Balık Kök Hücreleri: Sınıflandırma, Kaynakları, Karakteristik Özellikleri ve Uygulama Alanları

Öz

Kök hücreler farklılaşmamış hücre sınıfından, kendilerini yenileyebilme özelliğine sahip, özelleşmiş hücrelere farklılaşabilen hücrelerdir. Balıklarda ilk kök hücre çalışmaları 1992 yılında zebra balığı ile başlamıştır. Bu derlemede balık kök hücrelerin sınıflandırılması, kaynakları, önemleri, karakteristik özellikleri ve uygulama alanlarına değinilmiştir.

Anahtar Kelimeler

• Hücre hattı
• yarı-klonlama; transplantasyon; farklılaşma; eşey hücreleri

Fish Stem Cells: Classification, Resources, Characteristics and Application Areas

Abstract

Stem cells are a class of undifferentiated cells, have the potential for self-renewal that can differ to the specialized cells. First studies on stem cells in fish started with zebra fish in 1992. In this review, classification, resources, vital importance, characteristics and application areas of fish stem cell were clarified.

Keywords

• Cell line
• semi-cloning; transplantation; differentiation; germ cells

Kaynakça

1. Alvarez MC, Bejar J, Chen S, Hong Y. 2007. Fish ES cells and applications to biotechnology. Mar Biotechnol. 9(2):117-127. doi: 10.1007/s10126-006-6034-4
2. Ausoni S, Sartore S. 2009. From fish to amphibians to mammals: in search of novel strategies to optimize cardiac regeneration. J Cell Biol. 184(3):357-367. doi: 10.1083/jcb. 200810094
3. Béjar J, Hong Y, Alvarez MC. 1999. Towards obtaining es cells in the marine fish species Sparus aurata; multipassage maintenance, characterization and transfection. Genet Anal- Biomol E. 15(3-5):125-129. doi: 10.1016/S1050-3862(99)00015-7
4. Braasch I, Gehrke AR, Smith JJ, Kawasaki T, Manousaki T, Pasquier J, Amores A, Desvignes T, Batzel P, Catchen J, Berlin AM, Campbell MS, Barrell D, Martin KJ, Mulley JF, Ravi V, Lee AP, Nakamura T, Chalopin D, Fan S, Wcisel D, Canestro C, Sydes J, Beaudry FEG, Sun Y, Hertel J, Beam MJ, Fasold M, Ishiyama M, Johnson J, Kehr S, Lara M, Letaw JH, Litman GW, Litman RT, Mikami M, Ota T, Saha NT, Williams L, Stadler PF, Wang H, Taylor JS, Fontenot Q, Ferrara A, Searle SMJ, Aken B, Yandell M, Schneider I, Yoder JA, Volff JN, Meyer A, Amemiya CT, Venkatesh B, Holland PWH, Guiguen Y, Bobe J, Shubin NH, Palma FD, Alfoldi J, Toh KL, Postlethwait JH. 2016. The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nat Genet, 48(4):427-437. doi: 10.1038/ng.3526
5. Brian B. 2014. Distinct mechanisms underlie oral versus aboral regeneration in the hydractinia echinata. PhD. Thesis, National University of Ireland Galway, Pp.165.
6. Campbell KH, McWhir J, Ritchie WA, Wilmut I. 1996. Sheep cloned by nuclear transfer from a cultured cell line. Nature, 380(6569):64-66. doi: 10.1038/380064a0
7. Catton WT. 2012. Blood cell formation in certain teleost fishes. Blood. 6(1):39-60.
8. Chen S, Hong Y, Schartl M. 2002. Development of a positive-negative selection procedure for gene targeting in fish cells. Aquaculture, 214(1-4):67-79. doi: 10.1016/S0044-8486(01) 00811-0

9. Choi TY, Khalig M, Ko S, So J, Shin D. 2015. Hepatocyte-specific ablation in zebrafish to study biliary-driven regeneration. JVis Exp. 20(99):e52785. doi: 10.3791/52785
10. Collodi Y, Kamei A, Sharps D, Weber DB. 1992. Fish embryo cell cultures for derivation of stem cells and transgenic chimeras. Mol Mar Biol Biotechnol. 1(4-5):257-265.
11. Condic MI. 2014. Totipotency: What it is, and what it is not. Stem cells Dev. 23(8):796-812. doi: 10.1089/scd.2013.0364
12. Çek Ş. 2006. Early gonadal development and sex differentiation in rosy barb (puntius conchonius). Anim Biol. 56(3):335-350. doi: 10.1163/157075606778441895
13. Dash C, Routray P, Tripathy S, Verma DK, Guru BC, Meher PK, Nandi S, Eknath AE. 2010. Derivation and characterization of embryonic stem-like cells of Indian major carp Catla catla. J Fish Biol. 77(5):1096–1113. doi: 10.1111/j.1095-8649.2010.02755.x
14. Dahm R, Geisler R. 2006. Learning from Small Fry: The Zebra fish as a Genetic Model Organism for Aquaculture Fish Species. Mar Biotechnol. 8(4):329-345. doi: 10.1007/ s10126-006-5139-0
15. De Jong JJ, Burns CE, Chen AT, Pugach E, Mayhall EA, Smith ACH, Feldman HA, Zhou Y, Zon LI. 2011. Characterization of immune-matched hematopoietic transplantation in zebra fish. Blood. 117(16):4234-4242. doi: 10.1182/blood-2010-09-307488
16. Denker HW. 2014. Stem cell terminology ‘Synthetic embryos’: A new debate on totipotency omnipotency and pluripotency and how it relates to recent experimental data. Cell Tissues Organs. 199(4):221-227. doi: 10.1159/000370063
17. Diep CQ, Ma D, Deo RC, Holm TM, Naylor RW, Aroral N, Wingert RA, Bollig F, Djordjevic G, Lichman B, Zhu H, Ikenaga T, Ono F, Englert C, Cowan CA, Hukriede NA, Handin RI, Davidson AJ. 2011. Identification of adult nephron progenitors capable of kidney regeneration in zebra fish. Nature, 470(7332):95-100. doi: 10.1038/ nature09669
18. Evans MJ, Kaufman MH. 1981. Establishment in culture of pluripotential cells from Mouse embryos. Nature, 292(5819):154-156. doi:10.1038/292154a0
19. Fan L, Collodi P. 2006. Zebra fish embryonic stem cells. Methods in Enzymol. 418:64-77. doi:10.1016/S0076-6879(06)18004-0
20. Fan L, Moon J, Crodian J, Collodi P. 2006. Homologous recombination in zebra fish embryonic stem cells. Transgenic Res. 15(1):21-30. doi: 10.1007/s11248-005-3225-0
21. Fan L, Moon J, Wong TT, Crodian J, Collodi P. 2008. Zebra fish primordial germ cell cultures derived from vasa: RFP Transgenic Embryos. Stem Cells Dev. 17(3):585–597. doi: 10.1089/scd.2007.0178
22. Farlora R, Hattori-Ihara S, Takeuchi Y, Hayashi M, Octavera A, Yoshizaki G. 2013. Intraperitoneal germ cell transplantation in the Nile tilapia Oreochromis niloticus. Mar Biotechnol. 16(3):309-320. doi: 10.1007/s10126-013-9551-y
23. Fernández JA, Bubner EJ, Takeuchi Y, Yoshizaki G, Wang T, Cummins SF, Elizur A. 2015. Primordial germ cell migration in the yellowtail kingfish (Seriola lalandi) and identification of stromal cell-derived factor 1. Gen Comp Endocrinol. 213:16-23. doi: 10.1016/j.ygcen.2015.02.007
24. Galindo-Villegas J. 2016. Recent findings on vertebrate developmental immunity using the zebrafish model. Mol Immunol. 69:106-112. doi: 10.1016/j.molimm.2015.10.011
25. Grandel H, Kaslin J, Ganz J, Brand M. 2006. Neural stem cells and neurogenesis in the adult zebra fish brain: Origin, proliferation dynamics, migration and cell fate. Dev Biol. 295(1):263-277. doi: 10.1016/j.ydbio.2006.03.040
26. Guan G, Yan Y, Chen T, Yi M, Ni H, Naruse K, Nagahama Y, Hong Y. 2013. Nanos3 gene targeting in Medaka ES cells. Int J Biol Sci. 9(5):444-454. doi: 10.7150/ijbs.6507
27. Hall C, Crosier H, Crosier K. 2016. Inflammatory cytokines provide both infection-responsive and developmental signals for blood development: lessens from the zebrafish. Mol Immunol. 69:113-122. doi: 10.1016/j.molimm.2015.10.020
28. Hayashi M, Sato M, Nagasaka Y, Sadaie S, Kobayashi S, Yoshizaki G. 2014. Enrichment of spermatogonial stem cells using side population in teleost. Biol Reprod. 91(1):23,1-8. doi: 10.1095/biolreprod.113.114140
29. He J, Lu H, Zou Q, Luo L. 2014. Regeneration of liver after extreme hepatocyte loss occurs mainly via biliary trans differentiation in zebrafish. Gastroenterology. 146(3):789-800. doi: 10.1053/j.gastro.2013.11.045
30. Hong N, Zhendong L, Hong Y. 2011. Fish Stem Cell Cultures. Int J Biol Sci. 7(4):392-402. doi: 10.7150/ijbs.7.392
31. Hong Y, Winkler C, Schartl M. 1996. Pluripotency and differentiation of Embryonic stem cell lines from the medakafish (Oryzias latipes). Mech Dev. 60(1):33-44. doi: 10.1016/S0925 -4773(96)00596-5
32. Hong Y, Chen S, Gui J, Schartl M. 2004. Retention of the developmental pluripotency in medaka embryonic stem cells after gene transfer and long term drug selection for gene targeting in fish. Transgenic Res. 13(1):41-50. doi: 10.1023/B:TRAG.0000017172.71391.fa
33. Hong Y, MingYou XL, JianFang G, YunHan H. 2010. Fish germ cells. Sci China Life Sci. 53(4):435-446. doi: 10.1007/s11427-010-0058-8
34. Hong N, Yuan Y, Wang T, Yi W, Xu H, Zeng H, Song J, Hong Y. 2016. Dnd is a critical specifier of primordial germ cells in the Medaka fish. Stem Cell Reports. 6(3):411-421. doi: 10.1016/j.stemcr.2016.01.002
35. Ho SY, Pin GCW, Yang GJ, Sing LY, Kuen LMK, Ni H, Yunhan H, Khiong CW, Chong SCA. 2014. Derivation and long term culture of an embryonic stem cell-like line form zebrafish blastomeres under feeder free condition. Zebrafish. 11(5):407-420. doi: 10.1089/zeb.2013.0879
36. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, Kilian B, Quintais LT, Guerra-Assunção JA, Zhou Y, Gu Y, Yen J, Vogel JH, Eyre T, Redmond S, Banerjee R, Chi J, Fu B, Langley E, Maguire SF, Laird GK, Lloyd D, Kenyon E, Donaldson S, Sehra H, Almeida-King J, Loveland J, Trevanion S, Jones M, Quail M, Willey D, Hunt A, Burton J, Sims S, McLay K, Plumb B, Davis J, Clee C, Oliver K, Clark R, Riddle C, Elliot D, Threadgold G, Harden G, Ware D, Begum S, Mortimore B, Kerry G, Heath P, Phillimore B, Tracey A, Corby N, Dunn M, Johnson C, Wood J, Clark S, Pelan S, Griffiths G, Smith M, Glithero R, Howden P, Barker N, Lloyd C, Stevens C, Harley J, Holt K, Panagiotidis G, Lovell J, Beasley H, Henderson C, Gordon D, Auger K, Wright D, Collins J, Raisen C, Dyer L, Leung K, Robertson L, Ambridge K, Leongamornlert D, McGuire S, Gilderthorp R, Griffiths C, Manthravadi D, Nichol S, Barker G, Whitehead S, Kay M, Brown J, Murnane C, Gray E, Humphries M, Sycamore N, Barker D, Saunders D, Wallis J, Babbage A, Hammond S, Mashreghi-Mohammadi M, Barr L, Martin S, Wray P, Ellington A, Matthews N, Ellwood M, Woodmansey R, Clark G, Cooper J, Tromans A, Grafham D, Skuce C, Pandian R, Andrews R, Harrison E, Kimberley A, Garnett J, Fosker N, Hall R, Garner P, Kelly D, Bird C, Palmer S, Gehring I, Berger A, Dooley CM, Ersan-Ürün Z, Eser C, Geiger H, Geisler M, Karotki L, Kirn A, Konantz J, Konantz M, Oberländer M, Rudolph-Geiger S, Teucke M, Lanz C, Raddatz G, Osoegawa K, Zhu B, Rapp A, Widaa S, Langford C, Yang F, Schuster SC, Carter NP, Harrow J, Ning Z, Herrero J, Searle SM, Enright A, Geisler R, Plasterk RH, Lee C, Westerfield M, de Jong PJ, Zon LI, Postlethwait JH, Nüsslein-Volhard C, Hubbard TJ, Roest Crollius H, Rogers J, Stemple DL. 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 496(7446),498-503. doi: 10.1038/nature12111
37. Jopling CE, Sleep M, Raya M, Martí AR, Belmonte JCI. 2010. Zebra fish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature. 464(7288):606–609. doi: 10.1038/nature08899
38. Kobayashi I, Katakura F, Moritomo T. 2016. Isolation and characterization of hematopoietic stem cells in teleost fish. Dev Comp Immunol. 58:86-94. doi: 10.1016/j.dci.2016.01. 003
39. Lacerda SMSN, Batlouni SR, Silva SBG, Homem CSP, França LR. 2006. Germ cells transplantation in fish: the Nile-tilapia model. Animl Reprod. 3(2):146-159.
40. Lacerda SMSN, Batlouni SR, Assis LH, Resende FM, Silva SMC, Silva RC, Segatelli TM, França LR. 2008. Germ cell transplantation in tilapia (Oreochromis niloticus). Cybium, 32(2):115-118
41. Lacerda SMSN, Batlouni SR, Costa GMJ, Segatelli TM, Quirino BR, Queiroz BM, Kalapothakis E, França LR. 2010. A New and Fast Technique to Generate Offspring after Germ Cells Transplantation in Adult Fish: The Nile Tilapia (Oreochromis niloticus) Model. Plos One, 5(5):e10740. doi: 10.1371/journal.pone.0010740
42. Lacerda SMSN, Costa GMJ, Campos-Junior PHA, Segatelli TM, Yazawa R, Takeuchi Y, Morita T, Yoshizaki G, França LR. 2012. Germ cell transplantation as a potential biotechnological approach to fish reproduction. Fish Physiol Biochem. 39(1):3-11. doi: 10.1007/ s10695-012-9606-4
43. Lee S, Seki S, Katayama N, Yoshizaki G. 2015. Production of viable trout offspring derived from frozen whole fish. Scientific Reports. 5:1-12. doi: 10.1038/srep16045
44. Lenkowski JR, Raymond PA. 2014. Müller glia: stem cells for generation and regeneration of retinal neurons in teleost fish. Prog Retin Eye Res. 40:94-123. doi: 10.1016/j. preteyeres.2013.12.007
45. Lin CY, Chiang CY, Tsai HJ. 2016. Zebrafish and Medaka: new model organisms for modern biomedical research. J Biomed Sci. 23(1):19. doi: 10.1186/s12929-016-0236-5
46. Ma D, Zhang J, Lin H, Italiano J, Handin RI. 2012. The identification and characterization of zebra fish hematopoietic stem cells. Blood. 118(2):289-297. doi: 10.1182/blood-2010-12-327403
47. Ma D, Liu F. 2015. Genome editing and its application in model organisms. Genomics, Proteomics & Bioinformatics. 13(6):336-344. doi: 10.1016/j.gpb.2015.12.001.
48. Maeder ML, Gersbach, CA. 2016. Genome-editing technologies for gene and cell therapy. Mol Ther. 24(3):430-446. doi: 10.1038/mt.2016.10
49. MeiSheng Y, Ni H, YunHan H. 2009. Generation of medaka fish haploid embryonic stem cells. Science. 326(5951):430-433. doi: 10.1126/science.1175151
50. MeiSheng Y, Ni H, ZhenDong L, Yan Y, DanKe W, HaoBin Z, YunHan H. 2010. Medaka fish stem cells and their applications. Sci China Life Sci. 53(4):426-434. doi: 10.1007/s11427-010-0079-3.
51. Nagasawa K, Fernandes JMO, Yoshizaki G, Miwa M, Babiak I. 2013. Identification and migration of primordial germ cells in Atlantic salmon, salmo salar. Characterization of vasa dead end and lymphocyte antigen 75 genes. Mol Reprod Dev.80(2):118-131. doi: 10.1002/mrd.22142.
52. Nagasawa S, Hayashi KM, Furuya M, Iwasaki Y, Yoshizaki G. 2013. Short-term in vitro culturing improves transplant ability of type a spermatogonia in Rainbow trout (Oncorhynchus mykiss). Mol Reprod Dev. 80(9):763-773. doi: 10.1002/mrd.22208.
53. Nakajima S, Hayashi M, Kouguchi T, Yamaguchi K, Miwa M, Yoshizaki G. 2014. Expression patterns of gdnf and gfα1 in rainbow trout testis. Gene Expr Patterns.14(2):111-120. doi: 10.1016/j.gep.2014.01.006.
54. Nakamura S, Kobayashi K, Nishimura T, Tanaka M. 2011. Ovarian germ line stem cells in the teleost fish medaka (Oryzias latipes). Int J Biol Sci. 7(4): 403-409.
55. Nwokwa MC. 2012. The review of recent advances in fish genetics and biotechnology. Cont J Fisheries Aquatic Sci. 6(1):9-18 doi: 10.5707/cjfas.2012.6.1.9.18.
56. Okuda KS, Tan PJ, Patel V. 2016. Sprouting buds of zebrafish research in Malaysia: First Malaysia zebrafish disease model workshop. Zebrafish. 13(2):138-141. doi: 10.1089/zeb. 2015.1203.
57. Okutsu T, Suzuki K, Takeuchi Y, Yoshizaki G.2006. Testicular germ cells can colonize sexually undifferentiated embriyonic gonad and produce functional eggs in fish. Proc Natl Acad Sci U S A. 103(8):2725-2729. doi: 10.1073/pnas.0509218103.
58. Okutsu T, Shikina S, Kano M, Takeuchi Y, Yoshizaki G. 2007. Production of trout offspring from triploid salmon parents. Science, 317(5844):1517. doi: 10.1126/science.1145626.
59. Okutsu T, Shikina S, Sakamoto T, Mochizuki M, Yoshizaki G. 2015. Successful production of functional Y eggs derived from spermatogonia transplanted into female and subsequent production of YY super males in rainbow trout, Oncorhynhus mykiss. Aquaculture. 446:298-302. doi: 10.1016/j.aquaculture.2015.05.020.
60. Otteson DC, Hitchcock PF, 2003. Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration. Vision Res. 43(8):927–936. doi: 10.1016/S0042-6989 (02)00400-5.
61. Pan Z, Sun M, Liang X, Li J, Zhou F, Zhong Z, Zheng Y. 2016. The controversy challenges and potential benefits of putative female germ line stem cells research in mammals. Stem Cells Int. 1-9. doi: 10.1155/2016/1728278.
62. Prykhozhij SV, Vinothkumar R, Berman JN. 2016. A guide to computational tools and design strategies for genome editing experiments in zebrafish using CRISPR/Cas9. Zebrafish. 13(1):70-73. doi: 10.1089/zeb.2015.1158.
63. Psenicka M, Saito T, Linhartova Z, Gazo I. 2015. Isolation and transplantation of sturgeon early stage germ cells. Theriogenology. 83(6):1085-1092. doi:10.1016/j.theriogenology. 2014.12.010.
64. Saito T, Kazeto RG, Arai K, Yamaha E. 2008. Xenogenesis in teleost fish through generation of germ-line chimeras by single primordial germ cell transplantation. Biol Reprod 78(1):159-166. doi: 10.1095/biolreprod.107.060038.
65. Sato M, Morita T, Katayama N, Yoshizaki G. 2014. Production of genetically diversified fish seeds using spermatogonial transplantation. Aquaculture. 422-423:218-224. doi: 10.1016/j.aquaculture.2013.12.016.
66. Shang M, Su B, Lipke E, Perera DA, Li C, Qin Z, Li Y, Dunn DA, Cek S, Peatman E, Dunham RA. 2015. Spermatogonial stem cells specific marker identification in channel catfish Ictalurus punctatus and Blue Catfish I. furcatus. Fish Physiol Biochem. 41(6):1545-1556. doi: 10.1007/s10695-015-0106-1.
67. Shikina S, Nagasawa K, Hayashi M, Furuya M, Iwasaki Y, Yoshizaki G. 2013. Short-term in vitro culturing improves transplant ability of type a spermatogonia in Rainbow trout (Oncorhynchus mykiss). Mol Reprod Dev. 80(9):763-773. doi: 10.1002/mrd.22208.
68. Sosa MAG, De Gasperi R, Elder GA. 2010. Animal transgenesis: an overview. Brain Struct Funct. 214(2-3):91-109. doi: 10.1007/s00429-009-0230-8.
69. Staal FJT, Spaink HP, Fibbe WE. 2016. Visualizing human hematopoietic stem cell trafficking in vivo using zebrafish xenograft model. Stem Cells Dev. 25(4):360-365. doi: 10.1089/scd.2015.0195.
70. Tanaka M, Nakamura S, Saito D, Kobayashi K, Nishimura T. 2011. Ovarian structures that support reproductive cycle germ line stem cells and their niche structure in ovary. Indian J Sci Technol. 4(8): 93-94.
71. Taylor KL, Grant NJ. Temperley ND, Patton EE. 2010. Small molcule screening in zebra fish: an in vivo approach to identifying new chemical tools and drug leads. Cell Commun Signaling, 8(11):1-14. doi: 10.1186/1478-811X-8-11.
72. Tesarik J. 2002. Reproductive semi-cloning respecting biparental embryo origin embryos from syngamy between a gamete and a haploidized somatic cell. Hum Reprod. 17(8):1933-1937. doi: 10.1093/humrep/17.8.1933.
73. Tesarik J, Mendoza C. 2003. Somatic cell haploidization: an update. Reprod Biomed Online, 6(1):60-65. doi: 10.1016/S1472-6483(10)62056-1.
74. Tessarollo L, Palko ME, Akagi K, Coppola V. 2009. Gen targeting in Mouse embryonic stem cells. Methods Mol Biol. 530:141-164. doi: 10.1007/978-1-59745-471-1_8.
75. Thomson JA, Itskovits-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. 1998. Embryonic stem cell lines derived from human blastocysts. Science, 282(5391):1145-1147. doi: 10.1126/science.282.5391.1145.
76. Tsai HJ. 2008. Use of transgenic fish possessing special genes as model organisms and potential applications. J Genet Mol Biol. 19(1):22-38.
77. Wakamatsu Y, Ozato K, Hashimoto H, Kinoshita M, Sakaguchi M, Iwamatsu T, Hyodo-Taguchi Y, Tomita H. 1993. Generation of germ-line chimeras in medaka (Oryzias latipes). Mol Mar Biol Biotechnol. 2:325-332.
78. Wakamatsu Y, Ozato K, Sasado T. 1994. Establishment of a pluripotent cell line derived from a medaka (Oryzias latipes) blastula embryo. Mol Mar Biol Biotechnol, 3(4):185–191. doi:10.1016/S0925-4773(96)00596-5.
79. Wan Y, Almeida AD, Rulands S, Chalour N Muresan L, Wu Y, Simons BD, He J, Harris W. 2016. The ciliary marginal zone of the zebrafish retina: clonal and time-lapse analysis of a continuously growing tissue. Development. 143(7):1099-1107. doi: 10.1242/dev.133314.
80. Wong TT, Crodian J, Collodi P. 2011. Zebra fish Germ line Chimeras Produced by Transplantation of Ovarian Germ Cells into Sterile Host Larvae. Biol Reprod. 84(6):1190-1197. doi: 10.1095/biolreprod.110.088427.
81. Wong TT, Collodi P. 2012. Application of fish stem cell technology to aquaculture and marine biotechnology. In: Fletcher GL. Rise M L. eds. Aquaculture Biotechnology. Wiley. p.193-206. doi: 10.1002/9780470963159.ch12.
82. Yan Y, Du J, Chen T, Yi M, Li M, Wang S, Li CM, Hong Y. 2009. Establishment of medakafish as a model for stem cell-based gene therapy: Efficient gene delivery and potential chromosomal integration by baculoviral vectors. Exp Cell Res. 315(13):2322-2331. doi: 10.1016/j.yexcr.2009.04.015.
83. Yan Y, Hong N, Chen T, Li M, Wang T, Guan G, Qiao Y, Chen S, Schartl M, Li CM, Hong Y. 2013. P53 Gene targeting by homologous recombination in fish ES cells. PLOSone. 8(3):1-9. doi: 10.1371/journal.pone.0059400.
84. Yazawa R, Takeuchi Y, Morita T, Ishida M, Yoshizaki G. 2013. The Pacific Bluefin tuna (Thunnus orientalis) dead end gene is suitable as a specific molecular marker of type a spermatogonia. Mol Reprod Dev. 80(10):871-880. doi: 10.1002/mrd.22224.
85. Yi M, Hong N, Hong Y. 2009. Generation of medaka fish haploid embryonic stem cells. Science, 326(5951): 430-433. doi: 10.1126/science.1175151.
86. Yi, M, Hong N, Hong Y. 2010. Derivation and characterization of haploid embryonic stem cell cultures in medaka fish. Nat Protoc. 5(8): 1418-1430. doi: 10.1038/nprot.2010. 104.
87. Yoshizaki G, Takeuchi Y, Kobayashi T, Ihara S, Takeuchi T. 2002. Primordial germ cells: the blueprint for a piscine life. Fish Physiol Biochem. 26(1); 3-12. doi: 10.1023/A: 1023388317621.
88. Yoshizaki G, Ichikawa M, Hayashi M, Iwasaki Y, Miwa M, Shikina S, Okutsu T. 2010a. Sexual plasticity of ovarian germ cells in rainbow trout. Development. 137(8):1227-1230. doi: 10.1242/dev.044982.
89. Yoshizaki G, Okutsu T, Ichikawa M, Hayashi M, Takeuchi Y. 2010b. Sexual plasticity of rainbow trout germ cells. Anim Reprod. 3(7): 187-196.
90. Yoshizaki G, Okutsu T, Morita T, Terasawa M, Yazawa R, Takeuchi Y. 2012. Biological characteristics of fish germ cells and their applications to developmental biotechnology. Reprod Domest Anim. 47(4):187-92. doi: 10.1111/j.1439-0531.2012. 02074.