Neuronal Differentiation of Human Embryonic Stem Cell Derived Otic Neural Progenitors Using a Nanofibrillar Cellulose and Hydrogel Scaffold and Polyhedrin Delivery System

Download pdf

Kyle S. Coots1, Shun Kobayashi1, Duncan M. Chadly1, Kevin T. Nella1, Charles A. Miller1,

 Andrew Oleksijew1, John Kessler2, Akihiro J. Matsuoka1,3,4

1Department of Otolaryngology-Head and Neck Surgery, 2Department of Neurology, 3Department of Communication Sciences and Disorders, 4Knowles Hearing Center, Northwestern University,

Chicago and Evanston, IL, U.S.A.

INTRODUCTION

Stem cell therapy is a promising method to alleviate sensorineural hearing loss, but its potential is currently hindered by low cell survival post transplantation (1-4). The harsh, nutrient deprived environment of the cochlea is thought to be a leading factor in poor cell survival (5,6). To alleviate this problem, we have proposed to use GrowDex®-T as an artificial extracellular matrix that is capable of both providing scaffolding for cells to attach and as a way to keep slow releasing brain derived neurotrophic factor (BDNF) PODSTM -crystals in place.

MATERIALS

  • GrowDex-T 1% (Cat No. 200 103 005, UPM)
  • EZSPHERE™ (Nacalai)
  • BrainPhys™ Neuronal Medium (Cat No. 05790, Stem Cell Technologies)
  • BDNF-PODS™ (Cat No. PPH1-250, Cell Guidance Systems)
  • DMEM/F-12 supplemented with 1% N2 supplement, 2% B27 supplement, 2 mM glutamine, 100 μM beta-mercaptoethanol (all reagents were obtained from Life Technologies)

METHODS

Human embryonic stem cell (hESC) derived late-stage otic neural progenitors (ONPs), as previously described and characterized (7), were single dissociated from a traditional monolayer plate and transferred to a micro-fabricated three dimensional cell culturing device (EZSPHERE, Nacalai) that consists of uniformly sized microwells coated with a low-binding affinity polymer (2-methacryloylxyethyl phosphorycholine). Cells were cultured in an ONP maintenance media (ONPMM) (7) at 37°C, 5% CO2 for two days and allowed to form spheroids with diameters of roughly 250 𝜇m.

1.GrowDex-T stock was diluted to 0.25% (v/v) with PBS (-/-). 

2.100 𝜇l of 0.25% GrowDex-T was plated into a 48-well plate.

3.Spheroids were transferred into the GrowDex-T using a P200 micropipette tip and 500 𝜇l  of BrainPhys was gently added on top of the mixture.

4.75,000 BDNF-PODS (equal to 10 ng/ml) were added to the GrowDex-T. 

5.Spheroids were cultured for 7 days at 37°C, 5% CO2 with no media changes.

6.Following 7 days, the media was removed and the cells and GrowDex-T were fixed with 4% PFA and fluorescently stained for Peripherin, VGLUT2, and DAPI.

RESULTS

Immunocytochemical (ICC) analysis shows that the hESC-derived ONP spheroids stained positive for DAPI, Peripherin (peripheral neuron marker) and VGLUT2 (glutamate transporter marker) after one week in differentiation media. Z-stack (n=18) photomicrograph (Fig. 1) obtained using a Nikon A1(C) confocal microscope. Image shown from the ninth plane. Note that the 3D culture condition produces multiple image planes; differing apparent fluorescence intensities are caused by out-of-focus cells within spheres.

 

 

Figure 1. A Photomicrograph of ICC image on an immature glutamatergic neuronal spheroid stained with DAPI, Peripherin, and VGLUT2. Scale bar: 100 𝜇m.

CONCLUSIONS

Our results indicate that 0.25% GrowDex-T allows for robust differentiation of LONPs into immature glutamatergic peripheral neurons when supplemented with 75,000 BDNF-PODS. In conjunction with slow-releasing BDNF with PODS crystals, GrowDex-T can be a suitable artificial extracellular matrix that is potentially capable of facilitating survival and neurite growth of hESC-derived neuronal progenitors in the future.

REFERENCES

1.Chen W, Jongkamonwiwat N, Abbas L, Eshtan SJ, Johnson SL, Kuhn S, et al. Restoration of auditory evoked responses by human ES-cell-derived otic progenitors. Nature. Nature Publishing Group; 2012;490(7419):278–82.

2.Matsuoka AJ, Kondo T, Miyamoto RT, Hashino E. In vivo and in vitro characterization of bone marrow- derived stem cells in the cochlea. Laryngoscope. 2006;116(August):1363–7.

3.Matsuoka AJ, Kondo T, Miyamoto RT, Hashino E. Enhanced survival of bone-marrow-derived pluripotent stem cells in an animal model of auditory neuropathy. Laryngoscope. 2007;117(9):1629–35.

4.Corrales C, Pan L, Li H, Liberman MC, Heller S, Edge ASB. Engraftment and differentiation of embryonic stem cell–derived neural progenitor cells in the cochlear nerve trunk: Growth of processes into the organ of corti. J Neurobiol. 2006;66(13):489–500.

5.Reichardt LF, Huang EJ. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci. 2001;24:677–736.

6.Reichardt LF. Neurotrophin-regulated signalling pathways. Philos Trans R Soc B Biol Sci. 2006;361(1473):1545–64.

7.Matsuoka AJ, Morrissey ZD, Zhang C, Homma K, Belmadani A, Miller CA, et al. Directed Differentiation of Human Embryonic Stem Cells Toward Placode-Derived Spiral Ganglion-Like Sensory Neurons. Stem Cells Transl Med. 2017 Mar;6(3):923–36.