Spag16, an axonemal central apparatus gene, encodes a male germ cell nuclear speckle protein that regulates SPAG16 mRNA expression

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Nagarkatti Gude, David R ^a,b   Jaimez, Ruth ^c   Henderson, Scott C ^a   Teves, Maria E ^b   Zhang, Zhibing ^a,b   Strauss, Jerome F ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN SPAG16; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG; ISOPROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NUCLEAR PROTEIN; PF20 PROTEIN, MOUSE; RIBONUCLEOPROTEIN; SFRS2 PROTEIN, MOUSE;

5' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; AXONEME; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CHLAMYDOMONAS REINHARDTII; CONTROLLED STUDY; GENE; GENE AMPLIFICATION; GENE EXPRESSION REGULATION; GERM CELL; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; SPAG16 GENE; SPERMATOGENESIS; TRANSCRIPTION INITIATION SITE; UPREGULATION; ANIMAL; CELL LINE; GENETICS; MALE; METABOLISM; MOUSE; PHYSIOLOGY; TESTIS;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; MURINAE; MUS;

5' UNTRANSLATED REGIONS; ANIMALS; CELL LINE; GERM CELLS; HUMANS; MALE; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NUCLEAR PROTEINS; PROTEIN ISOFORMS; RIBONUCLEOPROTEINS; RNA, MESSENGER; SPERMATOGENESIS; TESTIS;

EID: 79957838808     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020625     Document Type: Article

References (46)

1. Luck DJ, (1984) Genetic and biochemical dissection of the eucaryotic flagellum. J Cell Biol 98: 789-794.
2. Porter ME, Sale WS, (2000) The 9+2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility. J Cell Biol 151: F37-42.
3. Adams GM, Huang B, Piperno G, Luck DJ, (1981) Central-pair microtubular complex of Chlamydomonas flagella: polypeptide composition as revealed by analysis of mutants. J Cell Biol 91: 69-76.
4. Dutcher SK, Huang B, Luck DJ, (1984) Genetic dissection of the central pair microtubules of the flagella of Chlamydomonas reinhardtii. J Cell Biol 98: 229-236.
5. Smith EF, Lefebvre PA, (1997) PF20 gene product contains WD repeats and localizes to the intermicrotubule bridges in Chlamydomonas flagella. Mol Biol Cell 8: 455-467.
6. Smith EF, Lefebvre PA, (1997) The role of central apparatus components in flagellar motility and microtubule assembly. Cell Motil Cytoskeleton 38: 1-8.
7. Zhang Z, Sapiro R, Kapfhamer D, Bucan M, Bray J, et al. (2002) A sperm-associated WD repeat protein orthologous to Chlamydomonas PF20 associates with Spag6, the mammalian orthologue of Chlamydomonas PF16. Mol Cell Biol 22: 7993-8004.
8. Zhang Z, Kostetskii I, Moss SB, Jones BH, Ho C, et al. (2004) Haploinsufficiency for the murine orthologue of Chlamydomonas PF20 disrupts spermatogenesis. Proc Natl Acad Sci U S A 101: 12946-12951.
9. Zhang Z, Kostetskii I, Tang W, Haig-Ladewig L, Sapiro R, et al. (2006) Deficiency of SPAG16L causes male infertility associated with impaired sperm motility. Biol Reprod 74: 751-759.
10. Lamond AI, Spector DL, (2003) Nuclear speckles: a model for nuclear organelles. Nat Rev Mol Cell Biol 4: 605-612.
11. Ricciardi S, Kilstrup-Nielsen C, Bienvenu T, Jacquette A, Landsberger N, et al. (2009) CDKL5 influences RNA splicing activity by its association to the nuclear speckle molecular machinery. Hum Mol Genet 18: 4590-4602.
12. Hu Y, Plutz M, Belmont AS, (2010) Hsp70 gene association with nuclear speckles is Hsp70 promoter specific. J Cell Biol 191: 711-719.
13. Shopland LS, Johnson CV, Byron M, McNeil J, Lawrence JB, (2003) Clustering of multiple specific genes and gene-rich R-bands around SC-35 domains: evidence for local euchromatic neighborhoods. J Cell Biol 162: 981-990.
14. Zhang Z, Zariwala MA, Mahadevan MM, Caballero-Campo P, Shen X, et al. (2007) A heterozygous mutation disrupting the SPAG16 gene results in biochemical instability of central apparatus components of the human sperm axoneme. Biol Reprod 77: 864-871.
15. Zhang Z, Shen X, Jones BH, Xu B, Herr JC, et al. (2008) Phosphorylation of mouse sperm axoneme central apparatus protein SPAG16L by a testis-specific kinase, TSSK2. Biol Reprod 79: 75-83.
16. Zhang Z, Tang W, Zhou R, Shen X, Wei Z, et al. (2007) Accelerated mortality from hydrocephalus and pneumonia in mice with a combined deficiency of SPAG6 and SPAG16L reveals a functional interrelationship between the two central apparatus proteins. Cell Motil Cytoskeleton 64: 360-376.
17. Lesich KA, Zhang Z, Kelsch CB, Ponichter KL, Strauss JF 3rd, et al. (2010) Functional deficiencies and a reduced response to calcium in the flagellum of mouse sperm lacking SPAG16L. Biol Reprod 82: 736-744.
18. Bastin P, Pullen TJ, Moreira-Leite FF, Gull K, (2000) Inside and outside of the trypanosome flagellum:a multifunctional organelle. Microbes Infect 2: 1865-1874.
19. Kohl L, Bastin P, (2005) The flagellum of trypanosomes. Int Rev Cytol 244: 227-285.
20. Inaba K, (2003) Molecular architecture of the sperm flagella: molecules for motility and signaling. Zoolog Sci 20: 1043-1056.
21. Inaba K, (2007) Molecular basis of sperm flagellar axonemes: structural and evolutionary aspects. Ann N Y Acad Sci 1101: 506-526.
22. Fajardo MA, Haugen HS, Clegg CH, Braun RE, (1997) Separate elements in the 3′ untranslated region of the mouse protamine 1 mRNA regulate translational repression and activation during murine spermatogenesis. Dev Biol 191: 42-52.
23. Kleene KC, (1996) Patterns of translational regulation in the mammalian testis. Mol Reprod Dev 43: 268-281.
24. Eddy EM, (2002) Male germ cell gene expression. Recent Prog Horm Res 57: 103-128.
25. Reddi PP, Flickinger CJ, Herr JC, (1999) Round spermatid-specific transcription of the mouse SP-10 gene is mediated by a 294-base pair proximal promoter. Biol Reprod 61: 1256-1266.
26. Reddi PP, Shore AN, Acharya KK, Herr JC, (2002) Transcriptional regulation of spermiogenesis: insights from the study of the gene encoding the acrosomal protein SP-10. J Reprod Immunol 53: 25-36.
27. Wang PJ, McCarrey JR, Yang F, Page DC, (2001) An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27: 422-426.
28. Eddy EM, O'Brien DA, (1998) Gene expression during mammalian meiosis. Curr Top Dev Biol 37: 141-200.
29. Beissbarth T, Borisevich I, Horlein A, Kenzelmann M, Hergenhahn M, et al. (2003) Analysis of CREM-dependent gene expression during mouse spermatogenesis. Mol Cell Endocrinol 212: 29-39.
30. Strausberg RL, Feingold EA, Grouse LH, Derge JG, Klausner RD, et al. (2002) Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc Natl Acad Sci U S A 99: 16899-16903.
31. Escalier D, (2006) Knockout mouse models of sperm flagellum anomalies. Hum Reprod Update 12: 449-461.
32. Neer EJ, Schmidt CJ, Nambudripad R, Smith TF, (1994) The ancient regulatory-protein family of WD-repeat proteins. Nature 371: 297-300.
33. Smith TF, Gaitatzes C, Saxena K, Neer EJ, (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24: 181-185.
34. Gallenberger M, Meinel DM, Kroeber M, Wegner M, Milkereit P, et al. (2011) Lack of WDR36 leads to preimplantation embryonic lethality in mice and delays the formation of small subunit ribosomal RNA in human cells in vitro. Hum Mol Genet 20: 422-435.
35. Lau CK, Bachorik JL, Dreyfuss G, (2009) Gemin5-snRNA interaction reveals an RNA binding function for WD repeat domains. Nat Struct Mol Biol 16: 486-491.
36. Lallena MJ, Correas I, (1997) Transcription-dependent redistribution of nuclear protein 4.1 to SC35-enriched nuclear domains. J Cell Sci 110 (Pt 2): 239-247.
37. Caceres JF, Misteli T, Screaton GR, Spector DL, Krainer AR, (1997) Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J Cell Biol 138: 225-238.
38. Brown JM, Green J, das Neves RP, Wallace HA, Smith AJ, et al. (2008) Association between active genes occurs at nuclear speckles and is modulated by chromatin environment. J Cell Biol 182: 1083-1097.
39. Hu Q, Kwon YS, Nunez E, Cardamone MD, Hutt KR, et al. (2008) Enhancing nuclear receptor-induced transcription requires nuclear motor and LSD1-dependent gene networking in interchromatin granules. Proc Natl Acad Sci U S A 105: 19199-19204.
40. Takizawa T, Gudla PR, Guo L, Lockett S, Misteli T, (2008) Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. Genes Dev 22: 489-498.
41. Zhao R, Bodnar MS, Spector DL, (2009) Nuclear neighborhoods and gene expression. Curr Opin Genet Dev 19: 172-179.
42. Spector DL, O'Keefe RT, Jimenez-Garcia LF, (1993) Dynamics of transcription and pre-mRNA splicing within the mammalian cell nucleus. Cold Spring Harb Symp Quant Biol 58: 799-805.
43. Marchler-Bauer A, Bryant SH, (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32: W327-331.
44. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, et al. (2009) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225-229.
45. Abramoff MD, Magelhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.
46. Horowitz E, Zhang Z, Jones BH, Moss SB, Ho C, et al. (2005) Patterns of expression of sperm flagellar genes: early expression of genes encoding axonemal proteins during the spermatogenic cycle and shared features of promoters of genes encoding central apparatus proteins. Mol Hum Reprod 11: 307-317.