An amputation resets positional information to a proximal identity in the regenerating zebrafish caudal fin

BMC Developmental Biology

Leonor Saúde¹  António Jacinto²  Sara Sousa³  Ana Sofia Azevedo³ 

[1] Instituto Gulbenkian de Ciência, Oeiras, P-2780-156, Portugal;CEDOC – Faculdade de Ciências Médicas, Universidade Nova de Lisboa, Lisbon, 1169-056, Portugal;PhD Programme in Experimental Biology and Biomedicine, Centro de Neurociências e Biologia Celular, Universidade de Coimbra, Coimbra, 3004-517, Portugal

关键词: Zebrafish;    Fgf;    Shh;    Bony ray bifurcations;    Caudal fin regeneration;   

Others  :  1086524
DOI  :  10.1186/1471-213X-12-24

 received in 2012-07-26, accepted in 2012-08-13,  发布年份 2012

【 摘 要 】

Background

Zebrafish has emerged as a powerful model organism to study the process of regeneration. This teleost fish has the ability to regenerate various tissues and organs like the heart, spinal cord, retina and fins. In this study, we took advantage of the existence of an excellent morphological reference in the zebrafish caudal fin, the bony ray bifurcations, as a model to study positional information upon amputation. We investigated the existence of positional information for bifurcation formation by performing repeated amputations at different proximal-distal places along the fin.

Results

We show that, while amputations performed at a long distance from the bifurcation do not change its final proximal-distal position in the regenerated fin, consecutive amputations done at 1 segment proximal to the bifurcation (near the bifurcation) induce a positional reset and progressively shift its position distally. Furthermore, we investigated the potential role of Shh and Fgf signalling pathways in the determination of the bifurcation position and observed that they do not seem to be involved in this process.

Conclusions

Our results reveal that, an amputation near the bifurcation inhibits the formation of the regenerated bifurcation in the pre-amputation position, inducing a distalization of this structure. This shows that the positional memory for bony ray bifurcations depends on the proximal-distal level of the amputation.

【 授权许可】

   
2012 Azevedo et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1 .

Figure 2 .

Figure 3 .

Figure 4 .

【 参考文献 】

• [1]Iovine MK: Conserved mechanisms regulate outgrowth in zebrafish fins. Nat Chem Biol 2007, 3(10):613-618.
• [2]Poss KD, Keating MT, Nechiporuk A: Tales of regeneration in zebrafish. Dev Dyn 2003, 226(2):202-210.
• [3]Nechiporuk A, Keating MT: A proliferation gradient between proximal and msxb-expressing distal blastema directs zebrafish fin regeneration. Development 2002, 129(11):2607-2617.
• [4]Whitehead GG, Makino S, Lien CL, Keating MT: fgf20 is essential for initiating zebrafish fin regeneration. Science 2005, 310(5756):1957-1960.
• [5]Stoick-Cooper CL, Weidinger G, Riehle KJ, Hubbert C, Major MB, Fausto N, Moon RT: Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 2007, 134(3):479-489.
• [6]Quint E, Smith A, Avaron F, Laforest L, Miles J, Gaffield W, Akimenko MA: Bone patterning is altered in the regenerating zebrafish caudal fin after ectopic expression of sonic hedgehog and bmp2b or exposure to cyclopamine. Proc Natl Acad Sci USA 2002, 99(13):8713-8718.
• [7]Azevedo AS, Grotek B, Jacinto A, Weidinger G, Saude L: The regenerative capacity of the zebrafish caudal fin is not affected by repeated amputations. PLoS One 2011, 6(7):e22820.
• [8]Murciano C, Fernandez TD, Duran I, Maseda D, Ruiz-Sanchez J, Becerra J, Akimenko MA, Mari-Beffa M: Ray-interray interactions during fin regeneration of Danio rerio. Dev Biol 2002, 252(2):214-224.
• [9]Laforest L, Brown CW, Poleo G, Geraudie J, Tada M, Ekker M, Akimenko MA: Involvement of the sonic hedgehog, patched 1 and bmp2 genes in patterning of the zebrafish dermal fin rays. Development 1998, 125(21):4175-4184.
• [10]Shkumatava A, Fischer S, Muller F, Strahle U, Neumann CJ: Sonic hedgehog, secreted by amacrine cells, acts as a short-range signal to direct differentiation and lamination in the zebrafish retina. Development 2004, 131(16):3849-3858.
• [11]Lee Y, Grill S, Sanchez A, Murphy-Ryan M, Poss KD: Fgf signaling instructs position-dependent growth rate during zebrafish fin regeneration. Development 2005, 132(23):5173-5183.
• [12]Tsonis PA: Patterning in the regenerating limb. Limb regeneration. Edited by Press CU, In; 1996:117-192.
• [13]White JA, Boffa MB, Jones B, Petkovich M: A zebrafish retinoic acid receptor expressed in the regenerating caudal fin. Development 1994, 120(7):1861-1872.
• [14]Geraudie J, Monnot MJ, Brulfert A, Ferretti P: Caudal fin regeneration in wild type and long-fin mutant zebrafish is affected by retinoic acid. Int J Dev Biol 1995, 39(2):373-381.
• [15]Poss KD, Shen J, Nechiporuk A, McMahon G, Thisse B, Thisse C, Keating MT: Roles for Fgf signaling during zebrafish fin regeneration. Dev Biol 2000, 222(2):347-358.
• [16]Akimenko MA, Johnson SL, Westerfield M, Ekker M: Differential induction of four msx homeobox genes during fin development and regeneration in zebrafish. Development 1995, 121(2):347-357.
• [17]Scadding SR, Maden M: Retinoic acid gradients during limb regeneration. Dev Biol 1994, 162(2):608-617.
• [18]da Silva SM, Gates PB, Brockes JP: The newt ortholog of CD59 is implicated in proximodistal identity during amphibian limb regeneration. Dev Cell 2002, 3(4):547-555.
• [19]Crawford K, Stocum DL: Retinoic acid coordinately proximalizes regenerate pattern and blastema differential affinity in axolotl limbs. Development 1988, 102(4):687-698.
• [20]Maden M: Positional information: knowing where you are in a limb. Curr Biol 2002, 12(22):R773-R775.
• [21]Blum N, Begemann G: Retinoic acid signaling controls the formation, proliferation and survival of the blastema during adult zebrafish fin regeneration. Development 2012, 139(1):107-116.
• [22]Rolland-Lagan AG, Paquette M, Tweedle V, Akimenko MA: Morphogen-based simulation model of ray growth and joint patterning during fin development and regeneration. Development 2012, 139(6):1188-1197.