New approach for fish breeding by chemical mutagenesis: Establishment of TILLING method in fugu (Takifugu rubripes) with ENU mutagenesis

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Kuroyanagi, Miwa ^a   Katayama, Takashi ^b   Imai, Tadashi ^b   Yamamoto, Yoshihisa ^b   Chisada, Shin ichi ^c   Yoshiura, Yasutoshi ^c   Ushijima, Tomokazu ^d   Matsushita, Tomonao ^d   Fujita, Masashi ^a   Nozawa, Aoi ^a   Suzuki, Yuzuru ^a   Kikuchi, Kiyoshi ^a   Okamoto, Hiroyuki ^c  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN FISHERIES RESEARCH AND EDUCATION AGENCY   (Japan)

^c FISHERIES RESEARCH AGENCY   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

Author keywords

ENU; Fish breeding; Fugu; HRM; Mutagenesis; Myostatin; TILLING

Indexed keywords

GENOMIC DNA; MYOSTATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREEDING METHOD; CHEMICAL MUTAGENESIS; CONTROLLED STUDY; DNA ISOLATION; DNA SEQUENCE; FEMALE; GENE TARGETING; GENETIC IMPROVEMENT; HATCHING; HIGH RESOLUTION MELTING ANALYSIS; MALE; MUTATION RATE; MYOSTATIN GENE; NONHUMAN; NONSENSE MUTATION; PISCICULTURE; PUFFER FISH; REVERSE GENETICS; TARGETING INDUCED LOCAL LESIONS IN GENOME METHOD;

BOVINAE; DANIO RERIO; MUS; ORYZIINAE; TAKIFUGU; TAKIFUGU RUBRIPES;

ALLELES; ANIMALS; BREEDING; CODON, NONSENSE; ETHYLNITROSOUREA; FEMALE; GENOME; MALE; MUTAGENESIS; REVERSE GENETICS; TAKIFUGU;

EID: 84887348201     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-786     Document Type: Article

References (46)

1. Moen T, Baranshi M, Sonesson AK, Kjøglum S. Confirmation and fine-mapping of a major QTL for resistance to infectious pancreatic necrosis in Atlantic salmon (Salmo salar): population-level associations between markers and trait. BMC Genomics 2009, 10:368-381. 10.1186/1471-2164-10-368, 2728743, 19664221.
2. Driever W, Solnica-Krezel L, Schier AF, Neuhauss SC, Malicki J, Stemple DL, Stainier DY, Zwartkruis F, Abdelilah S, Rangini Z, et al. A genetic screen for mutations affecting embryogenesis in zebrafish. Development 1996, 123:37-46.
3. Shima A, Shimada A. Development of a possible nonmammalian test system for radiation-induced germ-cell mutagenesis using a fish, the Japanese medaka (Oryzias latipes). Proc Natl Acad Sci U S A 1991, 88(6):2545-2549. 10.1073/pnas.88.6.2545, 51269, 2006189.
4. Loosli F, Koster RW, Carl M, Kuhnlein R, Henrich T, Mucke M, Krone A, Wittbrodt J. A genetic screen for mutations affecting embryonic development in medaka fish (Oryzias latipes). Mech Dev 2000, 97(1-2):133-139.
5. McCallum CM, Comai L, Greene EA, Henikoff S. Targeted screening for induced mutations. Nat Biotechnol 2000, 18(4):455-457. 10.1038/74542, 10748531.
6. Cooper JL, Till BJ, Laport RG, Darlow MC, Kleffner JM, Jamai A, El-Mellouki T, Liu S, Ritchie R, Nielsen N, et al. TILLING to detect induced mutations in soybean. BMC Plant Biol 2008, 8:9. 10.1186/1471-2229-8-9, 2266751, 18218134.
7. Suzuki T, Eiguchi M, Kumamaru T, Satoh H, Matsusaka H, Moriguchi K, Nagato Y, Kurata N. MNU-induced mutant pools and high performance TILLING enable finding of any gene mutation in rice. Mol Genet Genomics 2008, 279(3):213-223. 10.1007/s00438-007-0293-2, 17952471.
8. Slade AJ, Fuerstenberg SI, Loeffler D, Steine MN, Facciotti D. A reverse genetic, nontransgenic approach to wheat crop improvement by TILLING. Nat Biotechnol 2005, 23(1):75-81. 10.1038/nbt1043, 15580263.
9. Till BJ, Reynolds SH, Weil C, Springer N, Burtner C, Young K, Bowers E, Codomo CA, Enns LC, Odden AR, et al. Discovery of induced point mutations in maize genes by TILLING. BMC Plant Biol 2004, 4:12. 10.1186/1471-2229-4-12, 512284, 15282033.
10. Bentley A, MacLennan B, Calvo J, Dearolf CR. Targeted recovery of mutations in Drosophila. Genetics 2000, 156(3):1169-1173. 1461331, 11063692.
11. Gilchrist EJ, O'Neil NJ, Rose AM, Zetka MC, Haughn GW. TILLING is an effective reverse genetics technique for Caenorhabditis elegans. BMC Genomics 2006, 7:262. 10.1186/1471-2164-7-262, 1626091, 17049087.
12. Smits BM, Mudde J, Plasterk RH, Cuppen E. Target-selected mutagenesis of the rat. Genomics 2004, 83(2):332-334. 10.1016/j.ygeno.2003.08.010, 14706462.
13. Taniguchi Y, Takeda S, Furutani-Seiki M, Kamei Y, Todo T, Sasado T, Deguchi T, Kondoh H, Mudde J, Yamazoe M, et al. Generation of medaka gene knockout models by target-selected mutagenesis. Genome Biol 2006, 7(12):R116. 10.1186/gb-2006-7-12-r116, 1794429, 17156454.
14. Sood R, English MA, Jones M, Mullikin J, Wang DM, Anderson M, Wu D, Chandrasekharappa SC, Yu J, Zhang J, et al. Methods for reverse genetic screening in zebrafish by resequencing and TILLING. Methods 2006, 39(3):220-227. 10.1016/j.ymeth.2006.04.012, 16828311.
15. Till BJ, Zerr T, Bowers E, Greene EA, Comai L, Henikoff S. High-throughput discovery of rare human nucleotide polymorphisms by Ecotilling. Nucleic Acids Res 2006, 34(13):e99. 10.1093/nar/gkl479, 1540726, 16893952.
16. Kennedy CL, O'Bryan MK. N-ethyl-N-nitrosourea (ENU) mutagenesis and male fertility research. Hum Reprod Update 2006, 12(3):293-301. 10.1093/humupd/dmk004, 16436467.
17. Mullins MC, Hammerschmidt M, Haffter P, Nusslein-Volhard C. Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate. Curr Biol 1994, 4(3):189-202. 10.1016/S0960-9822(00)00048-8, 7922324.
18. Imai Y, Feldman B, Schier AF, Talbot WS. Analysis of chromosomal rearrangements induced by postmeiotic mutagenesis with ethylnitrosourea in zebrafish. Genetics 2000, 155(1):261-272. 1461089, 10790400.
19. Knapik EW. ENU mutagenesis in zebrafish-from genes to complex diseases. Mamm Genome 2000, 11(7):511-519. 10.1007/s003350010098, 10886014.
20. Jiang XY, Sun CF, Zhang QG, Zou SM. ENU-induced mutagenesis in grass carp (Ctenopharyngodon idellus) by treating mature sperm. PLoS One 2011, 6(10):e26475. 10.1371/journal.pone.0026475, 3195716, 22022617.
21. Riley BB, Grunwald DJ. Efficient induction of point mutations allowing recovery of specific locus mutations in zebrafish. Proc Natl Acad Sci U S A 1995, 92(13):5997-6001. 10.1073/pnas.92.13.5997, 41629, 7597068.
22. Solnica-Krezel L, Schier AF, Driever W. Efficient recovery of ENU-induced mutations from the zebrafish germline. Genetics 1994, 136(4):1401-1420. 1205920, 8013916.
23. Colbert T, Till BJ, Tompa R, Reynolds S, Steine MN, Yeung AT, McCallum CM, Comai L, Henikoff S. High-throughput screening for induced point mutations. Plant Physiol 2001, 126(2):480-484. 10.1104/pp.126.2.480, 1540114, 11402178.
24. Moens CB, Donn TM, Wolf-Saxon ER, Ma TP. Reverse genetics in zebrafish by TILLING. Brief Funct Genomic Proteomic 2008, 7(6):454-459. 10.1093/bfgp/eln046, 2899843, 19028802.
25. Gady AL, Hermans FW, Van de Wal MH, van Loo EN, Visser RG, Bachem CW. Implementation of two high through-put techniques in a novel application: detecting point mutations in large EMS mutated plant populations. Plant Methods 2009, 5:13. 10.1186/1746-4811-5-13, 2763861, 19811648.
26. Ishikawa T, Kamei Y, Otozai S, Kim J, Sato A, Kuwahara Y, Tanaka M, Deguchi T, Inohara H, Tsujimura T, et al. High-resolution melting curve analysis for rapid detection of mutations in a Medaka TILLING library. BMC Mol Biol 2010, 11:70. 10.1186/1471-2199-11-70, 2949603, 20840787.
27. Li F, Niu B, Huang Y, Meng Z. Application of high-resolution DNA melting for genotyping in lepidopteran non-model species: Ostrinia furnacalis (Crambidae). PLoS One 2012, 7(1):e29664. 10.1371/journal.pone.0029664, 3256165, 22253755.
28. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997, 387(6628):83-90. 10.1038/387083a0, 9139826.
29. Kambadur R, Sharma M, Smith TP, Bass JJ. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res 1997, 7(9):910-916.
30. McPherron AC, Lee SJ. Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci U S A 1997, 94(23):12457-12461. 10.1073/pnas.94.23.12457, 24998, 9356471.
31. Mosher DS, Quignon P, Bustamante CD, Sutter NB, Mellersh CS, Parker HG, Ostrander EA. A mutation in the myostatin gene increases muscle mass and enhances racing performance in heterozygote dogs. PLoS Genet 2007, 3(5):e79. 10.1371/journal.pgen.0030079, 1877876, 17530926.
32. Schuelke M, Wagner KR, Stolz LE, Hubner C, Riebel T, Komen W, Braun T, Tobin JF, Lee SJ. Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med 2004, 350(26):2682-2688. 10.1056/NEJMoa040933, 15215484.
33. Chisada S, Okamoto H, Taniguchi Y, Kimori Y, Toyoda A, Sakaki Y, Takeda S, Yoshiura Y. Myostatin-deficient medaka exhibit a double-muscling phenotype with hyperplasia and hypertrophy, which occur sequentially during post-hatch development. Dev Biol 2011, 359(1):82-94. 10.1016/j.ydbio.2011.08.027, 21925159.
34. Wansleeben C, van Gurp L, Feitsma H, Kroon C, Rieter E, Verberne M, Guryev V, Cuppen E, Meijlink F. An ENU-mutagenesis screen in the mouse: identification of novel developmental gene functions. PLoS One 2011, 6(4):e19357. 10.1371/journal.pone.0019357, 3084836, 21559415.
35. Russell WL, Kelly EM, Hunsicker PR, Bangham JW, Maddux SC, Phipps EL. Specific-locus test shows ethylnitrosourea to be the most potent mutagen in the mouse. Proc Natl Acad Sci U S A 1979, 76(11):5818-5819. 10.1073/pnas.76.11.5818, 411742, 293686.
36. Shibuya T, Horiya N, Matsuda H, Sakamoto K, Hara T. Dose-dependent induction of recessive mutations with N-ethyl-N-nitrosourea in primordial germ cells of male mice. Mutat Res 1996, 357(1-2):219-224.
37. Berry C, Thomas M, Langley B, Sharma M, Kambadur R. Single cysteine to tyrosine transition inactivates the growth inhibitory function of piedmontese myostatin. Am J Physiol Cell Physiol 2002, 283(1):C135-141. 10.1152/ajpcell.00458.2001, 12055081.
38. Henikoff S, Till BJ, Comai L. TILLING. Traditional mutagenesis meets functional genomics. Plant Physiol 2004, 135(2):630-636. 10.1104/pp.104.041061, 514099, 15155876.
39. Lee SJ, McPherron AC. Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci U S A 2001, 98(16):9306-9311. 10.1073/pnas.151270098, 55416, 11459935.
40. Bono C, Nuzzo D, Albeggiani G, Zizzo C, Francofonte D, Iemolo F, Sanzaro E, Duro G. Genetic screening of Fabry patients with EcoTILLING and HRM technology. BMC Res Notes 2011, 4:323. 10.1186/1756-0500-4-323, 3180462, 21896204.
41. Shima A, Shimada A. The Japanese medaka, Oryzias latipes, as a new model organism for studying environmental germ-cell mutagenesis. Environ Health Perspect 1994, 102(Suppl 12):33-35.
42. Wienholds E, Schulte-Merker S, Walderich B, Plasterk RH. Target-selected inactivation of the zebrafish rag1 gene. Science 2002, 297(5578):99-102. 10.1126/science.1071762, 12098699.
43. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, et al. The sequence of the human genome. Science 2001, 291:1304. 10.1126/science.1058040, 11181995.
44. Ohta H. Cryopreservation of teleost spermatozoa. Cryobiology and Cryotechnology 2008, 54(1):29-32.
45. Nickerson DA, Tobe VO, Taylor SL. PolyPhred: automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing. Nucleic Acids Res 1997, 25(14):2745-2751. 10.1093/nar/25.14.2745, 146817, 9207020.
46. Anai T, Yamada T, Hideshima R, Kinoshita T, Rahman SM, Takagi Y. Two high-oleic-acid soybean mutants, M23 and KK21, have disrupted microsomal omega-6 fatty acid desaturase, encoded by GmFAD2-1a. Breed Sci 2008, 58:447-452.