Post-transcriptional Wnt Signaling Governs Epididymal Sperm Maturation

Cell

Volumn 163, Issue 5, 2015, Pages 1225-1236

  Koch, Stefan ^a   Acebron, Sergio P ^a   Herbst, Jessica ^a   Hatiboglu, Gencay ^b   Niehrs, Christof ^a,c  

^a GERMAN CANCER RESEARCH CENTER   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c INSTITUTE OF MOLECULAR BIOLOGY IMB   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN PHOSPHATASE 1; SEPTIN; SEPTIN 4; UNCLASSIFIED DRUG; WNT PROTEIN; AXIN; AXIN1 PROTEIN, MOUSE; CCNYL1 PROTEIN, MOUSE; CYCLINE; GLYCOGEN SYNTHASE KINASE 3; SEPT4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIFFUSION; ENZYME INHIBITION; EPIDIDYMIS; MALE; MALE STERILITY; MOUSE; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; PROTEIN PHOSPHORYLATION; SOMATIC CELL; SPERMATOZOON MATURATION; SPERMATOZOON MOTILITY; SPERMATOZOON TAIL; UBIQUITINATION; WNT SIGNALING PATHWAY; ANIMAL; GENE EXPRESSION REGULATION; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; RNA PROCESSING;

ANIMALS; AXIN PROTEIN; CYCLINS; EPIDIDYMIS; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; MALE; MICE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA PROCESSING, POST-TRANSCRIPTIONAL; SEPTINS; SPERM MATURATION; WNT SIGNALING PATHWAY;

EID: 84947756267     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.10.029     Document Type: Article

References (59)

1. S.P. Acebron, E. Karaulanov, B.S. Berger, Y.L. Huang, and C. Niehrs Mitotic wnt signaling promotes protein stabilization and regulates cell size Mol. Cell 54 2014 663 674
2. J.N. Anastas, and R.T. Moon WNT signalling pathways as therapeutic targets in cancer Nat. Rev. Cancer 13 2013 11 26
3. A. Boyer, J.R. Yeh, X. Zhang, M. Paquet, A. Gaudin, M.C. Nagano, and D. Boerboom CTNNB1 signaling in sertoli cells downregulates spermatogonial stem cell activity via WNT4 PLoS ONE 7 2012 e29764
4. R.E. Braun Post-transcriptional control of gene expression during spermatogenesis Semin. Cell Dev. Biol. 9 1998 483 489
5. H. Clevers, and R. Nusse Wnt/β-catenin signaling and disease Cell 149 2012 1192 1205
6. P. Cohen The structure and regulation of protein phosphatases Annu. Rev. Biochem. 58 1989 453 508
7. D.S. Das, N. Wadhwa, N. Kunj, K. Sarda, B.S. Pradhan, and S.S. Majumdar Dickkopf homolog 3 (DKK3) plays a crucial role upstream of WNT/β-CATENIN signaling for Sertoli cell mediated regulation of spermatogenesis PLoS ONE 8 2013 e63603
8. G. Davidson, W. Wu, J. Shen, J. Bilic, U. Fenger, P. Stannek, A. Glinka, and C. Niehrs Casein kinase 1 gamma couples Wnt receptor activation to cytoplasmic signal transduction Nature 438 2005 867 872
9. G. Davidson, J. Shen, Y.L. Huang, Y. Su, E. Karaulanov, K. Bartscherer, C. Hassler, P. Stannek, M. Boutros, and C. Niehrs Cell cycle control of wnt receptor activation Dev. Cell 17 2009 788 799
10. Y. Fuchs, S. Brown, T. Gorenc, J. Rodriguez, E. Fuchs, and H. Steller Sept4/ARTS regulates stem cell apoptosis and skin regeneration Science 341 2013 286 289
11. J.C. Gross, V. Chaudhary, K. Bartscherer, and M. Boutros Active Wnt proteins are secreted on exosomes Nat. Cell Biol. 14 2012 1036 1045
12. M.V. Hadjihannas, D.B. Bernkopf, M. Brückner, and J. Behrens Cell cycle control of Wnt/β-catenin signalling by conductin/axin2 through CDC20 EMBO Rep. 13 2012 347 354
13. J.D. Holland, A. Klaus, A.N. Garratt, and W. Birchmeier Wnt signaling in stem and cancer stem cells Curr. Opin. Cell Biol. 25 2013 254 264
14. S.M. Huang, Y.M. Mishina, S. Liu, A. Cheung, F. Stegmeier, G.A. Michaud, O. Charlat, E. Wiellette, Y. Zhang, S. Wiessner, and et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling Nature 461 2009 614 620
15. Y.L. Huang, Z. Anvarian, G. Döderlein, S.P. Acebron, and C. Niehrs Maternal Wnt/STOP signaling promotes cell division during early Xenopus embryogenesis Proc. Natl. Acad. Sci. USA 112 2015 5732 5737
16. K. Inoki, H. Ouyang, T. Zhu, C. Lindvall, Y. Wang, X. Zhang, Q. Yang, C. Bennett, Y. Harada, K. Stankunas, and et al. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth Cell 126 2006 955 968
17. A. Kikuchi, H. Yamamoto, A. Sato, and S. Matsumoto New insights into the mechanism of Wnt signaling pathway activation Int. Rev. Cell Mol. Biol. 291 2011 21 71
18. N.G. Kim, C. Xu, and B.M. Gumbiner Identification of targets of the Wnt pathway destruction complex in addition to beta-catenin Proc. Natl. Acad. Sci. USA 106 2009 5165 5170
19. S.E. Kim, H. Huang, M. Zhao, X. Zhang, A. Zhang, M.V. Semonov, B.T. MacDonald, X. Zhang, J. Garcia Abreu, L. Peng, and X. He Wnt stabilization of β-catenin reveals principles for morphogen receptor-scaffold assemblies Science 340 2013 867 870
20. H. Kim, P. Vick, J. Hedtke, D. Ploper, and E.M. De Robertis Wnt Signaling Translocates Lys48-Linked Polyubiquitinated Proteins to the Lysosomal Pathway Cell Rep. 11 2015 1151 1159
21. H. Kissel, M.M. Georgescu, S. Larisch, K. Manova, G.R. Hunnicutt, and H. Steller The Sept4 septin locus is required for sperm terminal differentiation in mice Dev. Cell 8 2005 353 364
22. S. Kwitny, A.V. Klaus, and G.R. Hunnicutt The annulus of the mouse sperm tail is required to establish a membrane diffusion barrier that is engaged during the late steps of spermiogenesis Biol. Reprod. 82 2010 669 678
23. Q. Li, T.O. Ishikawa, H. Miyoshi, M. Oshima, and M.M. Taketo A targeted mutation of Nkd1 impairs mouse spermatogenesis J. Biol. Chem. 280 2005 2831 2839
24. V. Luga, L. Zhang, A.M. Viloria-Petit, A.A. Ogunjimi, M.R. Inanlou, E. Chiu, M. Buchanan, A.N. Hosein, M. Basik, and J.L. Wrana Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration Cell 151 2012 1542 1556
25. W. Luo, A. Peterson, B.A. Garcia, G. Coombs, B. Kofahl, R. Heinrich, J. Shabanowitz, D.F. Hunt, H.J. Yost, and D.M. Virshup Protein phosphatase 1 regulates assembly and function of the beta-catenin degradation complex EMBO J. 26 2007 1511 1521
26. B.T. MacDonald, K. Tamai, and X. He Wnt/beta-catenin signaling: components, mechanisms, and diseases Dev. Cell 17 2009 9 26
27. S. Maretto, M. Cordenonsi, S. Dupont, P. Braghetta, V. Broccoli, A.B. Hassan, D. Volpin, G.M. Bressan, and S. Piccolo Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors Proc. Natl. Acad. Sci. USA 100 2003 3299 3304
28. T. Matsuda, M. Ihara, H. Inoguchi, I.K. Kwon, K. Takamizawa, and S. Kidoaki Mechano-active scaffold design of small-diameter artificial graft made of electrospun segmented polyurethane fabrics J. Biomed. Mater. Res. A 73 2005 125 131
29. A.P. McMahon, and A. Bradley The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain Cell 62 1990 1073 1085
30. C. Metcalfe, and M. Bienz Inhibition of GSK3 by Wnt signalling - two contrasting models J. Cell Sci. 124 2011 3537 3544
31. P. Mikolcevic, R. Sigl, V. Rauch, M.W. Hess, K. Pfaller, M. Barisic, L.J. Pelliniemi, M. Boesl, and S. Geley Cyclin-dependent kinase 16/PCTAIRE kinase 1 is activated by cyclin Y and is essential for spermatogenesis Mol. Cell. Biol. 32 2012 868 879
32. A.R. Moser, H.C. Pitot, and W.F. Dove A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse Science 247 1990 322 324
33. D. Olmeda, S. Castel, S. Vilaró, and A. Cano Beta-catenin regulation during the cell cycle: implications in G2/M and apoptosis Mol. Biol. Cell 14 2003 2844 2860
34. A.E. Platts, D.J. Dix, H.E. Chemes, K.E. Thompson, R. Goodrich, J.C. Rockett, V.Y. Rawe, S. Quintana, M.P. Diamond, L.F. Strader, and S.A. Krawetz Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs Hum. Mol. Genet. 16 2007 763 773
35. D. Ploper, V.F. Taelman, L. Robert, B.S. Perez, B. Titz, H.W. Chen, T.G. Graeber, E. von Euw, A. Ribas, and E.M. De Robertis MITF drives endolysosomal biogenesis and potentiates Wnt signaling in melanoma cells Proc. Natl. Acad. Sci. USA 112 2015 E420 E429
36. B. Rivas, Z. Huang, and A.I. Agoulnik Normal fertility in male mice with deletion of β-catenin gene in germ cells Genesis 52 2014 328 332
37. P.C. Salinas Modulation of the microtubule cytoskeleton: a role for a divergent canonical Wnt pathway Trends Cell Biol. 17 2007 333 342
38. S. Sharma, A. Quintana, G.M. Findlay, M. Mettlen, B. Baust, M. Jain, R. Nilsson, A. Rao, and P.G. Hogan An siRNA screen for NFAT activation identifies septins as coordinators of store-operated Ca2+ entry Nature 499 2013 238 242
39. P. Sipilä, J. Jalkanen, I.T. Huhtaniemi, and M. Poutanen Novel epididymal proteins as targets for the development of post-testicular male contraception Reproduction 137 2009 379 389
40. J.H. Sitz, K. Baumgärtel, B. Hämmerle, C. Papadopoulos, P. Hekerman, F.J. Tejedor, W. Becker, and B. Lutz The Down syndrome candidate dual-specificity tyrosine phosphorylation-regulated kinase 1A phosphorylates the neurodegeneration-related septin 4 Neuroscience 157 2008 596 605
41. P.R. Somanath, S.L. Jack, and S. Vijayaraghavan Changes in sperm glycogen synthase kinase-3 serine phosphorylation and activity accompany motility initiation and stimulation J. Androl. 25 2004 605 617
42. A. Stolz, K. Neufeld, N. Ertych, and H. Bastians Wnt-mediated protein stabilization ensures proper mitotic microtubule assembly and chromosome segregation EMBO Rep. 16 2015 490 499
43. R. Sullivan, G. Frenette, and J. Girouard Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit Asian J. Androl. 9 2007 483 491
44. V.F. Taelman, R. Dobrowolski, J.L. Plouhinec, L.C. Fuentealba, P.P. Vorwald, I. Gumper, D.D. Sabatini, and E.M. De Robertis Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes Cell 143 2010 1136 1148
45. A. Touré, P. Lhuillier, J.A. Gossen, C.W. Kuil, D. Lhôte, B. Jégou, D. Escalier, and G. Gacon The testis anion transporter 1 (Slc26a8) is required for sperm terminal differentiation and male fertility in the mouse Hum. Mol. Genet. 16 2007 1783 1793
46. T. Tsukiyama, and T.P. Yamaguchi Mice lacking Wnt2b are viable and display a postnatal olfactory bulb phenotype Neurosci. Lett. 512 2012 48 52
47. T.T. Turner De Graaf's thread: the human epididymis J. Androl. 29 2008 237 250
48. T. Valenta, M. Gay, S. Steiner, K. Draganova, M. Zemke, R. Hoffmans, P. Cinelli, M. Aguet, L. Sommer, and K. Basler Probing transcription-specific outputs of β-catenin in vivo Genes Dev. 25 2011 2631 2643
49. S. Vijayaraghavan, D.T. Stephens, K. Trautman, G.D. Smith, B. Khatra, E.F. da Cruz e Silva, and P. Greengard Sperm motility development in the epididymis is associated with decreased glycogen synthase kinase-3 and protein phosphatase 1 activity Biol. Reprod. 54 1996 709 718
50. E. Vincan, and N. Barker The upstream components of the Wnt signalling pathway in the dynamic EMT and MET associated with colorectal cancer progression Clin. Exp. Metastasis 25 2008 657 663
51. M. Vinyoles, B. Del Valle-Pérez, J. Curto, R. Viñas-Castells, L. Alba-Castellón, A. García de Herreros, and M. Duñach Multivesicular GSK3 sequestration upon Wnt signaling is controlled by p120-catenin/cadherin interaction with LRP5/6 Mol. Cell 53 2014 444 457
52. K. Wang, N. Li, C.H. Yeung, J.Y. Li, H.Y. Wang, and T.G. Cooper Oncogenic Wnt/β-catenin signalling pathways in the cancer-resistant epididymis have implications for cancer research Mol. Hum. Reprod. 19 2013 57 71
53. D. Wu, and W. Pan GSK3: a multifaceted kinase in Wnt signaling Trends Biochem. Sci. 35 2010 161 168
54. X. Wu, X. Tu, K.S. Joeng, M.J. Hilton, D.A. Williams, and F. Long Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling Cell 133 2008 340 353
55. S. Xie, J. Xu, W. Ma, Q. Liu, J. Han, G. Yao, X. Huang, and Y. Zhang Lcn5 promoter directs the region-specific expression of cre recombinase in caput epididymidis of transgenic mice Biol. Reprod. 88 2013 71
56. C. Xu, N.G. Kim, and B.M. Gumbiner Regulation of protein stability by GSK3 mediated phosphorylation Cell Cycle 8 2009 4032 4039
57. J. Yang, S.K. Wang, M. Choi, B.M. Reid, Y. Hu, Y.L. Lee, C.R. Herzog, H. Kim-Berman, M. Lee, P.J. Benke, and et al. Taurodontism, variations in tooth number, and misshapened crowns in Wnt10a null mice and human kindreds Mol. Genet. Genomic Med. 3 2015 40 58
58. C.-H. Yeung, and T. Cooper Acquisition and development of sperm motility upon maturation in the epididymis B. Robaire, B. Hinton, The Epididymis: From Molecules to Clinical Practice 2002 Springer 417 434
59. Z. Zi, Z. Zhang, Q. Li, W. An, L. Zeng, D. Gao, Y. Yang, X. Zhu, R. Zeng, W.W. Shum, and et al. CCNYL1, but not CCNY, cooperates with CDK16 to regulate spermatogenesis in mouse PLoS Genet. 11 2015 e1005485