1,238
Views
31
CrossRef citations to date
0
Altmetric
Imaging on the Horizon–new Models: Review Article

Power and challenges of using zebrafish as a model for skeletal tissue imaging

&
Pages 161-173 | Received 30 Nov 2014, Accepted 23 Jan 2015, Published online: 17 Feb 2015

References

  • Harris MP, Henke K, Hawkins MB, Witten PE. Fish is fish: the use of experimental model species to reveal causes of skeletal diversity in evolution and disease. Appl Ichtyol 2014;30:616–29
  • Metscher BD, Ahlberg PE. Zebrafish in context: uses of a laboratory model in comparative studies. Dev Biol 1999;210:1–4
  • Witten PE, Huysseune A. A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biol Rev 2009;84:315–46
  • Owen R. The principal forms of the skeleton and the teeth as the basis for a system of natural history and comparative anatomy. New York: William Wood; 1854
  • Bird NC, Hernandez LP. Building an evolutionary innovation: differential growth in the modified vertebral elements of the zebrafish weberian apparatus. Zoology 2009;112:97–112
  • Smith MM, Hall BK. Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol Rev 1990;65:277–373
  • Sire JY, Huysseune A. Formation of dermal skeletal and dental tissues in fish: a comparative and evolutionary approach. Biol Rev 2003;78:219–49
  • Huysseune A. Skeletal system. In: Ostrander GK, ed. The laboratory fish. Part 4. Microscopic functional anatomy. San Diego (CA): Academic Press; 2000:307–17
  • Witten PE, Huysseune A. Mechanisms of chondrogenesis and osteogenesis in fins. In: Hall BK, ed. Fins into limbs: evolution, development, and transformation. Chicago (IL): The University of Chicago Press; 2007:79–92
  • Witten PE, Villwock W. Growth requires bone resorption at particular skeletal elements in a teleost fish with acellular bone (Oreochromis niloticus, Teleostei: Cichlidae). J Appl Ichthyol 1997;13:149–58
  • Cubbage CC, Mabee PM. Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae). J Morphol 1996;229:121–60
  • Witten PE, Hansen A, Hall BK. Features of mono- and multinucleated bone resorbing cells of the zebrafish Danio rerio and their contribution to skeletal development, remodeling and growth. J Morphol 2001;250:197–207
  • Witten PE, Huysseune A, Hall BK. A practical approach for the identification of the many cartilaginous tissues in teleost fish. J Appl Ichthyol 2010;26:257–62
  • Witten PE, Hall BK. Differentiation and growth of kype skeletal tissues in anadromous male atlantic salmon (Salmo salar). Int J Dev Biol 2002;46:719–30
  • Moss ML. Studies of the acellular bone of teleost fish. 1. Morphological and systematic variations. Acta Anat 1961;46:343–462
  • Smith-Vaniz WF, Kaufman LS, Glowacki J. Species-specific patterns of hyperostosis in marine teleost fishes. Mar Biol 1995;121:573–80
  • Witten PE, Hall BK. Seasonal changes in the lower jaw skeleton in male Atlantic salmon (Salmo salar L.): remodelling and regression of the kype after spawning. J Anat 2003;203:435–50
  • Meunier FJ. Skeleton. In: Panfili J, de Pontual H, Troadec H, Wright PJ, eds. Manuel of fish sclerochronology. Brest, France: Ifremer-IRD Coedition; 2002:65–88
  • Meunier FJ. The osteichtyes, from the paleozoic to the extant time, through histology and palaeohistology of bony tissues. Comptes Rendus Palevol 2011;10:347–55
  • Hall BK, Witten PE. The origin and plasticity of skeletal tissues in vertebrate evolution and development. In: Anderson JS, Sues H-D, eds. Major transitions in vertebrate evolution. Bloomington (IN): Indiana University Press; 2007:13–56
  • Benjamin M. The cranial cartilages of teleosts and their classification. J Anat 1990;169:153–72
  • Beresford WA. Cranial skeletal tissues: diversity and evolutionary trends. In: Hanken J, Hall BK, eds. The skull: patterns of structural and systematic diversity. Vol. 2. Chicago (IL): University of Chicago Press; 1993:69–130
  • Bensimon-Brito A, Cancela ML, Huysseune A, Witten PE. Vestiges, rudiments and fusion events: the zebrafish caudal fin endoskeleton in an evo-devo perspective. Evol Dev 2012;14:116–27
  • Huysseune A. Late skeletal development at the articulation between upper pharyngeal jaws and neurocranial base in the fish, Astatotilapia elegans, with the participation of a chondroid form of bone. Am J Anat 1986;177:119–37
  • Huysseune A, Verraes W. Carbohydrate histochemistry of mature chondroid bone in Astatotilapia elegans (Teleostei: Cichlidae) with a comparison to acellular bone and cartilage. Annls Sci Nat 1990;11:29–43
  • Huysseune A, Sire J-Y. Ultrastructural observations on chondroid bone in the teleost fish Hemichromis bimaculatus. Tissue Cell 1990;22:371–83
  • Kölliker A. On the different types in the microstructure of the skeletons of osseous fish. Proc Roy Soc Lond 1859;9:656–68
  • Meunier FJ, Huysseune A. The concept of bone tissue in osteichthyes. Net J Zool 1992;42:445–58
  • Meunier FJ. The acellularisation process in osteichthyan bone. Prog Zool 1989;35:443–5
  • Witten PE, Hall BK. Teleost skeletal plasticity: modulation, adaptation, and remodelling. Copeia; 2015 (in press)
  • Fjelldal PG, Grotmol S, Kryvi H, Gjerdet NR, Taranger GL, Hansen T, Porter MJR, Totland GK. Pinealectomy induces malformation of the spine and reduces the mechanical strength of the vertebrae in Atlantic salmon, Salmo salar. J Pineal Res 2004;36:132–9
  • Shkil FN, Stolero B, Sutton GA, Belay Abdissa B, Dmitriev SG, Shahar R. Effects of thyroid hormone treatment on the mineral density and mechanical properties of the African barb (Labeobarbus intermedius) skeleton. J Appl Ichthyol 2014;30:814–20
  • Dean MN, Shahar R. The structure-mechanics relationship and the response to load of the acellular bone of neoteleost fish: a review. J Appl Ichthyol 2012;28:320–9
  • Arratia G, Schultze HP, Casciotta J. Vertebral column and associated elements in dipnoans and comparison with other fishes: development and homology. J Morphol 2001;250:101–72
  • Bensimon-Brito A, Cardeira J, Cancela ML, Witten PE. Distinct patterns of notochord mineralization in zebrafish coincide with the localization of osteocalcin isoform 1 during early vertebral centra formation. BMC Dev Biol 2012;12:28
  • Nordvik K, Kryvi H, Totland GK, Grotmol S. The salmon vertebral body develops through mineralization of two preformed tissues that are encompassed by two layers of bone. J Anat 2005;206:103–14
  • Huxley TH. Observations on the development of some parts of the skeleton of fishes. Q J Microsc Sci (continued as J Cell Sci) 1859;7:33–46
  • Apschner A. Putting crystals in place, the regulation of biomineralization in zebrafish [PhD thesis]. Utrecht, The Netherlands: University of Utrecht; 2014. 144 p. ISBN 978-90-393-6242-6
  • Willems B, Buettner A, Huysseune A, Renn J, Witten PE, Winkler C. Conditional ablation of osteoblasts in medaka. Dev Biol 2012;364:128–37
  • Bonucci E. The osteocyte: the underestimated conductor of the bone orchestra. Rend Fis Acc Lincei 2009;20:237–54
  • Burger EH, Klein-Nullend J, Van Der Plas A. Function of osteocytes in bone – their role in mechanotransduction. J Nutr 1995;125:202S–3S
  • Capulli M, Paone R, Rucci N. Osteoblast and osteocyte: games without frontiers. Arch Biochem Biophys 2014;561:3–12
  • Drake MT, Farr JN. Inhibitors of sclerostin: emerging concepts. Curr Opin Rheumatol 2014;26:447–52
  • Witten PE. Enzyme histochemical characteristics of osteoblasts and mononucleated osteoclasts in a teleost fish with acellular bone (Oreochromis niloticus, Cichlidae). Cell Tissue Res 1997;287:591–9
  • To TT, Witten PE, Renn J, Bhattacharya D, Huysseune A, Winkler C. Rankl induced osteoclastogenesis leads to loss of mineralization in a medaka osteoporosis model. Development 2012;139:141–50
  • Rodger HD. Vertebral column fracture in farmed Atlantic salmon. Vet Rec 1991;129:199–200
  • Helland S, Denstadli V, Witten PE, Hjelde K, Storebakken T, Baeverfjord G. Occurrence of hyper dense vertebrae in Atlantic salmon (Salmo salar L.) fed diets with graded levels of phytic acid. Aquaculture 2006;261:603–14
  • Moss ML. Studies of the acellular bone of teleost fish. 2. Response to fracture under normal and acalcemic variations. Acta Anat 1962;48:46–60
  • Sousa S, Valerio F, Jacinto A. A new zebrafish bone crush injury model. BiO 2012;1:915–21
  • Sire J-Y, Akimenko MA. Scale development in fish: a review, with description of sonic hedgehog (shh) expression in the zebrafish (Danio rerio). Int J Dev Biol 2004;48:233–47
  • Geurtzen K, Knopf F, Wehner D, Huitema LFA, Leonie FA, Schulte-Merker S, Weidinger G. Mature osteoblasts dedifferentiate in response to traumatic bone injury in the zebrafish fin and skull. Development 2014;141:2225–34
  • Sousa S, Afonso N, Bensimon-Brito A, Fonseca M, Simões M, Leon J, Roehl H, Cancela ML, Jacinto A. Differentiated skeletal cells contribute to blastema formation during zebrafish fin regeneration. Development 2011;138:3897–905
  • Knopf F, Hammond C, Chekuru A, Fonseca M, Simões M, Leon J, Roehl H, Cancela ML, Jacinto A. Bone regenerates via dedifferentiation of osteoblasts in the zebrafish fin. Dev Cell 2011;20:713–24
  • Witten PE, Gil-Martens L, Huysseune A, Takle H, Hjelde K. Towards a classification and an understanding of developmental relationships of vertebral body malformations in Atlantic salmon (Salmo salar L.). Aquaculture 2009;295:6–14
  • Gregg CL, Butcher JT. Quantitative in vivo imaging of embryonic development: opportunities and challenges. Differentiation 2012;84:149–62
  • Guldberg RE, Ballock RT, Boyan BD, Duvall CL, Lin ASP, Nagaraja S, Oest M, Phillips J, Porter BS, Robertson G, Taylor W. Analyzing bone, blood vessels, and biomaterials with microcomputed tomography. Eng Med Biol Mag 2003;22:77–83
  • Deuerling JM, Rudy DJ, Niebur GL, Roeder RK. Improved accuracy of cortical bone mineralization measured by polychromatic microcomputed tomography using a novel high mineral density composite calibration phantom. Med Phys 2010;37:5138–45
  • Asharani PV, Keupp K, Semler O, Wang WS, Li Y, Thiele H, Yigit G, Pohl E, Becker J, Frommolt P, Sonntag C, Altmuller J, Zimmermann K, Greenspan DS, Akarsu NA, Netzer C, Schonau E, Wirth R, Hammerschmidt M, Nurnberg P, Wollnik B, Carney TJ. Attenuated BMP1 function compromises osteogenesis, leading to bone fragility in humans and zebrafish. Am J Hum Gen 2012;90:661–74
  • Hayes AJ, Reynolds S, Nowell MA, Meakin LB, Habicher J, Ledin J, Bashford A, Caterson B, Hammond CL. Spinal deformity in aged zebrafish is accompanied by degenerative changes to their vertebrae that resemble osteoarthritis. PLoS One 2013;8:12
  • Kranenbarg S, van Cleynenbreugel T, Schipper H, van Leeuwen J. Adaptive bone formation in acellular vertebrae of sea bass (Dicentrarchus labrax L.). J Exp Biol 2005;208:3493–502
  • Kranenbarg S, Waarsing JH, Muller M, Weinans H, van Leeuwen JL. Lordotic vertebra in sea bass (Dicentrarchus labrax L.) are adapted to increased loads. J Biomech 2005;38:1239–46
  • Cohen L, Dean M, Shipov A, Atkins A, Monsonego-Ornan E, Shahar R. Comparison of structural, architectural and mechanical aspects of cellular and acellular bone in two teleost fish. J Exp Biol 2012;215:1983–93
  • Siccardi AJ, Padgett-Vasquez S, Garris HW, Nagy TR, D'Abramo LR, Watts SA. Dietary strontium increases bone mineral density in intact zebrafish (Danio rerio): a potential model system for bone research. Zebrafish 2010;7:267–73
  • Pasco-Viel E, Charles C, Chevret P, Semon M, Tafforeau P, Viriot L, Laudet V. Evolutionary trends of the pharyngeal dentition in cypriniformes (Actinopterygii: Ostariophysi). PLoS One 2010;5:e11293
  • Atukorala ADS, Inohaya K, Baba O, Tabata MJ, Ratnayake R, Abduweli D, Kasugai S, Mitani H, Takano Y. Scale and Tooth phenotypes in medaka with a mutated ectodysplasin-a receptor: implications for the evolutionary origin of oral and pharyngeal teeth. Arch Histol Cytol 2010;73:139–48
  • Zehbe R, Haibel A, Riesemeier H, Gross U, Kirkpatrick CJ, Schubert H, Brochhausen C. Going beyond histology. synchrotron micro-computed tomography as a methodology for biological tissue characterization: from tissue morphology to individual cells. J R Soc Interface 2010;7:49–59
  • Westneat MW, Socha JJ, Lee WK. Advances in biological structure, function, and physiology using synchrotron X-ray imaging. Annu Rev Physiol 2008;70:119–42
  • Mahamid J, Aichmayer B, Shimoni E, Ziblat R, Li CH, Siegel S, Paris O, Fratzl P, Weiner S, Addadi L. Mapping amorphous calcium phosphate transformation into crystalline mineral from the cell to the bone in zebrafish fin rays. Proc Natl Acad Sci USA 2010;107:6316–21
  • Neues F, Goerlich R, Renn J, Beckmann F, Epple M. Skeletal deformations in medaka (Oryzias latipes) visualized by synchrotron radiation micro-computer tomography (SR mu CT). J Struct Biol 2007;160:236–40
  • Neues F, Arnold WH, Fischer J, Beckmann F, Gaengler P, Epple M. The skeleton and pharyngeal teeth of zebrafish (Danio rerio) as a model of biomineralization in vertebrates. Materialwiss Werkst 2006;37:426–31
  • Epple M, Neues F. Synchrotron microcomputer tomography for the non-destructive visualization of the fish skeleton. J Appl Ichthyol 2010;26:286–8
  • Sharpe J, Ahlgren U, Perry P, Hill B, Ross A, Hecksher-Sorensen J, Baldock R, Davidson D. Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 2002;296:541–5
  • Walls JR, Sled JG, Sharpe J, Henkelman RM. Resolution improvement in emission optical projection tomography. Phys Med Biol 2007;52:2775–90
  • Fieramonti L, Bassi A, Foglia EA, Pistocchi A, D'Andrea C, Valentini G, Cubeddu R, De Silvestri S, Cerullo G, Cotelli F. Time-gated optical projection tomography allows visualization of adult zebrafish internal structures. PLoS One 2012;7:e50744
  • Yang B, Treweek JB, Kulkarni RP, Deverman BE, Chen CK, Lubeck E, Shah S, Cai L, Gradinaru V. Single-cell phenotyping within transparent intact tissue through whole-body clearing. Cell 2014;158:945–58
  • Tainaka K, Kubota S, Suyama TQ, Susaki EA, Perrin D, Ukai-Tadenuma M, Ukai H, Ueda HR. Whole-body imaging with single-cell resolution by tissue decolorization. Cell 2014;159:911–24
  • Bryson-Richardson RJ, Cole N, Hall TE, Eckert S, Sharpe J, Currie PD. FishNet, an online database of zebrafish anatomy. MC Biol 2007;5:34. doi:10.1186/1741-7007-5-34
  • Eames BF, DeLaurier A, Ullmann B, Huycke TR, Nichols JT, Dowd J, McFadden M, Sasaki MM, Kimmel CB. FishFace: interactive atlas of zebrafish craniofacial development at cellular resolution. BMC Dev Biol 2013;13:23
  • Eames BF, Yan Y, Swartz ME, Levic DS, Knapnik EW, Postlethwait JH, Kimmel CB. Mutations in fam20b and xylt1 reveal that cartilage matrix controls timing of endochondral ossification by inhibiting chondrocyte maturation. PLoS Genet 2011;7:e1002246
  • Fraser GJ, Britz R, Hall A, Johanson Z, Smith MM. Replacing the first-generation dentition in pufferfish with an unique beak. Proc Natl Acad Sci USA 2012;109:8179–84
  • Taylor WR. An enzyme method of clearing and staining small vertebrates. Proc US Natn Mus 1967;122:1–17
  • Wassersug RJ. A procedure for differential staining of cartilage and bone in whole formalin-fixed vertebrates. Stain Technol 1976;51:131–4
  • Dingerkus G, Uhler LD. Enzyme clearing of alcian blue stained small vertebrates for demonstration of cartilage. Stain Technol 1977;52:229–32
  • Vandewalle P, Gluckmann I, Wagemans F. A critical assessment of the alcian blue/alizarine double staining in fish larvae and fry. Belg J Zool 1998;128:93–5
  • Springer VG, Johnson GD. Use and advantages of ethanol solution of alizarin red s dye for staining bone in fishes. Copeia 2000;1:300–1
  • Bird NC, Mabee PM. Developmental morphology of the axial skeleton of the zebrafish Danio rerio (Ostariophysi: Cyprinidae). Dev Dyn 2003;228:337–57
  • Walker MB, Kimmel CB. A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech Histochem 2007;82:23–8
  • Loizides M, Georgiou AN, Somarakis S, Witten PE, Koumoundouros G. A new type of lordosis and vertebral body compression in gilthead seabream (Sparus aurata Linnaeus, 1758): aetiology, anatomy and consequences for survival. J Fish Dis 2014;37:949–57
  • Clément A, Wiweger M, von der Hardt S, Rusch MA, Selleck SB, Chien C, Roehl HH. Regulation of zebrafish skeletogenesis by ext2/dackel and papst1/pinscher. PLoS Genet 2008;4:e1000136
  • Grabher C, Wittbrodt J. Meganuclease and transposon mediated transgenesis in medaka. Genome Biol 2007;8:S10
  • Suster ML, Abe G, Schouw A, Kawakami K. Transposon-mediated BAC transgenesis in zebrafish. Nat Protoc 2011;6:1998–2021
  • Zu Y, Tong X, Wang Z, Liu D, Pan R, Li Z, Hu Y, Luo Z, Huang P, Wu Q, Zhu Z, Zhang B, Lin S. TALEN-mediated precise genome modification by homologous recombination in zebrafish. Nat Methods 2013;10:329–31
  • Hwang WY, Fu Y, Reyon D, Maeder ML, Kaini P, Sander JD, Juong JK, Peterson RT, Joanna Yeh JR. Heritable and precise zebrafish genome editing using a CRISPR-Cas system. Plos One 2013;8:e68708
  • Weber T, Koester R. Genetic tools for multicolor imaging in zebrafish larvae. Methods 2013;62:279–91
  • Hammond C, Schulte-Merker S. Two populations of endochondral osteoblasts with differential sensitivity to hedgehog signaling. Development 2009;136:3991–4000
  • Dale RM, Topczewski J. Identification of an evolutionarily conserved regulatory element of the zebrafish col2a1a Gene. Dev Biol 2011;357:518–31
  • Knopf F, Hammond C, Chekuru A, Kurth T, Hans S, Weber CW, Mahatma G, Fisher S, Brand M, Schulte-Merker S, Weidinger G. Bone regenerates via dedifferentiation of osteoblasts in the zebrafish fin. Dev Cell 2011;20:713–24
  • Hammond CL, Moro E. Using transgenic reporters to visualize bone and cartilage signaling during development in vivo. Front Endocrinol 2012;3:91. doi: 10.3389/fendo.2012.00091
  • Balu M, Baldacchini T, Carter J, Krasieva TB, Zadoyan R, Tromberg BJ. Effect of excitation wavelength on penetration depth in nonlinear optical microscopy of turbid media. J Biom Opt 2009;14:010508
  • Kobat D, Horton GN, Xu C. In vivo two-photon microscopy to 1.6-mm depth in mouse cortex. J Biom Opt 2011;16:106014
  • Christensen DJ, Nedergaard M. Two-photon in vivo imaging of cells. Pediatr Nephrol 2011;26:1483–9
  • Pantazis P, Maloney J, Wu D, Fraser SE. Second harmonic generating (SHG) nanoprobes for in vivo imaging. Proc Natl Acad Sci USA 2010;107:14535–40
  • 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
  • Sun CK, Chu SW, Chen SY, Tsai TH, Liu TM, Lin CY, Tsaj HJ. Higher harmonic generation microscopy for developmental biology. J Struct Biol 2004;147:19–30
  • Chen M-H, Chen W-L, Sun Y, Fwu PT, Dong C-Y. Multiphoton autofluorescence and second-harmonic generation imaging of the tooth. J Biomed Opt 2007;12:064018. doi:10.1117/1.2812710
  • Huisken J, Stainier DYR. Selective plane illumination microscopy techniques in developmental biology. Development 2009;136:1963–75
  • Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ. Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Methods 2013;10:413–20
  • Tomer R, Khairy K, Amat F, Keller PJ. Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy. Nat Methods 2012;9:755–63
  • Truong TV, Supatto W, Koos DS, Choi JM, Fraser SE. Deep and fast live imaging with two-photon scanned light-sheet microscopy. Nat Methods 2011;8:757–60
  • Jemielita M, Taormina MJ, DeLaurier A, Kimmel CB, Parthasarathy R. Comparing phototoxicity during the development of a zebrafish craniofacial bone using confocal and light sheet fluorescence microscopy techniques. J Biophotonics 2013;6:920–8
  • Romer AS. The vertebrate body. Philadelphia (PA): W. B. Saunders Company; 1970

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.