Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-10T15:15:24.716Z Has data issue: false hasContentIssue false
  • English
  • Français

The Expression of Alkaline Phosphatase, Osteopontin, Osteocalcin, and Chondroitin Sulfate during Pectoral Fin Regeneration in Carassius auratus gibelio: A Combined Histochemical and Immunohistochemical Study

Published online by Cambridge University Press:  10 January 2013

Simona Stavri  and
Otilia Zarnescu
Simona Stavri
Affiliation:
Faculty of Biology, Laboratory of Histology and Developmental Biology, University of Bucharest, Splaiul Independentei 91-95, R-050095, Bucharest, Romania
Otilia Zarnescu*
Affiliation:
Faculty of Biology, Laboratory of Histology and Developmental Biology, University of Bucharest, Splaiul Independentei 91-95, R-050095, Bucharest, Romania
*
*Corresponding author. E-mail: otilia.zarnescu@bio.unibuc.ro
Get access

Abstract

Dermal bone is an important component of the teleost fins, and its ability to regenerate after fin amputation appears to be unlimited. The organic bone matrix contain type I collagen fibers, proteoglycans enriched in chondroitin sulfate, and noncollagenous matrix protein such as osteocalcin, osteopontin, and osteonectin. These molecules are synthesized by fin osteoblasts. Inorganic components chiefly consist of calcium and phosphate that form crystals of hydroxyapatite. Fin rays are described as models to study ossification. Due to this, the identification of the components involved in the synthesis of the organic and inorganic components of lepidotrichial bone are of great interest for the analysis of skeletal disorders in fish ossification. The present study investigates expression of alkaline phosphatase, osteopontin, osteocalcin, and chondroitin sulfate during pectoral fin regeneration in Carassius auratus gibelio. Alkaline phosphatase reaction has been found in the epidermis covering the wound, proximal blastema, near the cells that surround newly-formed lepidotrichia matrix and the tips of regenerating fin rays. Osteopontin has been observed throughout the regeneration blastema but excluded from the scleroblasts lining the inner side of the lepidotrichia. Osteocalcin and chondroitin sulfate expression coincides with the onset of mineralization of lepidotrichial matrix, suggesting its involvement in bone mineralization.

Keywords

alkaline phosphatasechondroitin sulfatecrucian carppectoral finosteopontinosteocalcinregeneration
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 19 , Issue 1 , February 2013 , pp. 233 - 242
Copyright
Copyright © Microscopy Society of America 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agarwal, S.K., Banerjee, T.K. & Mittal, A.K. (1980). A histochemical study of the epidermis of the climbing perch, Anabas testudineus (Anabantidae, Pisces). Z Mikrosk Anat Forsc 94, 143–159.Google Scholar
Agrawal, S.K., Banerjee, T.K. & Mittal, A.K. (1979). Enzymes in the epidermis of a fresh-water teleost Barbus sophor (Cyprinidae, Pisces). A histochemical investigation. Mikroskopie 35, 258–264.Google ScholarPubMed
Ahn, D. & Ho, R.K. (2008). Tri-phasic expression of posterior Hox genes during development of pectoral fins in zebrafish: Implications for the evolution of vertebrate paired appendages. Dev Biol 322, 220–233.Google Scholar
Akimenko, M.A, Johnson, S.L., Westerfield, M. & Ekker, M. (1995). Differential induction of four msx homeobox genes during fin development and regeneration in zebrafish. Development 121, 347–357.CrossRefGoogle ScholarPubMed
Alonso, M., Tabata, Y.A., Rigolino, M.G. & Tsukamoto, R.Y. (2000). Effect of induced triploidy on fin regeneration of juvenile rainbow trout, Oncorhynchus mykiss . J Exp Zool 287, 493–502.Google Scholar
Andreasen, E.A., Mathew, L.K., Löhr, C.V., Hasson, R. & Tanguay, R.L. (2007). Aryl hydrocarbon receptor activation impairs extracellular matrix remodeling during zebra fish fin regeneration. Toxicol Sci 95, 215–226.Google Scholar
Andreasen, E.A., Mathew, L.K. & Tanguay, R.L. (2006). Regenerative growth is impacted by TCDD: Gene expression analysis reveals extracellular matrix modulation. Toxicol Sci 92, 254–269.Google Scholar
Ballanti, P., Bradbeer, J.N., Bonucci, E., Coen, G., Mazzaferro, S. & Bianco, P. (1993). Evaluation of osteoblastic activity by morphometric comparison of alkaline phosphatase cytochemistry vs. tetracycline fluorescence. Bone 14, 321–326.Google Scholar
Banerjee, T.K., Agarwal, S.K., Rai, A.K. & Mittal, A.K. (1976). Histochemical localization of alkaline phosphatase, acid phosphatase, and succinic dehydrogenase activities in the epidermis of the freshwater teleost, Amphipnous cuchia (Hamilton) (Symbranchiformes, Pisces). Mikroskopie 32, 294–300.Google Scholar
Becerra, J., Montes, G.S., Bexiga, S.R. & Junqueira, L.C. (1983). Structure of the tail fin in teleosts. Cell Tissue Res 230, 127–137.Google Scholar
Beck, G.R. Jr., Zerler, B. & Moran, E. (2000). Phosphate is a specific signal for induction of osteopontin gene expression. Proc Natl Acad Sci USA 97, 8352–8357.CrossRefGoogle ScholarPubMed
Benjamin, M. & Ralphs, J.R. (1991). Extracellular matrix of connective tissues in the heads of teleosts. J Anat 179, 137–148.Google Scholar
Bloch, M.E. (1782). Oeconomische Naturgeschichte der Fische Deutschlands, pp. 1–37. Berlin: Erster Theil.Google Scholar
Böckelmann, P.K., Ochandio, B.S. & Bechara, I.J. (2010). Histological study of the dynamics in epidermis regeneration of the carp tail fin (Cyprinus carpio, Linnaeus, 1758). Braz J Biol 70, 217–223.Google Scholar
Bouvier, M., Couble, M.L., Hartmann, D.J, Gauthier, J.P. & Magloire, H. (1990). Ultrastructural and immunocytochemical study of bone-derived cells cultured in three-dimensional matrices: Influence of chondroitin-4 sulfate on mineralization. Differentiation 45, 128–137.Google Scholar
Brown, A.M., Fisher, S. & Iovine, M.K. (2009). Osteoblast maturation occurs in overlapping proximal-distal compartments during fin regeneration in zebrafish. Dev Dyn 238, 2922–2928.CrossRefGoogle ScholarPubMed
Declercq, H., Van Der Vreken, N., De Maeyer, E., Verbeeck, R., Schacht, E., De Ridder, L. & Cornelissen, M. (2004). Isolation, proliferation and differentiation of osteoblastic cells to study cell/biomaterial interactions: Comparison of different isolation techniques and source. Biomaterials 25, 757–768.Google Scholar
de Vrieze, E., Metz, J.R., Von den Hoff, J.W. & Flik, G. (2010). ALP, TRAcP and cathepsin K in elasmoid scales: A role in mineral metabolism? J Appl Ichthyol 26, 210–213.Google Scholar
Durán, I., Marí-Beffa, M., Santamaría, J.A., Becerra, J. & Santos-Ruiz, L. (2011). Actinotrichia collagens and their role in fin formation. Dev Biol 354, 160–172.Google Scholar
Edsall, S.C. & Franz-Odendaal, T.A. (2010). A quick whole-mount staining protocol for bone deposition and resorption. Zebrafish 7, 275–280.CrossRefGoogle ScholarPubMed
Franz-Odendaal, T.A., Hall, B.K. & Witten, P.E. (2006). Buried alive: How osteoblasts become osteocytes. Dev Dyn 235, 176–190.Google Scholar
Gavaia, P.J., Simes, D.C., Ortiz-Delgado, J.B., Viegas, C.S., Pinto, J.P., Kelsh, R.N., Sarasquete, M.C. & Cancela, M.L. (2006). Osteocalcin and matrix Gla protein in zebrafish (Danio rerio) and Senegal sole (Solea senegalensis): Comparative gene and protein expression during larval development through adulthood. Gene Expr Patterns 6, 637–652.Google Scholar
Géraudie, J. (1977). Initiation of the actinotrichial development in the early fin bud of the fish, Salmo . J Morphol 151, 353–361.Google Scholar
Géraudie, J. & Landis, W.J. (1982). The fine structure of the developing pelvic fin dermal skeleton in the trout Salmo gairdneri . Am J Anat 163, 141–156.Google Scholar
Géraudie, J., Monnot, M.J., Ridet, A., Thorogood, P. & Ferretti, P. (1994). Is exogenous retinoic acid necessary to alter positional information during regeneration of the fin in zebrafish? Prog Clin Biol Res 383B, 803–814.Google Scholar
Géraudie, J. & Singer, M. (1985). Necessity of an adequate nerve supply for regeneration of the amputated pectoral fin in the teleost Fundulus . J Exp Zool 234, 367–374.Google Scholar
Goss, R.J. & Stagg, M.W. (1957). The regeneration of fins and fin rays in Fundulus heteroclitus . J Exp Zool 136, 487–507.Google Scholar
Hall, B.K. (2005). Bones and cartilage. In Developmental and Evolutionary Skeletal Biology, vol. 1. San Diego, CA: Elsevier Academic Press.Google Scholar
Holtrop, M.E. (1990). Light and electron microscopical structure of the bone forming cells. In Bone: The Osteoblast and Osteocyte, Hall, B.K. (Ed.), pp. 1–40. Caldwell, NJ: The Telford Press.Google Scholar
Johnson, S.L. & Weston, J.A. (1995). Temperature-sensitive mutations that cause stage-specific defects in zebrafish fin regeneration. Genetics 141, 1583–1595.Google Scholar
Kawasaki, K., Suzuki, T. & Weiss, K.M. (2004). Genetic basis for the evolution of vertebrate mineralized tissues. Proc Natl Acad Sci USA 101, 11356–11361.Google Scholar
Kemp, N.E. & Park, J.H. (1970). Regeneration of lepidotrichia and actinotrichia in the tailfin of the teleost Tilapia mossambica . Dev Biol 22, 321–342.Google Scholar
Khalil, S.H. & Aziz, F.K. (1989). Regeneration of the caudal and pectoral fins of a bony fish, Gambusia (Haplochilus) schoelleri . Folia Morphologica 37, 208–212.Google Scholar
Knopf, F., Hammond, C., Chekuru, A., Kurth, T., Hans, S., Weber, C.W., Mahatma, G., Fisher, S., Brand, M., Schulte-Merker, S. & Weidinger, G. (2011). Bone regenerates via dedifferentiation of osteoblasts in the zebrafish fin. Dev Cell 20, 713–724.Google Scholar
Krossøy, C., Ornsrud, R. & Wargelius, A. (2009). Differential gene expression of bgp and mgp in trabecular and compact bone of Atlantic salmon (Salmo salar L.) vertebrae. J Anat 215, 663–672.Google Scholar
Lian, J.B., Roufosse, A.H., Reit, B. & Glimcher, M.J. (1982). Concentrations of osteocalcin and phosphoprotein as a function of mineral content and age in cortical bone. Calcif Tissue Int 34, S82–S87.Google Scholar
Marí-Beffa, M., Palmqvist, P., Marín-Girón, F., Montes, G.S. & Becerra, J. (1999). Morphometric study of the regeneration of individual rays in teleost tail fins. J Anat 195, 393–405.Google Scholar
Marí-Beffa, M., Santamaría, J.A., Murciano, C., Santos-Ruiz, L., Andrades, J.A., Guerado, E. & Becerra, J. (2007). Zebrafish fins as a model system for skeletal human studies. Sci World J 7, 1114–1127.Google Scholar
Mathew, L.K., Sengupta, S., Franzosa, J.A., Perry, J., La Du, J., Andreasen, E.A. & Tanguay, R.L. (2009). Comparative expression profiling reveals an essential role for raldh2 in epimorphic regeneration. J Biol Chem 284, 33642–33653.Google Scholar
Misof, B.Y. & Wagner, G.P. (1992). Regeneration in Salaria pavo (Blenniidae, Teleostei). Histogenesis of the regenerating pectoral fin suggests different mechanisms for morphogenesis and structural maintenance. Anat Embryol (Berl) 186, 153–165.Google Scholar
Mittal, A.K., Rai, A.K. & Banerjee, T.K. (1977). Histochemical localization of alkaline phosphatase and acid phosphatase activity in the skin of a freshwater teleost Heteropneustes fossilis-Bloch (Heteropneustidae, Pisces). Cell Mol Biol Incl Cyto Enzymol 22, 227–234.Google ScholarPubMed
Miyazaki, T., Miyauchi, S., Tawada, A., Anada, T., Matsuzaka, S. & Suzuki, O. (2008). Oversulfated chondroitin sulfate-E binds to BMP-4 and enhances osteoblast differentiation. J Cell Physiol 217, 769–777.Google Scholar
Montes, G.S., Becerra, J., Toledo, O.M., Gordilho, M.A. & Junqueira, L.C. (1982). Fine structure and histochemistry of the tail fin ray in teleosts. Histochemistry 75, 363–376.Google Scholar
Murciano, C., Fernández, T.D., Durán, I., Maseda, D., Ruiz-Sánchez, J., Becerra, J., Akimenko, M.A. & Marí-Beffa, M. (2002). Ray-interray interactions during fin regeneration of Danio rerio . Dev Biol 252, 214–224.Google Scholar
Murciano, C., Pérez-Claros, J., Smith, A., Avaron, F., Fernández, T.D., Durán, I., Ruiz-Sánchez, J., García, F., Becerra, J., Akimenko, M.A. & Marí-Beffa, M. (2007). Position dependence of hemiray morphogenesis during tail fin regeneration in Danio rerio . Dev Biol 312, 272–283.Google Scholar
Padhi, B.K., Joly, L., Tellis, P., Smith, A., Nanjappa, P., Chevrette, M., Ekker, M. & Akimenko, M.A. (2004). Screen for genes differentially expressed during regeneration of the zebrafish caudal fin. Dev Dyn 231, 527–541.Google Scholar
Rai, A.K. & Mittal, A.K. (1983). Histochemical response of alkaline phosphatase activity during the healing of cutaneous wounds in a cat-fish. Cell Mol Life Sci 39, 520–522.Google Scholar
Renn, J., Winkler, C., Schartl, M., Fischer, R. & Goerlich, R. (2006). Zebrafish and medaka as models for bone research including implications regarding space-related issues. Protoplasma 229, 209–214.Google Scholar
Rhee, S.H. & Tanaka, J. (2002). Self-assembly phenomenon of hydroxyapatite nanocrystals on chondroitin sulfate. J Mater Sci Mater Med 13, 597–600.Google Scholar
Santamaría, J.A. & Becerra, J. (1991). Tail fin regeneration in teleosts: Cell-extracellular matrix interaction in blastemal differentiation. J Anat 176, 9–21.Google Scholar
Santamaría, J.A., Marí-Beffa, M. & Becerra, J. (1992). Interactions of the lepidotrichial matrix components during tail fin regeneration in teleosts. Differentiation 49, 143–150.Google Scholar
Santamaría, J.A., Marí-Beffa, M., Santos-Ruiz, L. & Becerra, J. (1996). Incorporation of bromodeoxyuridine in regenerating fin tissue of the goldfish Carassius auratus . J Exp Zool 275, 300–307.Google Scholar
Santos-Ruiz, L., Santamaría, J.A., Ruiz-Sánchez, J. & Becerra, J. (2002). Cell proliferation during blastema formation in the regenerating teleost fin. Dev Dyn 223, 262–272.Google Scholar
Schneiders, W., Reinstorf, A., Ruhnow, M., Rehberg, S., Heineck, J., Hinterseher, I., Biewener, A., Zwipp, H. & Rammelt, S. (2008). Effect of chondroitin sulphate on material properties and bone remodelling around hydroxyapatite/collagen composites. J Biomed Mater Res A 85, 638–645.Google Scholar
Shao, J., Chen, D., Ye, Q., Cui, J., Li, Y. & Li, L. (2011). Tissue regeneration after injury in adult zebrafish: The regenerative potential of the caudal fin. Dev Dyn 240, 1271–1277.Google Scholar
Shao, J., Qian, X., Zhang, C. & Xu, Z. (2009). Fin regeneration from tail segment with musculature, endoskeleton, and scales. J Exp Zool B Mol Dev Evol 312, 762–769.Google Scholar
Suzuki, N., Suzuki, T. & Kurokawa, T. (2000). Suppression of osteoclastic activities by calcitonin in the scales of goldfish (freshwater teleost) and nibbler fish (seawater teleost). Peptides 21, 115–124.CrossRefGoogle ScholarPubMed
Tassava, R.A. & Goss, R.J. (1966). Regeneration rate and amputation level in fish fins and lizard tails. Growth 30, 9–21.Google Scholar
Tu, S. & Johnson, S.L. (2011). Fate restriction in the growing and regenerating zebrafish fin. Dev Cell 20, 725–732.Google Scholar
Wagner, G.P. & Misof, B.Y. (1992). Evolutionary modification of regenerative capability in vertebrates: A comparative study on teleost pectoral fin regeneration. J Exp Zool 261, 62–78.CrossRefGoogle ScholarPubMed
Wills, A.A., Kidd, A.R. 3rd, Lepilina, A. & Poss, K.D. (2008). Fgfs control homeostatic regeneration in adult zebrafish fins. Development 135, 3063–3070.Google Scholar
Witten, P.E. (1997). Enzyme histochemical characteristics of osteoblasts and mononucleated osteoclasts in a teleost fish with acellular bone (Oreochromis niloticus, Cichlidae). Cell Tissue Res 287, 591–599.Google Scholar
Witten, P.E. & Huysseune, A. (2007). Mechanisms of chondrogenesis and osteogenesis in fins. In Fins into Limbs: Evolution, Development and Transformation, Hall, B.K. (Ed.), pp. 79–92. Chicago, IL: Chicago University Press.Google Scholar
Witten, P.E. & Huysseune, A. (2009). A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biol Rev Camb Philos Soc 84, 315–346.Google Scholar
Witten, P.E. & Villwock, W. (1997). Growth requires bone resorption at particular skeletal elements in a teleost fish with acellular bone (Oreochromis niloticus, Teleostei: Cichlidae). J Appl Ichthyol 13, 149–158.Google Scholar
Zarnescu, O., Craciunescu, O. & Moldovan, L. (2010). Collagen-chondroitin sulphate-hydroxyapatite porous composites: A histochemical and electron microscopy approach. Microsc Microanal 16, 137–142.CrossRefGoogle ScholarPubMed
Zauner, H., Begemann, G., Marí-Beffa, M. & Meyer, A. (2003). Differential regulation of msx genes in the development of the gonopodium, an intromittent organ, and of the “sword,” a sexually selected trait of swordtail fishes (Xiphophorus). Evol Dev 5, 466–477.Google Scholar