Skip to main content

Conservation of intronic minisatellite polymorphisms in the SCK1/SHC2 gene of Hominidae

Abstract

The neuronally expressed Shc adaptor homolog SCK1/SHC2 gene contains an unusually high number of minisatellites. In humans, twelve different minisatellite sequences are located in introns of SCK1/SHC2 and ten of them are highly polymorphic. Here we used primers developed for humans to screen ten intronic loci of SCK1/SHC2 in chimpanzee and gorilla, and undertook a comprehensive analysis of the genomic sequence to address the evolutionary events driving these variable repeats. All ten loci amplified in chimpanzee and gorilla contained hypervariable and low-variability minisatellites. The human polymorphic locus TR1 was monomorphic in chimpanzee and gorilla, but we detected polymorphic alleles in these apes for the human monomorphic TR7 locus. When we examined the repeat size among these hominoids, there was no consistent variation by length from humans to great apes. In spite of the inconsistent evolutionary dynamics in repeat length variation, exon 16 was highly conserved between humans and great apes. These results suggest that non-coding intronic minisatellites do not show a consistent evolutionary paradigm but evolved with different patterns among each minisatellite locus. These findings provide important insight for minisatellite conservation during hominoid evolution.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2-1
Fig. 2-2
Fig. 2-3
Fig. 3

References

  • Ahn K, Gim JA, Ha HS, Han K, Kim HS (2013) The novel MER transposon-derived miRNAs in human genome. Gene 512:422–428

    CAS  Article  PubMed  Google Scholar 

  • Amarger V, Gauguier D, Yerle M, Apiou F, Pinton P, Giraudeau F, Monfouilloux S, Lathrop M, Dutrillaux B, Buard J et al (1998) Analysis of distribution in the human, pig, rat genomes points toward a general subtelomeric origin of minisatellite structures. Genomics 52:62–71

    CAS  Article  PubMed  Google Scholar 

  • Barros P, Blanco MG, Boan F, Gomez-Marquez J (2008) Evolution of a complex minisatellite DNA sequence. Mol Phylogenet Evol 49:488–494

    CAS  Article  PubMed  Google Scholar 

  • Bryce LA, Morrison N, Hoare SF, Muir S, Keith WN (2000) Mapping of the gene for the human telomerase reverse transcriptase, hTERT, to chromosome 5p15.33 by fluorescence in situ hybridization. Neoplasia 2:197–201

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Chakravarti A, Lynn A (1999) Meiotic mapping in human. In: Birren B, Green ED, Klapholz S, Myers RM, Roskams (eds) Genome analysis: a laboratory manual, vol 4, Cold Spring Harbor Laboratory Press, New York, pp 1–69

  • Gagneux P, Varki A (2001) Genetic differences between humans and great apes. Mol Phylogenet Evol 18:2–13

    CAS  Article  PubMed  Google Scholar 

  • Hacia JG (2001) Genome of the apes. Trends Genet 17:637–645

    CAS  Article  PubMed  Google Scholar 

  • International Human Genome Sequencing C (2004) Finishing the euchromatic sequence of the human genome. Nature 431:931–945

    Article  Google Scholar 

  • Kojima T, Yoshikawa Y, Takada S, Sato M, Nakamura T, Takahashi N, Copeland NG, Gilbert DJ, Jenkins NA, Mori N (2001) Genomic organization of the Shc-related phosphotyrosine adapters and characterization of the full-length Sck/ShcB: specific association of p68-Sck/ShcB with pp135. Biochem Biophys Res Commun 284:1039–1047

    CAS  Article  PubMed  Google Scholar 

  • Lavigne-Brunette L, Joly MA, Kelly S, Fregeau CJ, Aubin RA (2009) Application of human mini-satellite VNTR probes to genotyping in cynomolgus macaques. Res Vet Sci 87:245–248

    CAS  Article  PubMed  Google Scholar 

  • Leem SH, Kouprina N, Grimwood J, Kim JH, Mullokandov M, Yoon YH, Chae JY, Morgan J, Lucas S, Richardson P et al (2004) Closing the gaps on human chromosome 19 revealed genes with a high density of repetitive tandemly arrayed elements. Genome Res 14:239–246

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Li H, Wang JX, Wu DD, Wang HW, Tang NL, Zhang YP (2012) The origin and evolution of variable number tandem repeat of CLEC4M gene in the global human population. PLoS One 7:e30268

    Google Scholar 

  • Linardopoulou EV, Williams EM, Fan Y, Friedman C, Young JM, Trask BJ (2005) Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature 437:94–100

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Luzi L, Confalonieri S, Di Fiore PP, Pelicci PG (2000) Evolution of Shc functions from nematode to human. Curr Opin Genet Dev 10:668–674

    CAS  Article  PubMed  Google Scholar 

  • Nakamura T, Muraoka S, Sanokawa R, Mori N (1998) N-Shc and Sck, two neuronally expressed Shc adapter homologs. Their differential regional expression in the brain and roles in neurotrophin and Src signaling. J Biol Chem 273:6960–6967

    CAS  Article  PubMed  Google Scholar 

  • O’Bryan JP, Songyang Z, Cantley L, Der CJ, Pawson T (1996) A mammalian adaptor protein with conserved Src homology 2 and phosphotyrosine-binding domains is related to Shc and is specifically expressed in the brain. Proc Natl Acad Sci USA 93:2729–2734

    PubMed Central  Article  PubMed  Google Scholar 

  • Pelicci G, Lanfrancone L, Grignani F, McGlade J, Cavallo F, Forni G, Nicoletti I, Grignani F, Pawson T, Pelicci PG (1992) A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70:93–104

    CAS  Article  PubMed  Google Scholar 

  • Pelicci G, Dente L, De Giuseppe A, Verducci-Galletti B, Giuli S, Mele S, Vetriani C, Giorgio M, Pandolfi PP, Cesareni G et al (1996) A family of Shc related proteins with conserved PTB, CH1 and SH2 regions. Oncogene 13:633–641

    CAS  PubMed  Google Scholar 

  • Ponti G, Conti L, Cataudella T, Zuccato C, Magrassi L, Rossi F, Bonfanti L, Cattaneo E (2005) Comparative expression profiles of ShcB and ShcC phosphotyrosine adapter molecules in the adult brain. Neuroscience 133:105–115

    CAS  Article  PubMed  Google Scholar 

  • Richard GF, Dujon B (2006) Molecular evolution of minisatellites in hemiascomycetous yeasts. Mol Biol Evol 23:189–202

    CAS  Article  PubMed  Google Scholar 

  • Royle NJ, Clarkson RE, Wong Z, Jeffreys AJ (1988) Clustering of hypervariable minisatellites in the proterminal regions of human autosomes. Genomics 3:352–360

    CAS  Article  PubMed  Google Scholar 

  • Yuan Z, Sun X, Jiang D, Ding Y, Lu Z, Gong L, Liu H, Xie J (2010) Origin and evolution of a placental-specific microRNA family in the human genome. BMC Evol Biol 10:346

    PubMed Central  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Dong-A University research fund.

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sun-Hee Leem.

Additional information

Se-Lyun Yoon and Yunhee Jeong contributed equally to this study.

Electronic supplementary material

Below is the link to the electronic supplementary material.

13258_2014_175_MOESM1_ESM.pdf

Suppl. Figure S1. Association of minisatellites and other repeats in the human SCK1/SHC2 gene. A schematic diagram of the sequence spanning the SCK1/SHC2 gene is shown. (a) The approximate positions of minisatellites are indicated by asterisks. On top, a blown up portion of the insert shows the relative positions within introns of the twelve minisatellites. Ten minisatellites (TR1, 2, 3, 4, 7, 8, 9, 10, 11 and 12) analyzed for non-human hominoids were presented in black boxes on top. (b) The positions of transposable elements (MLT1C, MER20B) were predicted by RNAfold Webserver. Suppl. Figure S2. Graphical representations of individual allele size distributions for species and loci. The distributions are presented for human (white), chimpanzee (black) and gorilla (gray). Suppl. Figure S3. Hairpin structure of transposable elements. The secondary structures of two palindromic consensus sequences (MLT1C, MER20B) were predicted by the RNAfold Webserver. Consensus sequences containing palindromic sequences were referred from the Repbase browser of the Genetic Information Research Institute database. There size and minimum free energy are presented as MLT1C: 467 bp, -138.30 kcal/mol, MER20B: 783 bp, -256.20 kcal/mol, respectively. (PDF 172 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Yoon, SL., Jeong, Y., Kim, HS. et al. Conservation of intronic minisatellite polymorphisms in the SCK1/SHC2 gene of Hominidae. Genes Genom 36, 375–385 (2014). https://doi.org/10.1007/s13258-014-0175-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-014-0175-z

Keywords

  • SCK1/SHC2
  • Great apes
  • Minisatellites
  • Molecular evolution