The role of matrix proteins in eggshell formation

Journal of Poultry Science

Volumn 47, Issue 3, 2010, Pages 208-219

  Hincke, Maxwell T ^a   Nys, Yves ^b   Gautron, Joel ^b  

^a UNIVERSITY OF OTTAWA   (Canada)

^b STATION DE RECHERCHES AVICOLES   (France)

Author keywords

Calcite; Eggshell; Osteopontin; Ovocalyxin; Ovocleidin

Indexed keywords

EID: 77955066615     PISSN: 13467395     EISSN: 13490486     Source Type: Journal    
DOI: 10.2141/jpsa.009122     Document Type: Review

References (91)

1. Abatangelo G, Daga-Gordini D, Castellani I and Cortivo R. Some observations on the calcium ion binding to the eggshell matrix. Calcified Tissue Research, 26: 247-252. 1978.
2. Ahmed AM, Rodriguez-Navarro AB, Vidal ML, Gautron J, Garcia-Ruiz JM and Nys Y. Changes in eggshell mechanical properties, crystallographic texture and in matrix proteins induced by moult in hens. British Poultry Science, 46: 268-279. 2005.
3. Arazi H, Yoselewitz I, Malka Y, Kelner Y, Genin O and Pines M. Osteopontin and calbindin gene expression in the egg-shell gland as related to eggshell abnormalities. Poultry Science, 88: 647-53. 2009.
4. Arias JL, Fernandez MS, Dennis JE and Caplan AI. Collagens of the chicken eggshell membranes. Connective Tissue Research, 26: 37-45. 1991.
5. Arias JL, Fink DJ, Xiao SQ, Heuer AH and Caplan AI. Biomineralization and eggshells: cell-mediated acellular compartments of mineralized extracellular matrix. International Review of Cytology, 45: 217-250. 1993.
6. Arias JL, Jure C, Wiff JP, Fernandez MS, Fuenzalida V and Arias JL. Effect of sulfate content of biomacromolecules on the crystallization of calcium carbonate. Materials Research Society Symposium Proceedings, 711: 243-248. 2002.
7. Arias JL, Nakamura O, Fernandez MS, Wu JJ, Knigge P, Eyre DR, Caplan AI. Role of type X collagen on experimental mineralization of eggshell membranes. Connective Tissue Research, 36: 21-33. 1997.
8. Bar, A. Differential regulation of calbindin in the calcium-transporting organs of birds with high calcium requirements. Japanese Poultry Science, 46: 267-285. 2009.
9. Belcher AM, Wu XH, Christensen RJ, Hansma PK, Stucky GD and Morse DE. Control of crystal phase-switching and orientation by soluble shell proteins. Nature, 381: 56-58. 1996.
10. Bingle CD and Craven CJ. Meet the relatives: a family of BPI-and LBP-related proteins. Trends in Immunology, 25: 53-55. 2004.
11. Burley RW and Vadehra DV. The Avian Egg. Chemistry and Biology. Wiley Interscience. New York. 1989.
12. Carrino DA, Rodriquez JP and Caplan AI. Dermatan sulfate proteoglycans from the mineralized matrix of the avian eggshell. Connective Tissue Research, 36: 175-193. 1997.
13. Chien YC, Hincke MT and McKee MD. Avian eggshell structure and osteopontin. Cells, Tissue, Organs, 189: 38-43. 2009.
14. Chien YC, Hincke MT, Vali H and McKee MD. Ultrastructural matrix-mineral relationships in avian eggshell, and effects of osteopontin on calcite growth in vitro. Journal of Structural Biology, 163: 84-99. 2008.
15. Chowdhury SD. Shell membrane system in relation to latyrogen and copper deficiency. World's Poultry Science Journal, 46: 153-169. 1990.
16. Cortivo R, Castellani I, Martelli M, Michelotto G and Abatangelo G. Chemical characterization of the hen egg-shell matrix: isolation of an alkali-resistant peptide. Journal of Chromatography, 237: 127-135. 1982.
17. D'Ambrosio C, Arena S, Scaloni A, Guerrier L, Boschetti E, Mendieta ME, Citterio A and Righetti PG. Exploring the Chicken Egg White Proteome with Combinatorial Peptide Ligand Libraries. Journal of Proteome Research, 7: 3461-3474. 2008.
18. Deeming DC. Avian Incubation: Behavior, Environment, and Evolution. Oxford University Press. New York. 2002.
19. Dennis JE, Xiao S-Q, Agarwal M, Fink DJ, Heuer AH and Caplan AI. Microstructure of matrix and mineral components of eggshells from white leghorn chickens (Gallus gallus). Journal of Morphology, 228: 287-306. 1996.
20. Dominguez-Vera JM, Gautron J, Garcia-Ruiz J and Nys Y. The effect of avian uterine fluid on the growth behavior of calcite crystals. Poultry Science, 79: 901-907. 2000.
21. Dunn IC, Joseph NT, Bain M, Edmond A, Wilson PW, Milona P, Nys Y, Gautron J, Schmutz M, Preisinger R and Waddington D. Polymorphisms in eggshell organic matrix genes are associated with eggshell quality measurements in pedigree Rhode Island Red hens. Animal Genetics, 40: 110-114. 2008.
22. Dunn IC, Wilson PW, Lu Z, Bain MM, Crossan CL, Talbot RT and Waddington D. New hypotheses on the function of the avian shell gland derived from microarray analysis comparing tissue from juvenile and sexually mature hens. General and Comparative Endocrinology, 163: 225-232. 2009.
23. Falini G, Albeck S, Weiner S and Addadi L. Control of aragonite or calcite polymorphism by mollusk shell macromolecules. Science, 271: 67-69. 1996.
24. Farinazzo A, Restuccia U, Bachi A, Guerrier L, Fortis F, Boschetti E, Rasoli E, Citterio A and Righetti PG. Chicken egg yolk cytoplasmic proteome, mined via combinatorial peptide ligand libraries. Journal of Chromatography A, 1216: 1241-1252. 2009.
25. Fernandez MS, Araya M and Arias JL. Eggshells are shaped by a precise spatio-temporal arrangement of sequentially deposited macromolecules. Matrix Biology, 16: 13-20. 1997.
26. Fernandez MS, Escobar C, Lavelin I, Pines M and Arias JL. Localization of osteopontin in oviduct tissue and eggshell during different stages of the avian egg laying cycle. Journal of Structural Biology, 143: 171-180. 2003.
27. Fernandez MS, Moya A, Lopez L and Arias JL. Secretion pattern, ultrastructural localization and function of extracellular matrix molecules involved in eggshell formation. Matrix Biology, 19: 793-803. 2001.
28. Gautron J, Bain M, Solomon S and Nys Y. Soluble matrix of hen's eggshell extracts changes in vitro the rate of calcium carbonate precipitation and crystal morphology. British Poultry Science, 37: 853-866. 1996.
29. Gautron J, Hincke MT and Nys Y. Precursor matrix proteins in the uterine fluid change with stages of eggshell formation in hens. Connective Tissue Research, 36: 195-210. 1997.
30. Gautron J, Hincke MT, Panheleux M, Bain M, McKee MD, Solomon SE and Nys Y. Ovocalyxin-32, a novel chicken eggshell matrix protein. Isolation, amino acid sequencing, cloning, and immunocytochemical localization. Journal of Biological Chemistry, 276: 39243-39252. 2001a.
31. Gautron J, Hincke MT, Panheleux M, Garcia-Ruiz JM, Boldicke T and Nys Y. Ovotransferrin is a matrix protein of the hen eggshell membranes and basal calcified layer. Connective Tissue Research, 42: 255-267. 2001b.
32. Gautron J, Murayama E, Vignal A, Morisson M, McKee MD, Rehault S, Labas V, Belghazi M, Vidal ML, Nys Y and Hincke MT. Cloning of Ovocalyxin-36, a novel chicken eggshell protein related to lipopolysaccharide-binding proteins (LPB) bactericidal permeability-increasing proteins (BPI), and Plunc family proteins. Journal of Biological Chemistry, 282: 5273-5286. 2007.
33. Gautron J and Nys Y. Eggshell matrix proteins. In: Bioactive egg compounds. (Huopalahti R, Lopez-Fandino R, Anton M and Schade R eds.) pp. 103-108. Springer-Verlag. 2007.
34. Gautron J, Rodriguez-Navarro AB, Gomez-Morales J, Hernandez-Hernandez MA, Dunn IC, Bain M, Garcia-Ruiz JM and Nys Y. Evidence for the implication of chicken eggshell matrix proteins in the process of shell mineralization. In: Proceeding of the 9th international symposium on biomineralization (Biom 09). Pucon. Chile. 2005.
35. Harris ED, Blount JE and Leach RM Jr. Localization of lysyl oxidase in hen oviduct: implications in egg shell membrane formation and composition. Science, 208: 55-56. 1980.
36. Hernandez-Hernandez A, Gomez-Morales J, Rodriguez-Navarro AB, Gautron J, Nys Y and Garcia-Ruiz JM. Identification of some active proteins in the process of hen eggshell formation. Crystal Growth & Design, 8: 4330-4339. 2008.
37. Hincke MT. Ovalbumin is a component of the chicken eggshell matrix. Connective Tissue Research, 31: 227-233. 1995.
38. Hincke MT, Bernard A-M, Lee ER, Tsang CPW and Narbaitz R. Soluble protein constituents of the domestic fowl's egg-shell. British Poultry Science, 33: 505-516. 1992.
39. Hincke MT, Chien YC, Gerstenfeld LC and McKee MD. Colloidal-gold immunocytochemical localization of osteo-pontin in avian eggshell gland and eggshell. Journal of Histochemistry and Cytochemistry, 56: 467-476. 2008b.
40. Hincke MT, Gautron J, Mann K, Panheleux M, McKee MD, Bain M, Solomon SE and Nys Y. Purification of Ovocalyxin-32, a novel chicken eggshell matrix protein. Connective Tissue Research, 44: 16-19. 2003.
41. Hincke MT, Gautron J, Panheleux M, Garcia-Ruiz J, McKee MD and Nys Y. Identification and localization of lysozyme as a component of eggshell membranes and eggshell matrix. Matrix Biology, 19: 443-453. 2000.
42. Hincke MT, Gautron J, Tsang CPW, McKee MD and Nys Y. Molecular cloning and ultrastructural localization of the core protein of an eggshell matrix proteoglycan, Ovocleidin-116. Journal of Biological Chemistry, 274: 32915-32923. 1999.
43. Hincke MT and St Maurice M. Phosphorylation-dependent modulation of calcium carbonate precipitation by chicken egg-shell matrix proteins. In: Chemistry and Biology of Mineralized Tissues (Goldberg M, Boskey A, Robinson C eds) pp. 13-17. American Academy of Orthopaedic Surgeons. Rosemont, IL. 2000.
44. Hincke MT, Tsang CPW, Courtney M, Hill V and Narbaitz R. Purification and Immunochemistry of a soluble matrix protein of the chicken eggshell (Ovocleidin 17). Calcified Tissue International, 56: 578-583. 1995.
45. Hincke MT, Wellman-Labadie O, McKee MD, Gautron J, Nys Y and Mann K. Biosynthesis and structural assembly of eggshell components. In: Egg Bioscience and Biotechnology, (Mine Y. ed.). pp. 97-128. John Wiley and Sons. Hoboken. 2008a.
46. Horvat-Gordon M, Yu F, Burns D and Leach Jr R M Ovocleidin (OC 116) is present in avian skeletal tissues. Poultry Science, 87: 1618-1623. 2008.
47. International Chicken Genome Sequencing Consortium. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature, 432: 695-716. 2004.
48. Jimenez-Lopez C, Rodriguez-Navarro A, Domingez-Vera JM and Garcia-Ruiz JM. Influence of lysozyme on the precipitation of calcium carbonate. Kinetic and morphological study. Geochimica Cosmochimica Acta, 67: 1667-1676. 2003.
49. Jonchere V, Rehault-Godbert S, Hennequet-Antier C, Cabau C, Sibut V, Cogburn LA, Nys Y and Gautron J. Gene expression profiling to identify eggshell proteins involved in physical defense of the chicken egg. BMC Genomics, 11: 57. 2010.
50. Kamata R, Shiraishi F, Izumi T, Takahashi S, Shimizu A, Shiraishi H. Mechanisms of estrogen-induced effects in avian reproduction caused by transovarian application of a xenoestrogen, diethylstilbestrol. Archives of Toxicology, 83: 161-171. 2009.
51. Kawasaki K and Weiss K. Mineralized tissue and vertebrate evolution: the secretory calcium-binding phosphoprotein gene cluster. Proceedings of the National Academy of Science of the United States of America, 100: 4060-4065. 2003.
52. Kawasaki K and Weiss K. Evolutionary genetics of vertebrate tissue mineralization: the origin and evolution of the secretory calcium-binding phosphoprotein family. Journal of Experimental Zoology B, Molecular Development and Evolution, 306: 295-316. 2006.
53. Lakshminarayanan R, Joseph JS, Kini RM and Valiyaveettil S. Structure-function relationship of avian eggshell matrix proteins: a comparative study of two major eggshell matrix proteins, ansocalcin and OC-17. Biomacromolecules, 6: 741-51. 2005.
54. Lakshminarayanan R, Kini RM and Valiyaveettil S. Investigation of the role of ansocalcin in the biomineralization in goose eggshell matrix. Proceedings of the National Academy of Science of the United States of America, 99: 5155-5159. 2002.
55. Lakshminarayanan R, Valiyaveettil S, Roa VS and Kini RM. Purification, characterization, and in vitro mineralization studies of a novel goose eggshell matrix protein, ansocalcin. Journal of Biological Chemistry, 278: 2928-2936. 2003.
56. Lavelin I, Yarden N, Ben-Bassat S, Bar A and Pines M. Regulation of osteopontin gene expression during egg shell formation in the laying hen by mechanical strain. Matrix Biology, 17: 615-623. 1998.
57. Mann K. Isolation of a glycosylated form of the eggshell protein Ovocleidin and determination of the glycosylation site. Alternative glycosylation/phosphorylation at an Nglycosylation sequon. FEBS Letters, 463: 12-14. 1999.
58. Mann K. The chicken egg white proteome. Proteomics, 7: 3558-3568. 2007.
59. Mann K. Proteomic analysis of the chicken egg vitelline membrane. Proteomics, 8: 2322-2332. 2008.
60. Mann K, Gautron J, Nys Y, McKee MD, Bajari T, Schneider WJ and Hincke MT. Disulfide-linked heterodimeric clusterin is a component of the chicken eggshell matrix and egg white. Matrix Biology, 22: 397-407. 2003.
61. Mann K, Hincke MT and Nys Y Isolation of Ovocleidin-116 from chicken eggshells, correction of its amino acid sequence and identification of disulfide bonds and glycosylated Asn. Matrix Biology, 21: 383-387. 2002.
62. Mann K, Maček B and Olsen JV. Proteomic analysis of the acid-soluble organic matrix of the chicken calcified eggshell layer. Proteomics, 6: 3801-3810. 2006.
63. Mann K and Mann M. The chicken egg yolk plasma and granule proteomes. Proteomics, 8: 178-191. 2008.
64. Mann K, Olsen JV, Macek B, Gnad F and Mann M. Phospho-proteins of the chicken eggshell calcified layer. Proteomics, 7: 106-115. 2007.
65. Mann K and Siedler F. The amino acid sequence of Ovocleidin-17, a major protein of the avian eggshell calcified layer. Biochemistry and Molecular Biology Journal, 47: 997-1007. 1999.
66. Mann K and Siedler F. Ostrich (Struthio camelus) eggshell matrix contains two different C-type lectin-like proteins. Isolation, amino acid sequence and posttranslational modifications. Biochimica Biophysica Acta, 1696: 41-50. 2004.
67. Mann K and Siedler F. Amino acid sequences and phosphorylation sites of emu and rhea eggshell C-type lectin-like proteins. Comparative Biochemistry and Physiology B, 143: 160-170. 2006.
68. Marin-Garcia L, Fraontana-Uribe BA, Reyes-Grajeda JP, Stojanoff V, Serrano-Posada HJ and Moreno A. Chemical Recognition of Carbonate Anions by Proteins Involved in Biomineralization Processes and Their Influence on Calcite Crystal Growth. Crystal Growth and Design, 8: 1340-1345. 2008.
69. McKee MD and Nanci A. Osteopontin: an interfacial extra-cellular matrix protein in mineralized tissues. Connective Tissue Research, 35: 197-205. 1996.
70. Miksik I, Eckhardt A, Sedlakova P and Mikulikova K. Proteins of insoluble matrix of avian (Gallus gallus) eggshell. Connective Tissue Research, 48: 1-8. 2007.
71. Nimtz M, Conradt H and Mann K. LacdiNAc (GalNAcβ1-4 GlcNAc) is a major motif in N-glycan structures of the chicken eggshell protein Ovocleidin-116. Biochimica Biophysica Acta, 1675: 71-80. 2004.
72. Nys Y. Regulation of plasma 1,25(OH)2D3, of osteocalcin and of intestinal and uterine calbindin in hens. In: Avian Endocrinology (Sharp PJ ed) pp. 345-357. Journal of Endocrinology Ltd. Bristol. Great Britain. 1993.
73. Nys Y, Gautron J, Garcia-Ruiz JM and Hincke MT. Avian eggshell mineralization: biochemical and functional characterization of matrix proteins. Comptes Rendus Paleovol, 3: 549-562. 2004.
74. Nys Y, Hincke MT, Arias JL, Garcia-Ruiz JM and Solomon S. Avian Eggshell Mineralization. Poultry Avian Biology Reviews, 10: 143-166. 1999.
75. Nys Y, Zawadzki J, Gautron J and Mills AD. Whitening of brown-shelled eggs: mineral composition of uterine fluid and rate of protoporphyrin deposition. Poultry Science, 70: 1236-1245. 1991.
76. Pines M, Knopov V and Bar A. Involvement of osteopontin in egg shell formation in the laying chicken. Matrix Biology, 14: 765-771. 1994.
77. Reyes-Grajeda JP, Jauregui-Zuniga D, Rodriguez-Romero A, Hernandez-Santoyo A, Bolanos-Garcia VM and Moreno A. Crystallization and preliminary x-ray analysis of Ovocleidin-17 a major protein of the Gallus gallus eggshell calcified layer. Protein Peptide Letters, 9: 253-257. 2002.
78. Reyes-Grajeda JP, Marin-Garcia L, Stojanoff V and Moreno A. Purification, crystallization and preliminary X-ray analysis of struthiocalcin 1 from ostrich (Struthio camelus) eggshell. Acta Crystallographica F, 63: 987-989. 2007.
79. Reyes-Grajeda JP, Moreno A and Romero A. Crystal structure of Ovocleidin-17, a major protein of the calcified Gallus gallus eggshell: implications in the calcite mineral growth pattern. Journal of Biological Chemistry, 279: 40876-40881. 2004.
80. Roberts JR. Factors affecting egg internal quality and egg shell quality in laying hens. Journal of Poultry Science, 41: 161-177. 2004.
81. Robey PG. Vertebrate mineralized matrix proteins: structure and function. Connective Tissue Research, 35: 131-136. 1996.
82. Rodriguez-Navarro A, Kalin O, Nys Y and Garcia-Ruiz JM. Influence of the microstructure on the shell strength of eggs laid by hens of different ages. British Poultry Science, 43: 395-403. 2002.
83. Salih E, Ashkar S, Gerstenfeld LC and Glimcher MJ. Identification of the phosphorylated sites of metabolically 32P-labeled osteopontin from cultured chicken osteoblasts. Journal of Biological Chemistry 272: 13966-13973. 1997.
84. Schumann RR, Leong SR, Flaggs GW, Gray PW, Wright SD, Mathison JC, Tobias PS and Ulevitch RJ Structure and function of lipopolysaccharide binding protein. Science, 249: 1429-1431. 1990.
85. Seuss-Baum I. Nutritional Evaluation of Egg Compounds. In: Bioactive egg compounds. (Huopalahti R, Lopez-Fandino R, Anton M, Schade R eds) pp. 117-140. Springer-Verlag. Berlin. 2007.
86. Silyn-Roberts H and SharpRM. Crystal growth and the role of the organic network in eggshell biomineralization. Proceedings of the Royal Society, London B Biological Sciences, 227: 303-324. 1986.
87. Stapley J, Birkhead TR, Burke T and Slate J A linkage map of the zebra finch Taeniopygia guttata provides new insights into avian genome evolution. Genetics, 179: 651-667. 2008.
88. Whittow GC. Sturkie's Avian Physiology. 5th ed. Academic Press. San Diego. 2000.
89. Wong M, Hendrix MJC, Von der Mark K, Little C and Stern R. Collagen in the egg shell membranes of the hen. Developmental Biology, 104: 28-36. 1984.
90. Yang KT, Lin CY, Liou JS, Fan YH, Chiou SH, Huand CW, Wu CP, Lin EC, Chen CF, Lee YP, Lee WC, Ding ST, Cheng WT and Huang MC. Differentially expressed transcripts in shell glands from low and high egg production strains of chickens using cDNA microarrays. Animal Reproduction Science, 110: 113-124. 2007.
91. Zelensky AN and Gready JE. The C-type lectin-like domain superfamily. FEBS Journal, 272: 6179-217. 2005.