iTRAQ-based quantitative proteomic analysis of the initiation of head regeneration in planarians

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Geng, Xiaofang ^a   Wang, Gaiping ^a   Qin, Yanli ^a   Zang, Xiayan ^a   Li, Pengfei ^a   Geng, Zhi ^a   Xue, Deming ^a   Dong, Zimei ^a   Ma, Kexue ^a   Chen, Guangwen ^a   Xu, Cunshuan ^a  

^a HENAN NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; INITIATION FACTOR 2; MAMMALIAN TARGET OF RAPAMYCIN; HELMINTH PROTEIN; PEPTIDE; PROTEIN SERINE THREONINE KINASE;

AMPUTATION STUMP; ANTERIOR POSTERIOR AXIS; ARTICLE; CARBOHYDRATE METABOLISM; CELL MIGRATION; CELL POLARITY; CELL PROLIFERATION; CONTROLLED STUDY; DUGESIA JAPONICA; ENERGY METABOLISM; HEAD REGENERATION; MUSCLE CONTRACTION; NONHUMAN; OXIDATION REDUCTION STATE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEOMICS; REGENERATION; TURBELLARIA; ANIMAL; BIOSYNTHESIS; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HEAD; LIQUID CHROMATOGRAPHY; METABOLISM; PHYSIOLOGY; PLURIPOTENT STEM CELL; PROCEDURES; RANDOMIZATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; WOUND HEALING;

DUGESIA JAPONICA; PLANARIA; TURBELLARIA;

ANIMALS; CHROMATOGRAPHY, LIQUID; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENES, HELMINTH; HEAD; HELMINTH PROTEINS; PEPTIDES; PLANARIANS; PLURIPOTENT STEM CELLS; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; RANDOM ALLOCATION; REAL-TIME POLYMERASE CHAIN REACTION; REGENERATION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; WOUND HEALING;

EID: 84938849812     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132045     Document Type: Article

References (58)

1. Gentile L, Cebria F, Bartscherer K (2011) The planarian flatworm: an in vivo model for stem cell biology and nervous system regeneration. Dis Model Mech 4: 12-19. doi: 10.1242/dmm.006692 PMID: 21135057.
2. Wagner DE, Wang IE, Reddien PW (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332: 811-816. doi: 10.1126/science.1203983 PMID: 21566185.
3. Rink JC (2013) Stem cell systems and regeneration in planaria. Dev Genes Evol 223: 67-84. doi: 10.1007/s00427-012-0426-4 PMID: 23138344.
4. Eisenhoffer GT, Kang H, Sanchez Alvarado A (2008) Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 3: 327-339. doi: 10.1016/j.stem.2008.07.002 PMID: 18786419.
5. Wenemoser D, Reddien PW (2010) Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev Biol 344: 979-991. doi: 10.1016/j.ydbio.2010.06.017 PMID: 20599901.
6. Tanaka EM, Reddien PW (2011) The cellular basis for animal regeneration. Dev Cell 21: 172-185. doi: 10.1016/j.devcel.2011.06.016 PMID: 21763617.
7. Pellettieri J, Fitzgerald P, Watanabe S, Mancuso J, Green DR, Sanchez Alvarado A (2010) Cell death and tissue remodeling in planarian regeneration. Dev Biol 338: 76-85. doi: 10.1016/j.ydbio.2009.09.015 PMID: 19766622.
8. Wenemoser D, Lapan SW, Wilkinson AW, Bell GW, Reddien PW (2012) A molecular wound response program associated with regeneration initiation in planarians. Genes Dev 26: 988-1002. doi: 10.1101/gad.187377.112 PMID: 22549959.
9. Reddien PW, Sanchez Alvarado A (2004) Fundamentals of planarian regeneration. Annu Rev Cell Dev Biol 20: 725-757. doi: 10.1146/annurev.cellbio.20.010403.095114 PMID: 15473858.
10. Handberg-Thorsager M, Fernandez E, Salo E (2008) Stem cells and regeneration in planarians. Front Biosci 13: 6374-6394. PMID: 18508666.
11. Tasaki J, Shibata N, Sakurai T, Agata K, Umesono Y (2011) Role of c-Jun N-terminal kinase activation in blastema formation during planarian regeneration. Dev Growth Differ 53: 389-400. doi: 10.1111/j.1440-169X.2011.01254.x PMID: 21447099.
12. Tasaki J, Shibata N, Nishimura O, Itomi K, Tabata Y, Son F, et al. (2011) ERK signaling controls blastema cell differentiation during planarian regeneration. Development 138: 2417-2427. doi: 10.1242/dev.060764 PMID: 21610023.
13. Almuedo-Castillo M, Sureda-Gomez M, Adell T (2012) Wnt signaling in planarians: new answers to old questions. Int J Dev Biol 56: 53-65. doi: 10.1387/ijdb.113451ma PMID: 22450995.
14. Rink JC, Gurley KA, Elliott SA, Sanchez Alvarado A (2009) Planarian Hh signaling regulates regeneration polarity and links Hh pathway evolution to cilia. Science 326: 1406-1410. doi: 10.1126/science.1178712 PMID: 19933103.
15. Yazawa S, Umesono Y, Hayashi T, Tarui H, Agata K (2009) Planarian Hedgehog/Patched establishes anterior-posterior polarity by regulating Wnt signaling. Proc Natl Acad Sci U S A 106: 22329-22334. doi: 10.1073/pnas.0907464106 PMID: 20018728.
16. Reddien PW, Bermange AL, Kicza AM, Sanchez Alvarado A (2007) BMP signaling regulates the dorsal planarian midline and is needed for asymmetric regeneration. Development 134: 4043-4051. doi: 10.1242/dev.007138 PMID: 17942485.
17. Gurley KA, Rink JC, Sanchez Alvarado A (2008) Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 319: 323-327. doi: 10.1126/science.1150029 PMID: 18063757.
18. Petersen CP, Reddien PW (2008) Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 319: 327-330. doi: 10.1126/science.1149943 PMID: 18063755.
19. Petersen CP, Reddien PW (2011) Polarized notum activation at wounds inhibits Wnt function to promote planarian head regeneration. Science 332: 852-855. doi: 10.1126/science.1202143 PMID: 21566195.
20. Umesono Y, Tasaki J, Nishimura Y, Hrouda M, Kawaguchi E, Yazawa S, et al. (2013) The molecular logic for planarian regeneration along the anterior-posterior axis. Nature 500: 73-76. doi: 10.1038/nature12359 PMID: 23883928.
21. Shafiei MS, Rockey DC (2012) The function of integrin-linked kinase in normal and activated stellate cells: implications for fibrogenesis in wound healing. Lab Invest 92: 305-316. doi: 10.1038/labinvest.2011.155 PMID: 22064318.
22. Serrano I, Diez-Marques ML, Rodriguez-Puyol M, Herrero-Fresneda I, Raimundo Garcia del M, Dedhar S, et al. (2012) Integrin-linked kinase (ILK) modulates wound healing through regulation of hepatocyte growth factor (HGF). Exp Cell Res 318: 2470-2481. doi: 10.1016/j.yexcr.2012.08.001 PMID: 22971619.
23. Ho E, Dagnino L (2012) Emerging role of ILK and ELMO2 in the integration of adhesion and migration pathways. Cell Adh Migr 6: 168-172. doi: 10.4161/cam.20399 PMID: 22568984.
24. Agata K, Umesono Y (2008) Brain regeneration from pluripotent stem cells in planarian. Philos Trans R Soc Lond B Biol Sci 363: 2071-2078. doi: 10.1098/rstb.2008.2260 PMID: 18375378.
25. Qin YF, Fang HM, Tian QN, Bao ZX, Lu P, Zhao JM, et al. (2011) Transcriptome profiling and digital gene expression by deep-sequencing in normal/regenerative tissues of planarian Dugesia japonica. Genomics 97: 364-371. doi: 10.1016/j.ygeno.2011.02.002 PMID: 21333733.
26. Nishimura O, Hirao Y, Tarui H, Agata K (2012) Comparative transcriptome analysis between planarian Dugesia japonica and other platyhelminth species. BMC Genomics 13: 289. doi: 10.1186/1471-2164-13-289 PMID: 22747887.
27. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, et al. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3: 1154-1169. doi: 10.1074/mcp.M400129-MCP200 PMID: 15385600.
28. Adamidi C, Wang Y, Gruen D, Mastrobuoni G, You X, Tolle D, et al. (2011) De novo assembly and validation of planaria transcriptome by massive parallel sequencing and shotgun proteomics. Genome Res 21: 1193-1200. doi: 10.1101/gr.113779.110 PMID: 21536722.
29. Boser A, Drexler HC, Reuter H, Schmitz H, Wu G, Scholer HR, et al. (2013) SILAC proteomics of planarians identifies Ncoa5 as a conserved component of pluripotent stem cells. Cell Rep 5: 1142-1155. doi: 10.1016/j.celrep.2013.10.035 PMID: 24268775.
30. Fernandez-Taboada E, Rodriguez-Esteban G, Salo E, Abril JF (2011) A proteomics approach to decipher the molecular nature of planarian stem cells. BMC Genomics 12: 133. doi: 10.1186/1471-2164-12-133 PMID: 21356107.
31. Onal P, Grun D, Adamidi C, Rybak A, Solana J, Mastrobuoni G, et al. (2012) Gene expression of pluripotency determinants is conserved between mammalian and planarian stem cells. Embo j 31: 2755-2769. doi: 10.1038/emboj.2012.110 PMID: 22543868.
32. Geng X, Xu T, Niu Z, Zhou X, Zhao L, Xie Z, et al. (2014) Differential proteome analysis of the cell differentiation regulated by BCC, CRH, CXCR4, GnRH, GPCR, IL1 signaling pathways in Chinese fire-bellied newt limb regeneration. Differentiation. doi: 10.1016/j.diff.2014.10.002 PMID: 25465723.
33. Hsieh HC, Chen YT, Li JM, Chou TY, Chang MF, Huang SC, et al. (2009) Protein profilings in mouse liver regeneration after partial hepatectomy using iTRAQ technology. J Proteome Res 8: 1004-1013. doi: 10.1021/pr800696m PMID: 19099420.
34. Nicholson J, Neelagandan K, Huart AS, Ball K, Molloy MP, Hupp T (2012) An iTRAQ proteomics screen reveals the effects of the MDM2 binding ligand Nutlin-3 on cellular proteostasis. J Proteome Res 11: 5464-5478. doi: 10.1021/pr300698d PMID: 23039052.
35. Vizcaino JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Rios D, et al. (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol 32: 223-226. doi: 10.1038/nbt.2839 PMID: 24727771.
36. Dong Z, Yuwen Y, Wang Q, Chen G, Liu D (2012) Eight genes expression patterns during visual system regeneration in Dugesia japonica. Gene Expr Patterns 12: 1-6. doi: 10.1016/j.gep.2011.08.001 PMID: 21843655.
37. Huang da W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57. doi: 10.1038/nprot.2008.211 PMID: 19131956.
38. Wang G, Xu C, Zhi J, Hao Y, Zhang L, Chang C (2012) Gene expression profiles reveal significant differences between rat liver cancer and liver regeneration. Gene 504: 41-52. doi: 10.1016/j.gene.2012.04.086 PMID: 22575612.
39. Kramer A, Green J, Pollard J Jr., Tugendreich S (2014) Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics 30: 523-530. doi: 10.1093/bioinformatics/btt703 PMID: 24336805.
40. Kulkarni YM, Suarez V, Klinke DJ, 2nd (2010) Inferring predominant pathways in cellular models of breast cancer using limited sample proteomic profiling. BMC Cancer 10: 291. doi: 10.1186/1471-2407-10-291 PMID: 20550684.
41. Fraguas S, Barberan S, Iglesias M, Rodriguez-Esteban G, Cebria F (2014) egr-4, a target of EGFR signaling, is required for the formation of the brain primordia and head regeneration in planarians. Development 141: 1835-1847. doi: 10.1242/dev.101345 PMID: 24700819.
42. Sandmann T, Vogg MC, Owlarn S, Boutros M, Bartscherer K (2011) The head-regeneration transcriptome of the planarian Schmidtea mediterranea. Genome Biol 12: R76. doi: 10.1186/gb-2011-12-8-r76 PMID: 21846378.
43. Alibardi L (2014) Histochemical, Biochemical and Cell Biological aspects of tail regeneration in lizard, an amniote model for studies on tissue regeneration. Prog Histochem Cytochem 48: 143-244. doi: 10.1016/j.proghi.2013.12.001 PMID: 24387878.
44. Sun Y, Deng X, Li W, Yan Y, Wei H, Jiang Y, et al. (2007) Liver proteome analysis of adaptive response in rat immediately after partial hepatectomy. Proteomics 7: 4398-4407. doi: 10.1002/pmic.200600913 PMID: 17979177.
45. Guo T, Peters AH, Newmark PA (2006) A Bruno-like gene is required for stem cell maintenance in planarians. Dev Cell 11: 159-169. doi: 10.1016/j.devcel.2006.06.004 PMID: 16890156.
46. Solana J, Kao D, Mihaylova Y, Jaber-Hijazi F, Malla S, Wilson R, et al. (2012) Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNAseq, RNA interference and irradiation approach. Genome Biol 13: R19. doi: 10.1186/gb-2012-13-3-r19 PMID: 22439894.
47. Chen X, Xu C (2015) Protein expression profiling in head fragments during planarian regeneration after amputation. Dev Genes Evol 225: 79-93. doi: 10.1007/s00427-015-0494-3 PMID: 25697422.
48. Witchley JN, Mayer M, Wagner DE, Owen JH, Reddien PW (2013) Muscle cells provide instructions for planarian regeneration. Cell Rep 4: 633-641. doi: 10.1016/j.celrep.2013.07.022 PMID: 23954785.
49. Sakai T, Kato K, Watanabe K, Orii H (2002) Planarian pharynx regeneration revealed by the expression of myosin heavy chain-A. Int J Dev Biol 46: 329-332. PMID: 12068956.
50. Pascolini R, Tei S, Vagnetti D, Bondi C (1984) Epidermal cell migration during wound healing in Dugesia lugubris. Observations based on scanning electron microscopy and treatment with cytochalasin. Cell Tissue Res 236: 345-349. PMID: 6733761.
51. Wolf K, Alexander S, Schacht V, Coussens LM, von Andrian UH, van Rheenen J, et al. (2009) Collagen-based cell migration models in vitro and in vivo. Semin Cell Dev Biol 20: 931-941. doi: 10.1016/j.semcdb.2009.08.005 PMID: 19682592.
52. Alexander MS, Casar JC, Motohashi N, Myers JA, Eisenberg I, Gonzalez RT, et al. (2011) Regulation of DMD pathology by an ankyrin-encoded miRNA. Skelet Muscle 1: 27. doi: 10.1186/2044-5040-1-27 PMID: 21824387.
53. Rankin CR, Hilgarth RS, Leoni G, Kwon M, Den Beste KA, Parkos CA, et al. (2013) Annexin A2 regulates beta1 integrin internalization and intestinal epithelial cell migration. J Biol Chem 288: 15229-15239. doi: 10.1074/jbc.M112.440909 PMID: 23558678.
54. Iglesias M, Almuedo-Castillo M, Aboobaker AA, Salo E (2011) Early planarian brain regeneration is independent of blastema polarity mediated by the Wnt/beta-catenin pathway. Dev Biol 358: 68-78. doi: 10.1016/j.ydbio.2011.07.013 PMID: 21806978.
55. Nogi T, Zhang D, Chan JD, Marchant JS (2009) A novel biological activity of praziquantel requiring voltage-operated Ca2+ channel beta subunits: subversion of flatworm regenerative polarity. PLoS Negl Trop Dis 3: e464. doi: 10.1371/journal.pntd.0000464 PMID: 19554083.
56. Beane WS, Morokuma J, Adams DS, Levin M (2011) A chemical genetics approach reveals H, K-ATPase-mediated membrane voltage is required for planarian head regeneration. Chem Biol 18: 77-89. doi: 10.1016/j.chembiol.2010.11.012 PMID: 21276941.
57. Li JF, Duan HF, Wu CT, Zhang DJ, Deng Y, Yin HL, et al. (2013) HGF accelerates wound healing by promoting the dedifferentiation of epidermal cells through beta1-integrin/ILK pathway. Biomed Res Int 2013: 470418. doi: 10.1155/2013/470418 PMID: 24490163.
58. Gonzalez-Estevez C, Felix DA, Smith MD, Paps J, Morley SJ, James V, et al. (2012) SMG-1 and mTORC1 act antagonistically to regulate response to injury and growth in planarians. PLoS Genet 8: e1002619. doi: 10.1371/journal.pgen.1002619 PMID: 22479207.