Use and efficiency of morpholinos in Neotropical tadpole brains

Sarah C. Ludington, Lauren A O'Connell, Julie M Butler, Chloe Golde

Published: 2023-08-21 DOI: 10.17504/protocols.io.yxmvm23y6g3p/v1

Abstract

Antisense morpholinos are a common tool used to knockdown protein abundance in target tissues in fish and amphibians. However, protocols are largely limited to common aquatic research organisms, such as zebrafish or Xenopus frogs. The goal of this protocol is to enable in vivo morpholino delivery, visualization, and knockdown evaluation in the Neotropical tadpoles. We tested the efficiency of standard and Vivo-morpholinos in the knockdown of tyrosine hydroxylase protein, the rate limiting enzyme in dopamine synthesis, in the Mimetic poison frog (Ramitomeya imitator). We compared the knockdown efficacy of each morpholino at two different time points and the effect of knockdown on tadpole behavior. To quantify tyrosine hydroxylase knockdown efficiency, we developed a quick and inexpensive dot blotting method to evaluate protein levels within a single tadpole brain. We compared this method to chemiluminescent imaging and found both methods are sufficient to assess protein levels and discuss important differences in blot visualization techniques. Finally, we found morpholino knockdown reduced tadpole swimming, consistent with other studies implicanting dopamine as important in motor behaviors. We complement this protocol with a discussion of common challenges, suggestions for troubleshooting, and ideas for future improvement. Extending morpholino delivery and protein knockdown assessment to diverse amphibian species and labs with low budgets will enable the field to move forward more rapidly in the study of tadpole physiology and behavior.

Before start

Consult with your local animal ethics board prior to experimentation.

Steps

Anesthesia Preparation

1.

Mix 0.02g ethyl 3-aminobenzoate methanesulfonate (MS-222) and 0.08g sodium bicarbonate with 60 mL of tadpole water

2.

Store at 4C for up to one week

Electroporation Set-Up

3.

Remove the tips from two 1 mL serological pipettes using scissors and fasten them together with electrical tape and/or hot glue

Figure 1. Two serological pipettes with electrode needles (see Step 4) attached together using electrical tape and hot glue to secure
Figure 1. Two serological pipettes with electrode needles (see Step 4) attached together using electrical tape and hot glue to secure
4.

Mount the pipettes onto the micromanipulator and run one needle electrode wire through each pipette. Ensure the electrode needles are 1 mm apart and parallel to one another

FIgure 2. Two serological pipettes with electrode needles secured onto micromanipulator mount
FIgure 2. Two serological pipettes with electrode needles secured onto micromanipulator mount
5.

Attach the wires from the electrode needles to the capacitor and then to the stimulator. Set the stimulator parameters to 1 pps, 15 ms duration, 1 ms delay, and 30-50 V

Figure 3. Top view of electrode needles, capacitor, and stimulator connected
Figure 3. Top view of electrode needles, capacitor, and stimulator connected
Figure 4. Side view of electrode needles, capacitor, and stimulator connected
Figure 4. Side view of electrode needles, capacitor, and stimulator connected

Note
These parameters are a suggested starting point — optimizing the protocol for target molecules of interest and species-specific applications is recommended

Injection Set-Up

6.

Reconstitute morpholino solution (0.5 - 1.0 mM working concentration) in nuclease-free water

7.

Pull micropipettes from glass capillaries using a pipette puller

8.

Backfill the micropipette with mineral oil using a 28 gauge needle and 1 mL syringe

9.

Using forceps, break the micropipette at an angle to create a beveled tip. Performing this task using a dissection microscope is recommended

10.

Place the micropipette onto the injector plunger and tighten the collet

11.

Select an injection volume between 23-56 nL and set the injection rate to slow

Figure 5. Nanoject II settings for injection volumes
Figure 5. Nanoject II settings for injection volumes
Figure 6. Example injection setting at 23.0 nl and slow
Figure 6. Example injection setting at 23.0 nl and slow

Note
This injection volume range is a suggested starting point. Morpholinos can be slightly toxic, so optimizing the appropriate injection volume for species-specific application is recommended.

12.

Empty enough mineral oil to remove any bubbles and load 1-2 uL of morpholino solution

13.

Pipette 1-2 uL of morpholino solution onto a piece of Parafilm

14.

Gently dip the needle into the morpholino solution on the Parafilm and fill the micropipette without introducing air bubbles

15.

Construct a platform out of clay molded into the shape of a hill and fix on top of an empty Petri dish(es)

Figure 7. Hill-shaped bed mounted on top of Petri dishes to hold tadpoles
Figure 7. Hill-shaped bed mounted on top of Petri dishes to hold tadpoles
16.

Place the platform under a dissection microscope with the electrode on one side and the injector on the other

Figure 8. Full injection and electroporation set-up with clay tadpole platform positioned under dissection microscope
Figure 8. Full injection and electroporation set-up with clay tadpole platform positioned under dissection microscope

Injection and Electroporation

17.

Anesthetize the tadpole by placing it in a Petri dish of room temperature 0.03% MS-222 for 3-5 minutes

18.

Confirm the tadpole is completely sedated by checking for movement in response to stimuli

19.

Cover the clay platform with a Kimwipe damp with tadpole water

20.

Transfer the tadpole to the clay platform with a cut transfer pipette

Figure 9. Anesthetized tadpole laying dorsal side up on top of Kimwipe moistened with frog water on the clay platform
Figure 9. Anesthetized tadpole laying dorsal side up on top of Kimwipe moistened with frog water on the clay platform
21.

Adjust the position of the tadpole to be dorsal side up with its head in the clay depression

22.

Orient the tadpole so the head is facing away from the injector

23.

Lower the injector and insert the pipette needle into the brain, targeting the brain ventricle

24.

Inject the morpholino solution

Note
We recommend injecting with 23-56 nL (detailed in Step 11) to start for species-specific optimization

25.

Remove the pipette from the tadpole brain. Allow 10-20 sec before electroporation

Note
If delivering standard morpholinos, continue with the protocol. If delivering Vivo MOs, skip to step 30

26.

Orient the tadpole so the head is facing away from the electrode

27.

Lower the electrode needles until it is in full contact with the tadpole head on either side of the injection site

28.

Deliver the electrical pulses (4 total, half regular polarity and half reverse polarity)

Figure 10. Close-up of stimulator settings with pulse switch and polarity switch circled in red
Figure 10. Close-up of stimulator settings with pulse switch and polarity switch circled in red

Note
The given pulse number is a suggested starting point. Optimizing the protocol for targets of interest and species-specific applications is recommended

28.1.

Deliver 2 pulses on regular polarity with a 1s interval between each pulse

28.2.

Switch the polarity to reverse

28.3.

Deliver 2 pulses on reverse polarity with a 1s interval between each pulse

29.

Remove the electrode from the tadpole skin

30.

Transfer the tadpole to fresh tadpole water for several hours to recover

In vivo Visualization of Standard MO

31.

At least 24 hrs after electroporation, anesthetize the tadpole by placing it in a Petri dish of room temperature 0.03% MS-222 for 3-5 minutes

Note
Fluorescent signal can be imaged as soon as 24 hours post-electroporation. However, knockdown is most effective after previously translated protein of interest has been degraded. Optimizing timing based on target turnover rate and species-specific application is recommended

32.

Move the tadpole to a new, small, and empty Petri dish using a cut transfer pipette

33.

Place the Petri dish underneath the fluorescent stereomicroscope

34.

Turn on the stereomicroscope and set the filter to GFP

35.

Open the imaging software

36.

Locate the tadpole under the stereomicroscope and zoom in, centered on the brain area

37.

Capture and save the fluorescent image

38.

Transfer the tadpole to fresh tadpole water for several hours to recover

Preparing Protein Extraction and Dot Blot Solutions

39.

Prepare 1x Tris Buffered Saline (TBS)

39.1.

Mix 800mL distilled water with 6.05g Tris HCl and 8.76g NaCl

39.2.

Adjust pH to 7.6

39.3.

Add distilled water to bring to volume

39.4.

Store at 4C for up to 3 months

40.

Prepare 2% SDS in 1x TBS

40.1.

Mix 800 uL of 1x TBS with 200 uL of 10x SDS

40.2.

Store at 4C for up to 3 months

41.

Prepare 7x protease inhibitor stock

41.1.

Add 1 cOmplete Mini EDTA-free tablet to 1.5 mL of distilled water

41.2.

Store at 4C for up to one month

42.

Prepare lysis buffer

42.1.

Mix 857 uL 2% SDS in 1x TBS with 143 uL 7x protease inhibitor stock

43.

Prepare 1x TBST wash buffer

43.1.

Mix 500 mL of 1x TBS with 500 uL of Tween-20 (=0.01%)

Protein Extraction

44.

Anesthetize the tadpole by placing it in a Petri dish of room temperature 0.03% MS-222 for 5 minutes

45.

Sacrifice by rapid decapitation and dissect out tadpole brain

46.

Put the brain directly into 50-100uL of lysis buffer in a clean 1.5 mL microcentrifuge tube

Note
For later lysis and processing, rapid freeze with dry ice and store at -80C

47.

Homogenize the brain by hand with pestle or motorized tissue grinder

48.

Centrifuge tubes at 13000 rpm/18928 rcf for 90 min

49.

Measure protein concentration on Qubit

Note
Samples can be stored at -20 C before continuing the protocol. If proceeding from -20 C storage, allow samples to thaw on ice before proceeding with the dot blot

50.

Calculate sample amounts for desired protein concentration (i.e. 15 ug protein) brought to volume in 1x TBS for dotting 6 ul of sample onto each of two nitrocellulose membranes

51.

Transfer the supernatant to a new 1.5 mL microcentrifuge tube

Dot Blot

52.

Using a narrow-mouth pipette tip, carefully dot 2-4 uL of samples onto two nitrocellulose membranes in the same pattern

53.

Allow the membranes to fully dry, then rewet in 1x TBST for 10 min

54.

Block non-specific binding in 5% dry milk in 1x TBST for 1 hour at room temperature with gentle agitation

55.

Incubate with primary antibody against target of interest on one membrane and primary antibody against reference protein on second membrane (1:100-1000) in 5% dry milk in 1x TBST for 1 hour at room temperature with gentle agitation

Note
We recommend optimizing primary antibody concentrations using manufacturer’s recommendation and pilot dot blots before data collection

56.

Wash three times with 1x TBST for 10 min each at room temperature with gentle agitation

57.

Incubate with secondary antibody with HRP conjugate (1:2000-5000) with 2% BSA in 1x TBST for 1 hour at room temperature with gentle agitation

58.

Wash three times with 1x TBST for 5 min each at room temperature with gentle agitation

Note
If chemiluminescent imaging only is desired, perform steps 59, 60 and 64. If brightfield imaging only is desired, skip to step 61. For both imaging techniques, perform the rest of the protocol as written.

59.

Incubate with Clarity ECL substrate (equal volumes of each component, mixed) for 5 min in dark

60.

Image the membranes using a chemiluminescent imaging system (i.e. ChemiDoc)

Note
We recommend trying different lengths of exposure to minimize background. If subsequent brightfield imaging is desired, we recommend waiting overnight to perform the colorimetric reaction.

61.

Combine DI water, Opti-4CN dilutant, and Opti-4CN substrate according to Opti-4CN development kit and incubate membranes overnight

62.

Rinse membranes in DI water for up to 10 min. Let dry at RT for up to 30 min and seal with tape

63.

Image on brightfield next to normalized step ladder

64.

Measure optical density in ImageJ using mean gray values for each sample blotted across both membranes

65.

Calculate an optical density ratio of your protein of interested to that of your reference housekeeping protein

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