C. The coated pit and macropinocytic pathways serve distinct endosome populations. J Cell Biol 1994; 124: 689-703.
56. Mallard F, Antony C, Tenza D, Salamero J, Goud B, Johannes L. Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of shiga toxin B-fragment transport. J Cell Biol 1998; 143: 973-990.
57. Gengrinovitch S, Berman B, David G, Witte L, Neufeld G, Ron D. Glypican-1 is a VEGF165 binding proteoglycan that acts as an extracellular chaperone for VEGF165. J Biol Chem 1999; 274: 10816-10822.
58. Capila I, Linhardt RJ. Heparin-protein interactions. Angew Chem Int Ed Engl 2002; 41: 391-412.
59. Tkachenko E, Lutgens E, Stan RV, Simons M. Fibroblast growth factor 2 endocytosis in endothelial cells proceed via syndecan-4-dependent activation of Rac1 and a Cdc42-dependent macropinocytic pathway. J Cell Sci 2004; 117: 3189-3199.
60. Cooper A, Shaul Y. Clathrin-mediated endocytosis and lysosomal cleavage of hepatitis B virus capsid-like core particles. J Biol Chem 2006; 281: 16563-16569.
61. Bosch M, Benito A, Ribo M, Puig T, Beaumelle B, Vilanova M. A nuclear localization sequence endows human pancreatic ribonuclease with cytotoxic activity. Biochemistry 2004; 43: 2167-2177.
62. Haigis MC, Raines RT. Secretory ribonucleases are internalized by a dynamin-independent endocytic pathway. J Cell Sci 2002; 116: 313-324.
63. Meier O, Boucke K, Hammer SV, Keller S, Stidwill RP, Hemmi S, Greber UF. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J Cell Biol 2002; 158: 1119-1131.
64. Khalil IA, Kogure K, Futaki S, Harashima H. High density of octaarginine stimulates macropinocytosis leading to efficient intracellular trafficking for gene expression. J Biol Chem 2006; 281: 3544-3551.
65. Wu CM, Chang HT, Chang MD. Membrane-bound carboxypeptidase E facilitates the entry of eosinophil cationic protein into neuroendocrine cells. Biochem J 2004; 382: 841-848.
66. Boix E, Nikolovski Z, Moiseyev GP, Rosenberg HFC, Cuchillo CM, Nogues MV. Kinetic and product distribution analysis of human eosinophil cationic protein indicates a subsite arrangement that favors exonuclease-type activity. J Biol Chem 1999; 274: 15605-15614.
67. Wu SC, Chiang JR, Lin CW. Novel cell adhesive glycosaminoglycan-binding proteins of Japanese encephalitis virus. Biomacromolecules 2004; 5: 2160-2164.
68. Richard JP, Melikov K, Brooks H, Prevot P, Lebleu B, Chernomordik LV. Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors. J Biol Chem 2005; 280: 15300-15306.