The α-importome of mammalian germ cell maturation provides novel insights for importin biology

FASEB Journal

Volumn 28, Issue 8, 2014, Pages 3480-3493

  Arjomand, Arash ^a,b   Baker, Mark A ^b,c   Li, Chen ^a   Buckle, Ashley M ^a   Jans, David A ^a,b   Loveland, Kate L ^a,b   Miyamoto, Yoichi ^a  

^a MONASH UNIVERSITY   (Australia)

^b Australian Government Australian Research Council   (Australia)

^c UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

Mass spectrometry; Nuclear localization signal; Nuclear transport; Spermatogenesis

Indexed keywords

BINDING PROTEIN; IMPORTIN ALPHA2; IMPORTIN ALPHA3; IMPORTIN ALPHA4; IMPORTIN BETA1; KARYOPHERIN; NUCLEAR PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; GERM CELL; HAPLOIDY; INTRACELLULAR SPACE; MAMMAL CELL; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIMARY CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEOMICS; RAT; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; STOICHIOMETRY;

MASS SPECTROMETRY; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR TRANSPORT; SPERMATOGENESIS;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA KARYOPHERINS; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BETA KARYOPHERINS; CARRIER PROTEINS; CELL COMPARTMENTATION; DNA HELICASES; MALE; MEIOSIS; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PACHYTENE STAGE; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; SPERMATIDS; SPERMATOGENESIS; TRANSCRIPTION FACTORS;

EID: 84905234491     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-244913     Document Type: Article

References (43)

1. Pemberton, L. F., and Paschal, B. M. (2005) Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 6, 187-198 (Pubitemid 40298153)
2. Lange, A., Mills, R. E., Lange, C. J., Stewart, M., Devine, S. E., and Corbett, A. H. (2007) Classical nuclear localization signals: definition, function, and interaction with importin α. J. Biol. Chem. 282, 5101-5105 (Pubitemid 47093710)
3. Goldfarb, D. S., Corbett, A. H., Mason, D. A., Harreman, M. T., and Adam, S. A. (2004) Importin α: a multipurpose nucleartransport receptor. Trends Cell Biol. 14, 505-514
4. Conti, E., Uy, M., Leighton, L., Blobel, G., and Kuriyan, J. (1998) Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin α. Cell 94, 193-204 (Pubitemid 28348007)
5. Kobe, B. (1999) Autoinhibition by an internal nuclear localization signal revealed by the crystal structure of mammalian importin α. Nat. Struct. Biol. 6, 388-397
6. Kosugi, S., Hasebe, M., Matsumura, N., Takashima, H., Miyamoto-Sato, E., Tomita, M., and Yanagawa, H. (2009) Six classes of nuclear localization signals specific to different binding grooves of importin α. J. Biol. Chem. 284, 478-485
7. Kutay, U., Bischoff, F. R., Kostka, S., Kraft, R., and Gorlich, D. (1997) Export of importin α from the nucleus is mediated by a specific nuclear transport factor. Cell 90, 1061-1071 (Pubitemid 27408520)
8. Lindsay, M. E., Plafker, K., Smith, A. E., Clurman, B. E., and Macara, I. G. (2002) Npap60/Nup50 is a tri-stable switch that stimulates importin-α: β-mediated nuclear protein import. Cell 110, 349-360
9. Moroianu, J., Blobel, G., and Radu, A. (1997) RanGTP-mediated nuclear export of karyopherin α involves its interaction with the nucleoporin Nup153. Proc. Natl. Acad. Sci. U.S.A. 94, 9699-9704 (Pubitemid 27408126)
10. Ogawa, Y., Miyamoto, Y., Oka, M., and Yoneda, Y. (2012) The interaction between importin-α and Nup153 promotes importin- α/β-mediated nuclear import. Traffic 13, 934-946
11. Yasuhara, N., Yamagishi, R., Arai, Y., Mehmood, R., Kimoto, C., Fujita, T., Touma, K., Kaneko, A., Kamikawa, Y., Moriyama, T., Yanagida, T., Kaneko, H., and Yoneda, Y. (2013) Importin alpha subtypes determine differential transcription factor localization in embryonic stem cells maintenance. Dev. Cell 26, 123-135
12. Miyamoto, Y., Boag, P. R., Hime, G. R., and Loveland, K. L. (2012) Regulated nucleocytoplasmic transport during gametogenesis. Biochim. Biophys. Acta 1819, 616-630
13. Tsuji, L., Takumi, T., Imamoto, N., and Yoneda, Y. (1997) Identification of novel homologues of mouse importin α, the α subunit of the nuclear pore-targeting complex, and their tissuespecific expression. FEBS Lett. 416, 30-34 (Pubitemid 27470795)
14. Nadler, S. G., Tritschler, D., Haffar, O. K., Blake, J., Bruce, A. G., and Cleaveland, J. S. (1997) Differential expression and se-quence- specific interaction of karyopherin α with nuclear localization sequences. J. Biol. Chem. 272, 4310-4315 (Pubitemid 27078503)
15. Hogarth, C. A., Calanni, S., Jans, D. A., and Loveland, K. L. (2006) Importin α mRNAs have distinct expression profiles during spermatogenesis. Dev. Dyn. 235, 253-262 (Pubitemid 46939722)
16. Yasuhara, N., Oka, M., and Yoneda, Y. (2009) The role of the nuclear transport system in cell differentiation. Semin. Cell Dev. Biol. 20, 590-599
17. Major, A. T., Whiley, P. A., and Loveland, K. L. (2011) Expression of nucleocytoplasmic transport machinery: clues to regulation of spermatogenic development. Biochim. Biophys. Acta 1813, 1668-1688
18. Christiansen, A., and Dyrskjot, L. (2013) The functional role of the novel biomarker karyopherin α 2 (KPNA2) in cancer. Cancer Lett. 331, 18-23
19. Jans, D. A., Xiao, C. Y., and Lam, M. H. (2000) Nuclear targeting signal recognition: a key control point in nuclear transport? Bioessays 22, 532-544 (Pubitemid 30387974)
20. Russell, L. D., Ettlin, R. A., Sinha Hikim, A. P., and Clegg, E. D. (1990) Histological and Histopathological Evaluation of the Testis, Cache River Press, Clearwater, FL, USA
21. Miyamoto, Y., Baker, M. A., Whiley, P. A., Arjomand, A., Ludeman, J., Wong, C., Jans, D. A., and Loveland, K. L. (2013) Towards delineation of a developmental α-importome in the mammalian male germline. Biochim. Biophys. Acta 1833, 731-742
22. Whiley, P. A., Miyamoto, Y., McLachlan, R. I., Jans, D. A., and Loveland, K. L. (2012) Changing subcellular localization of nuclear transport factors during human spermatogenesis. Int. J. Androl. 35, 158-169
23. Tran, M. H., Aul, R. B., Xu, W., van der Hoorn, F. A., and Oko, R. (2012) Involvement of classical bipartite/karyopherin nuclear import pathway components in acrosomal trafficking and assembly during bovine and murid spermiogenesis. Biol. Reprod. 86, 84
24. Loveland, K. L., Hedger, M. P., Risbridger, G., Herszfeld, D., and De Kretser, D. M. (1993) Identification of receptor tyrosine kinases in the rat testis. Mol. Reprod. Dev. 36, 440-447 (Pubitemid 23354660)
25. Miyamoto, Y., Hieda, M., Harreman, M. T., Fukumoto, M., Saiwaki, T., Hodel, A. E., Corbett, A. H., and Yoneda, Y. (2002) Importin α can migrate into the nucleus in an importin β- and Ran-independent manner. EMBO J. 21, 5833-5842 (Pubitemid 35315281)
26. Yasuda, Y., Miyamoto, Y., Yamashiro, T., Asally, M., Masui, A., Wong, C., Loveland, K. L., and Yoneda, Y. (2012) Nuclear retention of importin α coordinates cell fate through changes in gene expression. EMBO J. 31, 83-94
27. Miyamoto, Y., Imamoto, N., Sekimoto, T., Tachibana, T., Seki, T., Tada, S., Enomoto, T., and Yoneda, Y. (1997) Differential modes of nuclear localization signal (NLS) recognition by three distinct classes of NLS receptors. J. Biol. Chem. 272, 26375-26381 (Pubitemid 27458853)
28. Hofmann, M. C., Narisawa, S., Hess, R. A., and Millan, J. L. (1992) Immortalization of germ cells and somatic testicular cells using the SV40 large T antigen. Exp. Cell Res. 201, 417-435
29. Lo, J. C., Jamsai, D., O'Connor, A. E., Borg, C., Clark, B. J., Whisstock, J. C., Field, M. C., Adams, V., Ishikawa, T., Aitken, R. J., Whittle, B., Goodnow, C. C., Ormandy, C. J., and O'Bryan, M. K. (2012) RAB-like 2 has an essential role in male fertility, sperm intra-flagellar transport, and tail assembly. PLoS Gen. 8, e1002969
30. Baker, M. A., Lane, D. J., Ly, J. D., De Pinto, V., and Lawen, A. (2004) VDAC1 is a transplasma membrane NADH-ferricyanide reductase. J. Biol. Chem. 279, 4811-4819 (Pubitemid 38199076)
31. Baker, M. A., Naumovski, N., Hetherington, L., Weinberg, A., Velkov, T., and Aitken, R. J. (2013) Head and flagella subcompartmental proteomic analysis of human spermatozoa. Proteomics 13, 61-74
32. Zhang, B., Kirov, S., and Snoddy, J. (2005) WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res. 33, W741-748 (Pubitemid 44530021)
33. Nakai, K., and Horton, P. (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 24, 34-36
34. Kosugi, S., Hasebe, M., Tomita, M., and Yanagawa, H. (2009) Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl. Acad. Sci. U.S.A. 106, 10171-10176
35. Ogawa, Y., Miyamoto, Y., Asally, M., Oka, M., Yasuda, Y., and Yoneda, Y. (2010) Two isoforms of npap60 (nup50) differentially regulate nuclear protein import. Mol. Biol. Cell 21, 9
36. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (Pubitemid 350162903)
37. Hachet, V., Kocher, T., Wilm, M., and Mattaj, I. W. (2004) Importin α associates with membranes and participates in nuclear envelope assembly in vitro. EMBO J. 23, 1526-1535 (Pubitemid 38579513)
38. Gruss, O. J., Carazo-Salas, R. E., Schatz, C. A., Guarguaglini, G., Kast, J., Wilm, M., Le Bot, N., Vernos, I., Karsenti, E., and Mattaj, I. W. (2001) Ran induces spindle assembly by reversing the inhibitory effect of importin α on TPX2 activity. Cell 104, 83-93 (Pubitemid 32144974)
39. Kotera, I., Sekimoto, T., Miyamoto, Y., Saiwaki, T., Nagoshi, E., Sakagami, H., Kondo, H., and Yoneda, Y. (2005) Importin α transports CaMKIV to the nucleus without utilizing importin β. EMBO J. 24, 942-951 (Pubitemid 40470143)
40. Ribbeck, K., Lipowsky, G., Kent, H. M., Stewart, M., and Gorlich, D. (1998) NTF2 mediates nuclear import of Ran. EMBO J. 17, 6587-6598 (Pubitemid 28521793)
41. Riddick, G., and Macara, I. G. (2005) A systems analysis of importin-α-β mediated nuclear protein import. J. Cell Biol. 168, 1027-1038
42. Wang, J., Gu, H., Lin, H., and Chi, T. (2012) Essential roles of the chromatin remodeling factor BRG1 in spermatogenesis in mice. Biol. Reprod. 86, 186
43. Becherel, O. J., Yeo, A. J., Stellati, A., Heng, E. Y., Luff, J., Suraweera, A. M., Woods, R., Fleming, J., Carrie, D., McKinney, K., Xu, X., Deng, C., and Lavin, M. F. (2013) Senataxin plays an essential role with DNA damage response proteins in meiotic recombination and gene silencing. PLoS Genet. 9, e1003435