Molecular approach to annelid regeneration: CDNA subtraction cloning reveals various novel genes that are upregulated during the large-scale regeneration of the oligochaete, Enchytraeus japonensis

Developmental Dynamics

Volumn 235, Issue 8, 2006, Pages 2051-2070

  Myohara, Maroko ^a   Niva, Cintia Carla ^a   Lee, Jae Min ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

Ejrup; Enchytraeus japonensis; Novel genes; Oligochaete annelid; Regeneration; Suppression subtractive hybridization

Indexed keywords

ADENYLOSUCCINATE LYASE; ALDEHYDE DEHYDROGENASE; ARGINASE; BETA TUBULIN; BLOOD CLOTTING FACTOR 10A; CADHERIN; CHITIN BINDING PROTEIN 5; COMPLEMENTARY DNA; ELONGATION FACTOR 1; ELONGATION FACTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBRILLARIN; FILAMIN A; GENE PRODUCT; GLUCOSIDASE; GLUTAMATE AMMONIA LIGASE; GLUTAMATE DEHYDROGENASE; GLYCINE TRANSPORTER 1; GLYCOSYLTRANSFERASE; INITIATION FACTOR; MATRILIN 3; METHIONINE ADENOSYLTRANSFERASE; MYOSIN HEAVY CHAIN; OXIDOREDUCTASE; PROTEASOME; PROTEIN DNAJ; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; SERINE PROTEINASE INHIBITOR; SIGNAL PEPTIDASE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANNELID WORM; ARTICLE; BLASTEMA; CELL PROLIFERATION; DNA LIBRARY; ENCHYTRAEUS JAPONENSIS; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE FUNCTION; HOUSEKEEPING GENE; IMMUNE RESPONSE; IN SITU HYBRIDIZATION; MEMBRANE TRANSPORT; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGENERATION; RNA INTERFERENCE; SEQUENCE ANALYSIS; SRC HOMOLOGY DOMAIN; SUPPRESSION SUBTRACTIVE HYBRIDIZATION; TRANSCRIPTION REGULATION; UNINDEXED SEQUENCE;

AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; OLIGOCHAETA; PROTEINS; REGENERATION; SEQUENCE ALIGNMENT; UP-REGULATION;

ANIMALIA; ANNELIDA; ENCHYTRAEUS JAPONENSIS;

EID: 33746950961     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.20849     Document Type: Article

References (52)

1. Abcouwer SF, Lohmann R, Bode BP, Lustig RJ, Souba WW. 1997. Induction of glutamine synthetase expression after major burn injury is tissue specific and temporally variable. J Trauma 42:421-428.
2. Adoutte A, Balavoine G, Lartillot N, Lespinet O, Prud'homme B, de Rosa R. 2000. The new animal phylogeny: reliability and implications. Proc Natl Acad Sci USA 97:4453-4456.
3. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
4. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. 1995. Short protocols in molecular biology. New York: Wiley.
5. Baguñà J. 1998. Planarians. In: Ferretti P, Géraudie J, editors. Cellular and molecular basis of regeneration: from invertebrates to humans. New York: John Wiley & Sons. p 135-165.
6. Bely AE, Wray GA. 2001. Evolution of regeneration and fission in annelids: insights from engrailed- and orthodenticle-class gene expression. Development 128: 2781-2791.
7. Bode H, Berking S, David CN, Gierer A, Schaller H, Trenkner E. 1973. Quantitative analysis of cell types during growth and morphogenesis in Hydra. Roux's Arch 171:269-285.
8. Bosch TCG, David CN. 1987. Stem cells of Hydra magnipapillata can differentiate into somatic cells and germ line cells. Dev Biol 121:182-191.
9. Carlson BM. 1998. Development and regeneration, with special emphasis on the amphibian limb. In: Ferretti P, Géraudie J, editors. Cellular and molecular basis of regeneration: from invertebrates to human. New York: John Wiley & Sons. p 411-450.
10. Chenchik A, Zhu Y, Diatchenko L, Li R, Hill J, Siebert P. 1998. Generation and use of high-quality cDNA from small amounts of total RNA by SMART PCR. In: Siebert P, Larrick J, editors. RT-PCR methods for gene cloning and analysis. Westborough, MA: BioTechniques Books. p 305-319.
11. Christensen RN, Tassava RA. 2000. Apical epithelial cap morphology and fibronectin gene expression in regenerating axolotl limbs. Dev Dyn 217:216-224.
12. Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD. 1996. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025-6030.
13. Dingwall C, Laskey RA. 1991. Nuclear targeting sequences: a consensus? Trends Biochem Sci 16:478-481.
14. D'Souza SE, Ginsberg MH, Plow EF. 1991. Arginyl-glycyl-aspartic acid (RGD): a cell adhesion motif. Trends Biochem Sci 16: 246-250.
15. Dupin F, Coulon J, Le Parco Y, Fontes M, Thouveny Y. 1991. Formation of the extracellular matrix during the epimorphic anterior regeneration of Owenia fusiformis: autoradiographical and in situ hybridization studies. Int J Dev Biol 35: 109-119.
16. Edelman GM. 1985. Expression of cell adhesion molecules during embryogenesis and regeneration. Exp Cell Res 161:1-16.
17. Gardiner DM, Carlson MRJ, Roy S. 1999. Towards a functional analysis of limb regeneration. Semin Cell Dev Biol 10: 385-393.
18. Hadjiargyrou M, Lombardo F, Zhao SC, Ahrens W, Joo J, Ahn H, Jurman M, White DW, Rubin CT. 2002. Transcriptional profiling of bone regeneration. Insight into the molecular complexity of wound repair. J Biol Chem 277:30177-30182.
19. Hatada S, Kinoshita M, Noda M, Asashima M. 1995. Identification of a Xenopus glutamine synthetase gene abundantly expressed in the embryonic nervous system but not in adult brain. FEBS Lett 371: 287-292.
20. Herlant-Meewis H. 1964. Regeneration in annelids. Adv Morphog 4:155-215.
21. Higashide T, Murakami A, McLaren MJ, Inana G. 1996. Cloning of the cDNA for a novel photoreceptor protein. J Biol Chem 271:1797-1804.
22. Hulo N, Sigrist CJ, Le Saux V, Langendijk-Genevaux PS, Bordoli L, Gattiker A, De Castro E, Bucher P, Bairoch A. 2004. Recent improvements to the PROSITE database. Nucleic Acids Res. 32:D134-137.
23. Jensen LJ, Gupta R, Blom N, Devos D, Tamames J, Kesmir C, Nielsen H, Staerfeldt HH, Rapacki K, Workman C, Andersen CA, Knudsen S, Krogh A, Valencia A, Brunak S. 2002. Prediction of human protein function from post-translational modifications and localization features. J Mol Biol 319:1257-1265.
24. Jensen LJ, Gupta R, Staerfeldt HH, Brunak S. 2003. Prediction of human protein function according to Gene Ontology categories. Bioinformatics 19:635-642.
25. Kim TH, Mars WM, Stolz DB, Petersen BE, Michalopoulos GK. 1997. Extracellular matrix remodeling at the early stages of liver regeneration in the rat. Hepatology 26:896-904.
26. King MW, Nguyen T, Calley J, Harty MW, Muzinich MC, Mescher AL, Chalfant C, N'Cho M, McLeaster K, McEntire J, Stocum D, Smith RC, Neff AW. 2003. Identification of genes expressed during Xenopus laevis limb regeneration by using subtractive hybridization. Dev. Dyn. 226: 398-409.
27. Landschulz WH, Johnson PF, McKnight SL. 1988. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240:1759-1764.
28. Lee JM, Nishimori Y, Hatakeyama M, Bae TW, Oishi K. 2000. Vitellogenin of the cicada Graptopsaltria nigrofuscata (Homoptera): analysis of its primary structure. Insect Biochem Mol Biol 30:1-7.
29. Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P. 2004. SMART 4.0: towards genomic data integration. Nucleic Acids Res 32:D142-144.
30. Maduro M, Pilgrim D. 1995. Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141:977-988.
31. Maduro MF, Gordon M, Jacobs R, Pilgrim DB. 2000. The UNC-119 family of neural proteins is functionally conserved between humans, Drosophila and C. elegans. J Neurogenet 13:191-212.
32. Manning AG, Crawford BD, Waskiewicz AJ, Pilgrim DB. 2004. unc-119 homolog required for normal development of the zebrafish nervous system. Genesis 40: 223-230.
33. Marenholz I, Zirra M, Fischer DF, Backendorf C, Ziegler A, Mischke D. 2001. Identification of human epidermal differentiation complex (EDC)-encoded genes by subtractive hybridization of entire YACs to a gridded keratinocyte cDNA library. Genome Res 11:341-355.
34. Mayer BJ. 2001. SH3 domains: complexity in moderation. J Cell Sci 114:1253-1263.
35. Myohara M. 2004. Differential tissue development during embryogenesis and regeneration in an annelid. Dev Dyn 231: 349-358.
36. Myohara M, Yoshida-Noro C, Kobari F, Tochinai S. 1999. Fragmenting oligochaete Enchytraeus japonensis: a new material for regeneration study. Dev Growth Differ 41:549-555.
37. Nardelli-Haefliger D, Shankland M. 1992. Lox2, a putative leech segment identity gene, is expressed in the same segmental domain in different stem cell lineages. Development 116:697-710.
38. Newmark PA, Sanchez Alvarado A. 2000. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220:142-153.
39. Quinones JL, Rosa R, Ruiz DL, Garcia-Arraras JE. 2002. Extracellular matrix remodeling and metalloproteinase involvement during intestine regeneration in the sea cucumber Holothuria glaberrima. Dev Biol 250:181-197.
40. Reddien PW, Bermange AL, Murfitt KJ, Jennings JR, Sanchez Alvarado A. 2005. Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev Cell 8:635-649.
41. Ricard D, Rogemond V, Charrier E, Aguera M, Bagnard D, Belin MF, Thomasset N, Honnorat J. 2001. Isolation and expression pattern of human Unc-33-like phosphoprotein 6/collapsin response mediator protein 5 (Ulip6/CRMP5): coexistence with Ulip2/CRMP2 in SemaSa- sensitive oligodendrocytes. J Neurosci 21:7203-7214.
42. Roper K, Gregory SL, Brown NH. 2002. The "spectraplakins": cytoskeletal giants with characteristics of both spectrin and plakin families. J Cell Sci 115:4215-4225.
43. Schmelz RM, Collado R, Myohara M. 2000. A taxonomic study of Enchytraeus japonensis (Enchytraeidae, Oligochaeta): morphological and biochemical comparisons with E. bigeminus. Zool Sci 17:505-516.
44. Schulte T, Paschke KA, Laessing U, Lottspeich F, Stuermer CA. 1997. Reggie-1 and reggie-2, two cell surface proteins expressed by retinal ganglion cells during axon regeneration. Development 124: 577-587.
45. Schultz J, Milpetz F, Bork P, Ponting CP. 1998. SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95:5857-5864.
46. Shimizu H, Zhang XM, Zhang JS, Leontovich A, Fei KY, Yan L, Sarras MP Jr. 2002. Epithelial morphogenesis in hydra requires de novo expression of extracellular matrix components and matrix metalloproteinases. Development 129: 1521-1532.
47. Swanson DA, Chang JT, Campochiaro PA, Zack DJ, Valle D. 1998. Mammalian orthologs of C. elegans unc-119 highly expressed in photoreceptors. Invest Ophthalmol Vis Sci 39:2085-2094.
48. Tazaki A, Kitayama A, Terasaka C, Watanabe K, Ueno N, Mochii M. 2005. Macroarray-based analysis of tail regeneration in Xenopus laevis larvae. Dev Dyn 233:1394-1404.
49. Thouveny Y, Tassava RA. 1998. Regeneration through phylogenesis. In: Ferretti P, Géraudie J, editors. Cellular and molecular basis of regeneration: from invertebrates to humans. New York: John Wiley & Sons. p 9-43.
50. Walsh FS, Doherty P. 1996. Cell adhesion molecules and neuronal regeneration. Curr Opin Cell Biol 8:707-713.
51. Xie D, Li A, Wang MH, Fan ZW, Feng HQ. 2005. LOCSVMPSI: a web server for subcellular localization of eukaryotic proteins using SVM and profile of PSI-BLAST. Nucleic Acids Res 33:W105-110.
52. + RNA with the CapFinder™ PCR cDNA library construction kit. Clontechniques XI:30-31.