Polypyrimidine tract binding protein 2 stabilizes phosphoglycerate kinase 2 mRNA in murine male germ cells by binding to its 3′UTR

Biology of Reproduction

Volumn 76, Issue 6, 2007, Pages 1025-1033

  Xu, Mingang ^a   Hecht, Norman B ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Gametogenesis; Gene regulation; Posttranscriptional control; RNA binding proteins; Spermatogenesis

Indexed keywords

MESSENGER RNA; PHOSPHOGLYCERATE KINASE; PHOSPHOGLYCERATE KINASE 2; POLYPYRIMIDINE TRACT BINDING PROTEIN; POLYPYRIMIDINE TRACT BINDING PROTEIN 1; POLYPYRIMIDINE TRACT BINDING PROTEIN 2; RNA BINDING PROTEIN; TRANS ACTING FACTOR; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GERM CELL; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA STABILITY; SPERMATOGENESIS; TESTIS;

ANIMALS; GENE EXPRESSION PROFILING; GERM CELLS; HELA CELLS; HUMANS; ISOENZYMES; MALE; MICE; MICE, INBRED STRAINS; NERVE TISSUE PROTEINS; PHOSPHOGLYCERATE KINASE; POLYPYRIMIDINE TRACT-BINDING PROTEIN; PROTEIN BINDING; REGULATORY ELEMENTS, TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; SPERMATOZOA; TESTIS; TRANSFECTION;

MURINAE;

EID: 34249673345     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.107.060079     Document Type: Article

References (49)

1. Kuersten S, Goodwin EB. The power of the 3′UTR: translational control and development. Nat Rev Genet 2003; 4:626-637.
2. Kierszenbaum AL, Tres LL. RNA transcription and chromatin structure during meiotic and postmeiotic stages of spermatogenesis. Fed Proc 1978; 37:2512-2516.
3. Braun RE. Post-transcriptional control of gene expression during spermatogenesis. Semin Cell Dev Biol 1998, 9:483-489.
4. Hecht NB. Molecular mechanisms of male germ cell differentiation. Bioessays 1998; 20:555-561.
5. 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 USA 2006; 103:7712-7717.
6. Banks RD, Blake CCF, Evans PR, Haser R, Rice DW, Hardy GW, Merrett M, Phillips AW. Sequence, structure and activity of phosphoglycerate kinase: a possible hinge-bending enzyme. Nature 1979; 279:773-777.
7. Lay AJ, Jiang XM, Kisker O, Flynn E, Underwood A, Condron R, Hogg PJ. Phosphoglycerate kinase acts in tumour angiogenesis as a disulphide reductase. Nature 2000; 408:869-873.
8. McCarrey JR, Thomas K, Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 1987; 326:501-505.
9. Robinson MO, McCarrey JR, Simon MI. Transcriptional regulatory regions of testis-specific PGK2 defined in transgenic mice. Proc Natl Acad Sci U S A 1989; 86:8437-8441.
10. McCarrey JR, Berg WM, Paragioudakis SJ, Zhang PL, Dilworth DD, Arnold BL, Rossi JJ. Differential transcription of Pgk genes during spermatogenesis in the mouse. Dev Biol 1992; 154:160-168.
11. Erickson RP, Kramer JM, Rittenhouse J, Salkeld A. Quantitation of mRNAs during mouse spermatogenesis: protamine-like histone and phosphoglycerate kinase-2 mRNAs increase after meiosis. Proc Natl Acad Sci USA 1980; 77:6086-6090.
12. Gold B, Fujimoto H, Kramer JM, Erickson RP, Hecht NB. Haploid accumulation and translational control of phosphoglycerate kinase-2 messenger RNA during mouse spermatogenesis. Dev Biol 1983; 98: 392-399.
13. Erickson RP, Michelson AM, Rosenberg MP, Sanchez E, Orkin SH. Post-meiotic transcription of phosphoglycerate-kinase 2 in mouse testes. Biosci Rep 1985; 5:1087-1091.
14. McCarrey JR, Kumari M, Aivaliotis MJ, Wang Z, Zhang P, Marshall F, Vandeberg JL. Analysis of the cDNA and encoded protein of the human testis-specific PGK-2 gene. Dev Genet 1996; 19:321-332.
15. Mizuno K, Goto M, Masamune Y, Nakanishi Y. A silencer-like cis element for the testis-specific phosphoglycerate-kinase-2-encoding gene. Gene 1992; 119:293-297.
16. Goto M, Masamune Y, Nakanishi Y. A factor stimulating transcription of the testis-specific Pgk-2 gene recognizes a sequence similar to the binding site for a transcription inhibitor of the somatic-type Pgk-1 gene. Nucleic Acids Res 1993; 21:209-214.
17. Zhang LP, Stroud J, Eddy CA, Walter CA, McCarrey JR. Multiple elements influence transcriptional regulation from the human testis-specific PGK2 promoter in transgenic mice. Biol Reprod 1999; 60:1329-1337.
18. Bluthmann H, Cicurel L, Kuntz GW, Haedenkamp G, Illmensee K. Immunohistochemical localization of mouse testis-specific phosphoglycerate kinase (PGK-2) by monoclonal antibodies. EMBO J 1982; 1:479-484.
19. Tillmar L, Carlsson C, Welsh N. Control of insulin mRNA stability in rat pancreatic islets. Regulatory role of a 3′-untranslated region pyrimidine-rich sequence. J Biol Chem 2002; 277:1099-1106.
20. Knoch KP, Bergen H, Borgonovo B, Saeger HD, Altkruger A, Verkade P, Solimena M. Polypyrimidine tract-binding protein promotes insulin secretory granule biogenesis. Nat Cell Biol 2004; 6:207-214.
21. Hamilton BJ, Genin A, Cron RQ, Rigby WF. Delineation of a novel pathway that regulates CD154 (CD40 ligand) expression. Mol Cell Biol 2003; 23:510-525.
22. Pautz A, Linker K, Hubrich T, Korhonen R, Altenhofer S, Kleinert H. The polypyrimidine tract-binding protein (PTB) is involved in the posttranscriptional regulation of human inducible nitric oxide synthase expression. J Biol Chem 2006; 281:32294-32302.
23. Han JR, Gu W, Hecht NB. Testis-brain RNA-binding protein, a testicular translational regulatory RNA-binding protein, is present in the brain and binds to the 3′ untranslated regions of transported brain mRNAs. Biol Reprod 1995; 53:707-717.
24. Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 1983; 11:1475-1489.
25. Cho YS, Chennathukuzhi VM, Handel MA, Eppig J, Hecht NB. The relative levels of translin-assoeiated factor X (TRAX) and testis brain RNA-binding protein determine their nucleocytoplasmic distribution in male germ cells. J Biol Chem 2004; 279:31514-31523.
26. Rouault TA, Hentze MW, Haile DJ, Harford JB, and Klausner RD. The iron-responsive element binding protein: a method for the affinity purification of a regulatory RNA-binding protein. Proc Natl Acad Sci U S A 1989; 86:5768-7572.
27. Polydorides AD, Okano HJ, Yang YY, Stefani G, Darnell RB. A brain-enriched polypyrimidine tract-binding protein antagonizes the ability of Nova to regulate neuron-specific alternative splicing. Proc Natl Acad Sci U S A 2000; 97:6350-6355.
28. Hall MP, Huang S, Black DL. Differentiation-induced colocalization of the KH-type splicing regulatory protein with polypyrimidine tract binding protein and the c-src pre-mRNA. Mol Biol Cell 2004; 15:774-786.
29. Markovtsov V, Nikolic JM, Goldman JA, Turck CW, Chou MY, Black DL. Cooperative assembly of an hnRNP complex induced by a tissue-specific homolog of polypyrimidine tract binding protein. Mol Cell Biol 2000; 20:7463-7479.
30. Chen CY, Gherzi R, Andersen JS, Gaietta G, Jürchott K, Royer HD, Mann M, Karin M. Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev 2000; 14:1236-1248.
31. Rahman L, Bliskovski V, Reinhold W, Zajac-Kaye M. Alternative splicing of brain-specific PTB defines a tissue-specific isoform pattern that predicts distinct functional roles. Genomics 2002; 80:245-249.
32. Kleene KC, Distel RJ, Hecht NB. Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse. Dev Biol 1984; 105:71-79.
33. Ghetti A, Pinol-Roma S, Michael W, Morandi C, Dreyfuss G. Nucleic Acids Res 1992; 20:3671-3678.
34. Hellen CU, Witherell GW, Schmid M, Shin SH, Pestova TV, Gil A, Wimmer E. A cytoplasmic 57-kDa protein that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine tract-binding protein. Proc Natl Acad Sci U S A 1993; 90: 7642-7646.
35. Mitchell SA, Spriggs KA, Coldwell MJ, Jackson RJ, Willis AE. The Apaf-1 internal ribosome entry segment attains the correct structural conformation for function via interactions with PTB and unr. Mol Cell 2003; 11:757-771.
36. Perez I, McAfee JG, Pattini JG. Multiple RRMs contribute to RNA binding specificity and affinity for polypyrimidine tract binding protein. Biochemistry 1997; 36:11881-11890.
37. Romanelli MG, Weighardt F, Biamonti G, Riva S, Morandi C. Sequence determinants for hnRNP 1 protein nuclear localization. Exp Cell Res 1997; 235:300-304.
38. Li B, Yen TSB. Characterization of the nuclear export signal of polypyrimidine tract-binding protein. J Biol Chem 2002; 277:10306-10314.
39. Morales CR, Lefrancois S, Chennathukuzhi V, El-Ally M, Wu X, Yang J, Gerton GL, Hecht NB. A TB-RBP and Ter ATPase complex accompanies specific mRNAs from nuclei through the nuclear pores and into intercellular bridges in mouse male germ cells. Dev Biol 2002; 246: 480-494.
40. Sully G, Dean JL, Wait R, Rawlinson L, Santalucia T, Saklatvala J, Clark AR. Structural and functional dissection of a conserved destabilizing element of cyclo-oxygenase-2 mRNA: evidence against the involvement of AUF-1 [AU-rich element/poly(U)-binding/degradation factor-1]. AUF-2, tristetraprolin. HuR (Hu antigen R) or FBP1 (far-upstream-sequence-element-binding protein 1). Biochem J 2004; 377:629-639.
41. Min H, Turck CW, Nikolic JM, Black DL. A new regulatory protein, KSRP, mediates exon inclusion through an intronic splicing enhancer. Genes Dev 1997; 11:1023-1036.
42. Gherzi R, Lee KY, Briata P, Wegmuller D, Moroni C, Karin M, Chen CY. A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol Cell 2004; 14:571-583.
43. Valcareel J, Gebauer F. Post-transcriptional regulation: the dawn of PTB. Curr Biol 1997; 7:705-708.
44. Black DL. Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 2003; 72:291-336.
45. Oberstrass FC, Auweter SD, Erat M, Hargous Y, Henning A, Wemer P, Reymond L, Amir-Ahmady B, Pitsch S, Black DL, Allain FH. Structure of PTB bound to RNA: specific binding and implications for splicing regulation. Science 2005; 309:2054-2057.
46. Chan RC, Black DL. Conserved intron elements repress splicing of a neuron-specific c-src exon in vitro. Mol Cell Biol 1995; 15:6377-6385.
47. Charlet-B N, Logan P, Singh G, Cooper TA. Dynamic antagonism between ETR-3 and PTB regulates cell type-specific alternative splicing. Mol Cell 2002; 9:649-658.
48. Cote CA, Gautreau D, Denegre JM, Kress TL, Terry NA, Mowry KL. A Xenopus protein related to hnRNP 1 has a role in cytoplasmic RNA localization. Mol Cell 1999; 4:431-437.
49. Xie J, Lee JA, Kress TL, Mowry KL, Black DL. Protein kinase A phosphorylation modulates transport of the polypyrimidine tract-binding protein. Proc Natl Acad Sci U S A 2003; 100:8776-8781.