Analysis of gene expression in normal and neoplastic human testis: New roles of RNA

International Journal of Andrology

Volumn 30, Issue 4, 2007, Pages 316-327

  Novotny, G W ^a   Nielsen, J E ^a   Sonne, S B ^a   Skakkebaek, N E ^a   Rajpert De Meyts, E ^a   Leffers, H ^a  

^a Rigshospitalet   (Denmark)

Author keywords

Carcinoma in situ; In situ hybridization; MicroRNA; mRNA; Non coding RNA; Sense antisense transcript; Testis

Indexed keywords

MESSENGER RNA; MICRORNA; RNA;

ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC REGULATION; HUMAN; HUMAN TISSUE; MALE; PRIORITY JOURNAL; PROTEIN FUNCTION; TESTIS TUMOR;

EID: 34547919948     PISSN: 01056263     EISSN: 13652605     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2007.00773.x     Document Type: Article

References (65)

1. Almstrup, K., Hoei-Hansen, C. E., Wirkner, U., Blake, J., Schwager, C., Ansorge, W., Nielsen, J. E., Skakkebaek, N. E., Rajpert-De Meyts, E. Leffers, H. (2004) Embryonic stem cell-like features of testicular carcinoma in situ revealed by genome-wide gene expression profiling. Cancer Research 64, 4736 4743.
2. Almstrup, K., Hoei-Hansen, C. E., Nielsen, J. E., Wirkner, U., Ansorge, W., Skakkebaek, N. E., Rajpert-De Meyts, E. Leffers, H. (2005) Genome-wide gene expression profiling of testicular carcinoma in situ progression into overt tumours. British Journal of Cancer 92, 1934 1941.
3. Almstrup, K., Leffers, H., Lothe, R. A., Skakkebaek, N. E., Sonne, S. B., Nielsen, J. E., Rajpert De-Meyts, E. Skotheim, R. I. (2007) Re-analysis of joint microarray data on testicular carcinoma in situ. International Journal of Andrology (in press).
4. Aravin, A., Gaidatzis, D., Pfeffer, S., Lagos-Quintana, M., Landgraf, P., Iovino, N. et al. (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442, 203 207.
5. Balhorn, R., Weston, S., Thomas, C. Wyrobek, A. J. (1984) DNA packaging in mouse spermatids. Synthesis of protamine variants and four transition proteins. Experimental Cell Research 150, 298 308.
6. Barad, O., Meiri, E., Avniel, A., Aharonov, R., Barzilai, A., Bentwich, I. et al. (2004) MicroRNA expression detected by oligonucleotide microarrays: system establishment and expression profiling in human tissues. Genome Research 14, 2486 2494.
7. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281 297.
8. Baskerville, S. Bartel, D. P. (2005) Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11, 241 247.
9. Batistatou, A., Scopa, C. D., Ravazoula, P., Nakanishi, Y., Peschos, D., Agnantis, N. J., Hirohashi, S. Charalabopoulos, K. A. (2005) Involvement of dysadherin and E-cadherin in the development of testicular tumours. British Journal of Cancer 93, 1382 1387.
10. Bentwich, I., Avniel, A., Karov, Y., Aharonov, R., Gilad, S., Barad, O. et al. (2005) Identification of hundreds of conserved and nonconserved human microRNAs. Nature Genetics 37, 766 770.
11. Bhattacharyya, S. N., Habermacher, R., Martine, U., Closs, E. I. Filipowicz, W. (2006) Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111 1124.
12. Chan, W. Y., Wu, S. M., Ruszczyk, L., Law, E., Lee, T. L., Baxendale, V., Lap-Yin Pang, A. Rennert, O. M. (2006) The complexity of antisense transcription revealed by the study of developing male germ cells. Genomics 87, 681 692.
13. Cheng, J., Kapranov, P., Drenkow, J., Dike, S., Brubaker, S., Patel, S. et al. (2005) Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 308, 1149 1154.
14. Chu, C. Y. Rana, T. M. (2006) Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. Public Library of Science Biology 4, e210.
15. Cummins, J. M., He, Y., Leary, R. J., Pagliarini, R., Diaz, L. A., Jr., Sjoblom, T. et al. (2006) The colorectal microRNAome. Proceedings of the National Academy of Sciences of the United States of America 103, 3687 3692.
16. Doench, J. G., Petersen, C. P. Sharp, P. A. (2003) siRNAs can function as miRNAs. Genes & Development 17, 438 442.
17. Faghihi, M. A. Wahlestedt, C. (2006) RNA interference is not involved in natural antisense mediated regulation of gene expression in mammals. Genome Biology 7, R38.
18. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. Mello, C. C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806 811.
19. Girard, A., Sachidanandam, R., Hannon, G. J. Carmell, M. A. (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442, 199 202.
20. Giwercman, A., Cantell, L. Marks, A. (1991) Placental-like alkaline phosphatase as a marker of carcinoma-in-situ of the testis. Comparison with monoclonal antibodies M2A and 43-9F. Acta pathologica, microbiologica, et immunologica Scandinavica 99, 586 594.
21. Griffiths-Jones, S. (2004) The microRNA registry. Nucleic Acids Research 32, D109 D111.
22. Griffiths-Jones, S., Grocock, R. J., van Dongen, S., Bateman, A. Enright, A. J. (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Research 34, D140 D144.
23. Grivna, S. T., Beyret, E., Wang, Z. Lin, H. (2006) A novel class of small RNAs in mouse spermatogenic cells. Genes & Development 20, 1709 1714.
24. Harrison, K. A., Druey, K. M., Deguchi, Y., Tuscano, J. M. Kehrl, J. H. (1994) A novel human homeobox gene distantly related to proboscipedia is expressed in lymphoid and pancreatic tissues. The Journal of Biological Chemistry 269, 19968 19975.
25. Hecht, N. B. (1998) Molecular mechanisms of male germ cell differentiation. Bioessays 20, 555 561.
26. Hoei-Hansen, C. E., Nielsen, J. E., Almstrup, K., Hansen, M. A., Skakkebaek, N. E., Rajpert-DeMeyts, E. Leffers, H. (2004) Identification of genes differentially expressed in testes containing carcinoma in situ. Molecular Human Reproduction 10, 423 431.
27. Hoei-Hansen, C. E., Rajpert-De Meyts, E., Daugaard, G. Skakkebaek, N. E. (2005) Carcinoma in situ testis, the progenitor of testicular germ cell tumours: a clinical review. Annals of Oncology 16, 863 868.
28. Honecker, F., Kersemaekers, A. M., Molier, M., Van Weeren, P. C., Stoop, H., De Krijger, R. R., Wolffenbuttel, K. P., Oosterhuis, W., Bokemeyer, C. Looijenga, L. H. (2004) Involvement of E-cadherin and beta-catenin in germ cell tumours and in normal male fetal germ cell development. The Journal of Pathology 204, 167 174.
29. Katayama, S., Tomaru, Y., Kasukawa, T., Waki, K., Nakanishi, M., Nakamura, M. et al. (2005) Antisense transcription in the mammalian transcriptome. Science 309, 1564 1566.
30. Kiyosawa, H., Yamanaka, I., Osato, N., Kondo, S. Hayashizaki, Y. (2003) Antisense transcripts with FANTOM2 clone set and their implications for gene regulation. Genome Research 13, 1324 1334.
31. Kiyosawa, H., Mise, N., Iwase, S., Hayashizaki, Y. Abe, K. (2005) Disclosing hidden transcripts: mouse natural sense-antisense transcripts tend to be poly(A) negative and nuclear localized. Genome Research 15, 463 474.
32. Lau, N. C., Lim, L. P., Weinstein, E. G. Bartel, D. P. (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294, 858 862.
33. Lavorgna, G., Dahary, D., Lehner, B., Sorek, R., Sanderson, C. M. Casari, G. (2004) In search of antisense. Trends in Biochemical Sciences 29, 88 94.
34. Lee, K., Haugen, H. S., Clegg, C. H. Braun, R. E. (1995) Premature translation of protamine 1 mRNA causes precocious nuclear condensation and arrests spermatid differentiation in mice. Proceedings of the National Academy of Sciences of the United States of America 92, 12451 12455.
35. Lee, Y., Jeon, K., Lee, J. T., Kim, S. Kim, V. N. (2002) MicroRNA maturation: stepwise processing and subcellular localization. The EMBO Journal 21, 4663 4670.
36. Lehmann, K. Schmidt, U. (2003) Group II introns: structure and catalytic versatility of large natural ribozymes. Critical Reviews in Biochemistry and Molecular Biology 38, 249 303.
37. Liu, C. G., Calin, G. A., Meloon, B., Gamliel, N., Sevignani, C., Ferracin, M. et al. (2004) An oligonucleotide microchip for genome-wide microRNA profiling in human and mouse tissues. Proceedings of the National Academy of Sciences of the United States of America 101, 9740 9744.
38. Liu, J., Rivas, F. V., Wohlschlegel, J., Yates, J. R. 3rd., Parker, R. Hannon, G. J. (2005) A role for the P-body component GW182 in microRNA function. Nature Cell Biology 7, 1261 1266.
39. Mattick, J. S. Makunin, I. V. (2006) Non-coding RNA. Human Molecular Genetics 15 Spec No 1, R17 R29.
40. Mineno, J., Okamoto, S., Ando, T., Sato, M., Chono, H., Izu, H. et al. (2006) The expression profile of microRNAs in mouse embryos. Nucleic Acids Research 34, 1765 1771.
41. Misra, S., Crosby, M. A., Mungall, C. J., Matthews, B. B., Campbell, K. S., Hradecky, P. et al. (2002) Annotation of the Drosophila melanogaster euchromatic genome: a systematic review. Genome Biology 3. research 0083.1-0083.22.
42. Nielsen, J. E., Hansen, M. A., Jorgensen, M., Tanaka, M., Almstrup, K., Skakkebaek, N. E. Leffers, H. (2003) Germ cell differentiation-dependent and stage-specific expression of LANCL1 in rodent testis. European Journal of Histochemistry 47, 215 222.
43. Nissen, P., Hansen, J., Ban, N., Moore, P. B. Steitz, T. A. (2000) The structural basis of ribosome activity in peptide bond synthesis. Science 289, 920 930.
44. Novotny, G. W., Sonne, S. B., Nielsen, J. E., Jonstrup, S. P., Hansen, M. A., Skakkebaek, N. E., Rajpert De-Meyts, E., Kjems, J. Leffers, H. (2007) Translational repression of E2F1 mRNA in carcinoma in situ and normal testis correlates with expression of the miR-17-92 cluster. Cell Death and Differentiation 14, 879 882.
45. O'Donnell, K. A., Wentzel, E. A., Zeller, K. I., Dang, C. V. Mendell, J. T. (2005) c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435, 839 843.
46. Olsen, P. H. Ambros, V. (1999) The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Developmental Biology 216, 671 680.
47. Osato, N., Yamada, H., Satoh, K., Ooka, H., Yamamoto, M., Suzuki, K. et al. (2003) Antisense transcripts with rice full-length cDNAs. Genome Biology 5, R5.
48. Rajpert-De Meyts, E. (2006) Developmental model for the pathogenesis of testicular carcinoma in situ: genetic and environmental aspects. Human Reproduction Update 12, 303 323.
49. Rehwinkel, J., Behm-Ansmant, I., Gatfield, D. Izaurralde, E. (2005) A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 11, 1640 1647.
50. Schwarz, D. S., Hutvagner, G., Du, T., Xu, Z., Aronin, N. Zamore, P. D. (2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell 115, 199 208.
51. Sherr, C. J. McCormick, F. (2002) The RB and p53 pathways in cancer. Cancer Cell 2, 103 112.
52. Skakkebaek, N. E. (1972) Possible carcinoma-in-situ of the testis. Lancet, 2, 516 517.
53. Skotheim, R. I., Lind, G. E., Monni, O., Nesland, J. M., Abeler, V. M., Fossa, S. D. et al. (2005) Differentiation of human embryonal carcinomas in vitro and in vivo reveals expression profiles relevant to normal development. Cancer Research 65, 5588 5598.
54. Sonne, S. B., Hoei-Hansen, C. E., Nielsen, J. E., Herlihy, A. S., Andersson, A. M., Almstrup, K., Daugaard, G., Skakkebaek, N. E., Leffers, H. Rajpert-De Meyts, E. (2006) CDH1 (E-cadherin) in testicular germ cell neoplasia: suppressed translation of mRNA in pre-invasive carcinoma in situ but increased protein levels in advanced tumours. Acta pathologica, microbiologica, et immunologica Scandinavica 114, 549 558.
55. Steger, K. (1999) Transcriptional and translational regulation of gene expression in haploid spermatids. Anatomy and Embryology 199, 471 487.
56. Steger, K. (2001) Haploid spermatids exhibit translationally repressed mRNAs. Anatomy and Embryology 203, 323 334.
57. Steger, K., Pauls, K., Klonisch, T., Franke, F. E. Bergmann, M. (2000) Expression of protamine-1 and -2 mRNA during human spermiogenesis. Molecular Human Reproduction 6, 219 225.
58. Thomson, J. M., Parker, J., Perou, C. M. Hammond, S. M. (2004) A custom microarray platform for analysis of microRNA gene expression. Nature Methods 1, 47 53.
59. Voorhoeve, P. M., le Sage, C., Schrier, M., Gillis, A. J., Stoop, H., Nagel, R. et al. (2006) A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 124, 1169 1181.
60. Watanabe, T., Takeda, A., Tsukiyama, T., Mise, K., Okuno, T., Sasaki, H., Minami, N. Imai, H. (2006) Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes & Development 20, 1732 1743.
61. Wykes, S. M., Nelson, J. E., Visscher, D. W., Djakiew, D. Krawetz, S. A. (1995) Coordinate expression of the PRM1, PRM2, and TNP2 multigene locus in human testis. DNA and Cell Biology 14, 155 161.
62. Yamada, K., Lim, J., Dale, J. M., Chen, H., Shinn, P., Palm, C. J. et al. (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302, 842 846.
63. Yelin, R., Dahary, D., Sorek, R., Levanon, E. Y., Goldstein, O., Shoshan, A. et al. (2003) Widespread occurrence of antisense transcription in the human genome. Nature Biotechnology 21, 379 386.
64. Yu, Z., Raabe, T. Hecht, N. B. (2005) MicroRNA Mirn122a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage. Biology of Reproduction 73, 427 433.
65. Zeng, Y., Yi, R. Cullen, B. R. (2003) MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proceedings of the National Academy of Sciences of the United States of America 100, 9779 9784.