A testis specific isoform of endophilin B1, endophilin B1t, interacts specifically with protein phosphatase-1cγ2 in mouse testis and is abnormally expressed in PP1cγ Null Mice

Biochemistry

Volumn 46, Issue 15, 2007, Pages 4635-4644

  Hrabchak, Christopher ^a   Henderson, Hannah ^a   Varmuza, Susannah ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOPHILIN B1; MAMMALIAN SPERMATOGENESIS; TESTIS ISOFORM;

AMINO ACIDS; BIOASSAY; GENES; IMMUNOLOGY; PROTEINS;

LIVING SYSTEMS STUDIES;

ENDOPHILIN; ENDOPHILIN B1; ENDOPHILIN B1T; PHOSPHOPROTEIN PHOSPHATASE 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE MUTATION; HOMOZYGOSITY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; KNOCKOUT GENE; MALE; MALE INFERTILITY; MOUSE; MOUSE MUTANT; NONHUMAN; NULL ALLELE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPERMATOGENESIS; TESTIS; TWO HYBRID SYSTEM; WILD TYPE;

ACYLTRANSFERASES; AMINO ACID SEQUENCE; ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CERCOPITHECUS AETHIOPS; COS CELLS; FEMALE; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN ISOFORMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TESTIS; TWO-HYBRID SYSTEM TECHNIQUES;

MAMMALIA; MUS;

EID: 34247264873     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi6025837     Document Type: Article

References (46)

1. Cohen, P. T. (2002) Protein Phosphatase 1-Targeted in Many Directions, J. Cell. Sci. 115, 241-256.
2. Bollen, M. (2001) Combinatorial Control of Protein Phosphatase-1, Trends Biochem. Sci. 26, 426-431.
3. Varmuza, S., Jurisicova, A., Okano, K., Hudson, J., Boekelheide, K., and Shipp, E. B. (1999) Spermiogenesis is Impaired in Mice Bearing a Targeted Mutation in the Protein Phosphatase 1cgamma Gene, Dev. Biol. 205, 98-110.
4. Axton, J. M., Dombradi, V., Cohen, P. T., and Glover, D. M. (1990) One of the Protein Phosphatase 1 Isoenzymes in Drosophila is Essential for Mitosis, Cell 63, 33-46.
5. Cheng, A., Dean, N. M., and Honkanen, R. E. (2000) Serine/ threonine Protein Phosphatase Type 1gamma1 is Required for the Completion of Cytokinesis in Human A549 Lung Carcinoma Cells, J. Biol. Chem. 275, 1846-1854.
6. Raghavan, S., Williams, I., Aslam, H., Thomas, D., Szoor, B., Morgan, G., Gross, S., Turner, J., Fernandes, J., VijayRaghavan, K., and Alphey, L. (2000) Protein Phosphatase 1beta is Required for the Maintenance of Muscle Attachments, Curr. Biol. 10, 269-272.
7. Ceulemans, H., and Bollen, M. (2004) Functional Diversity of Protein Phosphatase-1, a Cellular Economizer and Reset Button, Physiol. Rev. 84, 1-39.
8. Wakula, P., Beullens, M., Ceulemans, H., Stalmans, W., and Bollen, M. (2003) Degeneracy and Function of the Ubiquitous RVXF Motif that Mediates Binding to Protein Phosphatase-1, J. Biol. Chem. 278, 18817-18823.
9. Zhao, S., and Lee, E. Y. (1997) A Protein Phosphatase-1-Binding Motif Identified by the Panning of a Random Peptide Display Library, J. Biol. Chem. 272, 28368-28372.
10. Aggen, J. B., Nairn, A. C., and Chamberlin, R. (2000) Regulation of Protein Phosphatase-1, Chem. Biol. 7, R13-23.
11. Terry-Lorenzo, R. T., Carmody, L. C., Voltz, J. W., Connor, J. H., Li, S., Smith, F. D., Milgram, S. L., Colbran, R. J., and Shenolikar, S. (2002) The Neuronal Actin-Binding Proteins, Neurabin I and Neurabin II, Recruit Specific Isoforms of Protein Phosphatase-1 Catalytic Subunits, J. Biol. Chem. 277, 27716-27724.
12. Colbran, R. J., Bass, M. A., McNeill, R. B., Bollen, M., Zhao, S., Wadzinski, B. E., and Strack, S. (1997) Association of Brain Protein Phosphatase 1 with Cytoskeletal targeting/regulatory Subunits, J. Neurochem. 69, 920-929.
13. Shima, H., Hatano, Y., Chun, Y. S., Sugimura, T., Zhang, Z., Lee, E. Y., and Nagao, M. (1993) Identification of PP1 Catalytic Subunit Isotypes PP1 Gamma 1, PP1 Delta and PP1 Alpha in various Rat Tissues, Biochem. Biophys. Res. Commun. 192, 1289-1296.
14. Okano, K., Heng, H., Trevisanato, S., Tyers, M., and Varmuza, S. (1997) Genomic Organization and Functional Analysis of the Murine Protein Phosphatase 1c Gamma (Ppp1cc) Gene, Genomics 45, 211-215.
15. Jurisicova, A., Lopes, S., Meriano, J., Oppedisano, L., Casper, R. F., and Varmuza, S. (1999) DNA Damage in Round Spermatids of Mice with a Targeted Disruption of the Pp1cgamma Gene and in Testicular Biopsies of Patients with Non-Obstructive Azoospermia, Mol. Hum. Reprod. 5, 323-330.
16. Oppedisano, L., Haines, G., Hrabchak, C., Fimia, G., Elliott, R., Sassone-Corsi, P., and Varmuza, S. (2002) The Rate of Aneuploidy is Altered in Spermatids from Infertile Mice, Hum. Reprod. 17, 710-717.
17. Griswold, M. D. (1995) Interactions between Germ Cells and Sertoli Cells in the Testis, Biol. Reprod. 52, 211-216.
18. Shima, H., Haneji, T., Hatano, Y., Kasugai, I., Sugimura, T., and Nagao, M. (1993) Protein Phosphatase 1 Gamma 2 is Associated with Nuclei of Meiotic Cells in Rat Testis, Biochem. Biophys. Res. Commun. 194, 930-937.
19. Enz, R. (2002) The Metabotropic Glutamate Receptor mGluR7b Binds to the Catalytic Gamma-Subunit of Protein Phosphatase 1, J. Neurochem. 81, 1130-1140.
20. Chun, Y. S., Shima, H., Nagasaki, K., Sugimura, T., and Nagao, M. (1994) PP1 Gamma 2, a Testis-Specific Protein-serine/ threonine-Phosphatase Type 1 Catalytic Subunit, is Associated with a Protein having High Sequence Homology with the 78-kDa Glucose-Regulated Protein, a Member of the 70-kDa Heat Shock Protein Family, Proc. Natl. Acad. Sci. U. S. A. 91, 3319-3323.
21. Chun, Y. S., Park, J. W., Kim, G. T., Shima, H., Nagao, M., Kim, M. S., and Chung, M. H. (2000) A sds22 Homolog that is Associated with the Testis-Specific serine/threonine Protein Phosphatase 1gamma2 in Rat Testis, Biochem. Biophys. Res. Commun. 273, 972-976.
22. Hrabchak, C., and Varmuza, S. (2004) Identification of the Spermatogenic Zip Protein Spz1 as a Putative Protein Phosphatase-1 (PP1) Regulatory Protein that Specifically Binds the PP1cgamma2 Splice Variant in Mouse Testis, J. Biol. Chem. 279, 37079-37086.
23. Mann, M., Latham, K. E., and Varmuza, S. (1995) Identification of Genes Showing Altered Expression in Preimplantation and Early Postimplantation Parthenogenetic Embryos, Dev. Genet. 17, 223-232.
24. Elledge, S. J., Mulligan, J. T., Ramer, S. W., Spottswood, M., and Davis, R. W. (1991) Lambda YES: A Multifunctional cDNA Expression Vector for the Isolation of Genes by Complementation of Yeast and Escherichia Coli Mutations, Proc. Natl. Acad. Sci. U. S. A. 88, 1731-1735.
25. Nickoloff, J. A. (1995) Electroporation Protocols for Microorganisms, Humana Press, Totowa, NJ.
26. Sharma, R. C., and Schimke, R. T. (1996) Preparation of Electrocompetent E. Coli using Salt-Free Growth Medium, BioTechniques 20, 42-44.
27. Harlow, E., and Lane, D. (1988) Antibodies: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
28. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
29. Gluzman, Y. (1981) SV40-Transformed Simian Cells Support the Replication of Early SV40 Mutants, Cell 23, 175-182.
30. Misumi, Y., Oda, K., Fujiwara, T., Takami, N., Tashiro, K., and Ikehara, Y. (1991) Functional Expression of Furin Demonstrating its Intracellular Localization and Endoprotease Activity for Processing of Prealbumin and Complement Pro-C3, J. Biol. Chem. 266, 16954-16959.
31. Ludlow, J. W. (1998) Protein Phosphatase Protocols, Humana Press, Totowa, NJ.
32. Shenolikar, S., and Ingebritsen, T. S. (1984) Protein (Serine and Threonine) Phosphate Phosphatases, Methods Enzymol. 107, 102-129.
33. Iwamura, M., Abrahamsson, P. A., Benning, C. M., Cockett, A. T., and di Sant'Agnese, P. A. (1994) Androgen Receptor Immunostaining and its Tissue Distribution in Formalin-Fixed, Paraffin-Embedded Sections After Microwave Treatment, J. Histochem. Cytochem. 42, 783-788.
34. Modregger, J., Schmidt, A. A., Ritter, B., Huttner, W. B., and Plomann, M. (2003) Characterization of Endophilin B1b, a Brain-Specific Membrane-Associated Lysophosphatidic Acid Acyl Transferase with Properties Distinct from Endophilin A1, J. Biol. Chem. 278, 4160-4167.
35. Monshausen, M., Rehbein, M., Richter, D., and Kindler, S. (2002) The RNA-Binding Protein Staufen from Rat Brain Interacts with Protein Phosphatase-1, J. Neurochem. 81, 557-564.
36. Cuddeback, S. M., Yamaguchi, H., Komatsu, K., Miyashita, T., Yamada, M., Wu, C., Singh, S., and Wang, H. G. (2001) Molecular Cloning and Characterization of Bif-1. A Novel Src Homology 3 Domain-Containing Protein that Associates with Bax, J. Biol. Chem. 276, 20559-20565.
37. Liu, J., Wu, J., Oliver, C., Shenolikar, S., and Brautigan, D. L. (2000) Mutations of the Serine Phosphorylated in the Protein Phosphatase-1-Binding Motif in the Skeletal Muscle Glycogen-Targeting Subunit, Biochem. J. 346 (Part 1), 77-82.
38. Terry-Lorenzo, R. T., Elliot, E., Weiser, D. C., Prickett, T. D., Brautigan, D. L., and Shenolikar, S. (2002) Neurabins Recruit Protein Phosphatase-1 and Inhibitor-2 to the Actin Cytoskeleton, J. Biol. Chem. 277, 46535-46543.
39. Varmuza, S., and Ling, L. (2003) Increased Recombination Frequency Showing Evidence of Loss of Interference is Associated with Abnormal Testicular Histopathology, Mol. Reprod. Dev. 64, 499-506.
40. Oppedisano-Wells, L., and Varmuza, S. (2003) Protein Phosphatase lcgamma is Required in Germ Cells in Murine Testis, Mol. Reprod. Dev. 65, 157-166.
41. Song, W., and Zinsmaier, K. E. (2003) Endophilin and Synaptojanin Hook Up to Promote Synaptic Vesicle Endocytosis, Neuron 40, 665-667.
42. Schuske, K. R., Richmond, J. E., Matthies, D. S., Davis, W. S., Runz, S., Rube, D. A., van der Bliek, A. M., and Jorgensen, E. M. (2003) Endophilin is Required for Synaptic Vesicle Endocytosis by Localizing Synaptojanin, Neuron 40, 749-762.
43. Verstreken, P., Koh, T. W., Schulze, K. L., Zhai, R. G., Hiesinger, P. R., Zhou, Y., Mehta, S. Q., Cao, Y., Roos, J., and Bellen, H. J. (2003) Synaptojanin is Recruited by Endophilin to Promote Synaptic Vesicle Uncoating, Neuron 40, 733-748.
44. Fabian-Fine, R., Verstreken, P., Hiesinger, P. R., Horne, J. A., Kostyleva, R., Zhou, Y., Bellen, H. J., and Meinertzhagen, I. A. (2003) Endophilin Promotes a Late Step in Endocytosis at Glial Invaginations in Drosophila Photoreceptor Terminals, J. Neurosci. 23, 10732-10744.
45. Russell, L., and Clermont, Y. (1976) Anchoring Device between Sertoli Cells and Late Spermatids in Rat Seminiferous Tubules, Anat. Rec. 185, 259-278.
46. Guttman, J. A., Takai, Y., and Vogl, A. W. (2004) Evidence that Tubulobulbar Complexes in the Seminiferous Epithelium are Involved with Internalization of Adhesion Junctions, Biol. Reprod. 71, 548-559.