Second harmonic generation imaging reveals a distinct organization of collagen fibrils in locations associated with cartilage growth

References

• Hunziker EB. The elusive path to cartilage regeneration. Adv Mater. 2009;21:3419–24.
   PubMed Web of Science ®Google Scholar
• Buckwalter J, Mankin H. Articular cartilage : Part I. J Bone Jt Surg. 1997;79:600–11.
   Web of Science ®Google Scholar
• Hunziker EB, Michel M, Studer D. Ultrastructure of adult human articular cartilage matrix after cryotechnical processing. Microsc Res Tech. 1997;37:271–84.
   PubMed Web of Science ®Google Scholar
• Poole CA, Flint MH, Beaumont BW. Chondrons in cartilage: Ultrastructural analysis of the pericellular microenvironment in adult human articular cartilages. J Orthop Res. 1987;5:509–22.
   PubMed Web of Science ®Google Scholar
• Carlson CS, Hilley HD, Henrikson CK. Ultrastructure of normal epiphyseal cartilage of the articular-epiphyseal cartilage complex in growing swine. Am J Vet Res. 1985;46:306–13.
   PubMed Web of Science ®Google Scholar
• Hunziker EB, Kapfinger E, Geiss J. The structural architecture of adult mammalian articular cartilage evolves by a synchronized process of tissue resorption and neoformation during postnatal development. Osteoarthr Cartil. 2007;15:403–13.
   PubMed Web of Science ®Google Scholar
• Rivas R, Shapiro F. Structural stages in the development of the long bones and epiphyses. J Bone Jt Surg. 2002;84:85–100.
   PubMed Web of Science ®Google Scholar
• Clark JM, Norman A, Nötzli H. Postnatal development of the collagen matrix in rabbit tibial plateau articular cartilage. J Anat. 1997;191:215–21.
   PubMed Web of Science ®Google Scholar
• Ytrehus B, Carlson CS, Ekman S. Etiology and pathogenesis of osteochondrosis. Vet Pathol. 2007;44:429–48.
   PubMed Web of Science ®Google Scholar
• Mankin HJ. Localization of tritiated thymidine in articular cartilage of rabbits. III. Mature articular cartilage. J Bone Jt Surg Am. 1962;45:529–40.
   Web of Science ®Google Scholar
• Hayes AJ, MacPherson S, Morrison H, Dowthwaite G, Archer CW. The development of articular cartilage: Evidence for an appositional growth mechanism. Anat Embryol (Berl). 2001;203:469–79.
   PubMedGoogle Scholar
• Lutfi AM. Study of cell multiplication in the cartilaginous upper end of the tibia of the domestic fowl by tritiated thymidine autoradiography. Acta Anat (Basel). 1970;76:454–63.
   PubMedGoogle Scholar
• Hert J. Growth of the epiphyseal plate in circumference. Acta Anat (Basel). 1972;82:420–36.
   PubMedGoogle Scholar
• Stockwell RA. The ultrastructure of cartilage canals and the surrounding cartilage in the sheep fetus. J Anat. 1971;109:397–410.
   PubMed Web of Science ®Google Scholar
• Blumer MJF, Longato S, Richter E, Pérez MT, Konakci KZ, Fritsch H. The role of cartilage canals in endochondral and perichondral bone formation: Are there similarities between these two processes? J Anat. 2005;206:359–72.
   PubMed Web of Science ®Google Scholar
• Hellings IR, Ekman S, Hultenby K, Dolvik NI, Olstad K. Discontinuities in the endothelium of epiphyseal cartilage canals and relevance to joint disease in foals. J Anat. 2015;doi:10.1111/joa.12391.
   PubMed Web of Science ®Google Scholar
• Haines RW. The pseudoepiphysis of the first metacarpal of man. J Anat. 1974;117:145–58.
   PubMed Web of Science ®Google Scholar
• Campagnola PJ, Millard AC, Terasaki M, Hoppe PE, Malone CJ, Mohler WA. Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues. Biophys J. 2002;82:493–508.
   PubMed Web of Science ®Google Scholar
• 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;50:693–712.
   Google Scholar
• Lilledahl MB, Pierce DM, Ricken T, Holzapfel GA, Davies CDL. Structural analysis of articular cartilage using multiphoton microscopy: Input for biomechanical modeling. IEEE Trans Med Imaging. 2011;30:1635–48.
   PubMed Web of Science ®Google Scholar
• Cox G, Kable E, Jones A, Fraser I, Manconi F, Gorrell MD. 3-Dimensional imaging of collagen using second harmonic generation. J Struct Biol. 2003;141:53–62.
   PubMed Web of Science ®Google Scholar
• Chen X, Nadiarynkh O, Plotnikov S, Campagnola PJ. Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat Protoc. 2012;7:654–69.
   PubMed Web of Science ®Google Scholar
• Stoller P, Celliers PM, Reiser KM, Rubenchik AM. Quantitative second-harmonic generation microscopy in collagen. Appl Opt. 2003;42:5209–19.
   PubMed Web of Science ®Google Scholar
• Lacomb R, Nadiarnykh O, Townsend SS, Campagnola PJ. Phase matching considerations in second harmonic generation from tissues: Effects on emission directionality, conversion efficiency and observed morphology. Opt Commun. 2008;281:1823–32.
   PubMed Web of Science ®Google Scholar
• Chaudhary R, Campbell KR, Tilbury KB, Vanderby R, Block WF, Kijowski R, Campagnola PJ. Articular cartilage zonal differentiation via 3D Second-Harmonic Generation imaging microscopy. Connect Tissue Res. 2015;56:76–86.
   PubMed Web of Science ®Google Scholar
• Mansfield JC, Winlove CP. A multi-modal multiphoton investigation of microstructure in the deep zone and calcified cartilage. J Anat. 2012;220:405–16.
   PubMed Web of Science ®Google Scholar
• Houle M-A, Couture C-A, Bancelin S, Van der Kolk J, Auger E, Brown C, Popov K, Ramunno L, Légaré F. Analysis of forward and backward second harmonic generation images to probe the nanoscale structure of collagen within bone and cartilage. J Biophotonics. Wiley-VCH Verlag; 2015;8:993–1001.
   PubMed Web of Science ®Google Scholar
• Brown CP, Houle M, Chen M, Price AJ, Légaré F, Gill HS. Damage initiation and progression in the cartilage surface probed by nonlinear optical microscopy. J Mech Behav Biomed Mater. 2012;5:62–70.
   PubMed Web of Science ®Google Scholar
• Kumar R, Grønhaug KM, Romijn EI, Finnøy A, Davies CL, Drogset JO, Lilledahl MB. Polarization second harmonic generation microscopy provides quantitative enhanced molecular specificity for tissue diagnostics. J Biophotonics. 2014;8:730–9.
   PubMed Web of Science ®Google Scholar
• Olstad K, Kongsro J, Grindflek E, Dolvik NI. Ossification defects detected in CT scans represent early osteochondrosis in the distal femur of piglets. J Orthop Res. 2014;32:1014–23.
   PubMed Web of Science ®Google Scholar
• Ytrehus B, Carlson CS, Lundeheim N, Mathisen L, Reinholt FP, Teige J, Ekman S. Vascularisation and osteochondrosis of the epiphyseal growth cartilage of the distal femur in pigs: Development with age, growth rate, weight and joint shape. Bone. 2004;34:454–65.
   PubMed Web of Science ®Google Scholar
• Woodard JC, Becker HN, Poulos PW, Poulos Jr. PW. Effect of diet on longitudinal bone growth and osteochondrosis in swine. Vet Pathol. 1987;24:109–17.
   Google Scholar
• Campagnola PJ, Loew LM. Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms. Nat Biotechnol. 2003;21:1356–60.
   PubMed Web of Science ®Google Scholar
• Yeh AT, Hammer-Wilson MJ, Van Sickle DC, Benton HP, Zoumi A, Tromberg BJ, Peavy GM. Nonlinear optical microscopy of articular cartilage. Osteoarthritis Cartilage. 2005;13:345–52.
   PubMed Web of Science ®Google Scholar
• Wardale RJ, Duance VC. Quantification and immunolocalisation of porcine articular and growth plate cartilage collagens. J Cell Sci. 1993;984:975–84.
   Google Scholar
• Bland YS, Ashhurst DE. Development and ageing of the articular cartilage of the rabbit knee joint: Distribution of the fibrillar collagens. Anat Embryol (Berl). 1996;194:607–19.
   PubMedGoogle Scholar
• Eyre D. Collagen of articular cartilage. Arthritis Res. 2002;4:30–5.
   PubMedGoogle Scholar
• Lane JM, Weiss C. Review of articular cartilage collagen research. Arthritis Rheum. 1975;18:553–62.
   PubMed Web of Science ®Google Scholar
• Bancelin S, Aime C, Gusachenko I, Kowalczuk L, Coradin T, Schanne-Klein M-C. Determination of collagen fibril size via absolute measurements of second-harmonic generation signals. Nat Commun. 2014;1–8.
   Google Scholar
• Brown CP, Houle M-A, Popov K, Nicklaus M, Couture C-A, Laliberté M, Brabec T, Ruediger A, Carr AJ, Price AJ, Gill HS, Ramunno L, et al. Imaging and modeling collagen architecture from the nano to micro scale. Biomed Opt Express. 2013;5:233–43.
   PubMed Web of Science ®Google Scholar
• Benson RC, Meyer RA, Zaruba ME, McKhann GM. Cellular autofluorescence. Is it due to flavins? J Histochem Cytochem. 1979;27:44–8.
   PubMed Web of Science ®Google Scholar
• Lecocq M, Girard CA, Fogarty U, Beauchamp G, Richard H, Laverty S. Cartilage matrix changes in the developing epiphysis: early events on the pathway to equine osteochondrosis? Equine Vet J. 2008;40:442–54.
   PubMed Web of Science ®Google Scholar
• Ytrehus B, Ekman S, Carlson CS, Teige J, Reinholt FP. Focal changes in blood supply during normal epiphyseal growth are central in the pathogenesis of osteochondrosis in pigs. Bone. 2004;35:1294–306.
   PubMed Web of Science ®Google Scholar
• Weiss C, Rosenberg L, Helfet AJ. An ultrastructural study of normal young adult human articular cartilage. J Bone Joint Surg Am. 1968;50:663–74.
   PubMed Web of Science ®Google Scholar
• Hunziker EB, Lippuner K, Shintani N. How best to preserve and reveal the structural intricacies of cartilaginous tissue. Matrix Biol. Elsevier B.V.; 2014;39:33–43.
   PubMed Web of Science ®Google Scholar
• Rieppo J, Hyttinen MM, Halmesmaki E, Ruotsalainen H, Vasara A, Kiviranta I, Jurvelin JS, Helminen HJ. Changes in spatial collagen content and collagen network architecture in porcine articular cartilage during growth and maturation. Osteoarthritis Cartilage. 2009;17:448–55.
   PubMed Web of Science ®Google Scholar
• van Turnhout MC, Schipper H, van Lagen B, Zuilhof H, Kranenbarg S, van Leeuwen JL. Postnatal development of depth-dependent collagen density in ovine articular cartilage. BMC Dev Biol. 2010;10:108.
   PubMed Web of Science ®Google Scholar
• Temple MM, Bae WC, Chen MQ, Lotz M, Amiel D, Coutts RD, Sah RL. Age- and site-associated biomechanical weakening of human articular cartilage of the femoral condyle. Osteoarthr Cartil. 2007;15(9):1042–52.
   PubMed Web of Science ®Google Scholar
• Mansfield JC, Winlove CP, Moger J, Matcher SJ. Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy. J Biomed Opt. 2013;13:044020.
   Web of Science ®Google Scholar
• van Turnhout MC, Schipper H, Engel B, Buist W, Kranenbarg S, van Leeuwen JL. Postnatal development of collagen structure in ovine articular cartilage. BMC Dev Biol. 2010;10:62.
   PubMed Web of Science ®Google Scholar
• Benninghoff A. Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion. Zeitschrift fuer Zellforsch und Mikroskopische Anat. Springer-Verlag; 1925;2:783–862.
   Google Scholar
• Mittelstaedt D, Xia Y, Shmelyov A, Casciani N, Bidthanapally A. Quantitative determination of morphological and territorial structures of articular cartilage from both perpendicular and parallel sections by polarized light microscopy. Connect Tissue Res. 2011;52:512–22.
   PubMed Web of Science ®Google Scholar
• Wilsman NJ, Van Sickle DC. Cartilage canals, their morphology and distribution. Anat Rec. 1972;173:79–93.
   PubMedGoogle Scholar
• Lofgren M, Ekman S, Svala E, Lindahl A, Ley C, Skioldebrand E, Löfgren M, Ekman S, Svala E, Lindahl A, Ley C, Skiöldebrand E. Cell and matrix modulation in prenatal and postnatal equine growth cartilage, zones of Ranvier and articular cartilage. J Anat. 2014;225:548–68.
   PubMed Web of Science ®Google Scholar
• Zhang Z. Chondrons and the pericellular matrix of chondrocytes. Tissue Eng Part B Rev. 2014;21:267–77.
   PubMed Web of Science ®Google Scholar
• Kvist AJ, Johnson AE, Mörgelin M, Gustafsson E, Bengtsson E, Lindblom K, Aszadi A, Fässler R, Sasaki T, Timpl R, Aspberg A. Chondroitin sulfate perlecan enhances collagen fibril formation: Implications for perlecan chondrodysplasias. J Biol Chem. 2006;281:33127–39.
   PubMed Web of Science ®Google Scholar
• Sherwin AF, Carter DH, Poole CA, Hoyland JA, Ayad S. The distribution of type VI collagen in the developing tissues of the bovine femoral head. Histochem J. 1999;31:623–32.
   PubMedGoogle Scholar