Towards delineation of a developmental α-importome in the mammalian male germline

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 3, 2013, Pages 731-742

  Miyamoto, Yoichi ^a   Baker, Mark A ^b,c   Whiley, Penny A ^a,c   Arjomand, Arash ^a,c   Ludeman, Justin ^a   Wong, Chin ^a,c   Jans, David A ^a,c   Loveland, Kate L ^a,c  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF NEWCASTLE   (Australia)

^c Australian Government Australian Research Council   (Australia)

Author keywords

Importin ; NLS; Nuclear transport; SMC6; Spermatogenesis; Testis

Indexed keywords

DYNAMIN; KARYOPHERIN ALPHA; KARYOPHERIN BETA;

ALGORITHM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL NUCLEUS; CELL TYPE; CHROMOSOME 6; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MALE; MEIOSIS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; RAT; SPERMATOGENESIS; SYNOVIAL SARCOMA; TESTIS;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA KARYOPHERINS; ANIMALS; BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; MALE; MEIOSIS; NUCLEAR LOCALIZATION SIGNALS; PROTEOME; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS; TESTIS;

MAMMALIA; RATTUS;

EID: 84872179740     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.11.005     Document Type: Article

References (46)

1. Kerr J.B., Loveland K.L., O.B.MK, d.K.DM Cytology of the testis and intrinsic control mechanisms. Knobil and Neill's Physiology of Reproduction 2006, vol. 1:827-947. Elsevier. Neill JD (Ed.).
2. Hoelz A., Debler E.W., Blobel G. The structure of the nuclear pore complex. Annu Rev Biochem 2011, 80:613-643.
3. Marfori M., Mynott A., Ellis J.J., Mehdi A.M., Saunders N.F., Curmi P.M., et al. Molecular basis for specificity of nuclear import and prediction of nuclear localization. Biochim Biophys Acta 2011, 1813:1562-1577.
4. Miyamoto Y., Boag P.R., Hime G.R., Loveland K.L. Regulated nucleocytoplasmic transport during gametogenesis. Biochim Biophys Acta 2012, 1819:616-630.
5. Goldfarb D.S., Corbett A.H., Mason D.A., Harreman M.T., Adam S.A. Importin α: a multipurpose nuclear-transport receptor. Trends Cell Biol 2004, 14:505-514.
6. Mason D.A., Stage D.E., Goldfarb D.S. Evolution of the metazoan-specific importin alpha gene family. J Mol Evol 2009, 68:351-365.
7. Yasuda Y., Miyamoto Y., Yamashiro T., Asally M., Masui A., Wong C., et al. Nuclear retention of importin α coordinates cell fate through changes in gene expression. EMBO J 2012, 31:83-94.
8. Yasuhara N., Shibazaki N., Tanaka S., Nagai M., Kamikawa Y., Oe S., et al. Triggering neural differentiation of ES cells by subtype switching of importin-α. Nat Cell Biol 2007, 9:72-79.
9. Young J.C., Major A.T., Miyamoto Y., Loveland K.L., Jans D.A. Distinct effects of importin α2 and α4 on Oct3/4 localization and expression in mouse embryonic stem cells. FASEB J 2011, 25:3958-3965.
10. Major A.T., Whiley P.A., Loveland K.L. Expression of nucleocytoplasmic transport machinery: clues to regulation of spermatogenic development. Biochim Biophys Acta 2011, 1813:1668-1688.
11. Itman C., Miyamoto Y., Young J., Jans D.A., Loveland K.L. Nucleocytoplasmic transport as a driver of mammalian gametogenesis. Semin Cell Dev Biol 2009, 20:607-619.
12. Ly-Huynh J.D., Lieu K.G., Major A.T., Whiley P.A., Holt J.E., Loveland K.L., et al. Importin alpha2-interacting proteins with nuclear roles during mammalian spermatogenesis. Biol Reprod 2011, 85:1191-1202.
13. Meistrich M.L., Longtin J., Brock W.A., Grimes S.R., Mace M.L. Purification of rat spermatogenic cells and preliminary biochemical analysis of these cells. Biol Reprod 1981, 25:1065-1077.
14. Loveland K.L., Hedger M.P., Risbridger G., Herszfeld D., De Kretser D.M. Identification of receptor tyrosine kinases in the rat testis. Mol Reprod Dev 1993, 36:440-447.
15. Hogarth C.A., Jans D.A., Loveland K.L. Subcellular distribution of importins correlates with germ cell maturation. Dev Dyn 2007, 236:2311-2320.
16. Baker M.A., Hetherington L., Reeves G., Muller J., Aitken R.J. The rat sperm proteome characterized via IPG strip prefractionation and LC-MS/MS identification. Proteomics 2008, 8:2312-2321.
17. Kersey P.J., Duarte J., Williams A., Karavidopoulou Y., Birney E., Apweiler R. The International Protein Index: an integrated database for proteomics experiments. Proteomics 2004, 4:1985-1988.
18. Miyamoto Y., Hieda M., Harreman M.T., Fukumoto M., Saiwaki T., Hodel A.E., et al. Importin α can migrate into the nucleus in an importin β- and Ran-independent manner. EMBO J 2002, 21:5833-5842.
19. Miyamoto Y., Imamoto N., Sekimoto T., Tachibana T., Seki T., Tada S., et al. Differential modes of nuclear localization signal (NLS) recognition by three distinct classes of NLS receptors. J Biol Chem 1997, 272:26375-26381.
20. Brooks A.J., Johansson M., John A.V., Xu Y., Jans D.A., Vasudevan S.G. The interdomain region of dengue NS5 protein that binds to the viral helicase NS3 contains independently functional importin β1 and importin α/β-recognized nuclear localization signals. J Biol Chem 2002, 277:36399-36407.
21. Mi H., Lazareva-Ulitsky B., Loo R., Kejariwal A., Vandergriff J., Rabkin S., et al. The PANTHER database of protein families, subfamilies, functions and pathways. Nucleic Acids Res 2005, 33:D284-D288.
22. Kosugi S., Hasebe M., Tomita M., Yanagawa H. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci U S A 2009, 106:10171-10176.
23. Chen C.F., Li S., Chen Y., Chen P.L., Sharp Z.D., Lee W.H. The nuclear localization sequences of the BRCA1 protein interact with the importin-α subunit of the nuclear transport signal receptor. J Biol Chem 1996, 271:32863-32868.
24. Yeung P.L., Chen L.Y., Tsai S.C., Zhang A., Chen J.D. Daxx contains two nuclear localization signals and interacts with importin α3. J Cell Biochem 2008, 103:456-470.
25. Vaisberg E.A., Grissom P.M., McIntosh J.R. Mammalian cells express three distinct dynein heavy chains that are localized to different cytoplasmic organelles. J Cell Biol 1996, 133:831-842.
26. Asada M., Irie K., Morimoto K., Yamada A., Ikeda W., Takeuchi M., et al. ADIP, a novel Afadin- and α-actinin-binding protein localized at cell-cell adherens junctions. J Biol Chem 2003, 278:4103-4111.
27. Lorenzo O., Urbe S., Clague M.J. Systematic analysis of myotubularins: heteromeric interactions, subcellular localisation and endosome related functions. J Cell Sci 2006, 119:2953-2959.
28. Tonks N.K. Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 2006, 7:833-846.
29. Sperandio S., Poksay K.S., Schilling B., Crippen D., Gibson B.W., Bredesen D.E. Identification of new modulators and protein alterations in non-apoptotic programmed cell death. J Cell Biochem 2010, 111:1401-1412.
30. Asada M., Irie K., Yamada A., Takai Y. Afadin- and α-actinin-binding protein ADIP directly binds β'-COP, a subunit of the coatomer complex. Biochem Biophys Res Commun 2004, 321:350-354.
31. de Bruijn D.R., dos Santos N.R., Kater-Baats E., Thijssen J., van den Berk L., Stap J., et al. The cancer-related protein SSX2 interacts with the human homologue of a Ras-like GTPase interactor, RAB3IP, and a novel nuclear protein, SSX2IP. Genes Chromosomes Cancer 2002, 34:285-298.
32. Taylor E.M., Moghraby J.S., Lees J.H., Smit B., Moens P.B., Lehmann A.R. Characterization of a novel human SMC heterodimer homologous to the Schizosaccharomyces pombe Rad18/Spr18 complex. Mol Biol Cell 2001, 12:1583-1594.
33. De Piccoli G., Torres-Rosell J., Aragon L. The unnamed complex: what do we know about Smc5-Smc6?. Chromosome Res 2009, 17:251-263.
34. Lehmann A.R., Walicka M., Griffiths D.J., Murray J.M., Watts F.Z., McCready S., et al. The rad18 gene of Schizosaccharomyces pombe defines a new subgroup of the SMC superfamily involved in DNA repair. Mol Cell Biol 1995, 15:7067-7080.
35. Forwood J.K., Jans D.A. Nuclear import pathway of the telomere elongation suppressor TRF1: inhibition by importin α. Biochemistry 2002, 41:9333-9340.
36. Catimel B., Teh T., Fontes M.R., Jennings I.G., Jans D.A., Howlett G.J., et al. Biophysical characterization of interactions involving importin-α during nuclear import. J Biol Chem 2001, 276:34189-34198.
37. Blazek E., Meisterernst M. A functional proteomics approach for the detection of nuclear proteins based on derepressed importin alpha. Proteomics 2006, 6:2070-2078.
38. Fukumoto M., Sekimoto T., Yoneda Y. Proteomic Analysis of Importin α-interacting Proteins in Adult Mouse Brain. Cell Struct Funct 2011, 36:57-67.
39. Urrutia R. KRAB-containing zinc-finger repressor proteins. Genome Biol 2003, 4:231.
40. Turner I.A., Norman C.M., Churcher M.J., Newman A.J. Roles of the U5 snRNP in spliceosome dynamics and catalysis. Biochem Soc Trans 2004, 32:928-931.
41. Revenkova E., Eijpe M., Heyting C., Gross B., Jessberger R. Novel meiosis-specific isoform of mammalian SMC1. Mol Cell Biol 2001, 21:6984-6998.
42. Comtesse N., Maldener E., Meese E. Identification of a nuclear variant of MGEA5, a cytoplasmic hyaluronidase and a β-N-acetylglucosaminidase. Biochem Biophys Res Commun 2001, 283:634-640.
43. Patel H., Truant R., Rachubinski R.A., Capone J.P. Activity and subcellular compartmentalization of peroxisome proliferator-activated receptor α are altered by the centrosome-associated protein CAP350. J Cell Sci 2005, 118:175-186.
44. Yang S.N., Takeda A.A., Fontes M.R., Harris J.M., Jans D.A., Kobe B. Probing the specificity of binding to the major nuclear localization sequence-binding site of importin-alpha using oriented peptide library screening. J Biol Chem 2010, 285:19935-19946.
45. Bello O.D., Zanetti M.N., Mayorga L.S., Michaut M.A. RIM, Munc13, and Rab3A interplay in acrosomal exocytosis. Exp Cell Res 2012, 318:478-488.
46. Tran M.H., Aul R.B., Xu W., van der Hoorn F.A., Oko R. Involvement of classical bipartite/karyopherin nuclear import pathway components in acrosomal trafficking and assembly during bovine and murid spermiogenesis. Biol Reprod 2012, 86:84.