Post-transcriptional regulation of S-Phase genes in the dinoflagellate, karenia brevis

Journal of Eukaryotic Microbiology

Volumn 58, Issue 4, 2011, Pages 373-382

  Brunelle, Stephanie A ^a,b   Van Dolah, Frances M ^a,b  

^a CENTER FOR COASTAL ENVIRONMENTAL HEALTH AND BIOMOLECULAR RESEARCH   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Cell cycle; dinoflagellate; Karenia brevis; PCNA; post transcriptional regulation; S phase

Indexed keywords

CELL CYCLE PROTEIN; CYCLINE; MESSENGER RNA; PROTOZOAL PROTEIN; REPLICATION FACTOR A; REPLICATION FACTOR C; RIBONUCLEOTIDE REDUCTASE; TRANSCRIPTION FACTOR E2F;

BIOMARKER; CELL ORGANELLE; DINOFLAGELLATE; ENZYME ACTIVITY; GENE EXPRESSION; MOLECULAR ANALYSIS; POLYMERASE CHAIN REACTION; PROTEIN; QUANTITATIVE ANALYSIS; RED TIDE; STABILIZATION; TOXICITY;

ALGAL BLOOM; ARTICLE; BIOSYNTHESIS; CELL CYCLE S PHASE; CYTOLOGY; DINOFLAGELLATE; FLOW CYTOMETRY; GENE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROTEIN SYNTHESIS;

CELL CYCLE PROTEINS; DINOFLAGELLIDA; E2F TRANSCRIPTION FACTORS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENES, PROTOZOAN; HARMFUL ALGAL BLOOM; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BIOSYNTHESIS; PROTOZOAN PROTEINS; REPLICATION PROTEIN A; REPLICATION PROTEIN C; RIBONUCLEOTIDE REDUCTASES; RNA, MESSENGER; S PHASE; TRANSCRIPTION, GENETIC;

ATLANTIC OCEAN; GULF OF MEXICO;

DINOPHYCEAE; EUKARYOTA; KARENIA BREVIS; TRYPANOSOMA;

EID: 79960462848     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/j.1550-7408.2011.00560.x     Document Type: Article

References (52)

1. Archer, S. K., Luu, V. D., de Queiroz, R. A., Brems, S., &, Clayton, C., 2009. Trypanosoma brucei PUF9 regulates mRNAs for proteins involved in replicative processes over the cell cycle. PLoS Pathogens, 5: e1000565.
2. Bachvaroff, T. R., &, Place, A. R., 2008. From stop to start: tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellate Amphidinium carterae. PLoS ONE, 3: e2929.
3. Barbier, M., Leighfield, T. A., Soyer-Gobillard, M., &, Van Dolah, F. M., 2003. Permanent expression of a cyclin B homologue in the cell cycle of the dinoflagellate Karenia brevis. J. Eukaryot. Microbiol., 50: 123-131. (Pubitemid 36524600)
4. Bertomeu, T., &, Morse, D., 2004. Isolation of a dinoflagellate mitotic cyclin by functional complementation in yeast. Biochem. Biophys. Res. Comm., 323: 1172-1183. (Pubitemid 39296548)
5. Bertomeu, T., Rivoal, J., &, Morse, D., 2007. A dinoflagellate CDK5-like cyclin-dependent kinase. Biol. Cell, 99: 531-540. (Pubitemid 47365610)
6. Bradford, M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Ann. Biochem., 72: 248-254.
7. Brown, L. M., &, Ray, D. S., 1997. Cell cycle regulation of RPA1 transcript levels in the trypanosomatid Crithidia fasciculata. Nucleic Acids Res., 25: 3281-3289. (Pubitemid 27338688)
8. Brunelle, S. A., 2005. Circadian control in the dinoflagellate Karenia brevis: a role for blue light and characteristics of a blue light receptor. Masters Thesis, College of Charleston, Charleston, SC. 80 p.
9. Brunelle, S., Hazard, E. S., Sotka, E. E., &, Van Dolah, F. M., 2007. Characterization of a dinoflagellate cryptochrome blue-light receptor with a possible role in circadian control of the cell cycle. J. Phycol., 43: 509-518. (Pubitemid 46800436)
10. Chabes, A., &, Thelander, L., 2000. Controlled protein degradation regulates ribonucleotide reductase activity in proliferating mammalian cells during the normal cell cycle and in response to DNA damage and replication blocks. J. Biol. Chem., 275: 17747-17753. (Pubitemid 30430824)
11. Chabes, A. L., Pfleger, C. M., Kirschner, M. W., &, Thelander, L., 2003. Mouse ribonucleotide reductase R2 protein: a new target for anaphase-promoting complex-Cdh1-mediated proteolysis. Proc. Natl. Acad. Sci. USA, 100: 3925-3929. (Pubitemid 36418133)
12. Colby, T., Matthai, A., Boeckelmann, A., &, Stuible, H. P., 2006. SUMO-conjugating and SUMO-deconjugating enzymes from Arabidopsis. Plant Physiol., 142: 318-332. (Pubitemid 44412250)
13. Costas, E., &, Goyanes, V., 2005. Architecture and evolution of dinoflagellate chromosomes: an enigmatic origin. Cytogenet. Genome Res., 109: 268-275. (Pubitemid 40470332)
14. Essers, J., Theil, A. F., Baldeyron, C., van Cappellen, W. A., Houtsmuller, A. B., Kanaar, R., &, Vermeulen, W., 2005. Nuclear dynamics of PCNA in DNA replication and repair. Mol. Cell. Biol., 25: 9350-9359. (Pubitemid 41507836)
15. Fagan, T., Morse, D., &, Hastings, J. W., 1999. Circadian synthesis of a nuclear-encoded chloroplast glyceraldehyde-3-phosphate dehydrogenase in the dinoflagellate Gonyaulax polyedra is translationally controlled. Biochemistry, 38: 7689-7695.
16. Gardner, M. G., Bishop, R., Shah, T., de Villiers, E. P., Carlton, J. M., Hall, N., Ren, Q., Paulsen, I. T., Pain, A., Berriman, B., Wilson, R. J. M., Sato, S., Ralph, S. A., Mann, D. J., Xiong, Z., Shallom, S. J., Weidman, J., Jiang, L., Lynn, J., Weaver, B., Shoaibi, A., Domingo, A. R., Wasawo, D., Crabtree, J., Wortman, J. R., Haas, B., Angiuoli, S. V., Creasy, T. H., Lu, C., Suh, B., Silva, J. C., Utterback, T. R., Feldblyum, T. V., Pertea, M., Allen, J., Nierman, W. C., Taracha, E. L. N., Salzberg, S. L., White, O. R., Fitzhugh, H. A., Morzaria, S., Venter, J. C., Fraser, C. M., &, Nene, V., 2005. Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science, 309: 134-137. (Pubitemid 40934992)
17. Guillard, R. R. L., 1973. Division rates. In:, Stein, J. R., (ed.), Handbook of Phycological Methods: Culture Methods and Growth Measurements. Cambridge University Press, Cambridge, UK. p. 289-311.
18. Haracska, L., Torres-Ramos, C. A., Johnson, R. E., Prakash, S., &, Prakash, L., 2004. Opposing effects of ubiquitin conjugation and SUMO modification of PCNA on replicational bypass of DNA lesions in Saccharomyces cerevisiae. Mol. Cell. Biol., 24: 4267-4274. (Pubitemid 41070998)
19. Hoege, C., Pfander, B., Moldovan, G. L., Pyrowolakis, G., &, Jentsch, S., 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature, 419: 135-141. (Pubitemid 35025438)
20. Hou, Y., &, Lin, S., 2009. Distinct gene number-genome size relationships for eukaryotes and non-eukaryotes: gene content estimation for dinoflagellate genomes. PLoS ONE, 4: e6978.
21. Huysman, M. J. J., Maretns, C., Vandepoele, K., Gillard, J., Rayco, E., Heijde, M., Bowler, C., Inze, D., van de Peer, Y., Veylder, L., &, Vyverman, W., 2010. Genome-wide analysis of the diatom cell cycle unveils a novel type of cyclins involved in environmental signaling. Genome Biol., 11: 1-19.
22. Jensen, L. J., Jensen, T. S., de Lichtenberg, U., Brunak, S., &, Bork, P., 2006. Co-evolution of transcriptional and post-translational cell-cycle regulation. Nature, 443: 594-597. (Pubitemid 44527297)
23. Kumar, D., Minocha, N., Rajanala, K., &, Saha, S., 2009. The distribution pattern of proliferating cell nuclear antigen in the nuclei of Leishmania donovani. Microbiology, 155: 3748-3757.
24. Le, Q. H., Jovine, R., Markovic, P., &, Morse, D., 2001. Peridinin-chlorophyll a protein is not implicated in the photosynthesis rhythm of the dinoflagellate Gonyaulax despite circadian regulation of its translation. Biol. Rhythm Res., 32: 579-594. (Pubitemid 34025281)
25. Le, Q. H., Markovic, P., Hastings, J. W., Jovine, R. V. M., &, Morse, D., 1997. Structure and organization of the peridinin chlorophyll a binding protein gene in Gonyaulax polyedra. Mol. Gen. Genet., 255: 595-604.
26. Lidie, K. B., &, Van Dolah, F. M., 2007. Spliced leader RNA-mediated trans-splicing in a dinoflagellate, Karenia brevis. J. Eukaryot. Microbiol., 54: 427-435. (Pubitemid 47512290)
27. Lidie, K. B., Ryan, J. C., Barbier, M., &, Van Dolah, F. M., 2005. Gene expression in Florida red tide dinoflagellate Karenia brevis: analysis of an expressed sequence tag library and development of DNA microarray. Mar. Biotechnol., 7: 481-493. (Pubitemid 41551341)
28. Lin, S., Zhang, H., Zhuang, Y., Tran, B., &, Gill, J., 2010. Spliced leader-based metatranscriptiomic analyses lead to recognition of hidden genomic features in dinoflagellates. Proc. Natl. Acad. Sci. USA, 107: 20033-20038.
29. Liu, J., Jiao, N., Hong, H., Luo, T., &, Cai, H., 2005. Proliferating cell nuclear antigen (PCNA) as a marker of cell proliferation in the marine dinoflagellate Prorocentrum donghaiense Lu and the green alga Dunaliella salina Teodoresco. J. Appl. Phycol., 17: 323-330. (Pubitemid 41168319)
30. Liu, L. Y., &, Hastings, J. W., 2006. Novel and rapidly diverging intergenic sequences between tandem repeats of the luciferase genes in seven dinoflagellate species. J. Phycol., 42: 96-103.
31. Mittag, M., Li, L., &, Hastings, J. W., 1998. The mRNA level ofcircadian regulated Gonyaulax luciferase remains constant over the cycle. Chronobiol. Int., 15: 93-8. (Pubitemid 28077921)
32. Morse, D., Milos, P. M., Roux, E., &, Hastings, J. W., 1989. Circadian regulation of bioluminescence in Gonyaulax involves translational control. Proc. Natl. Acad. Sci. USA, 86: 172-176.
33. Murphy, W. J., Watkins, K. P., &, Agabian, N., 1986. Identification of a novel Y branch structure as an intermediate in trypanosome mRNA processing: evidence for trans-splicing. Cell, 47: 517-525. (Pubitemid 17215343)
34. Nassoury, N., Fritz, L., &, Morse, D., 2001. Circadian changes in ribulose-1,5-bisphosphate carboxylase/oxygenase distribution inside individual chloroplasts can account for the rhythm in dinoflagellate carbon fixation. Plant Cell, 13: 923-934. (Pubitemid 32375910)
35. Parker, J. L., Bucceri, A., Davies, A. A., Heidrich, K., Windecker, H., &, Ulrich, H. D., 2008. SUMO modification of PCNA is controlled by DNA. EMBO J., 27: 2422-2431.
36. Reichard, P., 1993. From RNA to DNA: why so many ribonucleotide reductases? Science, 260: 1773-1777. (Pubitemid 23244202)
37. Robbens, S., Khadaroo, B., Camasses, A., Derelle, E., Ferraz, C., Inze, D., Van de Peer, Y., &, Moreau, H., 2005. Genomi-wide analysis of core cell-cycle genes in the unicellular green alga, Ostreococcus tauri. Mol. Biol. Evol., 22: 589-597. (Pubitemid 40299508)
38. Rustici, G., Mata, J., Kivinen, K., Lio, P., Penkett, C. J., Burns, G., Hayles, J., Brazma, A., Nurse, P., &, Bahler, J., 2004. Periodic gene expression program of the fission yeast cell cycle. Nat. Genet., 36: 809-817. (Pubitemid 39014097)
39. Spellman, P. T., Sherlock, G., Zhang, M. Q., Iyer, V. R., Anders, K., Eisen, M. B., Brown, P. O., Botstein, D., &, Futcher, B., 1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell., 9: 3273-3297. (Pubitemid 28551928)
40. Steidinger, K. A., Vargo, G. A., Tester, P. A., &, Tomas, C. R., 1998. Bloom dynamics and physiology of Gymnodinium breve with emphasis on the Gulf of Mexico. In:, Anderson, D. M., Cembella, A. D., &, Hallegraeff, G. M., (ed.), Physiological Ecology of Harmful Algal Blooms. Springer-Verlag, Berlin. p. 133-153.
41. ten Lohuis, M. R., &, Miller, D. J., 1998. Light-regulated transcription of genes encoding peridinin chlorophyll a proteins and the major intrinsic light-harvesting complex proteins in the dinoflagellate Amphidinium carterae (Dinophyceae). Plant Physiol., 117: 189-196. (Pubitemid 128652792)
42. Toulza, E., Shin, M., Blanc, G., Audic, S., Laabir, M., Collos, Y., Claverie, J., &, Grzebyk, D., 2010. Transcriptome of proliferating Alexandrium cells. Appl. Environ. Microbiol., 76: 4521-4529.
43. Trachana, K., Jensen, L. J., &, Bork, P., 2010. Evolution and regulation of cellular periodic processes: a role for paralogs. EMBO Rep., 11: 233-238.
44. Umen, J. G., &, Goodenough, U. W., 2001. Control of cell division by a retinoblastoma protein homolog in Chlamydomonas. Gene. Dev., 15: 1652-1661. (Pubitemid 32702587)
45. Van Dolah, F. M., &, Leighfield, T. A., 1999. Diel phasing of the cell-cycle in the Florida red-tide dinoflagellate, Gymnodinium breve. J. Phycol., 35: 1404-1411. (Pubitemid 30049443)
46. Van Dolah, F. M., Lidie, K., Morey, J., Brunelle, S., Ryan, J., Monroe, E., &, Haynes, B., 2007. Microarray analysis of diurnal and circadian regulated genes in the Florida red-tide dinoflagellate, Karenia brevis. J. Phycol., 43: 741-752. (Pubitemid 47196282)
47. Vanhamme, L., &, Pays, E., 1995. Control of gene expression in trypanosomes. Microbiol. Rev., 59: 223-240.
48. Zhang, H., &, Lin, S., 2003. Complex gene structure of the form II Rubisco in the dinoflagellate Prorocentrum minimum (Dinophyceae). J. Phycol., 39: 1160-1171. (Pubitemid 38012648)
49. Zhang, H., Hou, Y., &, Lin, S., 2006a. Isolation and characterization of proliferating cell nuclear antigen from the dinoflagellate Pfiesteria piscicida. J. Eukaryot. Microbiol., 53: 142-150.
50. Zhang, H., Hou, Y., Miranda, L., Campbell, D. A., Sturm, N. R., Gaasterland, T., &, Lin, S., 2007. Spliced leader RNA trans-splicing in dinoflagellates. Proc. Natl. Acad. Sci. USA, 104: 4618-4623. (Pubitemid 47186274)
51. Zhang, Z., An, X., Yang, K., Perlstein, D. L., Hicks, L., Kelleher, N., Stubbe, J., &, Huang, M., 2006b. Nuclear localization of the Saccharomyces cerevisiae ribonucleotide reductase small subunit requires a karyopherin and a WD40 repeat protein. Proc. Natl. Acad. Sci. USA, 103: 1422-1427. (Pubitemid 43191181)
52. Zick, A., Onn, I., Bezalel, R., Margalit, H., &, Schlomai, J., 2005. Assigning functions to genes: identification of S-phase expressed genes in Leishmania major based on post-transcriptional control elements. Nucleic Acids Res., 33: 4235-4242. (Pubitemid 41487282)