Hen uterine gene expression profiling during eggshell formation reveals putative proteins involved in the supply of minerals or in the shell mineralization process

BMC Genomics

Joël Gautron¹  Christelle Hennequet-Antier¹  Yves Nys¹  Aurélien Brionne¹ 

[1] INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France

关键词: Organic matrix;    Mineral supply;    Biomineralization;    Transcriptome;    Uterus;    Eggshell;    Chicken;   

Others  :  1217662
DOI  :  10.1186/1471-2164-15-220

 received in 2013-12-12, accepted in 2014-03-11,  发布年份 2014

【 摘 要 】

Background

The chicken eggshell is a natural mechanical barrier to protect egg components from physical damage and microbial penetration. Its integrity and strength is critical for the development of the embryo or to ensure for consumers a table egg free of pathogens. This study compared global gene expression in laying hen uterus in the presence or absence of shell calcification in order to characterize gene products involved in the supply of minerals and / or the shell biomineralization process.

Results

Microarrays were used to identify a repertoire of 302 over-expressed genes during shell calcification. GO terms enrichment was performed to provide a global interpretation of the functions of the over-expressed genes, and revealed that the most over-represented proteins are related to reproductive functions. Our analysis identified 16 gene products encoding proteins involved in mineral supply, and allowed updating of the general model describing uterine ion transporters during eggshell calcification. A list of 57 proteins potentially secreted into the uterine fluid to be active in the mineralization process was also established. They were classified according to their potential functions (biomineralization, proteoglycans, molecular chaperone, antimicrobials and proteases/antiproteases).

Conclusions

Our study provides detailed descriptions of genes and corresponding proteins over-expressed when the shell is mineralizing. Some of these proteins involved in the supply of minerals and influencing the shell fabric to protect the egg contents are potentially useful biological markers for the genetic improvement of eggshell quality.

【 授权许可】

   
2014 Brionne et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Mine Y, Kovacks-Nolan J: New insights in biologically active proteins and peptides derived from hen egg. World’s Poultry Sci J 2006, 62:87-95.
• [2]Réhault-Godbert S, Hervé V, Gautron J, Cabau C, Nys Y: Molecules involved in chemical defence of the chicken egg. In Improving the safety and quality of eggs and egg products. Edited by Nys Y, Bain M, van Immerseel F. Cambridge: Woodhead Publishing limited; 2011:183-208. [Egg chemistry, production and consumption, Volume 1]
• [3]Mine Y, D’Silva I: Bioactive components in egg white. In Egg bioscience and biotechnology. Edited by Mine Y. Hoboken, New Jersey: John Wiley & Sons; 2008:141-184.
• [4]Gautron J, Nys Y: Function of eggshell matrix proteins. In Bioactive egg compounds. Edited by Huopalahti R, Lopez-Fandino R, Anton M, Schade R. Germany: Springer-Verlag; 2007:109-115.
• [5]Gautron J, Nys Y: Eggshell matrix proteins. In Bioactive egg compounds. Edited by Huopalahti R, Lopez-Fandino R, Anton M, Schade R. Germany: Springer-Verlag; 2007:103-108.
• [6]Hincke MT, Nys Y, Gautron J: The role of matrix proteins in eggshell formation. J Poul Sci 2010, 47(3):208-219.
• [7]Hincke MT, Nys Y, Gautron J, Mann K, Rodriguez-Navarro AB, McKee MD: The eggshell: structure, composition and mineralization. Front Biosci 2012, 17:1266-1280.
• [8]Nys Y, Gautron J, Garcia-Ruiz JM, Hincke MT: Avian eggshell mineralization: biochemical and functional characterization of matrix proteins. C R Palevol 2004, 3(6–7):549-562.
• [9]Tullet SG: Egg shell formation and quality. In Egg quality current problems and recent advances. Edited by Wells RG, Belyavin CG. London: Butterworth; 1987:123-146.
• [10]Gautron J, Hincke MT, Nys Y: Precursor matrix proteins in the uterine fluid change with stages of eggshell formation in hens. Connect Tissue Res 1997, 36(3):195-210.
• [11]Nys Y, Guyot N: Egg formation and chemistry. In Improving the Safety and Quality of Eggs and egg Products. Edited by Nys Y, Bain M, van Immerseel F. Cambridge: Woodhead Publishing limited; 2011:83-132. [Egg chemistry, production and consumption, Volume 1]
• [12]Weiner S: Biomineralization: a structural perspective. J Struct Biol 2008, 163(3):229-234.
• [13]Weiner S, Addadi L: Crystallization pathways in biomineralization. In Annual Review of Materials Research, Vol 41. Edited by Clarke DR, Fratzl P. Annual Reviews, 4139 El Camino Way, Po Box 10139, Palo Alto, Ca 94303-0897 USA; 2011:21-40.
• [14]Mann K, Macek B, Olsen JV: Proteomic analysis of the acid-soluble organic matrix of the chicken calcified eggshell layer. Proteomics 2006, 6(13):3801-3810.
• [15]Mann K, Olsen JV, Macek B, Gnad F, Mann M: Phosphoproteins of the chicken eggshell calcified layer. Proteomics 2007, 7(1):106-115.
• [16]Miksik I, Eckhardt A, Sedlakova P, Mikulikova K: Proteins of insoluble matrix of Avian (Gallus Gallus) eggshell. Connect Tissue Res 2007, 48(1):1-8.
• [17]Miksik I, Sedlakova P, Lacinova K, Pataridis S, Eckhardt A: Determination of insoluble avian eggshell matrix proteins. Anal Bioanal Chem 2009, 397(1):205-214.
• [18]Rose-Martel M, Jingwen D, Hincke MT: Proteomic analysis provides new insight into the chicken eggshell cuticle. J Proteomics 2012, 75(9):2697-2706.
• [19]Jonchere V, Rehault-Godbert S, Hennequet-Antier C, Cabau C, Sibut V, Cogburn LA, Nys Y, Gautron J: Gene expression profiling to identify eggshell proteins involved in physical defense of the chicken egg. BMC Genomics 2010., 11(57)
• [20]Nys Y, Zawadzki J, Gautron J, Mills AD: Whitening of brown-shelled eggs - mineral-composition of uterine fluid and rate of protoporphyrin deposition. Poult Sci 1991, 70(5):1236-1245.
• [21]Eastin WC Jr, Spaziani E: On the mechanism of calcium secretion in the avian shell gland (uterus). Biol Reprod 1978, 19(3):505-518.
• [22]Nys Y, Hincke MT, Arias JL, Garcia-Ruiz JM, Solomon SE: Avian eggshell mineralization. Avian Poult Biol Rev 1999, 10(3):143-166.
• [23]Jonchere V, Brionne A, Gautron J, Nys Y: Identification of uterine ion transporters for mineralisation precursors of the avian eggshell. BMC Physiol 2012, 12:10. BioMed Central Full Text
• [24]Nys Y: Regulation of 1,25 (OH)2D3, of osteocalcin and of intestinal and uterine calbindin in hens. In Avian Endocrinology. Edited by Sharp PJ. Bristol (UK): Journal of Endocrinology; 1993:345-357.
• [25]Nys Y, Nguyen TM, Williams J, Etches RJ: Blood-levels of ionized calcium, inorganic phosphorus, 1,25-dihydroxycholecalciferol and gonadal-hormones in hens laying hard-shelled or shell-less eggs. J Endocrinol 1986, 111(1):151-157.
• [26]Benjamini Y, Hochberg Y: Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Statist Soc B 1995, 57(1):289-300.
• [27]Hillier LW, Miller W, Birney E, Warren W, Hardison RC, Ponting CP, Bork P, Burt DW, Groenen MAM, Delany ME, Dodgson JB, Chinwalla AT, Cliften PF, Clifton SW, Delehaunty KD, Fronick C, Fulton RS, Graves TA, Kremitzki C, Layman D, Magrini V, McPherson JD, Miner TL, Minx P, Nash WE, Nhan MN, Nelson JO, Oddy LG, Pohl CS, Randall-Maher J: Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 2004, 432(7018):695-716.
• [28]Ensembl Gallus gallus [http://www.ensembl.org/Gallus_gallus/Info/Index webcite]
• [29]Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW: GenBank. Nucleic Acids Res 2013, 41(D1):D36-D42.
• [30]Entrez gene statistics [http://www.ncbi.nlm.nih.gov/projects/Gene/gentrez_stats.cgi?TAXORG=9031 webcite]
• [31]Entrez gene [http://www.ncbi.nlm.nih.gov/gene/ webcite]
• [32]Genomatix [http://www.genomatix.de webcite]
• [33]International protein index [http://www.ebi.ac.uk/IPI webcite]
• [34]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: Ensembl 2013. Nucleic Acids Res 2013, 41(D1):D48-D55.
• [35]Uniprot [http://www.uniprot.org/ webcite]
• [36]SignalP 4.1 server [http://www.cbs.dtu.dk/services/SignalP/ webcite]
• [37]TMHMM server 2.0 [http://www.cbs.dtu.dk/services/TMHMM/ webcite]
• [38]YLoc [http://abi.inf.uni-tuebingen.de/Services/YLoc/webloc.cgi webcite]
• [39]Briesemeister S, Rahnenfuhrer J, Kohlbacher O: Going from where to why-interpretable prediction of protein subcellular localization. Bioinformatics 2010, 26(9):1232-1238.
• [40]Briesemeister S, Rahnenfuhrer J, Kohlbacher O: YLoc-an interpretable web server for predicting subcellular localization. Nucleic Acids Res 2010, 38:W497-W502.
• [41]Addadi L, Weiner S: Control and design principles in biological mineralization. Angew Chem Int Ed 1992, 31:153-169.
• [42]Bar A, Striem S, Mayelafshar S, Lawson DEM: Differential regulation of calbindin-d28k messenger-rna in the intestine and eggshell gland of the laying hen. J Mol Endocrinol 1990, 4(2):93-99.
• [43]Nys Y, Mayelafshar S, Bouillon R, Vanbaelen H, Lawson DEM: Increases in calbindin d-28 k messenger-rna in the uterus of the domestic-fowl induced by sexual maturity and shell formation. Gen Comp Endocrinol 1989, 76(2):322-329.
• [44]Jeong W, Lim W, Kim J, Ahn SE, Lee HC, Jeong JW, Han JY, Song G, Bazer FW: Cell-specific and temporal aspects of gene expression in the chicken oviduct at different stages of the laying cycle. Biol Reprod 2012, 86(6):172.
• [45]Lavelin I, Meiri N, Einat M, Genina O, Pines M: Mechanical strain regulation of the chicken glypican-4 gene expression in the avian eggshell gland. Am J Physiol Regul Integr Comp Physiol 2002, 283(4):R853-R861.
• [46]Lavelin I, Yarden N, Ben-Bassat S, Bar A, Pines M: Regulation of osteopontin gene expression during Egg shell formation in the laying Hen by mechanical strain. Matrix Biol 1998, 17(8–9):615-623.
• [47]Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G: Gene Ontology: tool for the unification of biology. Nat Genet 2000, 25(1):25-29.
• [48]Burt DW, Carre W, Fell M, Law AS, Antin PB, Maglott DR, Weber JA, Schmidt CJ, Burgess SC, McCarthy FM: The chicken gene nomenclature committee report. BMC Genomics 2009, 10 Suppl 2:S5.
• [49]Bar A: Calcium transport in strongly calcifying laying birds: mechanisms and regulation. Comp Biochem Physiol A Mol Integr Physiol 2009, 152(4):447-469.
• [50]Tempel BL, Shilling DJ: The plasma membrane calcium ATPase and disease. Subcell Biochem 2007, 45:365-383.
• [51]Lorcher K, Hodges RD: Some possible mechanisms of formation of the carbonate fraction of egg shell calcium carbonate. Comp Biochem Physiol 1969, 28(1):119-128.
• [52]Gay CV, Mueller WJ: Cellular localization of carbonic anhydrase in avian tissues by labeled inhibitor autoradiography. J Histochem Cytochem 1973, 21(8):693-702.
• [53]Gay CV, Faleski EJ, Schraer H, Schraer R: Localization of carbonic anhydrase in avian gastric mucosa, shell gland and bone by immunohistochemistry. J Histochem Cytochem 1974, 22(8):819-825.
• [54]Gilmour KM: Perspectives on carbonic anhydrase. Comp Biochem Physiol A Mol Integr Physiol 2010, 157(3):193-197.
• [55]Lavelin I, Meiri N, Genina O, Alexiev R, Pines M: Na + −K + −ATPase gene expression in the avian eggshell gland: distinct regulation in different cell types. Am J Physiol Regul Integr Comp Physiol 2001, 281(4):R1169-R1176.
• [56]Gorokhova S, Bibert S, Geering K, Heintz N: A novel family of transmembrane proteins interacting with beta subunits of the Na, K-ATPase. Hum Mol Genet 2007, 16:2394-2410.
• [57]Gao L, Cong BG, Zhang LM, Ni X: Expression of the calcium-activated potassium channel in upper and lower segment human myometrium during pregnancy and parturition. Reprod Biol Endocrinol 2009, 7:27. BioMed Central Full Text
• [58]Greenwood IA, Yeung SY, Tribe RM, Ohya S: Loss of functional K + channels encoded by ether-a-go-go-related genes in mouse myometrium prior to labour onset. J Physiol 2009, 587(10):2313-2326.
• [59]Beyenbach KW, Wieczorek H: The V-type H + ATPase: molecular structure and function, physiological roles and regulation. J Exp Biol 2006, 209(4):577-589.
• [60]Ding ST, Chang CC, Shen TF: The effect of dietary magnesium and calcium level on the eggshell quality and mineral-content in plasma, eggshell and bone in laying Ttsaiya duck and leghorn hen. J Agric Assoc China 1992, 157:97-107.
• [61]Goytain A, Quamme GA: Functional characterization of the human solute carrier, SLC41A2. Biochem Biophys Res Commun 2005, 330(3):701-705.
• [62]Sahni J, Nelson B, Scharenberg AM: SLC41A2 encodes a plasma-membrane Mg2+ transporter. Biochem J 2007, 401:505-513.
• [63]Moomaw AS, Maguire ME: The Unique Nature of Mg2+ Channels. Physiology 2008, 23(5):275-285.
• [64]Ebel H, Gunther T: Magnesium metabolism - a review. J Clin Chem Clin Biochem 1980, 18(5):257-270.
• [65]Goytain A, Hines RM, Quamme GA: Functional characterization of NIPA2, a selective Mg2+ transporter. Am J Physiol Cell Physiol 2008, 295(4):C944-C953.
• [66]Turski ML, Thiele DJ: New roles for copper metabolism in cell proliferation, signaling, and disease. J Biol Chem 2009, 284(2):717-721.
• [67]Knutson MD: Steap proteins: implications for iron and copper metabolism. Nutr Rev 2007, 65(7):335-340.
• [68]Ohgami RS, Campagna DR, McDonald A, Fleming MD: The Steap proteins are metalloreductases. Blood 2006, 108(4):1388-1394.
• [69]Haguenauer A, Raimbault S, Masscheleyn S, Gonzalez-Barroso MD, Criscuolo F, Plamondon J, Miroux B, Ricquier D, Richard D, Bouillaud F, Pecqueur C: A new renal mitochondrial carrier, KMCP1, is up-regulated during tubular cell regeneration and induction of antioxidant enzymes. J Biol Chem 2005, 280(23):22036-22043.
• [70]Palmieri F: The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch 2004, 447(5):689-709.
• [71]Mann K: The chicken egg white proteome. Proteomics 2007, 7:3558-3568.
• [72]Nickel W: Pathways of unconventional protein secretion. Curr Opin Biotechnol 2010, 21(5):621-626.
• [73]Hincke MT, Chien Y-C, Gerstenfeld LC, McKee MD: Colloidal-gold immunocytochemical localization of osteopontin in avian eggshell gland and eggshell. J Histochem Cytochem 2008, 56(5):467-476.
• [74]Pines M, Knopov V, Bar A: Involvement of osteopontin in egg shell formation in the laying chicken. Matrix Biol 1995, 14(9):765-771.
• [75]Chien YC, Hincke MT, Vali H, McKee MD: Ultrastructural matrix-mineral relationships in avian eggshell, and effects of osteopontin on calcite growth in vitro. J Struct Biol 2008, 163(1):84-99.
• [76]Hincke MT, St Maurice M: phosphorylation-dependent modulation of calcium carbonate precipitation by chicken eggshell matrix proteins. In Chemistry and Biology of Mineralized Tissues. Edited by Goldberg M, Boskey A, Robinson C. Rosemont, IL 60018: American Academy of Orthopaedic Surgeons; 2000:13-17.
• [77]Hincke MT, Gautron J, Tsang CP, McKee MD, Nys Y: Molecular cloning and ultrastructural localization of the core protein of an eggshell matrix proteoglycan, ovocleidin-116. J Biol Chem 1999, 274(46):32915-32923.
• [78]Mann K, Hincke MT, Nys Y: Isolation of ovocleidin-116 from chicken eggshells, correction of its amino acid sequence and identification of disulfide bonds and glycosylated Asn. Matrix Biol 2002, 21(5):383-387.
• [79]Bardet C, Delgado S, Sire JY: MEPE evolution in mammals reveals regions and residues of prime functional importance. Cell Mol Life Sci 2010, 67(2):305-320.
• [80]Rosen H, Polakiewicz RD, Benzakine S, Barshavit Z: Proenkephalin-A in bone-derived cells. Proc Natl Acad Sci U S A 1991, 88(9):3705-3709.
• [81]Keene DR, San Antonio JD, Mayne R, McQuillan DJ, Sarris G, Santoro S, Iozzo RV: Decorin binds near the C terminus of type I collagen. J Biol Chem 2000, 275(29):21801-21804.
• [82]Sullivan MM, Barker TH, Funk SE, Karchin A, Seo NS, Hook M, Sanders J, Starcher B, Wight TN, Puolakkainen P, Sage EH: Matricellular hevin regulates decorin production and collagen assembly. J Biol Chem 2006, 281(37):27621-27632.
• [83]Fernandez MS, Araya M, Arias JL: Eggshells are shaped by a precise spatio-temporal arrangement of sequentially deposited macromolecules. Matrix Biol 1997, 16(1):13-20.
• [84]Fernandez MS, Moya A, Lopez L, Arias JL: Secretion pattern, ultrastructural localization and function of extracellular matrix molecules involved in eggshell formation. Matrix Biol 2001, 19(8):793-803.
• [85]Ito A, Shinmyo Y, Abe T, Oshima N, Tanaka H, Ohta K: Tsukushi is required for anterior commissure formation in mouse brain. Biochem Biophys Res Commun 2010, 402(4):813-818.
• [86]Filmus J, Capurro M, Rast J: Glypicans. Genome Biol 2008, 9(5):224. BioMed Central Full Text
• [87]Apte SS: A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms. J Biol Chem 2009, 284(46):31493-31497.
• [88]Mann K, Gautron J, Nys Y, McKee MD, Bajari T, Schneider WJ, Hincke MT: Disulfide-linked heterodimeric clusterin is a component of the chicken eggshell matrix and egg white. Matrix Biol 2003, 22(5):397-407.
• [89]Gautron J, Murayama E, Vignal A, Morisson M, McKee MD, Rehault S, Labas V, Belghazi M, Vidal ML, Nys Y, Hincke MT: Cloning of ovocalyxin-36, a novel chicken eggshell protein related to lipopolysaccharide-binding proteins, bactericidal permeability-increasing proteins, and plunc family proteins. J Biol Chem 2007, 282(8):5273-5286.
• [90]Bingle CD, Seal RL, Craven CJ: Systematic nomenclature for the PLUNC/PSP/BSP30/SMGB proteins as a subfamily of the BPI fold-containing superfamily. Biochem Soc Trans 2011, 39:977-983.
• [91]Harada H, Ohto U, Satow Y: Crystal structure of mouse MD-1 with endogenous phospholipid bound in its cavity. J Mol Biol 2010, 400(4):838-846.
• [92]Rehault-Godbert S, Labas V, Helloin E, Herve-Grepinet V, Slugocki C, Berges M, Bourin M-C, Brionne A, Poirier J-C, Gautron J, Coste F, Nys Y: Ovalbumin-related protein X is a heparin-binding Ov-Serpin exhibiting antimicrobial activities. J Biol Chem 2013, 288(24):17285-17295.
• [93]Réhault-Godbert S, Jousset N, Labas V, Hervé-Grépinet V, Nys Y, Gautron J: Identification of putative functional proteins in chicken eggshell. In XXIII World’s Poultry Congress: 30 June - 07 July 2008 2008. Brisbane (AUS; World\'s Poultry Science Association (Australian branch); 2008:114-118.
• [94]CRB GADIE [http://crb-gadie.inra.fr webcite]
• [95]Limma R package [http://www.bioconductor.org/packages/2.12/bioc/html/limma.html webcite]
• [96]Smyth GK: Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.
• [97]Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Federhen S, Feolo M, Geer LY, Helmberg W, Kapustin Y, Landsman D, Lipman DJ, Lu ZY, Madden TL, Madej T, Maglott DR, Marchler-Bauer A, Miller V, Mizrachi I, Ostell J, Panchenko A, Pruitt KD, Schuler GD, Sequeira E, Sherry ST, Shumway M: Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 2011, 38:D5-D16.
• [98]Kinsella RJ, Kahari A, Haider S, Zamora J, Proctor G, Spudich G, Almeida-King J, Staines D, Derwent P, Kerhornou A, Kersey P, Flicek P: Ensembl BioMarts: a hub for data retrieval across taxonomic space. Database 2011, 2011:bar030.
• [99]Primer3Plus software [http://www.bioinformatics.nl/cgi-bin/primer3plus/primer3plus.cgi webcite]
• [100]Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Meth 2011, 8(10):785-786.
• [101]Emanuelsson O, Brunak S, von Heijne G, Nielsen H: Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2007, 2(4):953-971.
• [102]Sigrist CJA, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, Bairoch A, Hulo N: PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res 2010, 38:D161-D166.
• [103]Gene expression omnibus [http://www.ncbi.nlm.nih.gov/geo webcite]