The Molecular Evolution of the Pif Family Proteins in Various Species of Mollusks

Marine Biotechnology

Volumn 15, Issue 2, 2013, Pages 145-158

  Suzuki, Michio ^a,b   Iwashima, Ai ^b   Kimura, Mariko ^b   Kogure, Toshihiro ^a   Nagasawa, Hiromichi ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Aragonite; Biomineralization; Chitin binding; Pif; Pinctada; VWA

Indexed keywords

BIOMINERALIZATION; CALCIUM CARBONATE; CHITIN; MOLECULAR BIOLOGY; MOLLUSCS; MORPHOLOGY; PLANTS (BOTANY); SHELLS (STRUCTURES);

ARAGONITE; CALCIUM CARBONATE CRYSTALS; CHITIN BINDING; CHITIN BINDING DOMAINS; MOLECULAR EVOLUTION; MYTILUS GALLOPROVINCIALIS; PINCTADA; VON WILLEBRAND FACTOR;

PROTEINS;

AMINO ACID; ARAGONITE; BIOMINERALIZATION; BIOTECHNOLOGY; BIVALVE; CALCIUM CARBONATE; CHITIN; COMMERCIAL SPECIES; COMMON ANCESTRY; GENE EXPRESSION; MARINE TECHNOLOGY; MOLECULAR ANALYSIS; PROTEIN; SHELL;

ANIMALIA; BIVALVIA; GASTROPODA; LOTTIA GIGANTEA; MOLLUSCA; MYTILUS GALLOPROVINCIALIS; PINCTADA; PINCTADA FUCATA; PINCTADA MARGARITIFERA; PINCTADA MAXIMA; PTERIA PENGUIN; SPHENISCIDAE;

EID: 84874116812     PISSN: 14362228     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10126-012-9471-2     Document Type: Article

References (50)

1. 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.
2. Berland S, Marie A, Duplat D, Milet C, Sire JY, Bedouet L (2011) Coupling proteomics and transcriptomics for the identification of novel and variant forms of mollusk shell proteins: a study with P. margaritifera. Chembiochem 12: 950-961.
3. Burgess TL, Kelly RB (1987) Constitutive and regulated secretion of proteins. Annu Rev Cell Biol 3: 243-293.
4. Elvin CM, Vuocolo T, Pearson RD, East IJ, Riding GA, Eisemann CH, Tellam RL (1996) Characterization of a major peritrophic membrane protein, peritrophin-44, from the larvae of Lucilia cuprina. cDNA and deduced amino acid sequences. J Biol Chem 271: 8925-8935.
5. Falini G, Albeck S, Weiner S, Addadi L (1996) Control of aragonite or calcite polymorphism by mollusk shell macromolecules. Science 271: 67-69.
6. Fuchigami T, Sasaki T (2005) The shell structure of the recent Patellogastropoda (Mollusca: Gastropoda). Paleontol Res 9: 143-168.
7. Gotliv BA, Kessler N, Sumerel JL, Morse DE, Tuross N, Addadi L, Weiner S (2005) Asprich: a novel aspartic acid-rich protein family from the prismatic shell matrix of the bivalve Atrina rigida. Chembiochem 6: 304-314.
8. Gregoire C (1957) Topography of the organic components in mother-of pearl. J Biophys Biochem Cytol 3: 797-808.
9. Hohenester E, Tisi D, Talts JF, Timpl R (1999) The crystal structure of a laminin G-like module reveals the molecular basis of alpha-dystroglycan binding to laminins, perlecan, and agrin. Mol Cell 4: 783-792.
10. Joubert C, Piquemal D, Marie B, Manchon L, Pierrat F, Zanella-Cleon I, Cochennec-Laureau N, Gueguen Y, Montagnani C (2010) Transcriptome and proteome analysis of Pinctada margaritifera calcifying mantle and shell: focus on biomineralization. BMC Genomics 11: 613-625.
11. Kawabata S, Nagayama R, Hirata M, Shigenaga T, Agarwala KL, Saito T, Cho J, Nakajima H, Takagi T, Iwanaga S (1996) Tachycitin, a small granular component in horseshoe crab hemocytes, is an antimicrobial protein with chitin-binding activity. J Biochem 120: 1253-1260.
12. Kono M, Hayashi N, Samata T (2000) Molecular mechanism of the nacreous layer formation in Pinctada maxima. Biochem Biophys Res Commun 269: 213-218.
13. Lee JO, Rieu P, Arnaout MA, Liddington R (1995) Crystal structure of the A domain from the alpha subunit of integrin CR3 (CD11b/CD18). Cell 80: 631-638.
14. Mann K, Siedler F, Treccani L, Heinemann F, Fritz M (2007) Perlinhibin, a cysteine-, histidine-, and arginine-rich miniprotein from abalone (Haliotis laevigata) nacre, inhibits in vitro calcium carbonate crystallization. Biophys J 93: 1246-1254.
15. Marie B, Le Roy N, Zanella-Cleon I, Becchi M, Marin F (2011) Molecular evolution of mollusc shell proteins: insights from proteomic analysis of the edible mussel Mytilus. J Mol Evol 72: 531-546.
16. Marin F, Corstjens P, de Gaulejac B, de Vrind-de JE, Westbroek P (2000) Mucins and molluscan calcification. Molecular characterization of mucoperlin, a novel mucin-like protein from the nacreous shell layer of the fan mussel Pinna nobilis (Bivalvia, Pteriomorphia). J Biol Chem 275: 20667-20675.
17. Marshall RC, Gillespie JM (1982) The tryptophan-rich keratin protein fraction of claws of the lizard Varanus gouldii. Comp Biochem Physiol B 71: 623-628.
18. Marxen JC, Nimtz M, Becker W, Mann K (2003) The major soluble 19. 6 kDa protein of the organic shell matrix of the freshwater snail Biomphalaria glabrata is an N-glycosylated dermatopontin. Biochim Biophys Acta 1650: 92-98.
19. Matsushiro A, Miyashita T, Miyamoto H, Morimoto K, Tonomura B, Tanaka A, Sato K (2003) Presence of protein complex is prerequisite for aragonite crystallization in the nacreous layer. Mar Biotechnol (N Y) 5: 37-44.
20. Michenfelder M, Fu G, Lawrence C, Weaver JC, Wustman BA, Taranto L, Evans JS, Morse DE (2003) Characterization of two molluscan crystal-modulating biomineralization proteins and identification of putative mineral binding domains. Biopolymers 70: 522-533.
21. Miyamoto H, Miyashita T, Okushima M, Nakano S, Morita T, Matsushiro A (1996) A carbonic anhydrase from the nacreous layer in oyster pearls. Proc Natl Acad Sci USA 93: 9657-9660.
22. Miyamoto H, Yano M, Miyashita T (2003) Similarities in the structure of nacrein, the shell-matrix protein, in a bivalve and a gastropod. J Moll Stud 69: 87-89.
23. Miyashita T, Takagi R, Okushima M, Nakano S, Miyamoto H, Nishikawa E, Matsushiro A (2000) Complementary DNA cloning and characterization of pearlin, a new class of matrix protein in the nacreous layer of oyster pearls. Mar Biotechnol (N Y) 2: 409-418.
24. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-25.
25. Samata T, Hayashi N, Kono M, Hasegawa K, Horita C, Akera S (1999) A new matrix protein family related to the nacreous layer formation of Pinctada fucata. FEBS Lett 462: 225-229.
26. Sarashina I, Yamaguchi H, Haga T, Iijima M, Chiba S, Endo K (2006) Molecular evolution and functionally important structures of molluscan dermatopontin: implications for the origins of molluscan shell matrix proteins. J Mol Evol 62: 307-318.
27. Shen Z, Jacobs-Lorena M (1999) Evolution of chitin-binding proteins in invertebrates. J Mol Evol 48: 341-347.
28. Shen X, Belcher AM, Hansma PK, Stucky GD, Morse DE (1997) Molecular cloning and characterization of lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens. J Biol Chem 272: 32472-32481.
29. Smirnov SP, McDearmon EL, Li S, Ervasti JM, Tryggvason K, Yurchenco PD (2002) Contributions of the LG modules and furin processing to laminin-2 functions. J Biol Chem 277: 18928-18937.
30. Sudo S, Fujikawa T, Nagakura T, Ohkubo T, Sakaguchi K, Tanaka M, Nakashima K, Takahashi T (1997) Structures of mollusc shell framework proteins. Nature 387: 563-564.
31. Suetake T, Tsuda S, Kawabata S, Miura K, Iwanaga S, Hikichi K, Nitta K, Kawano K (2000) Chitin-binding proteins in invertebrates and plants comprise a common chitin-binding structural motif. J Biol Chem 275: 17929-17932.
32. Suzuki M, Saruwatari K, Kogure T, Yamamoto Y, Nishimura T, Kato T, Nagasawa H (2009) An acidic matrix protein, Pif, is a key macromolecule for nacre formation. Science 325: 1388-1390.
33. Suzuki M, Kameda J, Sasaki T, Saruwatari K, Nagasawa H, Kogure T (2010) Characterization of the multilayered shell of a limpet, Lottia kogamogai (Mollusca: Patellogastropoda), using SEM-EBSD and FIB-TEM techniques. J Struct Biol 171: 223-230.
34. Suzuki M, Iwashima A, Tsutsui N, Ohira T, Kogure T, Nagasawa H (2011) Identification and characterisation of a calcium carbonate-binding protein, blue mussel shell protein (BMSP), from the nacreous layer. Chembiochem 12: 2478-2487.
35. Takahashi K, Yamamoto H, Onoda A, Doi M, Inaba T, Chiba M, Kobayashi A, Taguchi T, Okamura T, Ueyama N (2004) Highly oriented aragonite nanocrystal-biopolymer composites in an aragonite brick of the nacreous layer of Pinctada fucata. Chemm Comm 8: 996-997.
36. Talts JF, Timpl R (1999) Mutation of a basic sequence in the laminin alpha2LG3 module leads to a lack of proteolytic processing and has different effects on beta1 integrin-mediated cell adhesion and alpha-dystroglycan binding. FEBS Lett 458: 319-323.
37. Talts JF, Mann K, Yamada Y, Timpl R (1998) Structural analysis and proteolytic processing of recombinant G domain of mouse laminin alpha2 chain. FEBS Lett 426: 71-76.
38. Temkin I (2010) Molecular phylogeny of pearl oysters and their relatives (Mollusca, Bivalvia, Pterioidea). BMC Evol Biol 10: 342-369.
39. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-80.
40. Treccani L, Mann K, Heinemann F, Fritz M (2006) Perlwapin, an abalone nacre protein with three four-disulfide core (whey acidic protein) domains, inhibits the growth of calcium carbonate crystals. Biophys J 91: 2601-2608.
41. Tryggvason K (1993) The laminin family. Curr Opin Cell Biol 5: 877-882.
42. Tsukamoto D, Sarashina I, Endo K (2004) Structure and expression of an unusually acidic matrix protein of pearl oyster shells. Biochem Biophys Res Commun 320: 1175-1180.
43. Tuckwell D (1999) Evolution of von Willebrand factor A (VWA) domains. Biochem Soc Trans 27: 835-840.
44. Wada K (1961) Crystal growth of molluscan shells. Bull Nat Pearl Res Lab 7: 703-785.
45. Weiner S, Hood L (1975) Soluble protein of the organic matrix of mollusk shells: a potential template for shell formation. Science 190: 987-9.
46. Weiss IM, Kaufmann S, Mann K, Fritz M (2000) Purification and characterization of perlucin and perlustrin, two new proteins from the shell of the mollusc Haliotis laevigata. Biochem Biophys Res Commun 267: 17-21.
47. Whittaker CA, Hynes RO (2002) Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol Biol Cell 13: 3369-3387.
48. Yano M, Nagai K, Morimoto K, Miyamoto H (2007) A novel nacre protein N19 in the pearl oyster Pinctada fucata. Biochem Biophys Res Commun 362: 158-163.
49. Yu H, Talts JF (2003) Beta1 integrin and alpha-dystroglycan binding sites are localized to different laminin-G-domain-like (LG) modules within the laminin alpha5 chain G domain. Biochem J 371: 289-299.
50. Yurchenco PD, Sung U, Ward MD, Yamada Y, O'Rear JJ (1993) Recombinant laminin G domain mediates myoblast adhesion and heparin binding. J Biol Chem 268: 8356-8365.