Enrichment of distinct microfilament-associated and GTP-binding-proteins in membrane/microvilli fractions from lymphoid cells

Journal of Proteome Research

Volumn 7, Issue 7, 2008, Pages 2911-2927

  Hao, Jian Jiang ^a   Wang, Guanghui ^b   Pisitkun, Trairak ^c   Patino Lopez, Genaro ^a   Nagashima, Kunio ^d   Knepper, Mark A ^c   Shen, Rong Fong ^b   Shaw, Stephen ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^d SAIC FREDERICK INC   (United States)

Author keywords

Cofilin; Cytoskeleton; Label free quatitation; LC MS MS; Lymphocyte; Microvillus; MyolG; NHERF1; Proteome; Small GTP binding protein

Indexed keywords

COFILIN; CYTOSKELETON PROTEIN; EZRIN; GELSOLIN; GENE PRODUCT; GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE PROTEIN; MOESIN; MYOSIN; MYOSIN 1G; MYOSIN II; PROFILIN; PROTEIN NHERF1; RADIXIN; TALIN; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; LYMPHOID CELL; MASS SPECTROMETRY; MICROVILLUS; MOUSE; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; SPECIES COMPARISON; WESTERN BLOTTING; ANIMAL; CELL LINE; CELL MEMBRANE; CHEMISTRY; COMPARATIVE STUDY; ISOLATION AND PURIFICATION; PRE B LYMPHOCYTE; SPECIES DIFFERENCE; T LYMPHOCYTE; TANDEM MASS SPECTROMETRY; ULTRASTRUCTURE;

MINUTE VIRUS OF MICE;

ANIMALS; CELL LINE; CELL MEMBRANE; CHROMATOGRAPHY, LIQUID; GTP-BINDING PROTEINS; HUMANS; MICE; MICROFILAMENT PROTEINS; MICROVILLI; MONOMERIC GTP-BINDING PROTEINS; PRECURSOR CELLS, B-LYMPHOID; SPECIES SPECIFICITY; T-LYMPHOCYTES; TANDEM MASS SPECTROMETRY;

EID: 51649124968     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr800016a     Document Type: Article

References (80)

1. Butcher, E. C.; Williams, M.; Youngman, K.; Rott, L.; Briskin, M. Lymphocyte trafficking and regional immunity. Adv. Immunol. 1999, 72, 209-253.
2. Springer, T. A. Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu. Rev. Physiol. 1995, 57, 827-872.
3. Shimizu, Y.; Newman, W.; Tanaka, Y.; Shaw, S. Lymphocyte interactions with endothelial cells. Immunol. Today 1992, 13 (3), 106-112.
4. Anderson, A. O.; Anderson, N. D. Lymphocyte emigration from high endothelial venules in rat lymph nodes. Immunology 1976, 31 (5), 731-748.
5. van Ewijk, W.; Brons, N. H.; Rozing, J. Scanning electron microscopy of homing and recirculating lymphocyte populations. Cell Immunol. 1975, 19 (2), 245-261.
6. Picker, L. J.; Wamock, R. A.; Burns, A. R.; Doerschuk, C. M.; Berg, E. L.; Butcher, E. C. The neutrophil selectin LECAM-1 presents carbohydrate ligands to the vascular selectins ELAM-1 and GMP-140. Cell 1991, 66 (5), 921-933.
7. von Andrian, U. H.; Hasslen, S. R.; Nelson, R. D.; Erlandsen, S. L.; Butcher, E. C. A central role for microvillous receptor presentation in leukocyte adhesion under flow. Cell 1995, 82 (6), 989-999.
8. Brown, M. J.; Nijhara, R.; Hallam, J. A.; Gignac, M.; Yamada, K. M.; Erlandsen, S. L.; Delon, I.; Kruhlak, M.; Shaw, S. Chemokine stimulation of human peripheral blood T lymphocytes induces rapid dephosphorylation of ERM proteins, which facilitates loss of microvilli and polarization. Blood 2003, 102 (12), 3890-3899.
9. Majstoravich, S.; Zhang, J.; Nicholson-Dykstra, S.; Under, S.; Friedrich, W.; Siminovitch, K. A.; Higgs, H. N. Lymphocyte microvilli are dynamic, actin-dependent structures that do not require Wiskott-Aldrich syndrome protein (WASp) for their morphology. Blood 2004, 104 (5), 1396-1403.
10. Shao, J. Y.; Xu, J. A modified micropipette aspiration technique and its application to tether formation from human neutrophils. J. Biomech. Eng. 2002, 124 (4), 388-396.
11. Mooseker, M. S. Organization, chemistry, and assembly of the cytoskeletal apparatus of the intestinal brush border. Annu. Rev. Cell Biol. 1985, 1, 209-241.
12. Donowitz, M.; Cha, B.; Zachos, N. C.; Brett, C. L.; Sharma, A.; Tse, C. M.; Li, X. NHERF family and NHE3 regulation. J. Physiol. 2005, 567 (Pt 1), 3-11.
13. Weinman, E. J.; Cunningham, R.; Shenolikar, S. NHERF and regulation of the renal sodium-hydrogen exchanger NHE3. Pflugers Arch. 2005, 450 (3), 137-144.
14. Lin, H. W.; Schneider, M. E.; Kachar, B. When size matters: the dynamic regulation of stereocilia lengths. Curr. Opin. Cell Biol. 2005, 17(1), 55-61.
15. Reczek, D.; Bretscher, A. Identification of EPI64, a TBC/rabGAP domain-containing microvillar protein that binds to the first PDZ domain of EBP50 and E3KARP. J. Cell Biol. 2001, 153 (1), 191- 206.
16. Donowitz, M.; Singh, S.; Salahuddin, F. F.; Hogema, B. M.; Chen, Y.; Gucek, M.; Cole, R. N.; Zachos, N. C.; Kovbasnjuk, O.; Lapierre, L. A.; Broere, N.; Goldenring, J.; dejonge, H.; Li, X. Proteome of murine jejunal brush border membrane vesicles. J. Proteome Res. 2007, 6 (10), 4068-4079.
17. Morell, G.; Steplock, D.; Shenolikar, S.; Weinman, E. J. Identification of a putative Na(+)-H+ exchanger regulatory cofactor in rabbit renal BBM. Am. J. Physiol. 1990, 259 (6 Pt. 2), F867-871.
18. Reczek, D.; Berryman, M.; Bretscher, A. Identification of EBP50: A PDZ-containing phosphoprotein that associates with members of the ezrin-radixin-moesin family. J. Cell Biol. 1997, 139 (1), 169- 179.
19. Foster, L. J.; de Hoog, C. L.; Zhang, Y.; Zhang, Y.; Xie, X.; Mootha, V. K.; Mann, M. A mammalian organelle map by protein correlation profiling. Cell 2006, 125 (1), 187-199.
20. Wang, G.; Wu, W. W.; Zeng, W.; Chou, C. L.; Shen, R. F. Label-free protein quantification using LC-coupled ion trap or FT mass spectrometry: Reproducibility, linearity, and application with complex proteomes. J Proteome Res 2006, 5 (5), 1214-1223.
21. Bondarenko, P. V.; Chelius, D.; Shaler, T. A. Identification and relative quantitation of protein mixtures by enzymatic digestion followed by capillary reversed-phase liquid chromatography- tandem mass spectrometry. Anal. Chem. 2002, 74 (18), 4741-4749.
22. Wang, W.; Zhou, H.; Lin, H.; Roy, S.; Shaler, T. A.; Hill, L. R.; Norton, S.; Kumar, P.; Anderle, M.; Becker, C. H. Quantification of proteins and metabolites by mass spectrometry without isotopic labeling or spiked standards. Anal. Chem. 2003, 75 (18), 4818-4826.
23. Higgs, R. E.; Knierman, M. D.; Gelfanova, V.; Butler, J. P.; Hale, J. E. Comprehensive label-free method for the relative quantification of proteins from biological samples. J. Proteome Res. 2005, 4 (4), 1442-1450.
24. Li, X. J.; Yi, E. C.; Kemp, C. J.; Zhang, H.; Aebersold, R. A software suite for the generation and comparison of peptide arrays from sets of data collected by liquid chromatography-mass spectrometry. Mol. Cell. Proteomics 2005, 4 (9), 1328-1340.
25. Ley, K.; Tedder, T. F.; Kansas, G. S. L-selectin can mediate leukocyte rolling in untreated mesenteric venules in vivo independent of E- or P-selectin. Blood 1993, 82 (5), 1632-1638.
26. Dwir, O.; Kansas, G. S.; Alon, R. Cytoplasmic anchorage of L-selectin controls leukocyte capture and rolling by increasing the mechanical stability of the selectin tether. J. Cell Biol. 2001, 155 (1), 145-156.
27. Wahl, S. M.; Katona, I. M.; Stadler, B. M.; Wilder, R. L.; Helsel, W. E.; Wahl, L. M. Isolation of human mononuclear cell subsets by counterflow centrifugal elutriation (CCE). II. Functional properties of B-lymphocyte-, T-lymphocyte-, and monocyte-enriched fractions. Cell Immunol. 1984, 85 (2), 384-395.
28. van Rheenen, J.; Song, X.; van Roosmalen, W.; Cammer, M.; Chen, X.; Desmarais, V.; Yip, S. C.; Backer, J. M.; Eddy, R. J.; Condeelis, J. S. EGF-induced PIP2 hydrolysis releases and activates cofilin locally in carcinoma cells. J. Cell Biol. 2007, 179 (6), 1247-1259.
29. Carraway, K. L.; Huggins, J. W.; Cerra, R. F.; Yeltman, D. R.; Carraway, C. A. alpha-Actinin-containing branched microvilli isolated from an ascites adenocarcinoma. Nature 1980, 285 (5765), 508-510.
30. Booth, A. G.; Vanderpuye, O. A. Structure of human placental microvilli. Ciba Found. Symp. 1983, 95, 180-194.
31. Berryman, M.; Gary, R.; Bretscher, A. Ezrin oligomers are major cytoskeletal components of placental microvilli: a proposal for their involvement in cortical morphogenesis. J. Cell Biol. 1995, 131 (5), 1231-1242.
32. Hellman, U.; Wernstedt, C.; Gonez, J.; Heldin, C. H. Improvement of an "In-Gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal. Biochem. 1995, 224 (1), 451-455.
33. Moller, S.; Croning, M. D.; Apweiler, R. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 2001, 17 (7), 646-653.
34. Mariner, J. M.; McMahon, J. B.; O'Keefe, B. R.; Nagashima, K.; Boyd, M. R. The HTV-inactivating protein, cyanovirin-N, does not block gpl20-mediated virus-to-cell binding. Biochem. Biophys. Res. Commun. 1998, 248 (3), 841-845.
35. Muriaux, D.; Mirro, J.; Nagashima, K.; Harvin, D.; Rein, A. Murine leukemia virus nucleocapsid mutant particles lacking viral RNA encapsidate ribosomes. J. Virol. 2002, 76 (22), 11405-11413.
36. Ivetic, A.; Florey, O.; Deka, I.; Haskard, D. O.; Ager, A.; Ridley, A. J. Mutagenesis of the ezrin-radixin-moesin binding domain of L-selectin tail affects shedding, microvillar positioning, and leukocyte tethering. J. Biol Chem. 2004, 279 (32), 33263-33272.
37. Takeuchi, K.; Sato, N.; Kasahara, H.; Funayama, N.; Nagafuchi, A.; Yonemura, S.; Tsukita, S.; Tsukita, S. Perturbation of cell adhesion and microvilli formation by antisense oligonucleotides to ERM family members. J. Cell Biol. 1994, 125 (6), 1371-1384.
38. Brown, M. J.; Hallam, J. A.; Colucci-Guyon, E.; Shaw, S. Rigidity of circulating lymphocytes is primarily conferred by vimentin intermediate filaments. J. Immunol. 2001, 166 (11), 6640-6646.
39. Simpson, J. C.; Pepperkok, R. The subcellular localization of the mammalian proteome comes a fraction closer. GenomeBiology 2006, 7 (6), 222.
40. Gilchrist, A.; Au, C. E.; Hiding, J.; Bell, A. W.; Fernandez-Rodriguez, J.; Lesimple, S.; Nagaya, H.; Roy, L.; Gosline, S. J.; Hallett, M.; Paiement, J.; Kearney, R. E.; Nilsson, T.; Bergeron, J. J. Quantitative proteomics analysis of the secretory pathway. Cell 2006, 127 (6), 1265-1281.
41. Nebl, T.; Pestonjamasp, K. N.; Leszyk, J. D.; Crowley, J. L.; Oh, S. W.; Luna, E. J. Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. J. Biol. Chem. 2002, 277 (45), 43399-43409.
42. Tyska, M. J.; Mackey, A. T.; Huang, J. D.; Copeland, N. G.; Jenkins, N. A.; Mooseker, M. S. Myosin-la is critical for normal brush border structure and composition. Mol. Biol. Cell 2005, 16 (5), 2443-2457.
43. Batters, C.; Arthur, C. P.; Lin, A.; Porter, J.; Geeves, M. A.; Milligan, R. A.; Molloy, J. E.; Coluccio, L. M. Myolc is designed for the adaptation response in the inner ear. EMBO J. 2004, 23 (7), 1433- 1440.
44. Kim, S. V.; Mehal, W. Z.; Dong, X.; Heinrich, V.; Pypaert, M.; Mellman, 1.; Dembo, M.; Mooseker, M. S.; Wu, D.; Flavell, R. A. Modulation of cell adhesion and motility in the immune system by Myolf. Science 2006, 314 (5796), 136-139.
45. Bose, A.; Guilherme, A.; Robida, S. I.; Nicoloro, S. M.; Zhou, Q. L.; Jiang, Z. Y.; Pomerleau, D. P.; Czech, M. P. Glucose transporter recycling in response to insulin is facilitated by myosin Myolc. Nature 2002, 420 (6917), 821-824.
46. Tyska, M. J.; Mooseker, M. S. A role for myosin-1A in the localization of a brush border disaccharidase. J. Cell Biol. 2004, 165 (3), 395-405.
47. DesMarais, V.; Ghosh, M.; Eddy, R.; Condeelis, J. Cofilin takes the lead. J. Cell Sci. 2005, 118 (Pt 1), 19-26.
48. Andrianantoandro, E.; Pollard, T. D. Mechanism of Actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol. Cell 2006, 24 (1), 13-23.
49. Yonezawa, N.; Nishida, E.; Iida, K.; Yahara, I.; Sakai, H. Inhibition of the interactions of cofilin, destrin, and deoxyribonuclease I with Actin by phosphoinositides. J. Biol. Chem. 1990, 265 (15), 8382- 8386.
50. dos Remedios, C. G.; Chhabra, D.; Kekic, M.; Dedova, I. V.; Tsubakihara, M.; Berry, D. A.; Nosworthy, N. J. Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol Rev 2003, 83 (2), 433-473.
51. Fass, J.; Gehler, S.; Sarmiere, P.; Letourneau, P.; Bamburg, J. R. Regulating filopodial dynamics through Actin-depolymerizing factor/cofilin. Anat. Sci. Int. 2004, 79 (4), 173-183.
52. Ashworth, S. L.; Sandoval, R. M.; Hosford, M.; Bamburg, J. R.; Molitoris, B. A. Ischemic injury induces ADF relocalization to the apical domain of rat proximal tubule cells. Am. J. Physiol.: Renal Physiol. 2001, 280 (5), F886-894.
53. Gorbatyuk, V. Y.; Nosworthy, N. J.; Robson, S. A.; Bains, N. P.; Maciejewski, M. W.; Dos Remedios, C. G.; King, G. F. Mapping the phosphoinositide-binding site on chick cofilin explains how PIP2 regulates the cofilin-actin interaction. Mol. Cell 2006, 24 (4), 511-522.
54. Ono, S. Regulation of actin filament dynamics by actin depolymerizing factor/cofilin and actin-interacting protein 1: new blades for twisted filaments. Biochemistry 2003, 42 (46), 13363-13370.
55. Okada, K.; Ravi, H.; Smith, E. M.; Goode, B. L. Aipl and cofilin promote rapid turnover of yeast Actin patches and cables: a coordinated mechanism for severing and capping filaments. Mol. Biol. Cell 2006, 17 (7), 2855-2868.
56. Mayboroda, O.; Schluter, K.; Jockusch, B. M. Differential colocalization of profilin with microfilaments in PtK2 cells. Cell Motil. Cytoskeleton 1997, 37 (2), 166-177.
57. Skare, P.; Kreivi, J. P.; Bergstrom, A.; Karlsson, R. Profilin I colocalizes with speckles and Cajal bodies: a possible role in pre- mRNA splicing. Exp. Cell Res. 2003, 286 (1), 12-21.
58. Grenklo, S.; Johansson, T.; Bertilson, L.; Karlsson, R. Anti-actin antibodies generated against profilin:actin distinguish between non-filamentous and filamentous actin, and label cultured cells in a dotted pattern. Eur. J. Cell Biol. 2004, 83 (8), 413-423.
59. Hartwig, J. H.; Chambers, K. A.; Hopcia, K. L.; Kwiatkowski, D. J. Association of profilin with filament-free regions of human leukocyte and platelet membranes and reversible membrane binding during platelet activation. J. Cell Biol. 1989, 109 (4 Pt 1), 1571-1579.
60. Wettschureck, N.; Offermanns, S. Mammalian G proteins and their cell type specific functions. Physiol. Rev. 2005, 85 (4), 1159-1204.
61. Jordens, I.; Marsman, M.; Kuijl, C.; Neefjes, J. Rab proteins, connecting transport and vesicle fusion. Traffic 2005, 6 (12), 1070- 1077.
62. Jaffe, A. B.; Hall, A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 2005, 21, 247-269.
63. Hancock, J. F. Ras proteins: different signals from different locations. Nat. Rev. Mol. Cell. Biol. 2003, 4 (5), 373-384.
64. Heo, W. D.; Inoue, T.; Park, W. S.; Kim, M. L.; Park, B. O.; Wandless, T. J.; Meyer, T. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 2006, 314 (5804), 1458-1461.
65. Bos, J. L. linking Rap to cell adhesion. Curr. Opin. Cell Biol. 2005, 17 (2), 123-128.
66. Concha, M.; Vidal, A.; Garces, G.; Figueroa, C. D.; Caorsi, I. Physical interaction between Langerhans cells and T-lymphocytes during antigen presentation in vitro. J. Invest. Dermatol. 1993, 100 (4), 429-434.
67. Tsukita, S.; Oishi, K.; Sato, N.; Sagara, J.; Kawai, A.; Tsukita, S. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and Actin-based cytoskeletons. J. Cell Biol. 1994, 126 (2), 391-401.
68. DeGrendele, H. C.; Estess, P.; Picker, L. J.; Siegelman, M. H. CD44 and its ligand hyaluronate mediate rolling under physiologic flow: a novel lymphocyte-endothelial cell primary adhesion pathway. J. Exp. Med. 1996, 183 (3), 1119-1130.
69. Berry, K. L.; Hobert, O. Mapping functional domains of chloride intracellular channel (CLIC) proteins in vivo. J. Mol. Biol. 2006, 359 (5), 1316-1333.
70. Berryman, M.; Bretscher, A. Identification of a novel member of the chloride intracellular channel gene family (CLIC5) that associates with the Actin cytoskeleton of placental microvilli. Mol. Biol. Cell 2000, 11 (5), 1509-1521.
71. Gagnon, L. H.; Longo-Guess, C. M.; Berryman, M.; Shin, J. B.; Saylor, K. W.; Yu, H.; Gillespie, P. G.; Johnson, K. R. The chloride intracellular channel protein CLIC5 is expressed at high levels in hair cell stereocilia and is essential for normal inner ear function. J. Neurosci. 2006, 26 (40), 10188-10198.
72. Kirk, P.; Wilson, M. C.; Heddle, C.; Brown, M. H.; Barclay, A. N.; Halestrap, A. P. CD147 is tightly associated with lactate transporters MCT1 and MCT4 and facilitates their cell surface expression. EMBO J. 2000, 19 (15), 3896-3904.
73. Halestrap, A. P.; Price, N. T. The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem. J. 1999, 343 (2), 281-299.
74. Tall, E. G.; Spector, I.; Pentyala, S. N.; Bitter, I.; Rebecchi, M. J. Dynamics of phosphatidylinositol 4,5-bisphosphate in Actin-rich structures. Curr. Biol. 2000, 10 (12), 743-746.
75. Hokanson, D. E.; Laakso, J. M.; Lin, T.; Sept, D.; Ostap, E. M. Myolc binds phosphoinositides through a putative pleckstrin homology domain. Mol. Biol. Cell 2006, 17 (11), 4856-4865.
76. Bretscher, A.; Chambers, D.; Nguyen, R.; Reczek, D. Erm-Merlin and Ebp50 Protein Families in Plasma Membrane Organization and Function. Annu. Rev. Cell Dev. Biol. 2000, 16, 113-143.
77. Terawaki, S.; Kitano, K.; Hakoshima, T. Structural basis for type II membrane protein binding by ERM proteins revealed by the radixin-neutral endopeptidase 24.11 (NEP) complex. J. Biol. Chem. 2007, 282 (27), 19854-19862.
78. Arora, P. D.; McCulloch, C. A. Dependence of collagen remodelling on alpha-smooth muscle Actin expression by fibroblasts. J. Cell Physiol. 1994, 159 (1), 161-175.
79. Schmitt-Graff, A.; Chaponnier, C.; Gabbiani, G. Cytoskeletal organization of peripheral blood normal and leukemic lymphocytes and lymphoblasts. J. Submicrosc. Cytol. 1987, 19 (2), 329- 335.
80. Murphy, P. M. Molecular mimicry and the generation of host defense protein diversity. Cell 1993, 72 (6), 823-826.