Dynamics of zebrafish fin regeneration using a pulsed SILAC approach

Proteomics

Volumn 15, Issue 4, 2015, Pages 739-751

  Nolte, Hendrik ^a,c   Hölper, Soraya ^a   Housley, Michael P ^a   Islam, Shariful ^a   Piller, Tanja ^a   Konzer, Anne ^b   Stainier, Didier Y R ^a   Braun, Thomas ^a   Krüger, Marcus ^a,c  

^a MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Actinodin; Fin regeneration; Quantitative tissue proteomics; SILAC; Zebrafish

Indexed keywords

BINDING PROTEIN; BRG1 PROTEIN; CARBON 13; COLLAGEN; DISULFIDE; DNA BINDING PROTEIN; FIBRONECTIN; FIBRONECTIN 1B; HIGH MOBILITY GROUP PROTEIN; HISTONE; INTERLEUKIN ENHANCER BINDING PROTEIN 2; LIGAND; LUNG RESISTANCE PROTEIN; LYSINE; MATRILYSIN; MATRIN 3; MESSENGER RNA; NUCLEAR MATRIX PROTEIN; OXIDOREDUCTASE; PROSTAGLANDIN REDUCTASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); STABLE ISOTOPE; TAX PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; UNCLASSIFIED DRUG; ZEBRAFISH PROTEIN; PROTEOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS MATRIX; CELL PROLIFERATION; CELL STRESS; CONTROLLED STUDY; DISULFIDE BOND; DNA BINDING; DNA BINDING MOTIF; DNA PROTEIN COMPLEX; DROSOPHILA; ELECTROSPRAY MASS SPECTROMETRY; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; FIN (ORGAN); GENE EXPRESSION; GENE EXPRESSION PROFILING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IN SITU HYBRIDIZATION; INTRACELLULAR SPACE; ISOTOPE LABELING; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN GLYCOSYLATION; PROTEIN MICROARRAY; PROTEIN SYNTHESIS; PULSED SILAC; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SKIN DEFECT; TANDEM MASS SPECTROMETRY; TIME; TISSUE REGENERATION; WNT SIGNALING PATHWAY; YEAST; ZEBRA FISH; ANIMAL; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PROTEOMICS; REGENERATION; WOUND HEALING;

ACTINOTRICHIA; DANIO RERIO;

ANIMAL FINS; ANIMALS; GENE EXPRESSION REGULATION; ISOTOPE LABELING; POLYMERASE CHAIN REACTION; PROTEOME; PROTEOMICS; REGENERATION; TANDEM MASS SPECTROMETRY; WOUND HEALING; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84922790826     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201400316     Document Type: Article

References (42)

1. Gemberling, M., Bailey, T. J., Hyde, D. R., Poss, K. D., The zebrafish as a model for complex tissue regeneration. Trends Genet. 2013, 29, 611-620.
2. Nechiporuk, A., Poss, K. D., Johnson, S. L., Keating, M. T., Positional cloning of a temperature-sensitive mutant emmental reveals a role for sly1 during cell proliferation in zebrafish fin regeneration. Dev. Biol. 2003, 258, 291-306.
3. Goss, R. J., Stagg, M. W., The regeneration of fins and fin rays in Fundulus heteroclitus. J. Exp. Zool. 1957, 136, 487-507.
4. Laforest, L., Brown, C. W., Poleo, G., Geraudie, J. et al., Involvement of the sonic hedgehog, patched 1 and bmp2 genes in patterning of the zebrafish dermal fin rays. Development 1998, 125, 4175-4184.
5. Grotek, B., Wehner, D., Weidinger, G., Notch signaling coordinates cellular proliferation with differentiation during zebrafish fin regeneration. Development 2013, 140, 1412-1423.
6. Blum, N., Begemann, G., Retinoic acid signaling controls the formation, proliferation and survival of the blastema during adult zebrafish fin regeneration. Development 2012, 139, 107-116.
7. Whitehead, G. G., Makino, S., Lien, C. L., Keating, M. T., fgf20 is essential for initiating zebrafish fin regeneration. Science 2005, 310, 1957-1960.
8. Stoick-Cooper, C. L., Weidinger, G., Riehle, K. J., Hubbert, C. et al., Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 2007, 134, 479-489.
9. Padhi, B. K., Joly, L., Tellis, P., Smith, A. et al., Screen for genes differentially expressed during regeneration of the zebrafish caudal fin. Dev. Dyn. 2004, 231, 527-541.
10. Yoshinari, N., Ishida, T., Kudo, A., Kawakami, A., Gene expression and functional analysis of zebrafish larval fin fold regeneration. Dev. Biol. 2009, 325, 71-81.
11. Walther, T. C., Mann, M., Mass spectrometry-based proteomics in cell biology. J. Cell Biol. 2010, 190, 491-500.
12. Saxena, S., Singh, S. K., Lakshmi, M. G., Meghah, V. et al., Proteomic analysis of zebrafish caudal fin regeneration. Mol. Cell. Proteomics 2012, 11, M111. 014118.
13. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B. et al., Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1, 376-386.
14. Ong, S. E., Mann, M., Stable isotope labeling by amino acids in cell culture for quantitative proteomics. Methods Mol. Biol. 2007, 359, 37-52.
15. Kruger, M., Moser, M., Ussar, S., Thievessen, I. et al., SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function. Cell 2008, 134, 353-364.
16. Konzer, A., Ruhs, A., Braun, H., Jungblut, B. et al., Stable isotope labeling in zebrafish allows in vivo monitoring of cardiac morphogenesis. Mol. Cell. Proteomics 2013, 12, 1502-1512.
17. Nolte, H., Konzer, A., Ruhs, A., Jungblut, B. et al., Global protein expression profiling of zebrafish organs based on in vivo incorporation of stable isotopes. J. Proteome Res. 2014, 13, 2162-2174.
18. Schoenheimer, R., Rittenberg, D., Deuterium as an indicator in the study of intermediary metabolism. Science 1935, 82, 156-157.
19. Waterlow, J. C., Protein Turnover. CAB International 2006.
20. Claydon, A. J., Beynon, R., Proteome dynamics: revisiting turnover with a global perspective. Mol. Cell. Proteomics 2012, 11, 1551-1565.
21. Eichelbaum, K., Krijgsveld, J., Rapid temporal dynamics of transcription, protein synthesis, and secretion during macrophage activation. Mol. Cell. Proteomics 2014, 13, 792-810.
22. Westman-Brinkmalm, A., Abramsson, A., Pannee, J., Gang, C. et al., SILAC zebrafish for quantitative analysis of protein turnover and tissue regeneration. J. Proteomics 2011, 75, 425-434.
23. Looso, M., Borchardt, T., Kruger, M., Braun, T., Advanced identification of proteins in uncharacterized proteomes by pulsed in vivo stable isotope labeling-based mass spectrometry. Mol. Cell. Proteomics 2010, 9, 1157-1166.
24. Westerfield, M., The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio). University of Oregon Press, Eugene, OR 2000.
25. Andersen, J. S., Lam, Y. W., Leung, A. K., Ong, S. E. et al., Nucleolar proteome dynamics. Nature 2005, 433, 77-83.
26. Rappsilber, J., Ishihama, Y., Mann, M., Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 2003, 75, 663-670.
27. Thisse, C., Thisse, B., High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protocols 2008, 3, 59-69.
28. Poss, K. D., Shen, J., Nechiporuk, A., McMahon, G. et al., Roles for Fgf signaling during zebrafish fin regeneration. Dev. Biol. 2000, 222, 347-358.
29. Zhang, J., Wagh, P., Guay, D., Sanchez-Pulido, L. et al., Loss of fish actinotrichia proteins and the fin-to-limb transition. Nature 2010, 466, 234-237.
30. Price, J. C., Guan, S., Burlingame, A., Prusiner, S. B., Ghaemmaghami, S., Analysis of proteome dynamics in the mouse brain. Proc. Natl. Acad. Sci. USA 2010, 107, 14508-14513.
31. Cambridge, S. B., Gnad, F., Nguyen, C., Bermejo, J. L. et al., Systems-wide proteomic analysis in mammalian cells reveals conserved, functional protein turnover. J. Proteome Res. 2011, 10, 5275-5284.
32. Eden, E., Navon, R., Steinfeld, I., Lipson, D., Yakhini, Z., GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 2009, 3, 48.
33. Koester, A., Paulsen, A. Q., Garrett, A. S., Boyle, D. L. et al., Mimecan/osteoglycin-deficient mice have collagen fibril abnormalities. Mol. Vis. 2002, 31, 407-415.
34. Ibarz, A., Pinto, P. I., Power, D. M., Proteomic approach to skin regeneration in a marine teleost: modulation by oestradiol-17β. Mar. Biotechnol. (NY) 2013, 15, 629-46.
35. Reeves, R., Molecular biology of HMGA proteins: hubs of nuclear function. Gene 2001, 277, 63-81.
36. Tobin, D. M., Roca, F. J., Ray, J. P., Ko, D. C., Ramakrishnan, L., An enzyme that inactivates the inflammatory mediator leukotriene b4 restricts mycobacterial infection. PLoS One 2013, 8, e67828.
37. Messaritou, G., East, L., Roghi, C., Isacke, C. M., Yarwood, H., Membrane type-1 matrix metalloproteinase activity is regulated by the endocytic collagen receptor Endo180. J. Cell Sci. 2009, 122, 4042-4048.
38. Rhee, D. K., Marcelino, J., Baker, M., Gong, Y. et al., The secreted glycoprotein lubricin protects cartilage surfaces and inhibits synovial cell overgrowth. J. Clin. Invest. 2005, 115, 622-631.
39. Mathew, L. K., Sengupta, S., Franzosa, J. A., Perry, J. et al., Comparative expression profiling reveals an essential role for raldh2 in epimorphic regeneration. J. Biol. Chem. 2009, 284, 33642-33653.
40. Makino, S., Whitehead, G. G., Lien, C. L., Kim, S. et al., Heat-shock protein 60 is required for blastema formation and maintenance during regeneration. Proc. Natl. Acad. Sci. USA 2005, 102, 14599-14604.
41. Taherian, A., Krone, P. H., Ovsenek, N., A comparison of Hsp90alpha and Hsp90beta interactions with cochaperones and substrates. Biochem. Cell Biol. 2008, 86, 37-45.
42. Li, W., Li, Y., Guan, S., Fan, J. et al., Extracellular heat shock protein-90alpha: linking hypoxia to skin cell motility and wound healing. EMBO J. 2007, 26, 1221-1233.