Display options
Share it on

J Biomed Mater Res A. 2021 Sep;109(9):1646-1656. doi: 10.1002/jbm.a.37160. Epub 2021 Mar 09.

A biphasic response of polymerized Type 1 collagen architectures to dermatan sulfate.

Journal of biomedical materials research. Part A

Konkada Manattayil Jyothsna, Purba Sarkar, Keshav Kumar Jha, Lal Krishna A S, Varun Raghunathan, Ramray Bhat

Affiliations

  1. Department of Electrical Communication Engineering, Indian Institute of Science, Bangalore, Karnataka, India.
  2. Department of Molecular Reproduction, Development and Genetics, Indian Institute of Science, Bangalore, Karnataka, India.
  3. Department of Functional Interfaces, Leibniz Institute of Photonic Technology, Jena, Germany.

PMID: 33687134 DOI: 10.1002/jbm.a.37160

Abstract

Collagen I, the most abundant extracellular matrix (ECM) protein in vertebrate tissues provides mechanical durability to tissue microenvironments and regulates cell function. Its fibrillogenesis in biological milieu is predominantly regulated by dermatan sulfate proteoglycans, proteins conjugated with iduronic acid-containing dermatan sulfate (DS) glycosaminoglycans (GAG). Although DS is known to regulate tissue function through its modulation of Coll I architecture, a precise understanding of the latter remains elusive. We investigated this problem by visualizing the fibrillar pattern of fixed Coll I gels polymerized in the presence of varying concentrations of DS using second harmonic generation microscopy. Measuring mean second harmonic generation signal (which estimates the ordering of the fibrils), and surface occupancy (which estimates the space occupied by fibrils) supported by confocal reflectance microscopy, our observations indicated that the effect on fibril pattern of DS is contextual upon the latter's concentrations: Lower levels of DS resulted in sparse disorganized fibrils; higher levels restore organization, with fibrils occupying greater space. An appropriate change in elasticity as a result of DS levels was also observed through atomic force microscopy. Examination of dye-based GAG staining and scanning electron microscopy suggested distinct constitutions of Coll I gels when polymerized with higher and lower levels of DS. We observed that adhesion of the invasive ovarian cancer cells SKOV3 decreased for lower DS levels but was partially restored at higher DS levels. Our study shows how the Coll I gel pattern-tuning of DS is of relevance for understanding its biomaterial applications and possibly, pathophysiological functions.

© 2021 Wiley Periodicals LLC.

Keywords: collagen I; dermatan sulfate; second harmonic generation

References

  1. Mouw JK, Ou G, Weaver VM. Extracellular matrix assembly: a multiscale deconstruction. Nat Rev Mol Cell Biol. 2014;15(12):771-785. - PubMed
  2. Theocharis AD, Skandalis SS, Gialeli C, Karamanos NK. Extracellular matrix structure. Adv Drug Deliv Rev. 2016;97:4-27. - PubMed
  3. Bonnans C, Chou J, Werb Z. Remodelling the extracellular matrix in development and disease. Nat Rev Mol Cell Biol. 2014;15(12):786-801. - PubMed
  4. Scott JE. Proteoglycan-fibrillar collagen interactions. Biochem J. 1988;252(2):313-323. - PubMed
  5. Yanagishita M. Function of proteoglycans in the extracellular matrix. Acta Pathol Jpn. 1993;43(6):283-293. - PubMed
  6. Nash MA, Deavers MT, Freedman RS. The expression of decorin in human ovarian tumors. Clin Cancer Res. 2002;8(6):1754-1760. - PubMed
  7. Iozzo RV, Murdoch AD. Proteoglycans of the extracellular environment: clues from the gene and protein side offer novel perspectives in molecular diversity and function. FASEB J. 1996;10(5):598-614. - PubMed
  8. Chen S, Birk DE. The regulatory roles of small leucine-rich proteoglycans in extracellular matrix assembly. FEBS J. 2013;280(10):2120-2137. - PubMed
  9. Reese SP, Underwood CJ, Weiss JA. Effects of decorin proteoglycan on fibrillogenesis, ultrastructure, and mechanics of type I collagen gels. Matrix Biol. 2013;32(7-8):414-423. - PubMed
  10. Ameye L, Young MF. Mice deficient in small leucine-rich proteoglycans: novel in vivo models for osteoporosis, osteoarthritis, Ehlers-Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology. 2002;12(9):107R-116R. - PubMed
  11. Kowitsch A, Zhou G, Groth T. Medical application of glycosaminoglycans: a review. J Tissue Eng Regen Med. 2018;12(1):e23-e41. - PubMed
  12. Tierney CM, Jaasma MJ, O'Brien FJ. Osteoblast activity on collagen-GAG scaffolds is affected by collagen and GAG concentrations. J Biomed Mater Res A. 2009;91(1):92-101. - PubMed
  13. Prestwich GD. Hyaluronic acid-based clinical biomaterials derived for cell and molecule delivery in regenerative medicine. J Control Release. 2011;155(2):193-199. - PubMed
  14. Vallen MJ, Schmidt S, Oosterhof A, Bulten J, Massuger LF, van Kuppevelt TH. Primary ovarian carcinomas and abdominal metastasis contain 4,6-disulfated chondroitin sulfate rich regions, which provide adhesive properties to tumour cells. PloS One. 2014;9(11):e111806. - PubMed
  15. Li HP, Komuta Y, Kimura-Kuroda J, van Kuppevelt TH, Kawano H. Roles of chondroitin sulfate and dermatan sulfate in the formation of a lesion scar and axonal regeneration after traumatic injury of the mouse brain. J Neurotrauma. 2013;30(5):413-425. - PubMed
  16. Junqueira LC, Montes GS. Biology of collagen-proteoglycan interaction. Arch Histol Jpn. 1983;46(5):589-629. - PubMed
  17. Douglas T, Heinemann S, Mietrach C, et al. Interactions of collagen types I and II with chondroitin sulfates A-C and their effect on osteoblast adhesion. Biomacromolecules. 2007;8(4):1085-1092. - PubMed
  18. Gouignard N, Maccarana M, Strate I, von Stedingk K, Malmstrom A, Pera EM. Musculocontractural Ehlers-Danlos syndrome and neurocristopathies: dermatan sulfate is required for Xenopus neural crest cells to migrate and adhere to fibronectin. Dis Model Mech. 2016;9(6):607-620. - PubMed
  19. Mizumoto S, Kosho T, Yamada S, Sugahara K. Pathophysiological significance of dermatan sulfate proteoglycans revealed by human genetic disorders. Pharmaceuticals (Basel). 2017;10(2):34. - PubMed
  20. Nakamura A, Osonoi T, Terauchi Y. Relationship between urinary sodium excretion and pioglitazone-induced edema. J Diabetes Investig. 2010;1(5):208-211. - PubMed
  21. Appunni S, Anand V, Khandelwal M, Gupta N, Rubens M, Sharma A. Small leucine rich proteoglycans (decorin, biglycan and lumican) in cancer. Clin Chim Acta. 2019;491:1-7. - PubMed
  22. Bostrom P, Sainio A, Eigeliene N, et al. Human metaplastic breast carcinoma and Decorin. Cancer Microenviron. 2017;10(1-3):39-48. - PubMed
  23. Pavone FS, Campagnola PJ. Second Harmonic Generation Imaging. Boca Raton, FL: CRC Press; 2016. - PubMed
  24. Masters BR, So P: Handbook of Biomedical Nonlinear Optical Microscopy, USA: Oxford University Press; 2008. - PubMed
  25. Campagnola P, Dong CY. Second harmonic generation microscopy: principles and applications to disease diagnosis. Laser Photonics Rev. 2011;5(1):13-26. - PubMed
  26. Freund I, Deutsch M, Sprecher A. Connective tissue polarity: optical second-harmonic microscopy, crossed-beam summation,and small-angle scattering in rat-tail tendon. Biophys J. 1986;50(4):693-712. - PubMed
  27. Campagnola PJ, Dong CY. Second harmonic generation microscopy: principles and applications to disease diagnosis. Laser Photonics Rev. 2011;5(1):13-26. - PubMed
  28. Campagnola P. Second harmonic generation imaging microscopy: applications to diseases diagnostics. Anal Chem. 2011;83(9):3224-3231. - PubMed
  29. Rocha-Mendoza I, Yankelevich DR, Wang M, et al. Sum frequency vibrational spectroscopy: the molecular origins of the optical second-order nonlinearity of collagen. 2007;93(12):4433-4444. - PubMed
  30. W M, CW F, S L, XS X. Coherent nonlinear optical imaging: beyond fluorescence microscopy. Annu Rev Phys Chem. 2011;62:507-530. - PubMed
  31. Campbell KR, Campagnola PJ. Assessing local stromal alterations in human ovarian cancer subtypes via second harmonic generation microscopy and analysis. J Biomed Opt. 2017;22(11):1-7. - PubMed
  32. Watson JM, Rice PF, Marion SL, et al. Analysis of second-harmonic-generation microscopy in a mouse model of ovarian carcinoma. J Biomed Opt. 2012;17(7):076002. - PubMed
  33. Campbell KR, Chaudhary R, Handel JM, Patankar MS, Campagnola PJ. Polarization-resolved second harmonic generation imaging of human ovarian cancer. J Biomed Opt. 2018;23(6):1-8. - PubMed
  34. Chu S-W, Tai S-P, Chan M-C, et al. Thickness dependence of optical second harmonic generation in collagen fibrils. Opt Express. 2007;15(19):12005-12010. - PubMed
  35. A F, W N, K V, M. V: Medical image computing and computer-assisted Interventation. 1998. - PubMed
  36. Xu S, Kang CH, Gou X, et al. Quantification of liver fibrosis via second harmonic imaging of the Glisson's capsule from liver surface. J Biophotonics. 2016;9(4):351-363. - PubMed
  37. OTSU N. A Threshold selection method from gray-level histograms. IEEE Trans Syst Man Cybern Syst. 1979;9(1):62-66. - PubMed
  38. Chen X, Nadiarynkh O, Plotnikov S, Campagnola PJ. Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat Protoc. 2012;7(4):654-669. - PubMed
  39. Muir IF, Padilla-Lamb A, Stewart JE, Wheatley DN. Growth inhibition of cultured fibroblasts by extracts from human dermis. Br J Plast Surg. 1997;50(3):186-193. - PubMed
  40. Kuiper NJ, Sharma A. A detailed quantitative outcome measure of glycosaminoglycans in human articular cartilage for cell therapy and tissue engineering strategies. Osteoarthr Cartil. 2015;23(12):2233-2241. - PubMed
  41. Tovar AM, de Mattos DA, Stelling MP, Sarcinelli-Luz BS, Nazareth RA, Mourao PA. Dermatan sulfate is the predominant antithrombotic glycosaminoglycan in vessel walls: implications for a possible physiological function of heparin cofactor II. Biochim Biophys Acta. 2005;1740(1):45-53. - PubMed
  42. Ellis BJ, Lujan TJ, Dalton MS, Weiss JA. Medial collateral ligament insertion site and contact forces in the ACL-deficient knee. J Orthop Res. 2006;24(4):800-810. - PubMed
  43. Lin KH, Hino H, Maeda S, Inagaki H, Airat JV, Saito T. Albumin synthesis by rat hepatocytes cultured on collagen gels is sustained specifically by heparin. Exp Cell Res. 1995;219(2):717-721. - PubMed
  44. Kano K, Miyano T, Kato S. Effects of glycosaminoglycans on the development of in vitro-matured and -fertilized porcine oocytes to the blastocyst stage in vitro. Biol Reprod. 1998;58(5):1226-1232. - PubMed
  45. Abbadini M, Zhu GJ, Maggi A, Pangrazzi J, Donati MB, Mussoni L. Dermatan sulphate induces plasminogen activator release in the perfused rat hindquarters. Blood. 1987;70(6):1858-1860. - PubMed
  46. Eriksen GV, Malmstrom A, Uldbjerg N, Huszar G. A follicular fluid chondroitin sulfate proteoglycan improves the retention of motility and velocity of human spermatozoa. Fertil Steril. 1994;62(3):618-623. - PubMed
  47. Lin KH, Maeda S, Inagaki H, Saito T. Long-term culture of primary rat hepatocytes on heparin- or lambda carrageenan-containing collagen gels. Biosci Biotechnol Biochem. 1997;61(6):971-974. - PubMed
  48. Obrink B. A study of the interactions between monomeric tropocollagen and glycosaminoglycans. Eur J Biochem. 1973;33(2):387-400. - PubMed
  49. McLaughlin RW, De Stigter JK, Sikkink LA, Baden EM, Ramirez-Alvarado M. The effects of sodium sulfate, glycosaminoglycans, and Congo red on the structure, stability, and amyloid formation of an immunoglobulin light-chain protein. Protein Sci. 2006;15(7):1710-1722. - PubMed
  50. Thelin MA, Svensson KJ, Shi X, et al. Dermatan sulfate is involved in the tumorigenic properties of esophagus squamous cell carcinoma. Cancer Res. 2012;72(8):1943-1952. - PubMed
  51. Coster L, Fransson LA, Sheehan J, Nieduszynski IA, Phelps CF. Self-association of dermatan sulphate proteoglycans from bovine sclera. Biochem J. 1981;197(2):483-490. - PubMed
  52. Racey TJ, Rochon P, Mori F, Neville GA. Examination of a possible role for dermatan sulfate in the aggregation of commercial heparin samples. J Pharm Sci. 1989;78(3):214-218. - PubMed
  53. Yung S, Thomas GJ, Stylianou E, Williams JD, Coles GA, Davies M. Source of peritoneal proteoglycans. Human peritoneal mesothelial cells synthesize and secrete mainly small dermatan sulfate proteoglycans. Am J Pathol. 1995;146(2):520-529. - PubMed
  54. Benias PC, Wells RG, Sackey-Aboagye B, et al. Structure and distribution of an unrecognized Interstitium in human tissues. Sci Rep. 2018;8(1):4947. - PubMed
  55. Scott PG, Nakano T, Dodd CM, Pringle GA, Kuc IM. Proteoglycans of the articular disc of the bovine temporomandibular joint. II. Low molecular weight dermatan sulphate proteoglycan. Matrix. 1989;9(4):284-292. - PubMed
  56. McKee TJ, Perlman G, Morris M, Komarova SV. Extracellular matrix composition of connective tissues: a systematic review and meta-analysis. Sci Rep. 2019;9(1):10542. - PubMed
  57. Mauviel A, Santra M, Chen YQ, Uitto J, Iozzo RV. Transcriptional regulation of decorin gene expression. Induction by quiescence and repression by tumor necrosis factor-alpha. J Biol Chem. 1995;270(19):11692-11700. - PubMed
  58. Trowbridge JM, Gallo RL. Dermatan sulfate: new functions from an old glycosaminoglycan. Glycobiology. 2002;12(9):117R-125R. - PubMed
  59. Chen X, Huang Z, Xi G, Chen Y, Lin D, Wang J, Li Z, Sun L, Chen J, Chen R: Quantitative analysis of collagen change between normal and cancerous thyroid tissues based on SHG method. In: Tenth international conference on photonics and imaging in biology and medicine (PIBM 2011). 2012. - PubMed
  60. Campbell KR, Chaudhary R, Montano M, Iozzo RV, Bushman WA, Campagnola PJ. Second-harmonic generation microscopy analysis reveals proteoglycan decorin is necessary for proper collagen organization in prostate. J Biomed Opt. 2019;24(6):1-8. - PubMed
  61. Tilbury K, Campagnola PJ. Applications of second-harmonic generation imaging microscopy in ovarian and breast cancer. Perspect Medicin Chem. 2015;7:21-32. - PubMed
  62. LIAO P-S, CHEN T-S, CHUNG P-C. A fast algorithm for multilevel thresholding. J Inf Sci Eng. 2001;17(5):713-727. - PubMed
  63. Bredfeldt JS, Liu Y, Pehlke CA, et al. Computational segmentation of collagen fibers from second-harmonic generation images of breast cancer. J Biomed Opt. 2014;19:016007. - PubMed
  64. LBM G, Alex C-T, Wang F, et al. Collagen morphology and texture analysis: from statistics to classification. Sci Rep. 2013;3(2190):1-10. https://doi.org/10.1038/srep02190. - PubMed
  65. Williams RM, Zipfel WR, Webb WW. Interpreting second-harmonic generation images of collagen I fibrils. Biophys J. 2005;88:1377-1386. - PubMed
  66. Raghunathan V, Han Y, Korth O, Ge NH, Potma EO. Rapid vibrational imaging with sum frequency generation microscopy. Opt Lett. 2011;36(19):3891-3893. - PubMed

Publication Types

Grant support