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. 2012;80(4):269-80.
doi: 10.1159/000342485. Epub 2012 Nov 6.

Spinal transection induces widespread proliferation of cells along the length of the spinal cord in a weakly electric fish

Antiño R Allen  1 , G Troy Smith
Affiliations

Spinal transection induces widespread proliferation of cells along the length of the spinal cord in a weakly electric fish

Antiño R Allen et al. Brain Behav Evol. 2012.

Abstract

The ability to regenerate spinal cord tissue after tail amputation has been well studied in several species of teleost fish. The present study examined the proliferation and survival of cells following complete spinal cord transection rather than tail amputation in the weakly electric fish Apteronotus leptorhynchus. To quantify cell proliferation along the length of the spinal cord, fish were given a single bromodeoxyuridine (BrdU) injection immediately after spinal transection or sham surgery. Spinal transection significantly increased the density of BrdU⁺ cells along the entire length of the spinal cord at 1 day posttransection (dpt), and most newly generated cells survived up to 14 dpt. To examine longer-term survival of the newly proliferated cells, BrdU was injected for 5 days after the surgery, and fish were sacrificed at 14 or 30 dpt. Spinal transection significantly increased cell proliferation and/or survival, as indicated by an elevated density of BrdU⁺ cells in the spinal cords of spinally transected compared to sham-operated and intact fish. At 14 dpt, BrdU⁺ cells were abundant at all levels of the spinal cord. By 30 dpt, the density of BrdU⁺ cells had decreased at all levels of the spinal cord except at the tip of the tail. Thus, newly generated cells in the caudal-most segment of the spinal cord survived longer than those in more rostral segments. Our findings indicate that spinal cord transection stimulates widespread cellular proliferation; however, there were regional differences in the survival of the newly generated cells.

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Figures

Figure 1
Figure 1. Schematic diagrams showing the experimental design
Experiment 1: Immediately after spinal transection or sham surgery, fish were injected with BrdU then sacrificed 1 or 14 days post-transection (dpt). Experiment 2:BrdU injections were given once a day for 5 days after surgery, and fish were sacrificed 14 or 30 dpt.
Figure 2
Figure 2. Density of BrdU+ cells (Mean ±S.E.M.) in spinally transected and sham-operated fish given a single injection of BrdU
Fish were given a single injection of BrdU and sacrificed 1 or 14 days after surgery. Spinal transection significantly increased proliferation and/or survival as indicated by an elevated density of BrdU+ cells in the spinal cords of spinally transected compared to sham-operated fish (*ANOVA, effect of transection p<0.05).
Figure 3
Figure 3. Density of BrdU+ cells in spinally transected and sham operated fish as function of position, treatment, and survival time after a single BrdU injection on the day of surgery
a) At 1 dpt, significantly more BrdU+ cells were present in transected than sham-operated fish at every position of the spinal cord except the tip of the tail (*, Transected > sham, PLSD p<0.05). In sham operated fish, significantly more BrdU+ cells were present at the TT than at other rostro-caudal levels 1 dpt and 14 dpt (†, TT> other positions PLSD, p< 0.05). b) At 14 dpt, significantly more BrdU+ cells were present in transected than sham-operated fish along the entire length of the spinal cord (*, Transected > sham, PLSD p<0.05). In transected fish, more BrdU+ cells were present at AF and TT than at RTS and CTS (‡, PLSD, AF and TT > RTS and CTS p<0.05). As in the 1-day survival fish, more BrdU+ cells were present at the tip of the tail than other positions in the sham-operated fish (†, TT> other positions PLSD, p< 0.05).
Figure 4
Figure 4. Relative distance (Mean +/− SEM) of BrdU+ cells from the central canal as a function of rostro-caudal position along the tail
Y-axis represents the distance of cells from the central canal normalized to the average distance from the central canal to the edge of the spinal cord in each section. Transection did not affect the radial distribution of BrdU+ cells. BrdU+ cells were evenly distributed though out the spinal cord at each time period sampled.
Figure 5
Figure 5. Representative sections of the spinal cord immunohistochemically labeled for BrdU
Spinal cord sections illustrated were from the level of the caudal end of the anal fin (AF) and were taken from fish injected with BrdU for 5 days after spinal transection (a, d), sham surgery (b, e), or no treatment (c, f), and sacrificed 14 (a–c) or 30 (d–f) days later. Dorsal is up. BrdU+ cells (arrows) were present in unoperated, sham operated, and spinally transected fish. More BrdU+ cells were present in spinal cords of spinally transected fish than in control groups at both survival times. By 30 dpt, the density of BrdU+ cells decreased relative to 14 dpt. Scale bars, 80μm.
Figure 6
Figure 6. Density of BrdU+ cells (Mean +/− SEM) in spinally transected and control fish injected with BrdU for 5 days
Fish were injected with BrdU for 5 days after the surgery and sacrificed 14 or 30 days later. Spinal transection significantly increased proliferation and/or survival as indicated by an elevated density of BrdU+ cells in the spinal cords of spinally transected compared to sham-operated or unoperated fish (*, Fisher’s PLSD p<0.05).
Figure 7
Figure 7. Effects of survival time and position on the density of BrdU+ cells (Mean +/− SEM)
Density of BrdU+ cells in transected, sham operated, and unoperated individuals injected with BrdU for 5 days after treatment. a) Spinal transection significantly increased the density of BrdU+ cells uniformly along the entire length of the spinal cord at 14 days after treatment. *, Transected > Controls (ANOVA, Fisher’s PLSD, p<0.05). b) Transected fish continued to have a greater density of BrdU+ cells than control fish along the entire length of the spinal cord at 30 dpt. A higher density of BrdU+ cells were present at the tip of the tail than at other rostro-caudal levels, indicating that proliferated cells survived longer in the caudal-most spinal cord than in more rostral regions. *, transected > controls; †, TT> other positions (ANOVA, Fisher’s PLSD, p < 0.05). c) Density of BrdU+ cells (mean ± SEM) in transected individuals as a function of position and survival time. The density of BrdU+ cells decreased at rostral levels of the cord (RTS, CTS, AF), but not at the tip of the tail between 14 and 30 dpt. *, 14 dpt > 30 dpt, ANOVA p<0.001; †, TT > other positions at 30 dpt ANOVA, PLSD, p<0.001).
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