The ubiquilin gene family: Evolutionary patterns and functional insights

BMC Evolutionary Biology

Volumn 14, Issue 1, 2014, Pages

  Marín, Ignacio ^a  

^a INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

Gene duplication; Neurodegeneration; Spermiogenesis; Ubiquitin receptors; Ubiquitination

Indexed keywords

CARRIER PROTEIN;

ANIMAL; ARTICLE; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETIC SELECTION; GENETICS; HUMAN; MOLECULAR EVOLUTION; PHYLOGENY;

ANIMALS; CARRIER PROTEINS; DATABASES, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; HUMANS; PHYLOGENY; SELECTION, GENETIC;

EID: 84898631587     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-14-63     Document Type: Article

References (92)

1. Genetic interactions between CDC31 and KAR1, two genes required for duplication of the microtubule organizing center in Saccharomyces cerevisiae. Vallen EA, Ho W, Winey M, Rose MD, Genetics 1994 137 407 422 8070654 (Pubitemid 24157003)
2. Yeast ubiquitin-like genes are involved in duplication of the microtubule organizing center. Biggins S, Ivanovska I, Rose MD, J Cell Biol 1996 133 1331 1346 10.1083/jcb.133.6.1331 8682868 (Pubitemid 26192333)
3. Identification of XDRP1; a Xenopus protein related to yeast Dsk2p binds to the N-terminus of cyclin A and inhibits its degradation. Funakoshi M, Geley S, Hunt T, Nishimoto T, Kobayashi H, EMBO J 1999 18 5009 5018 10.1093/emboj/18.18.5009 10487753 (Pubitemid 29443803)
4. Ubiquitin-related proteins regulate interaction of vimentin intermediate filaments with the plasma membrane. Wu AL, Wang J, Zheleznyak A, Brown EJ, Mol Cell 1999 4 619 625 10.1016/S1097-2765(00)80212-9 10549293 (Pubitemid 29531141)
5. A family of ubiquitin-like proteins binds the ATPase domain of Hsp70-like Stch. Kaye FJ, Modi S, Ivanovska I, Koonin EV, Thress K, Kubo A, Kornbluth S, Rose MD, FEBS Lett. 2000 467 348 355 10.1016/S0014-5793(00)01135-2 10675567 (Pubitemid 30081763)
6. Identification of ubiquilin, a novel presenilin interactor that increases presenilin protein accumulation. Mah AL, Perry G, Smith MA, Monteiro MJ, J Cell Biol 2000 151 847 862 10.1083/jcb.151.4.847 11076969
7. The hPLIC proteins may provide a link between the ubiquitination machinery and the proteasome. Kleijnen MF, Shih AH, Zhou P, Kumar S, Soccio RE, Kedersha NL, Gill G, Howley PM, Mol Cell. 2000 6 409 419 10.1016/S1097-2765(00) 00040-X 10983987
8. Molecular cloning, chromosome mapping and characterization of UBQLN3 a testis-specific gene that contains an ubiquitin-like domain. Conklin D, Holderman S, Whitmore TE, Maurer M, Feldhaus AL, Gene 2000 249 91 98 10.1016/S0378-1119(00)00122-0 10831842 (Pubitemid 30265490)
9. Identification and characterization of an ataxin-1-interacting protein: A1Up, a ubiquitin-like nuclear protein. Davidson JD, Riley B, Burright EN, Duvick LA, Zoghbi HY, Orr HT, Hum Mol Genet. 2000 9 2305 2312 10.1093/oxfordjournals.hmg.a018922 11001934
10. Identification of a new cellular protein that can interact specifically with DAN. Ozaki T, Hishiki T, Toyama Y, Yuasa S, Nakagawara A, Sakiyama S, DNA Cell Biol 1997 16 985 991 10.1089/dna.1997.16.985 9303440 (Pubitemid 27387911)
11. Molecular cloning and expression analysis of the human DA41 gene and its mapping to chromosome 9q21.2-q21.3. Hanaoka E, Ozaki T, Ohira M, Nakamura Y, Suzuki M, Takahashi E, Moriya H, Nakagawara A, Sakiyama S, J Hum Genet. 2000 45 188 191 10.1007/s100380050209 10807547 (Pubitemid 30324124)
12. Molecular cloning of a novel ubiquitin-like protein, UBIN, that binds to ER targeting signal sequences. Matsuda M, Koide T, Yorihuzi T, Hosokawa N, Nagata K, Biochem Biophys Res Commun. 2001 280 535 540 10.1006/bbrc.2000.4149 11162551 (Pubitemid 32912824)
13. Identification of type 2 diabetes genes in Mexican Americans through genome-wide association studies. Hayes MG, Pluzhnikov A, Miyake K, Sun Y, Ng MC, Roe CA, Below JE, Nicolae RI, Konkashbaev A, Bell GI, Cox NJ, Hanis CL, Diabetes 2007 56 3033 3044 10.2337/db07-0482 17846124 (Pubitemid 350223640)
14. Budding yeast Dsk2p is a polyubiquitin-binding protein that can interact with the proteasome. Funakoshi M, Sasaki T, Nishimoto T, Kobayashi H, Proc Natl Acad Sci U S A 2002 99 745 750 10.1073/pnas.012585199 11805328 (Pubitemid 34106581)
15. Proteins containing the UBA domain are able to bind to multi-ubiquitin chains. Wilkinson CR, Seeger M, Hartmann-Petersen R, Stone M, Wallace M, Semple C, Gordon C, Nat Cell Biol 2001 3 939 943 10.1038/ncb1001-939 11584278 (Pubitemid 32952261)
16. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Elsasser S, Gali RR, Schwickart M, Larsen CN, Leggett DS, Müller B, Feng MT, Tübing F, Dittmar GA, Finley D, Nat Cell Biol. 2002 4 725 730 10.1038/ncb845 12198498 (Pubitemid 34993711)
17. The UBA2 domain functions as an intrinsic stabilization signal that protects Rad23 from proteasomal degradation. Heessen S, Masucci MG, Dantuma NP, Mol Cell 2005 18 225 235 10.1016/j.molcel.2005.03.015 15837425
18. Ubiquilin recruits Eps15 into ubiquitin-rich cytoplasmic aggregates via a UIM-UBL interaction. Regan-Klapisz E, Sorokina I, Voortman J, de Keizer P, Roovers RC, Verheesen P, Urbé S, Fallon L, Fon EA, Verkleij A, Benmerah A, van Bergen en Henegouwen PM, J Cell Sci 2005 118 4437 4450 10.1242/jcs.02571 16159959 (Pubitemid 41556342)
19. The UBL domain of PLIC-1 regulates aggresome formation. Heir R, Ablasou C, Dumontier E, Elliott M, Fagotto-Kaufmann C, Bedford FK, EMBO Rep. 2006 7 1252 1258 10.1038/sj.embor.7400823 17082820 (Pubitemid 44835094)
20. C-terminal UBA domains protect ubiquitin receptors by preventing initiation of protein degradation. Heinen C, Acs K, Hoogstraten D, Dantuma NP, Nat Commun. 2011 2 191 21304520
21. Ubiquitin receptor proteins hHR23a and hPLIC2 interact. Kang Y, Zhang N, Koepp DM, Walters KJ, J Mol Biol. 2007 365 1093 1101 10.1016/j.jmb.2006.10.056 17098253 (Pubitemid 46014186)
22. When ubiquitin meets ubiquitin receptors: a signalling connection. Di Fiore PP, Polo S, Hofmann K, Nat Rev Mol Cell Biol 2003 4 491 497 10.1038/nrm1124 12778128 (Pubitemid 36648594)
23. Delivery of ubiquitinated substrates to protein-unfolding machines. Elsasser S, Finley D, Nat Cell Biol 2005 7 742 749 10.1038/ncb0805-742 16056265 (Pubitemid 41079042)
24. Ubiquitin-like and ubiquitin-associated domain proteins: significance in proteasomal degradation. Su V, Lau AF, Cell Mol Life Sci 2009 66 2819 2833 10.1007/s00018-009-0048-9 19468686
25. Ubiquilins in the crosstalk among proteolytic pathways. Lee DY, Brown EJ, Biol Chem. 2012 393 441 447 22628307
26. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Husnjak K, Dikic I, Annu Rev Biochem 2012 81 291 322 10.1146/annurev-biochem-051810-094654 22482907
27. Emerging role of Alzheimer's disease-associated ubiquilin-1 in protein aggregation. Haapasalo A, Viswanathan J, Bertram L, Soininen H, Tanzi RE, Hiltunen M, Biochem Soc Trans. 2010 38 150 155 10.1042/BST0380150 20074050
28. Ubiquilin-1 and protein quality control in Alzheimer disease. El Ayadi A, Stieren ES, Barral JM, Boehning D, Prion 2013 7 164 169 10.4161/pri.23711 23360761
29. Overexpression of ubiquilin decreases ubiquitination and degradation of presenilin proteins. Massey LK, Mah AL, Ford DL, Miller J, Liang J, Doong H, Monteiro MJ, J Alzheimers Dis. 2004 6 79 92 15004330 (Pubitemid 38418560)
30. Family-based association between Alzheimer's disease and variants in UBQLN1. Bertram L, Hiltunen M, Parkinson M, Ingelsson M, Lange C, Ramasamy K, Mullin K, Menon R, Sampson AJ, Hsiao MY, Elliott KJ, Velicelebi G, Moscarillo T, Hyman BT, Wagner SL, Becker KD, Blacker D, Tanzi RE, N Engl J Med 2005 352 884 894 10.1056/NEJMoa042765 15745979 (Pubitemid 40300297)
31. Association study of the Ubiquilin gene with Alzheimer's disease. Bensemain F, Chapuis J, Tian J, Shi J, Thaker U, Lendon C, Iwatsubo T, Amouyel P, Mann D, Lambert JC, Neurobiol Dis. 2006 22 691 693 10.1016/j.nbd.2006.01.007 16504527 (Pubitemid 43832139)
32. The UBQLN1 polymorphism, UBQ-8i, at 9q22 is not associated with Alzheimer's disease with onset before 70 years. Brouwers N, Sleegers K, Engelborghs S, Bogaerts V, van Duijn CM, De Deyn PP, Van Broeckhoven C, Dermaut B, Neurosci Lett. 2006 392 72 74 10.1016/j.neulet.2005.08.064 16214290 (Pubitemid 41757578)
33. Genetic association of ubiquilin with Alzheimer's disease and related quantitative measures. Kamboh MI, Minster RL, Feingold E, DeKosky ST, Mol Psychiatry 2006 11 273 279 10.1038/sj.mp.4001775 16302009
34. Lack of association between UBQLN1 and Alzheimer disease. Slifer MA, Martin ER, Bronson PG, Browning-Large C, Doraiswamy PM, Welsh-Bohmer KA, Gilbert JR, Haines JL, Pericak-Vance MA, Am J Med Genet B Neuropsychiatr Genet. 2006 141B 208 213 10.1002/ajmg.b.30298 16526030
35. Ubiquilin 1 polymorphisms are not associated with late-onset Alzheimer's disease. Smemo S, Nowotny P, Hinrichs AL, Kauwe JS, Cherny S, Erickson K, Myers AJ, Kaleem M, Marlowe L, Gibson AM, Hollingworth P, O'Donovan MC, Morris CM, Holmans P, Lovestone S, Morris JC, Thal L, Li Y, Grupe A, Hardy J, Owen MJ, Williams J, Goate A, Ann Neurol. 2006 59 21 26 10.1002/ana.20673 16278862 (Pubitemid 43042867)
36. Relationship of the Ubiquilin 1 gene with Alzheimer's and Parkinson's disease and cognitive function. Arias-Vásquez A, de Lau L, Pardo L, Liu F, Feng BJ, Bertoli-Avella A, Isaacs A, Aulchenko Y, Hofman A, Oostra B, Breteler M, van Duijn C, Neurosci Lett. 2007 424 1 5 10.1016/j.neulet.2007.07. 015 17709205 (Pubitemid 47285490)
37. Analysis of UBQLN1 variants in a Polish Alzheimer's disease patient: control series. Golan MP, Melquist S, Safranow K, Styczyńska M, Słowik A, Kobryś M, Zekanowski C, Barcikowska M, Dement Geriatr Cogn Disord. 2008 25 366 371 10.1159/000121006 18340109 (Pubitemid 351562959)
38. Ubiquilin-1 is a molecular chaperone for the amyloid precursor protein. Stieren ES, El Ayadi A, Xiao Y, Siller E, Landsverk ML, Oberhauser AF, Barral JM, Boehning D, J Biol Chem. 2011 286 35689 35698 10.1074/jbc.M111.243147 21852239
39. Alzheimer's disease-associated ubiquilin-1 regulates presenilin-1 accumulation and aggresome formation. Viswanathan J, Haapasalo A, Böttcher C, Miettinen R, Kurkinen KM, Lu A, Thomas A, Maynard CJ, Romano D, Hyman BT, Berezovska O, Bertram L, Soininen H, Dantuma NP, Tanzi RE, Hiltunen M, Traffic 2011 12 330 348 10.1111/j.1600-0854.2010.01149.x 21143716
40. Ubiquilin-1 regulates amyloid precursor protein maturation and degradation by stimulating K63-linked polyubiquitination of lysine 688. El Ayadi A, Stieren ES, Barral JM, Boehning D, Proc Natl Acad Sci U S A 2012 109 13416 13421 10.1073/pnas.1206786109 22847417
41. Isolation and characterization of the Drosophila ubiquilin ortholog dUbqln: in vivo interaction with early-onset Alzheimer disease genes. Li A, Xie Z, Dong Y, McKay KM, McKee ML, Tanzi RE, Hum Mol Genet. 2007 16 2626 2639 10.1093/hmg/ddm219 17704509 (Pubitemid 47617729)
42. Ubiquilin antagonizes presenilin and promotes neurodegeneration in Drosophila. Ganguly A, Feldman RM, Guo M, Hum Mol Genet 2008 17 293 302 17947293
43. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Deng HX, Chen W, Hong ST, Boycott KM, Gorrie GH, Siddique N, Yang Y, Fecto F, Shi Y, Zhai H, Jiang H, Hirano M, Rampersaud E, Jansen GH, Donkervoort S, Bigio EH, Brooks BR, Ajroud K, Sufit RL, Haines JL, Mugnaini E, Pericak-Vance MA, Siddique T, Nature 2011 477 211 215 10.1038/nature10353 21857683
44. UBQLN2 mutations are rare in French and French-Canadian amyotrophic lateral sclerosis. Daoud H, Suhail H, Szuto A, Camu W, Salachas F, Meininger V, Bouchard JP, Dupré N, Dion PA, Rouleau GA, Neurobiol Aging 2012 33 2230.e1 2230.e5
45. Screening in ALS and FTD patients reveals 3 novel UBQLN2 mutations outside the PXX domain and a pure FTD phenotype. Synofzik M, Maetzler W, Grehl T, Prudlo J, Vom Hagen JM, Haack T, Rebassoo P, Munz M, Schöls L, Biskup S, Neurobiol Aging. 2012 33 2949.e13 2949.e17
46. UBQLN2/ubiquilin 2 mutation and pathology in familial amyotrophic lateral sclerosis. Williams KL, Warraich ST, Yang S, Solski JA, Fernando R, Rouleau GA, Nicholson GA, Blair IP, Neurobiol Aging. 2012 33 2527.e3 2527.e10
47. Potentiation of amyotrophic lateral sclerosis (ALS)-associated TDP-43 aggregation by the proteasome-targeting factor, ubiquilin 1. Kim SH, Shi Y, Hanson KA, Williams LM, Sakasai R, Bowler MJ, Tibbetts RS, J Biol Chem. 2009 284 8083 8092 10.1074/jbc.M808064200 19112176
48. Ubiquilin modifies TDP-43 toxicity in a Drosophila model of amyotrophic lateral sclerosis (ALS). Hanson KA, Kim SH, Wassarman DA, Tibbetts RS, J Biol Chem. 2010 285 11068 11072 10.1074/jbc.C109.078527 20154090
49. Pattern of ubiquilin pathology in ALS and FTLD indicates presence of C9ORF72 hexanucleotide expansion. Brettschneider J, Van Deerlin VM, Robinson JL, Kwong L, Lee EB, Ali YO, Safren N, Monteiro MJ, Toledo JB, Elman L, McCluskey L, Irwin DJ, Grossman M, Molina-Porcel L, Lee VM, Trojanowski JQ, Acta Neuropathol. 2012 123 825 839 10.1007/s00401-012-0970-z 22426854
50. The effects of the polyglutamine repeat protein ataxin-1 on the UbL-UBA protein A1Up. Riley BE, Xu Y, Zoghbi HY, Orr HT, J Biol Chem 2004 279 42290 42301 10.1074/jbc.M406284200 15280365 (Pubitemid 39313678)
51. Suppression of polyglutamine-induced toxicity in cell and animal models of Huntington's disease by ubiquilin. Wang H, Lim PJ, Yin C, Rieckher M, Vogel BE, Monteiro MJ, Hum Mol Genet 2006 15 1025 1041 10.1093/hmg/ddl017 16461334 (Pubitemid 43338242)
52. Identification of ubiquitin-interacting proteins in purified polyglutamine aggregates. Doi H, Mitsui K, Kurosawa M, Machida Y, Kuroiwa Y, Nukina N, FEBS Letters 2004 571 171 176 10.1016/j.febslet.2004.06.077 15280037 (Pubitemid 38992943)
53. Ubiquilin immunoreactivity in cytoplasmic and nuclear inclusions in synucleinopathies, polyglutamine diseases and intranuclear inclusión body disease. Mori F, Tanji K, Odagiri S, Toyoshima Y, Yoshida M, Ikeda T, Sasaki H, Kakita A, Takahashi H, Wakabayashi K, Acta Neuropathol. 2012 124 149 151 10.1007/s00401-012-0999-z 22661321
54. Unbiased screen reveals ubiquilin-a and -2 highly associated with huntingtin inclusions. Rutherford NJ, Lewis J, Clippinger AK, Thomas MA, Adamson J, Cruz PE, Cannon A, Xu G, Golde TE, Shaw G, Borchelt DR, Giasson BI, Brain Res. 2013 1524 62 73 23774650
55. Association of UBQLN1 mutation with Brown-Vialetto-Van Laere syndrome but not typical ALS. González-Pérez P, Lu Y, Chian RJ, Sapp PC, Tanzi RE, Bertram L, McKenna-Yasek D, Gao FB, Brown RH Jr, Neurobiol Dis. 2012 48 391 398 10.1016/j.nbd.2012.06.018 22766032
56. Overexpression of Dsk2/dUbqln results in severe developmental defects and lethality in Drosophila melanogaster that can be rescued by overexpression of the p54/Rpn10/S5a proteasomal subunit. Lipinszki Z, Pál M, Nagy O, Deák P, Hunyadi-Gulyas E, Udvardy A, FEBS J. 2011 278 4833 4844 10.1111/j.1742-4658.2011.08383.x 21973017
57. BioGPS and MyGene.info: organizing online, gene-centric information. Wu C, Macleod I, Su AI, Nucleic Acids Res 2013 41 Database issue 561 D565 23175613
58. A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Schultz N, Hamra FK, Garbers DL, Proc Natl Acad Sci U S A 2003 100 12201 12206 10.1073/pnas.1635054100 14526100 (Pubitemid 37271538)
59. The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis. Shima JE, McLean DJ, McCarrey JR, Griswold MD, Biol Reprod 2004 71 319 330 10.1095/biolreprod.103. 026880 15028632 (Pubitemid 38915339)
60. Transcriptome profiling of the murine testis during the first wave of spermatogenesis. Laiho A, Kotaja N, Gyenesei A, Sironen A, PLoS One 2013 8 61558 10.1371/journal.pone.0061558 23613874
61. UBQLN1 interacts with SPEM1 and participates in spermiogenesis. Bao J, Zhang J, Zheng H, Xu C, Yan W, Mol Cell Endocrinol 2010 327 89 97 10.1016/j.mce.2010.06.006 20558241
62. The conserved transcriptome in human and rodent male gametogenesis. Chalmel F, Rolland AD, Niederhauser-Wiederkehr C, Chung SS, Demougin P, Gattiker A, Moore J, Patard JJ, Wolgemuth DJ, Jégou B, Primig M, Proc Natl Acad Sci U S A. 2007 104 8346 8351 10.1073/pnas.0701883104 17483452 (Pubitemid 47175490)
63. PAML 4: Phylogenetic analysis by maximum likelihood. Yang Z, Mol Biol Evol 2007 24 1586 1591 10.1093/molbev/msm088 17483113 (Pubitemid 47236688)
64. Selection on coding regions determined Hox7 genes evolution. Fares MA, Bezemer D, Moya A, Marín I, Mol. Biol. Evol 2003 20 2104 2112 10.1093/molbev/msg222 12949154 (Pubitemid 38057774)
65. PAMLX: A graphical user interface for PAML. Xu B, Yang Z, Mol. Biol Evol 2013 30 2723 2724 10.1093/molbev/mst179 24105918
66. Diversification and specialization of plant RBR ubiquitin ligases. Marín I, PLoS One 2010 5 11579 10.1371/journal.pone.0011579 20644651
67. Evolution of plant HECT ubiquitin ligases. Marín I, PloS One 2013 8 68536 10.1371/journal.pone.0068536 23869223
68. PLIC proteins or ubiquilins regulate autophagy-dependent cell survival during nutrient starvation. N'Diaye EN, Kajihara KK, Hsieh I, Morisaki H, Debnath J, Brown EJ, EMBO Rep. 2009 10 173 179 10.1038/embor.2008.238 19148225
69. Ubiquilin functions in autophagy and is degraded by chaperone-mediated autophagy. Rothenberg C, Srinivasan D, Mah L, Kaushik S, Peterhoff CM, Ugolino J, Fang S, Cuervo AM, Nixon RA, Monteiro MJ, Hum Mol Genet. 2010 19 3219 3232 10.1093/hmg/ddq231 20529957
70. Ubiquilin4 is an adaptor protein that recruits Ubiquilin1 to the autophagy pathway. Lee DY, Arnott D, Brown EJ, EMBO Rep 2013 14 373 38 10.1038/embor.2013.22 23459205
71. Cross-species divergence of the major recognition pathways of ubiquitylated substrates for ubiquitin/26S proteasome-mediated proteolysis. Fatimababy AS, Lin YL, Usharani R, Radjacommare R, Wang HT, Tsai HL, Lee Y, Fu H, FEBS J. 2010 277 796 816 10.1111/j.1742-4658.2009.07531.x 20059542
72. Affinity makes the difference: nonselective interaction of the UBA domain of Ubiquilin-1 with monomeric ubiquitin and polyubiquitin chains. Zhang D, Raasi S, Fushman D, J Mol Biol 2008 377 162 180 10.1016/j.jmb.2007.12.029 18241885
73. Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: killing three birds with one stone. Sutovsky P, Microsc Res Tech 2003 61 88 102 10.1002/jemt.10319 12672125 (Pubitemid 36469238)
74. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 4: intercellular bridges, mitochondria, nuclear envelope, apoptosis, ubiquitination, membrane/voltage-gated channels, methylation/acetylation, and transcription factors. Hermo L, Pelletier RM, Cyr DG, Smith CE, Microsc Res Tech 2010 73 364 408 19941288
75. New insights to the ubiquitin-proteasome pathway (UPP) mechanism during spermatogenesis. Hou CC, Yang WX, Mol Biol Rep 2013 40 3213 3230 10.1007/s11033-012-2397-y 23268313
76. Mining and characterization of ubiquitin E3 ligases expressed in the mouse testis. Hou X, Zhang W, Xiao Z, Gan H, Lin X, Hou X, Zhang W, Xiao Z, Gan H, Lin X, Liao S, Han C, BMC Genomics 2012 13 495 10.1186/1471-2164-13-495 22992278
77. Gene expression in spermiogenesis. Tanaka H, Baba T, Cell Mol Life Sci 2005 62 344 354 10.1007/s00018-004-4394-y 15723169 (Pubitemid 40379248)
78. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 2: changes in spermatid organelles associated with development of spermatozoa. Hermo L, Pelletier RM, Cyr DG, Smith CE, Microsc Res Tech 2010 73 279 319 19941292
79. RBR ubiquitin ligases: diversification and streamlining in animal lineages. Marín I, J Mol Evol 2009 69 54 64 10.1007/s00239-009-9252-3 19526189
80. Origin and diversification of TRIM ubiquitin ligases. Marín I, PLoS One 2012 7 50030 10.1371/journal.pone.0050030 23185523
81. Puzzles of mammalian fertilization-and beyond. Bedford JM, Int J Dev Biol. 2008 52 415 426 10.1387/ijdb.072551jb 18649254
82. Monotremes provide a key to understanding the evolutionary significance of epididymal sperm maturation. Nixon B, Ecroyd HW, Dacheux JL, Jones RC, J Androl. 2011 32 665 671 10.2164/jandrol.110.012716 21441429
83. The role of actin and myosin during spermatogenesis. Sun X, Kovacs T, Hu YJ, Yang WX, Mol Biol Rep 2011 38 3993 4001 10.1007/s11033-010-0517-0 21107714
84. The dynamic cytoskeleton of the developing male germ cell. Sperry AO, Biol Cell 2012 104 297 305 10.1111/boc.201100102 22276751
85. Recent developments in the MAFFT multiple sequence alignment program. Katoh K, Toh H, Brief Bioinform 2008 9 286 298 10.1093/bib/bbn013 18372315 (Pubitemid 351890825)
86. GeneDoc: a tool for editing and annotating multiple sequence alignments. Nicholas KB, Nicholas HB jr, 1997 Distributed by the author
87. Ancient origin of animal U-box ubiquitin ligases. Marín I, BMC Evol Biol 2010 10 331 10.1186/1471-2148-10-331 20979629
88. Animal HECT ubiquitin ligases: evolution and functional implications. Marín I, BMC Evol Biol 2010 10 56 10.1186/1471-2148-10-56 20175895
89. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, Mol Biol Evol 2011 28 2731 2739 10.1093/molbev/msr121 21546353
90. Swofford DL, PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4 Sunderland, Massachusetts: Sinauer Associates 2003
91. Ensembl. Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, Gil L, García-Girón C, Gordon L, Hourlier T, Hunt S, Juettemann T, Kähäri AK, Keenan S, Komorowska M, Kulesha E, Longden I, Maurel T, McLaren WM, Muffato M, Nag R, Overduin B, Pignatelli M, Pritchard B, Pritchard E, et al. Nucleic Acids Res. 2013 41 Database issue 48 D55 23203987
92. InterProScan-an integration platform for the signature-recognition methods in InterPro. Zdobnov EM, Apweiler R, Bioinformatics 2001 17 847 848 10.1093/bioinformatics/17.9.847 11590104 (Pubitemid 32970486)