Share This Article:

In silico Study on Sulfated and Non-Sulfated Carbohydrate Chains from Proteoglycans in Cnidaria and Interaction with Collagen

Abstract Full-Text HTML Download Download as PDF (Size:3547KB) PP. 123-133
DOI: 10.4236/ojpc.2012.22017    3,811 Downloads   7,512 Views   Citations

ABSTRACT

Proteoglycans and collagen molecules are interacting with each other thereby forming various connective tissues. The sulfation pattern of proteoglycans differs depending on the kind of tissue and/or the degree of maturation. Tissues from Cnidaria are suitable examples for exploration of the effects in relation to the presence and the absence of sulfate groups, when studying characteristic fragments of the long proteoglycan carbohydrate chains in silico. It has been described that a non-sulfated chondroitin appears as a scaffold in early morphogenesis of all nematocyst types in Hydra. On the other hand, sulfated glucosaminoglycans play an important role in various developmental processes of Cnidaria. In order to understand this biological phenomenon on a sub-molecular level we have analysed the structures of sulfated and non-sulfated proteoglycan carbohydrate chains as well as the structure of diverse collagen molecules with computational methods including quantum chemical calculations. The strong interactions between the sulfate groups of the carbohydrates moieties in proteoglycans and positively charged regions of collagen are essential in stabilizing various Cnidaria tissues but could hinder the nematocyst formation and its proper function. The results of our quantum chemical calculations show that the sulfation pattern has a significant effect on the conformation of chondroitin structures under study.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

T. Eckert, S. Stötzel, M. Burg-Roderfeld, J. Sewing, T. Lütteke, N. E. Nifantiev, J. F. G. Vliegenthart and H. Siebert, "In silico Study on Sulfated and Non-Sulfated Carbohydrate Chains from Proteoglycans in Cnidaria and Interaction with Collagen," Open Journal of Physical Chemistry, Vol. 2 No. 2, 2012, pp. 123-133. doi: 10.4236/ojpc.2012.22017.

References

[1] T. De Beer, A. Inui, H. Tsuda, K. Sugahara and J. F. G. Vliegenthart, “Polydispersity in Sulfation Profile of Oligosaccharide Alditols Isolated from the Protein-Linkage Region and the Repeating Disaccharide Region of Chondroitin 4-Sulfate of Bovine Nasal Septal Cartilage,” European Journal of Biochemistry, Vol. 240, No. 3, 1996, pp. 789-797. doi:10.1111/j.1432-1033.1996.0789h.x
[2] P. Adamczyk, C. Zenkert, P. G. Balasubramanian, S. Yamada, S. Murakoshi, K. Sugahara, J. S. Hwang, T. Gojobori, T. W. Holstein and S. ?zbek, “A Non-Sulfated Chondroitin Stabilizes Membrane Tubulation in Cnidarian Organelles,” The Journal of Biological Chemistry, Vol. 285, 2010, pp. 25613-25623. doi:10.1074/jbc.M110.107904
[3] S. Yamada, H. Morimoto, T. Fujisawa and K. Sugahara, “Glycosaminglycans in Hydra Magnipapillata (Hydrozoa, Cnidaria): Demonstration of Chondroitin in the Developing Nematocyst, the Sting Organelle, and Structural Characterizayion of Glycosaminoglycans,” Glycobiology, Vol. 17, No. 8, 2007, pp. 886-894. doi:10.1093/glycob/cwm051
[4] H.-C. Siebert, E. Tajkhorshid and J. Dabrowski, “Barrier to Rotation around the Csp2-Csp2 Bond of the Ketoaldehyde Enol Ether MeC(O)==CH-OEt as Determined by 13C NMR and ab Initio Calculation,” The Journal of Physical Chemistry A, Vol. 105, No. 3, 2001, pp. 8488-8494. doi:10.1021/jp004476g
[5] J. H. van Lenthe, D. H. W. de Boer, R. W. A. Havenith, R. Schauer and H.-C. Siebert, “Ab Initio Calculations on Various Sialic Acids Provide Valuable Information about Sialic Acid-Specific Enzymes,” Journal of Molecular Structure: THEOCHEM, Vol. 667, No. 19-3, 2004, pp. 29-37. doi:10.1016/j.theochem.2004.01.013
[6] M. Remko and M. Hricovíni, “Theoretical Study of Structure and Properties of Hexuronic Acid and D-Glucosamine Structural Units of Glycosaminoglycans,” Structural Chemistry, Vol. 18, No. 5, 2007, pp. 537-547. doi:10.1007/s11224-007-9181-y
[7] M. Hricovíni, E. Scholtzová and F. Bízik, “B3LYP/6311++G** Study of Structure and Spin-Spin Coupling Constant in Heparin Disaccharide,” Carbohydrate Research, Vol. 342, No. 10, 2007, pp. 1350-1356. doi:10.1016/j.carres.2007.03.020
[8] E. Scholtzová, P. Mach and M. Hricovíni, “Structure of Sulfated Monosaccharides Studied by Quantum Chemical Methods,” Molecules, Vol. 8, No. 11, 2003, pp. 770-779. doi:10.3390/81100770
[9] “Hyperchem Professional 8.0,” Hypercube, Inc., Gainesville, 2007.
[10] M. J. Frisch, et al., “Gaussian 03, Revision B.03,” Gaussian, Inc., Pittsburgh, 2003.
[11] “Molegro-Trial Version 3.0.0,” 2008.
[12] H.-C. Siebert, M. Burg-Roderfeld, T. Eckert, S. St?tzel, U. Kirch, T. Diercks, M. J. Humphries, M. Frank, R. Wechselberger, E. Tajkhorshid and S. Oesser, “Interaction of tne α2A Domain of Integrin with Small Collagen Fragments,” Protein & Cell, Vol. 1, No. 4, 2010, pp. 393-405.
[13] A. G. Gerbst, N. E. Ustuzhanina, A. A. Grachev, E. A. Khatuntseva, D. E. Tsvetkov, A. S. Shashkov, A. I. Usov, M. E. Preobrazhenskaya, N. A. Ushakova and N. E. Nifantiev, “Synthesis, NMR and Conformational Studies of Fucoidan Fragments. V.[1] Linear 4,4’,4’’‐Tri‐O‐Sulfated and Parent Non‐Sulfated (1→3)‐Fucotrioside Fragments,” Journal of Carbohydrate Chemistry, Vol. 22, No. 2, 2003, pp. 109-122. doi:10.1081/CAR-120020481
[14] V. B. Krylov, A. A. Grachev, N. E. Ustyuzhanina, N. A. Ushakova, M. E. Preobrazhenskaya, N. I. Kozlova, M. N. Portsel, I. N. Konovalova, V. U. Novikov, H.-C. Siebert, A. S. Shashkov and N. E. Nifantiev, “Preliminary Structural Characterization, Anti-Inflammatory and Anticoagulant Activities of Chondroitin Sulfates from Marine Fish Cartilage,” Russian Chemical Bulletin, Vol. 60, 2011, pp. 746-753.
[15] E. Pokidysheva, A. G. Milbradt, S. Meier, C. Renner, D. Haussinger, H. P. Bachinger, L. Moroder, S. Grzesiek, T. W. Holstein, S. Ozbek and J. Engel, “The Structure of the Cys-Rich Terminal Domain of Hydra Minicollagen, Which Is Involved in Disulfide Networks of the Nematocyst Wall,” The Journal of Biological Chemistry, Vol. 279, 2004, pp. 30395-30401. doi:10.1074/jbc.M403734200
[16] J. Emsley, G. Knight, R. Farndale, M. Barnes and R. Liddington, “Structural Basis of Collagen Recognition by Integrin α2β1,” Cell, Vol. 101, No. 1, 2000, pp. 47-56. doi:10.1016/S0092-8674(00)80622-4
[17] A. G. Milbradt, C. Boulègue, L. Moroder and C. Renner, “The Two Cysteine-rich Head Domains of Minicollagen from Hydra Nematocysts Differ in their Cystine Framework and Overall Fold Despite an Identical Cysteine Sequence Pattern,” Journal of Molecular Biology, Vol. 354, No. 3, 2005, pp. 591-600. doi:10.1016/j.jmb.2005.09.080
[18] S. Meier, D. Haussinger, E. Pokidysheva, H. P. Bachinger and S. Grzesiek, “Determination of a High-Precision NMR Structure of the Minicollagen Cysteine Rich Domain from Hydra and Characterization of Its Disulfide Bond Formation,” FEBS Letters, Vol. 569, No. 1, 2004, pp. 112-116. doi:10.1016/j.febslet.2004.05.034
[19] J.-O. Lee, P. Rieu, M. A. Arnaout and R. Liddington, “Crystal Structure of the A Domain from the a SubUnit of Integrin CR3 (CD11 b/CD18),” Cell, Vol. 80, No. 4, 1995, pp. 631-638. doi:10.1016/0092-8674(95)90517-0
[20] S. Szczepanek, M. Cikala and C. N. David, “Poly-Gamma-Glutamate Synthesis during Formation of Nematocyst Capsules in Hydra,” Journal of Cell Science, Vol. 115, 2002, pp. 745-751.
[21] S. Berking and K. Herrmann, “Formation and Discharge of Nematocysts Is Controlled by a Proton Gradient across the Cyst Membrane,” Helgoland Marine Research, Vol. 60, No. 3, 2006, pp. 180-188. doi:10.1007/s10152-005-0019-y
[22] S. ?zbek, P. G. Balasubramanian and T. W. Holstein, “Cnidocyst Structure and the Biomechanics of Discharge,” Toxicon, Vol. 54, No. 8, 2009, pp. 1038-1045. doi:10.1016/j.toxicon.2009.03.006
[23] T. W. Holstein, M. Benoit, G. V. Herder, G. Wanner, C. N. David and H. E. Gaub, “Fibrous Mini-Collagens in Hydra Nematocysts,” Science, Vol. 265, No. 5170, 1994, pp. 402-404. doi:10.1126/science.265.5170.402
[24] G. Tettamanti, A. Grimaldi, T. Congiu,G. Perletti, M. Raspanti, R. Valvassori and M. de Eguileor, “Collagen Reorganization in Leech Wound Healing,” Biology of the Cell, Vol. 97, No. 7, 2005, pp. 557-568. doi:10.1042/BC20040085
[25] N. Ohta, M. Sato, K. Ushida, M. Kokubo, T. Baba, K. Taniguchi, M. Urai, K. Kihira and J. Mochida, “Jellyfish Mucin May Have Potential Disease-Modifying Effects on Osteoarthritis,” BMC Biotechnology, Vol. 9, No. 98, 2009, pp. 1-11. doi:10.1186/1472-6750-9-98
[26] N. Sapay, E. Cabannes, M. Petitou and A. Imberty, “Molecular Modeling of the Interaction between Heparan Sulfate and Cellular Growth Factors: Bringing Pieces Together,” Glycobiology, Vol. 21, No. 9, 2011, pp. 1181-1193. doi:10.1093/glycob/cwr052
[27] D. O. Croci, et al., “Fucans, but Not Fucomannoglucuronans, Determine the Biological Activities of Sulfated Polysaccharides from Laminaria Saccharina Brown Seaweed,” PLoS ONE, Vol. 6, 2011, pp. 1-10. doi:10.1371/journal.pone.0017283
[28] O. Raabe, C. Reich, S. Wenisch, A. Hild, M. Burg-Roderfeld, H.-C. Siebert and S. Arnhold, “Hydrolyzed Fish Collagen Induced Chondrogenic Differentiation of Equine Adipose Tissue-Derived Stromal Cells,” Histochemistry & Cell Biology, Vol. 134, No. 6, 2010, pp. 545-554. doi:10.1007/s00418-010-0760-4
[29] U. Technau and R. E. Steele, “Evolutionary Crossroads in Developmental Biology: Cnidaria,” Development, Vol. 138, 2011, pp. 1447-1458. doi:10.1242/dev.048959
[30] T. C. G. Bosch, “Hydra and the Evolution of Stem Cells,” BioEssays, Vol. 31, No. 4, 2009, pp. 478-486. doi:10.1002/bies.200800183
[31] J. S. Hwang, Y. Takaku, T. Momose, P. Adamczyk, S. ?zbek, K. Ikeo, K. Khalturin, G. Hemmrich, T. C. G. Bosch, T. W. Holstein, C. N. David and T. Gojobori, “Nematogalectin, a Nematocyst Protein with GlyXY and Galectin Domains, Demonstrates Nematocyte-Specific Alternative Splicing in Hydra,” PNAS, Vol. 107, No. 43, 2010, pp. 18539-18544. doi:10.1073/pnas.1003256107
[32] A. M. Wu, T. Singh, J.-H. Liu, S. André, M. Lensch, H.-C. Siebert, M. Krzeminski, A. M. J. J. Bonvin, H. Kaltner, J. H. Wu and H.-J. Gabius, “Adhesion/Growth-Regulatory Galectins: Insights into Their Ligand Selectivity Using Natural Glycoproteins and Glycotopes, ” Advances in Experimental Medicine and Biology, Vol. 705, 2011, pp. 117-141. doi:10.1007/978-1-4419-7877-6_7
[33] S. St?tzel, M. Schurink, H. Wienk, U. Siebler, M. Burg-Roderfeld, T. Eckert, B. Kulik, R. Wechselberger, J. Sewing, J. Steinmeyer, S. Oesser, R. Boelens and H.-C. Siebert, “Molecular Organization of Different Collagen Hydrolysates and Collagen Fragments as Revealed by a Combination of Atomic Force Microscopy (AFM) and Diffusion Ordered NMR Spectroscopy (DOSY),” ChemPhysChem, 2012.

  
comments powered by Disqus

Copyright © 2018 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.