Genetic control of spermiogenesis: Insights from the CREM gene and implications for human infertility

Reproductive BioMedicine Online

Volumn 10, Issue 1, 2005, Pages 64-71

  Krausz, Csilla ^a   Sassone Corsi, Paolo ^b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

ACT; CREM; Genetics; Infertility; Kinesin; Spermiogenesis

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ISOPROTEIN; KINESIN;

ARTICLE; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETIC REGULATION; GERM CELL; HUMAN; MALE; MALE INFERTILITY; MEIOSIS; MOLECULAR DYNAMICS; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REPRODUCTION; SIGNAL TRANSDUCTION; SPERMATOGENESIS;

EID: 11944258354     PISSN: 14726483     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1472-6483(10)60805-X     Document Type: Article

References (83)

1. Barak Y, Kogosowski A, Goldman S et al. 1998 Pregnancy and birth after transfer of embryos that developed from single-nucleated zygotes obtained by injection of round spermatids into oocytes. Fertility and Sterility 70, 67-70.
2. Behr R, Weinbauer GF 2000 CREM activator and repressor isoforms in human testis: sequence variations and inaccurate splicing during impaired spermatogenesis. Molecular Human Reproduction 6, 967-972.
3. Behr R, Weinbauer GF 2001 cAMP response element modulator (CREM): an essential factor for spermatogenesis in primates? International Journal of Andrology 24, 126-135.
4. Beissbarth T, Borisevich I, Horlein A et al. 2003 Analysis of CREM-dependent gene expression during mouse spermatogenesis. Molecular Cellular Endocrinology 212, 29-39.
5. Blendy JA, Kaestner KH, Weinbauer GF et al. 1996 Severe impairment of spermatogenesis in mice lacking the CREM gene. Nature 380, 162-165.
6. Carpenter AT 1987 Gene conversion, recombination nodules, and the initiation of meiotic synapsis. Bioessays 6, 232-236.
7. Cheung P, Allis CD, Sassone-Corsi P 2000 Signaling to chromatin through histone modifications. Cell 103, 263-271.
8. Clouthier DE, Avarbock MR, Maika SD et al. 1996 Rat spermatogenesis in mouse testis. Nature 381, 418-421.
9. De Cesare D, Sassone-Corsi P 2000 Transcriptional regulation by cyclic AMP-responsive factors. Progress in Nucleic Acid Research and Molecular Biology 64, 343-369.
10. De Cesare D, Fimia GM, Sassone-Corsi P 1999 Signaling routes to CREM and CREB: plasticity in transcriptional activation. Trends in Biochemical Sciences 24, 281-285.
11. De Cesare D, Fimia GM, Brancorsini S et al. 2003 Transcriptional control in male germ cells: general factor TFIIA participates in CREM-dependent gene activation. Molecular Endocrinology 17, 2554-2565.
12. Delmas V, van der Hoorn F, Mellstrom B et al. 1993 Induction of CREM activator proteins in spermatids: down-stream targets and implications for haploid germ cell differentiation. Molecular Endocrinology 7, 1502-1514.
13. de Rooij DG 2001 Proliferation and differentiation of spermatogonial stem cells. Reproduction 121, 347-354.
14. Desdouets C, Matesic G, Molina CA et al. 1995 Cell cycle regulation of cyclin A gene expression by the cyclic AMP-responsive transcription factors CREB and CREM. Molecular Cellular Biology 15, 3301-3309.
15. Dierich A, Sairam MR, Monaco L et al. 1998 Impairing follicle-stimulating hormone signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proceedings of the National Academy of Sciences of the USA 95, 13612-13617.
16. Eddy EM 1998 Regulation of gene expression during spermatogenesis. Seminars in Cell Developmental Biology 9, 451-457.
17. Eddy EM, O'Brien DA 1998 Gene expression during mammalian meiosis. Current Topics in Developmental Biology 37, 141-200.
18. Fimia GM, De Cesare D, Sassone-Corsi P 1998 Mechanisms of activation by CREB and CREM: phosphorylation, CBP, and a novel coactivator, ACT. Cold Spring Harbor Symposia Quantitative Biology 63, 631-642.
19. Fimia GM, De Cesare D, Sassone-Corsi P 1999 CBP-independent activation of CREM and CREB by the LIM-only protein ACT. Nature 398, 165-169.
20. Forti G, Krausz C 1998 Clinical review 100: evaluation and treatment of the infertile couple. Journal of Clinical Endocrinology and Metabolism 83, 4177-4188.
21. Foulkes NS, Borrelli E, Sassone-Corsi P 1991 CREM gene: use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription. Cell 64, 739-749.
22. Foulkes NS, Mellstrom B, Benusiglio E, Sassone-Corsi P 1992 Developmental switch of CREM function during spermatogenesis: from antagonist to activator. Nature 355, 80-84.
23. Foulkes NS, Schlotter F, Pevet P, Sassone-Corsi P 1993 Pituitary hormone FSH directs the CREM functional switch during spermatogenesis. Nature 362, 264-267.
24. Gellersen B, Kempf R, Telgmann R et al. 1997 Human endometrial stromal cells express novel isoforms of the transcriptional modulator CREM and up-regulate ICER in the course of decidualization. Molecular Endocrinology 11, 97-113.
25. Griswold MD 1998 The central role of Sertoli cells in spermatogenesis. Seminars in Cell and Developmental Biology 9, 411-416.
26. Ha H, van Wijnen AJ, Hecht NB 1997 Tissue-specific protein-DNA interactions of the mouse protamine 2 gene promoter. Journal of Cellular Biochemistry 64, 94-105.
27. Hecht NB 1998 Molecular mechanisms of male germ cell differentiation. Bioessays 20, 555-561.
28. Heidaran MA, Kistler WS 1987 Transcriptional and translational control of the message for transition protein 1, a major chromosomal protein of mammalian spermatids. Journal of Biological Chemistry 262, 13309-13315.
29. Hiller MA, Lin TY, Wood C, Fuller MT 2001 Developmental regulation of transcription by a tissue-specific TAF homolog. Genes and Development 15, 1021-1030.
30. Hurst S, Howes EA, Coadwell J, Jones R 1998 Expression of a testis-specific putative actin-capping protein associated with the developing acrosome during rat spermiogenesis. Molecular Reproduction and Development 49, 81-91.
31. Jurisicova A, Lopes S, Meriano J et al. 1999 DNA damage in round spermatids of mice with a targeted disruption of the Pp1cgamma gene and in testicular biopsies of patients with non-obstructive azoospermia. Molecular Human Reproduction 5, 323-330.
32. Kierszenbaum AL, Tres LL 1975 Structural and transcriptional features of the mouse spermatid genome. Journal of Cell Biology 65, 258-270.
33. Kimmins S, Kotaja N, Davidson I, Sassone-Corsi P 2004a Testis-specific transcription mechanisms promoting male germ-cell differentiation. Reproduction 128, 5-12.
34. Kimmins S, Kotaja N, Fienga G et al. 2004b A specific programme of gene transcription in male germ cells. Reproductive BioMedicine Online 8, 496-500.
35. Kistler MK, Sassone-Corsi P, Kistler WS 1994 Identification of a functional cyclic adenosine 3′,5′-monophosphate response element in the 5′-flanking region of the gene for transition protein 1 (TP1), a basic chromosomal protein of mammalian spermatids. Biology of Reproduction 51, 1322-1329.
36. Kleene KC 2001 A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mechanisms of Development 106, 3-23.
37. Kotaja N, De Cesare D, Macho B et al. 2004a Abnormal sperm in mice with targeted deletion of the act (activator of cAMP-responsive element modulator in testis) gene. Proceedings of the National Academy of Sciences of the USA 101, 10620-10625
38. Kotaja N, Kimmins, S, Brancorsini S et al. 2004b Preparation, isolation and characterization of stage-specific spermatogenic cells for cellular and molecular analysis. Nature Methods 1, 249-254.
39. Krausz C, Ford G, McElreavey K 2003 The Y chromosome and male fertility and infertility. International Journal of Andrology 26, 70-75.
40. Lin WW, Lamb DJ, Lipshultz LI, Kim ED 1998 Absence of cyclic adenosine 3′:5′ monophosphate responsive element modulator expression at the spermatocyte arrest stage. Fertility and Sterility 69, 533.
41. Macho B, Brancorsini S, Fimia GM et al. 2002 CREM-dependent transcription in male germ cells controlled by a kinesin. Science 298, 2388-2390.
42. Martianov I, Fimia GM, Dierich A et al. 2001 Late arrest of spermiogenesis and germ cell apoptosis in mice lacking the TBP-like TLF/TRF2 gene. Molecular Cell 7, 509-515
43. Martianov I, Brancorsini S, Gansmuller A et al. 2002 Distinct functions of TBP and TLF/TRF2 during spermatogenesis: requirement of TLF for heterochromatic chromocenter formation in haploid round spermatids. Development 129, 945-955.
44. Masquilier D, Foulkes NS, Mattei MG, Sassone-Corsi P 1993 Human CREM gene: evolutionary conservation, chromosomal localization, and inducibility of the transcript. Cell Growth and Differentiation 4, 931-937
45. Monesi V 1964 Ribonucleic acid synthesis during mitosis and meiosis in the mouse testis. Journal of Cell Biology 22, 521-532.
46. Montminy M 1997 Transcriptional regulation by cyclic AMP. Annual Review of Biochemistry 66, 807-822.
47. Nantel F, Monaco L, Foulkes NS et al. 1996 Spermiogenesis deficiency and germ-cell apoptosis in CREM-mutant mice. Nature 380, 159-162.
48. Ohbayashi T, Shimada M, Nakadai T et al. 2003 Vertebrate TBP-like protein (TLP/TRF2/,TLF) stimulates TATA-less terminal deoxynucleotidyl transferase promoters in a transient reporter assay, and TFIIA-binding capacity of TLP is required for this function. Nucleic Acids Research 31, 2127-2133.
49. Oppedisano L, Haines G, Hrabchak C et al. 2002 The rate of aneuploidy is altered in spermatids from infertile mice. Human Reproduction 17, 710-717.
50. Ortega S, Prieto I, Odajima J et al. 2003 Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nature Genetics 35, 25-31.
51. Palermo I, Litrico L, Emmanuele G et al. 2001 Cloning and expression of activator of CREM in testis in human testicular tissue. Biochemical and Biophysical Research Communications 283, 406-411.
52. Parra MT, Viera A, Gomez R et al. 2003 Dynamic relocalization of the chromosomal passenger complex proteins inner centromere protein (INCENP) and aurora-B kinase during male mouse meiosis Journal of Cell Science 116, 961-974
53. Peri A, Krausz C, Cioppi F et al. 1998 Cyclic adenosine 3′,5′-monophosphate-responsive element modulator gene expression in germ cells of normo- and oligoazoospermic men. Journal of Clinical Endocrinology and Metabolism 83, 3722-3726.
54. Pointud JC, Mengus G, Brancorsini S et al. 2003 The intracellular localisation of TAF7L, a paralogue of transcription factor TFIID subunit TAF7, is developmentally regulated during male germ-cell differentiation. Journal of Cell Science 116, 1847-1858.
55. Prieto P, Shaw P, Moore G 2004 Homologue recognition during meiosis is associated with change in chromatin conformation. Nature Cell Biology 6, 906-908.
56. Rosenberg MP, Aversa CR, Wallace R, Propst F 1995 Expression of the v-Mos oncogene in male meiotic germ cells of transgenic mice results in metaphase arrest. Cell Growth and Differentiation 6, 325-336
57. Rozman D, Fink M, Firma GM et al. 1999 Cyclic adenosine 3′,5′-monophosphate (cAMP)/cAMP-responsive element modulator (CREM)-dependent regulation of cholesterogenic lanosterol l4alpha-demethylase (CYP51) in spermatids. Molecular Endocrinology 13, 1951-1962.
58. Sassone-Corsi P 1995 Transcription factors responsive to cAMP. Annual Review of Cell and Developmental Biology 11, 355-377.
59. Sassone-Corsi P 1997 Transcriptional checkpoints determining the fate of male germ cells. Cell 88, 163-166.
60. Sassone-Corsi P 1998 CREM: a master-switch governing male germ cells differentiation and apoptosis Seminars in Developmental Biology 9, 475-482.
61. Sassone-Corsi P 2002 Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296, 2176-2178.
62. Schmidt EE, Schibler U 1995 High accumulation of components of the RNA polymerase II transcription machinery in rodent spermatids. Development 121, 2373-2383.
63. Sluka P, O'Donnell L, Stanton PG 2002 Stage-specific expression of genes associated with rat spermatogenesis: characterization by laser-capture microdissection and real-time polymerase chain reaction. Biology of Reproduction 67, 820-828.
64. Sousa M, Barros A, Takahashi K et al. 1999 Clinical efficacy of spermatid conception: analysis using a new spermatid classification scheme. Human Reproduction 14, 1279-1286.
65. Steger K, Klonisch T, Gavenis K et al. 1999 Round spermatids show normal testis-specific H1t but reduced cAMP-responsive element modulator and transition protein 1 expression in men with round-spermatid maturation arrest. Journal of Andrology 20, 747-754.
66. Steger K, Behr R, Kleiner I et al. 2004 Expression of activator of CREM in the testis (ACT) during normal and impaired spermatogenesis: correlation with CREM expression. Molecular Human Reproduction 10, 129-135.
67. Sun Z, Means RL, LeMagueresse B, Means AR 1995a Organization and analysis of the complete rat calmodulin-dependent protein kinase IV gene. Journal of Biological Chemistry 270, 29507-29514.
68. Sun Z, Sassone-Corsi P, Means AR 1995b Calspermin gene transcription is regulated by two cyclic-AMP response elements contained in an alternative promoter in the calmodulin kinase IV gene. Molecular Cell Biology 15, 561-571.
69. Tesarik J, Mendoza C, Testart J 1995 Viable embryos from injection of round spermatids into oocytes. New England Journal of Medicine 333, 525.
70. Toshima J, Nakagawara K, Mori M et al. 1998 Structural organization and chromosomal localization of the mouse tesk1 (testis-specific protein kinase 1) gene. Gene 206, 237-245.
71. Vanderzwalmen P, Zech H, Birkenfeld A et al. 1997 Intracytoplasmic injection of spermatids retrieved from testicular tissue: influence of testicular pathology, type of selected spermatids and oocyte activation. Human Reproduction 12, 1203-1213.
72. Wang PJ, McCarrey JR, Yang F, Page DC 2001 An abundance of X-linked genes expressed in spermatogonia. Nature Genetics 27, 422-426.
73. Weinbauer GF, Behr R, Bergmann M, Nieschlag E 1998 Testicular cAMP responsive element modulator (CREM) protein is expressed in round spermatids but is absent or reduced in men with round spermatid maturation arrest. Molecular Human Reproduction 4, 9-15.
74. Weitzel JM, Shiryaeva NB, Middendorff R et al. 2003 Testis-specific expression of rat mitochondrial glycerol-3-phosphate dehydrogenase in haploid male germ cells. Biology of Reproduction 68, 699-707.
75. West AP, Sharpe RM, Saunders PT 1994 Differential regulation of cyclic adenosine 3′,5′-monophosphate (cAMP) response element-binding protein and cAMP response element modulator messenger ribonucleic acid transcripts by follicle-stimulating hormone and androgen in the adult rat testis. Biology of Reproduction 50, 869-881.
76. Winer MA, Wolgemuth DJ 1993 The segment-specific pattern of A-raf expression in the mouse epididymis is regulated by testicular factors. Endocrinology 136, 2561-2572.
77. Yamanaka K, Sofikitis NV, Miyagawa I et al. 1997 Ooplasmic round spermatid nuclear injection procedures as an experimental treatment for nonobstructive azoospermia. Journal of Assisted Reproduction and Genetics 1, 55-62.
78. Yanagimachi R, Wakayama T, Kishikawa H et al. 2004 Production of fertile offspring from genetically infertile male mice. Proceedings of the National Academy of Sciences of the USA 101, 1691-1695.
79. 2+ oscillation-inducing abilities of round/elongated spermatids of mouse, hamster, rat, rabbit and human assessed by mouse oocyte activation assay. Human Reproduction 15, 2582-2590.
80. Yuan L, Liu JG, Zhao J et al. 2000 The marine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Molecular Cell 5, 73-83.
81. Zech H, Vanderzwalmen P, Prapas Y et al. 2000 Congenital malformations after intracytoplasmic injection of spermatids. Human Reproduction 15, 969-971.
82. Zheng Y, Martin-Deleon PA 1999 Characterization of the genomic structure of the murine Spam1 gene and its promoter: evidence for transcriptional regulation by a cAMP-responsive element. Molecular Reproduction and Development 54, 8-16.
83. Zhou Y, Sun Z, Means AR et al. 1996 cAMP-response element modulator tau is a positive regulator of testis angiotensin converting enzyme transcription. Proceedings of the National Academy of Sciences of the USA 93, 12262-12266.