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Comparative analysis of differentially expressed genes in Sika deer antler at different stages

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Abstract

Deer antlers serve as useful models of rapid growth and mineralization in mammals. During the period of rapid growth, the antlers of many species of deer will elongate by more than 2 cm per day, after which the antlers gradually ossify. However, little is known about the genes that are involved in their development, particularly the molecular mechanisms responsible for rapid growth and ossification. In our previous studies, we have reported on the transcriptome analysis of deer antlers at rapid growth and ossification stages. With the aim to get a comprehensive understanding of gene expression patterns during antler growth, in the present study, we performed a rigorous algorithm to identify differentially expressed genes between two different stages (60 and 90 days) during antler growth. A total of 16,905 significantly changed transcripts were identified. Those sequences were mapped to 5,573 genes with 2,217 genes up-regulated and 3,356 genes down-regulated (60 days vs. 90 days), including ribosomal proteins, translation initiation and elongation factors, transcription factors, signaling molecules and extracellular matrix proteins. We also performed the gene ontology (GO) functional enrichment and pathway enrichment analysis of gene expression patterns with hypergeometric test and Bonferroni Correction. Both the two stages were enriched with members of GO categories and distinct pathways. Our data represent the most comprehensive sequence resource available for the deer antler and provide a basis for further research on deer antler molecular genetics and functional genomics.

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Abbreviations

GO:

Gene ontology

COG:

Clusters of orthologous groups

KEGG:

Kyoto encyclopedia of genes and genomes

DEGs:

Differentially expressed genes

References

  1. Yao B, Zhao Y, Zhang M et al (2011) Generation and analysis of expressed sequence tags from the bone marrow of Chinese Sika deer. Mol Biol Rep 39(3):2981–2990

    Article  PubMed  Google Scholar 

  2. Szuwart T, Kierdorf H, Kierdorf U et al (2002) Histochemical and ultrastructural studies of cartilage resorption and acid phosphatase activity during antler growth in fallow deer (Dama dama). Anat Rec 268:66–72

    Article  PubMed  CAS  Google Scholar 

  3. Garcia RL, Sadighi M, Francis SM et al (1997) Expression of neurotrophin-3 in the growing velvet antler of the red deer Cervus elaphus. J Mol Endocrinol 19:173–182

    Article  PubMed  CAS  Google Scholar 

  4. Price J, Allen S (2004) Exploring the mechanisms regulating regeneration of deer antlers. Philos Trans R Soc Lond B Biol Sci 359:809–822

    Article  PubMed  CAS  Google Scholar 

  5. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  PubMed  CAS  Google Scholar 

  6. Metzker ML (2009) Sequencing technologies-the next generation. Nat Rev Genet 11:31–46

    Article  PubMed  Google Scholar 

  7. Yao B, Zhao Y, Wang Q et al (2012) De novo characterization of the antler tip of Chinese Sika deer transcriptome and analysis of gene expression related to rapid growth. Mol Cell Biochem 364:93–100

    Article  PubMed  CAS  Google Scholar 

  8. Yao B, Zhao Y, Zhang H et al (2012) Sequencing and de novo analysis of the Chinese Sika deer antler-tip transcriptome during the ossification stage using Illumina RNA-Seq technology. Biotechnol Lett 34(5):813–822

    Article  PubMed  CAS  Google Scholar 

  9. Li R, Zhu H, Ruan J et al (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272

    Article  PubMed  CAS  Google Scholar 

  10. Lee Y, Tsai J, Sunkara S et al (2005) The TIGR Gene Indices: clustering and assembling EST and known genes and integration with eukaryotic genomes. Nucleic Acids Res 33:D71–D74

    Article  PubMed  CAS  Google Scholar 

  11. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877

    Article  PubMed  CAS  Google Scholar 

  12. Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol: 138–148

  13. Conesa A, Götz S, García-Gómez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  PubMed  CAS  Google Scholar 

  14. Harris MA, Clark J, Ireland A et al (2004) The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261

    Article  PubMed  CAS  Google Scholar 

  15. Ye J, Fang L, Zheng H et al (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34(Web Server issue):W293–W297

    Article  PubMed  CAS  Google Scholar 

  16. Tatusov RL, Natale DA, Garkavtsev IV et al (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28

    Article  PubMed  CAS  Google Scholar 

  17. Kanehisa M, Goto S, Kawashima S et al (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277–D280

    Article  PubMed  CAS  Google Scholar 

  18. Mortazavi A, Williams BA, Mccue K et al (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:1–8

    Article  Google Scholar 

  19. Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995

    PubMed  CAS  Google Scholar 

  20. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔct method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  22. Shi CY, Yang H, Wei CL et al (2011) Deep sequencing of the Camellia sinensis transcriptome revealed candidate genes for major metabolic pathways of tea-specific compounds. BMC Genomics 12:131

    Article  PubMed  CAS  Google Scholar 

  23. Wang XW, Luan JB, Li JM et al (2010) De novo characterization of a whitefly transcriptome and analysis of its gene expression during development. BMC Genomics 11:400

    Article  PubMed  Google Scholar 

  24. Dever TE (2002) Gene-specific regulation by general translation factors. Cell 108:545–556

    Article  PubMed  CAS  Google Scholar 

  25. Chen FW, Ioannou YA (1999) Ribosomal proteins in cell proliferation and apoptosis. Int Rev Immunol 18:429–448

    Article  PubMed  CAS  Google Scholar 

  26. Bortoluzzi S, d’Alessi F, Romualdi C et al (2001) Differential expression of genes coding for ribosomal proteins in different human tissues. Bioinformatics 17:1152–1157

    Article  PubMed  CAS  Google Scholar 

  27. Kowalczyk P, Woszczyński M, Ostrowski J (2002) Increased expression of ribosomal protein S2 in liver tumors, posthepactomized livers, and proliferating hepatocytes in vitro. Acta Biochim Pol 49:615–624

    PubMed  CAS  Google Scholar 

  28. Hagner PR, Mazan-Mamczarz K, Dai B et al (2011) Ribosomal protein S6 is highly expressed in non-Hodgkin lymphoma and associates with mRNA containing a 5′ terminal oligopyrimidine tract. Oncogene 30:1531–1541

    Article  PubMed  CAS  Google Scholar 

  29. Kondoh N, Shuda M, Tanaka K et al (2001) Enhanced expression of S8, L12, L23a, L27 and L30 ribosomal protein mRNAs in human hepatocellular carcinoma. Anticancer Res 21:2429–2433

    PubMed  CAS  Google Scholar 

  30. He H, Sun Y (2007) Ribosomal protein S27L is a direct p53 target that regulates apoptosis. Oncogene 26:2707–2716

    Article  PubMed  CAS  Google Scholar 

  31. Khanna N, Sen S, Sharma H et al (2003) S29 ribosomal protein induces apoptosis in H520 cells and sensitizes them to chemotherapy. Biochem Bioph Res Co 304:26–35

    Article  CAS  Google Scholar 

  32. Zhang Y, Wolf GW, Bhat K et al (2003) Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol Cell Biol 23:8902–8912

    Article  PubMed  CAS  Google Scholar 

  33. Zanelli CF, Valentini SR (2007) Is there a role for eIF5A in translation? Amino Acids 33:351–835

    Article  PubMed  CAS  Google Scholar 

  34. Shahbazian D, Parsyan A, Petroulakis E et al (2010) Control of cell survival and proliferation by mammalian eukaryotic initiation factor 4B. Mol Cell Biol 30:1478–1485

    Article  PubMed  CAS  Google Scholar 

  35. Zhang L, Pan X, Hershey JWB (2007) Individual overexpression of five subunits of human translation initiation factor eIF3 promotes malignant transformation of immortal fibroblast cells. J Biol Chem 282:5790–5800

    Article  PubMed  CAS  Google Scholar 

  36. Djé MK, Mazabraud A, Viel A et al (1990) Three genes under different developmental control encode elongation factor 1-α in Xenopus laevis. Nucleic Acids Res 18:3489–3493

    Article  PubMed  Google Scholar 

  37. Xu K, Zhang Y, Ilalov K et al (2007) Cartilage oligomeric matrix protein associates with granulin-epithelin precursor (GEP) and potentiates GEP-stimulated chondrocyte proliferation. J Biol Chem 282:11347–11355

    Article  PubMed  CAS  Google Scholar 

  38. Kong L, Tian Q, Guo F et al (2010) Interaction between cartilage oligomeric matrix protein and extracellular matrix protein 1 mediates endochondral bone growth. Matrix Biol 29:276–286

    Article  PubMed  CAS  Google Scholar 

  39. Haglund L, Tillgren V, Addis L et al (2011) Identification and characterization of the integrin alpha2beta1 binding motif in chondroadherin mediating cell attachment. J Biol Chem 286:3925–3934

    Article  PubMed  CAS  Google Scholar 

  40. Zheng Q, Zhou G, Morello R et al (2003) Type X collagen gene regulation by Runx2 contributes directly to its hypertrophic chondrocyte-specific expression in vivo. J Cell Biol 162:833–842

    Article  PubMed  CAS  Google Scholar 

  41. Wilsman NJ, Farnum CE, Leiferman EM et al (1996) Differential growth by growth plates as a function of multiple parameters of chondrocytic kinetics. J Orthopaed Res 14:927–936

    Article  CAS  Google Scholar 

  42. Gelse K, Klinger P, Koch M et al (2011) Thrombospondin-1 prevents excessive ossification in cartilage repair tissue induced by osteogenic protein-1. Tissue Eng Part A 15–16:2101–2112

    Article  Google Scholar 

  43. Klinger P, Surmann-Schmitt C, Brem M et al (2011) Chondromodulin 1 stabilizes the chondrocyte phenotype and inhibits endochondral ossification of porcine cartilage repair tissue. Arthritis Rheum 63:2721–2731

    Article  PubMed  CAS  Google Scholar 

  44. Xu C, Zhang Z, Wu M et al (2011) Recombinant human midkine stimulates proliferation and decreases dedifferentiation of auricular chondrocytes in vitro. Exp Biol Med 236:1254–1262

    Article  CAS  Google Scholar 

  45. Terpstra L, Prud’homme J, Arabian A et al (2003) Reduced chondrocyte proliferation and chondrodysplasia in mice lacking the integrin-linked kinase in chondrocytes. J Cell Biol 162:139–148

    Article  PubMed  CAS  Google Scholar 

  46. Grashoff C, Aszódi A, Sakai T et al (2003) Integrin-linked kinase regulates chondrocyte shape and proliferation. EMBO Rep 4:432–438

    Article  PubMed  CAS  Google Scholar 

  47. Aberger F, Weidinger G, Grunz H et al (1998) Anterior specification of embryonic ectoderm: the role of the Xenopus cement gland-specific gene XAG-2. Mech Develop 72:115–130

    Article  CAS  Google Scholar 

  48. Brychtova V, Vojtesek B, Hrstka R et al (2011) Anterior gradient 2: a novel player in tumor cell biology. Cancer Lett 304:1–7

    Article  PubMed  CAS  Google Scholar 

  49. Kumar A, Godwin JW, Gates PB et al (2007) Molecular basis for the nerve dependence of limb regeneration in an adult vertebrate. Science 318:772–777

    Article  PubMed  CAS  Google Scholar 

  50. Newman B, Gigout LI, Sudre L et al (2001) Coordinated expression of matrix Gla protein is required during endochondral ossification for chondrocyte survival. J Cell Biol 154:659–666

    Article  PubMed  CAS  Google Scholar 

  51. Ivkovic S (2003) Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 130:2779–2791

    Article  PubMed  CAS  Google Scholar 

  52. Salati S, Zini R, Bianchi E et al (2008) Role of CD34 antigen in myeloid differentiation of human hematopoietic progenitor cells. Stem cells 26:950–959

    Article  PubMed  CAS  Google Scholar 

  53. Kopher RA, Penchev VR, Islam MS et al (2010) Human embryonic stem cell-derived CD34+ cells function as MSC progenitor cells. Bone 47:718–728

    Article  PubMed  CAS  Google Scholar 

  54. Francis SM, Suttie JM (1998) Detection of growth factors and proto-oncogene mRNA in the growing tip of red deer (Cervus elaphus) antler using reverse-transcriptase polymerase chain reaction (RT-PCR). J Exp Zool 281:36–42

    Article  PubMed  CAS  Google Scholar 

  55. Fisher MC, Meyer C, Garber G et al (2005) Role of IGFBP2, IGF-I and IGF-II in regulating long bone growth. Bone 37:741–750

    Article  PubMed  CAS  Google Scholar 

  56. Horiuchi K, Amizuka N, Takeshita S et al (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14:1239–1249

    Article  PubMed  CAS  Google Scholar 

  57. Contié S, Voorzanger-Rousselot N, Litvin J et al (2010) Development of a new ELISA for serum periostin: evaluation of growth-related changes and bisphosphonate treatment in mice. Calcif Tissue Int 87:341–350

    Article  PubMed  Google Scholar 

  58. Damazo AS, Moradi-Bidhendi N, Oliani SM et al (2007) Role of annexin 1 gene expression in mouse craniofacial bone development. Birth Defects Res A 79:524–532

    Article  CAS  Google Scholar 

  59. von der Mark K, von der Mark H (1977) The role of three genetically distinct collagen types in endochondral ossification and calcification of cartilage. J Bone Joint Surg Br 59B:458–464

    Google Scholar 

  60. Kirsch T, von der Mark K (1992) Remodelling of collagen types I, II and X and calcification of human fetal cartilage. Bone Miner 18:107–117

    Article  PubMed  CAS  Google Scholar 

  61. Carinci F, Bodo M, Tosi L et al (2002) Expression profiles of craniosynostosis-derived fibroblasts. Mol Med 8:638–644

    PubMed  CAS  Google Scholar 

  62. Gamer LW, Ho V, Cox K et al (2008) Expression and function of BMP3 during chick limb development. Dev Dynam 237:1691–1698

    Article  CAS  Google Scholar 

  63. Hinoi E, Bialek P, Chen YT et al (2006) Runx2 inhibits chondrocyte proliferation and hypertrophy through its expression in the perichondrium. Gene Dev 20:2937–2942

    Article  PubMed  CAS  Google Scholar 

  64. Bucay N, Sarosi I, Dunstan CR et al (1998) Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Gene Dev 12:1260–1268

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Key Technology Research and Development Program of the Ministry of Science and Technology of China (Grant No. 2011BAI03B00) and by the National Science and Technology Major Project of the Ministry of Science and Technology of China (Grant No. 2011ZX09401-305-09).

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Authors and Affiliations

  1. Jiangsu Kanion Pharmaceutical Co. Ltd, Lianyungang, 222001, China

    Wei Xiao

  2. State Key Laboratory of New-tech for Chinese Medicine Pharmaceutical Process, Lianyungang, 222001, China

    Wei Xiao

  3. Center for New Medicine Research, Changchun University of Chinese Medicine, Changchun, 130117, China

    Yu Zhao, Baojin Yao, Mei Zhang, Siming Wang & Hui Zhang

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  1. Yu Zhao
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  2. Baojin Yao
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  3. Mei Zhang
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  4. Siming Wang
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  5. Hui Zhang
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  6. Wei Xiao
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Correspondence to Wei Xiao.

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Zhao, Y., Yao, B., Zhang, M. et al. Comparative analysis of differentially expressed genes in Sika deer antler at different stages. Mol Biol Rep 40, 1665–1676 (2013). https://doi.org/10.1007/s11033-012-2216-5

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