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The expanded amelogenin polyproline region preferentially binds to apatite versus carbonate and promotes apatite crystal elongation
The transition from invertebrate calcium carbonate-based calcite and aragonite exo- and endoskeletons to the calcium phosphate-based vertebrate backbones and jaws composed of microscopic hydroxyapatite crystals is one of the great revolutions in the evolution of terrestrial organisms. To identify po...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2014
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4227485/ https://www.ncbi.nlm.nih.gov/pubmed/25426079 http://dx.doi.org/10.3389/fphys.2014.00430 |
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author | Gopinathan, Gokul Jin, Tianquan Liu, Min Li, Steve Atsawasuwan, Phimon Galang, Maria-Therese Allen, Michael Luan, Xianghong Diekwisch, Thomas G. H. |
author_facet | Gopinathan, Gokul Jin, Tianquan Liu, Min Li, Steve Atsawasuwan, Phimon Galang, Maria-Therese Allen, Michael Luan, Xianghong Diekwisch, Thomas G. H. |
author_sort | Gopinathan, Gokul |
collection | PubMed |
description | The transition from invertebrate calcium carbonate-based calcite and aragonite exo- and endoskeletons to the calcium phosphate-based vertebrate backbones and jaws composed of microscopic hydroxyapatite crystals is one of the great revolutions in the evolution of terrestrial organisms. To identify potential factors that might have played a role in such a transition, three key domains of the vertebrate tooth enamel protein amelogenin were probed for calcium mineral/protein interactions and their ability to promote calcium phosphate and calcium carbonate crystal growth. Under calcium phosphate crystal growth conditions, only the carboxy-terminus augmented polyproline repeat peptide, but not the N-terminal peptide nor the polyproline repeat peptide alone, promoted the formation of thin and parallel crystallites resembling those of bone and initial enamel. In contrast, under calcium carbonate crystal growth conditions, all three amelogenin-derived polypeptides caused calcium carbonate to form fused crystalline conglomerates. When examined for long-term crystal growth, polyproline repeat peptides of increasing length promoted the growth of shorter calcium carbonate crystals with broader basis, contrary to the positive correlation between polyproline repeat element length and apatite mineralization published earlier. To determine whether the positive correlation between polyproline repeat element length and apatite crystal growth versus the inverse correlation between polyproline repeat length and calcium carbonate crystal growth were related to the binding affinity of the polyproline domain to either apatite or carbonate, a parallel series of calcium carbonate and calcium phosphate/apatite protein binding studies was conducted. These studies demonstrated a remarkable binding affinity between the augmented amelogenin polyproline repeat region and calcium phosphates, and almost no binding to calcium carbonates. In contrast, the amelogenin N-terminus bound to both carbonate and apatite, but preferentially to calcium carbonate. Together, these studies highlight the specific binding affinity of the augmented amelogenin polyproline repeat region to calcium phosphates versus calcium carbonate, and its unique role in the growth of thin apatite crystals as they occur in vertebrate biominerals. Our data suggest that the rise of apatite-based biominerals in vertebrates might have been facilitated by a rapid evolution of specialized polyproline repeat proteins flanked by a charged domain, resulting in apatite crystals with reduced width, increased length, and tailored biomechanical properties. |
format | Online Article Text |
id | pubmed-4227485 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-42274852014-11-25 The expanded amelogenin polyproline region preferentially binds to apatite versus carbonate and promotes apatite crystal elongation Gopinathan, Gokul Jin, Tianquan Liu, Min Li, Steve Atsawasuwan, Phimon Galang, Maria-Therese Allen, Michael Luan, Xianghong Diekwisch, Thomas G. H. Front Physiol Physiology The transition from invertebrate calcium carbonate-based calcite and aragonite exo- and endoskeletons to the calcium phosphate-based vertebrate backbones and jaws composed of microscopic hydroxyapatite crystals is one of the great revolutions in the evolution of terrestrial organisms. To identify potential factors that might have played a role in such a transition, three key domains of the vertebrate tooth enamel protein amelogenin were probed for calcium mineral/protein interactions and their ability to promote calcium phosphate and calcium carbonate crystal growth. Under calcium phosphate crystal growth conditions, only the carboxy-terminus augmented polyproline repeat peptide, but not the N-terminal peptide nor the polyproline repeat peptide alone, promoted the formation of thin and parallel crystallites resembling those of bone and initial enamel. In contrast, under calcium carbonate crystal growth conditions, all three amelogenin-derived polypeptides caused calcium carbonate to form fused crystalline conglomerates. When examined for long-term crystal growth, polyproline repeat peptides of increasing length promoted the growth of shorter calcium carbonate crystals with broader basis, contrary to the positive correlation between polyproline repeat element length and apatite mineralization published earlier. To determine whether the positive correlation between polyproline repeat element length and apatite crystal growth versus the inverse correlation between polyproline repeat length and calcium carbonate crystal growth were related to the binding affinity of the polyproline domain to either apatite or carbonate, a parallel series of calcium carbonate and calcium phosphate/apatite protein binding studies was conducted. These studies demonstrated a remarkable binding affinity between the augmented amelogenin polyproline repeat region and calcium phosphates, and almost no binding to calcium carbonates. In contrast, the amelogenin N-terminus bound to both carbonate and apatite, but preferentially to calcium carbonate. Together, these studies highlight the specific binding affinity of the augmented amelogenin polyproline repeat region to calcium phosphates versus calcium carbonate, and its unique role in the growth of thin apatite crystals as they occur in vertebrate biominerals. Our data suggest that the rise of apatite-based biominerals in vertebrates might have been facilitated by a rapid evolution of specialized polyproline repeat proteins flanked by a charged domain, resulting in apatite crystals with reduced width, increased length, and tailored biomechanical properties. Frontiers Media S.A. 2014-11-11 /pmc/articles/PMC4227485/ /pubmed/25426079 http://dx.doi.org/10.3389/fphys.2014.00430 Text en Copyright © 2014 Gopinathan, Jin, Liu, Li, Atsawasuwan, Galang, Allen, Luan and Diekwisch. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Physiology Gopinathan, Gokul Jin, Tianquan Liu, Min Li, Steve Atsawasuwan, Phimon Galang, Maria-Therese Allen, Michael Luan, Xianghong Diekwisch, Thomas G. H. The expanded amelogenin polyproline region preferentially binds to apatite versus carbonate and promotes apatite crystal elongation |
title | The expanded amelogenin polyproline region preferentially binds to apatite versus carbonate and promotes apatite crystal elongation |
title_full | The expanded amelogenin polyproline region preferentially binds to apatite versus carbonate and promotes apatite crystal elongation |
title_fullStr | The expanded amelogenin polyproline region preferentially binds to apatite versus carbonate and promotes apatite crystal elongation |
title_full_unstemmed | The expanded amelogenin polyproline region preferentially binds to apatite versus carbonate and promotes apatite crystal elongation |
title_short | The expanded amelogenin polyproline region preferentially binds to apatite versus carbonate and promotes apatite crystal elongation |
title_sort | expanded amelogenin polyproline region preferentially binds to apatite versus carbonate and promotes apatite crystal elongation |
topic | Physiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4227485/ https://www.ncbi.nlm.nih.gov/pubmed/25426079 http://dx.doi.org/10.3389/fphys.2014.00430 |
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