Quantitative proteomics and bioinformatic analysis provide new insight into protein function during avian eggshell biomineralization

Journal of Proteomics

Volumn 113, Issue , 2015, Pages 178-193

  Marie, Pauline ^a   Labas, Valérie ^b   Brionne, Aurélien ^a   Harichaux, Grégoire ^b   Hennequet Antier, Christelle ^a   Nys, Yves ^a   Gautron, Joël ^a  

^a STATION DE RECHERCHES AVICOLES   (France)

^b UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

Author keywords

Chicken; Eggshell; Mineralization; Quantitative proteomics; Uterine fluid

Indexed keywords

CALCIUM BINDING PROTEIN; CHAPERONE; EGF LIKE REPEATS AND DISCOIDIN I LIKE DOMAIN 3 PROTEIN; LACTADHERIN; MATRIX PROTEIN; OVALBUMIN; OVOCALYXIN 21 PROTEIN; OVOCLEIDIN 17 PROTEIN; OVOTRANSFERRIN; UNCLASSIFIED DRUG; AVIAN PROTEIN; CHORION PROTEINS; EGG PROTEIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BIOINFORMATICS; BIOMINERALIZATION; EGG SHELL; FEMALE; GALLUS GALLUS; GEL CHROMATOGRAPHY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEOMICS; QUANTITATIVE ANALYSIS; TANDEM MASS SPECTROMETRY; UTERUS FLUID; ANIMAL; BIOLOGY; BONE MINERALIZATION; CHICKEN; GENETICS; METABOLISM; OOCYTE; PHYSIOLOGY;

AVES;

ANIMALS; AVIAN PROTEINS; CALCIFICATION, PHYSIOLOGIC; CHICKENS; COMPUTATIONAL BIOLOGY; EGG PROTEINS; FEMALE; OVUM; PROTEOMICS;

EID: 84911938941     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.09.024     Document Type: Article

References (85)

1. Réhault-Godbert S., Hervé V., Gautron J., Cabau C., Nys Y. Molecules involved in chemical defence of the chicken egg. Improving the safety and quality of eggs and egg products 2011, 183-208. Woodhead Publishing Limited, Cambridge. Y. Nys, M. Bain, F. Van Immerseel (Eds.).
2. Nys Y., Gautron J., Garcia-Ruiz J.M., Hincke M.T. Avian eggshell mineralization: biochemical and functional characterization of matrix proteins. C R Palevol 2004, 3:549-562.
3. Hincke M.T., Nys Y., Gautron J., Mann K., Rodriguez-Navarro A.B., McKee M.D. The eggshell: structure, composition and mineralization. Front Biosci 2012, 17:1266-1280.
4. Gautron J., Nys Y. Function of eggshell matrix proteins. Bioactive egg compounds 2007, 109-115. Springer-Verlag, Germany. R. Huopalahti, R. Lopez-Fandino, M. Anton, R. Schade (Eds.).
5. Hincke M.T., Nys Y., Gautron J. The role of matrix proteins in eggshell formation. J Poult Sci 2010, 47:208-219.
6. Nys Y., Zawadzki J., Gautron J., Mills A.D. Whitening of brown-shelled eggs: mineral composition of uterine fluid and rate of protoporphyrin deposition. Poult Sci 1991, 70:1236-1245.
7. Gautron J., Hincke M.T., Nys Y. Precursor matrix proteins in the uterine fluid change with stages of eggshell formation in hens. Connect Tissue Res 1997, 36:195-210.
8. Gautron J., Nau F., Mann K., Guerin-Dubiard C., Rehault S., Hincke M.T., et al. Molecular approaches for the identification of novel egg components. Worlds Poult Sci J 2007, 63:82-90.
9. Gautron J., Réhault-Godbert S., Nys Y. Use of high-throughput technology to identify new egg components. Improving the safety and quality of eggs and egg products 2011, 133-150. Woodhead Publishing Limited, Cambridge. Y. Nys, M. Bain, F. Van Immerseel (Eds.).
10. Mann K., Macek B., Olsen J.V. Proteomic analysis of the acid-soluble organic matrix of the chicken calcified eggshell layer. Proteomics 2006, 6:3801-3810.
11. Mann K., Olsen J.V., Macek B., Gnad F., Mann M. Phosphoproteins of the chicken eggshell calcified layer. Proteomics 2007, 7:106-115.
12. Miksik I., Eckhardt A., Sedlakova P., Mikulikova K. Proteins of insoluble matrix of avian (Gallus gallus) eggshell. Connect Tissue Res 2007, 48:1-8.
13. Miksik I., Sedlakova P., Lacinova K., Pataridis S., Eckhardt A. Determination of insoluble avian eggshell matrix proteins. Anal Bioanal Chem 2010, 397:205-214.
14. Rose-Martel M., Du J.W., Hincke M.T. Proteomic analysis provides new insight into the chicken eggshell cuticle. J Proteomics 2012, 75:2697-2706.
15. Brionne A., Nys Y., Hennequet-Antier C., Gautron J. 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 2014, 15:220.
16. Jonchere V., Rehault-Godbert S., Hennequet-Antier C., Cabau C., Sibut V., Cogburn L.A., et al. Gene expression profiling to identify eggshell proteins involved in physical defense of the chicken egg. BMC Genomics 2010, 11:57.
17. Nahnsen S., Bielow C., Reinert K., Kohlbacher O. Tools for label-free peptide quantification. Mol Cell Proteomics 2013, 12:549-556.
18. Labas V., Grasseau I., Cahier K., Gargaros A., Harichaux G., Teixeira-Gomes A.P., et al. Qualitative and quantitative peptidomic and proteomic approaches to phenotyping chicken semen. J Proteomics 2014, [in press]. 10.1016/j.jprot.2014.07.024.
19. Keller A., Nesvizhskii A.I., Kolker E., Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002, 74:5383-5392.
20. Nesvizhskii A.I., Keller A., Kolker E., Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 2003, 75:4646-4658.
21. Vizcaino J.A., Deutsch E.W., Wang R., Csordas A., Reisinger F., Rios D., et al. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol 2014, 32:223-226.
22. Sievers F., Wilm A., Dineen D., Gibson T.J., Karplus K., Li W.Z., et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011, 7.
23. Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., et al. BLAST plus: architecture and applications. BMC Bioinforma 2009, 10.
24. Marie P., Labas V., Brionne A., Harichaux G., Hennequet-Antier C., Nys Y., et al. Data set for the proteomic inventory and quantitative analysis of chicken uterine fluid during eggshell biomineralization. Data Brief 2014, [in press].
25. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374.
26. Gautron J., Hincke M.T., Panheleux M., Garcia-Ruiz J.M., Boldicke T., Nys Y. Ovotransferrin is a matrix protein of the hen eggshell membranes and basal calcified layer. Connect Tissue Res 2001, 42:255-267.
27. Gautron J., Murayama E., Vignal A., Morisson M., McKee M.D., Rehault S., et al. 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, 282:5273-5286.
28. Sun C., Xu G., Yang N. Differential label-free quantitative proteomic analysis of avian eggshell matrix and uterine fluid proteins associated with eggshell mechanical property. Proteomics 2013, 13:3523-3536.
29. 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.
30. Panheleux M., Nys Y., Williams J., Gautron J., Boldicke T., Hincke M.T. Extraction and quantification by ELISA of eggshell organic matrix proteins (ovocleidin-17, ovalbumin, ovotransferrin) in shell from young and old hens. Poult Sci 2000, 79:580-588.
31. Miksik I., Charvatova J., Eckhardt A., Deyl Z. Insoluble eggshell matrix proteins - their peptide mapping and partial characterization by capillary electrophoresis and high-performance liquid chromatography. Electrophoresis 2003, 24:843-852.
32. Hincke M.T. Ovalbumin is a component of the chicken eggshell matrix. Connect Tissue Res 1995, 31:227-233.
33. Wang X.Q., Wu C.M., Tao K., Zhao K., Wang J.Q., Xu H., et al. Influence of ovalbumin on CaCO(3) precipitation during in vitro biomineralization. J Phys Chem B 2010, 114:5301-5308.
34. Schwahn D., Balz M., Tremel W. Crystallization of the CaCO(3) mineral in the presence of the protein ovalbumin. Phys B 2004, 350:E947-E949.
35. Pipich V., Balz M., Wolf S.E., Tremel W., Schwahn D. Nucleation and growth of CaCO(3) mediated by the egg-white protein ovalbumin: a time-resolved in situ study using small-angle neutron scattering. J Am Chem Soc 2008, 130:6879-6892.
36. Mann K., Hincke M.T., 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, 21:383-387.
37. Hincke M.T., Tsang C.P., Courtney M., Hill V., Narbaitz R. Purification and immunochemistry of a soluble matrix protein of the chicken eggshell (ovocleidin 17). Calcif Tissue Int 1995, 56:578-583.
38. Reyes-Grajeda J.P., Moreno A., Romero A. Crystal structure of ovocleidin-17, a major protein of the calcified Gallus gallus eggshell - implications in the calcite mineral growth pattern. J Biol Chem 2004, 279:40876-40881.
39. Freeman C.L., Harding J.H., Quigley D., Rodger P.M. Simulations of ovocleidin-17 binding to calcite surfaces and its implications for eggshell formation. J Phys Chem C 2011, 115:8175-8183.
40. Rodriguez-Navarro A.B., Marie P., Nys Y., Hincke M.T., Gautron J. Amorphous calcium carbonate controls avian eggshell mineralization: a new paradigm for understanding rapid eggshell calcification. J Struct Biol 2014, [submitted for publication].
41. Gautron J., Hincke M.T., Mann K., Panheleux M., Bain M., McKee M.D., et al. Ovocalyxin-32, a novel chicken eggshell matrix protein - isolation, amino acid sequencing, cloning, and immunocytochemical localization. J Biol Chem 2001, 276:39243-39252.
42. Dunn I.C., Joseph N.T., Bain M., Edmond A., Wilson P.W., Milona P., et al. Polymorphisms in eggshell organic matrix genes are associated with eggshell quality measurements in pedigree Rhode Island Red hens. Anim Genet 2009, 40:110-114.
43. Dunn I.C., Rodriguez-Navarro A.B., McDade K., Schmutz M., Preisinger R., Waddington D., et al. Genetic variation in eggshell crystal size and orientation is large and these traits are correlated with shell thickness and are associated with eggshell matrix protein markers. Anim Genet 2012, 43:410-418.
44. Takahashi H., Yang D., Sasaki O., Furukawa T., Nirasawa K. Mapping of quantitative trait loci affecting eggshell quality on chromosome 9 in an F-2 intercross between two chicken lines divergently selected for eggshell strength. Anim Genet 2009, 40:779-782.
45. Fulton J.E., Soller M., Lund A.R., Arango J., Lipkin E. Variation in the ovocalyxin-32 gene in commercial egg-laying chickens and its relationship with egg production and egg quality traits. Anim Genet 2012, 43:102-113.
46. Takahashi H., Sasaki O., Nirasawa K., Furukawa T. Association between ovocalyxin-32 gene haplotypes and eggshell quality traits in an F-2 intercross between two chicken lines divergently selected for eggshell strength. Anim Genet 2010, 41:541-544.
47. Arias J.L., Nakamura O., Fernandez M.S., Wu J.J., Knigge P., Eyre D.R., et al. Role of type X collagen on experimental mineralization of eggshell membranes. Connect Tissue Res 1997, 36:21-33.
48. Schurpf T., Chen Q., Liu J.H., Wang R., Springer T.A., Wang J.H. The RGD finger of Del-1 is a unique structural feature critical for integrin binding. FASEB J 2012, 26:3412-3420.
49. Fan Y.F., Zhu W., Yang M., Zhu Y.Q., Shen F.X., Hao Q., et al. Del-1 gene transfer induces cerebral angiogenesis in mice. Brain Res 2008, 1219:1-7.
50. Raymond A., Ensslin M.A., Shur B.D. SED1/MFG-E8: a bi-motif protein that orchestrates diverse cellular interactions. J Cell Biochem 2009, 106:957-966.
51. Delanghe J.R., Langlois M.R. Hemopexin: a review of biological aspects and the role in laboratory medicine. Clin Chim Acta 2001, 312:13-23.
52. Mauk M.R., Rosell F.I., Lelj-Garolla B., Moore G.R., Mauk A.G. Metal ion binding to human hemopexin. Biochemistry 2005, 44:1864-1871.
53. Alberdi E., Hyde C.C., Becerra S.P. Pigment epithelium-derived factor (PEDF) binds to glycosaminoglycans: analysis of the binding site. Biochemistry 1998, 37:10643-10652.
54. Fernandez M.S., Araya M., Arias J.L. Eggshells are shaped by a precise spatio-temporal arrangement of sequentially deposited macromolecules. Matrix Biol 1997, 16:13-20.
55. Fernandez M.S., Moya A., Lopez L., Arias J.L. Secretion pattern, ultrastructural localization and function of extracellular matrix molecules involved in eggshell formation. Matrix Biol 2001, 19:793-803.
56. Hincke M.T., Gautron J., Tsang C.P.W., McKee M.D., Nys Y. Molecular cloning and ultrastructural localization of the core protein of an eggshell matrix proteoglycan, ovocleidin-116. J Biol Chem 1999, 274:32915-32923.
57. Hincke M.T., Gautron J., Panheleux M., Garcia-Ruiz J., McKee M.D., Nys Y. Identification and localization of lysozyme as a component of eggshell membranes and eggshell matrix. Matrix Biol 2000, 19:443-453.
58. Kraghhansen U., Vorum H. Quantitaive analyses of the interaction between calcium ions and human serum albumin. Clin Chem 1993, 39:202-208.
59. Dellett M., Hu W., Papadaki V., Ohnuma S.-i. Small leucine rich proteoglycan family regulates multiple signalling pathways in neural development and maintenance. Dev Growth Differ 2012, 54:327-340.
60. Grootjans J.J., Zimmermann P., Reekmans G., Smets A., Degeest G., Durr J., et al. Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc Natl Acad Sci U S A 1997, 94:13683-13688.
61. Chumnarnsilpa S., Loonchanta A., Xue B., Choe H., Urosev D., Wang H., et al. Calcium ion exchange in crystalline gelsolin. J Mol Biol 2006, 357:773-782.
62. 2+ regulation of gelsolin activity: binding and severing of F-actin. Biophys J 1998, 75:3101-3109.
63. Lind S.E., Smith D.B., Janmey P.A., Stossel T.P. Role of plasma gelsolin and the vitamin-d-binding properties in clearing actin from the circulation. J Clin Invest 1986, 78:736-742.
64. Janmey P.A., Stossel T.P., Lind S.E. Sequential binding of actin monomers to plasma gelsolin and its inhibition by vitamin-d-binding protein. Biochem Biophys Res Commun 1986, 136:72-79.
65. Chaponnier C., Janmey P.A., Yin H.L. The actin filament severing domain of plasma gelsolin. J Cell Biol 1986, 103:1473-1481.
66. Kubo A., Yuba-Kubo A., Tsukita S., Tsukita S., Amagai M. Sentan: a novel specific component of the apical structure of vertebrate motile cilia. Mol Biol Cell 2008, 19:5338-5346.
67. Gautron J., Nys Y. Eggshell matrix proteins. Bioactive egg compounds 2007, 103-108. R. Huopalahti, R. Lopez-Fandino, M. Anton, R. Schade (Eds.).
68. Mann K., Gautron J., Nys Y., McKee M.D., Bajari T., Schneider W.J., et al. Disulfide-linked heterodimeric clusterin is a component of the chicken eggshell matrix and egg white. Matrix Biol 2003, 22:397-407.
69. Ranganathan S., Simpson K.J., Shaw D.C., Nicholas K.R. The whey acidic protein family: a new signature motif and three-dimensional structure by comparative modeling. J Mol Graph 1999, 17:106-113.
70. Xing J., Wellman-Labadie O., Gautron J., Hincke M.T. Recombinant eggshell ovocalyxin-32: expression, purification and biological activity of the glutathione S-transferase fusion protein. Comp Biochem Physiol B Biochem Mol Biol 2007, 147:172-177.
71. Hincke M.T., St Maurice M. Phosphorylation-dependent modulation of calcium carbonate precipitation by chicken eggshell matrix proteins. Chemistry and biology of mineralized tissues 2000, 13-17. American Academy of Orthopaedic Surgeons, Rosemont, IL 60018. M. Goldberg, A. Boskey, C. Robinson (Eds.).
72. 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, 17:615-623.
73. Fischer G., Bang H. The refolding of urea-denaturated ribonuclease A is catalyzed by peptidyl-prolyl cis-trans isomerase. Biochim Biophys Acta 1985, 828:39-42.
74. Fischer G., Wittmannliebold B., Lang K., Kiefhaber T., Schmid F.X. Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 1989, 337:476-478.
75. Hengst U., Albrecht H., Hess D., Monard D. The phosphatidylethanolamine-binding protein is the prototype of a novel family of serine protease inhibitors. J Biol Chem 2001, 276:535-540.
76. Mine Y., D'Silva I. Bioactive components in egg white. Egg bioscience and biotechnology 2008, 141-184. John Wiley & Sons, Hoboken, New Jersey. Y. Mine (Ed.).
77. Herve-Grepinet V., Rehault-Godbert S., Labas V., Magallon T., Derache C., Lavergne M., et al. Purification and characterization of avian beta-defensin 11, an antimicrobial peptide of the hen egg. Antimicrob Agents Chemother 2010, 54:4401-4408.
78. van Dijk A., Veldhuizen E.J.A., Haagsman H.P. Avian defensins. Vet Immunol Immunopathol 2008, 124:1-18.
79. Gautron J., Rehault-Godbert S., Pascal G., Nys Y., Hincke M.T. Ovocalyxin-36 and other LBP/BPI/PLUNC-like proteins as molecular actors of the mechanisms of the avian egg natural defences. Biochem Soc Trans 2011, 39:971-976.
80. Bingle C.D., Seal R.L., Craven C.J. 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.
81. Cordeiro C.M.M., Esmaili H., Ansah G., Hincke M.T. Ovocalyxin-36 is a pattern recognition protein in chicken eggshell membranes. PLoS One 2013, 8.
82. Wellman-Labadie O., Lakshminarayanan R., Hincke M.T. Antimicrobial properties of avian eggshell-specific C-type lectin-like proteins. FEBS Lett 2008, 582:699-704.
83. Rehault-Godbert S., Labas V., Helloin E., Herve-Grepinet V., Slugocki C., Berges M., et al. Ovalbumin-related protein X is a heparin-binding Ov-Serpin exhibiting antimicrobial activities. J Biol Chem 2013, 288:17285-17295.
84. Wu J.P., Acero-Lopez A. Ovotransferrin: structure, bioactivities, and preparation. Food Res Int 2012, 46:480-487.
85. Bourin M., Gautron J., Berges M., Attucci S., Le Blay G., Labas V., et al. Antimicrobial potential of egg yolk ovoinhibitor, a multidomain Kazal-like inhibitor of chicken egg. J Agric Food Chem 2011, 59:12368-12374.