A biopsy sample reduction approach to identify significant alterations of the testicular transcriptome in the presence of Y-chromosomal microdeletions that are independent of germ cell composition

Human Genetics

Volumn 128, Issue 4, 2010, Pages 421-431

  Cappallo Obermann, Heike ^a   Von Kopylow, Kathrein ^a   Schulze, Wolfgang ^a   Spiess, Andrej Nikolai ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; SEMINAL PLASMA PROTEIN;

ARTICLE; CHROMOSOME DELETION Y; COHORT ANALYSIS; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; GERM CELL; HUMAN; MALE; MEIOSIS; MICROARRAY ANALYSIS; PHENOTYPE; PRIORITY JOURNAL; SERTOLI CELL; SPERMATOGENESIS; TESTIS BIOPSY; Y CHROMOSOMAL MICRODELETION; BIOPSY; CHROMOSOME DELETION; CLUSTER ANALYSIS; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; MALE INFERTILITY; METABOLISM; PATHOLOGY; SERTOLI CELL ONLY SYNDROME; TESTIS; Y CHROMOSOME;

BIOPSY; CHROMOSOME DELETION; CHROMOSOMES, HUMAN, Y; CLUSTER ANALYSIS; COHORT STUDIES; GENE EXPRESSION PROFILING; GERM CELLS; HUMANS; INFERTILITY, MALE; MALE; MEIOSIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEMINAL PLASMA PROTEINS; SERTOLI CELL-ONLY SYNDROME; SPERMATOGENESIS; TESTIS; GENETIC LOCI;

EID: 77957558749     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-010-0865-9     Document Type: Article

References (48)

1. Y Benjamini Y Hochberg 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing J R Stat Soc Ser B 57 289 300
2. A Brazma P Hingamp J Quackenbush G Sherlock P Spellman C Stoeckert J Aach W Ansorge CA Ball HC Causton T Gaasterland P Glenisson FC Holstege IF Kim V Markowitz JC Matese H Parkinson A Robinson U Sarkans S Schulze-Kremer J Stewart R Taylor J Vilo M Vingron 2001 Minimum information about a microarray experiment (MIAME)-toward standards for microarray data Nat Genet 29 365 371 10.1038/ng1201-365 11726920 1:CAS:528:DC%2BD3MXovFamurw%3D (Pubitemid 34326681)
3. DS Cram E Osborne RI McLachlan 2006 Y chromosome microdeletions: implications for assisted conception Med J Aust 185 433 434 17137433
4. DJ Elliott CF Bourgeois A Klink J Stevenin HJ Cooke 2000 A mammalian germ cell-specific RNA-binding protein interacts with ubiquitously expressed proteins involved in splice site selection Proc Natl Acad Sci USA 97 5717 5722 10.1073/pnas.97.11.5717 10823932 1:CAS:528:DC%2BD3cXjvFaktrs%3D (Pubitemid 30367464)
5. PJ Ellis RA Furlong SJ Conner J Kirkman-Brown M Afnan C Barratt DK Griffin NA Affara 2007 Coordinated transcriptional regulation patterns associated with infertility phenotypes in men J Med Genet 44 498 508 10.1136/jmg.2007.049650 17496197 1:CAS:528:DC%2BD2sXhtVensLzF (Pubitemid 47325736)
6. C Feig C Kirchhoff R Ivell O Naether W Schulze AN Spiess 2007 A new paradigm for profiling testicular gene expression during normal and disturbed human spermatogenesis Mol Hum Reprod 13 33 43 10.1093/molehr/gal097 17114209 1:CAS:528:DC%2BD28XhtlChtLjP (Pubitemid 44942722)
7. A Ferlin B Arredi C Foresta 2006 Genetic causes of male infertility Reprod Toxicol 22 133 141 10.1016/j.reprotox.2006.04.016 16806807 1:CAS:528:DC%2BD28Xmslyqur4%3D (Pubitemid 43994384)
8. C Ferras S Fernandes CJ Marques F Carvalho C Alves J Silva M Sousa A Barros 2004 AZF and DAZ gene copy-specific deletion analysis in maturation arrest and Sertoli cell-only syndrome Mol Hum Reprod 10 755 761 10.1093/molehr/gah104 15347736 1:CAS:528:DC%2BD2cXns1Omtrk%3D (Pubitemid 39345134)
9. C Foresta E Moro A Ferlin 2001 Y chromosome microdeletions and alterations of spermatogenesis Endocr Rev 22 226 239 10.1210/er.22.2.226 11294825 1:CAS:528:DC%2BD3MXjsFSntL0%3D (Pubitemid 32458160)
10. Gatta V, Raicu F, Ferlin A, Antonucci I, Scioletti AP, Garolla A, Palka G, Foresta C, Stuppia L (2010) Testis transcriptome analysis in male infertility: new insight on the pathogenesis of oligo-azoospermia in cases with and without AZFc microdeletion. BMC Genomics 11:401
11. C Geoffroy-Siraudin I Aknin-Seiffer C Metzler-Guillemain R Ghalamoun-Slaimi MF Bonzi R Levy MR Guichaoua 2007 Meiotic abnormalities in patients bearing complete AZFc deletion of Y chromosome Hum Reprod 22 1567 1572 10.1093/humrep/dem045 17428878 1:STN:280:DC%2BD2szgvFKjtA%3D%3D (Pubitemid 47055144)
12. K Hucklenbroich J Gromoll M Heinrich C Hohoff E Nieschlag M Simoni 2005 Partial deletions in the AZFc region of the Y chromosome occur in men with impaired as well as normal spermatogenesis Hum Reprod 20 191 197 10.1093/humrep/deh558 15498781 1:CAS:528:DC%2BD2MXisVShtg%3D%3D
13. D Jezek UA Knuth W Schulze 1998 Successful testicular sperm extraction (TESE) in spite of high serum follicle stimulating hormone and azoospermia: correlation between testicular morphology, TESE results, semen analysis and serum hormone values in 103 infertile men Hum Reprod 13 1230 1234 10.1093/humrep/13.5.1230 9647552 1:STN:280:DyaK1czgvFOltQ%3D%3D (Pubitemid 28279175)
14. N Kang-Decker GT Mantchev SC Juneja MA McNiven JM van Deursen 2001 Lack of acrosome formation in Hrb-deficient mice Science 294 1531 1533 10.1126/science.1063665 11711676 1:CAS:528:DC%2BD3MXosFCqsro%3D (Pubitemid 33063925)
15. K Kee VT Angeles M Flores HN Nguyen RA Reijo Pera 2009 Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation Nature 462 222 225 10.1038/nature08562 19865085 1:CAS:528:DC%2BD1MXhtlaksr3L
16. M Kent-First A Muallem J Shultz J Pryor K Roberts W Nolten L Meisner A Chandley G Gouchy L Jorgensen T Havighurst J Grosch 1999 Defining regions of the Y-chromosome responsible for male infertility and identification of a fourth AZF region (AZFd) by Y-chromosome microdeletion detection Mol Reprod Dev 53 27 41 10.1002/(SICI)1098-2795(199905)53:1<27::AID-MRD4>3.0.CO;2-W 10230814 1:CAS:528:DyaK1MXitleju7k%3D (Pubitemid 29222100)
17. SE Kleiman L Yogev R Hauser A Botchan BB Maymon G Paz H Yavetz 2007 Expression profile of AZF genes in testicular biopsies of azoospermic men Hum Reprod 22 151 158 10.1093/humrep/del341 16936303 1:CAS:528:DC%2BD28XhtlChtb3M (Pubitemid 44942679)
18. C Krausz L Quintana-Murci S Barbaux JP Siffroi H Rouba D Delafontaine N Souleyreau-Therville G Arvis JM Antoine E Erdei JP Taar A Tar E Jeandidier G Plessis T Bourgeron JP Dadoune M Fellous K McElreavey 1999 A high frequency of Y chromosome deletions in males with nonidiopathic infertility J Clin Endocrinol Metab 84 3606 3612 10.1210/jc.84.10.3606 10523003 1:CAS:528:DyaK1MXms1OhtLs%3D
19. C Krausz S Degl'Innocenti F Nuti A Morelli F Felici M Sansone G Varriale G Forti 2006 Natural transmission of USP9Y gene mutations: a new perspective on the role of AZFa genes in male fertility Hum Mol Genet 15 2673 2681 10.1093/hmg/ddl198 16893908 1:CAS:528:DC%2BD28Xps1Gnur8%3D (Pubitemid 44400394)
20. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Takamatsu K, Chuma S, Kojima-Kita K, Shiromoto Y, Asada N, Toyoda A, Fujiyama A, Totoki Y, Shibata T, Kimura T, Nakatsuji N, Noce T, Sasaki H, Nakano T (2010) MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev 24:887-892
21. MC Lardone DA Parodi R Valdevenito M Ebensperger A Piottante M Madariaga R Smith R Pommer N Zambrano A Castro 2007 Quantification of DDX3Y, RBMY1, DAZ and TSPY mRNAs in testes of patients with severe impairment of spermatogenesis Mol Hum Reprod 13 705 712 10.1093/molehr/gam057 17881721 1:CAS:528: DC%2BD2sXhsVensb%2FN (Pubitemid 47543409)
22. GL Law MP McGuinness CC Linder MD Griswold 1997 Expression of apolipoprotein E mRNA in the epithelium and interstitium of the testis and the epididymis J Androl 18 32 42 9089066 1:CAS:528:DyaK2sXit12murg%3D
23. J Lian X Zhang H Tian N Liang Y Wang C Liang X Li F Sun 2009 Altered microRNA expression in patients with non-obstructive azoospermia Reprod Biol Endocrinol 7 13 10.1186/1477-7827-7-13 19210773 1:CAS:528:DC%2BD1MXjslCqsL8%3D
24. A Luddi M Margollicci L Gambera F Serafini M Cioni V De Leo P Balestri P Piomboni 2009 Spermatogenesis in a man with complete deletion of USP9Y N Engl J Med 360 881 885 10.1056/NEJMoa0806218 19246359 1:CAS:528:DC%2BD1MXis1Cnsbk%3D
25. CM Luetjens J Gromoll M Engelhardt S Von Eckardstein M Bergmann E Nieschlag M Simoni 2002 Manifestation of Y-chromosomal deletions in the human testis: a morphometrical and immunohistochemical evaluation Hum Reprod 17 2258 2266 10.1093/humrep/17.9.2258 12202411 1:STN:280:DC%2BD38vksVaksQ%3D%3D
26. H Okada A Tajima K Shichiri A Tanaka K Tanaka I Inoue 2008 Genome-wide expression of azoospermia testes demonstrates a specific profile and implicates ART3 in genetic susceptibility PLoS Genet 4 e26 10.1371/journal.pgen.0040026 18266473 1:CAS:528:DC%2BD1cXksFeksbg%3D (Pubitemid 351328543)
27. L Quintana-Murci C Krausz E Heyer J Gromoll I Seifer DE Barton T Barrett NE Skakkebaek E Rajpert-De Meyts M Mitchell AC Lee MA Jobling K McElreavey 2001 The relationship between Y chromosome DNA haplotypes and Y chromosome deletions leading to male infertility Hum Genet 108 55 58 10.1007/s004390000424 11214908 1:CAS:528:DC%2BD3MXlsVWrsw%3D%3D (Pubitemid 32140543)
28. N Reynolds B Collier K Maratou V Bingham RM Speed M Taggart CA Semple NK Gray HJ Cooke 2005 Dazl binds in vivo to specific transcripts and can regulate the pre-meiotic translation of Mvh in germ cells Hum Mol Genet 14 3899 3909 10.1093/hmg/ddi414 16278232 1:CAS:528:DC%2BD2MXhtlChsr3L (Pubitemid 43020091)
29. C Ritz AN Spiess 2008 qpcR: an R package for sigmoidal model selection in quantitative real-time polymerase chain reaction analysis Bioinformatics 24 1549 1551 10.1093/bioinformatics/btn227 18482995 1:CAS:528:DC%2BD1cXnvV2rt7g%3D (Pubitemid 351911713)
30. Y Sato K Yoshida T Shinka S Nozawa Y Nakahori T Iwamoto 2006 Altered expression pattern of heat shock transcription factor, Y chromosome (HSFY) may be related to altered differentiation of spermatogenic cells in testes with deteriorated spermatogenesis Fertil Steril 86 612 618 10.1016/j.fertnstert.2006. 01.053 16952509 1:CAS:528:DC%2BD28XhtFCqsL7O (Pubitemid 44307033)
31. T Shinka Y Sato G Chen T Naroda K Kinoshita Y Unemi K Tsuji K Toida T Iwamoto Y Nakahori 2004 Molecular characterization of heat shock-like factor encoded on the human Y chromosome, and implications for male infertility Biol Reprod 71 297 306 10.1095/biolreprod.103.023580 15044259 1:CAS:528: DC%2BD2cXltFKku7g%3D (Pubitemid 38915337)
32. C Sigg C Hedinger 1981 Quantitative and ultrastructural study of germinal epithelium in testicular biopsies with "mixed atrophy" Andrologia 13 412 424 10.1111/j.1439-0272.1981.tb00074.x 7316230 1:STN:280: DyaL38%2FovFeqtA%3D%3D
33. SJ Silber R Alagappan LG Brown DC Page 1998 Y chromosome deletions in azoospermic and severely oligozoospermic men undergoing intracytoplasmic sperm injection after testicular sperm extraction Hum Reprod 13 3332 3337 10.1093/humrep/13.12.3332 9886509 1:CAS:528:DyaK1MXltFOmuw%3D%3D (Pubitemid 29002617)
34. M Simoni E Bakker C Krausz 2004 EAA/EMQN best practice guidelines for molecular diagnosis of y-chromosomal microdeletions. State of the art 2004 Int J Androl 27 240 249 10.1111/j.1365-2605.2004.00495.x 15271204 1:CAS:528:DC%2BD2cXns1GmsLc%3D (Pubitemid 39062086)
35. M Simoni F Tuttelmann J Gromoll E Nieschlag 2008 Clinical consequences of microdeletions of the Y chromosome: the extended Munster experience Reprod Biomed Online 16 289 303 10.1016/S1472-6483(10)60588-3 18284889 1:CAS:528:DC%2BD1cXjt1ylsLY%3D
36. H Skaletsky T Kuroda-Kawaguchi PJ Minx HS Cordum L Hillier LG Brown S Repping T Pyntikova J Ali T Bieri A Chinwalla A Delehaunty K Delehaunty H Du G Fewell L Fulton R Fulton T Graves SF Hou P Latrielle S Leonard E Mardis R Maupin J McPherson T Miner W Nash C Nguyen P Ozersky K Pepin S Rock T Rohlfing K Scott B Schultz C Strong A Tin-Wollam SP Yang RH Waterston RK Wilson S Rozen DC Page 2003 The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes Nature 423 825 837 10.1038/nature01722 12815422 1:CAS:528:DC%2BD3sXks1Kmtbk%3D (Pubitemid 36781267)
37. AN Spiess C Feig W Schulze F Chalmel H Cappallo-Obermann M Primig C Kirchhoff 2007 Cross-platform gene expression signature of human spermatogenic failure reveals inflammatory-like response Hum Reprod 22 2936 2946 10.1093/humrep/dem292 17921478 1:CAS:528:DC%2BD2sXht1Shu7nI (Pubitemid 351696823)
38. K Stouffs W Lissens G Verheyen L Van Landuyt A Goossens H Tournaye A Van Steirteghem I Liebaers 2004 Expression pattern of the Y-linked PRY gene suggests a function in apoptosis but not in spermatogenesis Mol Hum Reprod 10 15 21 10.1093/molehr/gah010 14665702 1:CAS:528:DC%2BD3sXpvVelt74%3D (Pubitemid 38195961)
39. C Sun H Skaletsky B Birren K Devon Z Tang S Silber R Oates DC Page 1999 An azoospermic man with a de novo point mutation in the Y-chromosomal gene USP9Y Nat Genet 23 429 432 10.1038/70539 10581029 1:CAS:528:DyaK1MXnvFOktbs%3D
40. A Tessari E Salata A Ferlin L Bartoloni ML Slongo C Foresta 2004 Characterization of HSFY, a novel AZFb gene on the Y chromosome with a possible role in human spermatogenesis Mol Hum Reprod 10 253 258 10.1093/molehr/gah036 14985478 1:CAS:528:DC%2BD2cXisF2lu74%3D (Pubitemid 38456030)
41. JP Theurillat U Zurrer-Hardi Z Varga A Barghorn E Saller C Frei M Storz S Behnke B Seifert M Fehr D Fink C Rageth C Linsenmeier B Pestalozzi YT Chen A Knuth D Jager H Moch 2008 Distinct expression patterns of the immunogenic differentiation antigen NY-BR-1 in normal breast, testis and their malignant counterparts Int J Cancer 122 1585 1591 10.1002/ijc.23241 18041742 1:CAS:528:DC%2BD1cXivVahs7o%3D (Pubitemid 351294967)
42. PH Vogt 2005 AZF deletions and Y chromosomal haplogroups: history and update based on sequence Hum Reprod Update 11 319 336 10.1093/humupd/dmi017 15890785 1:CAS:528:DC%2BD2MXmvVaksLY%3D (Pubitemid 40895462)
43. PH Vogt A Edelmann S Kirsch O Henegariu P Hirschmann F Kiesewetter FM Kohn WB Schill S Farah C Ramos M Hartmann W Hartschuh D Meschede HM Behre A Castel E Nieschlag W Weidner HJ Grone A Jung W Engel G Haidl 1996 Human Y chromosome azoospermia factors (AZF) mapped to different subregions in Yq11 Hum Mol Genet 5 933 943 10.1093/hmg/5.7.933 8817327 1:CAS:528:DyaK28Xkt1Cntrk%3D (Pubitemid 26232272)
44. PH Vogt CL Falcao R Hanstein J Zimmer 2008 The AZF proteins Int J Androl 31 383 394 10.1111/j.1365-2605.2008.00890.x 18462373 1:CAS:528: DC%2BD1cXhtVWqurjO
45. Y Wang C Barbacioru F Hyland W Xiao KL Hunkapiller J Blake F Chan C Gonzalez L Zhang RR Samaha 2006 Large scale real-time PCR validation on gene expression measurements from two commercial long-oligonucleotide microarrays BMC Genomics 7 59 10.1186/1471-2164-7-59 16551369 1:CAS:528:DC%2BD28XjvVCjur8%3D
46. G Wennemuth S Blocher WB Schill G Aumuller TK Monsees 2003 Bradykinin increases intracellular calcium levels in rat testis peritubular cells via the B2 receptor subtype Br J Pharmacol 138 351 358 10.1038/sj.bjp.0705039 12540526 1:CAS:528:DC%2BD3sXhtlSisbc%3D (Pubitemid 36188597)
47. M Zervakis ME Blazadonakis G Tsiliki V Danilatou M Tsiknakis D Kafetzopoulos 2009 Outcome prediction based on microarray analysis: a critical perspective on methods BMC Bioinformatics 10 53 10.1186/1471-2105-10-53 19200394 1:CAS:528:DC%2BD1MXit1aru7Y%3D
48. SW Zou JC Zhang XD Zhang SY Miao SD Zong Q Sheng LF Wang 2003 Expression and localization of VCX/Y proteins and their possible involvement in regulation of ribosome assembly during spermatogenesis Cell Res 13 171 177 10.1038/sj.cr.7290161 12862317 1:CAS:528:DC%2BD2cXivVSjtbo%3D