Colorful protein-based fluorescent probes for collagen imaging

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Aper, Stijn J A ^a   Van Spreeuwel, Ariane C C ^a   Van Turnhout, Mark C ^a   Van Der Linden, Ardjan J ^a   Pieters, Pascal A ^a   Van Der Zon, Nick L L ^a   De La Rambelje, Ser L ^a   Bouten, Carlijn V C ^a   Merkx, Maarten ^a  

^a EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; COLLAGEN; FLUORESCENT DYE; BACTERIAL PROTEIN; CARBOXYLIC ACID; HYBRID PROTEIN; OREGON GREEN 488 CARBOXYLIC ACID;

AFFINITY CHROMATOGRAPHY; ANIMAL EXPERIMENT; ARTICLE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; DEVELOPMENTAL BIOLOGY; FLUORESCENCE MICROSCOPY; FLUORESCENCE SPECTROSCOPY; GENETIC CODE; IMAGE ANALYSIS; IN VITRO STUDY; MOUSE; NONHUMAN; OPEN READING FRAME; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; STAPHYLOCOCCUS AUREUS; SWINE; TISSUE ENGINEERING; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE CELL; CELL CULTURE; CHEMISTRY; CYTOLOGY; FEMALE; FIBROBLAST; HUMAN; METABOLISM; NEWBORN; PERICARDIUM; PHOTON; SKIN; SPECTROFLUOROMETRY;

ANIMALS; ANIMALS, NEWBORN; BACTERIAL PROTEINS; CARBOXYLIC ACIDS; CELLS, CULTURED; COLLAGEN; FEMALE; FIBROBLASTS; FLUORESCENT DYES; HUMANS; MICE; MICE, INBRED C57BL; MYOCYTES, CARDIAC; PERICARDIUM; PHOTONS; RECOMBINANT FUSION PROTEINS; SKIN; SPECTROMETRY, FLUORESCENCE;

EID: 84916614237     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114983     Document Type: Article

References (52)

1. Boerboom RA, Krahn KN, Megens RT, van Zandvoort MA, Merkx M, et al. (2007) High resolution imaging of collagen organisation and synthesis using a versatile collagen specific probe. J Struct Biol 159: 392-399.
2. Gelse K, Poschl E, Aigner T (2003) Collagens - structure, function, and biosynthesis. Adv Drug Deliv Rev 55: 1531-1546.
3. Krahn KN, Bouten CV, van Tuijl S, van Zandvoort MA, Merkx M (2006) Fluorescently labeled collagen binding proteins allow specific visualization of collagen in tissues and live cell culture. Anal Biochem 350: 177-185.
4. Li Y, Yu SM (2013) Targeting and mimicking collagens via triple helical peptide assembly. Curr Opin Chem Biol 17: 968-975.
5. Zong Y, Xu Y, Liang X, Keene DR, Hook A, et al. (2005) A 'Collagen Hug' model for Staphylococcus aureus CNA binding to collagen. EMBO J 24: 4224-4236.
6. Glassman W, Byamsmith M, Garfield RE (1995) Changes in rat cervical collagen during gestation and after antiprogesterone treatment as measured in vivo with light-induced autofluorescence. Am J Obstet Gynecol 173: 1550-1556.
7. So P, Kim H, Kochevar I (1998) Two-Photon deep tissue ex vivo imaging of mouse dermal and subcutaneous structures. Opt Express 3: 339-350.
8. Voytik-Harbin SL, Rajwa B, Robinson JP (2001) Three-dimensional imaging of extracellular matrix and extracellular matrix-cell interactions. Methods Cell Biol 63: 583-597.
9. Campagnola PJ, Millard AC, Terasaki M, Hoppe PE, Malone CJ, et al. (2002) Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues. Biophys J 82: 493-508.
10. Cox G, Kable E, Jones A, Fraser IK, Manconi F, et al. (2003) 3-dimensional imaging of collagen using second harmonic generation. J Struct Biol 141: 53-62.
11. Freund I, Deutsch M, Sprecher A (1986) Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon. Biophys J 50: 693-712.
12. Fritze O, Schleicher M, Konig K, Schenke-Layland K, Stock U, et al. (2010) Facilitated noninvasive visualization of collagen and elastin in blood vessels. Tissue Eng Part C Methods 16: 705-710.
13. Teng SW, Tan HY, Peng JL, Lin HH, Kim KH, et al. (2006) Multiphoton autofluorescence and secondharmonic generation imaging of the ex vivo porcine eye. Invest Ophthalmol Vis Sci 47: 1216-1224.
14. Zipfel WR, Williams RM, Christie R, Nikitin AY, Hyman BT, et al. (2003) Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc Natl Acad Sci U S A 100: 7075-7080.
15. Zoumi A, Yeh A, Tromberg BJ (2002) Imaging cells and extracellular matrix in vivo by using secondharmonic generation and two-photon excited fluorescence. Proc Natl Acad Sci U S A 99: 11014-11019.
16. Junqueira LCU, Bignolas G, Brentani RR (1979) Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 11: 447-455.
17. Boerboom RA, Rubbens MP, Driessen NJB, Bouten CVC, Baaijens FPT (2008) Effect of strain magnitude on the tissue properties of engineered cardiovascular constructs. Ann Biomed Eng 36: 244-253.
18. Cox MAJ, Kortsmit J, Driessen N, Bouten CVC, Baaijens FPT (2010) Tissue-engineered heart valves develop native-like collagen fiber architecture. Tissue Eng Part A 16: 1527-1537.
19. de Jonge N, Kanters FMW, Baaijens FPT, Bouten CVC (2013) Strain-induced collagen organization at the micro-level in fibrin-based engineered tissue constructs. Ann Biomed Eng 41: 763-774.
20. de Jonge N, Muylaert DEP, Fioretta ES, Baaijens FPT, Fledderus JO, et al. (2013) Matrix production and organization by endothelial colony forming cells in mechanically strained engineered tissue constructs. PLoS One 8: e73161.
21. Foolen J, Deshpande VS, Kanters FMW, Baaijens FPT (2012) The influence of matrix integrity on stress-fiber remodeling in 3D. Biomaterials 33: 7508-7518.
22. Piechocka IK, van Oosten ASG, Breuls RGM, Koenderink GH (2011) Rheology of heterotypic collagen networks. Biomacromolecules 12: 2797-2805.
23. Riem Vis PW, Sluijter JP, Soekhradj-Soechit RS, van Herwerden LA, Kluin J, et al. (2012) Sequential use of human-derived medium supplements favours cardiovascular tissue engineering. J Cell Mol Med 16: 730-739.
24. Rubbens MP, Driessen-Mol A, Boerboom RA, Koppert MMJ, van Assen HC, et al. (2009) Quantification of the temporal evolution of collagen orientation in mechanically conditioned engineered cardiovascular tissues. Ann Biomed Eng 37: 1263-1272.
25. Rubbens MP, Mol A, Boerboom RA, Bank RA, Baaijens FPT, et al. (2009) Intermittent straining accelerates the development of tissue properties in engineered heart valve tissue. Tissue Eng Part A 15: 999-1008.
26. Rezakhaniha R, Agianniotis A, Schrauwen JTC, Griffa A, Sage D, et al. (2012) Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy. Biomech Model Mechanobiol 11: 461-473.
27. Schrauwen JTC, Vilanova A, Rezakhaniha R, Stergiopulos N, van de Vosse FN, et al. (2012) A method for the quantification of the pressure dependent 3D collagen configuration in the arterial adventitia. J Struct Biol 180: 335-342.
28. Chai CK, Akyildiz AC, Speelman L, Gijsen FJH, Oomens CWJ, et al. (2013) Local axial compressive mechanical properties of human carotid atherosclerotic plaques-characterisation by indentation test and inverse finite element analysis. J Biomech 46: 1759-1766.
29. Megens RTA, Egbrink MGAO, Cleutjens JPM, Kuijpers MJE, Schiffers PHM, et al. (2007) Imaging collagen in intact viable healthy and atherosclerotic arteries using fluorescently labeled CNA35 and twophoton laser scanning microscopy. Mol Imaging 6: 247-260.
30. Megens RTA, Egbrink MGAO, Merkx M, Slaaf DW, van Zandvoort MAMJ (2008) Two-photon microscopy on vital carotid arteries: imaging the relationship between collagen and inflammatory cells in atherosclerotic plaques. J Biomed Opt 13: 044022.
31. Huyghe JM, Jongeneelen CJM (2012) 3D non-affine finite strains measured in isolated bovine annulus fibrosus tissue samples. Biomech Model Mechanobiol 11: 161-170.
32. Brownfield DG, Venugopalan G, Lo A, Mori H, Tanner K, et al. (2013) Patterned collagen fibers orient branching mammary epithelium through distinct signaling modules. Curr Biol 23: 703-709.
33. Chen JQ, Lee SK, Abd-Elgaliel WR, Liang LF, Galende EY, et al. (2011) Assessment of cardiovascular fibrosis using novel fluorescent probes. PLoS One 6: e19097.
34. Klink A, Heynens J, Herranz B, Lobatto ME, Arias T, et al. (2011) In vivo characterization of a new abdominal aortic aneurysm mouse model with conventional and molecular magnetic resonance imaging. J Am Coll Cardiol 58: 2522-2530.
35. Sanders HM, Iafisco M, Pouget EM, Bomans PH, Nudelman F, et al. (2011) The binding of CNA35 contrast agents to collagen fibrils. Chem Commun (Camb) 47: 1503-1505.
36. Sanders HM, Strijkers GJ, Mulder WJ, Huinink HP, Erich SJ, et al. (2009) Morphology, binding behavior and MR-properties of paramagnetic collagen-binding liposomes. Contrast Media Mol Imaging 4: 81-88.
37. van Bochove GS, Sanders HMHF, de Smet M, Keizer HM, Mulder WJM, et al. (2012) Molecular MR imaging of collagen in mouse atherosclerosis by using paramagnetic CNA35 micelles. Eur J Inorg Chem: 2115-2125.
38. Danila D, Johnson E, Kee P (2013) CT imaging of myocardial scars with collagen-targeting gold nanoparticles. Nanomedicine 9: 1067-1076.
39. Mees G, Dierckx R, Mertens K, Vermeire S, Van Steenkiste M, et al. (2012) 99 m Tc-labeled tricarbonyl his-CNA35 as an imaging agent for the detection of tumor vasculature. J Nucl Med 53: 464-471.
40. Xia ZY, Xing Y, Jeon J, Kim YP, Gall J, et al. (2011) Immobilizing Reporters for Molecular Imaging of the Extracellular Microenvironment in Living Animals. ACS Chem Biol 6: 1117-1126.
41. Breurken M, Lempens EHM, Meijer EW, Merkx M (2011) Semi-synthesis of a protease-activatable collagen targeting probe. Chem Commun (Camb) 47: 7998-8000.
42. Breurken M, Lempens EHM, Merkx M (2010) Protease-Activatable Collagen Targeting Based on Protein Cyclization. Chembiochem 11: 1665-1668.
43. Goedhart J, von Stetten D, Noirclerc-Savoye M, Lelimousin M, Joosen L, et al. (2012) Structureguided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat Commun 3: 751.
44. Lawson ND, Scheer N, Pham VN, Kim CH, Chitnis AB, et al. (2001) Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 128: 3675-3683.
45. Ai HW, Hazelwood KL, Davidson MW, Campbell RE (2008) Fluorescent protein FRET pairs for ratiometric imaging of dual biosensors. Nat Methods 5: 401-403.
46. Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, et al. (2008) Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods 5: 545-551.
47. Shcherbakova DM, Hink MA, Joosen L, Gadella TWJ, Verkhusha VV (2012) An orange fluorescent protein with a large Stokes shift for single-excitation multicolor FCCS and FRET imaging. J Am Chem Soc 134: 7913-7923.
48. Weeke-Klimp A, Bax NAM, Bellu AR, Winter EM, Vrolijk J, et al. (2010) Epicardium-derived cells enhance proliferation, cellular maturation and alignment of cardiomyocytes. J Mol Cell Cardiol 49: 606-616.
49. van Spreeuwel AC, Bax NA, Bastiaens AJ, Foolen J, Loerakker S, et al. (2014) The influence of matrix (an)isotropy on cardiomyocyte contraction in engineered cardiac microtissues. Integr Biol (Camb).
50. Hattori F, Chen H, Yamashita H, Tohyama S, Satoh Y, et al. (2010) Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat Methods 7: 61-66.
51. Drobizhev M, Makarov NS, Tillo SE, Hughes TE, Rebane A (2011) Two-photon absorption properties of fluorescent proteins. Nat Methods 8: 393-399.
52. Shaner NC, Steinbach PA, Tsien RY (2005) A guide to choosing fluorescent proteins. Nat Methods 2: 905-909.