Yıl 2019, Cilt 7 , Sayı 3, Sayfalar 373 - 380 2019-09-28

Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis
Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis

Mustafa Ünal [1]


Being the primarily organic phase of bone, collagen type I is an important contributor to bone’s mechanical resistance to fracture. Gaining mechanistic insight into collagen stabilization mechanism is critical to developing new targets to prevent bone fracture. The role of water and hydroxyproline (Hyp) in collagen stability mechanism is still controversial. The aim of this study was to investigate the influences of Hyp and bound water on the collagen molecular stability. Four collagen like-peptide (CLP) models were compared in terms of conformational energies and hydrogen bonding types. CLP1 model represents regular collagen structure without water molecules while CLP2 model represents collagen structure without water and Hyp residue. CLPW1 and CLPW2 are the models of CLP1 and CLP2 with water molecules around them, respectively. Cumulative interpreting of four CLPs models was shed light on the factors influencing collagen stability in the frame of steric energy. Total steric energy was ordered as: CLP2 > CLP1 > CLPW2 > CLPW1, indicating that CLPW1 was the most stable collagen model. On the other hand, CLP2 was the least stable collagen model based on the steric energy comparison. In addition, the hydrogen bonding observed in the four models reveled that water molecules around the models help in binding collagen triple helix through different water bridges since they contributed extra way for binding of triple chains. Moreover, some of the observed water bridges involved directly the presence of Hyp residue. Cumulative results suggested the important role of bound water molecules and Hyp on collagen molecular stability.

Being the primarily organic phase of bone, collagen type I is an important contributor to bone’s mechanical resistance to fracture. Gaining mechanistic insight into collagen stabilization mechanism is critical to developing new targets to prevent bone fracture. The role of water and hydroxyproline (Hyp) in collagen stability mechanism is still controversial. The aim of this study was to investigate the influences of Hyp and bound water on the collagen molecular stability. Four collagen like-peptide (CLP) models were compared in terms of conformational energies and hydrogen bonding types. CLP1 model represents regular collagen structure without water molecules while CLP2 model represents collagen structure without water and Hyp residue. CLPW1 and CLPW2 are the models of CLP1 and CLP2 with water molecules around them, respectively. Cumulative interpreting of four CLPs models was shed light on the factors influencing collagen stability in the frame of steric energy. Total steric energy was ordered as: CLP2 > CLP1 > CLPW2 > CLPW1, indicating that CLPW1 was the most stable collagen model. On the other hand, CLP2 was the least stable collagen model based on the steric energy comparison. In addition, the hydrogen bonding observed in the four models reveled that water molecules around the models help in binding collagen triple helix through different water bridges since they contributed extra way for binding of triple chains. Moreover, some of the observed water bridges involved directly the presence of Hyp residue. Cumulative results suggested the important role of bound water molecules and Hyp on collagen molecular stability.
  • [1] M. Unal, A. Creecy, and J. S. Nyman, "The Role of Matrix Composition in the Mechanical Behavior of Bone," Curr Osteoporos Rep, vol. 16, pp. 205-215, 2018.
  • [2] L. Knott and A. J. Bailey, "Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance," Bone, vol. 22, pp. 181-187, 1998.
  • [3] J.-Y. Rho, L. Kuhn-Spearing, and P. Zioupos, "Mechanical properties and the hierarchical structure of bone," Medical Engineering & Physics, vol. 20, pp. 92-102, 1998.
  • [4] M. Unal, H. Jung, and O. Akkus, "Novel Raman Spectroscopic Biomarkers Indicate That Postyield Damage Denatures Bone's Collagen," Journal of Bone and Mineral Research, vol. 31, pp. 1015-1025, 2016.
  • [5] G. N. Ramachandran and G. Kartha, "Structure of collagen," Nature, vol. 176, pp. 593-5, Sep 24 1955.
  • [6] A. Rich and F. H. Crick, "The molecular structure of collagen," J Mol Biol, vol. 3, pp. 483-506, Oct 1961.
  • [7] M. D. Shoulders and R. T. Raines, "Collagen Structure and Stability," Annual Review of Biochemistry, vol. 78, pp. 929-958, 2009.
  • [8] C. L. Jenkins and R. T. Raines, "Insights on the conformational stability of collagen," Natural Product Reports, vol. 19, pp. 49-59, 2002.
  • [9] G. N. Ramachandran and G. Kartha, "Structure of collagen," Nature, vol. 174, pp. 269-70, Aug 7 1954.
  • [10] K. Okuyama, K. Okuyama, S. Arnott, M. Takayanagi, and M. Kakudo, "Crystal and molecular structure of a collagen-like polypeptide (Pro-Pro-Gly) 10," J Mol Biol, vol. 152, pp. 427-443, 1981.
  • [11] J. Bella, M. Eaton, B. Brodsky, and H. M. Berman, "Crystal and molecular structure of a collagen-like peptide at 1.9 A resolution," Science, vol. 266, pp. 75-81, 1994.
  • [12] S. Sakakibara, Y. Kishida, K. Okuyama, N. Tanaka, T. Ashida, and M. Kakudo, "Single crystals of (Pro-Pro-Gly) 10, a synthetic polypeptide model of collagen," J Mol Biol, vol. 65, pp. 371-373, 1972.
  • [13] E. Suzuki, R. Fraser, and T. MacRae, "Role of hydroxyproline in the stabilization of the collagen molecule via water molecules," International Journal of Biological Macromolecules, vol. 2, pp. 54-56, 1980.
  • [14] T. V. Burjanadze, "Thermodynamic substantiation of water‐bridged collagen structure," Biopolymers: Original Research on Biomolecules, vol. 32, pp. 941-949, 1992.
  • [15] J. Bella, B. Brodsky, and H. M. Berman, "Hydration structure of a collagen peptide," Structure, vol. 3, pp. 893-906, 1995.
  • [16] N. K. Shah, J. A. Ramshaw, A. Kirkpatrick, C. Shah, and B. Brodsky, "A host− guest set of triple-helical peptides: stability of Gly-XY triplets containing common nonpolar residues," Biochemistry, vol. 35, pp. 10262-10268, 1996.
  • [17] R. Berisio, L. Vitagliano, L. Mazzarella, and A. Zagari, "Crystal structure determination of the collagen-like polypeptide with repeating sequence Pro-Gyp-Gly: Implications for hydration," Biopolymers, vol. 56, pp. 8-13, 2001.
  • [18] A. Tamilselvan and D. Zhang, "Effect of hydration on molecular stability of bone collagen," Proceedings of the Ieee 28th Annual Northeast Bioengineering Conference, pp. 197-198, 2002.
  • [19] K. Mizuno, T. Hayashi, D. H. Peyton, and H. P. Bächinger, "Hydroxylation-induced Stabilization of the Collagen Triple Helix ACETYL-(GLYCYL-4 (R)-HYDROXYPROLYL-4 (R)-HYDROXYPROLYL) 10-NH2 FORMS A HIGHLY STABLE TRIPLE HELIX," Journal of Biological Chemistry, vol. 279, pp. 38072-38078, 2004.
  • [20] J. A. Howard, V. J. Hoy, D. O'Hagan, and G. T. Smith, "How good is fluorine as a hydrogen bond acceptor?," Tetrahedron, vol. 52, pp. 12613-12622, 1996.
  • [21] S. K. Holmgren, K. M. Taylor, L. E. Bretscher, and R. T. Raines, "Code for collagen's stability deciphered," Nature, vol. 392, p. 666, 1998.
  • [22] S. K. Holmgren, L. E. Bretscher, K. M. Taylor, and R. T. Raines, "A hyperstable collagen mimic," Chemistry & biology, vol. 6, pp. 63-70, 1999.
  • [23] T. Hiyama, K. Kanie, T. Kusumoto, Y. Morizawa, and M. Shimizu, "Properties of fluoroorganic compounds," Organofluorine Compounds: Chemistry and Applications, pp. 10-12, 2000.
  • [24] Y. Nishi, S. Uchiyama, M. Doi, Y. Nishiuchi, T. Nakazawa, T. Ohkubo, and Y. Kobayashi, "Different effects of 4-hydroxyproline and 4-fluoroproline on the stability of collagen triple helix," Biochemistry, vol. 44, pp. 6034-6042, 2005.
  • [25] J. Engel, H. T. Chen, D. J. Prockop, and H. Klump, "The triple helix⇌ coil conversion of collagen‐like polytripeptides in aqueous and nonaqueous solvents. Comparison of the thermodynamic parameters and the binding of water to (L‐Pro‐L‐Pro‐Gly) n and (L‐Pro‐L‐Hyp‐Gly) n," Biopolymers: Original Research on Biomolecules, vol. 16, pp. 601-622, 1977.
  • [26] D. L. Bodian, R. J. Radmer, S. Holbert, and T. E. Klein, "Molecular dynamics simulations of the full triple helical region of collagen type I provide an atomic scale view of the protein's regional heterogeneity," in Biocomputing 2011, ed: World Scientific, 2011, pp. 193-204.
  • [27] T. A. Halgren, "Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94," Journal of computational chemistry, vol. 17, pp. 490-519, 1996.
  • [28] U. Burkert, "Molecular mechanics," ACS monograph 177, 1982.
  • [29] T. W. Shattuck, "Colby College Molecular Mechanics Tutorial," ed: Colby College, Waterville, 2008.
  • [30] M. D. Hanwell, D. E. Curtis, D. C. Lonie, T. Vandermeersch, E. Zurek, and G. R. Hutchison, "Avogadro: an advanced semantic chemical editor, visualization, and analysis platform," Journal of cheminformatics, vol. 4, pp. 1-17, 2012.
  • [31] R. Fraser, T. MacRae, and E. Suzuki, "Chain conformation in the collagen molecule," J Mol Biol, vol. 129, pp. 463-481, 1979.
  • [32] J. K. Rainey and M. C. Goh, "A statistically derived parameterization for the collagen triple‐helix," Protein Science, vol. 11, pp. 2748-2754, 2002.
  • [33] K. Kawahara, Y. Nishi, S. Nakamura, S. Uchiyama, Y. Nishiuchi, T. Nakazawa, T. Ohkubo, and Y. Kobayashi, "Effect of hydration on the stability of the collagen-like triple-helical structure of [4 (R)-hydroxyprolyl-4 (R)-hydroxyprolylglycine] 10," Biochemistry, vol. 44, pp. 15812-15822, 2005.
Birincil Dil en
Konular Mühendislik
Bölüm Makaleler
Yazarlar

Orcid: 0000-0002-9518-8952
Yazar: Mustafa Ünal (Sorumlu Yazar)
Kurum: KARAMANOGLU MEHMETBEY UNIVERSITY
Ülke: Turkey


Tarihler

Yayımlanma Tarihi : 28 Eylül 2019

Bibtex @araştırma makalesi { apjes515201, journal = {Akademik Platform Mühendislik ve Fen Bilimleri Dergisi}, issn = {}, eissn = {2147-4575}, address = {}, publisher = {Akademik Platform}, year = {2019}, volume = {7}, pages = {373 - 380}, doi = {10.21541/apjes.515201}, title = {Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis}, key = {cite}, author = {Ünal, Mustafa} }
APA Ünal, M . (2019). Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis. Akademik Platform Mühendislik ve Fen Bilimleri Dergisi , 7 (3) , 373-380 . DOI: 10.21541/apjes.515201
MLA Ünal, M . "Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis". Akademik Platform Mühendislik ve Fen Bilimleri Dergisi 7 (2019 ): 373-380 <https://dergipark.org.tr/tr/pub/apjes/issue/44190/515201>
Chicago Ünal, M . "Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis". Akademik Platform Mühendislik ve Fen Bilimleri Dergisi 7 (2019 ): 373-380
RIS TY - JOUR T1 - Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis AU - Mustafa Ünal Y1 - 2019 PY - 2019 N1 - doi: 10.21541/apjes.515201 DO - 10.21541/apjes.515201 T2 - Akademik Platform Mühendislik ve Fen Bilimleri Dergisi JF - Journal JO - JOR SP - 373 EP - 380 VL - 7 IS - 3 SN - -2147-4575 M3 - doi: 10.21541/apjes.515201 UR - https://doi.org/10.21541/apjes.515201 Y2 - 2019 ER -
EndNote %0 Akademik Platform Mühendislik ve Fen Bilimleri Dergisi Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis %A Mustafa Ünal %T Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis %D 2019 %J Akademik Platform Mühendislik ve Fen Bilimleri Dergisi %P -2147-4575 %V 7 %N 3 %R doi: 10.21541/apjes.515201 %U 10.21541/apjes.515201
ISNAD Ünal, Mustafa . "Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis". Akademik Platform Mühendislik ve Fen Bilimleri Dergisi 7 / 3 (Eylül 2019): 373-380 . https://doi.org/10.21541/apjes.515201
AMA Ünal M . Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis. APJES. 2019; 7(3): 373-380.
Vancouver Ünal M . Bound Water and Hydroxyproline are the essential contributors to collagen molecular stability: A Computational Analysis. Akademik Platform Mühendislik ve Fen Bilimleri Dergisi. 2019; 7(3): 380-373.