Fluorescent spectroscopy of collagen as a diagnostic tool in medicine

Authors

  • Łukasz Saletnik Department of Vascular and Internal Diseases, Faculty of Health Sciences, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, Bydgoszcz, Poland https://orcid.org/0000-0001-7847-4351
  • Roland Wesołowski Department of Medical Biology and Biochemistry, Faculty of Medicine, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, Bydgoszcz, Poland https://orcid.org/0000-0003-2673-8313

DOI:

https://doi.org/10.20883/medical.e584

Keywords:

collagen, cross-links, excitation spectra, emission spectra, fluorescence spectroscopy

Abstract

Medicine continuously needs to improve the existing diagnostic solutions or introduce new ones. Despite the fact that collagen is a well described protein, collagen-related diseases represent the disorders requiring improvement particularly in terms of research tools. These diseases include connective tissue diseases, keratoconus, where a change in the structure of collagen is observed causing a deformation of the cornea, as well as neoplasms, in which the amount of collagen is multiplied in cells.

Fluorescence spectroscopy constitutes a highly sensitive, non-invasive research method, thus, its use in medicine can contribute to the development of excellent diagnostic methods. This method allows to determine the changing amount of the tested fluorophores, as well as the change of the pH of the environment in which these fluorophores are located. Until now, numerous studies on collagen have been performed using fluorescence spectroscopy. However, a detailed analysis of the literature revealed some discrepancies which have been summarized in this paper.

The collected experimental results allowed to conclude that the discrepancies in the obtained fluorescence excitation and emission spectra of collagen may result from the structural richness of collagen. Another reason for the variability of the results is the different experimental conditions, i.e. the excitation and detection of collagen fluorescence at different wavelengths. Therefore, it should be emphasized that collagen spectroscopy constitutes an extremely promising method, although the determination of the exact conditions of the experiment and their standardization are required in the research on the diagnostic use of this technique.

Downloads

Download data is not yet available.

References

Georgakoudi I, Jacobson BC, Müller MG, Sheets EE, Badizadegan K, Carr-Locke DL, Crum CP, Boone CW, Dasari RR, Van Dam J, Feld MS. NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes. Cancer Res. 2002 Feb 1;62(3):682-7. PMID: 11830520.

Borisova E, Pavlova P, Pavlova E, Troyanova P, Avramov L. Optical biopsy of human skin – a tool for cutaneous tumours' diagnosis. International Journal Bioautomotion. 2021;16(1):53–72.

Lakowicz JR. Principles of fluorescence spectroscopy. 3rd ed. New York: Springer; 2006. 954 p.

Vishwanath K, Ramanujam N. Fluorescence Spectroscopy In Vivo. In: Meyers RA, editor. Encyclopedia of Analytical Chemistry [Internet]. Chichester, UK: John Wiley & Sons, Ltd; 2011 [cited 2021 Oct 20]. p. a0102.pub2. Available from: https://onlinelibrary.wiley.com/doi/10.1002/9780470027318.a0102.pub2.

Pu Y, Tang GC, Wang WB, Savage HE, Schantz SP, Alfano RR. Native fluorescence spectroscopic evaluation of chemotherapeutic effects on malignant cells using nonnegative matrix factorization analysis. Technol Cancer Res Treat. 2011 Apr;10(2):113-20. doi: 10.7785/tcrt.2012.500186. PMID: 21381789.

Gillies R, Zonios G, Anderson RR, Kollias N. Fluorescence excitation spectroscopy provides information about human skin in vivo. J Invest Dermatol. 2000 Oct;115(4):704-7. doi: 10.1046/j.1523-1747.2000.00091.x. PMID: 10998147.

Smirnova OD, Rogatkin DA, Litvinova KS. COLLAGEN AS IN VIVO QUANTITATIVE FLUORESCENT BIOMARKERS OF ABNORMAL TISSUE CHANGES. J Innov Opt Health Sci. 2012 Apr;05(02):1250010. doi: 10.1142/S1793545812500101.

Shoulders MD, Raines RT. Collagen structure and stability. Annu Rev Biochem. 2009;78:929-58. doi: 10.1146/annurev.biochem.77.032207.120833. PMID: 19344236; PMCID: PMC2846778.

Saito M, Marumo K, Fujii K, Ishioka N. Single-column high-performance liquid chromatographic-fluorescence detection of immature, mature, and senescent cross-links of collagen. Anal Biochem. 1997 Nov 1;253(1):26-32. doi: 10.1006/abio.1997.2350. PMID: 9356137.

Verzijl N, DeGroot J, Ben ZC, Brau-Benjamin O, Maroudas A, Bank RA, Mizrahi J, Schalkwijk CG, Thorpe SR, Baynes JW, Bijlsma JW, Lafeber FP, TeKoppele JM. Crosslinking by advanced glycation end products increases the stiffness of the collagen network in human articular cartilage: a possible mechanism through which age is a risk factor for osteoarthritis. Arthritis Rheum. 2002 Jan;46(1):114-23. doi: 10.1002/1529-0131(200201)46:1<114::AID-ART10025>3.0.CO;2-P. PMID: 11822407.

Monnier VM, Kohn RR, Cerami A. Accelerated age-related browning of human collagen in diabetes mellitus. Proc Natl Acad Sci U S A. 1984 Jan;81(2):583-7. doi: 10.1073/pnas.81.2.583. PMID: 6582514; PMCID: PMC344723.

Poole AR, Kobayashi M, Yasuda T, Laverty S, Mwale F, Kojima T, Sakai T, Wahl C, El-Maadawy S, Webb G, Tchetina E, Wu W. Type II collagen degradation and its regulation in articular cartilage in osteoarthritis. Ann Rheum Dis. 2002 Nov;61 Suppl 2(Suppl 2):ii78-81. doi: 10.1136/ard.61.suppl_2.ii78. PMID: 12379630; PMCID: PMC1766700.

Kollias N, Gillies R, Moran M, Kochevar IE, Anderson RR. Endogenous skin fluorescence includes bands that may serve as quantitative markers of aging and photoaging. J Invest Dermatol. 1998 Nov;111(5):776-80. doi: 10.1046/j.1523-1747.1998.00377.x. PMID: 9804337.

Pu Y, Wang W, Yang Y, Alfano RR. Stokes shift spectroscopic analysis of multifluorophores for human cancer detection in breast and prostate tissues. J Biomed Opt. 2013 Jan;18(1):17005. doi: 10.1117/1.JBO.18.1.017005. PMID: 23296086.

Deyl Z, Praus R, Sulcová H, Goldman JN. Fluorescence of collagen - properties of tyrosine residues and another fluorescent element in calf skin collagen. FEBS Lett. 1969 Nov 12;5(3):187-191. doi: 10.1016/0014-5793(69)80328-5. PMID: 11947273.

Ionita I, Dragne A, Gaidau C, Dragomir T. Collagen Fluorescence Measurements On Nanosilver Treated Leather. Romanian Reports in Physics. 2010 Jan 1;62.

Richards-Kortum R, Rava R, Baraga J, Fitzmaurice M, Kramer J, Feld M. Survey of the UV and Visible Spectroscopic Properties of Normal and Atherosclerotic Human Artery Using Fluorescence EEMs. In: Pratesi R, editor. Optronic Techniques in Diagnostic and Therapeutic Medicine [Internet]. Boston, MA: Springer US; 1991 [cited 2021 Oct 14]. p. 129–38. Available from: http://link.springer.com/10.1007/978-1-4615-3766-3_10

Teale FW, Weber G. Ultraviolet fluorescence of the aromatic amino acids. Biochem J. 1957 Mar;65(3):476-82. doi: 10.1042/bj0650476. PMID: 13412650; PMCID: PMC1199900.

Bolboacă S, Jäntschi L. Amino acids sequence analysis on collagen. Bulletin USAMV-CN. 63-64/2007.

Robins SP. Cross-linking of collagen. Isolation, structural characterization and glycosylation of pyridinoline. Biochem J. 1983 Oct 1;215(1):167-73. doi: 10.1042/bj2150167. PMID: 6626172; PMCID: PMC1152377.

Séro L, Sanguinet L, Blanchard P, Dang BT, Morel S, Richomme P, Séraphin D, Derbré S. Tuning a 96-well microtiter plate fluorescence-based assay to identify AGE inhibitors in crude plant extracts. Molecules. 2013 Nov 19;18(11):14320-39. doi: 10.3390/molecules181114320. PMID: 24256925; PMCID: PMC6270619.

Gahunia HK, Lough A, Vieth R, Pritzker K. A cartilage derived novel compound DDP (2,6-dimethyldifuro-8-pyrone): isolation, purification, and identification. J Rheumatol. 2002 Jan;29(1):147-53. PMID: 11824951.

Nakamura K, Nakazawa Y, Ienaga K. Acid-stable fluorescent advanced glycation end products: vesperlysines A, B, and C are formed as crosslinked products in the Maillard reaction between lysine or proteins with glucose. Biochem Biophys Res Commun. 1997 Mar 6;232(1):227-30. doi: 10.1006/bbrc.1997.6262. PMID: 9125137.

Monnier VM, Vishwanath V, Frank KE, Elmets CA, Dauchot P, Kohn RR. Relation between complications of type I diabetes mellitus and collagen-linked fluorescence. N Engl J Med. 1986 Feb 13;314(7):403-8. doi: 10.1056/NEJM198602133140702. PMID: 3945267.

Bailey AJ, Sims TJ, Avery NC, Halligan EP. Non-enzymic glycation of fibrous collagen: reaction products of glucose and ribose. Biochem J. 1995 Jan 15;305 ( Pt 2)(Pt 2):385-90. doi: 10.1042/bj3050385. PMID: 7832750; PMCID: PMC1136373.

Kinnunen J, Kokkonen HT, Kovanen V, Hauta-Kasari M, Vahimaa P, Lammi MJ, Töyräs J, Jurvelin JS. Nondestructive fluorescence-based quantification of threose-induced collagen cross-linking in bovine articular cartilage. J Biomed Opt. 2012 Sep;17(9):97003. doi: 10.1117/1.JBO.17.9.097003. PMID: 22975679.

Gkogkolou P, Böhm M. Advanced glycation end products: Key players in skin aging? Dermatoendocrinol. 2012 Jul 1;4(3):259-70. doi: 10.4161/derm.22028. PMID: 23467327; PMCID: PMC3583887.

Vashishth D. Advanced Glycation End-products and Bone Fractures. IBMS Bonekey. 2009 Aug;6(8):268-278. doi: 10.1138/20090390. PMID: 27158323; PMCID: PMC4856156.

Verzijl N, DeGroot J, Oldehinkel E, Bank RA, Thorpe SR, Baynes JW, Bayliss MT, Bijlsma JW, Lafeber FP, Tekoppele JM. Age-related accumulation of Maillard reaction products in human articular cartilage collagen. Biochem J. 2000 Sep 1;350 Pt 2(Pt 2):381-7. PMID: 10947951; PMCID: PMC1221264.

Hirose J, Yamabe S, Takada K, Okamoto N, Nagai R, Mizuta H. Immunohistochemical distribution of advanced glycation end products (AGEs) in human osteoarthritic cartilage. Acta Histochem. 2011 Oct;113(6):613-8. doi: 10.1016/j.acthis.2010.06.007. Epub 2010 Jul 24. PMID: 20656335.

Prabhakaram M, Cheng Q, Feather MS, Ortwerth BJ. Structural elucidation of a novel lysine-lysine crosslink generated in a glycation reaction with L-threose. Amino Acids. 1997 Sep;12(3–4):225–36.

Degenhardt TP, Thorpe SR, Baynes JW. Chemical modification of proteins by methylglyoxal. Cell Mol Biol (Noisy-le-grand). 1998 Nov;44(7):1139-45. PMID: 9846896.

Basta G, Schmidt AM, De Caterina R. Advanced glycation end products and vascular inflammation: implications for accelerated atherosclerosis in diabetes. Cardiovasc Res. 2004 Sep 1;63(4):582-92. doi: 10.1016/j.cardiores.2004.05.001. PMID: 15306213.

Suárez G, Rajaram R, Bhuyan KC, Oronsky AL, Goidl JA. Administration of an aldose reductase inhibitor induces a decrease of collagen fluorescence in diabetic rats. J Clin Invest. 1988 Aug;82(2):624-7. doi: 10.1172/JCI113641. PMID: 3136193; PMCID: PMC303557.

Sionkowska A, Kamińska A. Changes induced by ultraviolet light in fluorescence of collagen in the presence of β-carotene. Journal of Photochemistry and Photobiology A: Chemistry. 1999 Feb;120(3):207–10. doi:10.1016/S1010-6030(98)00427-4.

Wu K, Liu W, Li G. The aggregation behavior of native collagen in dilute solution studied by intrinsic fluorescence and external probing. Spectrochim Acta A Mol Biomol Spectrosc. 2013 Feb;102:186-93. doi: 10.1016/j.saa.2012.10.048. Epub 2012 Nov 1. PMID: 23220534.

Downloads

Published

2022-01-20

How to Cite

1.
Saletnik Łukasz, Wesołowski R. Fluorescent spectroscopy of collagen as a diagnostic tool in medicine. JMS [Internet]. 2022 Jan. 20 [cited 2024 Mar. 28];91(1):e584. Available from: https://jms.ump.edu.pl/index.php/JMS/article/view/584

Issue

Section

Review Papers
Received 2021-11-07
Accepted 2021-12-12
Published 2022-01-20