AKAP3 synthesis is mediated by RNA binding proteins and PKA signaling during mouse spermiogenesis

Biology of Reproduction

Volumn 90, Issue 6, 2014, Pages

  Xu, Kaibiao ^a   Yang, Lele ^a   Zhao, Danyun ^a   Wu, Yaoyao ^b   Qi, Huayu ^a  

^a GUANGZHOU INSTITUTES OF BIOMEDICINE AND HEALTH   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

AKAP3; PKA; RNA binding protein; Spermiogenesis; Translation

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN 3; MESSENGER RNA; PROTEI PIWIL1; PROTEIN NONO; PROTEIN PABPC1; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; AKAP3 PROTEIN, MOUSE; ARGONAUTE PROTEIN; DNA BINDING PROTEIN; EPAB PROTEIN, MOUSE; NONO PROTEIN, MOUSE; PIWIL1 PROTEIN, MOUSE; POLYADENYLIC ACID BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL GRANULE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GERM CELL; IMMUNOPRECIPITATION; MALE; MEIOSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; RNA PROCESSING; SEMINIFEROUS TUBULE; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; ANIMAL; CELL CULTURE; CYTOLOGY; CYTOPLASM; GENETICS; INBRED MOUSE STRAIN; METABOLISM; PHYSIOLOGY; SPERMATOZOON TAIL;

A KINASE ANCHOR PROTEINS; ANIMALS; ARGONAUTE PROTEINS; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOPLASM; DNA-BINDING PROTEINS; MALE; MICE, INBRED STRAINS; POLY(A)-BINDING PROTEINS; PROTEIN BIOSYNTHESIS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; SPERM TAIL; SPERMATIDS; SPERMATOGENESIS;

EID: 84901625523     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.116111     Document Type: Article

References (65)

1. Oatley JM, Brinster RL. Regulation of spermatogonial stem cell selfrenewal in mammals. Annu Rev Cell Dev Biol 2008; 24:263-286.
2. Leblond CP, Clermont Y. Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the periodic acid-fuchsin sulfurous acid technique. Am J Anat 1952; 90:167-215.
3. Cooke HJ, Saunders PT. Mouse models of male infertility. Nat Rev Genet 2002; 3:790-801.
4. 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.
5. 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.
6. Iguchi N, Tobias J, Hecht N. 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.
7. Blendy JA, Kaestner KH, Weinbauer GF, Nieschlag E, Schutz G. Severe impairment of spermatogenesis in mice lacking the CREM gene. Nature 1996; 380:162-165.
8. Nantel F, Monaco L, Foulkes NS, Masquilier D, LeMeur M, Henriksen K, Dierich A, Parvinen M, Sassone-Corsi P. Spermiogenesis deficiency and germ-cell apoptosis in CREM-mutant mice. Nature 1996; 380:159-162.
9. Martianov I, Fimia GM, Dierich A, Pavinen M, Sassone-Corsi P, Davidson I. Late arrest of spermiogenesis and germ cell apoptosis in mice lacking the TBP-like TLF/TRF2 gene. Mol Cell 2001; 7:509-515.
10. Kotaja N, De Cesare D, Macho B, Monaco L, Brancorsini S, Goossens E, Tournaye H, Gansmuller A, Sassone-Corsi P. Abnormal sperm in mice with targeted deletion of the act (activator of cAMP-responsive element modulator in testis) gene. Proc Natl Acad Sci U S A 2004; 101: 10620-10625.
11. Braun RE. Packaging paternal chromosomes with protamine. Nat Genet 2001; 28:10-12.
12. Schafer M, Nayernia K, Engel W, Schafer U. Translational control in spermatogenesis. Dev Biol 1995; 172:344-352.
13. White-Cooper H, Schafer MA, Alphey LS, Fuller, MT. Transcriptional and post-transcriptional control mechanisms coordinate the onset of spermatid differentiation with meiosis I in Drosophila. Development 1998; 125:125-134.
14. Baker CC, Fuller MT. Translational control of meiotic cell cycle progression and spermatid differentiation in male germ cells by a novel eIF4G homolog. Development 2007; 134:2863-2869.
15. Bagarova J, Chowdhury T, Kimura M, Kleene K. Identification of elements in the Smcp 50 and 30 UTR that repress translation and promote the formation of heavy inactive mRNPs in spermatids by analysis of mutations in transgenic mice. Reproduction 2010; 140:853-864.
16. Giorgini F, Davies H, Braun R. MSY2 and MSY4 bind a conserved sequence in the 30 untranslated region of protamine 1 mRNA in vitro and in vivo. Mol Cell Biol 2001; 21:7010-7019.
17. 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.
18. Anderson P, Kedersha N. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 2009; 10:430-436.
19. Yokota S. Historical survey on chromatoid body research. Acta Histochem Cytochem 2008; 41:65-82.
20. Fawcett D, Eddy E, Phillips D. Observations on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis. Biol Reprod 1970; 2:129-153.
21. Comings D, Okada T. The chromatoid body in mouse spermatogenesis: evidence that it may be formed by the extrusion of nucleolar components. J Ultrastruct Res 1972; 39:15-23.
22. Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, Noce T. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 2000; 93:139-149.
23. Kotaja N, Bhattacharyya SN, Jaskiewicz L, Kimmins S, Parvinen M, Filipowicz W, Sassone-Corsi P. The chromatoid body of male germ cells: similarity with processing bodies and presence of Dicer and microRNA pathway components. Proc Natl Acad Sci U S A 2006; 103:2647-2652.
24. Yabuta Y, Ohta H, Abe T, Kurimoto K, Chuma S, Saitou M. TDRD5 is required for retrotransposon silencing, chromatoid body assembly, and spermiogenesis in mice. J Cell Biol 2011; 192:781-795.
25. Hosokawa M, Shoji M, Kitamura K, Tanaka T, Noce T, Chuma S, Nakatsuji N. Tudor-related proteins TDRD1/MTR-1, TDRD6 and TDRD7/TRAP: domain composition, intracellular localization, and function in male germ cells in mice. Dev Biol 2007; 301:38-52.
26. Giorgini F, Davies HG, Braun, RE. Translational repression by MSY4 inhibits spermatid differentiation in mice. Development 2002; 129: 3669-3679.
27. Morales CR, Lefrancois S, Chennathukuzhi V, El-Alfy M, Wu X, Yang J, Gerton GL, Hecht NB. ATB-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.
28. Taylor SS, Ilouz R, Zhang P, Kornev AP. Assembly of allosteric macromolecular switches: lessons from PKA. Nat Rev Mol Cell Biol 2012; 13:646-658.
29. Lonnerberg P, Parvinen M, Jahnsen T, Hansson V, Persson H. Stage- and cell-specific expression of cyclic adenosine 3',5'-monophosphate-dependent protein kinases in rat seminiferous epithelium. Biol Reprod 1992; 46: 1057-1068.
30. Nolan MA, Babcock DF, Wennemuth G, Brown W, Burton KA, McKnight GS. Sperm-specific protein kinase A catalytic subunit Calpha2 orchestrates cAMP signaling for male fertility. Proc Natl Acad Sci U S A 2004; 101:13483-13488.
31. Burton KA, McKnight GS. PKA, germ cells, and fertility. Physiology (Bethesda) 2007; 22:40-46.
32. Burton KA, McDermott DA, Wilkes D, Poulsen MN, Nolan MA, Goldstein M, Basson CT, McKnight GS. Haploinsufficiency at the protein kinase A RI alpha gene locus leads to fertility defects in male mice and men. Mol Endocrinol 2006; 20:2504-2513.
33. Skalhegg BS, Huang Y, Su T, Idzerda RL, McKnight GS, Burton KA. Mutation of the Calpha subunit of PKA leads to growth retardation and sperm dysfunction. Mol Endocrinol 2002; 16:630-639.
34. Kotaja N, Macho B, Sassone-Corsi P. Microtubule-independent and protein kinase A-mediated function of kinesin KIF17b controls the intracellular transport of activator of CREM in testis (ACT). J Biol Chem 2005; 280:31739-31745.
35. Scott JD, Dessauer CW, Tasken K. Creating order from chaos: cellular regulation by kinase anchoring. Annu Rev Pharmacol Toxicol 2013; 53: 187-210.
36. Huang L, Durick K, Weiner J, Chun J, Taylor SS. Identification of a novel protein kinase A anchoring protein that binds both type I and type II regulatory subunits. J Biol Chem 1997; 272:8057-8064.
37. Huang L, Durick K, Weiner J, Chun J, Taylor SS. D-AKAP2, a novel protein kinase A anchoring protein with a putative RGS domain. Proc Natl Acad Sci U S A 1997; 94:11184-11189.
38. Reinton N, Collas P, Haugen TB, Skalhegg BS, Hansson V, Jahnsen T, Tasken K. Localization of a novel human A-kinase-anchoring protein, hAKAP220, during spermatogenesis. Dev Biol 2000; 223:194-204.
39. Vijayaraghavan S, Liberty GA, Mohan J, Winfrey VP, Olson GE, Carr DW. Isolation and molecular characterization of AKAP110, a novel, sperm-specific protein kinase A-anchoring protein. Mol Endocrinol 1999; 13:705-717.
40. Carrera A, Gerton GL, Moss SB. The major fibrous sheath polypeptide of mouse sperm: structural and functional similarities to the A-kinase anchoring proteins. Dev Biol 1994; 165:272-284.
41. Lin R, Moss S, Rubin C. Characterization of S-AKAP84, a novel developmentally regulated A kinase anchor protein of male germ cells. J Biol Chem 1995; 270:27804-27811.
42. Brown PR, Miki K, Harper DB, Eddy EM. A-kinase anchoring protein 4 binding proteins in the fibrous sheath of the sperm flagellum. Biol Reprod 2003; 68:2241-2248.
43. Luconi M, Porazzi I, Ferruzzi P, Marchiani S, Forti G, Baldi E. Tyrosine phosphorylation of the a kinase anchoring protein 3 (AKAP3) and soluble adenylate cyclase are involved in the increase of human sperm motility by bicarbonate. Biol Reprod 2005; 72:22-32.
44. Newhall KJ, Criniti AR, Cheah CS, Smith KC, Kafer KE, Burkart AD, McKnight GS. Dynamic anchoring of PKA is essential during oocyte maturation. Curr Biol 2006; 16:321-327.
45. Tingley W, Pawlikowska L, Zaroff J, Kim T, Nguyen T, Young SG, Vranizan K, Kwok PY, Whooley MA, Conklin BR. Gene-trapped mouse embryonic stem cell-derived cardiac myocytes and human genetics implicate AKAP10 in heart rhythm regulation. Proc Natl Acad Sci U S A 2007; 104:8461-8466.
46. Miki K, Willis WD, Brown PR, Goulding EH, Fulcher KD, Eddy EM. Targeted disruption of the Akap4 gene causes defects in sperm flagellum and motility. Dev Biol 2002; 248:331-342.
47. Bajpai M, Fiedler SE, Huang Z, Vijayaraghavan S, Olson GE, Livera G, Conti M, Carr DW. AKAP3 selectively binds PDE4A isoforms in bovine spermatozoa. Biol Reprod 2006; 74:109-118.
48. Niu J, Vaiskunaite R, Suzuki N, Kozasa T, Carr DW, Dulin N, Voyno-Yasenetskaya TA. Interaction of heterotrimeric G13 protein with an Akinase-anchoring protein 110 (AKAP110) mediates cAMP-independent PKA activation. Curr Biol 2001; 11:1686-1690.
49. Carr DW, Fujita A, Stentz CL, Liberty GA, Olson GE, Narumiya S. Identification of sperm-specific proteins that interact with A-kinase anchoring proteins in a manner similar to the type II regulatory subunit of PKA. J Biol Chem 2001; 276:17332-17338.
50. Bellve AR. Purification, culture, and fractionation of spermatogenic cells. Methods Enzymol 1993; 225:84-113.
51. Deng W, Lin H. Miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2002; 2:819-830.
52. Kimura M, Ishida K, Kashiwabara S, Baba T. Characterization of two cytoplasmic poly (A)-binding proteins, PABPC1 and PABPC2, in mouse spermatogenic cells. Biol Reprod 2009; 80:545-554.
53. Bond CS, Fox AH. Paraspeckles: nuclear bodies built on long noncoding RNA. J Cell Biol 2009; 186:637-644.
54. Myojin R, Kuwahara S, Yasaki T, Matsunaga T, Sakurai T, Kimura M, Uesugi S, Kurihara Y. Expression and functional significance of mouse paraspeckle protein 1 on spermatogenesis. Biol Reprod 2004; 71:926-932.
55. Kuwahara S, Ikei A, Taguchi Y, Tabuchi Y, Fujimoto N, Obinata M, Uesugi S, Kurihara Y. PSPC1, NONO, and SFPQ are expressed in mouse Sertoli cells and may function as coregulators of androgen receptormediated transcription. Biol Reprod 2006; 75:352-359.
56. Grivna ST, Pyhtila B, Lin, H. MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci U S A 2006; 103:13415-13420.
57. Kleene K. Poly(A) shortening accompanies the activation of translation of five mRNAs during spermiogenesis in the mouse. Development 1989; 106:367-373.
58. 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.
59. Thomson T, Lin H. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol 2009; 25: 355-376.
60. Zhao S, Gou LT, Zhang M, Zu LD, Hua MM, Hua Y, Shi HJ, Li Y, Li J, Li D, Wang ED, Liu MF. piRNA-triggered MIWI ubiquitination and removal by APC/C in late spermatogenesis.Dev Cell 2013; 24:13-25.
61. Vourekas A, Zheng Q, Alexiou P, Maragkakis M, Kirino Y, Gregory BD, Mourelatos Z. Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis. Nat Struct Mol Biol 2012; 19:773-781.
62. Reuter M, Berninger P, Chuma S, Shah H, Hosokawa M, Funaya C, Antony C, Sachidanandam R, Pillai RS. Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 2011; 480:264-267.
63. Peruquetti R, de Mateo S, Sassone-Corsi P. Circadian proteins CLOCK and BMAL1 in the chromatoid body, a RNA processing granule of male germ cells. PLoS One 2012; 7:e42695.
64. Jungmann R, Kiryukhina O. Cyclic AMP and AKAP-mediated targeting of protein kinase A regulates lactate dehydrogenase subunit A mRNA stability. J Biol Chem 2005; 280:25170-25177.
65. Unal R, Pokrovskaya I, Tripathi P, Monia B, Kern P, Ranganathan G. Translational regulation of lipoprotein lipase in adipocytes: depletion of cellular protein kinase Calpha activates binding of the C subunit of protein kinase A to the 3'-untranslated region of the lipoprotein lipase mRNA. Biochem J 2008; 413:315-322.