Biosynthesis and Structural Assembly of Eggshell Components

Egg Bioscience and Biotechnology

Volumn , Issue , 2007, Pages 97-128

  Hincke, Maxwell T ^a   Wellman Labadie, Olivier ^a   Mckee, Marc D ^b   Gautron, Joël ^c   Nys, Yves ^c   Mann, Karlheinz ^d  

^a UNIVERSITY OF OTTAWA   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c STATION DE RECHERCHES AVICOLES   (France)

^d MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Eggshell biosynthesis and structural assembly; Eggshell biosynthesis mineralization; Eggshell proteomics

Indexed keywords

EID: 84890649475     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470181249.ch2     Document Type: Chapter

References (106)

1. Abatangelo G, Daga-Gordini D, Castellani I, Cortivo R (1978). Some observations on the calcium ion binding to the eggshell matrix. Calc Tissue Res 26: 247-252.
2. Ahmed AM, Rodriguez A, Vidal ML, Gautron J, Garcia-Ruiz JM, Nys Y (2003). Effect of moult on eggshell quality. Br Poultry Sci 44: 782-793.
3. Ahmed AM, Rodriguez-Navarro AB, Vidal ML, Gautron J, Garcia-Ruiz JM, Nys Y (2005). Changes in eggshell mechanical properties, crystallographic texture and in matrix proteins induced by moult in hens. Br Poultry Sci 46: 268-279.
4. Arias JL, Jure C, Wiff JP, Fernandez MS, Fuenzalida V, Arias JL (2002). Effect of sulfate content of biomacromolecules on the crystallization of calcium carbonate. Mater Res Soc Symp Proc 711: 243-248.
5. Arias JL, Nakamura O, Fernandez MS, Wu JJ, Knigge P, Eyre DR, Caplan AI (1997). Role of type X collagen on experimental mineralization of eggshell membranes. Connect Tissue Res 36: 21-33.
6. Arias JL, Fink DJ, Xiao SQ, Heuer AH, Caplan AI (1993). Biomineralization and eggshells: Cell-mediated acellular compartments of mineralized extracellular matrix. Int Rev Cytol 45: 217-250.
7. Arias JL, Carrino DA, Fernandez MS, Rodriguez JP, Dennis JE, Caplan AI (1992). Partial biochemical and immunochemical characterization of avian eggshell extracellular matrices. Arch Biochem Biophys 298: 203-302.
8. Arias JL, Fernandez MS, Dennis JE, Caplan AI (1991). Collagens of the chicken eggshell membranes. Connect Tissue Res 26: 37-45.
9. Arthur M, Depardieu F, Snaith HA, Reynolds PE, Courvalin P (1994). Contribution of VanY D,D,-carboxypeptidase to glycopeptide resistance in Enterococcus faecalis by hydrolysis of peptidoglycan precursors. Antimicrob. Agents Chemother 38 (9): 1899-1903.
10. Beamer LJ, Carroll SF, Eisenberg D (1997). Crystal structure of human BPI and two bound phospholipids at 2.4 angstrom resolution. Science 276 (5320): 1861-1864.
11. Belcher AM, Wu XH, Christensen RJ, Hansma PK, Stucky GD, Morse DE (1996). Control of crystal phase switching and orientation by soluble mollusc-shell proteins. Nature 381: 56-58.
12. Bera A, Herbert S, Jakob A, Vollmer W, Gotz F (2005). Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol Microbiol 55: 778-787.
13. Bingle CD, Craven CJ (2004). Meet the relatives: a family of BPI-and LBP-related proteins. Trends Immunol 25: 53-55.
14. Burgess SC (2003). Proteomics in the chicken: Tools for understanding immune responses to avian disease. Poultry Sci 83: 552-573.
15. Burley RW, Vadehra DV (1989). The Avian Egg. Chemistry and Biology. New York : Wiley-Interscience.
16. Burt DW (2005). Chicken genome: The current status and future opportunities. Genome Res 15: 1692-1698.
17. Chowdhury SD (1990). Shell membrane system in relation to latyrogen and copper deficiency. World' s Poultry Sci J 46: 153-169.
18. Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ (2003). Trans-shell infection by pathogenic micro-organisms reduces the shelf life of non-incubated bird' s eggs: A constraint on the onset of incubation? Proc Roy Soc Lond B 270: 2233-2240.
19. Cortivo R, Castellani I, Martelli M, Michelotto G, Abatangelo G (1982). Chemical characterization of the hen eggshell matrix: isolation of an alkali-resistant peptide. J Chromatogr 237: 127-135.
20. Corzo A, Kidd MT, Pharr GT, Burgess SC (2004). Initial mapping of the chicken blood plasma proteome. Int J Poultry Sci 3: 157-162.
21. Deeming DC (2002). Avian Incubation: Behaviour, Environment, and Evolution. New York: Oxford Univ Press.
22. Dennis JE, Xiao S-Q, Agarwal M, Fink DJ, Heuer AH, Caplan AI (1996). Microstructure of matrix and mineral components of eggshells from white leghorn chickens (Gallus gallus). J Morphol 228: 287-306.
23. De Reggi M, Gharib B (2001). Protein-X, pancreatic stone -, pancreatic thread -, reg - protein, P19, lithostathine, and now what? Characterization, structural analysis and putative function(s) of the major non-enzymatic protein of pancreatic secretions. Curr Protein Peptide Sci 2: 19-42.
24. Doherty MK, McLean L, Hayter JR, Pratt JM, Robertson DHL, El-Shafei A, Gaskell SJ, Benyon RJ (2004). The proteome of chicken skeletal muscle: Changes in soluble protein expression during growth in a layer strain. Proteomics 4: 2082-2093.
25. Dominguez-Vera JM, Gautron J, Garcia-Ruiz, JM, Nys Y (2000). The effect of avian uterine fluid on the growth behavior of calcite crystals. Poultry Sci 79: 901-907.
26. Dunn IC, Joseph NT, Milona P, Bain M, Edmond A, Wilson PW, Nys Y, Gautron J, Schmutz M, Preisinger R, Waddington D (2007). Polymorphisms in eggshell organic matrix genes are associated with eggshell quality measurements in pedigree Rhode Island Red hens (manuscript submitted).
27. Ewart KV, Fletcher GL (1993). Herring antifreeze protein: primary structure and evidence for a C-type lectin evolutionary origin. Mol Marine Biol Biotechnol 2 (1): 20-27.
28. Fernandez MS, Araya M, Arias JL (1997). Eggshells are shaped by a precise spatio - temporal arrangement of sequentially deposited macromolecules. Matrix Biol 16: 13-20.
29. Fernandez MS, Escobar C, Lavelin I, Pines M, Arias JL (2003). Localization of osteopontin in oviduct tissue and eggshell during different stages of the avian egg laying cycle. J Struct Biol 143: 171-180.
30. Fernandez MS, Moya A, Lopez L, Arias JL (2001). Secretion pattern, ultrastructural localization and function of extracellular matrix molecules involved in eggshell formation. Matrix Biol 19: 793-803.
31. Garcillán DA, Gómez-Esquer F, Diaz-Gil G, Martinez-Arribas F, Delcán J, Schneider J, Palomar MA, Linares R (2005). Proteomic analysis of the Gallus gallus embryo at stage-29 of development. Proteomics 5: 4946-4957.
32. Gautron J, Murayama E, Vignal A, Morisson M, McKee MD, Rehault S, Labas V, Belghazi M, Vidal ML, Nys Y, Hincke MT (2007). Cloning of ovocalyxin-36, a novel chicken eggshell protein related to lipopolysaccharide-binding proteins (LPB) bactericidal permeability-increasing proteins (BPI), and PLUNC family proteins. J Biol Chem (Epub ahead of print).
33. Gautron J, Rodriguez-Navarro AB, Gomez-Morales J, Hernandez-Hernandez MA, Dunn IC, Bain M, Garcia-Ruiz JM, Nys Y (2005). Evidence for the implication of chicken eggshell matrix proteins in the process of shell mineralization. Proc 9th Int Symp Biomineralization (Biom 09). Pucon, Chile.
34. Gautron J, Hincke MT, Panheleux M, Bain M, McKee MD, Solomon SE, Nys Y (2001a). Ovocalyxin-32, a novel chicken eggshell matrix protein. Isolation, amino acid sequencing, cloning, and immunocytochemical localization. J Biol Chem 276 (42): 39243-39252.
35. Gautron J, Hincke MT, Panheleux M, Garcia-Ruiz JM, Boldicke T, Nys Y (2001b). Ovotransferrin is a matrix protein of the hen eggshell membranes and basal calcified layer. Connect Tissue Res 42 (4): 255-267.
36. Gautron J., Hincke MT, Nys Y (1997). Precursor matrix proteins in the uterine fluid change with stages of eggshell formation in hens. Connect Tissue Res 36: 195-210.
37. Gautron J, Bain M, Solomon S, Nys Y (1996). S oluble matrix of hen's eggshell extracts changes in vitro the rate of calcium carbonate precipitation and crystal morphology. Br Poultry Sci 37: 853-866.
38. Ghim S-Y, Choi S-K, Shin B-S, Jeong Y-M, Sorokin A, Ehrlich SD, Park S-H (1998). Sequence analysis of the Bacillus subtilis 168 chromosome region between the ssp C and odh A loci (184 °-180 °). DNA Res 5: 195-201.
39. Guerin-Dubiard C, Pasco M, Molle D, Desert C, Croguennec T, Nau F (2006). Proteomic analysis of hen egg white. J Agric Food Chem 54 (11): 3901-3910.
40. Hagiwara K, Kikuchi T, Endo Y, Huqun Usui K, Takahashi M, Shibata N, Kusakabe T, Xin H, Hoshi S, Miki M, Inooka N, Tokue Y, Nukiwa T (2003). Mouse SWAM1 and SWAM2 are antibacterial proteins composed of a single whey acidic protein motif. J Immunol 170: 1973-1979.
41. Hamilton RMG (1986). The microstructure of the hens egg-shell-a short review. Food Microstruct 5: 99-110.
42. Hincke MT, Gautron J, Mann K, Panhéleux M, McKee MD, Bain M, Solomon SE, Nys Y (2003). Purification of ovocalyxin-32, a novel chicken eggshell matrix protein. Connect Tissue Res 44 (1): 16-19.
43. Hincke MT, Gautron J, Panhéleux M, Garcia-Ruiz J, McKee MD, Nys Y (2000a). Identification and localization of lysozyme as a component of eggshell membranes and eggshell matrix. Matrix Biol 19: 443-453.
44. Hincke MT, St. Maurice M, Nys Y, Gautron J, Panheleux M, T sang CPW, Bain MM, Solomon SE, McKee MD (2000b). Eggshell proteins and shell strength: Molecular biology of eggshell matrix proteins and industry applications. In: Sim JS, Nakai S, Guenter W, eds. Egg Nutrition and Newly Emerging Ovo-Bio Technologies. New York: CABI Publishing; pp 447-462.
45. Hincke MT, St. Maurice M (2000). Phosphorylation-dependent modulation of calcium carbonate precipitation by chicken eggshell matrix proteins. In: Goldberg M, Boskey A, Robinson C, eds. Chemistry and Biology of Mineralized Tissues. Rosemont, IL: American Academy of Orthopaedic Surgeons; pp 13-17.
46. Hincke MT, Gautron J, Tsang CPW, McKee MD, Nys Y (1999). Molecular cloning and ultrastructural localization of the core protein of an eggshell matrix proteoglycan, Ovocleidin-116. J Biol Chem 274: 32915-32923.
47. Hincke MT (1995). Ovalbumin is a component of the chicken eggshell matrix. Connect Tissue Res 31: 227-233.
48. Hincke MT, Tsang CPW, Courtney M, Hill V, Narbaitz R (1995). Purification and Immunochemistry of a soluble matrix protein of the chicken eggshell (Ovocleidin 17). Calc Tissue Int 56: 578-583.
49. Hincke MT, Bernard A-M, Lee ER, Tsang CPW, Narbaitz R (1992). Soluble protein constituents of the domestic fowl' s eggshell. Br Poultry Sci 33: 505-516.
50. Huang S-Y, Lin J-H, Chen Y-H, Chuang C-K, Chiu Y-F, Chen M-Y, Chen H-H, Lee W-C (2006). Analysis of chicken serum proteome and differential protein expression during development in single-comb White Leghorn hens. Proteomics 6: 2217-2224.
51. Hubacek JA, Buchler C, Aslanidis C, Schmitz G (1997). The genomic organization of the genes for human lipopolysaccharide binding protein (LBP) and bactericidal permeability increasing protein (BPI) is highly conserved. Biochem Biophys Res Commun 236 (2): 427-430.
52. Hunter GK, Szigety SK (1992). Effects of proteoglycan on hydroxyapatite formation under non-steady-state and pseudo-steady-state conditions. Matrix 12: 362-368.
53. Hunter GK (1991). Role of proteoglycan in the provisional calcification of cartilage. A review and reinterpretation. Clin Orthop Related Res 262: 256-280.
54. International Chicken Genome Sequencing Consortium (2004). Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695-716.
55. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M (2005). Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteom 4: 1265-1272.
56. Jimenez-Lopez C, Rodríguez-Navarro A, Domingez-Vera JM, Garcia-Ruiz JM (2003). Influence of lysozyme on the precipitation of calcium carbonate. Kinetic and morphological study. Geochim Cosmochim Acta 67: 1667-1676.
57. Kawasaki K, Weiss KM (2006). Evolutionary genetics of vertebrate tissue mineralization: the origin and evolution of the secretory calcium-binding phosphoprotein family. J Exper Zool Pt B Mol Devel Evol 306 (3): 295-316.
58. Lakshminarayanan R, Kini RM, Valiyaveettil S (2002). Investigation of the role of ansocalcin in the biomineralization in goose eggshell matrix. Proc Nat Acad Sci USA 99: 5155-5159.
59. Lakshminarayanan R, Valiyaveettil S, Roa VS, Kini RM (2003). Purification, characterization, and in vitro mineralization studies of a novel goose eggshell matrix protein, ansocalcin. J Biol Chem 278: 2928-2936.
60. Lakshminarayanan R, Joseph JS, Kini RM, Valiyaveettil S (2005). Structure-function relationship of avian eggshell matrix proteins: A comparative study of two major eggshell matrix proteins, ansocalcin and OC-17. Biomacromolecules 6: 741-751.
61. Liu Q, Yu L, Gao J, Fu Q, Zhang J, Zhang P, Chen J, Zhao S (2000). Cloning, tissue expression pattern and genomic organization of latexin, a human homologue of rat carboxypeptidase A inhibitor. Mol Biol Rep 27: 241-246.
62. Mann K, Olsen JV, Macek B, Gnad F, Mann M (2007). Phosphoproteins of the chicken eggshell calcified layer. Proteomics 7: 106-115.
63. Mann K, Siedler F (2006). Amino acid sequences and phosphorylation sites of emu and rhea eggshell C-type lectin-like proteins. Compar Biochem Physiol Pt B 143: 160-170.
64. Mann K, Macek B, Olsen JV (2006). Proteomic analysis of the acid-soluble organic matrix of the chicken calcified eggshell layer. Proteomics 6: 3801-3810.
65. Mann K (2004). Identification of major proteins of the organic matrix of the emu (Dromaius novaehollandiae) and rhea (Rhea americanus) eggshell calcified layer. Br Poultry Sci 45: 483-490.
66. Mann K, Siedler F (2004). Ostrich (Struthio camelus) eggshell matrix contains two different C-type lectin-like proteins. Isolation, amino acid sequence and posttranslational modifications. Biochim Biophys Acta 1696: 41-50.
67. Mann K, Gautron J, Nys Y, McKee MD, Bajari T, Schneider WJ, Hincke MT (2003). Disulfide-linked heterodimeric clusterin is a component of the chicken eggshell matrix and egg white. Matrix Biol 22 (5): 397-407.
68. Mann K (1999). Isolation of a glycosylated form of the eggshell protein ovocleidin and determination of the glycosylation site. Alternative glycosylation/phosphorylation at an N-glycosylation sequon. FEBS Lett 463: 12-14.
69. Mann K, Siedler F (1999). The amino acid sequence of ovocleidin-17, a major protein of the avian eggshell calcified layer. Biochem Mol Biol J 47: 997-1007.
70. Mann M, Ong S, Grønborg M, Steen H, Jensen ON, Pandey A (2002). Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome . Trends Biotechnol 20: 261-268.
71. Mann M, Hendrickson RC, Pandey A (2001). Analysis of proteins and proteomes by mass spectrometry. Annu Rev Biochem 70: 437-473.
72. McKee MD, Nanci A (1996). Osteopontin at mineralized tissue interfaces in bone, teeth, and osseointegrated implants: Ultrastructural distribution and implications for mineralized tissue formation, turnover, and repair. Microsc Res Tech 33: 141-164.
73. McKee MD, Nanci A (1995). Osteopontin and the bone remodeling sequence. Ann NY Acad Sci 760: 177-189.
74. McKee MD, Nanci A, Khan SR (1995). Ultrastructural immunodetection of osteopontin and osteocalcin as major matrix components of renal calculi. J Bone Mineral Res 10: 1913-1929.
75. Mine Y, Oberle C, Kassaify Z (2003). Eggshell matrix proteins as defence mechanism of avian eggs. J Agric Food Chem 51: 249-253.
76. Narbaitz R, Bastani B, Galvin NJ, Kapal VK, Levine DZ (1995). Ultrastructural and immunocytochemical evidence for the presence of polarised plasma membrane H(+)-ATPase in two specialised cell types in the chick embryo chorioallantoic membrane. J Anat 186 (Pt 2): 245-252.
77. Nys Y, Gautron J, Garcia-Ruiz JM, Hincke MT (2004). A vian eggshell mineralization: Biochemical and functional characterization of matrix proteins. CR Paleovol 3: 549-562.
78. Nys Y, Gautron J, McKee MD, Garcia-Ruiz JM, Hincke MT (2001). Biochemical and functional characterisation of eggshell matrix proteins in hens. World' s Poultry Sci J 57: 401-413.
79. Nys Y, Hincke M, Arias JL, Garcia-Ruiz JM, Solomon S (1999). Avian eggshell mineralization . Poultry Avian Biol Rev 10: 143-166.
80. Nys Y, Zawadzki J, Gautron J, Mills AD (1991). Whitening of brown-shelled eggs: Mineral composition of uterine fluid and rate of protoporphyrin deposition. Poultry Sci 70: 1236-1245.
81. Panheleux M, Nys Y, Williams J, Gautron J, Boldicke T, Hincke MT (2000). Extraction and quatification of eggshell matrix proteins (ovocleidins, ovalbumin, ovotransferrin) in shell from young and old hens. Poultry Sci 79: 580-588.
82. Panheleux M, Bain M, Fernandez MS, Morales I, Gautron J, A rias JL, Solomon SE, Hincke M, Nys Y (1999). Organic matrix composition and ultra-structure of eggshell: A comparative study. Br Poultry Sci 40: 240-252.
83. Parada C, Gato A, Aparicio M, Bueno D (2006). Proteome analysis of chick embryonic cerebrospinal fluid. Proteomics 6: 312-320.
84. Parsons AH (1982). Structure of the eggshell. Poultry Sci 61: 2013-2021.
85. Pines M, Knopov V, B ar A (1994). Involvement of osteopontin in egg shell formation in the laying chicken. Matrix Biol 14: 765-771.
86. Reyes-Grajeda JP, Moreno A, Romero A (2004). Crystal structure of ovocleidin-17, a major protein of the calcified Gallus gallus eggshell: Implications in the calcite mineral growth pattern. J Biol Chem 279: 40876-40881.
87. Robey PG (1996) Vertebrate mineralized matrix proteins: Structure and function. Connect Res Tissue 35 (1-4): 131-136.
88. Silphaduang U, Hincke MT, Nys Y, Mine Y (2006). Antimicrobial proteins in chicken reproductive system. Biochem Biophys Res Commun 340: 648-655.
89. Sparks NHC (1994). Shell accessory materials: Structure and function. In: Board RG, Fuller R, eds. Microbiology of the Avian Egg. London: Chapman & Hall.
90. Sparks NHC, Board RG (1984). Cuticle, shell porosity and water intake through hen' s eggshells. Br Poultry Sci 25: 267-276.
91. Steen H, Mann M (2004). The ABC' s (and XYZ' s) of peptide sequencing. Nat Rev/Mol Cell Biol 5: 699-711.
92. Uratani Y, Takiguchi-Hayashi K, Miyasaka N, Sato M, Jin M, Arimatsu Y (2000). Latexin, a carboxypeptidase A inhibitor, is expressed in rat peritoneal mast cells and is associated with granular structures distinct from secretory granules and lysosomes . Biochem J 346: 817-1826.
93. Vadehra DV, Baker RC, Naylor HB (1972). Distribution of lysozyme activity in the exteriors of eggs from Gallus gallus. Compar Biochem Biophys B 43: 503-508.
94. Valenti P, De Stasio A, Mastromerino P, Seganti L, Sinibaldi L, Orsi N (1981). Influence of bicarbonate and citrate on the bacteriostatic action of ovotransferrin towards staphylococci. FEMS Microbiol Lett 10: 77-79.
95. van Dijk A, Veldhuizen EJA, van Asten AJAM, Haagsman HP (2005). CMAP27, a novel chicken cathelicidin-like antimicrobial protein. Vet Immunol Immunopathol 106: 321-327.
96. von Hunolstein C, Ricci ML, Valenti P, Orefici G (1992). Lack of activity of transferrins towards Streptococcus spp. Med Microbiol Immunol 181: 351-357.
97. Watanabe H, Yamada Y, Kimata K (1998). Roles of aggrecan, a large chondroitin sulfate proteoglycan, in cartilage structure and function. J Biochem 124: 687-693.
98. Wellman-Labadie O, Picman J, Hincke MT (2007a). Antimicrobial activity of cuticle and outer eggshell protein extracts from three species of domestic fowl. Br Poult Sci (in revision).
99. Wellman-Labadie O, Picman J, Hincke MT (2007b). Antimicrobial activity of the anseriform outer eggshell and cuticle (submitted).
100. th ed. San Diego: Academic Press.
101. Wong M, Hendrix MJC, Von der Mark K, Little C, Stern R (1984). Collagen in the egg shell membranes of the hen. Devel Biol 104: 28-36.
102. Xiao Y, Cai Y, Bommineni YR, Fernando SC, Prakash O, Gilliland SE, Zhang G (2006). Identification and functional characterization of three chicken cathelicidins with potent antimicrobial activity. J Biol Chem 281: 2858-2867.
103. Xiao Y, Hughes AL, Ando J, Matsuda Y, Cheng J-F, Skinner-Noble D, Zhang G (2004). A genome-wide screen identifies a single ß-defensin gene cluster in the chicken: Implications for the origin and evolution of mammalian defensins. BioMed Central Genom 5: 56.
104. Xing J, Wellman-Labadie O, Gautron J, Hincke MT (2007). Recombinant eggshell ovocalyxin-32: Expression, purification and biological activity of the glutathione S-transferase fusion protein. Compar Biochem Physiol (in press).
105. Yang KT, Lin CY, Liou JS, Fan YH, Chiou SH, Huang CW, Wu CP, Lin EC, Chen CF, Lee YP, Lee WC, Ding ST, Cheng WT, Huang MC (2007) Differentially expressed transcripts in shell glands from low and high egg production strains of chickens using cDNA microarrays. Anim Reprod Sci (Epub ahead of print Sept 9, 2006).
106. Yoshimura Y, Ohashi H, Subedi K, Nishibori M, Isobe N (2006). Effects of age, egg - laying activity, and salmonella-inoculatioon on the expressions of gallinacin mRNA in the vagina of the hen oviduct. J Reprod Devel 52: 211-218.