Expression patterns of SP1 and sp3 during mouse spermatogenesis: SP1 down-regulation correlates with two successive promoter changes and translationally compromised transcripts

Biology of Reproduction

Volumn 79, Issue 2, 2008, Pages 289-300

  Ma, Wenli ^a   Horvath, Gary C ^a   Kistler, Malathi K ^a   Kistler, W Stephen ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Alternate promoter; Alternative splicing; Meiosis; Mouse; SP1; SP3; Spermatogenesis; Testis; Transcription factor

Indexed keywords

TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3;

ANIMAL TISSUE; ARTICLE; DOWN REGULATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; INTRON; MALE; MEIOSIS; MOUSE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PACHYTENE; PRIORITY JOURNAL; PROMOTER REGION; RNA TRANSLATION; SEQUENCE ANALYSIS; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPLICEOSOME;

ALTERNATIVE SPLICING; ANIMALS; ANIMALS, OUTBRED STRAINS; DOWN-REGULATION; GENE EXPRESSION PROFILING; MALE; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; PACHYTENE STAGE; PROMOTER REGIONS (GENETICS); PROTEIN BIOSYNTHESIS; RNA, MESSENGER; SP1 TRANSCRIPTION FACTOR; SP3 TRANSCRIPTION FACTOR; SPERMATOGENESIS;

EID: 48749097600     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.107.067082     Document Type: Article

References (72)

1. Dynan WS, Tjian R. The promoter-specific transcription factor Sp1 binds to upstream sequences in the SV40 early promoter. Cell 1983; 35:79-87.
2. Suske G, Bruford E, Philipsen S. Mammalian SP/KLF transcription factors: bring in the family. Genomics 2005; 85:551-556.
3. Suske G. The Sp-family of transcription factors. Gene 1999; 238:291-300.
4. Lomberk G, Urrutia R. The family feud: turning off Sp1 by Sp1-like KLF proteins. Biochem J 2005; 392:1-11.
5. Zhao C, Meng A. Sp1-like transcription factors are regulators of embryonic development in vertebrates. Dev Growth Differ 2005; 47:201-211.
6. Li L, He S, Sun JM, Davie JR. Gene regulation by Sp1 and Sp3. Biochem Cell Biol 2004; 82:460-471.
7. Kaczynski J, Cook T, Urrutia R. Sp1- and Kruppel-like transcription factors. Genome Biol 2003; 4:206.
8. Bouwman P, Philipsen S. Regulation of the activity of Sp1-related transcription factors. Mol Cell Endocrinol 2002; 195:27-38.
9. Kamemura K, Hart GW. Dynamic interplay between O-glycosylation and O-phosphorylation of nucleocytoplasmic proteins: a new paradigm for metabolic control of signal transduction and transcription. Prog Nucleic Acid Res Mol Biol 2003; 73:107-136.
10. Chu S, Ferro TJ. Sp1: regulation of gene expression by phosphorylation. Gene 2005; 348:1-11.
11. Clermont Y, Oko R, Hermo L. Cell biology of mammalian spermatogenesis. In: Desjardins C, Ewing LL (eds.), Cell and Molecular Biology of the Testis. New York: Oxford University Press; 1993:332-376.
12. Saffer JD, Jackson SP, Annarella MB. Developmental expression of Sp1 in the mouse. Mol Cell Biol 1991; 11:2189-2199.
13. Persengiev SP, Raval PJ, Rabinovitch S, Millette CF, Kilpatrick DL. Transcription factor Sp1 is expressed by three different developmentally regulated messenger ribonucleic acids in mouse spermatogenic cells. Endocrinology 1996; 137:638-646.
14. Thomas K, Sung DY, Yang J, Johnson K, Thompson W, Millette C, McCarrey J, Breitberg A, Gibbs R, Walker W. Identification, characterization, and functional analysis of Sp1 transcript variants expressed in germ cells during mouse spermatogenesis. Biol Reprod 2005; 72:898-907.
15. Persengiev SP, Saffer JD, Kilpatrick DL. An alternatively spliced form of the transcription factor Sp1 containing only a single glutamine-rich transactivation domain. Proc Natl Acad Sci U S A 1995; 92:9107-9111.
16. Doenecke D, Albig W, Bouterfa H, Drabent B. Organization and expression of H1 histone and H1 replacement histone genes. J Cell Biochem 1994; 54:423-431.
17. Wang ZF, Sirotkin AM, Buchold GM, Skoultchi AI, Marzluff WF. The mouse histone H1 genes: gene organization and differential regulation. J Mol Biol 1997; 271:124-138.
18. Clare SE, Fantz DA, Kistler WS, Kistler MK. The testis-specific histone H1t gene is strongly repressed by a G/C-rich region just downstream of the TATA Box. J Biol Chem 1997; 272:33028-33036.
19. Meergans T, Albig W, Doenecke D. Conserved sequence elements in human main type-H1 histone gene promoters: their role in H1 gene expression. Eur J Biochem 1998; 256:436-446.
20. Grimes SR, Wilkerson DC, Noss KR, Wolfe SA. Transcriptional control of the testis-specific histone H1t gene. Gene 2003; 304:13-21.
21. Horvath GC, Kistler WS, Kistler MK. RFX2 is a potential transcriptional regulatory factor for histone H1t and other genes expressed during the meiotic phase of spermatogenesis. Biol Reprod 2004; 71:1551-1559.
22. Heyting C, Dietrich AJ. Meiotic chromosome preparation and protein labeling. Methods Cell Biol 1991; 35:177-202.
23. Meistrich ML, Trostle PK, Frapart M, Erickson RP. Biosynthesis and localization of lactate dehydrogenase X in pachytene spermatocytes and spermatids of mouse testes. Dev Biol 1977; 60:428-441.
24. Bartell JG, Davis T, Kremer EJ, Dewey MJ, Kistler WS. Expression of the rat testis-specific histone H1t gene in transgenic mice. One kilobase of 5′-flanking sequence mediates correct expression of a lacZ fusion gene. J Biol Chem 1996; 271:4046-4054.
25. Rosen S, Skaletsky HJ. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds.), Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, NJ: Humana Press; 2000:365-386.
26. Bustin SA, Benes V, Nolan T, Pfaffl MW. Quantitative real-time RT-PCR - a perspective. J Mol Endocrinol 2005; 34:597-601.
27. Horvath GC, Clare SE, Kistler MK, Kistler WS. Characterization of the H1t promoter: role of conserved histone 1 AC and TG elements and dominance of the cap-proximal silencer. Biol Reprod 2001; 65:1074-1081.
28. Oakberg EF. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 1956; 99:507-516.
29. Russsell LD, Ettlin RA, Hikim APS, Clegg ED. Histological and Histopathological Evaluation of the Testis. Clearwater, FL: Cache River Press; 1990.
30. Cheng H, Leblond CP. Origin, differentiation, and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian Theory of the origin of the four epithelial cell types. Am J Anat 1974; 141:537-561.
31. Bellve AR, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM, Dym M. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J Cell Biol 1977; 74:68-85.
32. McCarrey JB. Development of the germ cell. In: Desjardins C, Ewing LL (eds.), Cell and Molecular Biology of the Testis. New York: Oxford University Press; 1993:58-89.
33. Waters SH, Distel RJ, Hecht NB. Mouse testes contain two size classes of actin mRNA that are differentially expressed during spermatogenesis. Mol Cell Biol 1985; 5:1649-1654.
34. Raverot G, Weiss J, Park SY, Hurley L, Jameson JL. Sox3 expression in undifferentiated spermatogonia is required for the progression of spermatogenesis. Dev Biol 2005; 283:215-225.
35. Kremer EJ, Kistler WS. Localization of mRNA for testis-specific histone H1t by in situ hybridization. Exp Cell Res 1991; 197:330-332.
36. Drabent B, Bode C, Bramlage B, Doenecke D. Expression of the mouse testicular histone gene H1t during spermatogenesis. Histochem Cell Biol 1996; 106:247-251.
37. Heidaran MA, Showman RM, Kistler WS. A cytochemical study of the transcriptional and translational regulation of nuclear transition protein 1 (TP1), a major chromosomal protein of mammalian spermatids. J Cell Biol 1988; 106:1427-1433.
38. 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.
39. Shima JE, McLean DJ, McCarrey JR, Griswold MD. The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis. Biol Reprod 2004; 71:319-330.
40. Chalmel F, Rollan AD, Niederhaurser-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.
41. Sapetschnig A, Koch F, Rischitor G, Mennenga T, Suske G. Complexity of translationally controlled transcription factor Sp3 isoform expression. J Biol Chem 2004; 279:42095-42105.
42. Kozak M. A short leader sequence impairs the fidelity of initiation by eukaryotic ribosomes. Gene Expr 1991; 1:111-115.
43. Horiuchi T, Aigaki T. Alternative trans-splicing: a novel mode of pre-mRNA processing. Biol Cell 2006; 98:135-140.
44. Kozak M. Pushing the limits of the scanning mechanism for initiation of translation. Gene 2002; 299:1-34.
45. Kleene KC. Patterns, mechanisms, and functions of translation regulation in mammalian spermatogenic cells. Cytogenet Genome Res 2003; 103:217-224.
46. Iguchi N, Tobias JW, Hecht NB. Expression profiling reveals meiotic male germ cell mRNAs that are translationally up- and down-regulated. Proc Natl Acad Sci U S A. 2006; 103:7712-7717.
47. Eddy EM, O'Brien DA. Gene expression during mammalian meiosis. Curr Top Dev Biol 1998; 37:141-200.
48. Clare SE, Hatfield WR, Fantz DA, Kistler WS, Kistler MK. Characterization of the promoter region of the rat testis-specific histone H1t gene. Biol Reprod 1997; 56:73-82.
49. Wilkerson DC, Wolfe SA, Grimes SR. H1t/GC-box and H1t/TE1 element are essential for promoter activity of the testis-specific histone H1t gene. Biol Reprod 2002; 67:1157-1164.
50. Zakeri ZF, Wolgemuth DJ, Hunt CR. Identification and sequence analysis of a new member of the mouse HSP70 gene family and characterization of its unique cellular and developmental pattern of expression in the male germ line. Mol Cell Biol 1988; 8:2925-2932.
51. Gebara MM, McCarrey JR. Protein-DNA interactions associated with the onset of testis-specific expression of the mammalian Pgk-2 gene. Mol Cell Biol 1992; 12:1422-1431.
52. Iannello RC, Kola I, Dahl HH. Temporal and tissue-specific interactions involving novel transcription factors and the proximal promoter of the mouse Pdha-2 gene. J Biol Chem 1993; 268:22581-22590.
53. Bonny C, Cooker LA, Goldberg E. Deoxyribonucleic acid-protein interactions and expression of the human testis-specific lactate dehydrogenase promoter: transcription factor Sp1 plays a major role. Biol Reprod 1998; 58:754-759.
54. Kim M, Li D, Yunxia C, Mueller K, Chears WS, DeJong J. Regulatory factor interactions and somatic silencing of the germ cell-specific ALF gene. J Biol Chem 2006; 281:34288-34298.
55. Thomas K, del Mazo J, Eversole P, Bellve A, Hiraoka Y, Li SSL, Simon M. Developmental regulation of expression of the lactate dehydrogenase (LDH) multigene family during mouse spermatogenesis. Development 1990; 109:483-493.
56. Rosario MO, Perkins SL, O'Brien DA, Allen RL, Eddy EM. Identification of the gene for the developmentally expressed 70 kDa heat-shock protein (P70) of mouse spermatogenic cells. Dev Biol 1992; 150:1-11.
57. Takakubo F, Dahl HH. The expression pattern of the pyruvate dehydrogenase E1 alpha subunit genes during spermatogenesis in adult mouse. Exp Cell Res 1992; 199:39-49.
58. Drabent B, Bode C, Miosge N, Herken R, Doenecke D. Expression of the mouse histone gene H1t begins at premeiotic stages of spermatogenesis. Cell Tissue Res 1998; 291:127-132.
59. Han SY, Zhou L, Upadhvava A, Lee SH, Parker KL, DeJong J. TFIIalpha/beta-like factor is encoded by a germ cell-specific gene whose expression is up-regulated with other general transcription factors during spermatogenesis in the mouse. Biol Reprod 2001; 64:507-517.
60. DeJong J. Basic mechanisms for the control of germ cell gene expression. Gene 2006; 366:39-50.
61. Yoshioka H, Geyer CB, Hornecker JL, Patel KT, McCarrey JR. Analysis in vivo of developmentally and evolutionarily dynamic protein-DNA interactions regulating transcription of the Pgk2 gene during mammalian spermatogenesis. Mol Cell Biol 2007; 27:7871-7885.
62. Tang H, Kung A, Goldberg E. Regulation of murine lactate dehydrogenase C (Ldhc) gene expression. Biol Reprod 2008; 78:455-461.
63. Kleene KC. A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mech Dev 2001; 106:3-23.
64. Mertineit C, Yoder JA, Taketo T, Laird DW, Trasler JM, Bestor TH. Sex-specific exons control DNA methyltransferase in mammalian germ cells. Development 1998; 125:889-897.
65. Shovlin TC, Bourc'his D, La Salle S, O'Doherty A, Trasler JM, Bestor TH, Walsh CP. Sex-specific promoters regulate Dnmt3L expression in mouse germ cells. Hum Reprod 2007; 22:457-467.
66. Gu W, Hecht NR. Translation of a testis-specific Cu/Zn superoxide dismutase (SOD-1) mRNA is regulated by a 65-kilodalton protein which binds to its 5′ untranslated region. Mol Cell Biol 1996; 16:4535-4543.
67. Hake LE, Hecht NB. Utilization of an alternative transcription initiation site of somatic cytochrome c in the mouse produces a testis-specific cytochrome c mRNA. J Biol Chem 1993; 268:4788-4797.
68. Rao SM, Howells RD. cis-Acting elements in the 5′-untranslated region of rat testis proenkephalin mRNA regulate translation of the precursor protein. J Biol Chem 1993; 268:22164-22169.
69. Kim TH, Barrera LO, Zheng M, Qu C, Singer MA, Richmond TA, Wu Y, Green RD, Ren B. A high-resolution map of active promoters in the human genome. Nature 2005; 436:876-880.
70. Nicolas M, Noe V, Ciudad CJ. Transcriptional regulation of the human Sp1 gene promoter by the specificity protein (Sp) family members nuclear factor Y (NF-Y) and E2F. Biochem J 2003; 371:265-275.
71. Kanai M, Wei D, Li Q, Jia Z, Ajani J, Le X, Yao J, Xie K. Loss of Kruppel-like factor 4 expression contributes to Sp1 overexpression and human gastric cancer development and progression. Clin Cancer Res 2006; 12:6395-6402.
72. Behr R, Kaestner KH. Developmental and cell type-specific expression of the zinc finger transcription factor Kruppel-like factor 4 (Klf4) in postnatal mouse testis. Mech Dev 2002; 115:167-169.