Elucidating the biochemical overwintering adaptations of larval Cucujus clavipes puniceus, a nonmodel organism, via high throughput proteomics

Journal of Proteome Research

Volumn 10, Issue 10, 2011, Pages 4634-4646

  Carrasco, Martin A ^a   Buechler, Steven A ^a   Arnold, Randy J ^b   Sformo, Todd ^c   Barnes, Brian M ^c   Duman, John G ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF ALASKA FAIRBANKS   (United States)

Author keywords

beetle; Cucujus clavipes; freeze avoiding; high throughput; low temperature biology; nonmodel organism; proteomics

Indexed keywords

2 ISOPROPYLMALATE SYNTHASE; ACTIN; ACYLTRANSFERASE; ALPHA ACTININ; CYTOCHROME C OXIDASE; CYTOSKELETON PROTEIN; DIHYDROFOLATE REDUCTASE; PROTEOME; TROPOMYOSIN; TUBULIN; ZINC FINGER PROTEIN;

ADAPTATION; ARTICLE; BEETLE; CATALYSIS; COLD TOLERANCE; CONTROLLED STUDY; CUCUJUS CLAVIPES PUNICEUS; CYTOSKELETON; ENZYME SUBSTRATE; FOREST; HIGH THROUGHPUT SCREENING; LARVA; LOW TEMPERATURE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEOMICS; SEASONAL VARIATION; SUMMER; TANDEM MASS SPECTROMETRY; UNITED STATES; UPREGULATION; WINTER; ZINC FINGER MOTIF;

ACCLIMATIZATION; ACTININ; ANIMALS; BEETLES; BIOCHEMISTRY; COLD TEMPERATURE; FREEZING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; TANDEM MASS SPECTROMETRY; TROPOMYOSIN; TUBULIN; UP-REGULATION;

COLEOPTERA; CUCUJUS CLAVIPES;

EID: 80053896193     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200518y     Document Type: Article

References (41)

1. Bennett, V. A.; Sformo, T.; Walters, K.; Toien, O.; Jeannet, K.; Hochstrasser, R.; Pan, Q.; Serriani, A. S.; Barnes, B. M.; Duman, J. G. Comparative overwintering physiology of Alaska and Indiana populations of the beetle Cucujus clavipes (Fabricius): roles of antifreeze proteins, polyols, dehydration and diapause J. Exp. Biol. 2005, 208, 4467-77 (Pubitemid 43028110)
2. Sformo, T.; Walters, K.; Jeannet, K.; Wowk, B.; Fahy, G. M.; Barnes, B. M.; Duman, J. G. Deep supercooling, vitrification and limited survival to -100°C in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae) larvae J. Exp. Biol. 2010, 213, 502-9
3. Walters, K. R.; Serianni, A. S.; Voituron, Y.; Sformo, T.; Barnes, B. M.; Duman, J. G. A thermal hysteresis-producing xylomannan glycolipid antifreeze associated with cold tolerance is found in diverse taxa J. Comp. Physiol. B 2011, 181 (5) 631-40
4. Shevchenko, A.; Sunyaev, S.; Loboda, A.; Shevchenko, A.; Bork, P.; Ens, W.; Standing, K. G. Charting the Proteomes of Organisms with Unsequenced Genomes by MALDI-Quadrupole Time-of-Flight Mass Spectrometry and BLAST Homology Searching Anal. Chem. 2001, 73, 1917-26 (Pubitemid 32862395)
5. Guercio, R. A. P.; Shevchenko, A.; Shevchenko, A.; Lozano, J. L. L.; Paba, J.; Sousa, M. V.; Ricart, C. A. O. Ontogenetic variations in the venom proteome of the Amazonian snake Bothrops atrox Proteome Sci. 2006, 4, 11-25
6. Behr, J.; Israel, L.; Ganzle, M. G.; Vogel, R. F. Proteomic Approach for Characterization of Hop-Inducible Proteins in Lactobacillus brevis Appl. Environ. Microb. 2007, 73, 3300-6 (Pubitemid 46834982)
7. Samyn, B.; Sergeant, K.; Carpentier, S.; Debyser, G.; Panis, B.; Swennen, R.; Beeumen, J. V. Functional Proteome Analysis of the Banana Plant (Musa spp.) Using de Novo Sequence Analysis of Derivatized Peptides J. Proteome Res. 2007, 6, 70-80 (Pubitemid 46173660)
8. Tannu, N. S.; Hemby, S. E. De novo protein sequence analysis of Macaca mulatta BMC Genomics 2007, 8, 270-9
9. Waridel, P.; Frank, A.; Thomas, H.; Surendranath, V.; Sunyaev, S.; Pevzner, P.; Shevchenko, A. Sequence similarity-driven proteomics in organisms with unknown genomes by LC-MS/MS and automated de novo sequencing Proteomics 2007, 7, 2318-29 (Pubitemid 47121523)
10. Junqueira, M.; Spirin, V.; Balbuena, T. S.; Thomas, H.; Adzhubei, I.; Sunyaev, S.; Shevshenko, A. Protein identification pipeline for the homology driven proteomics J. Proteomics 2008a, 71, 346-56
11. Junqueria, M.; Spirin, V.; Balbuena, T. S.; Waridel, P.; Surendranath, V.; Kryukov, G.; Adzhubei, I.; Thomas, H.; Sunyaev, S.; Shevchenko, A. Separating the Wheat from the Chaff: Unbiased Filtering of Background Tandem Mass Spectra Improves Protein Identification J. Proteome Res. 2008b, 7, 3382-95
12. Wielsch, N.; Thomas, H.; Surendranath, V.; Waridel, P.; Frank, A.; Pevzner, P.; Shevchenko, A. Rapid Validation of Protein Identifications with the Borderline Statistical Confidence via De Novo Sequencing and MS BLAST Searches J. Proteome Res. 2006, 5, 2448-56 (Pubitemid 44330839)
13. Grossman, J.; Fischer, B.; Baerenfaller, K.; Owiti, J.; Buhmann, J. M.; Gruissem, W.; Baginsky, S. A workflow to increase the detection rate of proteins from unsequenced organisms in high-throughput proteomics experiments Proteomics 2007, 7, 4245-54 (Pubitemid 350250470)
14. Samyn, B.; Sergeant, K.; Memmi, S.; Debyser, G.; Devreese, B.; Beeuman, J. V. MALDI-TOF/TOF de novo sequence analysis of 2-D PAGE-separated proteins from Halorhodospira halophila, a bacterium with unsequenced genome Electrophoresis 2006, 27, 2702-11 (Pubitemid 44069409)
15. Denlinger, D.L.; Lee, R. E. Low Temperature Biology of Insects; Cambridge University Press: New York, 2010.
16. Colinet, H.; Nguyen, T. T. A.; Cloutier, C.; Michaud, D.; Hance, T. Proteomic profiling of a parasitic wasp exposed to constant and fluctuating cold exposure Insect Biochem. Molec. 2007, 37, 1177-88 (Pubitemid 47488878)
17. Li, A. Q.; Butler, A. P.; Dean, D. H.; Denlinger, D. L. Proteomics of the flesh fly brain reveals an abundance of upregulated heat shock proteins during pupal diapause J. Insect Physiol. 2007, 53, 385-91 (Pubitemid 46498096)
18. Li, A.; Denlinger, D. L. Rapid cold hardening elicits changes in brain protein profiles of the flesh fly, Sarcophaga crassipalpis Insect Mol. Biol. 2008, 17, 565-72
19. Williams, K. R.; Stone, K. L. In gel digestion of SDS PAGE-separated Proteins: Observations from internal sequencing of 25 proteins. In Techniques in Protein Chemistry VI; Crabb, J. W., Ed.; Academic Press: Orlando, 1995; pp 143-52.
20. Perkins, D.; Pappin, D.; Creasy, D.; Cottrell, J. Probability-based protein identification by searching sequence databases using mass spectrometry data Electrophoresis 1999, 20, 3551-67 (Pubitemid 30007252)
21. Standing, K. G. Peptide and protein de novo sequencing by mass spectrometry Curr. Opin. Struct. Biol. 2003, 13, 595-601 (Pubitemid 37244114)
22. Pevtsov, S.; Fedulova, I.; Mirzai, H.; Buck, C.; Zhang, X. Performance Evaluation of Existing De Novo Sequencing Algorithms J. Proteome Res. 2006, 5, 3018-28 (Pubitemid 44754676)
23. Pitzer, E.; Masselot, A.; Colinge, J. Assessing peptide de novo sequencing algorithms performance on large and diverse data sets Proteomics 2007, 7, 3051-4 (Pubitemid 47477949)
24. Frank, A.; Pevzner, P. PepNovo: De Novo Peptide Sequencing via Probabilistic Network Modeling Anal. Chem. 2005, 77, 964-73 (Pubitemid 40261761)
25. Mackey, A. J.; Haystead, T. A. J.; Pearson, W. R. Getting More from Less Mol. Cell. Proteomics 2002, 1, 139-47
26. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 2007, 4, 207-14 (Pubitemid 46358868)
27. Shao, C.; Liu, Y.; Ruan, H.; Li, Y.; Wang, H.; Kohl, F.; Goropashnaya, A. V.; Fedorov, V. B.; Zeng, R.; Barnes, B. M.; Yan, J. Shotgun Proteomic Analysis of Hibernating Arctic Ground Squirrel Mol. Cell. Proteomics 2010, 9, 313-26
28. Liu, H.; Sadygov, R. G.; Yates, J. R. A model for Random Sampling and Estimation of Relative Protein Abundance in Shotgun Proteomics Anal. Chem. 2004, 76, 4193-201 (Pubitemid 38943698)
29. Mueller, L. N.; Brusniak, M. Y.; Mani, D. R.; Aebersold, R. An Assessment of Software Solutions for the Analysis of Mass Spectrometry Based Quantitative Proteomics Data J. Proteomics Res. 2008, 7, 51-61 (Pubitemid 351171115)
30. Carvalho, P. C.; Hewel, J.; Barbosa, V. C.; Yates, J. R. Identifying differences in protein expression levels by spectral counting and feature selection Genet. Mol. Res. 2008, 7, 342-56
31. Choi, H.; Fermin, D.; Nesvizhskii, A. I. Significance Analysis of Spectral Count Data in Label-free Shotgun Proteomics Mol. Cell. Proteomics 2008, 7, 2373-85
32. Li, M.; Gray, W.; Zhang, H.; Chung, C. H.; Billheimer, D.; Yarbrough, W. G.; Liebler, D. C.; Shyr, Y.; Slebos, R. J. C. Comparative Shotgun Proteomics Using Spectral Count Data and Quasi-Likelihood Modeling J. Proteome Res. 2010, 9, 4295-305
33. Heinecke, N. L.; Pratt, B. S.; Vaisar, T.; Becker, L. PepC: proteomics software for identifying differentially expressed proteins based on spectral counting Bioinformatics 2010, 26, 1574-5
34. Qin, W.; Neal, S. J.; Robertson, R. M.; Westwood, J. T.; Walker, V. K. Cold hardening and transcriptional change in Drosophila melanogaster Insect Mol. Biol. 2005, 14, 607-13 (Pubitemid 44914743)
35. Kim, M.; Robich, R. M.; Rinehart, J. P.; Denlinger, D. L. Upregulation of two actin genes and redistribution of actin during diapause and cold stress in the northern house mosquito, Culex pipiens J. Insect Physiol. 2006, 52, 1226-33 (Pubitemid 44750002)
36. Robich, R. M.; Rinehart, J. P.; Li, A. Q.; Kitchen, L. J.; Denlinger, D. L. Diapause-specific gene expression in the northern house mosquito, Culex pipiens L., identified by suppressive subtractive hybridization J. Insect Physiol. 2007, 53, 235-45 (Pubitemid 46349109)
37. Oono, Y.; Seki, M.; Satou, M.; Iida, K.; Akiyama, K.; Sakurai, T.; Fujita, M.; Shinozaki, K. Y.; Shinozaki, K. Monitoring expression profiles of Arabidopsis genes during cold acclimation and deacclimation using DNA microarrays Funct. Integr. Genomics 2006, 6, 212-34 (Pubitemid 43885070)
38. Zhang, J.; Goyer, C.; Pelletier, Y. Environmental stresses induce the expression of putative glycine rich insect cuticular protein genes in adult Leptinotarsa decemlineata (Say) Insect Mol. Biol. 2008, 17, 209-16 (Pubitemid 351677469)
39. Liu, X.; Kim, C. N.; Yang, J.; Jemmerson, R.; Wang, X. Induction of Apoptotic Program in Cell-Free Extracts: Requirements for dATP and Cytochrome c Cell 1996, 86, 147-57 (Pubitemid 26256586)
40. Cai, Q.; Greenway, S. C.; Storey, K. B. Differential regulation of the mitochondrial ADP/ATP tranlocase gene in wood frogs under freezing stress Biochim. Biophys. Acta 1997, 1351, 69-78 (Pubitemid 27315925)
41. Havlicková, V.; Kaplanová, V.; Nůsková, H.; Drahota, Z.; Houštěk, J. Knockdown of F1 epsilon subunit decreases mitochondrial content of ATP synthase and leads to accumulation of subunit c Biochim. Biophys. Acta 2010, 1797, 1124-9