Combining RNA and protein profiling data with network interactions identifies genes associated with spermatogenesis in mouse and human

Biology of Reproduction

Volumn 92, Issue 3, 2015, Pages

  Petit, Fabrice G ^a   Kervarrec, Christine ^a   Jamin, Soazik P ^a   Smagulova, Fatima ^a   Hao, Chunxiang ^a   Becker, Emmanuelle ^a   Jégou, Bernard ^a,b   Chalmel, Frédéric ^a   Primig, Michael ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b EHESP SCHOOL OF PUBLIC HEALTH   (France)

Author keywords

Epigenetics; Gene expression; Genomics; Interactome; Male fertility; Microarray; Proteome; RNA Seq; Spermatogenesis

Indexed keywords

1700019N19RIK PROTEIN; FAM71B PROTEIN; HIGH MOBILITY GROUP B4 PROTEIN; MESSENGER RNA; NUCLEAR PROTEIN; NUCLEIC ACID BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXR1; TRANSCRIPTION FACTOR SOX30; TRANSCRIPTION FACTOR ZFP597; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GERM CELL; HUMAN; HUMAN CELL; MALE; MALE FERTILITY; MOUSE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SEMINIFEROUS TUBULE; SERTOLI CELL; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; VASCULAR SMOOTH MUSCLE; AMINO ACID SEQUENCE; ANIMAL; COMPARATIVE STUDY; FERTILITY; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MOLECULAR GENETICS; PROTEIN MICROARRAY; SPECIES DIFFERENCE;

MAMMALIA; RODENTIA;

AMINO ACID SEQUENCE; ANIMALS; FERTILITY; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; MICE; MOLECULAR SEQUENCE DATA; PROTEIN ARRAY ANALYSIS; RNA, MESSENGER; SPECIES SPECIFICITY; SPERMATOGENESIS; TRANSCRIPTION FACTORS;

EID: 84928317326     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.126250     Document Type: Article

References (93)

1. Deutschbauer AM, Williams RM, Chu AM, Davis RW. Parallel phenotypic analysis of sporulation and postgermination growth in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2002; 99: 15530-15535.
2. Enyenihi AH, Saunders WS. Large-scale functional genomic analysis of sporulation and meiosis in Saccharomyces cerevisiae. Genetics 2003; 163: 47-54.
3. Colaiacovo MP, Stanfield GM, Reddy KC, Reinke V, Kim SK, Villeneuve AM. A targeted RNAi screen for genes involved in chromosome morphogenesis and nuclear organization in the Caenorhabditis elegans germline. Genetics 2002; 162:113-128.
4. Handel MA, Lessard C, Reinholdt L, Schimenti J, Eppig JJ. Mutagenesis as an unbiased approach to identify novel contraceptive targets. Mol Cell Endocrinol 2006; 250:201-205.
5. Jamsai D, O'Bryan MK. Mouse models in male fertility research. Asian J Androl 2011; 13:139-151.
6. O'Bryan MK, de Kretser D. Mouse models for genes involved in impaired spermatogenesis. Int J Androl 2006; 29:76-89 (discussion 105-108).
7. Chalmel F, Lardenois A, Evrard B, Mathieu R, Feig C, Demougin P, Gattiker A, Schulze W, Jegou B, Kirchhoff C, Primig M. Global human tissue profiling and protein network analysis reveals distinct levels of transcriptional germline-specificity and identifies target genes for male infertility. Hum Reprod 2012; 27:3233-3248.
8. Chalmel F, Rolland AD, Niederhauser-Wiederkehr C, Chung SS, Demougin P, Gattiker A, Moore J, Patard JJ, Wolgemuth DJ, Jegou B, Primig M. The conserved transcriptome in human and rodent male gametogenesis. Proc Natl Acad Sci U S A 2007; 104:8346-8351.
9. Schultz N, Hamra FK, Garbers DL. A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc Natl Acad Sci U S A 2003; 100:12201-12206.
10. Ellis PJ, Furlong RA, Wilson A, Morris S, Carter D, Oliver G, Print C, Burgoyne PS, Loveland KL, Affara NA. Modulation of the mouse testis transcriptome during postnatal development and in selected models of male infertility. Mol Hum Reprod 2004; 10:271-281.
11. Kim MS, Pinto SM, Getnet D, Nirujogi RS, Manda SS, Chaerkady R, Madugundu AK, Kelkar DS, Isserlin R, Jain S, Thomas JK, Muthusamy B, et al. A draft map of the human proteome. Nature 2014; 509:575-581.
12. Fagerberg L, Hallstrom BM, Oksvold P, Kampf C, Djureinovic D, Odeberg J, Habuka M, Tahmasebpoor S, Danielsson A, Edlund K, Asplund A, Sjostedt E, et al. Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibodybased proteomics. Mol Cell Proteomics 2014; 13:397-406.
13. Ong CT, Corces VG. Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat Rev Genet 2011; 12:283-293.
14. Vermeulen M, Timmers HT. Grasping trimethylation of histone H3 at lysine 4. Epigenomics 2010; 2:395-406.
15. Furey TS. ChIP-seq and beyond: new and improved methodologies to detect and characterize protein-DNA interactions. Nat Rev Genet 2012; 13:840-852.
16. Kittler R, Pelletier L, Buchholz F. Systems biology of mammalian cell division. Cell Cycle 2008; 7:2123-2128.
17. Lipshutz RJ, Fodor SP, Gingeras TR, Lockhart DJ. High density synthetic oligonucleotide arrays. Nat Genet 1999; 21:20-24.
18. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009; 10:57-63.
19. Cox J, Mann M. Quantitative, high-resolution proteomics for data-driven systems biology. Annu Rev Biochem 2011; 80:273-299.
20. Koh GC, Porras P, Aranda B, Hermjakob H, Orchard SE. Analyzing protein-protein interaction networks. J Proteome Res 2012; 11:2014-2031.
21. Ideker T, Krogan NJ. Differential network biology. Mol Syst Biol 2012; 8: 565.
22. Vidal M, Cusick ME, Barabasi AL. Interactome networks and human disease. Cell 2011; 144:986-998.
23. Costanzo MC, Engel SR, Wong ED, Lloyd P, Karra K, Chan ET, Weng S, Paskov KM, Roe GR, Binkley G, Hitz BC, Cherry JM. Saccharomyces genome database provides new regulation data. Nucleic Acids Res 2014; 42:D717-D725.
24. Koscielny G, Yaikhom G, Iyer V, Meehan TF, Morgan H, Atienza-Herrero J, Blake A, Chen CK, Easty R, Di Fenza A, Fiegel T, Grifiths M, et al. The International Mouse Phenotyping Consortium Web Portal, a unified point of access for knockout mice and related phenotyping data. Nucleic Acids Res 2014; 42:D802-D809.
25. Brown SD, Moore MW. The International Mouse Phenotyping Consortium: past and future perspectives on mouse phenotyping. Mamm Genome 2012; 23:632-640.
26. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, Mujica AO, Thomas M, Harrow J, Cox T, Jackson D, Severin J, et al. A conditional knockout resource for the genome-wide study of mouse gene function. Nature 2011; 474:337-342.
27. White JK, Gerdin AK, Karp NA, Ryder E, Buljan M, Bussell JN, Salisbury J, Clare S, Ingham NJ, Podrini C, Houghton R, Estabel J, et al. Genome-wide generation and systematic phenotyping of knockout mice reveals new roles for many genes. Cell 2013; 154:452-464.
28. Schofield PN, Hoehndorf R, Gkoutos GV. Mouse genetic and phenotypic resources for human genetics. Hum Mutat 2012; 33:826-836.
29. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10:R25.
30. Feng J, Liu T, Qin B, Zhang Y, Liu XS. Identifying ChIP-seq enrichment using MACS. Nat Protoc 2012; 7:1728-1740.
31. Gan H, Wen L, Liao S, Lin X, Ma T, Liu J, Song CX, Wang M, He C, Han C, Tang F. Dynamics of 5-hydroxymethylcytosine during mouse spermatogenesis. Nat Commun 2013; 4:1995.
32. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013; 14:R36.
33. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010; 28:511-515.
34. Smyth GK. limma: linear models for microarray data. In: Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S (eds.), Bioinformatics and Computational Biology Solutions Using R and Bioconductor. New York: Springer; 2005:397-420.
35. Thorvaldsdottir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2013; 14:178-192.
36. R Foundation for Statistical Computing [Internet]. Vienna: R Foundation. http://www. R-project.org. Accessed 1 January 2014.
37. Chalmel F, Primig M. The Annotation, Mapping, Expression and Network (AMEN) suite of tools for molecular systems biology. BMC Bioinformatics 2008; 9:86.
38. Coordinators NR. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 2014; 42:D7-D17.
39. Smagulova F, Brick K, Pu Y, Sengupta U, Camerini-Otero RD, Petukhova GV. Suppression of genetic recombination in the pseudoautosomal region and at subtelomeres in mice with a hypomorphic Spo11 allele. BMC Genomics 2013; 14:493.
40. van Dijk EL, Auger H, Jaszczyszyn Y, Thermes C. Ten years of nextgeneration sequencing technology. Trends Genet 2014; 30:418-426.
41. Shoji M, Kawarabayashi T, Harigaya Y, Yamaguchi H, Hirai S, Kamimura T, Sugiyama T. Alzheimer amyloid beta-protein precursor in sperm development. Am J Pathol 1990; 137:1027-1032.
42. Guo Q, Wang Z, Li H, Wiese M, Zheng H. APP physiological and pathophysiological functions: insights from animal models. Cell Res 2012; 22:78-89.
43. van Koningsbruggen S, Dirks RW, Mommaas AM, Onderwater JJ, Deidda G, Padberg GW, Frants RR, van der Maarel SM. FRG1P is localized in the nucleolus, Cajal bodies, and speckles. J Med Genet 2004; 41:e46.
44. Adelman CA, Petrini JH. ZIP4H (TEX11) deficiency in the mouse impairs meiotic double strand break repair and the regulation of crossing over. PLoS Genet 2008; 4:e1000042.
45. Yang F, Gell K, van der Heijden GW, Eckardt S, Leu NA, Page DC, Benavente R, Her C, Hoog C, McLaughlin KJ, Wang PJ. Meiotic failure in male mice lacking an X-linked factor. Genes Dev 2008; 22:682-691.
46. Ward JO, Reinholdt LG, Motley WW, Niswander LM, Deacon DC, Griffin LB, Langlais KK, Backus VL, Schimenti KJ, O'Brien MJ, Eppig JJ, Schimenti JC. Mutation in mouse Hei10, an E3 ubiquitin ligase, disrupts meiotic crossing over. PLoS Genet 2007; 3:e139.
47. Tanabe Y, Hirano A, Iwasato T, Itohara S, Araki K, Yamaguchi T, Ichikawa T, Kumanishi T, Aizawa Y, Takahashi H, Kakita A, Nawa H. Molecular characterization and gene disruption of a novel zinc-finger protein, HIT-4, expressed in rodent brain. J Neurochem 2010; 112: 1035-1044.
48. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P. Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 2008; 2008:420747.
49. Chowdhury TA, Kleene KC. Identification of potential regulatory elements in the 5' and 3' UTRs of 12 translationally regulated mRNAs in mammalian spermatids by comparative genomics. J Androl 2012; 33: 244-256.
50. Scheper GC, van der Knaap MS, Proud CG. Translation matters: protein synthesis defects in inherited disease. Nat Rev Genet 2007; 8:711-723.
51. Barbosa C, Peixeiro I, Romao L. Gene expression regulation by upstream open reading frames and human disease. PLoS Genet 2013; 9:e1003529.
52. Katoh M, Igarashi M, Fukuda H, Nakagama H, Katoh M. Cancer genetics and genomics of human FOX family genes. Cancer Lett 2013; 328: 198-206.
53. Thackray VG. Fox tales: regulation of gonadotropin gene expression by forkhead transcription factors. Mol Cell Endocrinol 2014; 385:62-70.
54. Catena R, Escoffier E, Caron C, Khochbin S, Martianov I, Davidson I. HMGB4, a novel member of the HMGB family, is preferentially expressed in the mouse testis and localizes to the basal pole of elongating spermatids. Biol Reprod 2009; 80:358-366.
55. Osaki E, Nishina Y, Inazawa J, Copeland NG, Gilbert DJ, Jenkins NA, Ohsugi M, Tezuka T, Yoshida M, Semba K. Identification of a novel Sryrelated gene and its germ cell-specific expression. Nucleic Acids Res 1999; 27:2503-2510.
56. Lane L, Argoud-Puy G, Britan A, Cusin I, Duek PD, Evalet O, Gateau A, Gaudet P, Gleizes A, Masselot A, Zwahlen C, Bairoch A. neXtProt: a knowledge platform for human proteins. Nucleic Acids Res 2012; 40: D76-D83.
57. Blake JA, Bult CJ, Eppig JT, Kadin JA, Richardson JE, Mouse Genome Database Group. The Mouse Genome Database: integration of and access to knowledge about the laboratory mouse. Nucleic Acids Res 2014; 42: D810-D817.
58. Bohgaki T, Bohgaki M, Cardoso R, Panier S, Zeegers D, Li L, Stewart GS, Sanchez O, Hande MP, Durocher D, Hakem A, Hakem R. Genomic instability, defective spermatogenesis, immunodeficiency, and cancer in a mouse model of the RIDDLE syndrome. PLoS Genet 2011; 7:e1001381.
59. Joyce EF, Tanneti SN, McKim KS. Drosophila hold'em is required for a subset of meiotic crossovers and interacts with the DNA repair endonuclease complex subunits MEI-9 and ERCC1. Genetics 2009; 181:335-340.
60. Souquet B, Abby E, Herve R, Finsterbusch F, Tourpin S, Le Bouffant R, Duquenne C, Messiaen S, Martini E, Bernardino-Sgherri J, Toth A, Habert R, et al. MEIOB targets single-strand DNA and is necessary for meiotic recombination. PLoS Genet 2013; 9:e1003784.
61. Zhang T, Murphy MW, Gearhart MD, Bardwell VJ, Zarkower D. The mammalian Doublesex homolog DMRT6 coordinates the transition between mitotic and meiotic developmental programs during spermatogenesis. Development 2014; 141:3662-3671.
62. Matzuk MM, Lamb DJ. The biology of infertility: research advances and clinical challenges. Nat Med 2008; 14:1197-1213.
63. Bao J, Yuan S, Maestas A, Bhetwal BP, Schuster A, Yan W. Stk31 is dispensable for embryonic development and spermatogenesis in mice. Mol Reprod Dev 2013; 80:786.
64. Zhou J, Leu NA, Eckardt S, McLaughlin KJ, Wang PJ. STK31/TDRD8, a germ cell-specific factor, is dispensable for reproduction in mice. PLoS ONE 2014; 9:e89471.
65. Hsu PD, Lander ES, Zhang F. Development and applications of CRISPRCas9 for genome engineering. Cell 2014; 157:1262-1278.
66. Kim H, Kim JS. A guide to genome engineering with programmable nucleases. Nat Rev Genet 2014; 15:321-334.
67. van Koningsbruggen S, Straasheijm KR, Sterrenburg E, de Graaf N, Dauwerse HG, Frants RR, van der Maarel SM. FRG1P-mediated aggregation of proteins involved in pre-mRNA processing. Chromosoma 2007; 116:53-64.
68. Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, Gil L, Giron CG, et al. Ensembl 2014. Nucleic Acids Res 2014; 42:D749-D755.
69. Schafer M, Nayernia K, Engel W, Schafer U. Translational control in spermatogenesis. Dev Biol 1995; 172:344-352.
70. Pickering BM, Willis AE. The implications of structured 5' untranslated regions on translation and disease. Semin Cell Dev Biol 2005; 16:39-47.
71. Lalmansingh AS, Karmakar S, Jin Y, Nagaich AK. Multiple modes of chromatin remodeling by Forkhead box proteins. Biochim Biophys Acta 2012; 1819:707-715.
72. Goertz MJ, Wu Z, Gallardo TD, Hamra FK, Castrillon DH. Foxo1 is required in mouse spermatogonial stem cells for their maintenance and the initiation of spermatogenesis. J Clin Invest 2011; 121:3456-3466.
73. Schmidt D, Ovitt CE, Anlag K, Fehsenfeld S, Gredsted L, Treier AC, Treier M. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 2004; 131:933-942.
74. Uhlenhaut NH, Treier M. Forkhead transcription factors in ovarian function. Reproduction 2011; 142:489-495.
75. Herrada G, Wolgemuth DJ. The mouse transcription factor Stat4 is expressed in haploid male germ cells and is present in the perinuclear theca of spermatozoa. J Cell Sci 1997; 110(Pt 14):1543-1553.
76. Wang G, Guo Y, Zhou T, Shi X, Yu J, Yang Y, Wu Y, Wang J, Liu M, Chen X, Tu W, Zeng Y, et al. In-depth proteomic analysis of the human sperm reveals complex protein compositions. J Proteomics 2013; 79: 114-122.
77. Amaral A, Castillo J, Ramalho-Santos J, Oliva R. The combined human sperm proteome: cellular pathways and implications for basic and clinical science. Hum Reprod Update 2014; 20:40-62.
78. Stros M. HMGB proteins: interactions with DNA and chromatin. Biochim Biophys Acta 2010; 1799:101-113.
79. Malarkey CS, Churchill ME. The high mobility group box: the ultimate utility player of a cell. Trends Biochem Sci 2012; 37:553-562.
80. Park S, Lippard SJ. Binding interaction of HMGB4 with cisplatinmodified DNA. Biochemistry 2012; 51:6728-6737.
81. Han F, Dong Y, Liu W, Ma X, Shi R, Chen H, Cui Z, Ao L, Zhang H, Cao J, Liu J. Epigenetic regulation of Sox30 is associated with testis development in mice. PLoS ONE 2014; 9:e97203.
82. Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B, Reyftmann L, Dechaud H, De Vos J, Hamamah S. The human cumulus-oocyte complex gene-expression profile. Hum Reprod 2006; 21: 1705-1719.
83. Kocabas AM, Crosby J, Ross PJ, Otu HH, Beyhan Z, Can H, Tam WL, Rosa GJ, Halgren RG, Lim B, Fernandez E, Cibelli JB. The transcriptome of human oocytes. Proc Natl Acad Sci U S A 2006; 103:14027-14032.
84. Cressman VL, Backlund DC, Avrutskaya AV, Leadon SA, Godfrey V, Koller BH. Growth retardation, DNA repair defects, and lack of spermatogenesis in BRCA1-deficient mice. Mol Cell Biol 1999; 19: 7061-7075.
85. Schwab KR, Smith GD, Dressler GR. Arrested spermatogenesis and evidence for DNA damage in PTIP mutant testes. Dev Biol 2013; 373: 64-71.
86. Loveland KL, Bakker M, Meehan T, Christy E, von Schonfeldt V, Drummond A, de Kretser D. Expression of Bambi is widespread in juvenile and adult rat tissues and is regulated in male germ cells. Endocrinology 2003; 144:4180-4186.
87. De Martino SP, Errington F, Ashworth A, Jowett T, Austin CA. sox30: a novel zebrafish sox gene expressed in a restricted manner at the midbrainhindbrain boundary during neurogenesis. Dev Genes Evol 1999; 209: 357-362.
88. Lioubinski O, Muller M, Wegner M, Sander M. Expression of Sox transcription factors in the developing mouse pancreas. Dev Dyn 2003; 227:402-408.
89. Han F, Liu W, Jiang X, Shi X, Yin L, Ao L, Cui Z, Li Y, Huang C, Cao J, Liu J. SOX30, a novel epigenetic silenced tumor suppressor, promotes tumor cell apoptosis by transcriptional activating p53 in lung cancer. Oncogene (in press). Published online ahead of print 1 December 2014; DOI: 10.1038/onc.2014.370.
90. Hu W, Zheng T, Wang J. Regulation of fertility by the p53 family members. Genes Cancer 2011; 2:420-430.
91. Feng Z, Zhang C, Kang HJ, Sun Y, Wang H, Naqvi A, Frank AK, Rosenwaks Z, Murphy ME, Levine AJ, Hu W. Regulation of female reproduction by p53 and its family members. FASEB J 2011; 25: 2245-2255.
92. Liu J, Zhang C, Hu W, Feng Z. Tumor suppressor p53 and its mutants in cancer metabolism. Cancer Lett 2015; 356:197-203.
93. Djureinovic D, Fagerberg L, Hallstrom B, Danielsson A, Lindskog C, Uhlen M, Ponten F. The human testis-specific proteome defined by transcriptomics and antibody-based profiling. Mol Hum Reprod 2014; 20: 476-488.