Identification of a molecular marker for type A spermatogonia by microarray analysis using gonadal cells from pvasa-GFP transgenic rainbow trout (Oncorhynchus mykiss)

Molecular Reproduction and Development

Volumn 76, Issue 3, 2009, Pages 246-254

  Yano, Ayaka ^a   Von Schalburg, Kris ^b   Cooper, Glenn ^b   Koop, Ben F ^b   Yoshizaki, Goro ^a,c  

^a TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

^b UNIVERSITY OF VICTORIA   (Canada)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GREEN FLUORESCENT PROTEIN; MOLECULAR MARKER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE STRUCTURE; GFP GENE; GONAD; MALE; MDH1 GENE; MICROARRAY ANALYSIS; NONHUMAN; NOTCH1 GENE; NUCLEOTIDE SEQUENCE; PFKFB4 GENE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAINBOW TROUT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RTILI GENE; SALMONID; SOMATIC CELL; SPERMATOGONIUM; SPERMATOGONIUM TYPE A; SPERMATOGONIUM TYPE B; TESTIS; UROD GENE; VASA GENE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOLOGICAL MARKERS; EXPRESSED SEQUENCE TAGS; FISH PROTEINS; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; IN SITU HYBRIDIZATION, FLUORESCENCE; LUMINESCENT AGENTS; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ONCORHYNCHUS MYKISS; PHYLOGENY; RECEPTOR, NOTCH1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPERMATOGONIA; TESTIS;

ONCORHYNCHUS MYKISS; SALMONIDAE;

EID: 61449106555     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.20947     Document Type: Article

References (53)

1. Artavanis-Tsakonas S, Rand MD, Lake RJ. 1999. Notch signaling: Cell fate control and signal integration in development. Science 284:770-776.
2. Artavanis-Tsakonas S, Matsuno K, Fortini ME. 1995. Notch signaling. Science 268:225-232.
3. Austin J, Kimble J. 1987. Glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51:589-599.
4. Austin J, Kimble J. 1989. Transcript analysis of glp-1 and lin-12, homologous genes required for cell interactions during development of C. elegans. Cell 58:565-571.
5. Bando H, Atsumi T, Nishio T, Niwa H, Mishima S, Shimizu C, Yoshioka N, Bucala R, Koike T. 2005. Phosphorylation of the 6-phosphofructo-2-kinase/ fructose 2,6-bisphosphatase/PFKFB3 family of glycolytic regulators in human cancer. Clin Cancer Res 11:5784-5792.
6. Billard R. 1986. Spermatogenesis and spermatology of some teleost fish species. Reprod Nutr Dev 2:877-920.
7. Bobarykina AY, Minchenko DO, Opentanova IL, Moenner M, Caro J, Esumi H, Minchenko OH. 2006. Hypoxic regulation of PFKFB-3 and PFKFB-4 gene expression in gastric and pancreatic cancer cell lines and expression of PFKFB genes in gastric cancers. Acta Biochim Pol 53:789-799.
8. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG, Braun RE. 2004. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 36:647-652.
9. Clark MD, Hennig S, Herwig R, Clifton SW, Marra MA, Lehrach H, Johnson SL, WU-GSC EST Group. 2001. An oligonucleotide fingerprint normalized and expressed sequence tag characterized zebrafish cDNA library. Genome Res 11:1594-1602.
10. Clark MS, Edwards YJ, Peterson D, Clifton SW, Thompson AJ, Sasaki M, Suzuki Y, Kikuchi K, Watabe S, Kawakami K, Sugano S, Elgar G, Johnson SL. 2003. Fugu ESTs: New resources for transcription analysis and genome annotation. Genome Res 13:2747-2753.
11. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukh- wani M, Orwig KE, Wolgemuth DJ, Pandolfi PP. 2004. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 36:653-659.
12. Crittenden SL, Troemel ER, Evans TC, Kimble J. 1994. GLP-1 is localized to the mitotic region of the C. elegans germ line. Development 120:2901-2911.
13. Dirami G, Ravindranath N, Achi MV, Dym M. 2001. Expression of Notch pathway components in spermatogonia and Sertoli cells of neonatal mice. J Androl 22:944-952.
14. Douglas SE. 2006. Microarray studies of gene expression in fish. OMICS 10:474-489.
15. Endo M, Oguri M. 1995. Chapter 8, Kidney. In: Takashima F, Hibiya T, editors. An atlas of fish histology: normal and pathological features. 2nd edition. New York: Fischer. pp 116-127.
16. Giuili G, Tomljenovic A, Labrecque N, Oulad-Abdelghani M, Rassoulzadegan M, Cuzin F. 2002. Murine spermatogonial stem cells: Targeted transgene expression and purification in an active state. EMBO Rep 3:753-759.
17. Gómez M, Manzano A, Navarro-Sabaté A, Duran J, Obach M, Perales JC, Bartrons R. 2005. Specific expression of pfkfb4 gene in spermatogonia germ cells and analysis of its 5'-flanking region. FEBS Lett 17:357-362.
18. Gong Z. 1999. Zebrafish expressed sequence tags and their applications. Methods Cell Biol 60:213-233.
19. Greenwald I. 1998. LIN-12/Notch signaling: Lessons from worms and flies. Genes Dev 12:1751-1762.
20. Hayashi T, Kageyama Y, Ishizaka K, Xia G, Kihara K, Oshima H. 2001. Requirement of Notch 1 and its ligand jagged 2 expressions for spermatogenesis in rat and human testes. J Androl 22:999-1011.
21. Hofmann MC, Braydich-Stolle L, Dym M. 2005. Isolation of male germ-line stem cells: Influence of GDNF. Dev Biol 279:114-124.
22. Katogi R, Nakatani Y, Shin-i T, Kohara Y, Inohaya K, Kudo A. 2004. Large-scale analysis of the genes involved in fin regeneration and blastema formation in the medaka, Oryzias latipes. Mech Dev 121:861-872.
23. Kobayashi T, Yoshizaki G, Takeuchi Y, Takeuchi T. 2004. Isolation of highly pure and viable primordial germ cells from rainbow trout by GFP-dependent flow cytometry. Mol Reprod Dev 67:91-100.
24. Kubota H, Avarbock MR, Brinster RL. 2003. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Natl Acad Sci USA 100:6487-6492.
25. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, Saarma M, Sariola H. 2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287:1489-1493.
26. Minchenko OH, Opentanova IL, Ogura T, Minchenko DO, Komi-sarenko SV, Caro J, Esumi H. 2005. Expression and hypoxia-responsiveness of 6-phosphofructo-2- kinase/fructose-2,6-bisphosphatase 4 in mammary gland malignant cell lines. Acta Biochim Pol 52:881-888.
27. Mori S, Kadokawa Y, Hoshinaga K, Marunouchi T. 2003. Sequential activation of Notch family receptors during mouse spermatogenesis. Dev Growth Differ 45:7-13.
28. Nakamura M, Okinaga S, Arai K. 1984. Metabolism of pachytene primary spermatocytes from rat testes: Pyruvate maintenance of adenosine triphosphate level. Biol Reprod 30:1187-1197.
29. Nye JS, Kopan R. 1995. Vertebrate ligands for Notch. Curr Biol 5:966-969.
30. Ohmura M, Yoshida S, Ide Y, Nagamatsu G, Suda T, Ohbo K. 2004. Spatial analysis of germ stem cell development in Oct-4/EGFP transgenic mice. Arch Histol Cytol 67:285-296.
31. Okutsu T, Suzuki K, Takeuchi Y, Takeuchi T, Yoshizaki G. 2006. Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. Proc Natl Acad Sci USA 103:2725-2729.
32. Okutsu T, Shikina S, Kanno M, Takeuchi Y, Yoshizaki G. 2007. Production of trout offspring from triploid salmon parents. Science 317:1517.
33. Patiño R, Takashima F. 1995. Chapter 9 Gonads. In: Takashima F, Hibiya T, editors. An atlas of fish histology: Normal and pathological features. 2nd edition. New York: Fischer. p 128-153.
34. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002-2007.
35. Pudney J. 1995. Spermatogenesis in nonmammalian vertebrates. Microsc Res Tech 32:459-497.
36. Rise ML, von Schalburg KR, Brown GD, Mawer MA, Devlin RH, Kuipers N, Busby M, Beetz-Sargent M, Alberto R, Gibbs AR, Hunt P, Shukin R, Zeznik JA, Nelson C, Jones SR, Smailus DE, Jones SJ, Schein JE, Marra MA, Butterfield YS, Stott JM, Ng SH, Davidson WS, Koop BF. 2004. Development and application of a salmonid EST database and cDNA microarray: Data mining and interspecific hybridization characteristics. Genome Res 14:478-490.
37. Saal LH, Troein C, Vallon-Christersson J, Gruvberger S, Borg A, Peterson C. 2002. BioArray Software Environment (BASE): a platform for comprehensive management and analysis of microarray data. Genome Biol 3: software 0003.1-0003.6.
38. Sahin Z, Bayram Z, Celik-Ozenci C, Akkoyunlu G, Seval Y, Erdogru T, Ustunel I, Baykara M, Demir R. 2005. Effect of experimental varicocele on the expressions of Notch 1, 2 and 3 in rat testes: An immunohistochemical study. Fertil Steril 83:86-94.
39. 6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci USA 96:5504-5509.
40. Shinohara T, Avarbock MR, Brinster RL. 2000. Functional analysis of spermatogonial stem cells in Steel and cryptorchid infertile mouse models. Dev Biol 220:401-411.
41. Shinohara T, Orwig KE, Avarbock MR, Brinster RL. 2000. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc Natl Acad Sci USA 97:8346-8351.
42. Sawatari E, Shikina S, Takeuchi T, Yoshizaki G. 2007. A novel transforming growth factor-β superfamily member expressed in gonadal somatic cells enhances primordial germ cell and spermatogonial proliferation in rainbow trout (Oncorhynchus mykiss). Dev Biol 301:266-275.
43. Tax FE, Yeargers JJ, Thomas JH. 1994. Sequence of C. elegans lag-2 reveals a cell-signalling domain shared with Delta and Serrate of Drosophila. Nature 368:150-154.
44. Tokuda M, Kadokawa Y, Kurahashi H, Marunouchi T. 2007. CDH1 is a specific marker for undifferentiated spermatogonia in mouse testes. Biol Reprod 76:130-141.
45. Ton C, Hwang DM, Dempsey AA, Tang HC, Yoon J, Lim M, Mably JD, Fishman MC, Liew CC. 2000. Identification, characterization, and mapping of expressed sequence tags from an embryonic zebrafish heart cDNA library. Genome Res 10:1915-1927.
46. Uyeda K, Furuya E, Richards CS, Yokoyama M. 1982. Fructose- 2,6-P2, chemistry and biological function. Mol Cell Biochem 48:97-120.
47. Varnum-Finney B, Purton LE, Yu M, Brashem-Stein C, Flowers D, Staats S, Moore KA, Le Roux I, Mann R, Gray G, Artavanis-Tsakonas S, Bernstein ID. 1998. The Notch ligand, Jagged-1, influences the development of primitive hematopoietic precursor cells. Blood 91:4084-4091.
48. von Schalburg KR, Rise ML, Cooper GA, Brown GD, Gibbs AR, Nelson CC, Davidson WS, Koop BF. 2005. Fish and chips: Various methodologies demonstrate utility of a 16,006-gene salmonid microarray. BMC Genom 6:126.
49. von Schalburg KR, McCarthy SP, Rise ML, Hutson JC, Davidson WS, Koop BF.2006. Expression of morphogenic genes in mature ovarian and testicular tissues: Potential stem-cell niche markers and patterning factors. Mol Reprod Dev 73:142-152.
50. von Schonfeldt V, Wistuba J, Schlatt S. 2004. Notch-1, c-kit and GFRalpha-1 are developmentally regulated markers for premeiotic germ cells. Cytogenet Genome Res 105:235-239.
51. Yano A, Suzuki K, Yoshizaki G. 2008. Flow-cytometric isolation of testicular germ cells from rainbow trout (Oncorhynchus mykiss) carrying the green fluorescent protein gene driven by trout vasa regulatory regions. Biol Reprod 78:151-158.
52. Yochem J, Greenwald I. 1989. Glp-1 and lin-12, genes implicated in distinct cell-cell interactions in C. elegans, encode similar transmembrane proteins. Cell 58:553-563.
53. Yoshida S, Takakura A, Ohbo K, Abe K, Wakabayashi J, Yamamoto M, Suda T, Nabeshima Y. 2004. Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev Biol 269:447-458.