Identification of proteins from a cell wall fraction of the diatom Thalassiosira pseudonana: Insights into silica structure formation

Molecular and Cellular Proteomics

Volumn 5, Issue 1, 2006, Pages 182-193

  Frigeri, Luciano G ^a   Radabaugh, Timothy R ^b   Haynes, Paul A ^b   Hildebrand, Mark ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; GLUTAMATE ACETYLTRANSFERASE; MESSENGER RNA; ORNITHINE DECARBOXYLASE INHIBITOR; POLYAMINE DERIVATIVE; SILICON DIOXIDE;

CELL CYCLE; CELL FRACTIONATION; CELL WALL; CONTROLLED STUDY; CORRELATION ANALYSIS; DIATOM; ENZYME SPECIFICITY; GENETIC CODE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEOMICS; REVIEW; RNA ANALYSIS; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY;

ACETYLTRANSFERASES; ALGAL PROTEINS; CELL CYCLE PROTEINS; CELL WALL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DATABASES, PROTEIN; DIATOMS; ENZYME INHIBITORS; NANOSTRUCTURES; NANOTECHNOLOGY; ORNITHINE DECARBOXYLASE; PEPTIDE FRAGMENTS; POLYAMINES; RNA, MESSENGER; SILICON DIOXIDE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUBCELLULAR FRACTIONS;

ALGAE; BACILLARIOPHYTA; EUKARYOTA; THALASSIOSIRA PSEUDONANA;

EID: 31644445185     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M500174-MCP200     Document Type: Review

References (93)

1. Pickett-Heaps, J., Schmid, A.-M. M., and Edgar, L. A. (1990) The cell biology of diatom valve formation, in Progress in Phycological Research (Round, F. E., and Chapman, D. J., eds) pp. 1-168, Biopress Ltd., Bristol, UK
2. Round, F. E., Crawford, R. M., and Mann, D. G. (1990) The Diatoms: Biology and Morphology of the Genera, p. 747, Cambridge University Press, Bath, UK
3. Crawford, R. M., and Schmid, A. M. (1986) Ultrastructure of silica deposition in diatoms, in Biomineralization in Lower Plants and Animals (Lead-beater, B. S., and Riding, R., eds) Vol. 30, pp. 291-314, The Systematics Society, London
4. Drum, R. W., and Pankratz, H. S. (1964) Post mitotic fine structure of Gomphonema parvulum. J. Ultrastruct. Res. 10, 217-223
5. Reimann, B. E. F., Lewin, J. C., and Volcani, B. E. (1966) Studies on the biochemistry and fine structure of silica shell formation in diatoms. II. The structure of the cell wall of Navicula pelliculosa (Breb.) Hilse. J. Phycol. 2, 74-84
6. Schmid, A. M., Borowitzka, M. A., and Volcani, B. E. (1981) Morphogenesis and biochemistry of diatom cell walls, in Cytomorphogenesis in Plants (Kiermayer, O., ed) Vol. 8, pp. 63-97, Springer-Verlag, New York
7. Edgar, L. A., and Pickett-Heaps, J. D. (1984) Valve morphogenesis in the pennate diatom Navicula cuspidata. J. Phycol. 20, 47-61
8. Pickett-Heaps, J. D. (1983) Valve morphogenesis and the microtubule center in three species of the diatom Nitzschia. J. Phycol. 19, 269-281
9. Pickett-Heaps, J. D., and Kowalski, S. E. (1981) Valve morphogenesis and the microtubule center of the diatom Hantzschia amphioxysis. Eur J. Cell Biol. 25, 150-170
10. Pickett-Heaps, J. D., Tippit, D. H., and Andreozzi, J. A. (1979) Cell division in the pennate diatom Pinullaria. IV. Valve morphogenesis. Biol. Cell. 35, 199-206
11. Kröger, N., Bergsdorf, C., and Sumper, M. (1994) A new calcium-binding glycoprotein family constitutes a major diatom cell-wall component. EMBO J. 13, 4676-4683
12. Swift, D. M., and Wheeler, A. P. (1992) Evidence of an organic matrix from diatom biosilica. J. Phycol. 28, 202-209
13. Kröger, N., Bergsdorf, C., and Sumper, M. (1996) Frustulins: domain conservation in a protein family associated with diatom cell walls. Eur. J. Biochem. 239, 259-264
14. Kröger, N., Lorenz, S., Brunner, E., and Sumper, M. (2002) Self-assembly of highly phosphorylated silaffins and their function in biosilica morphogenesis. Science 298, 584-586
15. Kröger, N., Deutzmann, R., Bergsdorf, C., and Sumper, M. (2000) Species-specific polyamines from diatoms control silica morphology. Proc. Natl. Aced. Sci. U. S. A, 97, 14133-14138
16. Kröger, N., Deutzmann, R., and Sumper, M. (1999) Polycationic peptides from diatom biosilica that direct silica nanosphere formation. Science 286, 1129-1132
17. Kröger, N., Lehmann, G., Rachel, R., and Sumper, M. (1997) Characterization of a 200-kDa diatom protein that is specifically associated with a silica-based substructure of the cell wall. Eur. J. Biochem. 250, 99-105
18. Kröger, N., and Wetherbee, R. (2000) Pleuralins are involved in theca differentiation in the diatom Cylindrotheca fusiformis. Protist 151, 263-273
19. Kröger, N., Deutzmann, R., and Sumper, M. (2001) Silica-precipitating peptides from diatoms. The chemical structure of silaffin-1A from Cylindrotheca fusiformis. J. Biol. Chem. 276, 26066-26070
20. Poulsen, N., and Kröger, N. (2004) Silica morphogenesis by alternative processing of silaffins in the diatom Thalassiosira pseudonana. J. Biol. Chem. 279, 42993-42999
21. Kröger, N., and Sumper, M. (1998) Diatom cell wall proteins and the cell biology of silica biomineralization. Protist 149, 213-219
22. Poulsen, N., Sumper, M., and Kröger, N. (2003) Biosilica formation in diatoms: Characterization of native silaffin-2 and its role in silica morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 100, 12075-12080
23. Blank, G. S., and Sullivan, C. W. (1983) Diatom mineralization of silicic acid VI. The effects of microtubule inhibitors on silicic acid metabolism in Navicula saprophila. J. Phycol. 19, 39-44
24. Cohn, S. A., Nash, J., and Pickett-Heaps, J. D. (1989) The effect of drugs on diatom valve morphogenesis. Protoplasma 149, 130-143
25. Pickett-Heaps, J. (1998) Cell division and morphogenesis of the centric diatom Chaetoceros decipiens (Bacillariophyceae). II. Electron microscopy and a new paradigm for tip growth. J. Phycol 34, 995-1004
26. Schmid, A.-M. M. (1980) Valve morphogenesis in diatoms: a pattern-related filamentous system in pennates and the effect of APM, colchicine, and osmotic pressure. Nova Hedwigia 33, 811-847
27. van de Meene, A. M. L., and Pickett-Heaps, J. D. (2002) Valve morphogenesis in the centric diatom Proboscia alata Sundstrom. J. Phycol. 38, 351-363
28. van de Meene, A. M. L., and Pickett-Heaps, J. D. (2004) Valve morphogenesis in the centric diatom Rhizosolenia setigera (Bacillariophyceae, Centrales) and its taxonomic implications. Eur. J. Phycol. 39, 93-104
29. Schmid, A.-M., and Schulz, D. (1979) Wall morphogenesis in diatoms: deposition of silica by cytoplasmic vesicles. Protoplasma 100, 267-288
30. Schmid, A.-M. M., and Volcani, B. E. (1983) Wall morphogenesis in Coscinodiscus wailesii. I. Valve morphology and development of its architecture. J. Phycol. 19, 387-402
31. Sumper, M. (2002) A phase separation model for the nanopatterning of diatom biosilica. Science 295, 2430-2433
32. Armbrust, E., Berges, J., Bowler, C., Green, B., Martinez, D., Putnam, N., Zhou, S., Allen, A., Apt, K., Bechner, M., Brzezinski, M., Chaal, B., Chiovitti, A., Davis, A., Demarest, M., Detter, J., Glavina, T., Goodstein, D., Hadi, M., Hellsten, U., Hildebrand, M., Jenkins, B., Jurka, J., Kapitonov, V., Kröger, N., Lau, W., Lane, T., Larimer, F., Lippmeier, J., Lucas, S., Medina, M., Montsant, A., Obornik, M., Parker, M., Palenik, B., Pazour, G., Richardson, P., Rynearson, T., Saito, M., Schwartz, D., Thamatrakoln, K., Valentin, K., Vardi, A., Wilkerson, F., and Rokhsar, D. (2004) The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science 306, 79-86
33. Hildebrand, M., Dahlin, K., and Volcani, B. E. (1998) Characterization of a silicon transporter gene family in Cylindrotheca fusiformis: sequences, expression analysis, and identification of homologs in other diatoms. Mol. Gen. Genet. 260, 480-486
34. Hildebrand, M., Volcani, B. E., Gassmann, W., and Schroeder, J. I. (1997) A gene family of silicon transporters. Nature 385, 688-689
35. Coombs, J., Halicki, P. J., Holm-Hansen, O., and Volcani, B. E. (1967) Studies on the biochemistry and fine structure of silica shell formation in diatoms. Changes in concentration of nucleoside triphosphates during synchronized division of Cylindrotheca fusiformis Reimann and Lewin. Exp. Cell Res. 47, 302-314
36. Coombs, J., Halicki, P. J., Holm-Hansen, O., and Volcani, B. E. (1967) Studies on the biochemistry and fine structure of silica shell formation in diatoms. II. Changes in concentration of nucleoside triphosphates in silicon-starvation synchrony of Navicula pelliculosa (Breb.) Hilse. Exp. Cell Res. 47, 315-328
37. Darley, W. M., and Volcani, B. E. (1969) Role of silicon in diatom metabolism: a silicon requirement for deoxyribonucleic acid synthesis in the diatom Cylindrotheca fusiformis Reimann and Lewin. Exp. Cell Res. 58, 334-342
38. Lewin, J. C., Reimann, B. E. F., Busby, W. F., and Volcani, B. E. (1966) Silica shell formation in synchronously dividing diatoms, in Cell Synchrony: Studies in Biosynthetic Regulation (Cameron, I. L., and Padilla, G. M., eds) pp. 169-188, Academic Press Wrightsville, NC
39. Hildebrand, M., Higgins, D. R., Busser, K., and Volcani, B. E. (1993) Siliconresponsive cDNA clones isolated from the marine diatom Cylindrotheca fusitormis. Gene (Amst.) 132, 213-218
40. Reeves, C. D., and Volcani, B. E. (1985) Messenger RNA and polypeptide accumulation patterns in synchronized cultures of Cylindrotheca fusiformis. J. Gen. Microbio. 131, 1735-1744
41. Li, C.-W., Chu, S., and Lee, M. (1989) Characterizing the silicon deposition vesicle of diatoms. Protoplasma 151, 158-163
42. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal. Chem. 68, 850-858
43. Gharahdaghi, F., Weinberg, C. R., Meagher, D. A., Imai, B. S., and Mische, S. M. (1999) Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis 20, 601-605
44. Wilm, M., Shevchenko, A., Houthaeve, T., Breit, S., Schweigerer, L., Fotsis, T., and Mann, M. (1996) Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379, 466-469
45. Andon, N. L., Hollingworth, S., Koller, A., Greenland, A. J., Yates, J. R., III, and Haynes, P. A. (2002) Proteomic characterization of wheat amyloplasts using identification of proteins by tandem mass spectrometry. Proteomics, 2, 1156-1168
46. Carr, S., Aebersold, R., Baldwin, M., Burlingame, A., Clauser, K., and Nesvizhskii, A. (2004) The need for guidelines in publication of peptide and protein identification data. Working Group on Publication Guidelines for Peptide and Protein Identification Data. Moh Cell. Proteomics 3, 531-533
47. Eng, J., McCormack, A. L., and Yates, J. R., III (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Mass Spectrom. 5, 976-989
48. Yates, J. R., III, Eng, J. K., McCormack, A. L., and Schieltz, D. (1995) A method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal. Chem. 67, 1426-1436
49. Andon, N. L., Eckert, D., Yates, J. R., III and Haynes, P. A. (2003) High-throughput functional affinity purification of mannose binding proteins from Oryza sativa. Proteomics 3, 1270-1278
50. Breci, L., Hattrup, E., Keeler, M., Letarte, J., Johnson, R., and Haynes, P. A. (2005) Comprehensive proteomics in yeast using chromatographic fractionation, gas phase fractionation, protein gel electrophoresis, and isoelectric focusing. Proteomics 5, 2018-2028
51. Tabb, D. L., McDonald, W. H., and Yates, J. R., III (2002) DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1, 21-26
52. Hofmann, K., and Stoffel, W. (1993) TMbase - a database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler 374, 166
53. Lupas, A., Van Dyke, M., and Stock, J. (1991) Predicting coiled coils from protein sequences. Science 252, 1162-1164
54. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410
55. Hildebrand, M., and Dahlin, K. (2000) Nitrate transporter genes from the diatom Cylindrotheca fusiformis (Bacillariophyceae): mRNA levels controlled by nitrogen source and by the cell cycle. J. Phycol. 36, 702-713
56. Kakkar, R.K., and Sawhney, V.K. (2002) Polyamine research in plants - a changing perspective. Phys. Plant 116, 281-292
57. Milovic, V., Turchanowa, L., Khomutov, A. R., Khomutov, R. M., Caspary, W. F., and Stein, J. (2001) Hydroxylamine-containing inhibitors of polyamine biosynthesis and impairment of colon cancer cell growth. Biochem. Pharmacol. 61, 199-206
58. Tabor, C. W., and Tabor, H. (1984) Polyamines. Annu. Rev. Biochem. 53, 749-790
59. Futcher, B., Latter, G. I., Monardo, P., McLaughlin, C. S., and Garrels, J. I. (1999) A sampling of the yeast proteome. Mol. Cell. Biol. 19, 7357-7368
60. Stolc, V., Samanta, M. P., Tongprasit, W., Sethi, H., Liang, S. D., Nelson, D. C., Hegeman, A., Nelson, C., Rancour, D., Bednarek, S., Ulrich, E. L., Zhao, Q., Wrobel, R. L., Newman, C. S., Fox, B. G., Phillips, G. N., Markley, J. L., and Sussman, M. R. (2005) Identification of transcribed sequences in Arabidopsis thaliana by using high-resolution genome tiling arrays. Proc. Natl. Acad. Sci. U. S. A. 102, 4453-4458
61. Coluccio, L. M. (1997) Myosin I. Am. J. Physiol 273, C347-C359
62. Ostap, E. M., and Pollard, T. D. (1996) Overlapping functions of myosin-I isoforms? J. Cell Biol. 133, 221-224
63. King, S. M. (2000) The dynein microtubule motor. Biochim. Biophys. Acta 1496, 60-75
64. El Ghouzzi, V., Dagoneau, N., Kinning, E., Thauvin-Robinet, C., Chemaitilly, W., Prost-Squarcioni, C., Al-Gazall, L. I., Verloes, A., Le Merrer, M., Munnich, A., Trembath, R. C., and Cormier-Daire, V. (2003) Mutations in a novel gene Dymeclin (FLJ20071) are responsible for Dyggve-Melchior-Clausen syndrome. Hum. Mol. Genet. 12, 367-364
65. Frolich, K. U., Fries, H. W., Rudiger, M., Erdmann, R., Botstein, D., and Mecke, D. (1991) Yeast-cell cycle protein CDC48p shows full-length homology to the mammalian protein VCP and is a member of a protein family involved in secretion, peroxisome formation, and gene-expression. J. Cell Biol. 114, 443-453
66. Hirsch, C., Jarosch, E., Sommer, T., and Wolf, D. H. (2004) Endoplasmic reticulum-associated protein degradation-one model fits all? Biochim. Biophys. Acta 1695, 215-223
67. Jarosch, E., Geiss-Friedlander, R., Meusser, B., Walter, J., and Sommer, T. (2002) Protein dislocation from the endoplasmic reticulum - pulling out the suspect. Traffic 3, 530-536
68. Blatch, G. L., and Lassle, M. (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21, 932-939
69. Lamb, J. R., Tugendreich, S., and Hieter, P. (1995) Tetratricopeptide repeat interactions: to TPR or not to TPR? Trends Biochem. Sci. 20, 257-259
70. Drennan, D., and Ryazanov, A. G. (2004) α-Kinases: analysis of the family and comparison with conventional protein kinases. Prog. Biophys. Mol. Biol. 85, 1-32
71. de la Roche, M. A., and Cote, G. P. (2001) Regulation of Dictyostelium myosin I and II. Biochim. Biophys. Acta 1525, 245-261
72. Rawlings, N. D., Tolle, D. P., and Barrett, A. J. (2004) Evolutionary families of peptidase inhibitors. Biochern. J. 378, 705-716
73. Price, M. P., Thompson, R. J., Eshcol, J. O., Wemmie, J. A., and Benson, C. J. (2004) Stomatin modulates gating of acid-sensing ion channels. J. Biol. Chem. 279, 53886-53891
74. Snyers, L., ThinesSempoux, D., and Prohaska, R. (1997) Colocalization of stomatin (band 7.2b) and actin microfilaments in UAC epithelial cells. Eur. J. Cell Biol. 73, 281-285
75. McClung, J. K., Jupe, E. R, Liu, X. T., and Dellorco, R. T. (1995) Prohibitin-potential role in senescence, development, and tumor suppression. Exp. Gerontol. 30, 99-124
76. Snedden, W. A., and Fromm, H. (1997) Characterization of the plant homologue of prohibitin, a gene associated with antiproliferative activity in mammalian cells. Plant Mol. Biol. 33, 753-756
77. Arnold, I., and Langer, T. (2002) Membrane protein degradation by AAA proteases in mitochondria. Biochim. Biophys. Acta 1592, 89-96
78. Zurzolo, C., and Bowler, C. (2001) Exploring bioinorganic pattern formation in diatoms. A story of polarized trafficking. Plant Phys. 127, 1339-1345
79. Suzuki, H., Kamakura, M., Morii, M., and Takeguchi, N. (1997) The phospholipid flippase activity of gastric vesicles. J. Biol. Chem. 272, 10429-10434
80. Szyperski, T., Fernandez, C., Mumenthaler, C., and Wuthrich, K. (1998) Structure comparison of human glioma pathogenesis-related protein GliPR and the plant pathogenesis-related protein P14a indicates a functional link between the human immune systern and a plant defense system. Proc. Natl. Acad. Sci. U. S. A. 95, 2262-2266
81. Van Loon, L. C., and Van Strien, E. A. (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 55, 85-97
82. Hoagland, K. D., Rowoski, J. R., Gretz, M. R., and Roener, S. C. (1993) Diatom extracellular polymeric substances: function, fine structure, chemistry, and physiology. J. Phycol. 29, 537-566
83. Davis, A. K., Hildebrand, M., and Palenik, B. (2005) Characterization of a cell-surface protein associated with the girdle band region of the diatom Thalassiosira pseudonana. J. Phycol. 41, 577-589
84. Pintard, L., Willems, A., and Peter, M. (2004) Cullin-based ubiquitin ligases: Cul3-BTB complexes join the family. EMBO J. 23, 1681-1687
85. Mathias, N., Johnson, S. L., Winey, M., Adams, A. E., Goetsch, L., Pringle, J. R., Byers B., and Goebl, M. G. (1996) Cdc53p acts in concert with Cdc4p and Cdc34p to control the G1-to-S-phase transition and identities a conserved family of proteins. Mol. Cell. Biol. 16, 6634-6643
86. Kipreos, E. T., Lander, L. E., Wing, J. P., He, W. W., and Hedgecock, E. M. (1996) cul-1 is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell 85, 829-839
87. Bumatowska-Hledin, M. A., Spielman, W. S., Smith, W. L., Shi, P., Meyer, J. M., and Dewitt, D. L. (1995) Expression cloning of an AVP-activated, calcium-mobilizing receptor from rabbit kidney medulla. Am. J. Phys. 268, F1198-F1210
88. Hildebrand, M., and Wetherbee, R. (2003) Components and control of silicification indiatoms, in Progress in Molecular and Subcellular Biology: Silicon Biomineralization (Muller, W. E. G., ed) Vol. 33, pp. 11-57, Springer-Verlag, Heidelberg, Germany
89. Falciatore, A., Casotti, R., Leblanc, C., Abrescia, C., and Bowler, C. (1999) Transformation of nonselectable reporter genes in marine diatoms. Mar. Biotechnol 1, 239-251
90. Fischer, H., Robl, I., Sumper, M., and Kröger, N. (1999) Targeting and covalent modification of cell wall and membrane proteins heterologously expressed in the diatom Cylindrotheca fusiformis (Bacillariophyceae). J. Phycol. 35, 113-120
91. Apt, K. E., Kroth-Pancic, P. G., and Grossman, A. R. (1996) Stable nuclear transformation of the diatom Phaeodactylum tricomutum. Mol. Gen. Genet. 252, 572-579
92. Dunahay, T. G., Jarvis, E. E., and Roessler, P. G. (1995) Genetic transformation of the diatoms Cyclotella cryptica and Navicula seprophila. J. Phycol. 31, 1004-1012
93. Zaslavskaia, L. A., Lippmeier, J. C., Kroth, P. G., Grossman, A. R., and Apt, K. E. (2000) Transformation of the diatom Phaeodactylum tricomutum with a variety of selectable marker and reporter genes. J. Phycol. 36, 379-386