Interactions of amelogenin with phospholipids

Bekshe Lokappa, Sowmya; Chandrababu, Karthik Balakrishna; Dutta, Kaushik; Perovic, Iva; Evans, John Spencer; Moradian-Oldak, Janet

doi:10.1002/bip.22573

Title: Interactions of amelogenin with phospholipids

Journal Article · Fri Nov 21 23:00:00 EST 2014 · Biopolymers

DOI: https://doi.org/10.1002/bip.22573 · OSTI ID:1342890

Bekshe Lokappa, Sowmya ^[1]; Chandrababu, Karthik Balakrishna ^[2]; Dutta, Kaushik ^[3]; Perovic, Iva ^[3]; Evans, John Spencer ^[3]; Moradian-Oldak, Janet ^[2]

Univ. of Southern California, Los Angeles, CA (United States); Office of Scientific and Technical Information (OSTI)
Univ. of Southern California, Los Angeles, CA (United States)
New York Univ., New York, NY (United States)

Amelogenin protein has the potential to interact with other enamel matrix proteins, mineral, and cell surfaces. In this paper, we investigated the interactions of recombinant amelogenin rP172 with small unilamellar vesicles as model membranes, toward the goal of understanding the mechanisms of amelogenin–cell interactions during amelogenesis. Dynamic light scattering (DLS), fluorescence spectroscopy, circular dichroism (CD), and nuclear magnetic resonance (NMR) were used. In the presence of phospholipid vesicles, a blue shift in the Trp fluorescence emission maxima of rP172 was observed (~334 nm) and the Trp residues of rP172 were inaccessible to the aqueous quencher acrylamide. DLS studies indicated complexation of rP172 and phospholipids, although the possibility of fusion of phospholipids following amelogenin addition cannot be ruled out. NMR and CD studies revealed a disorder–order transition of rP172 in a model membrane environment. Strong fluorescence resonance energy transfer from Trp in rP172 to DNS-bound-phospholipid was observed, and fluorescence polarization studies indicated that rP172 interacted with the hydrophobic core region of model membranes. Finally, our data suggest that amelogenin has ability to interact with phospholipids and that such interactions may play key roles in enamel biomineralization as well as reported amelogenin signaling activities.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: New York Univ. (NYU), NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: FG02-03ER46099

OSTI ID:: 1342890

Journal Information:: Biopolymers, Journal Name: Biopolymers Journal Issue: 2 Vol. 103; ISSN 0006-3525

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (50)

Interaction of amelogenin with hydroxyapatite crystals: An adherence effect through amelogenin molecular self-association Moradian-Oldak, J.; Tan, J.; Fincham, A. G. Biopolymers, Vol. 46, Issue 4 https://doi.org/10.1002/(SICI)1097-0282(19981005)46:4<225::AID-BIP4>3.0.CO;2-R	journal	October 1998
Changes in the quaternary structure of amelogenin when adsorbed onto surfaces Tarasevich, Barbara J.; Lea, Scott; Bernt, William Biopolymers, Vol. 91, Issue 2 https://doi.org/10.1002/bip.21095	journal	February 2009
Structural adaptation of tooth enamel protein amelogenin in the presence of SDS micelles: Amelogenin Structural Adaptation in SDS Chandrababu, Karthik Balakrishna; Dutta, Kaushik; Lokappa, Sowmya Bekshe Biopolymers, Vol. 101, Issue 5 https://doi.org/10.1002/bip.22415	journal	February 2014
Probing the self-association, intermolecular contacts, and folding propensity of amelogenin: TFE-Induced Folding Propensities of Amelogenin Ndao, Moise; Dutta, Kaushik; Bromley, Keith M. Protein Science, Vol. 20, Issue 4 https://doi.org/10.1002/pro.603	journal	March 2011
Analysis of secondary structure and self-assembly of amelogenin by variable temperature circular dichroism and isothermal titration calorimetry Lakshminarayanan, Rajamani; Yoon, Il; Hegde, Balachandra G. Proteins: Structure, Function, and Bioinformatics, Vol. 76, Issue 3 https://doi.org/10.1002/prot.22369	journal	August 2009
The Structural Biology of the Developing Dental Enamel Matrix Fincham, A. G.; Moradian-Oldak, J.; Simmer, J. P. Journal of Structural Biology, Vol. 126, Issue 3 https://doi.org/10.1006/jsbi.1999.4130	journal	June 1999
NMRPipe: A multidimensional spectral processing system based on UNIX pipes Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW. Journal of Biomolecular NMR, Vol. 6, Issue 3 https://doi.org/10.1007/BF00197809	journal	November 1995
Amelogenin gene splice products: potential signaling molecules Veis, A. Cellular and Molecular Life Sciences (CMLS), Vol. 60, Issue 1 https://doi.org/10.1007/s000180300003	journal	January 2003
A study of the phospholipids of bovine dental tissues—I Shapiro, I. M.; Wuthier, R. E.; Irving, J. T. Archives of Oral Biology, Vol. 11, Issue 5 https://doi.org/10.1016/0003-9969(66)90156-7	journal	May 1966
Lipid analysis of rat enamel and dentine Prout, R. E. S.; Odutuga, A. A.; Tring, F. C. Archives of Oral Biology, Vol. 18, Issue 3 https://doi.org/10.1016/0003-9969(73)90161-1	journal	March 1973
Cyclical changes in pH in bovine developing enamel as sequential bands Sasaki, S.; Takagi, T.; Suzuki, M. Archives of Oral Biology, Vol. 36, Issue 3 https://doi.org/10.1016/0003-9969(91)90090-H	journal	January 1991
Use of fluorescent probes to monitor molecular order and motions within liposome bilayers Lentz, Barry R. Chemistry and Physics of Lipids, Vol. 64, Issue 1-3 https://doi.org/10.1016/0009-3084(93)90060-G	journal	September 1993
Amelogenesis imperfecta phenotype–genotype correlations with two amelogenin gene mutations Hart, P. S.; Aldred, M. J.; Crawford, P. J. M. Archives of Oral Biology, Vol. 47, Issue 4 https://doi.org/10.1016/S0003-9969(02)00003-1	journal	April 2002
The intrinsic pKa values for phosphatidylserine and phosphatidylethanolamine in phosphatidylcholine host bilayers Tsui, F. C.; Ojcius, D. M.; Hubbell, W. L. Biophysical Journal, Vol. 49, Issue 2 https://doi.org/10.1016/S0006-3495(86)83655-4	journal	February 1986
Regulated gene expression dictates enamel structure and tooth function Paine, Michael L.; White, Shane N.; Luo, Wen Matrix Biology, Vol. 20, Issue 5-6 https://doi.org/10.1016/S0945-053X(01)00153-6	journal	September 2001
Analysis of self-assembly and apatite binding properties of amelogenin proteins lacking the hydrophilic C-terminal Moradian-Oldak, Janet; Bouropoulos, Nikolaos; Wang, Lingli Matrix Biology, Vol. 21, Issue 2 https://doi.org/10.1016/S0945-053X(01)00190-1	journal	March 2002
Amelogenins: Multi-Functional Enamel Matrix Proteins and Their Binding Partners Haruyama, Naoto; Hatakeyama, Junko; Moriyama, Keiji Journal of Oral Biosciences, Vol. 53, Issue 3 https://doi.org/10.1016/S1349-0079(11)80009-5	journal	January 2011
Kinetics and thermodynamics of the interaction of 1-anilino-naphthalene-8-sulfonate with proteins Cattoni, Diego I.; Kaufman, Sergio B.; Flecha, F. Luis González Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1794, Issue 11 https://doi.org/10.1016/j.bbapap.2009.08.007	journal	November 2009
Leucine-rich amelogenin peptide induces osteogenesis by activation of the Wnt pathway Warotayanont, Rungnapa; Frenkel, Baruch; Snead, Malcolm L. Biochemical and Biophysical Research Communications, Vol. 387, Issue 3 https://doi.org/10.1016/j.bbrc.2009.07.058	journal	September 2009
A survey of carbonic anhydrase mRNA expression in enamel cells Lacruz, Rodrigo S.; Hilvo, Mika; Kurtz, Ira Biochemical and Biophysical Research Communications, Vol. 393, Issue 4 https://doi.org/10.1016/j.bbrc.2010.02.116	journal	March 2010
Enamel inspired nanocomposite fabrication through amelogenin supramolecular assembly Fan, Yuwei; Sun, Zhi; Wang, Rizhi Biomaterials, Vol. 28, Issue 19 https://doi.org/10.1016/j.biomaterials.2007.02.016	journal	July 2007
The role of bioactive nanofibers in enamel regeneration mediated through integrin signals acting upon C/EBPα and c-Jun Huang, Z.; Newcomb, C. J.; Zhou, Y. Biomaterials, Vol. 34, Issue 13 https://doi.org/10.1016/j.biomaterials.2013.01.054	journal	April 2013
The effect of recombinant mouse amelogenins on the formation and organization of hydroxyapatite crystals in vitro Beniash, Elia; Simmer, James P.; Margolis, Henry C. Journal of Structural Biology, Vol. 149, Issue 2 https://doi.org/10.1016/j.jsb.2004.11.001	journal	February 2005
pH triggered self-assembly of native and recombinant amelogenins under physiological pH and temperature in vitro Wiedemann-Bidlack, Felicitas B.; Beniash, Elia; Yamakoshi, Yasuo Journal of Structural Biology, Vol. 160, Issue 1 https://doi.org/10.1016/j.jsb.2007.06.007	journal	October 2007
The role of charge and hydrophobicity in peptide-lipid interaction: a comparative study based on tryptophan fluorescence measurements combined with the use of aqueous and hydrophobic quenchers De Kroon, Anton I. P. M.; Soekarjo, Mark W.; De Gier, Johannes Biochemistry, Vol. 29, Issue 36 https://doi.org/10.1021/bi00488a006	journal	September 1990
Cooperative Effects in Binding by Bovine Serum Albumin. I. The Binding of 1-Anilino-8-naphthalenesulfonate. Fluorimetric Titrations ^* Daniel, Ezra; Weber, Gregorio Biochemistry, Vol. 5, Issue 6 https://doi.org/10.1021/bi00870a016	journal	June 1966
Phosphorylation and Ionic Strength Alter the LRAP–HAP Interface in the N-Terminus Lu, Jun-xia; Xu, Yimin Sharon; Shaw, Wendy J. Biochemistry, Vol. 52, Issue 13 https://doi.org/10.1021/bi400071a	journal	March 2013
The Tooth Enamel Protein, Porcine Amelogenin, Is an Intrinsically Disordered Protein with an Extended Molecular Configuration in the Monomeric Form ^† Delak, Katya; Harcup, Craig; Lakshminarayanan, Rajamani Biochemistry, Vol. 48, Issue 10 https://doi.org/10.1021/bi802175a	journal	March 2009
In situ AFM Study of Amelogenin Assembly and Disassembly Dynamics on Charged Surfaces Provides Insights on Matrix Protein Self-Assembly Chen, Chun-Long; Bromley, Keith M.; Moradian-Oldak, Janet Journal of the American Chemical Society, Vol. 133, Issue 43 https://doi.org/10.1021/ja206849c	journal	November 2011
Mimicking the Self-Organized Microstructure of Tooth Enamel Wang, Lijun; Guan, Xiangying; Yin, Haoyong The Journal of Physical Chemistry C, Vol. 112, Issue 15 https://doi.org/10.1021/jp077105+	journal	March 2008
Adsorption of Amelogenin onto Self-Assembled and Fluoroapatite Surfaces Tarasevich, Barbara J.; Lea, Scott; Bernt, William The Journal of Physical Chemistry B, Vol. 113, Issue 7 https://doi.org/10.1021/jp804548x	journal	February 2009
Hierarchical self-assembly of amelogenin and the regulation of biomineralization at the nanoscale Fang, P. -A.; Conway, J. F.; Margolis, H. C. Proceedings of the National Academy of Sciences, Vol. 108, Issue 34 https://doi.org/10.1073/pnas.1106228108	journal	August 2011
Tyrosyl Motif in Amelogenins Binds N -Acetyl-d-glucosamine Ravindranath, Rajeswari M. H.; Moradian-Oldak, Janet; Fincham, Alan G. Journal of Biological Chemistry, Vol. 274, Issue 4 https://doi.org/10.1074/jbc.274.4.2464	journal	January 1999
Role of 20-kDa Amelogenin (P148) Phosphorylation in Calcium Phosphate Formation in Vitro Kwak, Seo-Young; Wiedemann-Bidlack, Felicitas B.; Beniash, Elia Journal of Biological Chemistry, Vol. 284, Issue 28 https://doi.org/10.1074/jbc.M109.020370	journal	May 2009
Perturbed Amelogenin Secondary Structure Leads to Uncontrolled Aggregation in Amelogenesis Imperfecta Mutant Proteins Lakshminarayanan, Rajamani; Bromley, Keith M.; Lei, Ya-Ping Journal of Biological Chemistry, Vol. 285, Issue 52 https://doi.org/10.1074/jbc.M110.131136	journal	October 2010
Dissecting Amelogenin Protein Nanospheres: CHARACTERIZATION OF METASTABLE OLIGOMERS Bromley, Keith M.; Kiss, Andrew S.; Lokappa, Sowmya Bekshe Journal of Biological Chemistry, Vol. 286, Issue 40 https://doi.org/10.1074/jbc.M111.250928	journal	August 2011
Both Acidic and Basic Amino Acids in an Amphitropic Enzyme, CTP:Phosphocholine Cytidylyltransferase, Dictate Its Selectivity for Anionic Membranes Johnson, Joanne E.; Xie, Mingtang; Singh, Laila M. R. Journal of Biological Chemistry, Vol. 278, Issue 1 https://doi.org/10.1074/jbc.M206072200	journal	October 2002
Molecular Conformation of Porcine Amelogenin in Solution: Three Folding Units at the N-terminal, Central, and C-Terminal Regions1 Goto, Yuji; Kogure, Eiichi; Takagi, Toshio The Journal of Biochemistry, Vol. 113, Issue 1 https://doi.org/10.1093/oxfordjournals.jbchem.a124003	journal	January 1993
On the formation of amelogenin microribbons Moradian-Oldak, Janet; Du, Chang; Falini, Giuseppe European Journal of Oral Sciences, Vol. 114, Issue s1 https://doi.org/10.1111/j.1600-0722.2006.00285.x	journal	May 2006
Structural Changes in Amelogenin upon Self-assembly and Mineral Interactions Beniash, E.; Simmer, J. P.; Margolis, H. C. Journal of Dental Research, Vol. 91, Issue 10 https://doi.org/10.1177/0022034512457371	journal	August 2012
Characterization of Recombinant Pig Enamelysin Activity and Cleavage of Recombinant Pig and Mouse Amelogenins Ryu, O. H.; Fincham, A. G.; Hu, C. -C. Journal of Dental Research, Vol. 78, Issue 3 https://doi.org/10.1177/00220345990780030601	journal	March 1999
Developmental Changes in the PH of Enamel Fluid and Its Effects On Matrix-Resident Proteinases Smith, C. E.; Issid, M.; Margolis, H. C. Advances in Dental Research, Vol. 10, Issue 2 https://doi.org/10.1177/08959374960100020701	journal	November 1996
Amelogenin is a Cell Adhesion Protein Hoang, A. M.; Klebe, R. J.; Steffensen, B. Journal of Dental Research, Vol. 81, Issue 7 https://doi.org/10.1177/154405910208100713	journal	July 2002
Role of Macromolecular Assembly of Enamel Matrix Proteins in Enamel Formation Margolis, H. C.; Beniash, E.; Fowler, C. E. Journal of Dental Research, Vol. 85, Issue 9 https://doi.org/10.1177/154405910608500902	journal	September 2006
Validation of Amelogenesis Imperfecta Inferred from Amelogenin Evolution Delgado, S.; Ishiyama, M.; Sire, J. -Y. Journal of Dental Research, Vol. 86, Issue 4 https://doi.org/10.1177/154405910708600405	journal	April 2007
P hospholipids in A melogenesis and D entinogenesis Goldberg, M.; Septier, D. Critical Reviews in Oral Biology & Medicine, Vol. 13, Issue 3 https://doi.org/10.1177/154411130201300305	journal	May 2002
Functional Domains for Amelogenin Revealed by Compound Genetic Defects Paine, Michael L.; Luo, Wen; Zhu, Dan-Hong Journal of Bone and Mineral Research, Vol. 18, Issue 3 https://doi.org/10.1359/jbmr.2003.18.3.466	journal	March 2003
The Role of Secondary Structure in the Entropically Driven Amelogenin Self-Assembly Lakshminarayanan, Rajamani; Fan, Daming; Du, Chang Biophysical Journal, Vol. 93, Issue 10 https://doi.org/10.1529/biophysj.107.113936	journal	November 2007
Role of the N-terminal peptide of amelogenin on osteoblastic differentiation of human mesenchymal stem cells Olivares-Navarrete, R.; Vesper, K.; Hyzy, Sl European Cells and Materials, Vol. 28 https://doi.org/10.22203/eCM.v028a01	journal	July 2014
Protein-mediated Enamel Mineralization Moradian-Oldak, Janet Frontiers in Bioscience, Vol. 17, Issue 7 https://doi.org/10.2741/4034	journal	January 2012

Cited By (3)

TGF-β1 autocrine signalling and enamel matrix components Kobayashi-Kinoshita, Saeko; Yamakoshi, Yasuo; Onuma, Kazuo Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep33644	journal	September 2016
Amelogenin and enamel biomimetics Ruan, Qichao; Moradian-Oldak, Janet Journal of Materials Chemistry B, Vol. 3, Issue 16 https://doi.org/10.1039/c5tb00163c	journal	January 2015
Molecular insights into hypomineralized enamel Malmberg, Per; Norén, Jörgen G.; Bernin, Diana European Journal of Oral Sciences, Vol. 127, Issue 4 https://doi.org/10.1111/eos.12619	journal	April 2019

Similar Records

Controls of Nature: Secondary, tertiary, and quaternary structure of the enamel protein amelogenin in solution and on hydroxyapatite

Journal Article · Mon Nov 30 23:00:00 EST 2020 · Journal of Structural Biology · OSTI ID:1674955

Shaw, Wendy J.; Tarasevich, Barbara J.; Buchko, Garry W.; +2 more

Solid-State NMR Identification of Intermolecular Interactions in Amelogenin Bound to Hydroxyapatite

Journal Article · Thu Nov 01 00:00:00 EDT 2018 · Biophysical Journal · OSTI ID:1503553

Arachchige, Rajith Jayasinha; Burton, Sarah D.; Lu, Jun-Xia; +8 more

A solution NMR investigation into the impaired self-assembly properties of two murine amelogenins containing the point mutations T21→I or P41→T

Journal Article · Mon Aug 26 00:00:00 EDT 2013 · Archives of Biochemistry and Biophysics, 537(2):217-224 · OSTI ID:1091431

Buchko, Garry W.; Lin, Genyao; Tarasevich, Barbara J.; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
amelogenin
cell membrane
enamel
intrinsically disordered protein
lipid vesicles

Title: Interactions of amelogenin with phospholipids

Citation Formats

References (50)

Cited By (3)

Similar Records

Related Subjects