Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Microarray Analysis of Genes Involved with Shell Strength in Layer Shell Gland at the Early Stage of Active Calcification

  • Liu, Zhangguo (The Nurturing Station for the State Key Laboratory of Subtropical Silviculture, Zhejiang A & F University) ;
  • Zheng, Qi (Department of Biology, 104 Lynch Laboratory, University of Pennsylvania) ;
  • Zhang, Xueyu (Institute of Poultry Science, Chinese Academy of Agricultural Science) ;
  • Lu, Lizhi (Institute of Animal Husbandry and Veterinary Science, Zhejiang Provincial Academy of Agricultural Science)
  • Received : 2012.07.18
  • Accepted : 2012.09.15
  • Published : 2013.05.01
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Abstract

The objective of this study was to get a comprehensive understanding of how genes in chicken shell gland modulate eggshell strength at the early stage of active calcification. Four 32-week old of purebred Xianju hens with consistent high or low shell breakage strength were grouped into two pairs. Using Affymetrix Chicken Array, a whole-transcriptome analysis was performed on hen's shell gland at 9 h post oviposition. Gene ontology enrichment analysis for differentially expressed (DE) transcripts was performed using the web-based GOEAST, and the validation of DE-transcripts was tested by qRT-PCR. 1,195 DE-transcripts, corresponding to 941 unique genes were identified in hens with strong eggshell compared to weak shell hens. According to gene ontology annotations, there are 77 DE-transcripts encoding ion transporters and secreted extracellular matrix proteins, and at least 26 DE-transcripts related to carbohydrate metabolism or post-translation glycosylation modification; furthermore, there are 88 signaling DE-transcripts. GO term enrichment analysis suggests that some DE-transcripts mediate reproductive hormones or neurotransmitters to affect eggshell quality through a complex suite of biophysical processes. These results reveal some candidate genes involved with eggshell strength at the early stage of active calcification which may facilitate our understanding of regulating mechanisms of eggshell quality.

Keywords

References

  1. Ahmed, A. M. H., A. B. Rodriguez-Navarro, M. L. Vidal, J. Gautron, J. M. Garcia-Ruiz and Y. Nys. 2005. Changes in eggshell mechanical properties, crystallographic texture and in matrix proteins induced by moult in hens. Br. Poult. Sci. 46:268-279. https://doi.org/10.1080/00071660500065425
  2. Barrionuevo, F. J ., M. Burgos , G. Scherer and R. Jimenez . 2012. Genes promoting and disturbing testis development. Histol. Histopathol. 27:1361-1383.
  3. Burnashev, N. 1998. Calcium permeability of ligand-gated channels. Cell Calcium. 24:325-332. https://doi.org/10.1016/S0143-4160(98)90056-2
  4. Boyer, A., E. Lapointe, X. Zheng, R. G. Cowan, H. Li, S. M. Quirk, F. J. DeMayo, J. S. Richards, and D. Boerboom. 2010. WNT4 is required for normal ovarian follicle development and female fertility. FASEB J. 24:3010-3025. https://doi.org/10.1096/fj.09-145789
  5. Carrino, D. A., J. P. Rodriguez and A. I. Caplan. 1997. Dermatan sulfate proteoglycans from the mineralized matrix of the avian eggshell. Connect. Tissue Res. 36:175-193. https://doi.org/10.3109/03008209709160219
  6. Chen , B., P. Suo , B. Wang , J. Wang , L. Yang , S. Zhou , Y. Zhu , X. M a and Y. Cao. 2011. Mutation analysis of the WNT4 gene in Han Chinese women with premature ovarian failure. Reprod. Biol. Endocrinol. 9:75. https://doi.org/10.1186/1477-7827-9-75
  7. Cheuk, B. L. and S. W. Cheng. 2011. Differential expression of elastin assembly genes in patients with Stanford Type A aortic dissection using microarray analysis. J. Vasc. Surg. 53:1071-1078. https://doi.org/10.1016/j.jvs.2010.11.035
  8. Childs, T. J., M. H. Watson, J. S. Sanghera, D. L. Campbell, S. L. Pelech and A. S. Mak. 1992. Phosphorylation of smooth muscle caldesmon by mitogen-activated protein (MAP) kinase and expression of MAP kinase in differentiated smooth muscle cells. J. Biol. Chem. 267:22853-22859.
  9. Creger, C. R., H. Phillips and J. T. Scott. 1976. Formation of an eggshell. Poult. Sci. 55:1717-1723. https://doi.org/10.3382/ps.0551717
  10. Diaz, F. J ., K. Anthony and A. N. Halfhill . 2011. Early avian follicular development is characterized by changes in transcripts involved in steroidogenesis, paracrine signaling and transcription. Mol. Reprod. Dev. 78:212-223. https://doi.org/10.1002/mrd.21288
  11. Dunn, I. C., P. W. Wilson, Z. Lu, M. M. Bain, C. L. Crossan, R. T. Talbot and D. Waddington. 2009. New hypotheses on the function of the avian shell gland derived from microarray analysis comparing tissue from juvenile and sexually mature hens. Gen. Comp. Endocrinol. 163:225-232. https://doi.org/10.1016/j.ygcen.2009.03.006
  12. Fodor, J., C. Matta, T. JuhAsz, T. OlAh, M. GOnczi, Z. Szijgyarto, P. Gergely, L. Csernoch and R. Zakany. 2009. Ionotropic purinergic receptor P2X4 is involved in the regulation of chondrogenesis in chicken micromass cell cultures. Cell Calcium. 45:421-430. https://doi.org/10.1016/j.ceca.2009.02.004
  13. Franco , H. L., D . Dai, K. Y . Lee, C. A . Rubel, D . Roop, D . Boerboom, J. W . Jeong, J. P . Lydon, I. C . Bagchi, M. K . Bagchi and F. J . Demayo. 2011. WNT4 is a key regulator of normal postnatal uterine development and progesterone signaling during embryo implantation and decidualization in the mouse. FASEB J. 25:1176-1187. https://doi.org/10.1096/fj.10-175349
  14. Gautron, J., M. T. Hincke, K. MANN, M. Panheleux, M. Bain, M. D. McKee, S. E. Solomon and Y. Nys. 2001a. Ovocalyxin-32, a novel chicken eggshell matrix protein: Isolation, amino acid sequencing, cloning and immunocytochemical localization. J. Biol. Chem. 276:39243-39252. https://doi.org/10.1074/jbc.M104543200
  15. Gautron, J., M. T. Hincke, M. Panheleux, J. M. Garcia-Ruiz, T. Boldicke and Y. Nys. 2001b. Ovotransferrin is a matrix protein of the hen eggshell membranes and basal calcified layer. Connect. Tissue Res. 42:255-267. https://doi.org/10.3109/03008200109016840
  16. Gautron, J., E. Murayama, A. Vignal, M. Morisson, M. D. McKee, S. Rehault, V. Labas, M. Belghazi, M. L Vidal, Y. Nys and M. T. Hincke. 2007. Cloning of Ovocalyxin-36, a novel chicken eggshell protein related to lipopolysaccharide-binding proteins (LBP), bactericidal permeability-increasing proteins (BPI), and plunc family proteins. J. Biol. Chem. 282:5273-5286. https://doi.org/10.1074/jbc.M610294200
  17. Greenfield, E. M., D. C. Wilson and M. A. Crenshaw. 1984. Ionotropic nucleation of calcium carbonate by molluscan matrix. Amer. Zool. 24:925-932.
  18. Hambrock, H. O ., B . Kaufmann, S . Müller, F. G . Hanisch, K . Nose, M . Paulsson, P . Maurer and U . Hartmann. 2004. Structural characterization of TSC-36/Flik: Analysis of two charge isoforms. J. Biol. Chem. 279:11727-11735. https://doi.org/10.1074/jbc.M309318200
  19. Hincke, M. T. 1995. Ovalbumin is a component of the chicken eggshell matrix. Connect. Tissue Res. 31:227-233. https://doi.org/10.3109/03008209509010814
  20. Hincke, M. T., J. Gautron, M. Panheleux, J. Garcia-Ruiz, M. D. McKee and Y. Nys. 2000. Identification and localization of lysozyme as a component of eggshell membranes and eggshell matrix. Matrix Biol. 19:443-453. https://doi.org/10.1016/S0945-053X(00)00095-0
  21. Hincke, M. T., C. P. Tsang, M. Courtney, V. Hill and R. Narbaitz. 1995. Purification and immunochemistry of a soluble matrix protein of the chicken eggshell (Ovocleidin 17). Calcif. Tissue Int. 56:578-583. https://doi.org/10.1007/BF00298593
  22. Hsieh, M., M. A. Johnson, N. M. Greenberg and J. S. Richards. 2002. Regulated expression of Wnts and Frizzleds at specific stages of follicular development in the rodent ovary. Endocrinology. 143:898-908. https://doi.org/10.1210/en.143.3.898
  23. Johnson, A. L. 1986. Reproduction in the female. In: Avian Physiology. 4th ed. (Ed. P. D. Sturkie). Springer-Verlag, New York.
  24. Jonchere, V., S. Rehault-Godbert, C. Hennequet-Antier, C. Cabau, V. Sibut, L. A Cogburn, Y. Nys and J. Gautron. 2010. Gene expression profiling to identify eggshell proteins involved in physical defense of the chicken egg. BMC Genomics. 11:57-75. https://doi.org/10.1186/1471-2164-11-57
  25. Kelley, C. G., G. Lavorgna, M. E. Clark, E. Boncinelli and P. L. Mellon. 2000. The Otx2 homeoprotein regulates expression from the gonadotropin-releasing hormone proximal promoter. Mol. Endocrinol. 14:1246-1256. https://doi.org/10.1210/me.14.8.1246
  26. Khuong, T. T. and D. K. Jeong. 2011. Adipogenic differentiation of chicken epithelial oviduct cells using only chicken serum. In Vitro Cell. Dev. Biol. Anim. 47:609-614. https://doi.org/10.1007/s11626-011-9452-1
  27. Lakshminarayanan, R., R. M. Kini and S. Valiyaveettil. 2002. Investigation of the role of ansocalcin in the biomineralization in goose eggshell matrix. Proc. Natl. Acad. Sci. U.S.A. 99:5155-5159. https://doi.org/10.1073/pnas.072658899
  28. Lavelin, I., N. Meiri, M. Einat, O. Genina and M. Pines. 2002. Mechanical strain regulation of the chicken glypican-4 gene expression in the avian eggshell gland. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283:R853-R861.
  29. Lavelin, I., N. Yarden, S. Ben-Bassat, A. Bar and M. Pines. 1998. Regulation of osteopontin gene expression during egg shell formation in the laying hen by mechanical strain. Matrix Biol. 17:615-623. https://doi.org/10.1016/S0945-053X(98)90112-3
  30. Layman, W. S., E. A. Hurd and D. M. Martin. 2011. Reproductive dysfunction and decreased GnRH neurogenesis in a mouse model of CHARGE syndrome. Hum. Mol. Genet. 20:3138-3150. https://doi.org/10.1093/hmg/ddr216
  31. Lerner, F., M. Niere, A. Ludwig and M. Ziegler. 2001. Structural and functional characterization of human NAD kinase. Biochem. Biophys. Res. Commun. 288:69-74. https://doi.org/10.1006/bbrc.2001.5735
  32. Mann, K. 1999. Isolation of a glycosylated form of the chicken eggshell protein ovocleidin and determination of the glycosylation site. Alternative glycosylation/phosphorylation at an N-glycosylation sequon. FEBS Lett. 463:12-14. https://doi.org/10.1016/S0014-5793(99)01586-0
  33. Mann, K., J. Gautron, Y. Nys, M. D. McKee, T. Bajari, W. J. Schneider and M. T. Hincke. 2003. Disulfide-linked heterodimeric clusterin is a component of the chicken eggshell matrix and egg white. Matrix Biol. 22:397-407. https://doi.org/10.1016/S0945-053X(03)00072-6
  34. Mann, K., B. Macek and J. V. Olsen. 2006. Proteomic analysis of the acid-soluble organic matrix of the chicken calcified eggshell layer. Proteomics. 6:3801-3810. https://doi.org/10.1002/pmic.200600120
  35. Mann, K., J. V. Olsen, B. Macek, F. Gnad and M. Mann. 2007. Phosphoproteins of the chicken eggshell calcified layer. Proteomics. 7:106-115. https://doi.org/10.1002/pmic.200600635
  36. Nishii, N., N. Nejime, C. Yamauchi, N. Yanai, K. Shinozuka and T. Nakabayashi. 2009. Effects of ATP on the intracellular calcium level in the osteoblastic TBR31-2 cell line. Biol. Pharm. Bull. 32:18-23. https://doi.org/10.1248/bpb.32.18
  37. Nys, Y., J. Gautron, J. M. Garcia-Ruiz and M. T. Hincke. 2004. Avian eggshell mineralization: biochemical and functional characterization of matrix proteins. C. R. Palevol. 3:549-562. https://doi.org/10.1016/j.crpv.2004.08.002
  38. Ohira, K. and M. Hayashi. 2009. A new aspect of the TrkB signaling pathway in neural plasticity. Curr. Neuropharmacol. 7:276-285. https://doi.org/10.2174/157015909790031210
  39. Orriss, I. R., J. C. Utting, A. Brandao-Burch, K. Colston, B. R. Grubb, G. Burnstock and T. R. Arnett. 2007. Extracellular nucleotides block bone mineralization in vitro: Evidence for dual inhibitory mechanisms involving both P2Y2 receptors and pyrophosphate. Endocrinology 148:4208-4216. https://doi.org/10.1210/en.2007-0066
  40. Peluffo , M. C., M. J . Murphy, S. T . Baughman, R. L . Stouffer and J. D . Hennebold. 2011. Systematic analysis of protease gene expression in the rhesus macaque ovulatory follicle: metalloproteinase involvement in follicle rupture. Endocrinology 152:3963-3974. https://doi.org/10.1210/en.2011-1172
  41. Pines, M., V. Knopov and A. Bar. 1995. Involvement of osteopontin in egg shell formation in the laying chicken. Matrix Biol. 14:765-771. https://doi.org/10.1016/S0945-053X(05)80019-8
  42. Pollak, N., M. Niere and M. Ziegler. 2007. NAD kinase levels control the NADPH concentration in human cells. J. Biol. Chem. 282:33562-33571. https://doi.org/10.1074/jbc.M704442200
  43. Reyes-Grajeda, J. P., A. Moreno and A. Romero. 2004. Crystal structure of ovocleidin-17, a major protein of the calcified Gallus gallus eggshell. J. Biol. Chem. 279:40876-40881. https://doi.org/10.1074/jbc.M406033200
  44. Ramakers, C., J. M. Ruijter, R. H. Deprez, A. F. Moorman. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339:62-66. https://doi.org/10.1016/S0304-3940(02)01423-4
  45. Rhinn, M., A. Dierich, W. Shawlot, R. R. Behringer, M. Le Meur and S. L. Ang. 1998. Sequential roles for Otx2 in visceral endoderm and neuroectoderm for forebrain and midbrain induction and specification. Development. 125:845-856.
  46. Ruijter, J. M., C. Ramakers, W. M. Hoogaars, Y. Karlen, O. Bakker, M. J. van den Hoff, A. F. Moorman. 2009. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 37:e45-e45. https://doi.org/10.1093/nar/gkp045
  47. Sauveur, B. and M. Reviers . 1988. Reproduction des volailles et production d'oeufs. INRA Editions, Paris.
  48. Solomon, S. E. 1999. Gordon Memorial Lecture. An egg ist ein ei, es un huevo, est un oeuf. Br. Poult. Sci. 40:5-11.
  49. Sutherland, C., B. S. Renaux, D. J. Mckay and M. P. Walsh. 1994. Phosphorylation of caldesmon by smooth-muscle casein kinase II. J. Muscle Res. Cell Motil. 15:440-456. https://doi.org/10.1007/BF00122118
  50. Umezu, T., H. Yamanouchi, Y. Iida, M. Miura and Y. Tomooka. 2010. Follistatin-like-1, a diffusible mesenchymal factor determines the fate of epithelium. Proc. Natl. Acad. Sci. USA. 107:4601-4606. https://doi.org/10.1073/pnas.0909501107
  51. Veis, A. 1989. Chemical and biochemical perspectives. in: Biomineralization (Ed. S. Mann, J. Webb and R. J. P. Williams) pp. 189. VCH, Weinhein, New York.
  52. Yang, K. T., C. Y. Lin, J. S. Liou, Y. H. Fan, S. H. Chiou, C. W. Huang, C. P. Wu, E. C. Lin, C. F. Chen, Y. P. Lee, W. C. Lee, S. T. Ding, W. T. Cheng and M. C. Huang. 2007. Differentially expressed transcripts in shell glands from low and high egg production strains of chickens using cDNA microarrays. Anim. Reprod. Sci. 101:113-124. https://doi.org/10.1016/j.anireprosci.2006.09.004
  53. Yoshizaki, K., S. Yamamoto, A. Yamada, K. Yuasa, T. Iwamoto, E. Fukumoto, H. Harada, M. Saito, A. Nakasima, K. Nonaka, Y. Yamada and S. Fukumoto. 2008. Neurotrophic factor neurotrophin-4 regulates ameloblastin expression via full-length TrkB. J. Biol. Chem. 283:3385-3391. https://doi.org/10.1074/jbc.M704913200
  54. Zheng, Q. and X. J. Wang. 2008. GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Res. 36:358-363. https://doi.org/10.1093/nar/gkn276
  55. Zmuda, J. M ., L. M. Yerges-Armstrong , S. P. Moffett , L. Klei , C. M. Kammerer , K. Roeder , J. A. Cauley , A. Kuipers , K. E. Ensrud , C. S. Nestlerode , A. R. Hoffman , C. E. Lewis , T. F. Lang , E. Barrett-Connor , R. E. Ferrell , E. S. Orwoll and Osteoporotic Fractures in Men (MrOS) Study Group . 2011. Genetic analysis of vertebral trabecular bone density and cross-sectional area in older men. Osteoporos Int. 22:1079-1090. https://doi.org/10.1007/s00198-010-1296-0

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