RNA processing and the control of spermatogenesis

Frontiers of Hormone Research

Volumn 25, Issue , 1999, Pages 34-58

  Walker, William H ^a   Delfino, Frank J ^a   Habener, Joel F ^b,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; HORMONE; MESSENGER RNA; TRANSCRIPTION FACTOR;

ALTERNATIVE RNA SPLICING; ANIMAL; GENETICS; HUMAN; MALE; METABOLISM; REVIEW; RNA SPLICING; SPERMATOGENESIS;

ALTERNATIVE SPLICING; ANIMALS; HORMONES; HUMANS; MALE; RECEPTORS, CELL SURFACE; RNA SPLICING; RNA, MESSENGER; SPERMATOGENESIS; TRANSCRIPTION FACTORS;

EID: 0033287168     PISSN: 03013073     EISSN: None     Source Type: Book Series    
DOI: 10.1159/000060996     Document Type: Article

References (85)

1. Hecht NB: Gene expression during male germ cell development; in Desjardins C, Ewing LL (eds): Cell and Molecular Biology of the Testis. New York, Oxford University Press, 1993, vol 400-432.
2. Eddy EM, Welch JE, O'Brien DA: Gene expression during spermatogenesis; in de Krester DM (ed): Molecular Biology of the Male Reproductive System. New York, Academic Press, 1993, vol 181-232.
3. Wolgemuth DJ, Watrin F: List of cloned mouse genes with unique expression patterns during spermatogenesis. Genome 1991;1:283-288.
4. Gharib SD,Wierman ME, Shupnik MA, Chin WW: Molecular biology of the pituitary gonadotropins. Endocr Rev 1990;11:177-199.
5. Zhang F-P, Rannikko A, Huhtaniemi L: Isolation and characterization of testis-specific cDNAs for luteinizing hormone b-subunit in the rat. Biochem Biophys Res Commun 1995;210:858-865.
6. Ivell R,Wather N, Morley S: Proopiomelanocortin cDNA sequences from the bovine ovary indicate alternative non-functional transcriptional initiation and a new polymorphism. Nucl Acids Res 1988;16:7747.
7. Jeannotte L, Burbach JPH, Drouin J: Unusual proopiomelanocortin ribonucleic acids in extrapituitary tissues: Intronless transcripts in tests and long poly (A) tails in hypothalamus. Mol Endocrinol 1987;1:749-757.
8. Garrett J, Collard MW, Douglass JO: Translational control of germ cell-expressed mRNA imposed by alternative splicing: Opioid peptide gene expression in rat testis. Mol Cell Biol 1989;9:4381-4389.
9. Kilpatrick DL, Borland K, Jin DF: Differential expression of opioid peptide genes by testicular germ cells and somatic cells. Proc Natl Acad Sci USA 1987;84:5695-5699.
10. Kilpatrick DL, Howells RD, Noe M, Bailey LC, Udenfriend S: Expression of proenkephalin mRNA and its peptide products in mammalian testis and ovary. Proc Natl Acad Sci USA 1985;82:7467-7469.
11. Foo N-C, Funkhouser JM, Carter DA, Murphy D: A testis-specific promoter in the rat vasopressin gene. J Biol Chem 1994;269:659-667.
12. Lefebvre DL, Zingg HH: Novel vasopressin gene-related transcripts in rat testis. Mol Endocrinol 1991;5:645-652.
13. Rawlings SR: PACAP, PACAP receptors, and intracellular signalling. Mol Cell Endocrinol 1994;101:C5-C9.
14. Shioda S, Legradi G, Leung WC, Makajo S, Nakaya K, Arimura A: Localization of pituitary adenylate cyclase-activating polypeptide and its messenger ribonucleic acid in the rat testis by light and electron microscopic immunocyochemistry and in situ hybridization. Endocrinology 1994;135:818-825.
15. Kononen J, Paavola M, Penttila T-L, Parvinen M, Pelto-Huikko M: Stage-specific expression of pituitary adenylate cyclase-activating polypeptide (PACAP) mRNA in the rat seminiferous tubules. Endocrinology 1994;135:2291-2294.
16. Hannibal J, Fahrenkrug J: Expression of pituitary adenylate cyclase activating polypeptide (PACAP) gene by rat spermatogenic cells. Regul Pept 1995;55:111-115.
17. West AP, McKinnell C, Sharpe RM, Saunders PT: Pituitary adenylate cyclase activating polypeptide can regulate testicular germ cell protein synthesis in vitro. J Endocrinol 1995;144:215-223.
18. Hurley JD, Gardiner JV, Jones PM, Bloom SR: Cloning and molecular characterization of complementary deoxyribonucleic acid corresponding to a novel form of pituitary adenylate cyclaseactivating polypeptide messenger ribonucleic acid in the rat testis. Endocrinology 1995;136:550-557.
19. Simoni M, Gromoli J, Niesclag E: The follicle-stimulating hormone receptor: Biochemistry, molecular biology, physiology, and pathophysiology. Endocr Rev 1997;18:739-773.
20. Wienbaur GF, Behre HM, Fingscheidt U, Nieschlag E: Human follicle-stimulating hormone exerts a stimulatory effect on spermatogenesis, testicular size, and serum inhibin levels in the gonadotropinreleasing hormone antagonist-treated nonhuman primate (Macaca fascicularis). Endocrinology 1991;129:1831-1839.
21. Gromoll J, Gadermann T, Nieschlag E: Molecular cloning of a truncated isoform of the human follicle-stimulating hormone receptor. Biochem Biophys Res Commun 1992;188:1077-1083.
22. O'Shaughnessy PJ, Dudley K: Discrete splicing alternatives in mRNA encoding the extracellular domain of the testis FSH receptor in the normal and hypogonadal (hpg) mouse. J Endocrinol 1993;10:363-366.
23. Heckert LL, Griswold MD: Expression of follicle-stimulating hormone receptor mRNA in rat testis and Sertoli cells. Mol Endocrinol 1991;5:670-677.
24. Gromoll J, Dankbar B, Sharma RS, Nieschlag E: Molecular cloning of the testicular follicle stimulating hormone receptor of the non human primate Macaca fascicularis and identification of multiple transcripts in the testis. Biochem Biophys Res Commun 1993;196:1066-1072.
25. Loosfelt H, Misrahi M, Atger M, et al: Cloning and sequencing of porcine LH-hCG receptor cDNA: Variants lacking transmembrane domain. Science 1989;245:525-528.
26. Tsai-Morris CH, Buczko E, Wang W, Dufau ML: Intronic nature of the rat luteinizing hormone receptor gene defines a soluble receptor subspecies with hormone binding activity. J Biol Chem 1990;265:19385-19388.
27. Zhang F-P, Rannikko AS, Manna PR, Fraser HM, Huhtamaniemi IT: Cloning and functional expression of the luteinizing hormone receptor complementary deoxyribonucleic acid from the marmoset monkey testis: Absence of sequences encoding exon 10 in other species. Endocrinology 1997;138:2481-2490.
28. Inagaki N, Yoshida H, Mizuta M, et al: Cloning and functional characterization of a third pituitary adenylate cyclase-activating polypeptide receptor subtype expressed in insulin-secreting cells. Proc Natl Acad Sci USA 1994;91:2679-2683.
29. Krempels K, Usdin TB, Hrta G, Mezey E: PACAP acts through VIP type 2 receptors in the rat testis. Neuropeptides 1995;29:315-320.
30. Heindel JJ, Powell CJ, Paschall CS, Arimura A, Culler MD: A novel hypothalamic peptide, pituitary adenylate cyclase activating peptide, modulates Sertoli cells function in vitro. Biol Reprod 1992;47:800-806.
31. Kangasniemi M, Kaipia A, Toppari J, Mali P, Huhtaniem I, Parvinen M: Cellular regulation of basal and FSH-stimulated cyclic AMP production in irradiated rat testes. Anat Rec 1990;227:32-36.
32. Chatterjee TK, Liu X, Davisson RL, Fisher RA: Genomic organization of the rat pituitary adenylate cyclase-activating polypeptide receptor gene. J Biol Chem 1997;272:12122-12131.
33. Spengler D, Waeber C, Pantaloni C, et al: Differential signal transduction by five splice variants of the PACAP receptor. Nature 1993;365:170-171.
34. Pantaloni C, Brabet P, Bilanges B, et al: Alternative splicing in the N-terminal extracellular domain of the pituitary adenylate cyclase-activating polypeptide (PACAP) receptor modulates receptor selectivity and relative potencies of PACAP-27 and PACAP-38 in phospholipase C activation. J Biol Chem 1996;271:22146-22151.
35. Muramatsu T, Kincaid R: Molecular cloning and chromosomal mapping of the human gene for the testis-specific catalytic subunit of the calmodulin-dependent protein phosphatase (calcineurin A). Biochem Biophys Res Commun 1992;188:265-271.
36. Mbikay M, Raffin-Sanson M, Tadros H, Sirois F, Seidah NG, Chretien M: Structure of the gene for the testis-specific proprotein convertase 4 and of its alternative messenger RNA isoforms. Genomics 1994;20:231-237.
37. Seidah NG, Day R, Hamelin G, Gaspar A, Collard MW, Chretien M: Testicular expression of PC4 in the rat: Molecular diversity of a novel germcell-specific Kex2/Subtilisin-like proprotein convertase. Mol Endocrinol 1992;6:1559-1570.
38. Meijer D, Harmans A, von Lidern M, et al: Molecular characterization of the testis-specific c-abl mRNA in mouse. EMBO J 1987;6:4041-4048.
39. Oppi C, Shore SK, Ruddy EP: Nucleotide sequence of testis-derived c-abl cDNAs: Implications for testis-specific transcription and abl oncogene activation. Proc Natl Acad Sci 1987;84:8200-8204.
40. Zakeri Z, Ponsetto C, Wolgemouth DJ: Translational regulation of the novel haploid-specific transcripts for the c-abl proto-oncogene and a member of the 70 kDa heat-shock protein gene family in the male germ line. Dev Biol 1988;125:417-422.
41. Wang Y, Gologorsky MS, Lin M,Wilcox JN, Marsden PA: A novel, testis-specific mRNA transcript encoding an NH2-terminal truncated nitric-oxide synthase. J Biol Chem 1997;272:11392-11401.
42. Walker WH, Habener JF: Role of transcription factors CREB and CREM in cAMP-regulated transcription during spermatogenesis. Trends Endocrinol Metab 1996;7:133-138.
43. Waeber G, Meyer TE, LeSieur M, Hermann H, Gérard N, Habener JF: Developmental stagespecific expression of the cyclic AMP response element binding protein CREB during spermatogenesis involves alternative exon splicing. Mol Endocrinol 1991;5:1418-1430.
44. West AP, Sharpe RM. Saunders PTK: 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. Biol Reprod 1994;50:869-881.
45. Molina CA, Foulkes NS, Lalli E, Sassone-Corsi P: Inducibility and negative autoregulation of CREM: An alternative promoter directs the expression of ICER, an early response repressor. Cell 1993;75:875-886.
46. Delmas V, van der Hoorn F, Mellstrom B, Jegou B, Sassone-Corsi P: Induction of CREM activator proteins in spermatids: Down-stream targets and implications for haploid germ cell differentiation. Mol Endocrinol 1993;7:1502-1514.
47. Monoco L, Foulkes N, Sassone-Corsi P: Pituitary follicle-stimulating hormone (FSH) induces CREMgene expression in Sertoli cells: Involvement in long termdesensitization of the FSH receptor. Proc Natl Acad Sci USA 1995;92:10673-10677.
48. Hoeffler JP, Habener JF: Characterization of a cAMP regulatory element binding protein. Trends Endocrinol Metab 1990;13:184-188.
49. Ruppert S, Cole TJ, Boshart M, Schmid E, Schutz G: Multiple mRNA isoforms of the transcription activator protein CREB: Generation by alternative splicing and specific expression in primary spermatocytes. EMBO J 1992;11:1503-1512.
50. Yamamoto KK, Gonzalez GA, Menzel P, Rivier J, Montminy MR: Characterization of a bipartite activator domain in transcription factor CREB. Cell 1990;60:611-617.
51. Walker WH, Girardet C, Habener JF: Alternative exon splicing controls a translational switch from activator to repressor isoforms of transcription factor CREB during spermatogenesis. J Biol Chem 1996;271:20145-21050.
52. Gellersen B, Kempf R, Telgmann R: Human endometrial stromal cells express novel isoforms of the transcriptional modulator CREM and up-regulate ICER in the course of decidualization. Mol Endocrinol 1997;11:97-113.
53. Girardet C, Walker WH, Habener JF: An alternatively spliced polycistronic mRNA encoding cyclic adenosine 3′,5′-monophosphate (cAMP) responsive element binding protein (CREB) in human testis extenguises expression of an internally translated inhibitor CREB isoform. Mol Endocrinol 1996;10:879-891.
54. Waeber G, Habener JF: Novel testis germ cell-specific transcript of the CREB gene contains an alternative spliced exon with multiple in-frame stop codons. Endocrinology 1992;131:2010-2015.
55. Sanborn BM, Millian JL, Meistrich ML, Moore LC: Alternative splicing of CREB and CREM mRNAs in an immortalized germ cell line. J Androl 1997;18:62-70.
56. Foulkes NS, Borrelli E, Sassone-Corsi P: CREM gene: Use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription. Cell 1991;64:739-749.
57. Foulkes NS, Mellstrom B, Benusiglio E, Sassone-Corsi P: Developmental switch of CREM function during spermatogenesis: From antagonist to activator. Nature 1992;355:80-84.
58. Laoide BM, Foulkes NS, Schlotter F, Sassone-Corsi P: The functional versatility of CREM is determined by its modular structure. EMBO J 1993;12:1179-1191.
59. Fujimoto T, Fujisawa J, Yoshida M: Novel isoforms of human cyclic AMP-responsive element modulator (hCREM) mRNA. J Biochem 1994;115:298-303.
60. Walker WH, Sanborn BM, Habener JF: An isoform of transcription factor CREM expressed during spermatogenesis lacks the phosphorylation domain and represses cAMP-induced transcription. Proc Natl Acad Sci USA 1994;91:12423-12427.
61. Uyttersprot N, Miot F: Dog CREM transcription factors: Cloning, tissue distribution, and identification of new isoforms. BBRC 1997;237:74-78.
62. Foulkes NS, Schlotter F, Pevet P, Sassone-Corsi P: Pituitary hormone FSH directs the CREM functional switch during spermatogenesis. Nature 1993;362:264-267.
63. 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.
64. Thompson LH, Brookman KW, Jones NJ, Allen SA, Carrano AV: Molecular cloning of the human XRCC1 gene, which corrects defective DNA strand break repair and sister chromatid exchange. Mol Cell Biol 1990;10:6160-6171.
65. Mackey ZB, Ramos W, Levin DS,Walter CA, McCarrey JR, Tomkinson AE: An alternative splicing event which occurs in mouse pachytene spermatocytes generates a form of DNA ligase III with distinct biochemical properties that may function in meiotic recombination. Mol Cell Biol 1997;17:989-998.
66. Kanai Y, Kanai-Azuma M, Noce T, et al: Identification of two Sox17 messenger RNA isoforms, with and without the high mobility group box region, and their differential expression in mouse spermatogenesis. J Cell Biol 1996;133:667-681.
67. Goodson ML, Sarge KD: Regulated expression of heat shock factor 1 isoforms with distinct leucine zipper arrays via tissue-dependent alternative splicing. Biochem Biophys Res Commun 1995;211:943-949.
68. Gold B, Hecht NB: Differential compartmentalization of messenger ribonucleic acid in murine testis. Biochemistry 1981;20:480-487.
69. Gold B, Stern L, Bradlay FM, Hecht NB: Gene expression during mammalian spermatogenesis. II. Stage-specific differences in mRNA populations. J Exp Zool 1983;225:123-134.
70. Gu W, Hecht NB: 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.
71. Kleene KC: Patterns of translational regulation in the mammalian testis. Mol Reprod Dev 1996;43:268-281.
72. Kleene KC, Distel RJ, Hecht NB: cDNA clones encoding cytoplasmic poly(A)+ RNAs which first appear at detectable levels in haploid phases of spermatogenesis in the mouse. Dev Biol 1983;98:455-464.
73. Mali P, Kaipia A, Kangasniemi M, et al: Stage-specific expression of nucleoprotein mRNAs during rat and mouse spermatogenesis. Reprod Fertil Dev 1989;1:369-382.
74. Yelick PC, Kwon YH, Flynn JF, Borzorgzadeh A, Kleene KC, Hecht NB: Mouse transition protein 1 is translationally regulated during the postmeiotic stages of spermatogenesis. Mol Reprod Dev 1989;1:193-200.
75. Kleene KC, Distel RJ, Hecht NB: Translational regulation and deadenylation of a protamine mRNA during spermatogenesis in the mouse. Dev Biol 1984;105:71-79.
76. Braun RE, Peschon JJ, Behringer RR, Brinster RL, Palmiter RD: Protamine 3′ untranslated sequences regulate temporal translational control and subcellular localization of growth hormone in spermatids of transgenic mice. Genes Dev 1989;3:793-802.
77. Kwon YK, Hecht NB: Cytoplasmic protein binding to highly conserved sequences in the 3′ untranslated region of mouse protamine 2 mRNA, a translationally regulated transcript of male germ cells. Proc Natl Acad Sci USA 1991;88:3584-3588.
78. Kwon YK, Hecht NB: Binding of a phosphoprotein to the 3′ untranslated region of the mouse protamine 2 mRNA temporally represses its translation. Mol Cell Biol 1993;13:6547-6557.
79. Fajardo MA, Butner KA, Lee K, Braun RE: Germ cell-specific proteins interact with the 3′ untranslated regions of prm-1 and prm-2 mRNA. Dev Biol 1994;166:643-653.
80. Schumacher JM, Lee K, Edelhoff S, Braun RE: Spnr, a murine RNA-binding protein that is localized to cytoplasmic microtubules. J Cell Biol 1995;129:1023-1032.
81. Schumacher JM, Lee K, Edelhoff S, Braun RE: Distribution of Tenr, an RNA-binding protein, in a lattice-like network within the spermatid nucleus in the mouse. Biol Reprod 1995;52:1274-1283.
82. Lee K, Fajardo M, Braun RE: A testis cytoplasmic RNA-binding protein that has the properties of a translational repressor. Mol Cell Biol 1996;16:3023-3034.
83. Schmidt EE, Schibler U: High accumulation of components of the RNA polymerase II transcription machinery in rodent spermatids. Development 1995;121:2373-2383.
84. Schmidt EE, Schibler U: Developmental testis-specific regulation of mRNA levels and mRNA translational efficiencies for TATA-binding protein mRNA isoforms. Dev Biol 1997;184:138-149.
85. Schmidt EE, Ohbauyashi T, Makino Y, Tamura T-A, Schibler U: Spermatid-specific overexpression of the TATA-binding protein gene involves recruitment of two potent testis-specific promoters. J Biol Chem 1997;272:5326-5334.