Sperm-specific AKAP3 is a dual-specificity anchoring protein that interacts with both protein kinase a regulatory subunits via conserved N-terminal amphipathic peptides

Molecular Reproduction and Development

Volumn 81, Issue 7, 2014, Pages 595-607

  Xu, Kaibiao ^a   Qi, Huayu ^a  

^a GUANGZHOU INSTITUTES OF BIOMEDICINE AND HEALTH   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN 3; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IALPHA; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IIALPHA; UNCLASSIFIED DRUG; AKAP3 PROTEIN, HUMAN; AKAP3 PROTEIN, MOUSE; CYCLIC AMP; PEPTIDE;

ANIMAL CELL; ARTICLE; CYTOPLASM; GERM CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MEIOSIS; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SPERM; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT;

A KINASE ANCHOR PROTEINS; AMINO ACID SEQUENCE; ANIMALS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HEK293 CELLS; HUMANS; MALE; MICE; MOLECULAR SEQUENCE DATA; PEPTIDES; SEQUENCE ALIGNMENT; SPERMATIDS;

EID: 84904381504     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.22329     Document Type: Article

References (49)

1. Alto NM, Soderling SH, Hoshi N, Langeberg LK, Fayos R, Jennings PA, Scott JD. 2003. Bioinformatic design of A-kinase anchoring protein-in silico: A potent and selective peptide antagonist of type II protein kinase A anchoring. Proc Natl Acad Sci USA 100:4445-4450.
2. Aye TT, Mohammed S, van der Toorn HW, van Veen TA, van der Heyden MA, Scholten A, Heck AJ. 2009. Selectivity in enrichment of cAMP-dependent protein kinase regulatory subunits type I and type II and their interactors using modified cAMP affinity resins. Mol Cell Proteomics 8:1016-1028.
3. Bajpai M, Fiedler SE, Huang Z, Vijayaraghavan S, Olson GE, Livera G, Conti M, Carr DW. 2006. AKAP3 selectively binds PDE4A isoforms in bovine spermatozoa. Biol Reprod 74:109-118.
4. Beavo J, Brunton L. 2002. Cyclic nucleotide research-Still expanding after half a century. Nat Rev Mol Cell Biol 3:710-718.
5. Bellve AR. 1993. Purification, culture, and fractionation of spermatogenic cells. Methods Enzymol 225:84-113.
6. Brown PR, Miki K, Harper DB, Eddy EM. 2003. A-kinase anchoring protein 4 binding proteins in the fibrous sheath of the sperm flagellum. Biol Reprod 68:2241-2248.
7. Burton KA, McKnight GS. 2007. PKA, germ cells, and fertility. Physiology (Bethesda) 22:40-46.
8. Burton KA, McDermott DA, Wilkes D, Poulsen MN, Nolan MA, Goldstein M, Basson CT, McKnight GS. 2006. Haploinsufficiency at the protein kinase A RI alpha gene locus leads to fertility defects in male mice and men. Mol Endocrinol 20:2504-2513.
9. Carlson CR, Lygren B, Berge T, Hoshi N, Wong W, Tasken K, Scott JD. 2006. Delineation of type I protein kinase A-selective signaling events using an RI anchoring disruptor. J Biol Chem 281:21535-21545.
10. Carlucci A, Lignitto L, Feliciello A. 2008. Control of mitochondria dynamics and oxidative metabolism by cAMP, AKAPs and the proteasome. Trends Cell Biol 18:604-613.
11. Carr DW, Stofko-Hahn RE, Fraser ID, Bishop SM, Acott TS, Brennan RG, Scott JD. 1991. Interaction of the regulatory subunit (RII) of cAMP-dependent protein kinase with RII-anchoring proteins occurs through an amphipathic helix binding motif. J Biol Chem 266:14188-14192.
12. Carr DW, Fujita A, Stentz CL, Liberty GA, Olson GE, Narumiya S. 2001. 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 276:17332-17338.
13. Chen Q, Lin RY, Rubin CS. 1997. Organelle-specific targeting of protein kinase AII (PKAII). Molecular and in situ characterization of murine A kinase anchor proteins that recruit regulatory subunits of PKAII to the cytoplasmic surface of mitochondria. J Biol Chem 272:15247-15257.
14. Clegg CH, Cadd GG, McKnight GS. 1988. Genetic characterization of a brain-specific form of the type I regulatory subunit of cAMP-dependent protein kinase. Proc Natl Acad Sci USA 85:3703-3707.
15. Day ME, Gaietta GM, Satri M, Koller A, Mackey MR, Scott JD, Perkins GA, Ellisman MH, Taylor SS. 2011. Isoform-specific targeting of PKA to multivesicular bodies. J Cell Biol 193:347-363.
16. Gold MG, Lygren B, Dokurno P, Hoshi N, McConnachie G, Tasken K, Carlson CR, Scott JD, Barford D. 2006. Molecular basis of AKAP specificity for PKA regulatory subunits. Mol Cell 24:383-395.
17. Hou T, Li Y, Wang W. 2011. Prediction of peptides binding to the PKA RIIalpha subunit using a hierarchical strategy. Bioinformatics 27:1814-1821.
18. Huang LJ, Durick K, Weiner JA, Chun J, Taylor SS. 1997a. Identification of a novel protein kinase A anchoring protein that binds both type I and type II regulatory subunits. J Biol Chem 272:8057-8064.
19. Huang LJ, Durick K, Weiner JA, Chun J, Taylor SS. 1997b. D-AKAP2, a novel protein kinase A anchoring protein with a putative RGS domain. Proc Natl Acad Sci USA 94:11184-11189.
20. Imaizumi-Scherrer T, Faust DM, Barradeau S, Hello R, Weiss MC. 2001. Type I protein kinase a is localized to interphase microtubules and strongly associated with the mitotic spindle. Exp Cell Res 264:250-265.
21. Jarnaess E, Ruppelt A, Stokka AJ, Lygren B, Scott JD, Tasken K. 2008. Dual specificity A-kinase anchoring proteins (AKAPs) contain an additional binding region that enhances targeting of protein kinase A type I. J Biol Chem 283:33708-33718.
22. Johnson LR, Foster JA, Haig-Ladewig L, Vanscoy H, Rubin CS, Moss SB, Gerton GL. 1997. Assembly of AKAP82, a protein kinase A anchor protein, into the fibrous sheath of mouse sperm. Dev Biol 192:340-350.
23. Kammerer S, Burns-Hamuro L, Ma Y, Hamon S, Canaves J, Shi MM, Nelson MR, Sing CF, Cantor CR, Taylor SS, Braun A. 2003. Amino acid variant in the kinase binding domain of dual-specific A kinase-anchoring protein 2: A disease susceptibility polymorphism. Proc Natl Acad Sci USA 100:4066-4071.
24. Kim C, Xuong NH, Taylor SS. 2005. Crystal structure of a complex between the catalytic and regulatory (RIalpha) subunits of PKA. Science 307:690-696.
25. Kinderman FS, Kim C, von Daake S, Ma Y, Pham BQ, Spraggon G, Xuong NH, Jennings PA, Taylor SS. 2006. A dynamic mechanism for AKAP binding to RII isoforms of cAMP-dependent protein kinase. Mol Cell 24:397-408.
26. Kirschner LS, Carney JA, Pack SD, Taymans SE, Giatzakis C, Cho YS, Cho-Chung YS, Stratakis CA. 2000. Mutations of the gene encoding the protein kinase A type I-alpha regulatory subunit in patients with the Carney complex. Nat Genet 26:89-92.
27. Kotaja N, Macho B, Sassone-Corsi P. 2005. 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 280:31739-31745.
28. Landmark BF, Oyen O, Skalherg BS, Fauske B, Jahnsen T, Hansson V. 1993. Cellular location and age-dependent changes of the regulatory subunits of cAMP-dependent protein kinase in rat testis. J Reprod Fertil 99:323-334.
29. Lester LB, Coghlan VM, Nauert B, Scott JD. 1996. Cloning and characterization of a novel A-kinase anchoring protein. AKAP 220: Association with testicular peroxisomes. J Biol Chem 271:9460-9465.
30. Luconi M, Carloni V, Marra F, Ferruzzi P, Forti G, Baldi E. 2004. Increased phosphorylation of AKAP by inhibition of phosphatidylinositol 3-kinase enhances human sperm motility through tail recruitment of protein kinase A. J Cell Sci 117:1235-1246.
31. Ma Y, Taylor SS. 2002. A 15-residue bifunctional element in D-AKAP1 is required for both endoplasmic reticulum and mitochondrial targeting. J Biol Chem 277:27328-27336.
32. Macho B, Brancorsini S, Fimia GM, Setou M, Hirokawa N, Sassone-Corsi P. 2002. CREM-dependent transcription in male germ cells controlled by a kinesin. Science 298:2388-2390.
33. Meetei A, Ullas K, Vasupradha V, Rao M. 2002. Involvement of protein kinase A in the phosphorylation spermatidal protein TP2 and its effect on DNA condensation. Biochemistry 41:185-195.
34. Miki K, Eddy E. 1998. Identification of tethering domains for protein kinase A type Ialpha regulatory subunits on sperm fibrous sheath protein FSC1. J Biol Chem 273:34384-34390.
35. Miki K, Willis WD, Brown PR, Goulding EH, Fulcher KD, Eddy EM. 2002. Targeted disruption of the Akap4 gene causes defects in sperm flagellum and motility. Dev Biol 248:331-342.
36. Newell AE, Fiedler SE, Ruan JM, Pan J, Wang PJ, Deininger J, Corless CL, Carr DW. 2008. Protein kinase A RII-like (R2D2) proteins exhibit differential localization and AKAP interaction. Cell Motil Cytoskeleton 65:539-552.
37. Niu J, Vaiskunaite R, Suzuki N, Kozasa T, Carr DW, Dulin N, Voyno-Yasenetskaya TA. 2001. Interaction of heterotrimeric G13 protein with an A-kinase-anchoring protein 110 (AKAP110) mediates cAMP-independent PKA activation. Curr Biol 11:1686-1690.
38. Nolan MA, Babcock DF, Wennemuth G, Brown W, Burton KA, McKnight GS. 2004. Sperm-specific protein kinase A catalytic subunit Calpha2 orchestrates cAMP signaling for male fertility. Proc Natl Acad Sci USA 101:13483-13488.
39. Reinton N, Orstavik S, Haugen TB, Jahnsen T, Tasken K, Skalhegg BS. 2000. A novel isoform of human cyclic 3′, 5′-adenosine monophosphate-dependent protein kinase, c alpha-s, localizes to sperm midpiece. Biol Reprod 63:607-611.
40. Sarma GN, Kinderman FS, Kim C, von Daake S, Chen L, Wang BC, Taylor SS. 2010. Structure of D-AKAP2: PKA RI complex: Insights into AKAP specificity and selectivity. Structure 18:155-166.
41. Scott JD, Dessauer CW, Tasken K. 2013. Creating order from chaos: Cellular regulation by kinase anchoring. Annu Rev Pharmacol Toxicol l53:187-210.
42. Skalhegg BS, Huang Y, Su T, Idzerda RL, McKnight GS, Burton KA. 2002. Mutation of the Calpha subunit of PKA leads to growth retardation and sperm dysfunction. Mol Endocrinol 16:630-639.
43. Smith SB, White HD, Siegel JB, Krebs EG. 1981. Cyclic AMP-dependent protein kinase I: Cyclic nucleotide binding, structural changes, and release of the catalytic subunits. Proc Natl Acad Sci USA 78:1591-1595.
44. Taylor SS, Ilouz R, Zhang P, Kornev AP. 2012. Assembly of allosteric macromolecular switches: Lessons from PKA. Nat Rev Mol Cell Biol 13:646-658.
45. Vijayaraghavan S, Liberty GA, Mohan J, Winfrey VP, Olson GE, Carr DW. 1999. Isolation and molecular characterization of AKAP110, a novel, sperm-specific protein kinase A-anchoring protein. Mol Endocrinol 13:705-717.
46. Visconti PE, Johnson LR, Oyaski M, Fornes M, Moss SB, Gerton GL, Kopf GS. 1997. Regulation, localization, and anchoring of protein kinase A subunits during mouse sperm capacitation. Dev Biol 192:351-363.
47. Wong W, Scott JD. 2004. AKAP signalling complexes: Focal points in space and time. Nat Rev Mol Cell Biol l5:959-970.
48. Zhang X, Odom DT, Koo SH, Conkright MD, Canettieri G, Best J, Chen H, Jenner R, Herbolsheimer E, Jacobsen E, Kadam S, Ecker JR, Emerson B, Hogenesch JB, Unterman T, Young RA, Montminy M. 2005. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci USA A102:4459-4464.
49. Zhang P, Smith-Nguyen EV, Keshwani MM, Deal MS, Kornev AP, Taylor SS. 2012. Structure and allostery of the PKA RIIbeta tetrameric holoenzyme. Science 335:712-716.